@article{manrique_caselli_matias-hernandez_franks_colombo_gregis_2023, title={Assessing the role of REM13, REM34 and REM46 during the transition to the reproductive phase in Arabidopsis thaliana}, volume={5}, ISSN={["1573-5028"]}, DOI={10.1007/s11103-023-01357-1}, abstractNote={AbstractREM (reproductive meristem) transcription factors have been proposed as regulators of plant reproductive development mainly based on their specific expression patterns in reproductive structures, but their roles are still largely unknown probably because of their redundancy. We selected three REM genes (REM13, REM34 and REM46) for functional analysis, based on their genome position and/or co-expression data.Our results suggest that these genes have a role in flowering time regulation and may modulate cell cycle progression. In addition, protein interaction experiments revealed that REM34 and REM46 interact with each other, suggesting that they might work cooperatively to regulate cell division during inflorescence meristem commitment.Previous attempts of using co-expression data as a guide for functional analysis of REMs were limited by the transcriptomic data available at the time. Our results uncover previously unknown functions of three members of the REM family of Arabidopsis thaliana and open the door to more comprehensive studies of the REM family, where the combination of co-expression analysis followed by functional studies might contribute to uncovering the biological roles of these proteins and the relationship among them.}, journal={PLANT MOLECULAR BIOLOGY}, author={Manrique, Silvia and Caselli, Francesca and Matias-Hernandez, Luis and Franks, Robert G. and Colombo, Lucia and Gregis, Veronica}, year={2023}, month={May} } @article{manrique_cavalleri_guazzotti_villarino_simonini_bombarely_higashiyama_grossniklaus_mizzotti_pereira_et al._2023, title={HISTONE DEACETYLASE19 Controls Ovule Number Determination and Transmitting Tract Differentiation}, volume={12}, ISSN={["1532-2548"]}, DOI={10.1093/plphys/kiad629}, abstractNote={Abstract The gynoecium is critical for the reproduction of flowering plants as it contains the ovules and the tissues that foster pollen germination, growth, and guidance. These tissues, known as the reproductive tract (ReT), comprise the stigma, style, and transmitting tract (TT). The ReT and ovules originate from the carpel margin meristem (CMM) within the pistil. SHOOT MERISTEMLESS (STM) is a key transcription factor for meristem formation and maintenance. In all above-ground meristems, including the CMM, local STM downregulation is required for organ formation. However, how this downregulation is achieved in the CMM is unknown. Here, we have studied the role of HISTONE DEACETYLASE 19 (HDA19) in Arabidopsis (Arabidopsis thaliana) during ovule and ReT differentiation based on the observation that the hda19-3 mutant displays a reduced ovule number and fails to differentiate the TT properly. Fluorescence-activated cell sorting coupled with RNA-sequencing revealed that in the CMM of hda19-3 mutants, genes promoting organ development are downregulated while meristematic markers, including STM, are upregulated. HDA19 was essential to downregulate STM in the CMM, thereby allowing ovule formation and TT differentiation. STM is ectopically expressed in hda19-3 at intermediate stages of pistil development, and its downregulation by RNA interference alleviated the hda19-3 phenotype. Chromatin immunoprecipitation assays indicated that STM is a direct target of HDA19 during pistil development and that the transcription factor SEEDSTICK is also required to regulate STM via histone acetylation. Thus, we identified factors required for the downregulation of STM in the CMM, which is necessary for organogenesis and tissue differentiation.}, journal={PLANT PHYSIOLOGY}, author={Manrique, Silvia and Cavalleri, Alex and Guazzotti, Andrea and Villarino, Gonzalo H. and Simonini, Sara and Bombarely, Aureliano and Higashiyama, Tetsuya and Grossniklaus, Ueli and Mizzotti, Chiara and Pereira, Ana Marta and et al.}, year={2023}, month={Dec} } @article{flores-vergara_oneal_costa_villarino_roberts_balaguer_coimbra_willis_franks_2020, title={Developmental Analysis of Mimulus Seed Transcriptomes Reveals Functional Gene Expression Clusters and Four Imprinted, Endosperm-Expressed Genes}, volume={11}, url={http://dx.doi.org/10.3389/fpls.2020.00132}, DOI={10.3389/fpls.2020.00132}, abstractNote={The double fertilization of the female gametophyte initiates embryogenesis and endosperm development in seeds via the activation of genes involved in cell differentiation, organ patterning, and growth. A subset of genes expressed in endosperm exhibit imprinted expression, and the correct balance of gene expression between parental alleles is critical for proper endosperm and seed development. We use a transcriptional time series analysis to identify genes that are associated with key shifts in seed development, including genes associated with secondary cell wall synthesis, mitotic cell cycle, chromatin organization, auxin synthesis, fatty acid metabolism, and seed maturation. We relate these genes to morphological changes in Mimulus seeds. We also identify four endosperm-expressed transcripts that display imprinted (paternal) expression bias. The imprinted status of these four genes is conserved in other flowering plants, suggesting that they are functionally important in endosperm development. Our study explores gene regulatory dynamics in a species with ab initio cellular endosperm development, broadening the taxonomic focus of the literature on gene expression in seeds. Moreover, it is the first to validate genes with imprinted endosperm expression in Mimulus guttatus, and will inform future studies on the genetic causes of seed failure in this model system.}, journal={Frontiers in Plant Science}, publisher={Frontiers Media SA}, author={Flores-Vergara, Miguel A. and Oneal, Elen and Costa, Mario and Villarino, Gonzalo and Roberts, Caitlyn and Balaguer, Maria Angels De Luis and Coimbra, Sílvia and Willis, John and Franks, Robert G.}, year={2020}, month={Feb} } @article{liu_zhang_xie_franks_xiang_2019, title={Functional characterization of Terminal Flower1 homolog in Cornus canadensis by genetic transformation}, volume={38}, ISSN={0721-7714 1432-203X}, url={http://dx.doi.org/10.1007/S00299-019-02369-2}, DOI={10.1007/s00299-019-02369-2}, abstractNote={TFL1homologCorcanTFL1suppresses the initiation of inflorescence development and regulates the inflorescence morphology inCornus canadensis. In flowering plants, there is a wide range of variation of inflorescence morphology. Despite the ecological and evolutionary importance, efforts devoted to the evolutionary study of the genetic basis of inflorescence morphology are far fewer compared to those on flower development. Our previous study on gene expression patterns suggested a CorTFL1-CorAP1 based model for the evolution of determinate umbels, heads, and mini dichasia from elongated inflorescences in Cornus. Here, we tested the function of CorcanTFL1 in regulating inflorescence development in Cornus canadensis through Agrobacterium-mediated transformation. We showed that transgenic plants overexpressing CorcanTFL1 displayed delayed or suppressed inflorescence initiation and development and extended periods of vegetative growth. Transgenic plants within which CorcanTFL1 had been down-regulated displayed earlier emergence of inflorescence and a reduction of bract and inflorescence sizes, conversions of leaves to bracts and axillary leaf buds to small inflorescences at the uppermost node bearing the inflorescence, or phyllotaxy changes of inflorescence branches and leaves from decussate opposite to spirally alternate. These observations support an important role of CorcanTFL1 in determining flowering time and the morphological destinies of leaves and buds at the node bearing the inflorescence. The evidence is in agreement with the predicted function of CorTFL1 from the gene expression model, supporting a key role of CorTFL1 in the evolutionary divergence of inflorescence forms in Cornus.