@article{ortiz_de smet_sozzani_locke_2024, title={"Field-grown soybean shows genotypic variation in physiological and seed composition responses to heat stress during seed development" (vol 195, 104768, 2022)}, volume={220}, ISSN={["1873-7307"]}, DOI={10.1016/j.envexpbot.2024.105668}, journal={ENVIRONMENTAL AND EXPERIMENTAL BOTANY}, author={Ortiz, Anna C. and De Smet, Ive and Sozzani, Rosangela and Locke, Anna M.}, year={2024}, month={Apr} }
 @article{madison_tahir_broeck_phan_horn_sozzani_2024, title={Cell-material interactions in 3D bioprinted plant cells}, url={https://doi.org/10.1101/2024.01.30.578043}, DOI={10.1101/2024.01.30.578043}, abstractNote={Abstract}, author={Madison, Imani and Tahir, Maimouna and Broeck, Lisa Van and Phan, Linh and Horn, Timothy and Sozzani, Rosangela}, year={2024}, month={Feb} }
 @article{baker_schunk_scholz_merck_muenich_westerhoff_elser_duckworth_gatiboni_islam_et al._2024, title={Global-to-Local Dependencies in Phosphorus Mass Flows and Markets: Pathways to Improving System Resiliency in Response to Exogenous Shocks}, volume={5}, ISSN={["2328-8930"]}, url={http://dx.doi.org/10.1021/acs.estlett.4c00208}, DOI={10.1021/acs.estlett.4c00208}, abstractNote={Uneven global distribution of phosphate rock deposits and the supply chains to transport phosphorus (P) make P fertilizers vulnerable to exogenous shocks, including commodity market shocks; extreme weather events or natural disasters; and geopolitical instability, such as trade disputes, disruption of shipping routes, and war. Understanding bidirectional risk transmission (global-to-local and local-to-global) in P supply and consumption chains is thus essential. Ignoring P system interdependencies and associated risks could have major impacts on critical infrastructure operations and increase the vulnerability of global food systems. We highlight recent unanticipated events and cascading effects that have impacted P markets globally. We discuss the need to account for exogenous shocks in local assessments of P flows, policies, and infrastructure design choices. We also provide examples of how accounting for undervalued global risks to the P industry can hasten the transition to a sustainable P future. For example, leveraging internal P recycling loops, improving plant P use efficiency, and utilizing legacy soil P all enhance system resiliency in the face of exogenous shocks and long-term anticipated threats. Strategies applied at the local level, which are embedded within national and global policy systems, can have global-scale impacts in derisking the P supply chain.}, journal={ENVIRONMENTAL SCIENCE & TECHNOLOGY LETTERS}, author={Baker, Justin and Schunk, Nathan and Scholz, Matt and Merck, Ashton and Muenich, Rebecca Logsdon and Westerhoff, Paul and Elser, James J. and Duckworth, Owen W. and Gatiboni, Luke and Islam, Minhazul and et al.}, year={2024}, month={May} }
 @article{perez-sancho_broeck_garcia-caparros_sozzani_2024, title={Insights into multilevel spatial regulation within the root stem cell niche}, volume={86}, ISSN={["1879-0380"]}, url={https://doi.org/10.1016/j.gde.2024.102200}, DOI={10.1016/j.gde.2024.102200}, abstractNote={All differentiated root cells derive from stem cells spatially organized within the stem cell niche (SCN), a microenvironment located within the root tip. Here, we compiled recent advances in the understanding of how the SCN drives the establishment and maintenance of cell types. The quiescent center (QC) is widely recognized as the primary driver of cell fate determination, but it is recently considered a convergence center of multiple signals. Cell identity of the cortex endodermis initials is mainly driven by the regulatory feedback loops between transcription factors (TFs), acting as mobile signals between neighboring cells, including the QC. As exemplified in the vascular initials, the precise spatial expression of these regulatory TFs is connected with a dynamic hormonal interplay. Thus, stem cell maintenance and cell differentiation are regulated by a plethora of signals forming a complex, multilevel regulatory network. Integrating the transcriptional and post-translational regulations, protein–protein interactions, and mobile signals into models will be fundamental for the comprehensive understanding of SCN maintenance and differentiation.}, journal={CURRENT OPINION IN GENETICS & DEVELOPMENT}, author={Perez-Sancho, Jessica and Broeck, Lisa and Garcia-Caparros, Pedro and Sozzani, Rosangela}, year={2024}, month={Jun} }
 @article{haverroth_gobble_bradley_harris-gilliam_fischer_williams_long_sozzani_2024, title={The Black American experience: Answering the global challenge of broadening participation in STEM/agriculture}, volume={1}, ISSN={["1532-298X"]}, url={https://doi.org/10.1093/plcell/koae002}, DOI={10.1093/plcell/koae002}, journal={PLANT CELL}, author={Haverroth, Eduardo and Gobble, Mariah and Bradley, Latosha and Harris-Gilliam, Kailyn and Fischer, Alicia and Williams, Cranos and Long, Terri and Sozzani, Rosangela}, year={2024}, month={Jan} }
 @article{van den broeck_bhosale_song_fonseca de lima_ashley_zhu_zhu_van de cotte_neyt_ortiz_et al._2023, title={Functional annotation of proteins for signaling network inference in non-model species}, volume={14}, ISSN={2041-1723}, url={http://dx.doi.org/10.1038/s41467-023-40365-z}, DOI={10.1038/s41467-023-40365-z}, abstractNote={Abstract}, number={1}, journal={Nature Communications}, publisher={Springer Science and Business Media LLC}, author={Van den Broeck, Lisa and Bhosale, Dinesh Kiran and Song, Kuncheng and Fonseca de Lima, Cássio Flavio and Ashley, Michael and Zhu, Tingting and Zhu, Shanshuo and Van De Cotte, Brigitte and Neyt, Pia and Ortiz, Anna C. and et al.}, year={2023}, month={Aug} }
 @article{bennett_brady_dinneny_helariutta_sozzani_2023, title={Obituary Philip N. Benfey (1953-2023)}, volume={58}, ISSN={["1878-1551"]}, DOI={10.1016/j.devcel.2023.10.013}, abstractNote={“When I started to work in systems biology, I kept running across this term ‘emergent behavior,’ and it was really not clear to me, and so as with many things for me, an analogy was very helpful. The analogy I’d like to propose to you is that of a flock of birds, the idea being the following, that you can study a single bird as much as you like and you will never understand how a flock works, because a flock is all about the interactions between birds, and those interactions can lead to some really interesting complex behavior …”—Philip Benfey Professor Philip Benfey, a leading figure in plant biology, passed away on September 26, 2023, at the age of 70. Philip will be deeply missed by his family and friends. He adored his wife, Elisabeth, and their children, Sam and Julian. He was very proud of their achievements. We extend our heartfelt condolences to them as well as to his wider family, his current and former trainees, and his colleagues and friends as we all mourn his loss. Philip has been a giant presence in the field of plant biology over the past several decades—literally, scientifically, and legacy-wise. Everyone who met Philip could not help but be impressed by his imposing physical presence, his intelligence, and his scientific vision. Philip considered himself an “accidental scientist,” who after touring the world for 6 years ended up at the University of Paris VI. From there he went to graduate school at Harvard Medical School, where he completed his thesis with Phil Leder. Thereafter, he performed postdoctoral work with Nam-Hai Chua at the Rockefeller University. His independent career featured several distinct phases and approaches, each marked by a seminal scientific discovery or research innovation. Philip’s impressive independent career took off at NYU, where he adopted the Arabidopsis root as his experimental model to study the genetic regulation of plant development. He pioneered genetic screens to isolate root mutants influencing radial patterning. As a result, his lab identified a pair of GRAS family transcription factors, SHORT-ROOT (SHR) and SCARECROW (SCR), that specify the asymmetric cell division and subsequent cell specification processes separating endodermal and cortex tissue identities. Philip’s team later discovered that SHR is a mobile transcription factor that is produced in the innermost vascular domain of the root and moves from there, through the plasmodesmata, to the adjacent endodermal/cortex stem cell.1Nakajima K. Sena G. Nawy T. Benfey P.N. Intercellular movement of the putative transcription factor SHR in root patterning.Nature. 2001; 413: 307-311https://doi.org/10.1038/35095061Crossref PubMed Scopus (648) Google Scholar In this stem cell, SHR then forms a complex with SCR, and this complex is required for the asymmetric division separating the two cell layers. The formation of this complex also provides a sequestration mechanism to restrict the further movement of SHR and thereby to regulate the number of cell layers in the root. Although prior to this study it had been shown that proteins, even transcription factors, can move through plasmodesmata, the SHR-SCR model on radial patterning was the first to highlight the importance of mobile transcription factors, today a widely recognized principle of plant development. Throughout this period, Philip’s team worked closely with the lab of Ben Scheres at Utrecht University, investigating the interaction of the SHR-SCR module with other transcription factors and developmental signals that define radial patterning and provide the basis for our current understanding. After moving to Duke in 2002, Philip published a series of highly influential papers describing a transformative research approach. While plant single-cell transcriptomics are now de rigueur, his work was truly ahead of its time. Philip believed that resolving gene expression in Arabidopsis root tissues in space and time could help identify the full complement of factors required for cell-type patterning and acquisition of identity. He, along with Ken Birnbaum, took advantage of fluorescent activated cell sorting (FACS) coupled with the many transcriptional reporter lines that mark individual cell types or populations of cell types in the root. FACS was and is a frequently used tool in animal research, but he was able to convince cytometry facility operators to let plant biologists load in their protoplasts to have the machine recognize GFP-positive cells; and scientists in the lab trained in RNA extraction from very small sample sizes. Microarray analysis on this material subsequently reported near-transcriptome-scale gene expression. Since a cell’s developmental trajectory can be tracked along the root’s longitudinal axis, simply cutting a root into several pieces along this axis and isolating RNA/performing microarray analysis, plus some clever computational tools, could capture gene expression in time over the root’s longitudinal axis. Successive papers in Science, including Brady et al., 2007,2Brady S.M. Orlando D.A. Lee J.Y. Wang J.Y. Koch J. Dinneny J.R. Mace D. Ohler U. Benfey P.N. A high-resolution root spatiotemporal map reveals dominant expression patterns.Science. 2007; 318: 801-806https://doi.org/10.1126/science.1146265Crossref PubMed Scopus (888) Google Scholar demonstrated a wealth of expression pattern types and their changes over a cell type’s developmental trajectory. These data are now used by scientists all over the world to determine the expression pattern of their gene(s) of interest. These methods were used to further profile whole-transcriptome gene expression when RNAseq was in its infancy, followed by small RNA levels, protein, and metabolite abundance. These datasets served as a framework for the annotation of every single-cell transcriptome paper that has recently been published. Philip next pioneered systems biology approaches to propel the field of plant developmental biology forward to become more predictive and quantitative. His team exploited these approaches to discover how asymmetric cell division is regulated in roots. By cleverly utilizing fluorescence-activated cell sorting and single-cell gene expression analysis, he discovered a direct connection between developmental subnetworks and the cell division machinery. Philip later explored how emergent behavior transcends a series of switches influenced by high (for asymmetric cell divisions) and low concentrations (for symmetric cell divisions) of proteins. Philip recognized that to understand complex regulatory processes it is critical to quantitatively analyze protein movement and protein-protein interactions in time and space. This led Philip and Ross Sozzani’s teams to study the SHR-SCR regulatory network, where intercellular movement of SHR and interaction with its target SCR controls root patterning and cell fate specification.3Clark N.M. Hinde E. Winter C.M. Fisher A.P. Crosti G. Blilou I. Gratton E. Benfey P.N. Sozzani R. Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy.Elife. 2016; 5e14770Crossref Scopus (68) Google Scholar Key parameters such as SHR mobility, oligomeric state, and association with SCR were quantified using advanced spectroscopy techniques and incorporated into a mathematical model. This seminal quantitative systems biology paper revealed that the timing of SHR protein movement and SHR-SCR stoichiometry play critical regulatory roles during root development. While able to generate seminal research discoveries at the disciplinary interface, Philip considered himself first and foremost a developmental biologist and used plants as an ideal model system to explore questions of cell fate determination. However, the standard practice in developmental biology, of minimizing the impact of the environment on the organism to study such processes, is counter to the nature of roots, which grow in intimate association with the complex and dynamic soil environment. If tissue-specific transcriptomics revealed a rich regulatory landscape for each cell, how much of this architecture was dependent on the specific environmental conditions under which the plants were grown? To address this question, Philip’s lab generated the first spatial maps of roots exposed to environmental stresses, including iron and sulfur deprivation, high salinity, and low pH.4Dinneny J.R. Long T.A. Wang J.Y. Jung J.W. Mace D. Pointer S. Barron C. Brady S.M. Schiefelbein J. Benfey P.N. Cell identity mediates the response of Arabidopsis roots to abiotic stress.Science. 2008; 320: 942-945https://doi.org/10.1126/science.1153795Crossref PubMed Scopus (599) Google Scholar Many of the transcriptional responses were regulated in a cell-type-specific manner, which resulted in major shifts in cell-type function, with many canonical functions only occurring under a narrow range of environmental conditions. Thus, this work showed that plants offered profound insights into the intricacies of cell identity. This identity is intrinsically linked to the environment, which serves as a critical factor in determining how this cellular property is realized through gene expression. While Philip was a stalwart proponent of Arabidopsis as a model system, his interest in understanding plants with more complex root systems, and in applying this knowledge to solve real-world problems, led to deep dives into the use of crop plants, especially rice, and the development of innovative phenotyping approaches. From custom-fabricated microfluidic devices to the use of optical tomography and image analysis algorithms, which generated three-dimensional representations of root system architecture,5Topp C.N. Iyer-Pascuzzi A.S. Anderson J.T. Lee C.-R. Zurek P.R. Symonova O. Zheng Y. Bucksch A. Mileyko Y. Galkovskyi T. et al.3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture.Proc. Natl. Acad. Sci. USA. 2013; 110: 1695-1704Crossref PubMed Scopus (0) Google Scholar Philip was essential in identifying nascent technologies that could be applied to this emerging area. Such work inspired Philip to establish two companies, Grassroots Biotechnology and Hi Fidelity Genetics, which leveraged these innovative methods to advance crop biotechnology solutions. Philip’s impact on the field of plant biology extends far beyond his pioneering basic and applied research discoveries and the technological innovations outlined above. What set Philip apart from his peer group was the unparalleled roll call of international researchers who worked in his laboratory and are now leaders in the plant biology field around the world. These several generations of researchers Philip has mentored arguably represent his greatest scientific legacy.}, number={22}, journal={DEVELOPMENTAL CELL}, author={Bennett, Malcolm J. and Brady, Siobhan M. and Dinneny, Jose R. and Helariutta, Yka and Sozzani, Ross}, year={2023}, month={Nov}, pages={2413–2415} }
 @article{madison_gillan_peace_gabrieli_broeck_jones_sozzani_2023, title={Phosphate starvation: response mechanisms and solutions}, volume={8}, ISSN={["1460-2431"]}, url={https://doi.org/10.1093/jxb/erad326}, DOI={10.1093/jxb/erad326}, abstractNote={Abstract}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={Madison, Imani and Gillan, Lydia and Peace, Jasmine and Gabrieli, Flavio and Broeck, Lisa and Jones, Jacob L. and Sozzani, Rosangela}, editor={Ort, DonaldEditor}, year={2023}, month={Aug} }
 @inproceedings{mahatma_broeck_morffy_staller_strader_sozzani_2023, title={Prediction and functional characterization of transcriptional activation domains}, url={https://doi.org/10.1109/CISS56502.2023.10089768}, DOI={10.1109/CISS56502.2023.10089768}, abstractNote={Gene expression is induced by transcription factors (TFs) through their activation domains (ADs). However, ADs are unconserved, intrinsically disordered sequences without a secondary structure, making it challenging to recognize and predict these regions and limiting our ability to identify TFs. Here, we address this challenge by leveraging a neural network approach to systematically predict ADs. As input for our neural network, we used computed properties for amino acid (AA) side chain and secondary structure, rather than relying on the raw sequence. Moreover, to shed light on the features learned by our neural network and greatly increase interpretability, we computed the input properties most important for an accurate prediction. Our findings further highlight the importance of aromatic and negatively charged AA and reveal the importance of unknown AA properties. Taking advantage of these most important features, we used an unsupervised learning approach to classify the ADs into 10 subclasses, which can further be explored for AA specificity and AD functionality. Overall, our pipeline, relying on supervised and unsupervised machine learning, shed light on the non-linear properties of ADs.}, author={Mahatma, Saloni and Broeck, Lisa Van and Morffy, Nicholas and Staller, Max V and Strader, Lucia C and Sozzani, Rosangela}, year={2023}, month={Mar} }
 @article{gaudinier_broeck_moreno-risueño_rodriguez-medina_sozzani_brady_2023, title={Quantitative Modeling of the Short-Term Response to Nitrogen Availability that Coordinates Early Events in Lateral Root Initiation}, url={https://doi.org/10.1101/2023.12.05.570292}, DOI={10.1101/2023.12.05.570292}, abstractNote={Abstract}, author={Gaudinier, Allison and Broeck, Lisa Van and Moreno-Risueño, Miguel and Rodriguez-Medina, Joel and Sozzani, Rosangela and Brady, Siobhan M.}, year={2023}, month={Dec} }
 @article{beretta_franchini_din_lacchini_broeck_sozzani_orozco-arroyo_caporali_adam_jouannic_et al._2023, title={The ALOG family members OsG1L1 and OsG1L2 regulate inflorescence branching in rice}, volume={4}, ISSN={["1365-313X"]}, url={https://doi.org/10.1111/tpj.16229}, DOI={10.1111/tpj.16229}, abstractNote={SUMMARY}, journal={PLANT JOURNAL}, author={Beretta, Veronica M. and Franchini, Emanuela and Din, Israr Ud and Lacchini, Elia and Broeck, Lisa and Sozzani, Rosangela and Orozco-Arroyo, Gregorio and Caporali, Elisabetta and Adam, Helene and Jouannic, Stefan and et al.}, year={2023}, month={Apr} }
 @article{ortiz_de smet_sozzani_locke_2022, title={Field-grown soybean shows genotypic variation in physiological and seed composition responses to heat stress during seed development}, volume={195}, ISSN={0098-8472}, url={http://dx.doi.org/10.1016/j.envexpbot.2021.104768}, DOI={10.1016/j.envexpbot.2021.104768}, abstractNote={An average temperature increase between 2.6 and 4.8 °C, along with more frequent extreme temperatures, will challenge crop productivity by the end of the century. To investigate genotypic variation in soybean response to elevated temperature, six soybean (Glycine max) genotypes were subjected to elevated air temperature of + 4.5 °C above ambient for 28 days in open-top field chambers. Gas exchange and chlorophyll fluorescence were measured before and during heating and yield as well as seed composition were evaluated at maturity. Results show that long-term elevated air temperature increased nighttime respiration, increased the maximum velocity of carboxylation by Rubisco, impacted seed protein concentration, and reduced seed oil concentration across genotypes. The genotypes in this study varied in temperature responses for photosynthetic CO2 assimilation, stomatal conductance, photosystem II operating efficiency, quantum efficiency of CO2 assimilation, and seed protein concentration at maturity. These diverse responses among genotypes to elevated air temperature during seed development in the field, reveal the potential for soybean heat tolerance to be improved through breeding and underlines the importance of identifying efficient selection strategies for stress-tolerant crops.}, journal={Environmental and Experimental Botany}, publisher={Elsevier BV}, author={Ortiz, Anna C. and De Smet, Ive and Sozzani, Rosangela and Locke, Anna M.}, year={2022}, month={Mar}, pages={104768} }
 @article{thomas_broeck_spurney_sozzani_frank_2022, title={Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation}, volume={34}, ISSN={["1532-298X"]}, url={https://doi.org/10.1093/plcell/koab246}, DOI={10.1093/plcell/koab246}, abstractNote={Abstract}, number={1}, journal={PLANT CELL}, publisher={Oxford University Press (OUP)}, author={Thomas, Hannah and Broeck, Lisa and Spurney, Ryan and Sozzani, Rosangela and Frank, Margaret}, year={2022}, month={Jan}, pages={535–556} }
 @article{muhammad_clark_haque_williams_sozzani_long_2022, title={POPEYE intercellular localization mediates cell-specific iron deficiency responses}, volume={8}, ISSN={["1532-2548"]}, url={https://doi.org/10.1093/plphys/kiac357}, DOI={10.1093/plphys/kiac357}, abstractNote={Abstract}, journal={PLANT PHYSIOLOGY}, publisher={Oxford University Press (OUP)}, author={Muhammad, DurreShahwar and Clark, Natalie M. and Haque, Samiul and Williams, Cranos M. and Sozzani, Rosangela and Long, Terri A.}, year={2022}, month={Aug} }
 @article{adhikari_aryal_redpath_broeck_ashrafi_philbrick_jacobs_sozzani_louws_2022, title={RNA-Seq and Gene Regulatory Network Analyses Uncover Candidate Genes in the Early Defense to Two Hemibiotrophic Colletorichum spp. in Strawberry}, volume={12}, ISSN={["1664-8021"]}, DOI={10.3389/fgene.2021.805771}, abstractNote={Two hemibiotrophic pathogens, Colletotrichum acutatum (Ca) and C. gloeosporioides (Cg), cause anthracnose fruit rot and anthracnose crown rot in strawberry (Fragaria × ananassa Duchesne), respectively. Both Ca and Cg can initially infect through a brief biotrophic phase, which is associated with the production of intracellular primary hyphae that can infect host cells without causing cell death and establishing hemibiotrophic infection (HBI) or quiescent (latent infections) in leaf tissues. The Ca and Cg HBI in nurseries and subsequent distribution of asymptomatic infected transplants to fruit production fields is the major source of anthracnose epidemics in North Carolina. In the absence of complete resistance, strawberry varieties with good fruit quality showing rate-reducing resistance have frequently been used as a source of resistance to Ca and Cg. However, the molecular mechanisms underlying the rate-reducing resistance or susceptibility to Ca and Cg are still unknown. We performed comparative transcriptome analyses to examine how rate-reducing resistant genotype NCS 10-147 and susceptible genotype ‘Chandler’ respond to Ca and Cg and identify molecular events between 0 and 48 h after the pathogen-inoculated and mock-inoculated leaf tissues. Although plant response to both Ca and Cg at the same timepoint was not similar, more genes in the resistant interaction were upregulated at 24 hpi with Ca compared with those at 48 hpi. In contrast, a few genes were upregulated in the resistant interaction at 48 hpi with Cg. Resistance response to both Ca and Cg was associated with upregulation of MLP-like protein 44, LRR receptor-like serine/threonine-protein kinase, and auxin signaling pathway, whereas susceptibility was linked to modulation of the phenylpropanoid pathway. Gene regulatory network inference analysis revealed candidate transcription factors (TFs) such as GATA5 and MYB-10, and their downstream targets were upregulated in resistant interactions. Our results provide valuable insights into transcriptional changes during resistant and susceptible interactions, which can further facilitate assessing candidate genes necessary for resistance to two hemibiotrophic Colletotrichum spp. in strawberry.}, journal={FRONTIERS IN GENETICS}, author={Adhikari, Tika B. and Aryal, Rishi and Redpath, Lauren E. and Broeck, Lisa and Ashrafi, Hamid and Philbrick, Ashley N. and Jacobs, Raymond L. and Sozzani, Rosangela and Louws, Frank J.}, year={2022}, month={Mar} }
