@article{dai_zhai_lin_wang_meng_li_mao_gao_ma_zhang_et al._2023, title={Cell-type-specific PtrWOX4a and PtrVCS2 form a regulatory nexus with a histone modification system for stem cambium development in Populus trichocarpa}, ISSN={["2055-0278"]}, DOI={10.1038/s41477-022-01315-7}, abstractNote={Stem vascular cambium cells in forest trees produce wood for materials and energy. WOX4 affects the proliferation of such cells in Populus. Here we show that PtrWOX4a is the most highly expressed stem vascular-cambium-specific (VCS) gene in P. trichocarpa, and its expression is controlled by the product of the second most highly expressed VCS gene, PtrVCS2, encoding a zinc finger protein. PtrVCS2 binds to the PtrWOX4a promoter as part of a PtrWOX13a-PtrVCS2-PtrGCN5-1-PtrADA2b-3 protein tetramer. PtrVCS2 prevented the interaction between PtrGCN5-1 and PtrADA2b-3, resulting in H3K9, H3K14 and H3K27 hypoacetylation at the PtrWOX4a promoter, which led to fewer cambium cell layers. These effects on cambium cell proliferation were consistent across more than 20 sets of transgenic lines overexpressing individual genes, gene-edited mutants and RNA interference lines in P. trichocarpa. We propose that the tetramer-PtrWOX4a system may coordinate genetic and epigenetic regulation to maintain normal vascular cambium development for wood formation.}, journal={NATURE PLANTS}, author={Dai, Xiufang and Zhai, Rui and Lin, Jiaojiao and Wang, Zhifeng and Meng, Dekai and Li, Meng and Mao, Yuli and Gao, Boyuan and Ma, Hongyan and Zhang, Baofeng and et al.}, year={2023}, month={Jan} }
 @article{sulis_jiang_yang_marques_matthews_miller_lan_cofre-vega_liu_sun_et al._2023, title={Multiplex CRISPR editing of wood for sustainable fiber production}, volume={381}, ISSN={["1095-9203"]}, url={http://europepmc.org/abstract/med/37440632}, DOI={10.1126/science.add4514}, abstractNote={The domestication of forest trees for a more sustainable fiber bioeconomy has long been hindered by the complexity and plasticity of lignin, a biopolymer in wood that is recalcitrant to chemical and enzymatic degradation. Here, we show that multiplex CRISPR editing enables precise woody feedstock design for combinatorial improvement of lignin composition and wood properties. By assessing every possible combination of 69,123 multigenic editing strategies for 21 lignin biosynthesis genes, we deduced seven different genome editing strategies targeting the concurrent alteration of up to six genes and produced 174 edited poplar variants. CRISPR editing increased the wood carbohydrate-to-lignin ratio up to 228% that of wild type, leading to more-efficient fiber pulping. The edited wood alleviates a major fiber-production bottleneck regardless of changes in tree growth rate and could bring unprecedented operational efficiencies, bioeconomic opportunities, and environmental benefits.}, number={6654}, journal={SCIENCE}, author={Sulis, Daniel B. and Jiang, Xiao and Yang, Chenmin and Marques, Barbara M. and Matthews, Megan L. and Miller, Zachary and Lan, Kai and Cofre-Vega, Carlos and Liu, Baoguang and Sun, Runkun and et al.}, year={2023}, month={Jul}, pages={216-+} }
 @article{liu_gao_sun_li_zhang_wang_zhou_sulis_wang_chiang_et al._2022, title={Dimerization of PtrMYB074 and PtrWRKY19 mediates transcriptional activation of PtrbHLH186 for secondary xylem development in Populus trichocarpa}, volume={5}, ISSN={["1469-8137"]}, url={http://europepmc.org/abstract/med/35152419}, DOI={10.1111/nph.18028}, abstractNote={Wood formation is controlled by transcriptional regulatory networks (TRNs) involving regulatory homeostasis determined by combinations of transcription factor (TF)-DNA and TF-TF interactions. Functions of TF-TF interactions in wood formation are still in the early stages of identification. PtrMYB074 is a woody dicot-specific TF in a TRN for wood formation in Populus trichocarpa. Here, using yeast two-hybrid and bimolecular fluorescence complementation, we conducted a genome-wide screening for PtrMYB074 interactors and identified 54 PtrMYB074-TF