Plant CellPub Date : 2024-09-03DOI: 10.1093/plcell/koae176
Peter Farkas, Teresa B Fitzpatrick
{"title":"Two pyridoxal phosphate homeostasis proteins are essential for management of the coenzyme pyridoxal 5'-phosphate in Arabidopsis.","authors":"Peter Farkas, Teresa B Fitzpatrick","doi":"10.1093/plcell/koae176","DOIUrl":"10.1093/plcell/koae176","url":null,"abstract":"<p><p>Coenzyme management is important for homeostasis of the pool of active metabolic enzymes. The coenzyme pyridoxal 5'-phosphate (PLP) is involved in diverse enzyme reactions including amino acid and hormone metabolism. Regulatory proteins that contribute to PLP homeostasis remain to be explored in plants. Here, we demonstrate the importance of proteins annotated as PLP homeostasis proteins (PLPHPs) for controlling PLP in Arabidopsis (Arabidopsis thaliana). A systematic analysis indicates that while most organisms across kingdoms have a single PLPHP homolog, Angiosperms have two. PLPHPs from Arabidopsis bind PLP and exist as monomers, in contrast to reported PLP-dependent enzymes, which exist as multimers. Disrupting the function of both PLPHP homologs perturbs vitamin B6 (pyridoxine) content, inducing a PLP deficit accompanied by light hypersensitive root growth, unlike PLP biosynthesis mutants. Micrografting studies show that the PLP deficit can be relieved distally between shoots and roots. Chemical treatments probing PLP-dependent reactions, notably those for auxin and ethylene, provide evidence that PLPHPs function in the dynamic management of PLP. Assays in vitro show that Arabidopsis PLPHP can coordinate PLP transfer and withdrawal from other enzymes. This study thus expands our knowledge of vitamin B6 biology and highlights the importance of PLP coenzyme homeostasis in plants.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371154/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141493086","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 : 2024-09-03DOI: 10.1093/plcell/koae164
Na Young Kang, Min-Jung Kim, Seon Jeong, Sun Young Moon, Jin Sun Kim, Jin Jeon, Boyoung Lee, Mi Rha Lee, Jungmook Kim
{"title":"HIGH PLOIDY2-mediated SUMOylation of transcription factor ARR1 controls two-component signaling in Arabidopsis.","authors":"Na Young Kang, Min-Jung Kim, Seon Jeong, Sun Young Moon, Jin Sun Kim, Jin Jeon, Boyoung Lee, Mi Rha Lee, Jungmook Kim","doi":"10.1093/plcell/koae164","DOIUrl":"10.1093/plcell/koae164","url":null,"abstract":"<p><p>Cytokinins regulate plant growth, development, and responses to environmental stresses such as cold via phosphorelay from cytokinin receptors to the ARABIDOPSIS RESPONSE REGULATORs (ARRs). However, the molecular mechanisms underlying the activation of type-B ARR transcriptional activity in Arabidopsis (Arabidopsis thaliana) remain unclear. Here, we show that the E3 SUMO ligase HIGH PLOIDY2 SUMOylates ARR1, a type-B ARR, at K236, triggering its activation. Cold- or cytokinin-induced phosphorylation of ARR1 at D89 is crucial for its interaction with HPY2. Lysine 236 is critical for ARR1's transactivation without compromising its DNA-binding ability, while D89 is crucial for ARR1's binding to target gene promoters. Cytokinin enhances ARR1's chromatin binding, but cold does not. ARR1 K236 plays a critical role in promoting histone H3 acetylation in response to both cytokinin and cold without affecting chromatin binding. The K236R mutation in ARR1 reduces target gene expression and alters cytokinin and cold response phenotypes. This study unveils a mechanism of ARR1 activation wherein phosphorylated ARR1 interacts with HPY2 and binds to chromatin in response to cytokinin. Cold triggers a phosphorelay targeting chromatin-bound ARR1. HPY2 then catalyzes ARR1 SUMOylation at K236, enhancing histone H3 acetylation and leading to transcriptional activation of ARR1 in response to both cold and cytokinin.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371144/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141180553","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 : 2024-09-03DOI: 10.1093/plcell/koae159
Yumeng Chen, Gaochen Jin, Mengyu Liu, Lanlan Wang, Yonggen Lou, Ian Baldwin, Ran Li