 @article{broeck_spurney_fisher_schwartz_clark_nguyen_madison_gobble_long_sozzani_2021, title={A hybrid model connecting regulatory interactions with stem cell divisions in the root}, volume={2}, url={https://doi.org/10.1017/qpb.2021.1}, DOI={10.1017/qpb.2021.1}, abstractNote={Abstract}, journal={Quantitative Plant Biology}, publisher={Cambridge University Press (CUP)}, author={Broeck, Lisa Van and Spurney, Ryan J. and Fisher, Adam P. and Schwartz, Michael and Clark, Natalie M. and Nguyen, Thomas T. and Madison, Imani and Gobble, Mariah and Long, Terri and Sozzani, Rosangela}, year={2021} }
 @article{roszak_heo_blob_toyokura_sugiyama_balaguer_lau_hamey_cirrone_madej_et al._2021, title={Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization}, volume={374}, ISSN={["1095-9203"]}, DOI={10.1126/science.aba5531}, abstractNote={Root meristem controls}, number={6575}, journal={SCIENCE}, author={Roszak, Pawel and Heo, Jung-Ok and Blob, Bernhard and Toyokura, Koichi and Sugiyama, Yuki and Balaguer, Maria Angels de Luis and Lau, Winnie W. Y. and Hamey, Fiona and Cirrone, Jacopo and Madej, Ewelina and et al.}, year={2021}, month={Dec}, pages={1577-+} }
 @misc{schwartz_peters_hunt_abdul-matin_broeck_sozzani_2021, title={Divide and Conquer: The Initiation and Proliferation of Meristems}, volume={40}, ISSN={["1549-7836"]}, url={http://dx.doi.org/10.1080/07352689.2021.1915228}, DOI={10.1080/07352689.2021.1915228}, abstractNote={Abstract In contrast to animals, which complete organogenesis early in their development, plants continuously produce organs, and structures throughout their entire lifecycle. Plants achieve the continuous growth of organs through the initiation and maintenance of meristems that populate the plant body. Plants contain two apical meristems, one at the shoot and one root, to produce the lateral organs of the shoot and the cell files of the root, respectively. Additional meristems within the plant produce branches while others produce the cell types within the vasculature system. Throughout development, plants must balance producing organs and maintaining their meristems, which requires tightly controlled regulations. This review focuses on the various plant meristems, how cells within these meristems maintain their identity, and particularly the molecular players that regulate stem cell maintenance. In addition, we summarize cell types which share molecular features with meristems, but do not follow the same rules regarding maintenance, including pericycle and rachis founder cells. Together, these populations of cells contribute to the entire organogenesis of plants.}, number={2}, journal={CRITICAL REVIEWS IN PLANT SCIENCES}, publisher={Informa UK Limited}, author={Schwartz, Michael F. and Peters, Rachel and Hunt, Aitch M. and Abdul-Matin, Abdul-Khaliq and Broeck, Lisa and Sozzani, Rosangela}, year={2021}, month={Mar}, pages={147–156} }
 @article{orozco-navarrete_song_casanal_sozzani_flors_sanchez-sevilla_trinkl_hoffmann_merchante_schwab_et al._2021, title={Down-regulation of Fra a 1.02 in strawberry fruits causes transcriptomic and metabolic changes compatible with an altered defense response}, volume={8}, ISSN={["2052-7276"]}, DOI={10.1038/s41438-021-00492-4}, abstractNote={Abstract}, number={1}, journal={HORTICULTURE RESEARCH}, author={Orozco-Navarrete, Begona and Song, Jina and Casanal, Ana and Sozzani, Rosangela and Flors, Victor and Sanchez-Sevilla, Jose F. and Trinkl, Johanna and Hoffmann, Thomas and Merchante, Catharina and Schwab, Wilfried and et al.}, year={2021}, month={Mar} }
 @article{thomas_broeck_spurney_sozzani_frank_2021, title={Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation}, volume={2}, url={https://doi.org/10.1101/2021.02.26.433082}, DOI={10.1101/2021.02.26.433082}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Thomas, Hannah and Broeck, Lisa Van and Spurney, Ryan and Sozzani, Rosangela and Frank, Margaret}, year={2021}, month={Feb} }
 @article{clark_nolan_wang_song_montes_valentine_guo_sozzani_yin_walley_2021, title={Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis}, volume={12}, ISSN={["2041-1723"]}, DOI={10.1038/s41467-021-26165-3}, abstractNote={Abstract}, number={1}, journal={NATURE COMMUNICATIONS}, author={Clark, Natalie M. and Nolan, Trevor M. and Wang, Ping and Song, Gaoyuan and Montes, Christian and Valentine, Conner T. and Guo, Hongqing and Sozzani, Rosangela and Yin, Yanhai and Walley, Justin W.}, year={2021}, month={Oct} }
 @article{betegon-putze_mercadal_bosch_planas-riverola_marques-bueno_vilarrasa-blasi_frigola_burkart_martinez_conesa_et al._2021, title={Precise transcriptional control of cellular quiescence by BRAVO/WOX5 complex in Arabidopsis roots}, volume={17}, ISSN={["1744-4292"]}, DOI={10.15252/msb.20209864}, abstractNote={Root growth and development are essential features for plant survival and the preservation of terrestrial ecosystems. In the Arabidopsis primary root apex, stem-cell specific transcription factors BRAVO and WOX5 co-localize at the Quiescent Center (QC) cells, where they repress cell division so that these cells can act as a reservoir to replenish surrounding stem cells, yet their molecular connection remains unknown. Here, by using empirical evidence and mathematical modeling, we establish the precise regulatory and molecular interactions between BRAVO and WOX5. We found that BRAVO and WOX5 regulate each other besides forming a transcription factor complex in the QC necessary to preserve overall root growth and architecture. Our results unveil the importance of transcriptional regulatory circuits at the quiescent and stem cells to the control of organ initiation and growth of plant tissues.}, number={6}, journal={MOLECULAR SYSTEMS BIOLOGY}, author={Betegon-Putze, Isabel and Mercadal, Josep and Bosch, Nadja and Planas-Riverola, Ainoa and Marques-Bueno, Mar and Vilarrasa-Blasi, Josep and Frigola, David and Burkart, Rebecca C. and Martinez, Cristina and Conesa, Ana and et al.}, year={2021}, month={Jun} }
 @article{spurney_schwartz_gobble_sozzani_broeck_2021, title={Spatiotemporal Gene Expression Profiling and Network Inference: A Roadmap for Analysis, Visualization, and Key Gene Identification}, volume={2328}, ISBN={["978-1-0716-1533-1"]}, ISSN={["1940-6029"]}, DOI={10.1007/978-1-0716-1534-8_4}, abstractNote={Gene expression data analysis and the prediction of causal relationships within gene regulatory networks (GRNs) have guided the identification of key regulatory factors and unraveled the dynamic properties of biological systems. However, drawing accurate and unbiased conclusions requires a comprehensive understanding of relevant tools, computational methods, and their workflows. The topics covered in this chapter encompass the entire workflow for GRN inference including: (1) experimental design; (2) RNA sequencing data processing; (3) differentially expressed gene (DEG) selection; (4) clustering prior to inference; (5) network inference techniques; and (6) network visualization and analysis. Moreover, this chapter aims to present a workflow feasible and accessible for plant biologists without a bioinformatics or computer science background. To address this need, TuxNet, a user-friendly graphical user interface that integrates RNA sequencing data analysis with GRN inference, is chosen for the purpose of providing a detailed tutorial.}, journal={MODELING TRANSCRIPTIONAL REGULATION}, author={Spurney, Ryan and Schwartz, Michael and Gobble, Mariah and Sozzani, Rosangela and Broeck, Lisa}, year={2021}, pages={47–65} }
 @article{crook_willoughby_hazak_okuda_vandermolen_soyars_cattaneo_clark_sozzani_hothorn_et al._2020, title={BAM1/2 receptor kinase signaling drives CLE peptide-mediated formative cell divisions in Arabidopsis roots}, volume={117}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.2018565117}, abstractNote={Significance}, number={51}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Crook, Ashley D. and Willoughby, Andrew C. and Hazak, Ora and Okuda, Satohiro and VanDerMolen, Kylie R. and Soyars, Cara L. and Cattaneo, Pietro and Clark, Natalie M. and Sozzani, Rosangela and Hothorn, Michael and et al.}, year={2020}, month={Dec}, pages={32750–32756} }
 @inbook{buckner_madison_melvin_long_sozzani_williams_2020, title={BioVision Tracker: A semi-automated image analysis software for spatiotemporal gene expression tracking in Arabidopsis thaliana}, volume={160}, ISBN={9780128215333}, ISSN={0091-679X}, url={http://dx.doi.org/10.1016/bs.mcb.2020.04.017}, DOI={10.1016/bs.mcb.2020.04.017}, abstractNote={Fluorescence microscopy can produce large quantities of data that reveal the spatiotemporal behavior of gene expression at the cellular level in plants. Automated or semi-automated image analysis methods are required to extract data from these images. These data are helpful in revealing spatial and/or temporal-dependent processes that influence development in the meristematic region of plant roots. Tracking spatiotemporal gene expression in the meristem requires the processing of multiple microscopy imaging channels (one channel used to image root geometry which serves as a reference for relating locations within the root, and one or more channels used to image fluorescent gene expression signals). Many automated image analysis methods rely on the staining of cell walls with fluorescent dyes to capture cellular geometry and overall root geometry. However, in long time-course imaging experiments, dyes may fade which hinders spatial assessment in image analysis. Here, we describe a procedure for analyzing 3D microscopy images to track spatiotemporal gene expression signals using the MATLAB-based BioVision Tracker software. This software requires either a fluorescence image or a brightfield image to analyze root geometry and a fluorescence image to capture and track temporal changes in gene expression.}, booktitle={Methods in Cell Biology}, publisher={Elsevier}, author={Buckner, Eli and Madison, Imani and Melvin, Charles and Long, Terri and Sozzani, Rosangela and Williams, Cranos}, year={2020}, pages={419–436} }
 @article{van norman_strader_sozzani_2020, title={Editorial overview: Directionality and precision - how signaling and gene regulation drive plant development and growth}, volume={57}, ISSN={["1879-0356"]}, DOI={10.1016/j.pbi.2020.11.001}, journal={CURRENT OPINION IN PLANT BIOLOGY}, author={Van Norman, Jaimie M. and Strader, Lucia C. and Sozzani, Rosangela}, year={2020}, month={Oct}, pages={A1–A3} }
 @article{broeck_spurney_fisher_schwartz_clark_nguyen_madison_gobble_long_sozzani_2020, title={Exchange of molecular and cellular information: a hybrid model that integrates stem cell divisions and key regulatory interactions}, url={https://doi.org/10.1101/2020.11.30.404426}, DOI={10.1101/2020.11.30.404426}, abstractNote={Abstract}, author={Broeck, Lisa Van and Spurney, Ryan J. and Fisher, Adam P. and Schwartz, Michael and Clark, Natalie M. and Nguyen, Thomas T. and Madison, Imani and Gobble, Mariah and Long, Terri and Sozzani, Rosangela}, year={2020}, month={Dec} }
