{"title":"The transcription factors ZAT5 and BLH2/4 regulate homogalacturonan demethylesterification in Arabidopsis seed coat mucilage.","authors":"Minmin Xie, Anming Ding, Yongfeng Guo, Jinhao Sun, Wanya Qiu, Mingli Chen, Zhiyuan Li, Shanshan Li, Gongke Zhou, Yan Xu, Meng Wang, Aurore Richel, Daping Gong, Yingzhen Kong","doi":"10.1093/plcell/koae209","DOIUrl":"10.1093/plcell/koae209","url":null,"abstract":"<p><p>The level of methylesterification alters the functional properties of pectin, which is believed to influence plant growth and development. However, the mechanisms that regulate demethylesterification remain largely unexplored. Pectin with a high degree of methylesterification is produced in the Golgi apparatus and then transferred to the primary cell wall where it is partially demethylesterified by pectin methylesterases (PMEs). Here, we show that in Arabidopsis (Arabidopsis thaliana) seed mucilage, pectin demethylesterification is negatively regulated by the transcription factor ZINC FINGER FAMILY PROTEIN5 (ZAT5). Plants carrying null mutations in ZAT5 had increased PME activity, decreased pectin methylesterification, and produced seeds with a thinner mucilage layer. We provide evidence that ZAT5 binds to a TGATCA motif and thereby negatively regulates methylesterification by reducing the expression of PME5, HIGHLY METHYL ESTERIFIED SEEDS (HMS)/PME6, PME12, and PME16. We also demonstrate that ZAT5 physically interacts with BEL1-LIKE HOMEODOMAIN2 (BLH2) and BLH4 transcription factors. BLH2 and BLH4 are known to modulate pectin demethylesterification by directly regulating PME58 expression. The ZAT5-BLH2/4 interaction provides a mechanism to control the degree of pectin methylesterification in seed coat mucilage by modifying each transcription factor's ability to regulate the expression of target genes encoding PMEs. Taken together, these findings reveal a transcriptional regulatory module comprising ZAT5, BLH2, and BLH4, that functions in modulating the demethylesterification of homogalacturonan in seed coat mucilage.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4491-4510"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449064/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748886","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/koae205
Bradley Laflamme
{"title":"From the archives: A plant immune hub before, after, and way after its discovery.","authors":"Bradley Laflamme","doi":"10.1093/plcell/koae205","DOIUrl":"10.1093/plcell/koae205","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4267-4269"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449005/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141752389","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":"Dual roles of the MPK3 and MPK6 mitogen-activated protein kinases in regulating Arabidopsis stomatal development.","authors":"Mengyun Wu, Shiyuan Wang, Panpan Ma, Bixin Li, Huiqing Hu, Ziling Wang, Qin Qiu, Yujie Qiao, Dongdong Niu, Wolfgang Lukowitz, Shuqun Zhang, Mengmeng Zhang","doi":"10.1093/plcell/koae225","DOIUrl":"10.1093/plcell/koae225","url":null,"abstract":"<p><p>An Arabidopsis (Arabidopsis thaliana) mitogen-activated protein kinase (MAPK) cascade composed of YODA (YDA)-MKK4/MKK5-MPK3/MPK6 plays an essential role downstream of the ERECTA (ER)/ER-LIKE (ERL) receptor complex in regulating stomatal development in the leaf epidermis. STOMAGEN (STO), a peptide ligand produced in mesophyll cells, competes with EPIDERMAL PATTERNING FACTOR2 (EPF2) for binding ER/ERL receptors to promote stomatal formation. In this study, we found that activation of MPK3/MPK6 suppresses STO expression. Using MUTE and STO promoters that confer epidermis- and mesophyll-specific expression, respectively, we generated lines with cell-specific activation and suppression of MPK3/MPK6. The activation or suppression of MPK3/MPK6 in either epidermis or mesophyll cells is sufficient to alter stomatal differentiation. Epistatic analyses demonstrated that STO overexpression can rescue the suppression of stomatal formation conferred by the mesophyll-specific expression of the constitutively active MKK4DD or MKK5DD, but not by the epidermis-specific expression of these constitutively active MKKs. These data suggest that STO is downstream of MPK3/MPK6 in mesophyll cells, but upstream of MPK3/MPK6 in epidermal cells in stomatal development signaling. This function of the MPK3/MPK6 cascade allows it to coordinate plant epidermis development based on its activity in mesophyll cells during leaf development.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4576-4593"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141894014","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-10-03DOI: 10.1093/plcell/koae222