{"title":"Multiomic analyses reveal key sectors of jasmonate-mediated defense responses in rice.","authors":"Yumeng Chen, Gaochen Jin, Mengyu Liu, Lanlan Wang, Yonggen Lou, Ian Baldwin, Ran Li","doi":"10.1093/plcell/koae159","DOIUrl":"10.1093/plcell/koae159","url":null,"abstract":"<p><p>The phytohormone jasmonate (JA) plays a central role in plant defenses against biotic stressors. However, our knowledge of the JA signaling pathway in rice (Oryza sativa) remains incomplete. Here, we integrated multiomic data from three tissues to characterize the functional modules involved in organizing JA-responsive genes. In the core regulatory sector, MYC2 transcription factor transcriptional cascades are conserved in different species but with distinct regulators (e.g. bHLH6 in rice), in which genes are early expressed across all tissues. In the feedback sector, MYC2 also regulates the expression of JA repressor and catabolic genes, providing negative feedback that truncates the duration of JA responses. For example, the MYC2-regulated NAC (NAM, ATAF1/2, and CUC2) transcription factor genes NAC1, NAC3, and NAC4 encode proteins that repress JA signaling and herbivore resistance. In the tissue-specific sector, many late-expressed genes are associated with the biosynthesis of specialized metabolites that mediate particular defensive functions. For example, the terpene synthase gene TPS35 is specifically induced in the leaf sheath and TPS35 functions in defense against oviposition by brown planthoppers and the attraction of this herbivore's natural enemies. Thus, by characterizing core, tissue-specific, and feedback sectors of JA-elicited defense responses, this work provides a valuable resource for future discoveries of key JA components in this important crop.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371138/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141158775","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 : 2024-09-03DOI: 10.1093/plcell/koae170
Jannis Rinne, Markus Niehaus, Nieves Medina-Escobar, Henryk Straube, Frank Schaarschmidt, Nils Rugen, Hans-Peter Braun, Marco Herde, Claus-Peter Witte
{"title":"Three Arabidopsis UMP kinases have different roles in pyrimidine nucleotide biosynthesis and (deoxy)CMP salvage.","authors":"Jannis Rinne, Markus Niehaus, Nieves Medina-Escobar, Henryk Straube, Frank Schaarschmidt, Nils Rugen, Hans-Peter Braun, Marco Herde, Claus-Peter Witte","doi":"10.1093/plcell/koae170","DOIUrl":"10.1093/plcell/koae170","url":null,"abstract":"<p><p>Pyrimidine nucleotide monophosphate biosynthesis ends in the cytosol with uridine monophosphate (UMP). UMP phosphorylation to uridine diphosphate (UDP) by UMP KINASEs (UMKs) is required for the generation of all pyrimidine (deoxy)nucleoside triphosphates as building blocks for nucleic acids and central metabolites like UDP-glucose. The Arabidopsis (Arabidopsis thaliana) genome encodes five UMKs and three belong to the AMP KINASE (AMK)-like UMKs, which were characterized to elucidate their contribution to pyrimidine metabolism. Mitochondrial UMK2 and cytosolic UMK3 are evolutionarily conserved, whereas cytosolic UMK1 is specific to the Brassicaceae. In vitro, all UMKs can phosphorylate UMP, cytidine monophosphate (CMP) and deoxycytidine monophosphate (dCMP), but with different efficiencies. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated nuclease 9 (Cas9)-induced null mutants were generated for UMK1 and UMK2, but not for UMK3, since frameshift alleles were lethal for germline cells. However, a mutant with diminished UMK3 activity showing reduced growth was obtained. Metabolome analyses of germinating seeds and adult plants of single- and higher-order mutants revealed that UMK3 plays an indispensable role in the biosynthesis of all pyrimidine (deoxy)nucleotides and UDP-sugars, while UMK2 is important for dCMP recycling that contributes to mitochondrial DNA stability. UMK1 is primarily involved in CMP recycling. We discuss the specific roles of these UMKs referring also to the regulation of pyrimidine nucleoside triphosphate synthesis.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371195/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141311416","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 : 2024-09-03DOI: 10.1093/plcell/koae154
Toshiyuki Sakai, Mauricio P Contreras, Claudia Martinez-Anaya, Daniel Lüdke, Sophien Kamoun, Chih-Hang Wu, Hiroaki Adachi