 @article{van den broeck_gordon_inzé_williams_sozzani_2020, title={Gene Regulatory Network Inference: Connecting Plant Biology and Mathematical Modeling}, volume={11}, ISSN={1664-8021}, url={http://dx.doi.org/10.3389/fgene.2020.00457}, DOI={10.3389/fgene.2020.00457}, abstractNote={Plant responses to environmental and intrinsic signals are tightly controlled by multiple transcription factors (TFs). These TFs and their regulatory connections form gene regulatory networks (GRNs), which provide a blueprint of the transcriptional regulations underlying plant development and environmental responses. This review provides examples of experimental methodologies commonly used to identify regulatory interactions and generate GRNs. Additionally, this review describes network inference techniques that leverage gene expression data to predict regulatory interactions. These computational and experimental methodologies yield complex networks that can identify new regulatory interactions, driving novel hypotheses. Biological properties that contribute to the complexity of GRNs are also described in this review. These include network topology, network size, transient binding of TFs to DNA, and competition between multiple upstream regulators. Finally, this review highlights the potential of machine learning approaches to leverage gene expression data to predict phenotypic outputs.}, journal={Frontiers in Genetics}, publisher={Frontiers Media SA}, author={Van den Broeck, Lisa and Gordon, Max and Inzé, Dirk and Williams, Cranos and Sozzani, Rosangela}, year={2020}, month={May} }
 @inbook{madison_melvin_buckner_williams_sozzani_long_2020, title={MAGIC: Live imaging of cellular division in plant seedlings using lightsheet microscopy}, volume={160}, ISBN={9780128215333}, ISSN={0091-679X}, url={http://dx.doi.org/10.1016/bs.mcb.2020.04.004}, DOI={10.1016/bs.mcb.2020.04.004}, abstractNote={Imaging technologies have been used to understand plant genetic and developmental processes, from the dynamics of gene expression to tissue and organ morphogenesis. Although the field has advanced incredibly in recent years, gaps remain in identifying fine and dynamic spatiotemporal intervals of target processes, such as changes to gene expression in response to abiotic stresses. Lightsheet microscopy is a valuable tool for such studies due to its ability to perform long-term imaging at fine intervals of time and at low photo-toxicity of live vertically oriented seedlings. In this chapter, we describe a detailed method for preparing and imaging Arabidopsis thaliana seedlings for lightsheet microscopy via a Multi-Sample Imaging Growth Chamber (MAGIC), which allows simultaneous imaging of at least four samples. This method opens new avenues for acquiring imaging data at a high temporal resolution, which can be eventually probed to identify key regulatory time points and any spatial dependencies of target developmental processes.}, booktitle={Methods in Cell Biology}, publisher={Elsevier}, author={Madison, Imani and Melvin, Charles and Buckner, Eli and Williams, Cranos and Sozzani, Rosangela and Long, Terri}, year={2020}, pages={405–418} }
 @article{clark_van den broeck_guichard_stager_tanner_blilou_grossmann_iyer-pascuzzi_maizel_sparks_et al._2020, title={Novel Imaging Modalities Shedding Light on Plant Biology: Start Small and Grow Big}, volume={71}, ISSN={1543-5008 1545-2123}, url={http://dx.doi.org/10.1146/annurev-arplant-050718-100038}, DOI={10.1146/annurev-arplant-050718-100038}, abstractNote={ The acquisition of quantitative information on plant development across a range of temporal and spatial scales is essential to understand the mechanisms of plant growth. Recent years have shown the emergence of imaging methodologies that enable the capture and analysis of plant growth, from the dynamics of molecules within cells to the measurement of morphometricand physiological traits in field-grown plants. In some instances, these imaging methods can be parallelized across multiple samples to increase throughput. When high throughput is combined with high temporal and spatial resolution, the resulting image-derived data sets could be combined with molecular large-scale data sets to enable unprecedented systems-level computational modeling. Such image-driven functional genomics studies may be expected to appear at an accelerating rate in the near future given the early success of the foundational efforts reviewed here. We present new imaging modalities and review how they have enabled a better understanding of plant growth from the microscopic to the macroscopic scale. }, number={1}, journal={Annual Review of Plant Biology}, publisher={Annual Reviews}, author={Clark, Natalie M. and Van den Broeck, Lisa and Guichard, Marjorie and Stager, Adam and Tanner, Herbert G. and Blilou, Ikram and Grossmann, Guido and Iyer-Pascuzzi, Anjali S. and Maizel, Alexis and Sparks, Erin E. and et al.}, year={2020}, month={Apr}, pages={789–816} }
 @article{clark_fisher_berckmans_van den broeck_nelson_nguyen_bustillo-avendaño_zebell_moreno-risueno_simon_et al._2020, title={Protein complex stoichiometry and expression dynamics of transcription factors modulate stem cell division}, volume={117}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.2002166117}, DOI={10.1073/pnas.2002166117}, abstractNote={
            Stem cells divide and differentiate to form all of the specialized cell types in a multicellular organism. In the
            Arabidopsis
            root, stem cells are maintained in an undifferentiated state by a less mitotically active population of cells called the quiescent center (QC). Determining how the QC regulates the surrounding stem cell initials, or what makes the QC fundamentally different from the actively dividing initials, is important for understanding how stem cell divisions are maintained. Here we gained insight into the differences between the QC and the cortex endodermis initials (CEI) by studying the mobile transcription factor SHORTROOT (SHR) and its binding partner SCARECROW (SCR). We constructed an ordinary differential equation model of SHR and SCR in the QC and CEI which incorporated the stoichiometry of the SHR-SCR complex as well as upstream transcriptional regulation of SHR and SCR. Our model prediction, coupled with experimental validation, showed that high levels of the SHR-SCR complex are associated with more CEI division but less QC division. Furthermore, our model prediction allowed us to propose the putative upstream SHR regulators SEUSS and WUSCHEL-RELATED HOMEOBOX 5 and to experimentally validate their roles in QC and CEI division. In addition, our model established the timing of QC and CEI division and suggests that SHR repression of QC division depends on formation of the SHR homodimer. Thus, our results support that SHR-SCR protein complex stoichiometry and regulation of SHR transcription modulate the division timing of two different specialized cell types in the root stem cell niche.
          }, number={26}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Clark, Natalie M. and Fisher, Adam P. and Berckmans, Barbara and Van den Broeck, Lisa and Nelson, Emily C. and Nguyen, Thomas T. and Bustillo-Avendaño, Estefano and Zebell, Sophia G. and Moreno-Risueno, Miguel A. and Simon, Rüdiger and et al.}, year={2020}, month={Jun}, pages={15332–15342} }
 @article{spurney_broeck_clark_fisher_balaguer_sozzani_2020, title={tuxnet: a simple interface to process RNA sequencing data and infer gene regulatory networks}, volume={101}, ISSN={["1365-313X"]}, url={https://doi.org/10.1111/tpj.14558}, DOI={10.1111/tpj.14558}, abstractNote={Summary}, number={3}, journal={PLANT JOURNAL}, author={Spurney, Ryan J. and Broeck, Lisa and Clark, Natalie M. and Fisher, Adam P. and Balaguer, Maria A. de Luis and Sozzani, Rosangela}, year={2020}, month={Feb}, pages={716–730} }
 @article{buckner_madison_chou_matthiadis_melvin_sozzani_williams_long_2019, title={Automated Imaging, Tracking, and Analytics Pipeline for Differentiating Environmental Effects on Root Meristematic Cell Division}, volume={10}, ISSN={1664-462X}, url={http://dx.doi.org/10.3389/fpls.2019.01487}, DOI={10.3389/fpls.2019.01487}, abstractNote={Exposure of plants to abiotic stresses, whether individually or in combination, triggers dynamic changes to gene regulation. These responses induce distinct changes in phenotypic characteristics, enabling the plant to adapt to changing environments. For example, iron deficiency and heat stress have been shown to alter root development by reducing primary root growth and reducing cell proliferation, respectively. Currently, identifying the dynamic temporal coordination of genetic responses to combined abiotic stresses remains a bottleneck. This is, in part, due to an inability to isolate specific intervals in developmental time where differential activity in plant stress responses plays a critical role. Here, we observed that iron deficiency, in combination with temporary heat stress, suppresses the expression of iron deficiency-responsive pPYE::LUC (POPEYE::luciferase) and pBTS::LUC (BRUTUS::luciferase) reporter genes. Moreover, root growth was suppressed less under combined iron deficiency and heat stress than under either single stress condition. To further explore the interaction between pathways, we also created a computer vision pipeline to extract, analyze, and compare high-dimensional dynamic spatial and temporal cellular data in response to heat and iron deficiency stress conditions at high temporal resolution. Specifically, we used fluorescence light sheet microscopy to image Arabidopsis thaliana roots expressing CYCB1;1:GFP, a marker for cell entry into mitosis, every 20 min for 24 h exposed to either iron sufficiency, iron deficiency, heat stress, or combined iron deficiency and heat stress. Our pipeline extracted spatiotemporal metrics from these time-course data. These metrics showed that the persistency and timing of CYCB1;1:GFP signal were uniquely different under combined iron deficiency and heat stress conditions versus the single stress conditions. These metrics also indicated that the spatiotemporal characteristics of the CYCB1;1:GFP signal under combined stress were more dissimilar to the control response than the response seen under iron deficiency for the majority of the 24-h experiment. Moreover, the combined stress response was less dissimilar to the control than the response seen under heat stress. This indicated that pathways activated when the plant is exposed to both iron deficiency and heat stress affected CYCB1;1:GFP spatiotemporal function antagonistically}, journal={Frontiers in Plant Science}, publisher={Frontiers Media SA}, author={Buckner, Eli and Madison, Imani and Chou, Hsuan and Matthiadis, Anna and Melvin, Charles E. and Sozzani, Rosangela and Williams, Cranos and Long, Terri A.}, year={2019}, month={Nov} }
 @article{vallarino_merchante_sánchez‐sevilla_luis balaguer_pott_ariza_casañal_posé_vioque_amaya_et al._2019, title={Characterizing the involvement of
            FaMADS9
            in the regulation of strawberry fruit receptacle development}, volume={18}, ISBN={1467-7652}, ISSN={1467-7644 1467-7652}, url={http://dx.doi.org/10.1111/pbi.13257}, DOI={10.1111/pbi.13257}, abstractNote={Abstract}, number={4}, journal={Plant Biotechnology Journal}, publisher={Wiley}, author={Vallarino, José G. and Merchante, Catharina and Sánchez‐Sevilla, José F. and Luis Balaguer, María Angels and Pott, Delphine M. and Ariza, María T. and Casañal, Ana and Posé, David and Vioque, Amalia and Amaya, Iraida and et al.}, year={2019}, month={Oct}, pages={929–943} }
 @article{haque_ahmad_clark_williams_sozzani_2019, title={Computational prediction of gene regulatory networks in plant growth and development}, volume={47}, ISSN={1369-5266}, url={http://www.sciencedirect.com/science/article/pii/S1369526618300839}, DOI={10.1016/j.pbi.2018.10.005}, abstractNote={Plants integrate a wide range of cellular, developmental, and environmental signals to regulate complex patterns of gene expression. Recent advances in genomic technologies enable differential gene expression analysis at a systems level, allowing for improved inference of the network of regulatory interactions between genes. These gene regulatory networks, or GRNs, are used to visualize the causal regulatory relationships between regulators and their downstream target genes. Accordingly, these GRNs can represent spatial, temporal, and/or environmental regulations and can identify functional genes. This review summarizes recent computational approaches applied to different types of gene expression data to infer GRNs in the context of plant growth and development. Three stages of GRN inference are described: first, data collection and analysis based on the dataset type; second, network inference application based on data availability and proposed hypotheses; and third, validation based on in silico, in vivo, and in planta methods. In addition, this review relates data collection strategies to biological questions, organizes inference algorithms based on statistical methods and data types, discusses experimental design considerations, and provides guidelines for GRN inference with an emphasis on the benefits of integrative approaches, especially when a priori information is limited. Finally, this review concludes that computational frameworks integrating large-scale heterogeneous datasets are needed for a more accurate (e.g. fewer false interactions), detailed (e.g. discrimination between direct versus indirect interactions), and comprehensive (e.g. genetic regulation under various conditions and spatial locations) inference of GRNs.}, journal={Current Opinion in Plant Biology}, publisher={Elsevier BV}, author={Haque, Samiul and Ahmad, Jabeen S. and Clark, Natalie M. and Williams, Cranos M. and Sozzani, Rosangela}, year={2019}, month={Feb}, pages={96–105} }