}, number={3}, journal={Plant Cell Reports}, publisher={Springer Science and Business Media LLC}, author={Liu, Xiang and Zhang, Jian and Xie, Deyu and Franks, Robert G. and Xiang, Qiu-Yun}, year={2019}, month={Jan}, pages={333–343} } @article{sehra_franks_2017, title={Redundant CArG Box Cis-motif Activity Mediates SHATTERPROOF2 Transcriptional Regulation during Arabidopsis thaliana Gynoecium Development}, volume={8}, ISSN={["1664-462X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85034058138&partnerID=MN8TOARS}, DOI={10.3389/fpls.2017.01712}, abstractNote={In the Arabidopsis thaliana seed pod, pod shatter and seed dispersal properties are in part determined by the development of a longitudinally orientated dehiscence zone (DZ) that derives from cells of the gynoecial valve margin (VM). Transcriptional regulation of the MADS protein encoding transcription factors genes SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2) are critical for proper VM identity specification and later on for DZ development. Current models of SHP1 and SHP2 regulation indicate that the transcription factors FRUITFULL (FUL) and REPLUMLESS (RPL) repress these SHP genes in the developing valve and replum domains, respectively. Thus the expression of the SHP genes is restricted to the VM. FUL encodes a MADS-box containing transcription factor that is predicted to act through CArG-box containing cis-regulatory motifs. Here we delimit functional modules within the SHP2 cis-regulatory region and examine the functional importance of CArG box motifs within these regulatory regions. We have characterized a 2.2kb region upstream of the SHP2 translation start site that drives early and late medial domain expression in the gynoecium, as well as expression within the VM and DZ. We identified two separable, independent cis-regulatory modules, a 1kb promoter region and a 700bp enhancer region, that are capable of giving VM and DZ expression. Our results argue for multiple independent cis-regulatory modules that support SHP2 expression during VM development and may contribute to the robustness of SHP2 expression in this tissue. Additionally, three closely positioned CArG box motifs located in the SHP2 upstream regulatory region were mutated in the context of the 2.2kb reporter construct. Mutating simultaneously all three CArG boxes caused a moderate de-repression of the SHP2 reporter that was detected within the valve domain, suggesting that these CArG boxes are involved in SHP2 repression in the valve.}, journal={FRONTIERS IN PLANT SCIENCE}, author={Sehra, Bhupinder and Franks, Robert G.}, year={2017}, month={Oct} } @article{ma_liu_franks_xiang_2016, title={Alterations of CorTFL1 and CorAP1 expression correlate with major evolutionary shifts of inflorescence architecture in Cornus (Cornaceae) - a proposed model for variation of closed inflorescence forms}, volume={216}, ISSN={0028646X}, url={http://doi.wiley.com/10.1111/nph.14197}, DOI={10.1111/nph.14197}, abstractNote={Summary TFL1‐, AP1‐ and LFY‐like genes are known to be key regulators of inflorescence development. However, it remains to be tested whether the evolutionary modifications of inflorescence morphology result from shifts in their expression patterns. We compared the spatiotemporal expression patterns of CorTFL1, CorAP1 and CorLFY in six closely related Cornus species that display four types of closed inflorescence morphology using quantitative real‐time polymerase chain reaction (qRT‐PCR) and RNA in situ hybridization. Character mapping on the phylogeny was conducted to identify evolutionary changes and to assess the correlation between changes in gene expression and inflorescence morphology. Results demonstrated variation of gene expression patterns among species and a strong correlation between CorTFL1 expression and the branch index of the inflorescence type. Evolutionary changes in CorTFL1 and CorAP1 expression co‐occurred on the phylogeny with the morphological changes underpinning inflorescence divergence. The study found a clear correlation between the expression patterns of CorTFL1 and CorAP1 and the inflorescence architecture in a natural system displaying closed inflorescences. The results suggest a role for the alteration in CorTFL1 and CorAP1 expression during the evolutionary modification of inflorescences in Cornus. We propose that a TFL1‐like and AP1‐like gene‐based model may explain variation of closed inflorescences in Cornus and other lineages. }, number={2}, journal={New Phytologist}, publisher={Wiley}, author={Ma, Qing and Liu, Xiang and Franks, Robert G. and Xiang, Qiu-Yun Jenny}, year={2016}, pages={519–535} } @article{liu_zhang_abuahmad_franks_xie_xiang_2016, title={Analysis of two TFL1 homologs of dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering}, volume={243}, ISSN={0032-0935, 1432-2048}, url={http://link.springer.com/10.1007/s00425-016-2466-x}, DOI={10.1007/s00425-016-2466-x}, abstractNote={Two TFL1 -like genes, CorfloTFL1 and CorcanTFL1 cloned from Cornus florida and C. canadensis, function in regulating the transition to reproductive development in Arabidopsis. TERMINAL FLOWER 1 (TFL1) is known to regulate inflorescence development in Arabidopsis thaliana and to inhibit the transition from a vegetative to reproductive phase within the shoot apical meristem. Despite the importance, TFL1 homologs have been functionally characterized in only a handful eudicots. Here we report the role of TFL1 homologs of Cornus L. in asterid clade of eudicots. Two TFL1-like genes, CorfloTFL1 and CorcanTFL1, were cloned from Cornus florida (a tree) and C. canadensis (a subshrub), respectively. Both are deduced to encode proteins of 175 amino acids. The amino acid sequences of these two Cornus TFL1 homologs share a high similarity to Arabidopsis TFL1 and phylogenetically more close to TFL1 paralogous copy ATC (Arabidopsis thaliana CENTRORADIALIS homologue). Two genes are overexpressed in wild-type and tfl1 mutant plants of A. thaliana. The over-expression of each gene in wild-type Arabidopsis plants results in delaying flowering time, increase of plant height and cauline and rosette leaf numbers, excessive shoot buds, and secondary inflorescence branches. The over-expression of each gene in the tfl1 mutant rescued developmental defects, such as the early determinate inflorescence development, early flowering time, and other vegetative growth defects, to normal phenotypes of wild-type plants. These transgenic phenotypes are inherited in progenies. All data indicate that CorfloTFL1 and CorcanTFL1 have conserved the ancestral function of TFL1 and CEN regulating flowering time and inflorescence determinacy.}, number={5}, journal={Planta}, publisher={Springer Science and Business Media LLC}, author={Liu, Xiang and Zhang, Jian and Abuahmad, Ahmad and Franks, Robert G. and Xie, De-Yu and Xiang, Qiu-Yun}, year={2016}, month={May}, pages={1129–1141} } @article{liu_zhang_abuahmad_franks_xie_xiang_planta_2016, title={Analysis of two TFL1 homologs of dogwood species (Cornus L.) indicates functional conservation in control of transition to flowering.}, url={http://europepmc.org/abstract/med/26825444}, author={Liu, X. and Zhang, J. and Abuahmad, A. and Franks, R.G. and Xie, D.Y. and Xiang, Q.Y. and Planta}, year={2016}, month={Jan} } @article{oneal_willis_franks_2016, title={Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus}, volume={210}, ISSN={["1469-8137"]}, url={http://europepmc.org/abstract/med/26824345}, DOI={10.1111/nph.13842}, abstractNote={Summary Divergence of developmental mechanisms within populations could lead to hybrid developmental failure, and might be a factor driving speciation in angiosperms. We investigate patterns of endosperm and embryo development in Mimulus guttatus and the closely related, serpentine endemic Mimulus nudatus, and compare them to those of reciprocal hybrid seed. We address whether disruption in hybrid seed development is the primary source of reproductive isolation between these sympatric taxa. M. guttatus and M. nudatus differ in the pattern and timing of endosperm and embryo development. Some hybrid seeds exhibit early disruption of endosperm development and are completely inviable, while others develop relatively normally at first, but later exhibit impaired endosperm proliferation and low germination success. These developmental patterns are reflected in mature hybrid seeds, which are either small and flat (indicating little to no endosperm) or shriveled (indicating reduced endosperm volume). Hybrid seed inviability forms a potent reproductive barrier between M. guttatus and M. nudatus. We shed light on the extent of developmental variation between closely related species within the M. guttatus species complex, an important ecological model system, and provide a partial mechanism for the hybrid barrier between M. guttatus and M. nudatus. }, number={3}, journal={NEW PHYTOLOGIST}, author={Oneal, Elen and Willis, John H. and Franks, Robert G.}, year={2016}, month={May}, pages={1107–1120} } @article{franks_2016, place={Clifton, N.J}, title={Histological Analysis of the Arabidopsis Gynoecium and Ovules Using Chloral Hydrate Clearing and Differential Interference Contrast Light Microscopy}, volume={1457}, ISBN={["978-1-4939-3793-6"]}, ISSN={["1064-3745"]}, url={http://europepmc.org/abstract/med/27557569}, DOI={10.1007/978-1-4939-3795-0_1}, abstractNote={The use of chloral hydrate optical clearing paired with differential interference contrast microscopy allows the analysis of internal structures of developing plant organs without the need for paraffin embedding and sectioning. This approach is appropriate for the analysis of the developing gynoecium or seedpod of the flowering plant Arabidopsis thaliana and many other types of fixed plant material. Early stages of ovule development are observable with this approach.}, journal={OOGENESIS: METHODS AND PROTOCOLS}, author={Franks, Robert G.