Anthony E Postiglione, Allison M Delange, Mohammad Foteh Ali, Eric Y Wang, Maarten Houben, Stacy L Hahn, Maleana G Khoury, Colleen M Roark, Molly Davis, Robert W Reid, James B Pease, Ann E Loraine, Gloria K Muday
{"title":"Flavonols improve tomato pollen thermotolerance during germination and tube elongation by maintaining reactive oxygen species homeostasis.","authors":"Anthony E Postiglione, Allison M Delange, Mohammad Foteh Ali, Eric Y Wang, Maarten Houben, Stacy L Hahn, Maleana G Khoury, Colleen M Roark, Molly Davis, Robert W Reid, James B Pease, Ann E Loraine, Gloria K Muday","doi":"10.1093/plcell/koae222","DOIUrl":"10.1093/plcell/koae222","url":null,"abstract":"<p><p>Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The tomato (Solanum lycopersicum) anthocyanin reduced (are) mutant harbors a mutation in FLAVANONE 3-HYDROXYLASE (F3H), resulting in impaired flavonol antioxidant biosynthesis. The are mutant has reduced pollen performance and seed set relative to the VF36 parental line, phenotypes that are accentuated at elevated temperatures. Transformation of are with the wild-type F3H gene, or chemical complementation with flavonols, prevented temperature-dependent reactive oxygen species (ROS) accumulation in pollen and restored the reduced viability, germination, and tube elongation of are to VF36 levels. Overexpression of F3H in VF36 prevented temperature-driven ROS increases and impaired pollen performance, revealing that flavonol biosynthesis promotes thermotolerance. Although stigmas of are had reduced flavonol and elevated ROS levels, the growth of are pollen tubes was similarly impaired in both are and VF36 pistils. RNA-seq was performed at optimal and stress temperatures in are, VF36, and the F3H overexpression line at multiple timepoints across pollen tube elongation. The number of differentially expressed genes increased over time under elevated temperatures in all genotypes, with the greatest number in are. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that lead to reproductive failure.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4511-4534"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449072/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141894015","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":"Large-volume fully automated cell reconstruction generates a cell atlas of plant tissues.","authors":"Zijian Hu, Jiazheng Liu, Shiya Shen, Weiqian Wu, Jingbin Yuan, Weiwei Shen, Lingyu Ma, Guangchao Wang, Shunyao Yang, Xiuping Xu, Yaning Cui, Zhenchen Li, Lijun Shen, Linlin Li, Jiahui Bian, Xi Zhang, Hua Han, Jinxing Lin","doi":"10.1093/plcell/koae250","DOIUrl":"https://doi.org/10.1093/plcell/koae250","url":null,"abstract":"<p><p>The geometric shape and arrangement of individual cells play a role in shaping organ functions. However, analyzing multicellular features and exploring their connectomes in centimeter-scale plant organs remain challenging. Here, we established a set of frameworks named Large-Volume Fully Automated Cell Reconstruction (LVACR), enabling the exploration of three-dimensional (3D) cytological features and cellular connectivity in plant tissues. Through benchmark testing, our framework demonstrated superior efficiency in cell segmentation and aggregation, successfully addressing the inherent challenges posed by light sheet fluorescence microscopy (LSFM) imaging. Using LVACR, we successfully established a cell atlas of different plant tissues. Cellular morphology analysis revealed differences of cell clusters and shapes in between different poplar (P. simonii Carr. and P. canadensis Moench.) seeds, whereas topological analysis revealed that they maintained conserved cellular connectivity. Furthermore, LVACR spatiotemporally demonstrated an initial burst of cell proliferation, accompanied by morphological transformations at an early stage in developing the shoot apical meristem. During subsequent development, cell differentiation produced anisotropic features, thereby resulting in various cell shapes. Overall, our findings provided valuable insights into the precise spatial arrangement and cellular behavior of multicellular organisms, thus enhancing our understanding of the complex processes underlying plant growth and differentiation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142293250","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant CellPub Date : 2024-09-03DOI: 10.1093/plcell/koae099
Xiaohong Zhuang, Baiying Li, Liwen Jiang