 @article{smet_sevilem_luis balaguer_wybouw_mor_miyashima_blob_roszak_jacobs_boekschoten_et al._2019, title={DOF2.1 Controls Cytokinin-Dependent Vascular Cell Proliferation Downstream of TMO5/LHW}, volume={29}, ISSN={["1879-0445"]}, DOI={10.1016/j.cub.2018.12.041}, abstractNote={To create a three-dimensional structure, plants rely on oriented cell divisions and cell elongation. Oriented cell divisions are specifically important in procambium cells of the root to establish the different vascular cell types [1, 2]. These divisions are in part controlled by the auxin-controlled TARGET OF MONOPTEROS5 (TMO5) and LONESOME HIGHWAY (LHW) transcription factor complex [3-7]. Loss-of-function of tmo5 or lhw clade members results in strongly reduced vascular cell file numbers, whereas ectopic expression of both TMO5 and LHW can ubiquitously induce periclinal and radial cell divisions in all cell types of the root meristem. TMO5 and LHW interact only in young xylem cells, where they promote expression of two direct target genes involved in the final step of cytokinin (CK) biosynthesis, LONELY GUY3 (LOG3) and LOG4 [8, 9] Therefore, CK was hypothesized to act as a mobile signal from the xylem to trigger divisions in the neighboring procambium cells [3, 6]. To unravel how TMO5/LHW-dependent cytokinin regulates cell proliferation, we analyzed the transcriptional responses upon simultaneous induction of both transcription factors. Using inferred network analysis, we identified AT2G28510/DOF2.1 as a cytokinin-dependent downstream target gene. We further showed that DOF2.1 controls specific procambium cell divisions without inducing other cytokinin-dependent effects such as the inhibition of vascular differentiation. In summary, our results suggest that DOF2.1 and its closest homologs control vascular cell proliferation, thus leading to radial expansion of the root.}, number={3}, journal={CURRENT BIOLOGY}, author={Smet, Wouter and Sevilem, Iris and Luis Balaguer, Maria Angels and Wybouw, Brecht and Mor, Eliana and Miyashima, Shunsuke and Blob, Bernhard and Roszak, Pawel and Jacobs, Thomas B. and Boekschoten, Mark and et al.}, year={2019}, month={Feb}, pages={520-+} }
 @article{miyashima_roszak_sevilem_toyokura_blob_heo_mellor_help-rinta-rahko_otero_smet_et al._2019, title={Mobile PEAR transcription factors integrate hormone and miRNA cues to prime cambial growth}, volume={565}, ISSN={0028-0836, 1476-4687}, url={http://www.nature.com/articles/s41586-018-0839-y}, DOI={10.1038/s41586-018-0839-y}, abstractNote={Apical growth in plants initiates upon seed germination, whereas radial growth is primed only during early ontogenesis in procambium cells and activated later by the vascular cambium1. Although it is not known how radial growth is organized and regulated in plants, this system resembles the developmental competence observed in some animal systems, in which pre-existing patterns of developmental potential are established early on2,3. Here we show that in Arabidopsis the initiation of radial growth occurs around early protophloem-sieve-element cell files of the root procambial tissue. In this domain, cytokinin signalling promotes the expression of a pair of mobile transcription factors—PHLOEM EARLY DOF 1 (PEAR1) and PHLOEM EARLY DOF 2 (PEAR2)—and their four homologues (DOF6, TMO6, OBP2 and HCA2), which we collectively name PEAR proteins. The PEAR proteins form a short-range concentration gradient that peaks at protophloem sieve elements, and activates gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by the HD-ZIP III proteins, well-known polarity transcription factors4—the expression of which is concentrated in the more-internal domain of radially non-dividing procambial cells by the function of auxin, and mobile miR165 and miR166 microRNAs. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, and thereby establish a negative-feedback loop that forms a robust boundary that demarks the zone of cell division. Taken together, our data establish that during root procambial development there exists a network in which a module that links PEAR and HD-ZIP III transcription factors integrates spatial information of the hormonal domains and miRNA gradients to provide adjacent zones of dividing and more-quiescent cells, which forms a foundation for further radial growth. Radial growth in the roots of Arabidopsis, which is mediated by gene expression activated by the mobile PEAR1 and PEAR2 transcription factors, is initiated around protophloem-sieve-element cell files of procambial tissue.}, number={7740}, journal={Nature}, author={Miyashima, Shunsuke and Roszak, Pawel and Sevilem, Iris and Toyokura, Koichi and Blob, Bernhard and Heo, Jung-ok and Mellor, Nathan and Help-Rinta-Rahko, Hanna and Otero, Sofia and Smet, Wouter and et al.}, year={2019}, month={Jan}, pages={490–494} }
 @article{powers_holehouse_korasick_schreiber_clark_jing_emenecker_han_tycksen_hwang_et al._2019, title={Nucleo-cytoplasmic Partitioning of ARF Proteins Controls Auxin Responses in Arabidopsis thaliana}, volume={76}, ISSN={["1097-4164"]}, DOI={10.1016/j.molcel.2019.06.044}, abstractNote={The phytohormone auxin plays crucial roles in nearly every aspect of plant growth and development. The auxin response factor (ARF) transcription factor family regulates auxin-responsive gene expression and exhibits nuclear localization in regions of high auxin responsiveness. Here we show that the ARF7 and ARF19 proteins accumulate in micron-sized assemblies within the cytoplasm of tissues with attenuated auxin responsiveness. We found that the intrinsically disordered middle region and the folded PB1 interaction domain of ARFs drive protein assembly formation. Mutation of a single lysine within the PB1 domain abrogates cytoplasmic assemblies, promotes ARF nuclear localization, and results in an altered transcriptome and morphological defects. Our data suggest a model in which ARF nucleo-cytoplasmic partitioning regulates auxin responsiveness, providing a mechanism for cellular competence for auxin signaling.}, number={1}, journal={MOLECULAR CELL}, author={Powers, Samantha K. and Holehouse, Alex S. and Korasick, David A. and Schreiber, Katherine H. and Clark, Natalie M. and Jing, Hongwei and Emenecker, Ryan and Han, Soeun and Tycksen, Eric and Hwang, Ildoo and et al.}, year={2019}, month={Oct}, pages={177-+} }
 @article{clark_buckner_fisher_nelson_nguyen_simmons_balaguer_butler-smith_sheldon_bergmann_et al._2019, title={Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks}, volume={10}, ISSN={["2041-1723"]}, DOI={10.1038/s41467-019-13132-2}, abstractNote={Abstract}, journal={NATURE COMMUNICATIONS}, author={Clark, Natalie M. and Buckner, Eli and Fisher, Adam P. and Nelson, Emily C. and Nguyen, Thomas T. and Simmons, Abigail R. and Balaguer, Maria A. de Luis and Butler-Smith, Tiara and Sheldon, Parnell J. and Bergmann, Dominique C. and et al.}, year={2019}, month={Dec} }
 @article{di mambro_svolacchia_dello ioio_pierdonati_salvi_pedrazzini_vitale_perilli_sozzani_benfey_et al._2019, title={The Lateral Root Cap Acts as an Auxin Sink that Controls Meristem Size}, volume={29}, ISSN={["1879-0445"]}, DOI={10.1016/j.cub.2019.02.022}, abstractNote={Plant developmental plasticity relies on the activities of meristems, regions where stem cells continuously produce new cells [1]. The lateral root cap (LRC) is the outermost tissue of the root meristem [1], and it is known to play an important role during root development [2-6]. In particular, it has been shown that mechanical or genetic ablation of LRC cells affect meristem size [7, 8]; however, the molecular mechanisms involved are unknown. Root meristem size and, consequently, root growth depend on the position of the transition zone (TZ), a boundary that separates dividing from differentiating cells [9, 10]. The interaction of two phytohormones, cytokinin and auxin, is fundamental in controlling the position of the TZ [9, 10]. Cytokinin via the ARABIDOPSIS RESPONSE REGULATOR 1 (ARR1) control auxin distribution within the meristem, generating an instructive auxin minimum that positions the TZ [10]. We identify a cytokinin-dependent molecular mechanism that acts in the LRC to control the position of the TZ and meristem size. We show that auxin levels within the LRC cells depends on PIN-FORMED 5 (PIN5), a cytokinin-activated intracellular transporter that pumps auxin from the cytoplasm into the endoplasmic reticulum, and on irreversible auxin conjugation mediated by the IAA-amino synthase GRETCHEN HAGEN 3.17 (GH3.17). By titrating auxin in the LRC, the PIN5 and the GH3.17 genes control auxin levels in the entire root meristem. Overall, our results indicate that the LRC serves as an auxin sink that, under the control of cytokinin, regulates meristem size and root growth.}, number={7}, journal={CURRENT BIOLOGY}, author={Di Mambro, Riccardo and Svolacchia, Noemi and Dello Ioio, Raffaele and Pierdonati, Emanuela and Salvi, Elena and Pedrazzini, Emanuela and Vitale, Alessandro and Perilli, Serena and Sozzani, Rosangela and Benfey, Philip N. and et al.}, year={2019}, month={Apr}, pages={1199-+} }
 @article{asafen_clark_goyal_jacobsen_dima_chen_sozzani_reeves_2018, title={Dorsal/NF-κB exhibits a dorsal-to-ventral mobility gradient in the Drosophila embryo}, url={https://doi.org/10.1101/320754}, DOI={10.1101/320754}, abstractNote={Abstract Morphogen-mediated patterning is a highly dynamic developmental process. To obtain an accurate understanding of morphogen gradients, biophysical parameters such as protein diffusivities must be quantified in vivo . The dorsal-ventral (DV) patterning of early Drosophila embryos by the NF-κB homolog Dorsal (Dl) is an excellent system for understanding morphogen gradient formation. Dl gradient formation is controlled by the inhibitor Cactus/IκB (Cact), which regulates the nuclear import and diffusion of Dl protein. However, quantitative measurements of spatiotemporal Dl movement are currently lacking. Here, we use scanning fluorescence correlation spectroscopy to quantify the mobility of Dl. We find that the diffusivity of Dl varies along the DV axis, with lowest diffusivities on the ventral side, and the DV asymmetry in diffusivity is exclusive to the nuclei. Moreover, we also observe that nuclear export rates are lower in the ventral and lateral regions of the embryo. Both cross correlation spectroscopy measurements and a computational model of Dl/DNA binding suggest that DNA binding of Dl, which is more prevalent on the ventral side of the embryo, is correlated to a lower diffusivity and nuclear export rate. We propose that the variation in Dl/DNA binding along the DV axis is dependent on Cact binding Dl, which prevents Dl from binding DNA in dorsal and lateral regions of the embryo. Thus, our results highlight the complexity of morphogen gradient dynamics and the need for quantitative measurements of biophysical interactions in such systems.}, author={Asafen, Hadel Al and Clark, Natalie M. and Goyal, Etika and Jacobsen, Thomas and Dima, Sadia Siddika and Chen, Hung-Yuan and Sozzani, Rosangela and Reeves, Gregory T.}, year={2018}, month={May} }
 @article{o'lexy_kasai_clark_fujiwara_sozzani_gallagher_2018, title={Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose}, volume={69}, ISSN={["1460-2431"]}, DOI={10.1093/jxb/ery171}, abstractNote={As sessile organisms, plants continually modify their growth to adapt to changes in their environment. Here we show that significant changes in plasmodesmatal permeability underlie root responses to nutrient stress.}, number={15}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={O'Lexy, Ruthsabel and Kasai, Koji and Clark, Natalie and Fujiwara, Toru and Sozzani, Rosangela and Gallagher, Kimberly L.}, year={2018}, month={Jul}, pages={3715–3728} }