}, year={2016}, pages={1–7} } @article{gong_flores-vergara_hong_chu_lim_franks_liu_xu_physiology_2016, title={SEUSS Integrates Gibberellin Signaling with Transcriptional Inputs from the SHR-SCR-SCL3 Module to Regulate Middle Cortex Formation in the Arabidopsis Root}, volume={170}, ISSN={["1532-2548"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84959314828&partnerID=MN8TOARS}, DOI={10.1104/pp.15.01501}, abstractNote={The transcription factor SEU promotes middle cortex formation through a network of transcription factor interactions. A decade of studies on middle cortex (MC) formation in the root endodermis of Arabidopsis (Arabidopsis thaliana) have revealed a complex regulatory network that is orchestrated by several GRAS family transcription factors, including SHORT-ROOT (SHR), SCARECROW (SCR), and SCARECROW-LIKE3 (SCL3). However, how their functions are regulated remains obscure. Here we show that mutations in the SEUSS (SEU) gene led to a higher frequency of MC formation. seu mutants had strongly reduced expression of SHR, SCR, and SCL3, suggesting that SEU positively regulates these genes. Our results further indicate that SEU physically associates with upstream regulatory sequences of SHR, SCR, and SCL3; and that SEU has distinct genetic interactions with these genes in the control of MC formation, with SCL3 being epistatic to SEU. Similar to SCL3, SEU was repressed by the phytohormone GA and induced by the GA biosynthesis inhibitor paclobutrazol, suggesting that SEU acts downstream of GA signaling to regulate MC formation. Consistently, we found that SEU mediates the regulation of SCL3 by GA signaling. Together, our study identifies SEU as a new critical player that integrates GA signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate MC formation in the Arabidopsis root.}, number={3}, journal={PLANT PHYSIOLOGY}, publisher={American Society of Plant Biologists (ASPB)}, author={Gong, X. and Flores-Vergara, M.A. and Hong, J.H. and Chu, H. and Lim, J. and Franks, Robert G. and Liu, Z. and Xu, J. and physiology, Plant}, year={2016}, month={Mar}, pages={1675–1683} } @article{gong_flores-vergara_hong_chu_lim_franks_liu_xu_2016, title={SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root.}, url={http://europepmc.org/abstract/med/26818732}, journal={Plant physiology}, author={Gong, X and Flores-Vergara, MA and Hong, JH and Chu, H and Lim, J and Franks, RG and Liu, Z and Xu, J}, year={2016}, month={Jan} } @article{villarino_hu_manrique_flores-vergara_sehra_robles_brumos_stepanova_colombo_sundberg_et al._2016, title={Transcriptomic Signature of the SHATTERPROOF2 Expression Domain Reveals the Meristematic Nature of Arabidopsis Gynoecial Medial Domain}, volume={171}, ISSN={["1532-2548"]}, url={http://europepmc.org/abstract/med/26983993}, DOI={10.1104/pp.15.01845}, abstractNote={Transcriptional profiles of spatially and temporally restricted cell populations from the Arabidopsis gynoecium reveals the meristematic nature of the gynoecial medial domain. Plant meristems, like animal stem cell niches, maintain a pool of multipotent, undifferentiated cells that divide and differentiate to give rise to organs. In Arabidopsis (Arabidopsis thaliana), the carpel margin meristem is a vital meristematic structure that generates ovules from the medial domain of the gynoecium, the female floral reproductive structure. The molecular mechanisms that specify this meristematic region and regulate its organogenic potential are poorly understood. Here, we present a novel approach to analyze the transcriptional signature of the medial domain of the Arabidopsis gynoecium, highlighting the developmental stages that immediately proceed ovule initiation, the earliest stages of seed development. Using a floral synchronization system and a SHATTERPROOF2 (SHP2) domain-specific reporter, paired with FACS and RNA sequencing, we assayed the transcriptome of the gynoecial medial domain with temporal and spatial precision. This analysis reveals a set of genes that are differentially expressed within the SHP2 expression domain, including genes that have been shown previously to function during the development of medial domain-derived structures, including the ovules, thus validating our approach. Global analyses of the transcriptomic data set indicate a similarity of the pSHP2-expressing cell population to previously characterized meristematic domains, further supporting the meristematic nature of this gynoecial tissue. Our method identifies additional genes including novel isoforms, cis-natural antisense transcripts, and a previously unrecognized member of the REPRODUCTIVE MERISTEM family of transcriptional regulators that are potential novel regulators of medial domain development. This data set provides genome-wide transcriptional insight into the development of the carpel margin meristem in Arabidopsis.}, number={1}, journal={PLANT PHYSIOLOGY}, author={Villarino, Gonzalo H. and Hu, Qiwen and Manrique, Silvia and Flores-Vergara, Miguel and Sehra, Bhupinder and Robles, Linda and Brumos, Javier and Stepanova, Anna N. and Colombo, Lucia and Sundberg, Eva and et al.}, year={2016}, month={May}, pages={42–61} } @misc{sehra_franks_2015, title={Auxin and cytokinin act during gynoecial patterning and the development of ovules from the meristematic medial domain}, volume={4}, ISSN={["1759-7692"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84943583197&partnerID=MN8TOARS}, DOI={10.1002/wdev.193}, abstractNote={The gynoecium is the female reproductive structure of flowering plants, and is the site of ovule and seed development. The gynoecium is critical for reproductive competence and for agricultural productivity in many crop plants. In this review we focus on molecular aspects of the development of the Arabidopsis thaliana gynoecium. We briefly introduce gynoecium structure and development and then focus on important research advances published within the last year. We highlight what has been learned recently with respect to: (1) the role of auxin in the differential development of the medial and lateral domains of the Arabidopsis gynoecium; (2) the interaction between cytokinin and auxin during gynoecial development; (3) the role of auxin in the termination of the floral meristem and in the transition of floral meristem to gynoecium; and (4) recent studies that suggest a degree of evolutionary conservation of auxin mechanisms during gynoecial development in other eudicots. WIREs Dev Biol 2015, 4:555–571. doi: 10.1002/wdev.193This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms Plant Development > Inflorescence, Flower, and Fruit Development }, number={6}, journal={WILEY INTERDISCIPLINARY REVIEWS-DEVELOPMENTAL BIOLOGY}, author={Sehra, Bhupinder and Franks, Robert G.}, year={2015}, pages={555–571} } @article{liu_franks_2015, title={Molecular basis of fruit development}, volume={6}, ISSN={["1664-462X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84923218692&partnerID=MN8TOARS}, DOI={10.3389/fpls.2015.00028}, abstractNote={The fruit is a vital plant structure that supports seed development and dispersal, and is an indispensable part of the human diet. The 11 articles within this special research topic focus on the molecular mechanisms of early fruit development and span a diversity of species and experimental approaches. Since the gynoecium, the female floral structure, is the precursor of all or part of the fruit, several articles are focused on mechanisms of gynoecium development. The articles can be organized into several groups based on common themes highlighted below.}, number={FEB}, journal={FRONTIERS IN PLANT SCIENCE}, author={Liu, Zhongchi and Franks, Robert G.}, year={2015}, month={Feb} } @book{liu_franks_2015, title={Molecular basis of fruit development}, DOI={10.3389/978-2-88919-460-5}, journal={Frontiers Research Topics}, publisher={Frontiers SA Media}, year={2015} } @article{franks_2014, title={Corrigendum: [Novel functional roles for PERIANTHIA and SEUSS during floral organ identity specification, floral meristem termination and gynoecial development]}, volume={5}, ISSN={["1664-462X"]}, url={http://europepmc.org/abstract/med/25221562}, DOI={10.3389/fpls.2014.00434}, abstractNote={*Correspondence: Robert G. Franks, Department of Plant and Microbial Biology, North Carolina State University, 2548 Thomas Hall, Campus Box 7614, Raleigh, NC 27695-7614, USA e-mail: rgfranks@ncsu.edu The gynoecium is the female reproductive structure of angiosperm flowers. In Arabidopsis thaliana the gynoecium is composed of two carpels that are fused into a tube-like structure. As the gynoecial primordium arises from the floral meristem, a specialized meristematic structure, the carpel margin meristem (CMM), develops from portions of the medial gynoecial domain. The CMM is critical for reproductive competence because it gives rise to the ovules, the precursors of the seeds. Here we report a functional role for the transcription factor PERIANTHIA (PAN) in the development of the gynoecial medial domain and the formation of ovule primordia. This function of PAN is revealed in pan aintegumenta (ant) as well as seuss (seu) pan double mutants that form reduced numbers of ovules. Previously, PAN was identified as a regulator of perianth organ number and as a direct activator of AGAMOUS (AG) expression in floral whorl four. However, the seu pan double mutants display enhanced ectopic AG expression in developing sepals and the partial transformation of sepals to petals indicating a novel role for PAN in the repression of AG in floral whorl one. These results indicate that PAN functions as an activator or repressor of AG expression in a whorl-specific fashion. The seu pan double mutants also display enhanced floral indeterminacy, resulting in the formation of “fifth whorl” structures and disruption of WUSCHEL (WUS) expression patterns revealing a novel role for SEU in floral meristem termination.