pairs. Of these pairs, 53 are novel. We focused on the PtrMYB074-PtrWRKY19 pair, the most highly expressed and xylem-specific interactor, and its direct transregulatory target, PtrbHLH186, the xylem-specific one of the pair's only two direct TF target genes. Using transient and CRISPR-mediated transgenesis in P. trichocarpa coupled with chromatin immunoprecipitation and electrophoretic mobility shift assays, we demonstrated that PtrMYB074 is recruited by PtrWRKY19 and that the PtrMYB074-PtrWRKY19 dimers are required to transactive PtrbHLH186. Overexpressing PtrbHLH186 in P. trichocarpa resulted in retarded plant growth, increased guaiacyl lignin, a higher proportion of smaller stem vessels and strong drought-tolerant phenotypes. Knowledge of the PtrMYB074-PtrWRKY19-PtrbHLH186 regulation may help design genetic controls of optimal growth and wood formation to maximize beneficial wood properties while minimizing negative effects on growth.}, journal={NEW PHYTOLOGIST}, author={Liu, Huizi and Gao, Jinghui and Sun, Jiatong and Li, Shuang and Zhang, Baofeng and Wang, Zhuwen and Zhou, Chenguang and Sulis, Daniel Barletta and Wang, Jack P. and Chiang, Vincent L. and et al.}, year={2022}, month={Mar} }
 @article{yu_zhou_li_li_lin_wang_chiang_li_2022, title={p A PtrLBD39-mediated transcriptional network regulates tension wood formation in Populus trichocarpa}, volume={3}, ISSN={["2590-3462"]}, url={http://europepmc.org/abstract/med/35059630}, DOI={10.1016/j.xplc.2021.100250}, abstractNote={Tension wood (TW) is a specialized xylem tissue formed in angiosperm trees under gravitational stimulus or mechanical stresses (e.g., bending). The genetic regulation that underlies this important mechanism remains poorly understood. Here, we used laser capture microdissection of stem xylem cells coupled with full transcriptome RNA-sequencing to analyze TW formation in Populus trichocarpa. After tree bending, PtrLBD39 was the most significantly induced transcription factor gene; it has a phylogenetically paired homolog, PtrLBD22. CRISPR-based knockout of PtrLBD39/22 severely inhibited TW formation, reducing cellulose and increasing lignin content. Transcriptomic analyses of CRISPR-based PtrLBD39/22 double mutants showed that these two genes regulate a set of TW-related genes. Chromatin immunoprecipitation sequencing (ChIP-seq) was used to identify direct targets of PtrLBD39. We integrated transcriptomic analyses and ChIP-seq assays to construct a transcriptional regulatory network (TRN) mediated by PtrLBD39. In this TRN, PtrLBD39 directly regulates 26 novel TW-responsive transcription factor genes. Our work suggests that PtrLBD39 and PtrLBD22 specifically control TW formation by mediating a TW-specific TRN in Populus.}, number={1}, journal={PLANT COMMUNICATIONS}, author={Yu, Jing and Zhou, Chenguang and Li, Danning and Li, Shuang and Lin, Ying-Chung Jimmy and Wang, Jack P. and Chiang, Vincent L. and Li, Wei}, year={2022}, month={Jan} }
 @misc{li_he_gao_zhou_chiang_li_2021, title={Histone Acetylation Changes in Plant Response to Drought Stress}, volume={12}, ISSN={["2073-4425"]}, DOI={10.3390/genes12091409}, abstractNote={Drought stress causes recurrent damage to a healthy ecosystem because it has major adverse effects on the growth and productivity of plants. However, plants have developed drought avoidance and resilience for survival through many strategies, such as increasing water absorption and conduction, reducing water loss and conversing growth stages. Understanding how plants respond and regulate drought stress would be important for creating and breeding better plants to help maintain a sound ecosystem. Epigenetic marks are a group of regulators affecting drought response and resilience in plants through modification of chromatin structure to control the transcription of pertinent genes. Histone acetylation is an ubiquitous epigenetic mark. The level of histone acetylation, which is regulated by histone acetyltransferases (HATs) and histone deacetylases (HDACs), determines whether the chromatin is open or closed, thereby controlling access of DNA-binding proteins for transcriptional activation. In this review, we summarize histone acetylation changes in plant response to drought stress, and review the functions of HATs and HDACs in drought response and resistance.}, number={9}, journal={GENES}, author={Li, Shuang and He, Xu and Gao, Yuan and Zhou, Chenguang and Chiang, Vincent L. and Li, Wei}, year={2021}, month={Sep} }