{"title":"The NRC0 gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants.","authors":"Toshiyuki Sakai, Mauricio P Contreras, Claudia Martinez-Anaya, Daniel Lüdke, Sophien Kamoun, Chih-Hang Wu, Hiroaki Adachi","doi":"10.1093/plcell/koae154","DOIUrl":"10.1093/plcell/koae154","url":null,"abstract":"<p><p>Nucleotide-binding domain and leucine-rich repeat-containing receptor (NLR) proteins can form complex receptor networks to confer innate immunity. An NLR-REQUIRED FOR CELL DEATH (NRC) is a phylogenetically related node that functions downstream of a massively expanded network of disease resistance proteins that protect against multiple plant pathogens. In this study, we used phylogenomic methods to reconstruct the macroevolution of the NRC family. One of the NRCs, termed NRC0, is the only family member shared across asterid plants, leading us to investigate its evolutionary history and genetic organization. In several asterid species, NRC0 is genetically clustered with other NLRs that are phylogenetically related to NRC-dependent disease resistance genes. This prompted us to hypothesize that the ancestral state of the NRC network is an NLR helper-sensor gene cluster that was present early during asterid evolution. We provide support for this hypothesis by demonstrating that NRC0 is essential for the hypersensitive cell death that is induced by its genetically linked sensor NLR partners in 4 divergent asterid species: tomato (Solanum lycopersicum), wild sweet potato (Ipomoea trifida), coffee (Coffea canephora), and carrot (Daucus carota). In addition, activation of a sensor NLR leads to higher-order complex formation of its genetically linked NRC0, similar to other NRCs. Our findings map out contrasting evolutionary dynamics in the macroevolution of the NRC network over the last 125 million years, from a functionally conserved NLR gene cluster to a massive genetically dispersed network.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371149/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141248351","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 : 2024-09-03DOI: 10.1093/plcell/koae165
{"title":"Correction to: A commitment for life: Decades of unraveling the molecular mechanisms behind seed dormancy and germination.","authors":"","doi":"10.1093/plcell/koae165","DOIUrl":"10.1093/plcell/koae165","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371189/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141458712","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 : 2024-09-03DOI: 10.1093/plcell/koae186
Rory Osborne
{"title":"From the archives: Stress signaling-U-box proteins in the cold stress response, sensor activation in response to salt stress, and early work on salicylic acid signaling.","authors":"Rory Osborne","doi":"10.1093/plcell/koae186","DOIUrl":"10.1093/plcell/koae186","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371131/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141458713","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}
{"title":"The U-box E3 ubiquitin ligase PUB35 negatively regulates ABA signaling through AFP1-mediated degradation of ABI5.","authors":"Chang Du, Meng Liu, Yujie Yan, Xiaoyu Guo, Xiuping Cao, Yuzhe Jiao, Jiexuan Zheng, Yanchun Ma, Yuting Xie, Hongbo Li, Chengwei Yang, Caiji Gao, Qingzhen Zhao, Zhonghui Zhang","doi":"10.1093/plcell/koae194","DOIUrl":"10.1093/plcell/koae194","url":null,"abstract":"<p><p>Abscisic acid (ABA) signaling is crucial for plant responses to various abiotic stresses. The Arabidopsis (Arabidopsis thaliana) transcription factor ABA INSENSITIVE 5 (ABI5) is a central regulator of ABA signaling. ABI5 BINDING PROTEIN 1 (AFP1) interacts with ABI5 and facilitates its 26S-proteasome-mediated degradation, although the detailed mechanism has remained unclear. Here, we report that an ABA-responsive U-box E3 ubiquitin ligase, PLANT U-BOX 35 (PUB35), physically interacts with AFP1 and ABI5. PUB35 directly ubiquitinated ABI5 in a bacterially reconstituted ubiquitination system and promoted ABI5 protein degradation in vivo. ABI5 degradation was enhanced by AFP1 in response to ABA treatment. Phosphorylation of the T201 and T206 residues in ABI5 disrupted the ABI5-AFP1 interaction and affected the ABI5-PUB35 interaction and PUB35-mediated degradation of ABI5 in vivo. Genetic analysis of seed germination and seedling growth showed that pub35 mutants were hypersensitive to ABA as well as to salinity and osmotic stresses, whereas PUB35 overexpression lines were hyposensitive. Moreover, abi5 was epistatic to pub35, whereas the pub35-2 afp1-1 double mutant showed a similar ABA response to the two single mutants. Together, our results reveal a PUB35-AFP1 module involved in fine-tuning ABA signaling through ubiquitination and 26S-proteasome-mediated degradation of ABI5 during seed germination and seedling growth.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371175/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141458715","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 : 2024-09-03DOI: 10.1093/plcell/koae173