{"title":"Autophagosome biogenesis and organelle homeostasis in plant cells.","authors":"Xiaohong Zhuang, Baiying Li, Liwen Jiang","doi":"10.1093/plcell/koae099","DOIUrl":"10.1093/plcell/koae099","url":null,"abstract":"<p><p>Autophagy is one of the major highly inducible degradation processes in response to plant developmental and environmental signals. In response to different stimuli, cellular materials, including proteins and organelles, can be sequestered into a double membrane autophagosome structure either selectively or nonselectively. The formation of an autophagosome as well as its delivery into the vacuole involves complex and dynamic membrane processes. The identification and characterization of the conserved autophagy-related (ATG) proteins and their related regulators have greatly advanced our understanding of the molecular mechanism underlying autophagosome biogenesis and function in plant cells. Autophagosome biogenesis is tightly regulated by the coordination of multiple ATG and non-ATG proteins and by selective cargo recruitment. This review updates our current knowledge of autophagosome biogenesis, with special emphasis on the core molecular machinery that drives autophagosome formation and autophagosome-organelle interactions under abiotic stress conditions.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3009-3024"},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371174/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140306511","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/koae167
Lu Zhang, Lu Wang, Yongchen Fang, Yuhao Gao, Shulin Yang, Jun Su, Junbei Ni, Yuanwen Teng, Songling Bai
{"title":"Phosphorylated transcription factor PuHB40 mediates ROS-dependent anthocyanin biosynthesis in pear exposed to high light.","authors":"Lu Zhang, Lu Wang, Yongchen Fang, Yuhao Gao, Shulin Yang, Jun Su, Junbei Ni, Yuanwen Teng, Songling Bai","doi":"10.1093/plcell/koae167","DOIUrl":"10.1093/plcell/koae167","url":null,"abstract":"<p><p>Plants are increasingly vulnerable to environmental stresses because of global warming and climate change. Stress-induced reactive oxygen species (ROS) accumulation results in plant cell damage, even cell death. Anthocyanins are important antioxidants that scavenge ROS to maintain ROS homeostasis. However, the mechanism underlying ROS-induced anthocyanin accumulation is unclear. In this study, we determined that the HD-Zip I family member transcription factor PuHB40 mediates ROS-dependent anthocyanin biosynthesis under high-light stress in pear (Pyrus ussuriensis). Specifically, PuHB40 induces the PuMYB123-like-PubHLH3 transcription factor complex for anthocyanin biosynthesis. The PuHB40-mediated transcriptional activation depends on its phosphorylation level, which is regulated by protein phosphatase PP2A. Elevated ROS content maintains high PuHB40 phosphorylation levels while also enhancing the PuHB40-induced PuMYB123-like transcription by decreasing the PuPP2AA2 expression, ultimately leading to increased anthocyanin biosynthesis. Our study reveals a pathway regulating the ROS-induced anthocyanin biosynthesis in pears, further clarifying the mechanism underlying the abiotic stress-induced anthocyanin biosynthesis, which may have implications for improving plant stress tolerance.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3562-3583"},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371158/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141262610","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/koae178
Klaas J van Wijk
{"title":"Intra-chloroplast proteases: A holistic network view of chloroplast proteolysis.","authors":"Klaas J van Wijk","doi":"10.1093/plcell/koae178","DOIUrl":"10.1093/plcell/koae178","url":null,"abstract":"<p><p>Different proteases and peptidases are present within chloroplasts and nonphotosynthetic plastids to process precursor proteins and to degrade cleaved chloroplast transit peptides and damaged, misfolded, or otherwise unwanted proteins. Collectively, these proteases and peptidases form a proteolysis network, with complementary activities and hierarchies, and build-in redundancies. Furthermore, this network is distributed across the different intra-chloroplast compartments (lumen, thylakoid, stroma, envelope). The challenge is to determine the contributions of each peptidase (system) to this network in chloroplasts and nonphotosynthetic plastids. This will require an understanding of substrate recognition mechanisms, degrons, substrate, and product size limitations, as well as the capacity and degradation kinetics of each protease. Multiple extra-plastidial degradation pathways complement these intra-chloroplast proteases. This review summarizes our current understanding of these intra-chloroplast proteases in Arabidopsis and crop plants with an emphasis on considerations for building a qualitative and quantitative network view.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3116-3130"},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371162/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141331606","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/koae207