 @article{shibata_breuer_kawamura_clark_rymen_braidwood_morohashi_busch_benfey_sozzani_et al._2018, title={GTL1 and DF1 regulate root hair growth through transcriptional repression of ROOT HAIR DEFECTIVE 6-LIKE 4 in Arabidopsis}, volume={145}, ISSN={["1477-9129"]}, DOI={10.1242/dev.159707}, abstractNote={ABSTRACT}, number={3}, journal={DEVELOPMENT}, author={Shibata, Michitaro and Breuer, Christian and Kawamura, Ayako and Clark, Natalie M. and Rymen, Bart and Braidwood, Luke and Morohashi, Kengo and Busch, Wolfgang and Benfey, Philip N. and Sozzani, Rosangela and et al.}, year={2018}, month={Feb} }
 @inbook{clark_fisher_sozzani_2018, place={New York, NY}, series={Methods in Molecular Biology}, title={Identifying Differentially Expressed Genes Using Fluorescence-Activated Cell Sorting (FACS) and RNA Sequencing from Low Input Samples}, volume={1819}, ISBN={978-1-4939-8617-0 978-1-4939-8618-7}, url={http://link.springer.com/10.1007/978-1-4939-8618-7_6}, DOI={10.1007/978-1-4939-8618-7_6}, abstractNote={Cell type-specific gene expression profiles are useful for understanding genes that are important for the development of different tissues and organs. Here, we describe how to perform fluorescence-activated cell sorting (FACS) on Arabidopsis root protoplasts to isolate specific cell types in the root. We then detail how to extract and process RNA from a very low number of cells (≥40 cells) for RNA sequencing (RNA seq). Finally, we describe how to process RNA seq data using TopHat and how to identify differentially expressed genes using PoissonSeq.}, booktitle={Computational Cell Biology}, publisher={Springer New York}, author={Clark, Natalie M. and Fisher, Adam P. and Sozzani, Rosangela}, editor={Stechow, Louise von and Santos Delgado, AlbertoEditors}, year={2018}, pages={139–151}, collection={Methods in Molecular Biology} }
 @inproceedings{buckner_ottley_williams_luis balaguer_melvin_sozzani_2018, place={Honolulu, HI}, title={Tracking Gene Expression via Light Sheet Microscopy and Computer Vision in Living Organisms}, ISBN={978-1-5386-3646-6}, url={https://ieeexplore.ieee.org/document/8512416/}, DOI={10.1109/EMBC.2018.8512416}, abstractNote={Automated tracking of spatiotemporal gene expression using in vivo microscopy images have given great insight into understanding developmental processes in multicellular organisms. Many existing analysis tools rely on the fluorescent tagging of cell wall or cell nuclei localized proteins to assess position, orientation, and overall shape of an organism; information necessary for determining locations of gene expression activity. Particularly in plants, organism lines that have fluorescent tags can take months to develop, which can be time consuming and costly. We propose an automated solution for analyzing spatial characteristics of gene expression without the necessity of fluorescent tagged cell walls or cell nuclei. Our solution indicates, segments, and tracks gene expression using a fluorescent imaging channel of a light sheet microscope while determining gene expression location within an organism from a Brightfield (non-fluorescent) imaging channel. We use the images obtained from the Arabidopsis thaliana root as a proof of concept for our solution by studying the effects of heat shock stress on CYCLIN B1 protein production.}, booktitle={2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC)}, publisher={IEEE}, author={Buckner, Eli and Ottley, Chanae and Williams, Cranos and Luis Balaguer, Angels de and Melvin, Charles E. and Sozzani, Rosangela}, year={2018}, month={Jul}, pages={818–821} }
 @article{di mambro_de ruvo_pacifici_salvi_sozzani_benfey_busch_novak_ljung_di paola_et al._2017, title={Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root}, volume={114}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.1705833114}, abstractNote={Significance}, number={36}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Di Mambro, Riccardo and De Ruvo, Micol and Pacifici, Elena and Salvi, Elena and Sozzani, Rosangela and Benfey, Philip N. and Busch, Wolfgang and Novak, Ondrej and Ljung, Karin and Di Paola, Luisa and et al.}, year={2017}, month={Sep}, pages={E7641–E7649} }
 @article{liao_melvin_sozzani_jones_elston_jones_2017, title={Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling}, volume={12}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0190000}, abstractNote={In animal cells, activation of heterotrimeric G protein signaling generally occurs when the system’s cognate signal exceeds a threshold, whereas in plant cells, both the amount and the exposure time of at least one signal, D-glucose, are used toward activation. This unusual signaling property called Dose-Duration Reciprocity, first elucidated in the genetic model Arabidopsis thaliana, is achieved by a complex that is comprised of a 7-transmembrane REGULATOR OF G SIGNALING (RGS) protein (AtRGS1), a Gα subunit that binds and hydrolyzes nucleotide, a Gβγ dimer, and three WITH NO LYSINE (WNK) kinases. D-glucose is one of several signals such as salt and pathogen-derived molecular patterns that operates through this protein complex to activate G protein signaling by WNK kinase transphosphorylation of AtRGS1. Because WNK kinases compete for the same substrate, AtRGS1, we hypothesize that activation is sensitive to the AtRGS1 amount and that modulation of the AtRGS1 pool affects the response to the stimulant. Mathematical simulation revealed that the ratio of AtRGS1 to the kinase affects system sensitivity to D-glucose, and therefore illustrates how modulation of the cellular AtRGS1 level is a means to change signal-induced activation. AtRGS1 levels change under tested conditions that mimic physiological conditions therefore, we propose a previously-unknown mechanism by which plants react to changes in their environment.}, number={12}, journal={PLOS ONE}, author={Liao, Kang-Ling and Melvin, Charles E. and Sozzani, Rosangela and Jones, Roger D. and Elston, Timothy C. and Jones, Alan M.}, year={2017}, month={Dec} }
 @article{wendrich_moller_li_saiga_sozzani_benfey_de rybel_weijers_2017, title={Framework for gradual progression of cell ontogeny in the Arabidopsis root meristem}, volume={114}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.1707400114}, abstractNote={Significance}, number={42}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Wendrich, Jos R. and Moller, Barbara K. and Li, Song and Saiga, Shunsuke and Sozzani, Rosangela and Benfey, Philip N. and De Rybel, Bert and Weijers, Dolf}, year={2017}, month={Oct}, pages={E8922–E8929} }
 @article{coneva_frank_balaguer_li_sozzani_chitwood_2017, title={Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted Tomato Solanum pennellii}, volume={175}, ISSN={["1532-2548"]}, DOI={10.1104/pp.17.00790}, abstractNote={Leaf thickness in desert-adapted tomato is characterized by the anatomic and transcriptional alterations that are uncovered by QTL analysis of introgression lines. Thicker leaves allow plants to grow in water-limited conditions. However, our understanding of the genetic underpinnings of this highly functional leaf shape trait is poor. We used a custom-built confocal profilometer to directly measure leaf thickness in a set of introgression lines (ILs) derived from the desert tomato Solanum pennellii and identified quantitative trait loci. We report evidence of a complex genetic architecture of this trait and roles for both genetic and environmental factors. Several ILs with thick leaves have dramatically elongated palisade mesophyll cells and, in some cases, increased leaf ploidy. We characterized the thick IL2-5 and IL4-3 in detail and found increased mesophyll cell size and leaf ploidy levels, suggesting that endoreduplication underpins leaf thickness in tomato. Next, we queried the transcriptomes and inferred dynamic Bayesian networks of gene expression across early leaf ontogeny in these lines to compare the molecular networks that pattern leaf thickness. We show that thick ILs share S. pennellii-like expression profiles for putative regulators of cell shape and meristem determinacy as well as a general signature of cell cycle-related gene expression. However, our network data suggest that leaf thickness in these two lines is patterned at least partially by distinct mechanisms. Consistent with this hypothesis, double homozygote lines combining introgression segments from these two ILs show additive phenotypes, including thick leaves, higher ploidy levels, and larger palisade mesophyll cells. Collectively, these data establish a framework of genetic, anatomical, and molecular mechanisms that pattern leaf thickness in desert-adapted tomato.}, number={1}, journal={PLANT PHYSIOLOGY}, author={Coneva, Viktoriya and Frank, Margaret H. and Balaguer, Maria A. de Luis and Li, Mao and Sozzani, Rosangela and Chitwood, Daniel H.}, year={2017}, month={Sep}, pages={376–391} }
 @inbook{de luis balaguer_sozzani_2017, place={New York, NY}, series={Methods in Molecular Biology}, title={Inferring Gene Regulatory Networks in the Arabidopsis Root Using a Dynamic Bayesian Network Approach}, volume={1629}, ISBN={978-1-4939-7124-4 978-1-4939-7125-1}, url={http://link.springer.com/10.1007/978-1-4939-7125-1_21}, DOI={10.1007/978-1-4939-7125-1_21}, abstractNote={Gene regulatory network (GRN) models have been shown to predict and represent interactions among sets of genes. Here, we first show the basic steps to implement a simple but computationally efficient algorithm to infer GRNs based on dynamic Bayesian networks (DBNs), and we then explain how to approximate DBN-based GRN models with continuous models. In addition, we show a MATLAB implementation of the key steps of this method, which we use to infer an Arabidopsis root GRN.}, booktitle={Plant Gene Regulatory Networks}, publisher={Springer New York}, author={Luis Balaguer, Maria Angels de and Sozzani, Rosangela}, editor={Kaufmann, Kerstin and Mueller-Roeber, BerndEditors}, year={2017}, pages={331–348}, collection={Methods in Molecular Biology} }
 @inbook{clark_sozzani_2017, place={New York, NY}, series={Methods in Molecular Biology}, title={Measuring Protein Movement, Oligomerization State, and Protein–Protein Interaction in Arabidopsis Roots Using Scanning Fluorescence Correlation Spectroscopy (Scanning FCS)}, volume={1610}, ISBN={978-1-4939-7001-8 978-1-4939-7003-2}, url={http://link.springer.com/10.1007/978-1-4939-7003-2_16}, DOI={10.1007/978-1-4939-7003-2_16}, abstractNote={Scanning fluorescence correlation spectroscopy (scanning FCS) can be used to determine protein movement, oligomerization state, and protein–protein interaction. Here, we describe how to use the scanning FCS techniques of raster image correlation spectroscopy (RICS) and pair correlation function (pCF) to determine the rate and direction of protein movement. In addition, we detail how number and brightness (N&B) and cross-correlation analyses can be used to determine oligomerization state and binding ratios of protein complexes. We specifically describe how to acquire suitable images for scanning FCS analysis using the model plant Arabidopsis and how to perform the various analyses using the SimFCS software.}, booktitle={Plant Genomics}, publisher={Springer New York}, author={Clark, Natalie M. and Sozzani, Rosangela}, editor={Busch, WolfgangEditor}, year={2017}, pages={251–266}, collection={Methods in Molecular Biology} }
 @article{balaguer_fisher_clark_fernandez-espinosa_moller_weijers_lohmann_williams_lorenzo_sozzani_et al._2017, title={Predicting gene regulatory networks by combining spatial and temporal gene expression data in Arabidopsis root stem cells}, volume={114}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.1707566114}, abstractNote={Significance}, number={36}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Balaguer, M. A. D. and Fisher, A. P. and Clark, N. M. and Fernandez-Espinosa, M. G. and Moller, B. K. and Weijers, D. and Lohmann, J. U. and Williams, C. and Lorenzo, O. and Sozzani, Rosangela and et al.}, year={2017}, month={Sep}, pages={E7632–E7640} }