}, journal={FRONTIERS IN PLANT SCIENCE}, author={Franks, Robert G.}, year={2014}, month={Aug} } @book{flower development: open questions and future directions_2014, volume={1110}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84898771360&partnerID=MN8TOARS}, DOI={10.1007/978-1-4614-9408-9-5}, abstractNote={Almost three decades of genetic and molecular analyses have resulted in detailed insights into many of the processes that take place during flower development and in the identification of a large number of key regulatory genes that control these processes. Despite this impressive progress, many questions about how flower development is controlled in different angiosperm species remain unanswered. In this chapter, we discuss some of these open questions and the experimental strategies with which they could be addressed. Specifically, we focus on the areas of floral meristem development and patterning, floral organ specification and differentiation, as well as on the molecular mechanisms underlying the evolutionary changes that have led to the astounding variations in flower size and architecture among extant and extinct angiosperms.}, journal={Methods in Molecular Biology}, year={2014}, pages={103–124} } @article{wynn_seaman_jones_franks_2014, title={Novel functional roles for PERIANTHIA and SEUSS during floral organ identity specification, floral meristem termination, and gynoecial development}, volume={5}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84901002654&partnerID=MN8TOARS}, DOI={10.3389/fpls.2014.00130}, abstractNote={The gynoecium is the female reproductive structure of angiosperm flowers. In Arabidopsis thaliana the gynoecium is composed of two carpels that are fused into a tube-like structure. As the gynoecial primordium arises from the floral meristem, a specialized meristematic structure, the carpel margin meristem (CMM), develops from portions of the medial gynoecial domain. The CMM is critical for reproductive competence because it gives rise to the ovules, the precursors of the seeds. Here we report a functional role for the transcription factor PERIANTHIA (PAN) in the development of the gynoecial medial domain and the formation of ovule primordia. This function of PAN is revealed in pan aintegumenta (ant) as well as seuss (seu) pan double mutants that form reduced numbers of ovules. Previously, PAN was identified as a regulator of perianth organ number and as a direct activator of AGAMOUS (AG) expression in floral whorl four. However, the seu pan double mutants display enhanced ectopic AG expression in developing sepals and the partial transformation of sepals to petals indicating a novel role for PAN in the repression of AG in floral whorl one. These results indicate that PAN functions as an activator or repressor of AG expression in a whorl-specific fashion. The seu pan double mutants also display enhanced floral indeterminacy, resulting in the formation of “fifth whorl” structures and disruption of WUSCHEL (WUS) expression patterns revealing a novel role for SEU in floral meristem termination.}, number={APR}, journal={Frontiers in Plant Science}, author={Wynn, A.N. and Seaman, A.A. and Jones, A.L. and Franks, Robert G.}, year={2014} } @article{larsson_roberts_claes_franks_sundberg_2014, title={Polar Auxin Transport Is Essential for Medial versus Lateral Tissue Specification and Vascular-Mediated Valve Outgrowth in Arabidopsis Gynoecia[W]}, volume={166}, ISSN={["1532-2548"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84914129165&partnerID=MN8TOARS}, DOI={10.1104/pp.114.245951}, abstractNote={Polar transport of the plant hormone auxin in female reproductive organ primordia establishes positional cues for medial versus lateral tissue specification and induces lateral domain outgrowth. Although it is generally accepted that auxin is important for the patterning of the female reproductive organ, the gynoecium, the flow as well as the temporal and spatial actions of auxin have been difficult to show during early gynoecial development. The primordium of the Arabidopsis (Arabidopsis thaliana) gynoecium is composed of two congenitally fused, laterally positioned carpel primordia bisected by two medially positioned meristematic regions that give rise to apical and internal tissues, including the ovules. This organization makes the gynoecium one of the most complex plant structures, and as such, the regulation of its development has remained largely elusive. By determining the spatiotemporal expression of auxin response reporters and localization of PINFORMED (PIN) auxin efflux carriers, we have been able to create a map of the auxin flow during the earliest stages of gynoecial primordium initiation and outgrowth. We show that transient disruption of polar auxin transport (PAT) results in ectopic auxin responses, broadened expression domains of medial tissue markers, and disturbed lateral preprocambium initiation. Based on these results, we propose a new model of auxin-mediated gynoecial patterning, suggesting that valve outgrowth depends on PIN1-mediated lateral auxin maxima as well as subsequent internal auxin drainage and provascular formation, whereas the growth of the medial domains is less dependent on correct PAT. In addition, PAT is required to prevent the lateral domains, at least in the apical portion of the gynoecial primordium, from obtaining medial fates.}, number={4}, journal={PLANT PHYSIOLOGY}, author={Larsson, Emma and Roberts, Christina J. and Claes, Andrea R. and Franks, Robert G. and Sundberg, Eva}, year={2014}, month={Dec}, pages={1998–U1237} } @article{lee_wynn_franks_hwang_lim_kim_2014, title={The arabidopsis thaliana GRF-interacting factor gene family plays an essential role in control of male and female reproductive development}, volume={386}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84892481215&partnerID=MN8TOARS}, DOI={10.1016/j.ydbio.2013.12.009}, abstractNote={Reproductive success of angiosperms relies on the precise development of the gynoecium and the anther, because their primary function is to bear and to nurture the embryo sac/female gametophyte and pollen, in which the egg and sperm cells, respectively, are generated. It has been known that the GRF-INTERACTING FACTOR (GIF) transcription co-activator family of Arabidopsis thaliana (Arabidopsis) consists of three members and acts as a positive regulator of cell proliferation. Here, we demonstrate that GIF proteins also play an essential role in development of reproductive organs and generation of the gamete cells. The gif1 gif2 gif3 triple mutant, but not the single or double mutants, failed to establish normal carpel margin meristem (CMM) and its derivative tissues, such as the ovule and the septum, resulting in a split gynoecium and no observable embryo sac. The gif triple mutant also displayed severe structural and functional defects in the anther, producing neither microsporangium nor pollen grains. Therefore, we propose that the GIF family of Arabidopsis is a novel and essential component required for the cell specification maintenance during reproductive organ development and, ultimately, for the reproductive competence.}, number={1}, journal={Developmental Biology}, author={Lee, B.H. and Wynn, A.N. and Franks, R.G. and Hwang, Y.-S. and Lim, J. and Kim, J.H.}, year={2014}, pages={12–24} } @article{shu_livingston_franks_boston_woloshuk_payne_2015, title={Tissue-specific gene expression in maize seeds during colonization by Aspergillus flavus and Fusarium verticillioides}, volume={16}, ISSN={["1364-3703"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84937630553&partnerID=MN8TOARS}, DOI={10.1111/mpp.12224}, abstractNote={SummaryAspergillus flavus and Fusarium verticillioides are fungal pathogens that colonize maize kernels and produce the harmful mycotoxins aflatoxin and fumonisin, respectively. Management practice based on potential host resistance to reduce contamination by these mycotoxins has proven difficult, resulting in the need for a better understanding of the infection process by these fungi and the response of maize seeds to infection. In this study, we followed the colonization of seeds by histological methods and the transcriptional changes of two maize defence‐related genes in specific seed tissues by RNA in situ hybridization. Maize kernels were inoculated with either A. flavus or F. verticillioides 21–22 days after pollination, and harvested at 4, 12, 24, 48, 72, 96 and 120 h post‐inoculation. The fungi colonized all tissues of maize seed, but differed in their interactions with aleurone and germ tissues. RNA in situ hybridization showed the induction of the maize pathogenesis‐related protein, maize seed (PRms) gene in the aleurone and scutellum on infection by either fungus. Transcripts of the maize sucrose synthase‐encoding gene, shrunken‐1 (Sh1), were observed in the embryo of non‐infected kernels, but were induced on infection by each fungus in the aleurone and scutellum. By comparing histological and RNA in situ hybridization results from adjacent serial sections, we found that the transcripts of these two genes accumulated in tissue prior to the arrival of the advancing pathogens in the seeds. A knowledge of the patterns of colonization and tissue‐specific gene expression in response to these fungi will be helpful in the development of resistance.