Lei Chu, Jixin Zhuang, Miaowei Geng, Yashi Zhang, Jing Zhu, Chunyu Zhang, Arp Schnittger, Bin Yi, Chao Yang
{"title":"ASYNAPSIS3 has diverse dosage-dependent effects on meiotic crossover formation in Brassica napus.","authors":"Lei Chu, Jixin Zhuang, Miaowei Geng, Yashi Zhang, Jing Zhu, Chunyu Zhang, Arp Schnittger, Bin Yi, Chao Yang","doi":"10.1093/plcell/koae207","DOIUrl":"10.1093/plcell/koae207","url":null,"abstract":"<p><p>Crossovers create genetic diversity and are required for equal chromosome segregation during meiosis. Crossover number and distribution are highly regulated by different mechanisms that are not yet fully understood, including crossover interference. The chromosome axis is crucial for crossover formation. Here, we explore the function of the axis protein ASYNAPSIS3. To this end, we use the allotetraploid species Brassica napus; due to its polyploid nature, this system allows a fine-grained dissection of the dosage of meiotic regulators. The simultaneous mutation of all 4 ASY3 alleles results in defective synapsis and drastic reduction of crossovers, which is largely rescued by the presence of only one functional ASY3 allele. Crucially, while the number of class I crossovers in mutants with 2 functional ASY3 alleles is comparable to that in wild type, this number is significantly increased in mutants with only one functional ASY3 allele, indicating that reducing ASY3 dosage increases crossover formation. Moreover, the class I crossovers on each bivalent in mutants with 1 functional ASY3 allele follow a random distribution, indicating compromised crossover interference. These results reveal the distinct dosage-dependent effects of ASY3 on crossover formation and provide insights into the role of the chromosome axis in patterning recombination.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3838-3856"},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371185/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141760358","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/koae160
Shiv Kumar Meena, Marti Quevedo, Sarah Muniz Nardeli, Clément Verez, Susheel Sagar Bhat, Vasiliki Zacharaki, Peter Kindgren
{"title":"Antisense transcription from stress-responsive transcription factors fine-tunes the cold response in Arabidopsis.","authors":"Shiv Kumar Meena, Marti Quevedo, Sarah Muniz Nardeli, Clément Verez, Susheel Sagar Bhat, Vasiliki Zacharaki, Peter Kindgren","doi":"10.1093/plcell/koae160","DOIUrl":"10.1093/plcell/koae160","url":null,"abstract":"<p><p>Transcription of antisense long noncoding RNAs (lncRNAs) occurs pervasively across eukaryotic genomes. Only a few antisense lncRNAs have been characterized and shown to control biological processes, albeit with idiosyncratic regulatory mechanisms. Thus, we largely lack knowledge about the general role of antisense transcription in eukaryotic organisms. Here, we characterized genes with antisense transcription initiating close to the poly(A) signal of genes (PAS genes) in Arabidopsis (Arabidopsis thaliana). We compared plant native elongation transcript sequencing (plaNET-seq) with RNA sequencing during short-term cold exposure and detected massive differences between the response in active transcription and steady-state levels of PAS gene-derived mRNAs. The cold-induced expression of transcription factors B-BOX DOMAIN PROTEIN28 (BBX28) and C2H2-TYPE ZINC FINGER FAMILY PROTEIN5 (ZAT5) was detected by plaNET-seq, while their steady-state level was only slightly altered due to high mRNA turnover. Knockdown of BBX28 and ZAT5 or of their respective antisense transcripts severely compromised plant freezing tolerance. Decreased antisense transcript expression levels resulted in a reduced cold response of BBX28 and ZAT5, revealing a positive regulatory role of both antisense transcripts. This study expands the known repertoire of noncoding transcripts. It highlights that native transcription approaches can complement steady-state RNA techniques to identify biologically relevant players in stress responses.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3467-3482"},"PeriodicalIF":10.0,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371176/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141158769","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}