 @article{fisher_sozzani_2016, title={Gene and networks regulating the root stem cell niche of Arabidopsis}, volume={29}, ISSN={["1879-0356"]}, DOI={10.1016/j.pbi.2015.11.002}, abstractNote={Stem cells are the source of different cell types and tissues in all multicellular organisms. In plants, the balance between stem cell self-renewal and differentiation of their progeny is crucial for correct tissue and organ formation. How transcriptional programs precisely control stem cell maintenance and identity, and what are the regulatory programs influencing stem cell asymmetric cell division (ACD), are key questions that researchers have sought to address for the past decade. Successful efforts in genetic, molecular, and developmental biology, along with mathematical modeling, have identified some of the players involved in stem cell regulation. In this review, we will discuss several studies that characterized many of the genetic programs and molecular mechanisms regulating stem cell ACD and their identity in the Arabidopsis root. We will also highlight how the growing use of mathematical modeling provides a comprehensive and quantitative perspective on the design rules governing stem cell ACDs.}, journal={Curr Opin Plant Biol}, author={Fisher, A.P. and Sozzani, R.}, year={2016}, month={Feb}, pages={38–43} }
 @article{slattery_grennan_sivaguru_sozzani_ort_2016, title={Light sheet microscopy reveals more gradual light attenuation in light-green versus dark-green soybean leaves}, volume={67}, ISSN={["1460-2431"]}, DOI={10.1093/jxb/erw246}, abstractNote={Highlight Light sheet microscopy, a novel approach to quantifying light profiles, showed more gradual light attenuation in light-green soybean leaves compared to dark-green soybean.}, number={15}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={Slattery, Rebecca A. and Grennan, Aleel K. and Sivaguru, Mayandi and Sozzani, Rosangela and Ort, Donald R.}, year={2016}, month={Aug}, pages={4697–4709} }
 @article{de luis balaguer_ramos-pezzotti_rahhal_melvin_johannes_horn_sozzani_2016, title={Multi-sample Arabidopsis Growth and Imaging Chamber (MAGIC) for long term imaging in the ZEISS Lightsheet Z.1}, volume={419}, ISSN={1095-564X}, DOI={10.1016/j.ydbio.2016.05.029}, abstractNote={Time-course imaging experiments on live organisms are critical for understanding the dynamics of growth and development. Light-sheet microscopy has advanced the field of long-term imaging of live specimens by significantly reducing photo-toxicity and allowing fast acquisition of three-dimensional data over time. However, current light-sheet technology does not allow the imaging of multiple plant specimens in parallel. To achieve higher throughput, we have developed a Multi-sample Arabidopsis Growth and Imaging Chamber (MAGIC) that provides near-physiological imaging conditions and allows high-throughput time-course imaging experiments in the ZEISS Lightsheet Z.1. Here, we illustrate MAGIC's imaging capabilities by following cell divisions, as an indicator of plant growth and development, over prolonged time periods. To automatically quantify the number of cell divisions in long-term experiments, we present a FIJI-based image processing pipeline. We demonstrate that plants imaged with our chamber undergo cell divisions for >16 times longer than those with the glass capillary system supplied by the ZEISS Z1.}, number={1}, journal={Developmental Biology}, author={Luis Balaguer, Maria Angels de and Ramos-Pezzotti, Marina and Rahhal, Morjan B. and Melvin, Charles E. and Johannes, Eva and Horn, Timothy J. and Sozzani, Rosangela}, year={2016}, month={Jan}, pages={19–25} }
 @article{clark_hinde_winter_fisher_crosti_blilou_gratton_benfey_sozzani_2016, title={Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy}, volume={5}, journal={Elife}, author={Clark, N. M. and Hinde, E. and Winter, C. M. and Fisher, A. P. and Crosti, G. and Blilou, I. and Gratton, E. and Benfey, P. N. and Sozzani, R.}, year={2016} }
 @article{moreno-risueno_sozzani_yardimici_petricka_vernoux_blilou_alonso_winter_ohler_scheres_et al._2015, title={Bird and Scarecrow proteins organize tissue formation in Arabidopsis roots}, volume={350}, ISSN={["1095-9203"]}, DOI={10.1126/science.aad1171}, abstractNote={Multifunctional root regulators}, number={6259}, journal={Science}, author={Moreno-Risueno, MA. and Sozzani, R. and Yardimici, GG. and Petricka, JJ. and Vernoux, T. and Blilou, I. and Alonso, J. and Winter, CM. and Ohler, U. and Scheres, B. and et al.}, year={2015}, pages={426–430} }
 @misc{sozzani_busch_spalding_benfey_2014, title={Advanced imaging techniques for the study of plant growth and development}, volume={19}, ISSN={["1878-4372"]}, DOI={10.1016/j.tplants.2013.12.003}, abstractNote={A variety of imaging methodologies are being used to collect data for quantitative studies of plant growth and development from living plants. Multi-level data, from macroscopic to molecular, and from weeks to seconds, can be acquired. Furthermore, advances in parallelized and automated image acquisition enable the throughput to capture images from large populations of plants under specific growth conditions. Image-processing capabilities allow for 3D or 4D reconstruction of image data and automated quantification of biological features. These advances facilitate the integration of imaging data with genome-wide molecular data to enable systems-level modeling.}, number={5}, journal={TRENDS IN PLANT SCIENCE}, author={Sozzani, Rosangela and Busch, Wolfgang and Spalding, Edgar P. and Benfey, Philip N.}, year={2014}, month={May}, pages={304–310} }
 @misc{clark_balaguer_sozzani_2014, title={Experimental data and computational modeling link auxin gradient and development in the Arabidopsis root}, volume={5}, journal={Frontiers in Plant Science}, author={Clark, N. M. and Balaguer, M. A. D. and Sozzani, R.}, year={2014} }
 @article{gallagher_sozzani_lee_2014, title={Intercellular Protein Movement: Deciphering the Language of Development}, volume={30}, ISSN={["1530-8995"]}, DOI={10.1146/annurev-cellbio-100913-012915}, abstractNote={ Development in multicellular organisms requires the coordinated production of a large number of specialized cell types through sophisticated signaling mechanisms. Non-cell-autonomous signals are one of the key mechanisms by which organisms coordinate development. In plants, intercellular movement of transcription factors and other mobile signals, such as hormones and peptides, is essential for normal development. Through a combination of different approaches, a large number of non-cell-autonomous signals that control plant development have been identified. We review some of the transcriptional regulators that traffic between cells, as well as how changes in symplasmic continuity affect and are affected by development. We also review current models for how mobile signals move via plasmodesmata and how movement is inhibited. Finally, we consider challenges in and new tools for studying protein movement. }, journal={ANNUAL REVIEW OF CELL AND DEVELOPMENTAL BIOLOGY, VOL 30}, author={Gallagher, Kimberly L. and Sozzani, Rosangela and Lee, Chin-Mei}, year={2014}, pages={207–233} }
 @misc{kajala_ramakrishna_fisher_bergmann_de smet_sozzani_weijers_brady_2014, title={Omics and modelling approaches for understanding regulation of asymmetric cell divisions in arabidopsis and other angiosperm plants}, volume={113}, ISSN={["1095-8290"]}, DOI={10.1093/aob/mcu065}, abstractNote={BACKGROUND
Asymmetric cell divisions are formative divisions that generate daughter cells of distinct identity. These divisions are coordinated by either extrinsic ('niche-controlled') or intrinsic regulatory mechanisms and are fundamentally important in plant development.


SCOPE
This review describes how asymmetric cell divisions are regulated during development and in different cell types in both the root and the shoot of plants. It further highlights ways in which omics and modelling approaches have been used to elucidate these regulatory mechanisms. For example, the regulation of embryonic asymmetric divisions is described, including the first divisions of the zygote, formative vascular divisions and divisions that give rise to the root stem cell niche. Asymmetric divisions of the root cortex endodermis initial, pericycle cells that give rise to the lateral root primordium, procambium, cambium and stomatal cells are also discussed. Finally, a perspective is provided regarding the role of other hormones or regulatory molecules in asymmetric divisions, the presence of segregated determinants and the usefulness of modelling approaches in understanding network dynamics within these very special cells.


CONCLUSIONS
Asymmetric cell divisions define plant development. High-throughput genomic and modelling approaches can elucidate their regulation, which in turn could enable the engineering of plant traits such as stomatal density, lateral root development and wood formation.}, number={7}, journal={ANNALS OF BOTANY}, author={Kajala, Kaisa and Ramakrishna, Priya and Fisher, Adam and Bergmann, Dominique C. and De Smet, Ive and Sozzani, Rosangela and Weijers, Dolf and Brady, Siobhan M.}, year={2014}, month={Jun}, pages={1083–1105} }
 @misc{sozzani_iyer-pascuzzi_2014, title={Postembryonic control of root meristem growth and development}, volume={17}, ISSN={["1879-0356"]}, DOI={10.1016/j.pbi.2013.10.005}, abstractNote={Organ development in multicellular organisms is dependent on the proper balance between cell proliferation and differentiation. In the Arabidopsis root apical meristem, meristem growth is the result of cell divisions in the proximal meristem and cell differentiation in the elongation and differentiation zones. Hormones, transcription factors and small peptides underpin the molecular mechanisms governing these processes. Computer modeling has aided our understanding of the dynamic interactions involved in stem cell maintenance and meristem activity. Here we review recent advances in our understanding of postembryonic root stem cell maintenance and control of meristem size.}, journal={CURRENT OPINION IN PLANT BIOLOGY}, author={Sozzani, Rosangela and Iyer-Pascuzzi, Anjali}, year={2014}, month={Feb}, pages={7–12} }
 @article{moubayidin_di mambro_sozzani_pacifici_salvi_terpstra_bao_van dijken_dello ioio_perilli_et al._2013, title={Spatial Coordination between Stem Cell Activity and Cell Differentiation in the Root Meristem}, volume={26}, ISSN={15345807}, url={https://linkinghub.elsevier.com/retrieve/pii/S1534580713003882}, DOI={10.1016/j.devcel.2013.06.025}, abstractNote={A critical issue in development is the coordination of the activity of stem cell niches with differentiation of their progeny to ensure coherent organ growth. In the plant root, these processes take place at opposite ends of the meristem and must be coordinated with each other at a distance. Here, we show that in Arabidopsis, the gene SCR presides over this spatial coordination. In the organizing center of the root stem cell niche, SCR directly represses the expression of the cytokinin-response transcription factor ARR1, which promotes cell differentiation, controlling auxin production via the ASB1 gene and sustaining stem cell activity. This allows SCR to regulate, via auxin, the level of ARR1 expression in the transition zone where the stem cell progeny leaves the meristem, thus controlling the rate of differentiation. In this way, SCR simultaneously controls stem cell division and differentiation, ensuring coherent root growth.}, number={4}, journal={Developmental Cell}, author={Moubayidin, Laila and Di Mambro, Riccardo and Sozzani, Rosangela and Pacifici, Elena and Salvi, Elena and Terpstra, Inez and Bao, Dongping and van Dijken, Anja and Dello Ioio, Raffaele and Perilli, Serena and et al.}, year={2013}, month={Aug}, pages={405–415} }
 @article{cruz-ramírez_díaz-triviño_blilou_grieneisen_sozzani_zamioudis_miskolczi_nieuwland_benjamins_dhonukshe_et al._2012, title={A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division}, volume={150}, ISSN={1097-4172}, DOI={10.1016/j.cell.2012.07.017}, abstractNote={<h2>Summary</h2> In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the <i>Arabidopsis</i> root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting <i>CYCD6;1</i> transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a "flip flop" that constrains asymmetric cell division to the stem cell region.}, number={5}, journal={Cell}, author={Cruz-Ramírez, Alfredo and Díaz-Triviño, Sara and Blilou, Ikram and Grieneisen, Verônica A. and Sozzani, Rosangela and Zamioudis, Christos and Miskolczi, Pál and Nieuwland, Jeroen and Benjamins, René and Dhonukshe, Pankaj and et al.}, year={2012}, month={Aug}, pages={1002–1015} }
