Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae198
Jayne Griffiths, Annalisa Rizza, Bijun Tang, Wolf B Frommer, Alexander M Jones
{"title":"GIBBERELLIN PERCEPTION SENSOR 2 reveals genesis and role of cellular GA dynamics in light-regulated hypocotyl growth.","authors":"Jayne Griffiths, Annalisa Rizza, Bijun Tang, Wolf B Frommer, Alexander M Jones","doi":"10.1093/plcell/koae198","DOIUrl":"10.1093/plcell/koae198","url":null,"abstract":"<p><p>The phytohormone gibberellic acid (GA) is critical for environmentally sensitive plant development including germination, skotomorphogenesis, and flowering. The Förster resonance energy transfer biosensor GIBBERELLIN PERCEPTION SENSOR1, which permits single-cell GA measurements in vivo, has been used to observe a GA gradient correlated with cell length in dark-grown, but not light-grown, hypocotyls. We sought to understand how light signaling integrates into cellular GA regulation. Here, we show how the E3 ligase CONSTITUTIVE PHOTOMORPHOGENESIS1 (COP1) and transcription factor ELONGATED HYPOCOTYL 5 (HY5) play central roles in directing cellular GA distribution in skoto- and photomorphogenic hypocotyls, respectively. We demonstrate that the expression pattern of the GA biosynthetic enzyme gene GA20ox1 is the key determinant of the GA gradient in dark-grown hypocotyls and is a target of COP1 signaling. We engineered a second generation GPS2 biosensor with improved orthogonality and reversibility. GPS2 revealed a previously undetectable cellular pattern of GA depletion during the transition to growth in the light. This GA depletion partly explains the resetting of hypocotyl growth dynamics during photomorphogenesis. Achieving cell-level resolution has revealed how GA distributions link environmental conditions with morphology and morphological plasticity. The GPS2 biosensor is an ideal tool for GA studies in many conditions, organs, and plant species.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4426-4441"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449061/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748857","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae210
María A Ortega, Rhodesia M Celoy, Francisco Chacon, Yinan Yuan, Liang-Jiao Xue, Saurabh P Pandey, MaKenzie R Drowns, Brian H Kvitko, Chung-Jui Tsai
{"title":"Altering cold-regulated gene expression decouples the salicylic acid-growth trade-off in Arabidopsis.","authors":"María A Ortega, Rhodesia M Celoy, Francisco Chacon, Yinan Yuan, Liang-Jiao Xue, Saurabh P Pandey, MaKenzie R Drowns, Brian H Kvitko, Chung-Jui Tsai","doi":"10.1093/plcell/koae210","DOIUrl":"10.1093/plcell/koae210","url":null,"abstract":"<p><p>In Arabidopsis (Arabidopsis thaliana), overproduction of salicylic acid (SA) increases disease resistance and abiotic stress tolerance but penalizes growth. This growth-defense trade-off has hindered the adoption of SA-based disease management strategies in agriculture. However, investigation of how SA inhibits plant growth has been challenging because many SA-hyperaccumulating Arabidopsis mutants have developmental defects due to the pleiotropic effects of the underlying genes. Here, we heterologously expressed a bacterial SA synthase gene in Arabidopsis and observed that elevated SA levels decreased plant growth and reduced the expression of cold-regulated (COR) genes in a dose-dependent manner. Growth suppression was exacerbated at below-ambient temperatures. Severing the SA-responsiveness of individual COR genes was sufficient to overcome the growth inhibition caused by elevated SA at ambient and below-ambient temperatures while preserving disease- and abiotic-stress-related benefits. Our results show the potential of decoupling SA-mediated growth and defense trade-offs for improving crop productivity.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4293-4308"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448890/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141760357","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae042
David Rolo, Omar Sandoval-Ibáñez, Wolfram Thiele, Mark A Schöttler, Ines Gerlach, Reimo Zoschke, Joram Schwartzmann, Etienne H Meyer, Ralph Bock