 @article{liu_liu_yu_wang_sun_li_lin_chiang_li_wang_2021, title={Transcriptional reprogramming of xylem cell wall biosynthesis in tension wood}, volume={186}, ISSN={["1532-2548"]}, url={https://doi.org/10.1093/plphys/kiab038}, DOI={10.1093/plphys/kiab038}, abstractNote={Abstract Tension wood (TW) is a specialized xylem tissue developed under mechanical/tension stress in angiosperm trees. TW development involves transregulation of secondary cell wall genes, which leads to altered wood properties for stress adaptation. We induced TW in the stems of black cottonwood (Populus trichocarpa, Nisqually-1) and identified two significantly repressed transcription factor (TF) genes: class B3 heat-shock TF (HSFB3-1) and MYB092. Transcriptomic analysis and chromatin immunoprecipitation (ChIP) were used to identify direct TF–DNA interactions in P. trichocarpa xylem protoplasts overexpressing the TFs. This analysis established a transcriptional regulatory network in which PtrHSFB3-1 and PtrMYB092 directly activate 8 and 11 monolignol genes, respectively. The TF–DNA interactions were verified for their specificity and transactivator roles in 35 independent CRISPR-based biallelic mutants and overexpression transgenic lines of PtrHSFB3-1 and PtrMYB092 in P. trichocarpa. The gene-edited trees (mimicking the repressed PtrHSFB3-1 and PtrMYB092 under tension stress) have stem wood composition resembling that of TW during normal growth and under tension stress (i.e., low lignin and high cellulose), whereas the overexpressors showed an opposite effect (high lignin and low cellulose). Individual overexpression of the TFs impeded lignin reduction under tension stress and restored high levels of lignin biosynthesis in the TW. This study offers biological insights to further uncover how metabolism, growth, and stress adaptation are coordinately regulated in trees.}, number={1}, journal={PLANT PHYSIOLOGY}, publisher={Oxford University Press (OUP)}, author={Liu, Baoguang and Liu, Juan and Yu, Jing and Wang, Zhifeng and Sun, Yi and Li, Shuang and Lin, Ying-Chung Jimmy and Chiang, Vincent L. and Li, Wei and Wang, Jack P.}, year={2021}, month={May}, pages={250–269} }
 @article{yeh_wang_miao_ma_kao_hsu_yu_hung_lin_kuan_et al._2019, title={A novel synthetic-genetic-array-based yeast one-hybrid system for high discovery rate and short processing time}, volume={29}, ISSN={["1549-5469"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85071056042&partnerID=MN8TOARS}, DOI={10.1101/gr.245951.118}, abstractNote={Eukaryotic gene expression is often tightly regulated by interactions between transcription factors (TFs) and their DNA cis targets. Yeast one-hybrid (Y1H) is one of the most extensively used methods to discover these interactions. We developed a high-throughput meiosis-directed yeast one-hybrid system using the Magic Markers of the synthetic genetic array analysis. The system has a transcription factor-DNA interaction discovery rate twice as high as the conventional diploid-mating approach and a processing time nearly one-tenth of the haploid-transformation method. The system also offers the highest accuracy in identifying TF-DNA interactions that can be authenticated in vivo by chromatin immunoprecipitation. With these unique features, this meiosis-directed Y1H system is particularly suited for constructing novel and comprehensive genome-scale gene regulatory networks for various organisms.}, number={8}, journal={GENOME RESEARCH}, author={Yeh, Chung-Shu and Wang, Zhifeng and Miao, Fang and Ma, Hongyan and Kao, Chung-Ting and Hsu, Tzu-Shu and Yu, Jhong-He and Hung, Er-Tsi and Lin, Chia-Chang and Kuan, Chen-Yu and et al.}, year={2019}, month={Aug}, pages={1343–1351} }