Zeyun Xue, Marina Ferrand, Elodie Gilbault, Olivier Zurfluh, Gilles Clément, Anne Marmagne, Stéphanie Huguet, José M Jiménez-Gómez, Anne Krapp, Christian Meyer, Olivier Loudet
{"title":"Natural variation in response to combined water and nitrogen deficiencies in Arabidopsis.","authors":"Zeyun Xue, Marina Ferrand, Elodie Gilbault, Olivier Zurfluh, Gilles Clément, Anne Marmagne, Stéphanie Huguet, José M Jiménez-Gómez, Anne Krapp, Christian Meyer, Olivier Loudet","doi":"10.1093/plcell/koae173","DOIUrl":"10.1093/plcell/koae173","url":null,"abstract":"<p><p>Understanding plant responses to individual stresses does not mean that we understand real-world situations, where stresses usually combine and interact. These interactions arise at different levels, from stress exposure to the molecular networks of the stress response. Here, we built an in-depth multiomic description of plant responses to mild water (W) and nitrogen (N) limitations, either individually or combined, among 5 genetically different Arabidopsis (Arabidopsis thaliana) accessions. We highlight the different dynamics in stress response through integrative traits such as rosette growth and the physiological status of the plants. We also used transcriptomic and metabolomic profiling during a stage when the plant response was stabilized to determine the wide diversity in stress-induced changes among accessions, highlighting the limited reality of a \"universal\" stress response. The main effect of the W × N interaction was an attenuation of the N-deficiency syndrome when combined with mild drought, but to a variable extent depending on the accession. Other traits subject to W × N interactions are often accession specific. Multiomic analyses identified a subset of transcript-metabolite clusters that are critical to stress responses but essentially variable according to the genotype factor. Including intraspecific diversity in our descriptions of plant stress response places our findings in perspective.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371182/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141446767","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 : 2024-09-03DOI: 10.1093/plcell/koae142
Yanan Liu, Edan Jackson, Xueru Liu, Xingchuan Huang, Renier A L van der Hoorn, Yuelin Zhang, Xin Li
{"title":"Proteolysis in plant immunity.","authors":"Yanan Liu, Edan Jackson, Xueru Liu, Xingchuan Huang, Renier A L van der Hoorn, Yuelin Zhang, Xin Li","doi":"10.1093/plcell/koae142","DOIUrl":"10.1093/plcell/koae142","url":null,"abstract":"<p><p>Compared with transcription and translation, protein degradation machineries can act faster and be targeted to different subcellular compartments, enabling immediate regulation of signaling events. It is therefore not surprising that proteolysis has been used extensively to control homeostasis of key regulators in different biological processes and pathways. Over the past decades, numerous studies have shown that proteolysis, where proteins are broken down to peptides or amino acids through ubiquitin-mediated degradation systems and proteases, is a key regulatory mechanism to control plant immunity output. Here, we briefly summarize the roles various proteases play during defence activation, focusing on recent findings. We also update the latest progress of ubiquitin-mediated degradation systems in modulating immunity by targeting plant membrane-localized pattern recognition receptors, intracellular nucleotide-binding domain leucine-rich repeat receptors, and downstream signaling components. Additionally, we highlight recent studies showcasing the importance of proteolysis in maintaining broad-spectrum resistance without obvious yield reduction, opening new directions for engineering elite crops that are resistant to a wide range of pathogens with high yield.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371161/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140897468","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}