{"title":"CO-EXPRESSED WITH PSI ASSEMBLY1 (CEPA1) is a photosystem I assembly factor in Arabidopsis.","authors":"David Rolo, Omar Sandoval-Ibáñez, Wolfram Thiele, Mark A Schöttler, Ines Gerlach, Reimo Zoschke, Joram Schwartzmann, Etienne H Meyer, Ralph Bock","doi":"10.1093/plcell/koae042","DOIUrl":"10.1093/plcell/koae042","url":null,"abstract":"<p><p>Photosystem I (PSI) forms a large macromolecular complex of ∼580 kDa that resides in the thylakoid membrane and mediates photosynthetic electron transfer. PSI is composed of 18 protein subunits and nearly 200 co-factors. The assembly of the complex in thylakoid membranes requires high spatial and temporal coordination, and is critically dependent on a sophisticated assembly machinery. Here, we report and characterize CO-EXPRESSED WITH PSI ASSEMBLY1 (CEPA1), a PSI assembly factor in Arabidopsis (Arabidopsis thaliana). The CEPA1 gene was identified bioinformatically as being co-expressed with known PSI assembly factors. Disruption of the CEPA1 gene leads to a pale phenotype and retarded plant development but does not entirely abolish photoautotrophy. Biophysical and biochemical analyses revealed that the phenotype is caused by a specific defect in PSI accumulation. We further show that CEPA1 acts at the post-translational level and co-localizes with PSI in nonappressed thylakoid membranes. In native gels, CEPA1 co-migrates with thylakoid protein complexes, including putative PSI assembly intermediates. Finally, protein-protein interaction assays suggest cooperation of CEPA1 with the PSI assembly factor PHOTOSYSTEM I ASSEMBLY3 (PSA3). Together, our data support an important but nonessential role of CEPA1 in PSI assembly.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4179-4211"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449006/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139932422","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae232
Thi Chi Tran, Karoline Mähl, Christian Kappel, Yuri Dakhiya, Arun Sampathkumar, Adrien Sicard, Michael Lenhard
{"title":"Altered interactions between cis-regulatory elements partially resolve BLADE-ON-PETIOLE genetic redundancy in Capsella rubella.","authors":"Thi Chi Tran, Karoline Mähl, Christian Kappel, Yuri Dakhiya, Arun Sampathkumar, Adrien Sicard, Michael Lenhard","doi":"10.1093/plcell/koae232","DOIUrl":"10.1093/plcell/koae232","url":null,"abstract":"<p><p>Duplicated genes are thought to follow one of three evolutionary trajectories that resolve their redundancy: neofunctionalization, subfunctionalization, or pseudogenization. Differences in expression patterns have been documented for many duplicated gene pairs and interpreted as evidence of subfunctionalization and a loss of redundancy. However, little is known about the functional impact of such differences and about their molecular basis. Here, we investigate the genetic and molecular basis for the partial loss of redundancy between the two BLADE-ON-PETIOLE genes BOP1 and BOP2 in red shepherd's purse (Capsella rubella) compared to Arabidopsis (Arabidopsis thaliana). While both genes remain almost fully redundant in A. thaliana, BOP1 in C. rubella can no longer ensure wild-type floral organ numbers and suppress bract formation, due to an altered expression pattern in the region of the cryptic bract primordium. We use two complementary approaches, transgenic rescue of A. thaliana atbop1 atbop2 double mutants and deletions in the endogenous AtBOP1 promoter, to demonstrate that several BOP1 promoter regions containing conserved noncoding sequences interact in a nonadditive manner to control BOP1 expression in the bract primordium and that changes in these interactions underlie the evolutionary divergence between C. rubella and A. thaliana BOP1 expression and activity. Similarly, altered interactions between cis-regulatory regions underlie the divergence in functional promoter architecture related to the control of floral organ abscission by BOP1. These findings highlight the complexity of promoter architecture in plants and suggest that changes in the interactions between cis-regulatory elements are key drivers for evolutionary divergence in gene expression and the loss of redundancy.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4637-4657"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448885/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142000589","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae191
Jian-Ping An, Lei Zhao, Yun-Peng Cao, Di Ai, Miao-Yi Li, Chun-Xiang You, Yuepeng Han