 @article{lin_chen_li_li_wang_shi_tunlaya-anukit_shuai_wang_ma_et al._2017, title={Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa}, volume={114}, ISSN={["0027-8424"]}, url={http://europepmc.org/abstract/med/29078399}, DOI={10.1073/pnas.1714422114}, abstractNote={Secondary cell wall (SCW) biosynthesis is the biological process that generates wood, an important renewable feedstock for materials and energy. NAC domain transcription factors, particularly Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND) proteins, are known to regulate SCW differentiation. The regulation of VND and SND is important to maintain homeostasis for plants to avoid abnormal growth and development. We previously identified a splice variant, PtrSND1-A2IR , derived from PtrSND1-A2 as a dominant-negative regulator, which suppresses the transactivation of all PtrSND1 family members. PtrSND1-A2IR also suppresses the self-activation of the PtrSND1 family members except for its cognate transcription factor, PtrSND1-A2, suggesting the existence of an unknown factor needed to regulate PtrSND1-A2 Here, a splice variant, PtrVND6-C1IR , derived from PtrVND6-C1 was discovered that suppresses the protein functions of all PtrVND6 family members. PtrVND6-C1IR also suppresses the expression of all PtrSND1 members, including PtrSND1-A2, demonstrating that PtrVND6-C1IR is the previously unidentified regulator of PtrSND1-A2 We also found that PtrVND6-C1IR cannot suppress the expression of its cognate transcription factor, PtrVND6-C1PtrVND6-C1 is suppressed by PtrSND1-A2IR Both PtrVND6-C1IR and PtrSND1-A2IR cannot suppress their cognate transcription factors but can suppress all members of the other family. The results indicate that the splice variants from the PtrVND6 and PtrSND1 family may exert reciprocal cross-regulation for complete transcriptional regulation of these two families in wood formation. This reciprocal cross-regulation between families suggests a general mechanism among NAC domain proteins and likely other transcription factors, where intron-retained splice variants provide an additional level of regulation.}, number={45}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Lin, Ying-Chung Jimmy and Chen, Hao and Li, Quanzi and Li, Wei and Wang, Jack P. and Shi, Rui and Tunlaya-Anukit, Sermsawat and Shuai, Peng and Wang, Zhifeng and Ma, Hongyan and et al.}, year={2017}, month={Nov}, pages={E9722–E9729} }
 @article{loziuk_parker_li_lin_wang_li_sederoff_chiang_muddiman_2015, title={Elucidation of Xylem-Specific Transcription Factors and Absolute Quantification of Enzymes Regulating Cellulose Biosynthesis in Populus trichocarpa}, volume={14}, ISSN={["1535-3907"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84942916917&partnerID=MN8TOARS}, DOI={10.1021/acs.jproteome.5b00233}, abstractNote={Cellulose, the main chemical polymer of wood, is the most abundant polysaccharide in nature.1 The ability to perturb the abundance and structure of cellulose microfibrils is of critical importance to the pulp and paper industry as well as for the textile, wood products, and liquid biofuels industries. Although much has been learned at the transcript level about the biosynthesis of cellulose, a quantitative understanding at the proteome level has yet to be established. The study described herein sought to identify the proteins directly involved in cellulose biosynthesis during wood formation in Populus trichocarpa along with known xylem-specific transcription factors involved in regulating these key proteins. Development of an effective discovery proteomic strategy through a combination of subcellular fractionation of stem differentiating xylem tissue (SDX) with recently optimized FASP digestion protocols, StageTip fractionation, as well as optimized instrument parameters for global proteomic analysis using the quadrupole-orbitrap mass spectrometer resulted in the deepest proteomic coverage of SDX protein from P. trichocarpa with 9,146 protein groups being identified (1% FDR). Of these, 20 cellulosic/hemicellulosic enzymes and 43 xylem-specific transcription factor groups were identified. Finally, selection of surrogate peptides led to an assay for absolute quantification of 14 cellulosic proteins in SDX of P. trichocarpa.}, number={10}, journal={JOURNAL OF PROTEOME RESEARCH}, author={Loziuk, Philip L. and Parker, Jennifer and Li, Wei and Lin, Chien-Yuan and Wang, Jack P. and Li, Quanzi and Sederoff, Ronald R. and Chiang, Vincent L. and Muddiman, David C.}, year={2015}, month={Oct}, pages={4158–4168} }