 @article{liberman_sozzani_benfey_2012, title={Integrative systems biology: an attempt to describe a simple weed}, volume={15}, ISSN={1879-0356}, DOI={10.1016/j.pbi.2012.01.004}, abstractNote={Genome-scale studies hold great promise for revealing novel plant biology. Because of the complexity of these techniques, numerous considerations need to be made before embarking on a study. Here we focus on the Arabidopsis model system because of the wealth of available genome-scale data. Many approaches are available that provide genome-scale information regarding the state of a given organism (e.g. genomics, epigenomics, transcriptomics, proteomics, metabolomics interactomics, ionomics, phenomics, etc.). Integration of all of these types of data will be necessary for a comprehensive description of Arabidopsis. In this review we propose that 'triangulation' among transcriptomics, proteomics and metabolomics is a meaningful approach for beginning this integrative analysis and uncovering a systems level perspective of Arabidopsis biology.}, number={2}, journal={Current Opinion in Plant Biology}, author={Liberman, Louisa M. and Sozzani, Rosangela and Benfey, Philip N.}, year={2012}, month={Apr}, pages={162–167} }
 @article{engstrom_andersen_gumulak-smith_hu_orlova_sozzani_bowman_2011, title={Arabidopsis homologs of the petunia hairy meristem gene are required for maintenance of shoot and root indeterminacy}, volume={155}, ISSN={1532-2548}, DOI={10.1104/pp.110.168757}, abstractNote={Abstract}, number={2}, journal={Plant Physiology}, author={Engstrom, Eric M. and Andersen, Carl M. and Gumulak-Smith, Juliann and Hu, John and Orlova, Evguenia and Sozzani, Rosangela and Bowman, John L.}, year={2011}, month={Feb}, pages={735–750} }
 @article{sozzani_benfey_2011, title={High-throughput phenotyping of multicellular organisms: finding the link between genotype and phenotype}, volume={12}, ISSN={1474-760X}, url={https://doi.org/10.1186/gb-2011-12-3-219}, DOI={10.1186/gb-2011-12-3-219}, abstractNote={High-throughput phenotyping approaches (phenomics) are being combined with genome-wide genetic screens to identify alterations in phenotype that result from gene inactivation. Here we highlight promising technologies for 'phenome-scale' analyses in multicellular organisms.}, number={3}, journal={Genome Biology}, author={Sozzani, Rosangela and Benfey, Philip N.}, year={2011}, month={Mar}, pages={219} }
 @article{sozzani_cui_moreno-risueno_busch_van norman_vernoux_brady_dewitte_murray_benfey_2010, title={Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth}, volume={466}, ISSN={0028-0836 1476-4687}, url={http://dx.doi.org/10.1038/nature09143}, DOI={10.1038/nature09143}, abstractNote={The development of multicellular organisms relies on the coordinated control of cell divisions leading to proper patterning and growth. The molecular mechanisms underlying pattern formation, particularly the regulation of formative cell divisions, remain poorly understood. In Arabidopsis, formative divisions generating the root ground tissue are controlled by SHORTROOT (SHR) and SCARECROW (SCR). Here we show, using cell-type-specific transcriptional effects of SHR and SCR combined with data from chromatin immunoprecipitation-based microarray experiments, that SHR regulates the spatiotemporal activation of specific genes involved in cell division. Coincident with the onset of a specific formative division, SHR and SCR directly activate a D-type cyclin; furthermore, altering the expression of this cyclin resulted in formative division defects. Our results indicate that proper pattern formation is achieved through transcriptional regulation of specific cell-cycle genes in a cell-type- and developmental-stage-specific context. Taken together, we provide evidence for a direct link between developmental regulators, specific components of the cell-cycle machinery and organ patterning.}, number={7302}, journal={Nature}, publisher={Springer Science and Business Media LLC}, author={Sozzani, R. and Cui, H. and Moreno-Risueno, M. A. and Busch, W. and Van Norman, J. M. and Vernoux, T. and Brady, S. M. and Dewitte, W. and Murray, J. A. H. and Benfey, P. N.}, year={2010}, month={Jul}, pages={128–132} }
 @article{sozzani_maggio_giordo_umana_ascencio-ibañez_hanley-bowdoin_bergounioux_cella_albani_2010, title={The E2FD/DEL2 factor is a component of a regulatory network controlling cell proliferation and development in Arabidopsis}, volume={72}, ISSN={1573-5028}, DOI={10.1007/s11103-009-9577-8}, abstractNote={An emerging view of plant cell cycle regulators, including the E2F transcription factors, implicates them in the integration of cell proliferation and development. Arabidopsis encodes six E2F proteins that can act as activators or repressors of E2F-responsive genes. E2FA, E2FB and E2FC interact with the retinoblastoma-like RBR protein and bind to DNA together with their DP partners. In contrast, E2FD, E2FE and E2FF (also known as DEL2, DEL1 and DEL3) are atypical E2Fs that possess duplicated DNA binding regions, lack trans-activating and RBR-binding domains and are believed to act as transcriptional inhibitors/repressors. E2FE/DEL1 has been shown to inhibit the endocycle and E2FF/DEL3 appears to control cell expansion but the role of E2FD/DEL2 has not been reported so far. In this study, we investigated the expression of E2FD/DEL2 and analysed the accumulation of its product. These studies revealed that E2FD/DEL2 accumulation is subject to negative post-translational regulation mediated by the plant hormone auxin. Moreover, the analysis of mutant and transgenic plants characterized by altered expression of E2FD/DEL2 has revealed that this atypical E2F can affect plant growth by promoting cell proliferation and repressing cell elongation. Overexpression of E2FD/DEL2 increased the expression of E2FA, E2FB and E2FE/DEL1 whereas its inactivation led to the up-regulation of genes encoding repressors of cell division. These results suggest that E2FD/DEL2 is part of a regulatory network that controls the balance between cell proliferation and development in Arabidopsis.}, number={4-5}, journal={Plant Molecular Biology}, author={Sozzani, Rosangela and Maggio, Caterina and Giordo, Roberta and Umana, Elisabetta and Ascencio-Ibañez, Jose Trinidad and Hanley-Bowdoin, Linda and Bergounioux, Catherine and Cella, Rino and Albani, Diego}, year={2010}, month={Mar}, pages={381–395} }
 @article{sozzani_cui_moreno-risueno_busch_van norman_vernoux_brady_dewitte_murray_benfey_2010, title={The SHR/SCR pathway directly activates genes involved in asymmetric cell division in the Arabidopsis root}, volume={466}, number={7302}, journal={Nature}, author={Sozzani, R. and Cui, H. and Moreno-Risueno, M.A. and Busch, W. and Van Norman, J.M. and Vernoux, T. and Brady, S.M. and Dewitte, W. and Murray, J.A. and Benfey, P.N.}, year={2010}, pages={128–132} }
 @article{benfey_cui_twigg_long_iyer-pascuzzi_tsukagoshi_sozzani_jackson_van norman_moreno-risueno_2009, title={Development rooted in interwoven networks}, volume={331}, ISSN={0012-1606}, url={http://dx.doi.org/10.1016/j.ydbio.2009.05.012}, DOI={10.1016/j.ydbio.2009.05.012}, abstractNote={Freshwater planarians appear to utilize inductive signals to specify their germ cell lineage: germ cells are believed to form post-embryonically from the pluripotent somatic stem cells, known as neoblasts. Previously, we identified a planarian homolog of nanos (Smed-nanos) and demonstrated by RNA interference (RNAi) that this gene is required for the development, maintenance, and regeneration of planarian germ cells. We have performed microarray analyses to compare gene expression profiles between planarians with early germ cells and those without them. We identified ∼300 genes that are significantly down-regulated in animals lacking early germ cells. This data set contains genes implicated in germ cell development in other organisms, conserved genes not yet reported to have germ cell-related functions, and novel genes. Analysis using putative domain functions (Clusters of Orthologous Groups) suggested diverse molecular functions, including cytoskeletal components, metabolism, RNA processing and modification, transcription, as well as signal transduction. Top hits have been validated by in situ hybridization. Functional analyses of these genes via RNA interference are being carried out. Thus far, we have identified several genes that, when knocked down by RNAi, cause various defects in germ cell development, including: impaired testes development; loss of spermatogonial stem cells; meiotic failure; and defects in sperm elongation. This work will contribute to our knowledge of conserved regulators of germ cell differentiation. (Supported by NIH-NICHD R01-HD043403.)}, number={2}, journal={Developmental Biology}, publisher={Elsevier BV}, author={Benfey, Philip N. and Cui, Hongchang and Twigg, Richard and Long, Terri and Iyer-Pascuzzi, Anjali and Tsukagoshi, Hironaka and Sozzani, Rosangela and Jackson, Terry and Van Norman, Jaimie and Moreno-Risueno, Miguel}, year={2009}, month={Jul}, pages={386} }
 @article{ni_sozzani_blanchet_domenichini_reuzeau_cella_bergounioux_raynaud_2009, title={The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function}, volume={184}, ISSN={1469-8137}, DOI={10.1111/j.1469-8137.2009.02961.x}, abstractNote={* Minichromosome maintenance (MCM) proteins are subunits of the pre-replication complex that probably function as DNA helicases during the S phase of the cell cycle. Here, we investigated the function of AtMCM2 in Arabidopsis. * To gain an insight into the function of AtMCM2, we combined loss- and gain-of-function approaches. To this end, we analysed two null alleles of AtMCM2, and generated transgenic plants expressing AtMCM2 downstream of the constitutive 35S promoter. * Disruption of AtMCM2 is lethal at a very early stage of embryogenesis, whereas its over-expression results in reduced growth and inhibition of endoreduplication. In addition, over-expression of AtMCM2 induces the formation of additional initials in the columella root cap. In the plt1,2 mutant, defective for root apical meristem maintenance, over-expression of AtMCM2 induces lateral root initiation close to the root tip, a phenotype not reported in the wild-type or in plt1,2 mutants, even when cell cycle regulators, such as AtCYCD3;1, were over-expressed. * Taken together, our results provide evidence for the involvement of AtMCM2 in DNA replication, and suggest that it plays a crucial role in root meristem function.}, number={2}, journal={The New Phytologist}, author={Ni, Di An and Sozzani, Rosangela and Blanchet, Sophie and Domenichini, Séverine and Reuzeau, Christophe and Cella, Rino and Bergounioux, Catherine and Raynaud, Cécile}, year={2009}, month={Oct}, pages={311–322} }
 @article{ascencio-ibáñez_sozzani_lee_chu_wolfinger_cella_hanley-bowdoin_2008, title={Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection}, volume={148}, ISSN={0032-0889}, DOI={10.1104/pp.108.121038}, abstractNote={Abstract}, number={1}, journal={Plant Physiology}, author={Ascencio-Ibáñez, José Trinidad and Sozzani, Rosangela and Lee, Tae-Jin and Chu, Tzu-Ming and Wolfinger, Russell D. and Cella, Rino and Hanley-Bowdoin, Linda}, year={2008}, month={Sep}, pages={436–454} }
 @article{sozzani_maggio_varotto_canova_bergounioux_albani_cella_2006, title={Interplay between Arabidopsis Activating Factors E2Fb and E2Fa in Cell Cycle Progression and Development}, volume={140}, ISSN={0032-0889, 1532-2548}, url={http://www.plantphysiol.org/content/140/4/1355}, DOI={10.1104/pp.106.077990}, abstractNote={Abstract}, number={4}, journal={Plant Physiology}, author={Sozzani, Rosangela and Maggio, Caterina and Varotto, Serena and Canova, Sabrina and Bergounioux, Catherine and Albani, Diego and Cella, Rino}, year={2006}, month={Apr}, pages={1355–1366} }
 @article{raynaud_sozzani_glab_domenichini_perennes_cella_kondorosi_bergounioux_2006, title={Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis}, volume={47}, ISSN={0960-7412}, DOI={10.1111/j.1365-313X.2006.02799.x}, abstractNote={Summary}, number={3}, journal={The Plant Journal: For Cell and Molecular Biology}, author={Raynaud, Cécile and Sozzani, Rosangela and Glab, Nathalie and Domenichini, Séverine and Perennes, Claudette and Cella, Rino and Kondorosi, Eva and Bergounioux, Catherine}, year={2006}, month={Aug}, pages={395–407} }