}, number={7}, journal={MOLECULAR PLANT PATHOLOGY}, author={Shu, Xiaomei and Livingston, David P., III and Franks, Robert G. and Boston, Rebecca S. and Woloshuk, Charles P. and Payne, Gary A.}, year={2015}, month={Sep}, pages={662–674} } @misc{larsson_franks_sundberg_2013, title={Auxin and the Arabidopsis thaliana gynoecium}, volume={64}, ISSN={["0022-0957"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84878306681&partnerID=MN8TOARS}, DOI={10.1093/jxb/ert099}, abstractNote={Recent research is beginning to reveal how intricate networks of hormones and transcription factors coordinate the complex patterning of the gynoecium, the female reproductive structure of flowering plants. This review summarizes recent advances in understanding of how auxin biosynthesis, transport, and responses together generate specific gynoecial domains. This review also highlights areas where future research endeavours are likely to provide additional insight into the homeostatic molecular mechanisms by which auxin regulates gynoecium development.}, number={9}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={Larsson, Emma and Franks, Robert G. and Sundberg, Eva}, year={2013}, month={Jun}, pages={2619–2627} } @article{liu_franks_feng_liu_fu_(jenny) xiang_2013, title={Characterization of the sequence and expression pattern of LFY homologues from dogwood species (Cornus) with divergent inflorescence architectures}, volume={112}, ISSN={0305-7364, 1095-8290}, url={https://academic.oup.com/aob/article-lookup/doi/10.1093/aob/mct202}, DOI={10.1093/aob/mct202}, abstractNote={BACKGROUND AND AIMS LFY homologues encode transcription factors that regulate the transition from vegetative to reproductive growth in flowering plants and have been shown to control inflorescence patterning in model species. This study investigated the expression patterns of LFY homologues within the diverse inflorescence types (head-like, umbel-like and inflorescences with elongated internodes) in closely related lineages in the dogwood genus (Cornus s.l.). The study sought to determine whether LFY homologues in Cornus species are expressed during floral and inflorescence development and if the pattern of expression is consistent with a function in regulating floral development and inflorescence architectures in the genus. METHODS Total RNAs were extracted using the CTAB method and the first-strand cDNA was synthesized using the SuperScript III first-strand synthesis system kit (Invitrogen). Expression of CorLFY was investigated by RT-PCR and RNA in situ hybridization. Phylogenetic analyses were conducted using the maximum likelihood methods implemented in RAxML-HPC v7.2.8. KEY RESULTS cDNA clones of LFY homologues (designated CorLFY) were isolated from six Cornus species bearing different types of inflorescence. CorLFY cDNAs were predicted to encode proteins of approximately 375 amino acids. The detection of CorLFY expression patterns using in situ RNA hybridization demonstrated the expression of CorLFY within the inflorescence meristems, inflorescence branch meristems, floral meristems and developing floral organ primordia. PCR analyses for cDNA libraries derived from reverse transcription of total RNAs showed that CorLFY was also expressed during the late-stage development of flowers and inflorescences, as well as in bracts and developing leaves. Consistent differences in the CorLFY expression patterns were not detected among the distinct inflorescence types. CONCLUSIONS The results suggest a role for CorLFY genes during floral and inflorescence development in dogwoods. However, the failure to detect expression differences between the inflorescence types in the Cornus species analysed suggests that the evolutionary shift between major inflorescence types in the genus is not controlled by dramatic alterations in the levels of CorLFY gene transcript accumulation. However, due to spatial, temporal and quantitative limitations of the expression data, it cannot be ruled out that subtle differences in the level or location of CorLFY transcripts may underlie the different inflorescence architectures that are observed across these species. Alternatively, differences in CorLFY protein function or the expression or function of other regulators (e.g. TFL1 and UFO homologues) may support the divergent developmental trajectories.}, number={8}, journal={Annals of Botany}, publisher={Oxford University Press (OUP)}, author={Liu, Juan and Franks, Robert G. and Feng, Chun-Miao and Liu, Xiang and Fu, Cheng-Xin and (Jenny) Xiang, Qiu-Yun}, year={2013}, month={Nov}, pages={1629–1641} } @article{zhang_franks_liu_kang_keebler_schaff_huang_xiang_2013, title={De novo Sequencing, Characterization, and Comparison of Inflorescence Transcriptomes of Cornus canadensis and C. florida (Cornaceae)}, volume={8}, ISSN={1932-6203}, url={https://dx.plos.org/10.1371/journal.pone.0082674}, DOI={10.1371/journal.pone.0082674}, abstractNote={Background Transcriptome sequencing analysis is a powerful tool in molecular genetics and evolutionary biology. Here we report the results of de novo 454 sequencing, characterization, and comparison of inflorescence transcriptomes of two closely related dogwood species, Cornus canadensis and C. florida (Cornaceae). Our goals were to build a preliminary source of genome sequence data, and to identify genes potentially expressed differentially between the inflorescence transcriptomes for these important horticultural species. Results The sequencing of cDNAs from inflorescence buds of C. canadensis (cc) and C. florida (cf), and normalized cDNAs from leaves of C. canadensis resulted in 251799 (ccBud), 96245 (ccLeaf) and 114648 (cfBud) raw reads, respectively. The de novo assembly of the high quality (HQ) reads resulted in 36088, 17802 and 21210 unigenes for ccBud, ccLeaf and cfBud. A reference transcriptome for C. canadensis was built by assembling HQ reads of ccBud and ccLeaf, containing 40884 unigenes. Reference mapping and comparative analyses found 10926 sequences were putatively specific to ccBud, and 6979 putatively specific to cfBud. Putative differentially expressed genes between ccBud and cfBud that are related to flower development and/or stress response were identified among 7718 shared sequences by ccBud and cfBud. Bi-directional BLAST found 87 (41.83% of 208) of Arabidopsis genes related to inflorescence development had putative orthologs in the dogwood transcriptomes. Comparisons of the shared sequences by ccBud and cfBud yielded 65931 high quality SNPs between two species. The twenty unigenes with the most SNPs are listed as potential genetic markers for evolutionary studies. Conclusions The data provide an important, although preliminary, information platform for functional genomics and evolutionary developmental biology in Cornus. The study identified putative candidates potentially involved in the genetic regulation of inflorescence evolution and/or disease resistance in dogwoods for future analyses. Results of the study also provide markers useful for dogwood phylogenomic studies.}, number={12}, journal={PLoS ONE}, publisher={Public Library of Science (PLoS)}, author={Zhang, Jian and Franks, Robert G. and Liu, Xiang and Kang, Ming and Keebler, Jonathan E. M. and Schaff, Jennifer E. and Huang, Hong-Wen and Xiang, Qiu-Yun (Jenny)}, editor={Wang, TingEditor}, year={2013}, month={Dec}, pages={e82674} } @book{franks_2014, title={Scanning Electron Microscopy analysis of floral development}, volume={1110}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84934439650&partnerID=MN8TOARS}, DOI={10.1007/978-1-4614-9408-9_13}, abstractNote={Scanning Electron Microscopy (SEM) allows the morphological characterization of the surface features of floral and inflorescence structures in a manner that retains the topography or three-dimensional appearance of the structure. Even at relatively low magnification levels it is possible to characterize early developmental stages. Using medium to high power magnification at later stages of development, cell surface morphology can be visualized allowing the identification of specific epidermal cell types. The analysis of the altered developmental progressions of mutant plants can provide insight into the developmental processes that are disrupted in that mutant background.}, journal={Methods in Molecular Biology}, author={Franks, R.G.