 @article{li_lin_li_shi_lin_chen_chuang_qu_sederoff_chiang_2014, title={A robust chromatin immunoprecipitation protocol for studying transcription factor-DNA interactions and histone modifications in wood-forming tissue}, volume={9}, ISSN={["1750-2799"]}, DOI={10.1038/nprot.2014.146}, number={9}, journal={NATURE PROTOCOLS}, author={Li, Wei and Lin, Ying-Chung and Li, Quanzi and Shi, Rui and Lin, Chien-Yuan and Chen, Hao and Chuang, Ling and Qu, Guan-Zheng and Sederoff, Ronald R. and Chiang, Vincent L.}, year={2014}, month={Sep}, pages={2180–2193} }
 @article{lin_li_chen_li_sun_shi_lin_wang_chen_chuang_et al._2014, title={A simple improved-throughput xylem protoplast system for studying wood formation}, volume={9}, ISSN={["1750-2799"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84907026654&partnerID=MN8TOARS}, DOI={10.1038/nprot.2014.147}, number={9}, journal={NATURE PROTOCOLS}, author={Lin, Ying-Chung and Li, Wei and Chen, Hao and Li, Quanzi and Sun, Ying-Hsuan and Shi, Rui and Lin, Chien-Yuan and Wang, Jack P. and Chen, Hsi-Chuan and Chuang, Ling and et al.}, year={2014}, month={Sep}, pages={2194–2205} }
 @article{lin_li_sun_kumari_wei_li_tunlaya-anukit_sederoff_chiang_2013, title={SND1 Transcription Factor-Directed Quantitative Functional Hierarchical Genetic Regulatory Network in Wood Formation in Populus trichocarpa}, volume={25}, ISSN={["1532-298X"]}, DOI={10.1105/tpc.113.117697}, abstractNote={Wood is an essential renewable raw material for industrial products and energy. However, knowledge of the genetic regulation of wood formation is limited. We developed a genome-wide high-throughput system for the discovery and validation of specific transcription factor (TF)-directed hierarchical gene regulatory networks (hGRNs) in wood formation. This system depends on a new robust procedure for isolation and transfection of Populus trichocarpa stem differentiating xylem protoplasts. We overexpressed Secondary Wall-Associated NAC Domain 1s (Ptr-SND1-B1), a TF gene affecting wood formation, in these protoplasts and identified differentially expressed genes by RNA sequencing. Direct Ptr-SND1-B1-DNA interactions were then inferred by integration of time-course RNA sequencing data and top-down Graphical Gaussian Modeling-based algorithms. These Ptr-SND1-B1-DNA interactions were verified to function in differentiating xylem by anti-PtrSND1-B1 antibody-based chromatin immunoprecipitation (97% accuracy) and in stable transgenic P. trichocarpa (90% accuracy). In this way, we established a Ptr-SND1-B1-directed quantitative hGRN involving 76 direct targets, including eight TF and 61 enzyme-coding genes previously unidentified as targets. The network can be extended to the third layer from the second-layer TFs by computation or by overexpression of a second-layer TF to identify a new group of direct targets (third layer). This approach would allow the sequential establishment, one two-layered hGRN at a time, of all layers involved in a more comprehensive hGRN. Our approach may be particularly useful to study hGRNs in complex processes in plant species resistant to stable genetic transformation and where mutants are unavailable.}, number={11}, journal={PLANT CELL}, author={Lin, Ying-Chung and Li, Wei and Sun, Ying-Hsuan and Kumari, Sapna and Wei, Hairong and Li, Quanzi and Tunlaya-Anukit, Sermsawat and Sederoff, Ronald R. and Chiang, Vincent L.}, year={2013}, month={Nov}, pages={4324–4341} }