{"title":"The SMXL8-AGL9 module mediates crosstalk between strigolactone and gibberellin to regulate strigolactone-induced anthocyanin biosynthesis in apple.","authors":"Jian-Ping An, Lei Zhao, Yun-Peng Cao, Di Ai, Miao-Yi Li, Chun-Xiang You, Yuepeng Han","doi":"10.1093/plcell/koae191","DOIUrl":"10.1093/plcell/koae191","url":null,"abstract":"<p><p>Although the strigolactone (SL) signaling pathway and SL-mediated anthocyanin biosynthesis have been reported, the molecular association between SL signaling and anthocyanin biosynthesis remains unclear. In this study, we identified the SL signal transduction pathway associated with anthocyanin biosynthesis and the crosstalk between gibberellin (GA) and SL signaling in apple (Malus × domestica). ELONGATED HYPOCOTYL5 (HY5) acts as a key node integrating SL signaling and anthocyanin biosynthesis, and the SL-response factor AGAMOUS-LIKE MADS-BOX9 (AGL9) promotes anthocyanin biosynthesis by activating HY5 transcription. The SL signaling repressor SUPPRESSOR OF MAX2 1-LIKE8 (SMXL8) interacts with AGL9 to form a complex that inhibits anthocyanin biosynthesis by downregulating HY5 expression. Moreover, the E3 ubiquitin ligase PROTEOLYSIS1 (PRT1) mediates the ubiquitination-mediated degradation of SMXL8, which is a key part of the SL signal transduction pathway associated with anthocyanin biosynthesis. In addition, the GA signaling repressor REPRESSOR-of-ga1-3-LIKE2a (RGL2a) mediates the crosstalk between GA and SL by disrupting the SMXL8-AGL9 interaction that represses HY5 transcription. Taken together, our study reveals the regulatory mechanism of SL-mediated anthocyanin biosynthesis and uncovers the role of SL-GA crosstalk in regulating anthocyanin biosynthesis in apple.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4404-4425"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448916/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141451204","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae204
Nancy A Eckardt, Ralph Bock, Roberta Croce, J Clark Lagarias, Sabeeha S Merchant, Kevin Redding
{"title":"Focus on photosynthesis.","authors":"Nancy A Eckardt, Ralph Bock, Roberta Croce, J Clark Lagarias, Sabeeha S Merchant, Kevin Redding","doi":"10.1093/plcell/koae204","DOIUrl":"10.1093/plcell/koae204","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3895-3896"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448878/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141731327","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae227
Tao Shi, Zhiyan Gao, Jinming Chen, Yves Van de Peer
{"title":"Dosage sensitivity shapes balanced expression and gene longevity of homoeologs after whole-genome duplications in angiosperms.","authors":"Tao Shi, Zhiyan Gao, Jinming Chen, Yves Van de Peer","doi":"10.1093/plcell/koae227","DOIUrl":"10.1093/plcell/koae227","url":null,"abstract":"<p><p>Following whole-genome duplication (WGD), duplicate gene pairs (homoeologs) can evolve varying degrees of expression divergence. However, the determinants influencing these relative expression level differences (RFPKM) between homoeologs remain elusive. In this study, we analyzed the RFPKM between homoeologs in 3 angiosperms, Nymphaea colorata, Nelumbo nucifera, and Acorus tatarinowii, all having undergone a single WGD since the origin of angiosperms. Our results show significant positive correlations in RFPKM of homoeologs among tissues within the same species, and among orthologs across these 3 species, indicating convergent expression balance/bias between homoeologous gene copies following independent WGDs. We linked RFPKM between homoeologs to gene attributes associated with dosage-balance constraints, such as protein-protein interactions, lethal-phenotype scores in Arabidopsis (Arabidopsis thaliana) orthologs, domain numbers, and expression breadth. Notably, homoeologs with lower RFPKM often had more interactions and higher lethal-phenotype scores, indicating selective pressures favoring balanced expression. Also, homoeologs with lower RFPKM were more likely to be retained after WGDs in angiosperms. Within Nelumbo, greater RFPKM between homoeologs correlated with increased cis- and trans-regulatory differentiation between species, highlighting the ongoing escalation of gene expression divergence. We further found that expression degeneration in 1 copy of homoeologs is inclined toward nonfunctionalization. Our research highlights the importance of balanced expression, shaped by dosage-balance constraints, in the evolutionary retention of homoeologs in plants.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4323-4337"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7616505/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141910032","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}