}, year={2014}, pages={263–273} } @article{feng_liu_yu_xie_franks_xiang_2012, title={Evolution of bract development and B‐class MADS box gene expression in petaloid bracts of Cornus s. l. (Cornaceae)}, volume={196}, ISSN={0028-646X 1469-8137}, url={http://dx.doi.org/10.1111/j.1469-8137.2012.04255.x}, DOI={10.1111/j.1469-8137.2012.04255.x}, abstractNote={Despite increasing interest in the molecular mechanisms of floral diversity, few studies have investigated the developmental and genetic bases of petaloid bracts. This study examined morphological patterns of bract initiation and expression patterns of B-class MADS-box genes in bracts of several Cornus species. We suggest that petaloid bracts in this genus may not share a single evolutionary origin. Developmental pathways of bracts and spatiotemporal expression of B-class genes in bracts and flowers were examined for four closely related dogwood species. Divergent morphological progressions and gene expression patterns were found in the two sister lineages with petaloid bracts, represented by Cornus florida and Cornus canadensis. Phylogeny-based analysis identified developmental and gene expression changes that are correlated with the evolution of petaloid bracts in C. florida and C. canadensis. Our data support the existence of independent evolutionary origins of petaloid bracts in C. canadensis and C. florida. Additionally, we suggest that functional transference within B-class gene families may have contributed to the origin of bract petaloidy in C. florida. However, the underlying mechanisms of petaloid bract development likely differ between C. florida and C. canadensis. In the future this hypothesis can be tested by functional analyses of Cornus B-class genes.}, number={2}, journal={New Phytologist}, publisher={Wiley}, author={Feng, Chun‐Miao and Liu, Xiang and Yu, Yi and Xie, Deyu and Franks, Robert G. and Xiang, Qiu‐Yun (Jenny)}, year={2012}, month={Aug}, pages={631–643} } @article{liu_feng_franks_qu_xie_xiang_2013, title={Plant regeneration and genetic transformation of C. canadensis: a non-model plant appropriate for investigation of flower development in Cornus (Cornaceae)}, volume={32}, ISSN={0721-7714, 1432-203X}, url={http://link.springer.com/10.1007/s00299-012-1341-x}, DOI={10.1007/s00299-012-1341-x}, abstractNote={KEY MESSAGE : Efficient Agrobacterium -mediated genetic transformation for investigation of genetic and molecular mechanisms involved in inflorescence architectures in Cornus species. Cornus canadensis is a subshrub species in Cornus, Cornaceae. It has recently become a favored non-model plant species to study genes involved in development and evolution of inflorescence architectures in Cornaceae. Here, we report an effective protocol of plant regeneration and genetic transformation of C. canadensis. We use young inflorescence buds as explants to efficiently induce calli and multiple adventitious shoots on an optimized induction medium consisting of basal MS medium supplemented with 1 mg/l of 6-benzylaminopurine and 0.1 mg/l of 1-naphthaleneacetic acid. On the same medium, primary adventitious shoots can produce a large number of secondary adventitious shoots. Using leaves of 8-week-old secondary shoots as explants, GFP as a reporter gene controlled by 35S promoter and hygromycin B as the selection antibiotic, a standard procedure including pre-culture of explants, infection, co-cultivation, resting and selection has been developed to transform C. canadensis via Agrobacterium strain EHA105-mediated transformation. Under a strict selection condition using 14 mg/l hygromycin B, approximately 5 % explants infected by Agrobacterium produce resistant calli, from which clusters of adventitious shoots are induced. On an optimized rooting medium consisting of basal MS medium supplemented with 0.1 mg/l of indole-3-butyric acid and 7 mg/l hygromycin B, most of the resistant shoots develop adventitious roots to form complete transgenic plantlets, which can grow normally in soil. RT-PCR analysis demonstrates the expression of GFP transgene. Green fluorescence emitted by GFP is observed in transgenic calli, roots and cells of transgenic leaves under both stereo fluorescence microscope and confocal microscope. The success of genetic transformation provides an appropriate platform to investigate the molecular mechanisms by which the various inflorescence forms are developed in Cornus plants.}, number={1}, journal={Plant Cell Reports}, publisher={Springer Science and Business Media LLC}, author={Liu, Xiang and Feng, Chun-Miao and Franks, Robert and Qu, Rongda and Xie, De-Yu and Xiang, Qiu-Yun Jenny}, year={2013}, month={Jan}, pages={77–87} } @article{feng_xiang_franks_2011, title={Phylogeny-based developmental analyses illuminate evolution of inflorescence architectures in dogwoods (Cornus s. l., Cornaceae)}, volume={191}, ISSN={["1469-8137"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-79960555236&partnerID=MN8TOARS}, DOI={10.1111/j.1469-8137.2011.03716.x}, abstractNote={• Inflorescence architecture is important to angiosperm reproduction, but our knowledge of the developmental basis underlying the evolution of inflorescence architectures is limited. Using a phylogeny-based comparative analysis of developmental pathways, we tested the long-standing hypothesis that umbel evolved from elongated inflorescences by suppression of inflorescence branches, while head evolved from umbels by suppression of pedicels. • The developmental pathways of six species of Cornus producing different inflorescence types were characterized by scanning electron microscopy (SEM) and histological analysis. Critical developmental events were traced over the molecular phylogeny to identify evolutionary changes leading to the formation of umbels and heads using methods accounting for evolutionary time and phylogenetic uncertainty. • We defined 24 developmental events describing the developmental progression of the different inflorescence types. The evolutionary transition from paniculate cymes to umbels and heads required alterations of seven developmental events occurring at different evolutionary times. • Our results indicate that heads and umbels evolved independently in Cornus from elongated forms via an umbellate dichasium ancestor and this process involved several independent changes. Our findings shed novel insights into head and umbel evolution concealed by outer morphology. Our work illustrates the importance of combining developmental and phylogenetic data to better define morphological evolutionary processes.}, number={3}, journal={NEW PHYTOLOGIST}, author={Feng, Chun-Miao and Xiang, Qiu-Yun and Franks, Robert G.}, year={2011}, pages={850–869} } @article{wynn_rueschhoff_franks_2011, title={Transcriptomic Characterization of a Synergistic Genetic Interaction during Carpel Margin Meristem Development in Arabidopsis thaliana}, volume={6}, ISSN={["1932-6203"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-80054838468&partnerID=MN8TOARS}, DOI={10.1371/journal.pone.0026231}, abstractNote={In flowering plants the gynoecium is the female reproductive structure. In Arabidopsis thaliana ovules initiate within the developing gynoecium from meristematic tissue located along the margins of the floral carpels. When fertilized the ovules will develop into seeds. SEUSS (SEU) and AINTEGUMENTA (ANT) encode transcriptional regulators that are critical for the proper formation of ovules from the carpel margin meristem (CMM). The synergistic loss of ovule initiation observed in the seu ant double mutant suggests that SEU and ANT share overlapping functions during CMM development. However the molecular mechanism underlying this synergistic interaction is unknown. Using the ATH1 transcriptomics platform we identified transcripts that were differentially expressed in seu ant double mutant relative to wild type and single mutant gynoecia. In particular we sought to identify transcripts whose expression was dependent on the coordinated activities of the SEU and ANT gene products. Our analysis identifies a diverse set of transcripts that display altered expression in the seu ant double mutant tissues. The analysis of overrepresented Gene Ontology classifications suggests a preponderance of transcriptional regulators including multiple members of the REPRODUCTIVE MERISTEMS (REM) and GROWTH-REGULATING FACTOR (GRF) families are mis-regulated in the seu ant gynoecia. Our in situ hybridization analyses indicate that many of these genes are preferentially expressed within the developing CMM. This study is the first step toward a detailed description of the transcriptional regulatory hierarchies that control the development of the CMM and ovule initiation. Understanding the regulatory hierarchy controlled by SEU and ANT will clarify the molecular mechanism of the functional redundancy of these two genes and illuminate the developmental and molecular events required for CMM development and ovule initiation.}, number={10}, journal={PLOS ONE}, author={Wynn, April N. and Rueschhoff, Elizabeth E. and Franks, Robert G.}, year={2011}, month={Oct} } @article{note-wilson_azhakanandam_franks_2010, title={Polar auxin transport together with AINTEGUMENTA and REVOLUTA coordinate early Arabidopsis gynoecium development}, volume={346}, ISSN={["1095-564X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-77956879407&partnerID=MN8TOARS}, DOI={10.1016/j.ydbio.2010.07.016}, abstractNote={In flowering plants the gynoecium is the female reproductive structure and the site of oogenesis, fertilization, and maturation of the embryo and the seed. Proper development of the gynoecium requires that the early gynoecial primordium be partitioned into distinct spatial domains with divergent fates. Regulated transport of the phytohormone auxin previously has been shown to play a role in the patterning of spatial domains along the apical–basal axis of the gynoecium. Here we establish a role for auxin transport in patterning along the medio-lateral axis of the gynoecial ovary. We demonstrate that auxin transport is required for the development of the medial ovary domain that contains the carpel margin meristem, a vital female reproductive structure. Disruptions in auxin transport enhance the medial domain defects observed in aintegumenta and revoluta mutant genotypes. AINTEGUMENTA and REVOLUTA are likely to function in parallel and partially overlapping pathways required for medial domain development. Our data indicate that different ovary domains are differentially sensitive to the reduction of polar auxin transport and the loss of AINTEGUMENTA and REVOLUTA activity. We suggest that an auxin-mediated positional cue is important for the differential specification of the medial and lateral ovary domains.}, number={2}, journal={DEVELOPMENTAL BIOLOGY}, author={Note-Wilson, Staci and Azhakanandam, Sridevi and Franks, Robert G.}, year={2010}, month={Oct}, pages={181–195} } @article{nole-wilson_rueschhoff_bhatti_franks_2010, title={Synergistic disruptions in seuss cyp85A2 double mutants reveal a role for brassinolide synthesis during gynoecium and ovule development}, volume={10}, ISSN={["1471-2229"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-77956486883&partnerID=MN8TOARS}, DOI={10.1186/1471-2229-10-198}, abstractNote={Abstract Background The Arabidopsis SEUSS (SEU) gene encodes a transcriptional adaptor protein that is required for a diverse set of developmental events, including floral organ identity specification, as well as gynoecium, ovule and embryo development. In order to better understand the molecular mechanisms of SEUSS action we undertook a genetic modifier screen to identify seuss-modifier (sum) mutations. Results Screening of M2 lines representing approximately 5,000 M1 individuals identified mutations that enhance the seuss mutant phenotypic disruptions in ovules and gynoecia; here we describe the phenotype of the sum63 mutant and enhanced disruptions of ovule and gynoecial development in the seu sum63 double mutant. Mapping and genetic complementation tests indicate that sum63 is allelic to CYP85A2 (AT3G30180) a cytochrome p450 enzyme that catalyzes the final steps in the synthesis of the phytohormone brassinolide. Conclusions Our identification of mutations in CYP85A2 as enhancers of the seuss mutant phenotype suggests a previously unrecognized role for brassinolide synthesis in gynoecial and ovule outer integument development. The work also suggests that seuss mutants may be more sensitive to the loss or reduction of brassinolide synthesis than are wild type plants. }, journal={BMC PLANT BIOLOGY}, author={Nole-Wilson, Staci and Rueschhoff, Elizabeth E. and Bhatti, Huda and Franks, Robert G.}, year={2010}, month={Sep} } @article{bao_azhakanandam_franks_2010, title={SEUSS and SEUSS-LIKE Transcriptional Adaptors Regulate Floral and Embryonic Development in Arabidopsis}, volume={152}, ISSN={["1532-2548"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-75949107013&partnerID=MN8TOARS}, DOI={10.1104/pp.109.146183}, abstractNote={AbstractMultimeric protein complexes are required during development to regulate transcription and orchestrate cellular proliferation and differentiation. The Arabidopsis (Arabidopsis thaliana) SEUSS (SEU) gene encodes a transcriptional adaptor that shares sequence similarity with metazoan Lim domain-binding transcriptional adaptors. In Arabidopsis, SEU forms a physical complex with the LEUNIG transcriptional coregulator. This complex regulates a number of diverse developmental events, including proper specification of floral organ identity and number and the development of female reproductive tissues derived from the carpel margin meristem. In addition to SEU, there are three Arabidopsis SEUSS-LIKE (SLK) genes that encode putative transcriptional adaptors. To determine the functions of the SLK genes and to investigate the degree of functional redundancy between SEU and SLK genes, we characterized available slk mutant lines in Arabidopsis. Here, we show that mutations in any single SLK gene failed to condition an obvious morphological abnormality. However, by generating higher order mutant plants, we uncovered a degree of redundancy between the SLK genes and between SLK genes and SEU. We report a novel role for SEU and the SLK genes during embryonic development and show that the concomitant loss of both SEU and SLK2 activities conditions severe embryonic and seedling defects characterized by a loss of the shoot apical meristem. Furthermore, we demonstrate that SLK gene function is required for proper development of vital female reproductive tissues derived from the carpel margin. We propose a model that posits that SEU and SLK genes support organ development from meristematic regions through two different pathways: one that facilitates auxin response and thus organ initiation and a second that sustains meristematic potential through the maintenance of SHOOTMERISTEM-LESS and PHABULOSA expression.}, number={2}, journal={PLANT PHYSIOLOGY}, author={Bao, Fang and Azhakanandam, Sridevi and Franks, Robert G.}, year={2010}, month={Feb}, pages={821–836} } @article{azhakanandam_nole-wilson_bao_franks_2008, title={SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development}, volume={146}, ISSN={["0032-0889"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-48949120198&partnerID=MN8TOARS}, DOI={10.1104/pp.107.114751}, abstractNote={AbstractThe Arabidopsis (Arabidopsis thaliana) gynoecium, the female floral reproductive structure, requires the action of genes that specify positional identities during its development to generate an organ competent for seed development and dispersal. Early in gynoecial development, patterning events divide the primordium into distinct domains that will give rise to specific tissues and organs. The medial domain of the gynoecium gives rise to the ovules, and several other structures critical for reproductive competence. Here we report a synergistic genetic interaction between seuss and aintegumenta mutants resulting in a complete loss of ovule initiation and a reduction of the structures derived from the medial domain. We show that patterning events are disrupted early in the development of the seuss aintegumenta gynoecia and we identify PHABULOSA (PHB), REVOLUTA, and CRABS CLAW (CRC) as potential downstream targets of SEUSS (SEU) and AINTEGUMENTA (ANT) regulation. Our genetic data suggest that SEU additionally functions in pathways that are partially redundant and parallel to PHB, CRC, and ANT. Thus, SEU and ANT are part of a complex and robust molecular system that coordinates patterning cues and cellular proliferation along the three positional axes of the developing gynoecium.}, number={3}, journal={PLANT PHYSIOLOGY}, author={Azhakanandam, Sridevi and Nole-Wilson, Staci and Bao, Fang and Franks, Robert G.}, year={2008}, month={Mar}, pages={1165–1181} } @article{franks_liu_fischer_2006, title={SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals}, volume={224}, ISSN={["0032-0935"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-33745961426&partnerID=MN8TOARS}, DOI={10.1007/s00425-006-0264-6}, abstractNote={Unlike in animals where cell migrations and programmed cell death play key roles in organ shape determination, in plants organ shape is largely a result of coordinated cellular growth (cell divisions and cell elongations). We have investigated the role of the SEUSS and LEUNIG genes in Arabidopsis thaliana (L.) Heynh. petal development to better understand the molecular mechanisms through which cellular growth and organ shape are coordinated in plants. SEUSS and LEUNIG encode components of a putative transcriptional regulatory complex that controls organ identity specification through the repression of the floral organ identity gene AGAMOUS. SEUSS and LEUNIG also regulate petal shape through AGAMOUS-independent mechanisms; however, the molecular and cellular actions of SEUSS and LEUNIG during petal development are unknown. Here we show that SEUSS and LEUNIG control blade cell number and vasculature development within the petal. Furthermore, SEUSS and LEUNIG regulate petal polarity along the adaxial/abaxial axis. We present a model where SEUSS and LEUNIG are required to potentiate the key polarity genes PHABULOSA and FILAMENTOUS FLOWER/YABBY1 and thus influence cellular growth within the developing petal blade.}, number={4}, journal={PLANTA}, author={Franks, Robert G. and Liu, Zhongchi and Fischer, Robert L.}, year={2006}, month={Sep}, pages={801–811} } @article{bao_franks_levin_liu_2004, title={Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems}, volume={16}, ISSN={["1532-298X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-2942672959&partnerID=MN8TOARS}, DOI={10.1105/tpc.021147}, abstractNote={A common aspect of gene regulation in all developmental systems is the sustained repression of key regulatory genes in inappropriate spatial or temporal domains. To understand the mechanism of transcriptional repression of the floral homeotic gene AGAMOUS (AG), we identified two mutations in the BELLRINGER (BLR) gene based on a striking floral phenotype, in which homeotic transformations from sepals to carpels are found in flowers derived from old terminating shoots. Furthermore, this phenotype is drastically enhanced by growth at a high temperature and by combining blr with mutants of LEUNIG and SEUSS, two putative transcriptional corepressors of AG. We showed that the floral phenotype of blr mutants is caused by derepression of AG, suggesting that BLR functions as a transcription repressor. Because BLR encodes a BELL1-like (BELL) homeobox protein, direct binding of BLR to AG cis-regulatory elements was tested by gel-shift assays, and putative BLR binding motifs were identified. In addition, these putative BLR binding motifs were shown to be conserved in 17 of the 29 Brassicaceae species by phylogenetic footprinting. Because BELL homeobox proteins are a family of plant-specific transcription factors with 12 members in Arabidopsis thaliana, our findings will facilitate the identification of regulatory targets of other BELL proteins and help determine their biological functions. The age-dependent and high temperature–enhanced derepression of AG in blr mutants led us to propose that AG expression might be regulated by a thermal time-dependent molecular mechanism.}, number={6}, journal={PLANT CELL}, author={Bao, XZ and Franks, RG and Levin, JZ and Liu, ZC}, year={2004}, month={Jun}, pages={1478–1489} } @article{franks_wang_levin_liu_2002, title={SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG}, volume={129}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0036333380&partnerID=MN8TOARS}, number={1}, journal={Development}, author={Franks, R.G. and Wang, C. and Levin, J.Z. and Liu, Z.}, year={2002}, pages={253–263} } @article{franks_wang_levin_liu_development_2002, title={SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG.}, volume={129}, url={http://europepmc.org/abstract/med/11782418}, number={1}, author={Franks, R.G. and Wang, C. and Levin, J.Z. and Liu, Z. and Development}, year={2002}, month={Jan}, pages={253–263} } @article{franks_liu_2010, title={Floral Homeotic Gene Regulation}, DOI={10.1002/9780470650813.ch2}, journal={Horticultural Reviews}, publisher={John Wiley & Sons, Inc.}, author={Franks, Robert G. and Liu, Zhongchi}, year={2010}, month={Jun}, pages={41–77} } @article{liu_franks_klink_2000, title={Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA}, volume={12}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0033768403&partnerID=MN8TOARS}, DOI={10.1105/tpc.12.10.1879}, abstractNote={The carpel is the female reproductive organ of flowering plants. In Arabidopsis, congenital fusion of two carpels leads to the formation of an enclosed gynoecium. The margins of the two fused carpels are meristematic in nature and give rise to placentas, ovules, septa, abaxial repla, and the majority of the stylar and stigmatic tissues. Thus, understanding how the marginal tissues are specified and identifying genes that direct their development may provide important insight into higher plant reproductive development. In this study, we show that LEUNIG and AINTEGUMENTA are two critical regulators of marginal tissue development. Double mutants of leunig aintegumenta fail to develop placentas, ovules, septa, stigma, and style. This effect is specific to the leunig aintegumenta double mutant and is not found in other double mutant combinations such as leunig apetala2 or aintegumenta apetala2. Additional analyses indicate that the absence of marginal tissues in leunig aintegumenta double mutants is not mediated by ectopic AGAMOUS. We propose that LEUNIG and AINTEGUMENTA act together to control the expression of common target genes that regulate cell proliferation associated with marginal tissue development.}, number={10}, journal={Plant Cell}, author={Liu, Z. and Franks, R.G. and Klink, V.P.}, year={2000}, pages={1879–1891} } @article{ka_rg_y_st_development_1994, title={Control of CNS midline transcription by asymmetric E-box-like elements: similarity to xenobiotic responsive regulation.}, volume={120}, url={http://europepmc.org/abstract/med/7821222}, number={12}, author={Ka, Wharton and Rg, Franks and Y, Kasai and St, Crews and Development}, year={1994}, month={Dec}, pages={3563–3569} } @article{controls of cns midline transcription by asymmetric e-box-like elements: similarity to xenobiotic responsive regulation_1994, volume={120}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0028172292&partnerID=MN8TOARS}, number={12}, journal={Development}, year={1994}, pages={3563–3569} } @article{franks_crews_1994, title={Transcriptional activation domains of the single-minded bHLH protein are required for CNS midline cell development}, volume={45}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0028353775&partnerID=MN8TOARS}, DOI={10.1016/0925-4773(94)90013-2}, abstractNote={The single-minded gene functions as a master developmental regulator within the midline cell lineage of the embryonic central nervous system of Drosophila melanogaster. Genetic experiments suggest that Single-minded can function as a transcriptional activator. Regions of the Single-minded protein were fused to the DNA binding domain of the mammalian transcription factor Sp1 and shown to activate transcription from a reporter gene linked to Sp1 binding sites. Three independent activation domains were identified in the carboxy terminal region of Single-minded that include areas rich in serine, threonine, glutamine and proline residues. Germ line transformation experiments indicate that the carboxy terminal activation domains, the PAS dimerization domain, and the putative DNA binding basic domain of Single-minded are required for expression of CNS midline genes in vivo. These results define in vivo a functional activation domain within Single-minded and suggest a model in which Single-minded activates transcription through a direct interaction with promoter elements of CNS midline genes.}, number={3}, journal={Mechanisms of Development}, author={Franks, R.G. and Crews, S.T.}, year={1994}, pages={269–277} } @article{crews_franks_hu_matthews_nambu_1992, title={Drosophila single‐minded gene and the molecular genetics of CNS midline development}, volume={261}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0026832030&partnerID=MN8TOARS}, DOI={10.1002/jez.1402610303}, abstractNote={AbstractOur goal is to understand the molecular mechanisms that govern the formation of the central nervous system. In particular, we have focused on the development of a small group of neurons and glia that lie along the midline of the Drosophila CNS. These midline cells possess a number of unique attributes which make them particularly amenable to molecular, cellular, and genetic examinations of nervous system formation and function. In addition, the midline cells exhibit distinctive ontogeny, morphology, anatomical position, and patterns of gene expression which suggest that they may provide unique functions to the developing CNS. The single‐minded gene encodes a nuclear protein which is specifically expressed in the midline cells and has been shown to play a crucial role in midline cell development and CNS formation. Genetic experiments reveal that sim is required for the expression of many CNS midline genes which are thought to be involved in the proper differentiation of these cells.In order to identify additional genes which are expressed in some or all of the midline cells at different developmental stages, a technique known as enhancer trap screening was employed. This screen led to the identification of a large number of potential genes which exhibit various midline expression patterns and may be involved in discrete aspects of midline cell development. Further molecular, genetic, and biochemical analyses of sim and several of the enhancer trap lines are being pursued. This should permit elucidation of the genetic hierarchy which acts in the specification, differentiation, and function of these CNS midline cells.}, number={3}, journal={Journal of Experimental Zoology}, author={Crews, S and Franks, R and Hu, S and Matthews, B and Nambu, J}, year={1992}, pages={234–244} } @article{nambu_franks_hu_crews_1990, title={The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells}, volume={63}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-0025107026&partnerID=MN8TOARS}, DOI={10.1016/0092-8674(90)90288-P}, abstractNote={The single-minded (itsim) gene of Drosophila encodes a nuclear protein that plays a critical role in the development of the neurons, glia, and other nonneuronal cells that lie along the midline of the embryonic CNS. Using distinct cell fate markers, we observe that in sim mutant embryos the midline cells fail to differentiate properly into their mature CNS cell types and do not take their appropriate positions within the developing CNS. We further present evidence that sim is required for midline expression of a group of genes including sllt, Toll, rhombold, engralled, and a gene at 91F; that the sim mutant CNS defect may be largely due to loss of midline slit expression; and that the snall gene is required to repress sim and other midline genes in the presumptive mesoderm.}, number={1}, journal={Cell}, author={Nambu, J.R. and Franks, R.G. and Hu, S. and Crews, S.T.}, year={1990}, pages={63–75} }