Programmed cell death (PCD) occurs in different tissues in response to a number of different signals in plant cells. Drawing from work in several different contexts, including root-cap cell differentiation, plant response to biotic and abiotic stress, and some self-incompatibility (SI) systems, the data suggest that, despite differences, there are underlying commonalities in the early decision-making stages of PCD. Here, we focus on how 2 cellular events, increased [Ca2+]cyt levels and cytosolic acidification, appear to act as early signals involved in regulating both developmental and stimulus-induced PCD in plant cells.
{"title":"Regulating programmed cell death in plant cells: Intracellular acidification plays a pivotal role together with calcium signaling.","authors":"Maurice Bosch, Vernonica Franklin-Tong","doi":"10.1093/plcell/koae245","DOIUrl":"10.1093/plcell/koae245","url":null,"abstract":"<p><p>Programmed cell death (PCD) occurs in different tissues in response to a number of different signals in plant cells. Drawing from work in several different contexts, including root-cap cell differentiation, plant response to biotic and abiotic stress, and some self-incompatibility (SI) systems, the data suggest that, despite differences, there are underlying commonalities in the early decision-making stages of PCD. Here, we focus on how 2 cellular events, increased [Ca2+]cyt levels and cytosolic acidification, appear to act as early signals involved in regulating both developmental and stimulus-induced PCD in plant cells.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4692-4702"},"PeriodicalIF":10.0,"publicationDate":"2024-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11530775/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142086143","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":"From the archives: Epidermal affairs-EVER links floral scent with cuticular waxes, while SPL9 and DEWAX connect them to diurnal regulation, and FIDDLEHEAD takes on a function in the epidermis.","authors":"Christian Damian Lorenzo","doi":"10.1093/plcell/koae231","DOIUrl":"10.1093/plcell/koae231","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4675-4677"},"PeriodicalIF":10.0,"publicationDate":"2024-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11530769/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141982991","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}
Photorespiration is an energetically costly metabolic pathway in plants that responds to environmental stresses. The molecular basis of the regulation of the photorespiratory cycle under stress conditions remains unclear. Here, we discovered that FERONIA (FER) regulates photorespiratory flow under salt stress in Arabidopsis (Arabidopsis thaliana). FER mutation results in hypersensitivity to salt stress, but disruption of ferredoxin-dependent glutamate synthase 1 (GLU1), an enzyme that participates in the photorespiratory pathway by producing glutamate, greatly suppresses fer-4 hypersensitivity to salt stress primarily due to reduced glycine yield. In contrast, disrupting mitochondrial serine hydroxymethyltransferase1 (SHM1), which is supposed to increase glycine levels by hampering the conversion of glycine to serine in the photorespiratory cycle, aggravates fer-4 hypersensitivity to salt stress. Biochemical data show that FER interacts with and phosphorylates SHM1, and this phosphorylation modulates SHM1 stability. Additionally, the production of proline and its intermediate △1-pyrroline-5-carboxylate (P5C), which are both synthesized from glutamate, also contributes to fer-4 hypersensitivity to salt stress. In conclusion, this study elucidates the functional mechanism of FER in regulating salt tolerance by modulating photorespiratory flux, which greatly broadens our understanding of how plants adapt to high salinity.
{"title":"FERONIA regulates salt tolerance in Arabidopsis by controlling photorespiratory flux.","authors":"Wei Jiang, Zhihao Wang, Yali Li, Xin Liu, Yuying Ren, Chao Li, Shengji Luo, Rahul Mohan Singh, Yan Li, Chanhong Kim, Chunzhao Zhao","doi":"10.1093/plcell/koae246","DOIUrl":"10.1093/plcell/koae246","url":null,"abstract":"<p><p>Photorespiration is an energetically costly metabolic pathway in plants that responds to environmental stresses. The molecular basis of the regulation of the photorespiratory cycle under stress conditions remains unclear. Here, we discovered that FERONIA (FER) regulates photorespiratory flow under salt stress in Arabidopsis (Arabidopsis thaliana). FER mutation results in hypersensitivity to salt stress, but disruption of ferredoxin-dependent glutamate synthase 1 (GLU1), an enzyme that participates in the photorespiratory pathway by producing glutamate, greatly suppresses fer-4 hypersensitivity to salt stress primarily due to reduced glycine yield. In contrast, disrupting mitochondrial serine hydroxymethyltransferase1 (SHM1), which is supposed to increase glycine levels by hampering the conversion of glycine to serine in the photorespiratory cycle, aggravates fer-4 hypersensitivity to salt stress. Biochemical data show that FER interacts with and phosphorylates SHM1, and this phosphorylation modulates SHM1 stability. Additionally, the production of proline and its intermediate △1-pyrroline-5-carboxylate (P5C), which are both synthesized from glutamate, also contributes to fer-4 hypersensitivity to salt stress. In conclusion, this study elucidates the functional mechanism of FER in regulating salt tolerance by modulating photorespiratory flux, which greatly broadens our understanding of how plants adapt to high salinity.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4732-4751"},"PeriodicalIF":10.0,"publicationDate":"2024-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11530776/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142086142","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}
Yukihisa Goto, Yasuhiro Kadota, Malick Mbengue, Jennifer D Lewis, Hidenori Matsui, Noriko Maki, Bruno Pok Man Ngou, Jan Sklenar, Paul Derbyshire, Arisa Shibata, Yasunori Ichihashi, David S Guttman, Hirofumi Nakagami, Takamasa Suzuki, Frank L H Menke, Silke Robatzek, Darrell Desveaux, Cyril Zipfel, Ken Shirasu
Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) such as ELONGATION Factor-TU (EF-TU) RECEPTOR (EFR) and FLAGELLIN SENSING 2 (FLS2), which recognize bacterial EF-Tu and flagellin, respectively. These PRRs belong to the leucine-rich repeat receptor kinase (LRR-RK) family and activate the production of reactive oxygen species via the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD). The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogen effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative coimmunoprecipitation analysis using EFR, FLS2, and RBOHD in Arabidopsis thaliana. We identified QIAN SHOU KINASE 1 (QSK1), an LRR-RK, as a PRR-RBOHD complex-associated protein. QSK1 downregulated FLS2 and EFR abundance, functioning as a negative regulator of PRR-triggered immunity (PTI). QSK1 was targeted by the bacterial effector HopF2Pto, a mono-ADP ribosyltransferase, reducing FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2Pto transcriptionally downregulated PROSCOOP genes encoding important stress-regulated phytocytokines and their receptor MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2. Importantly, HopF2Pto requires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide insights into the mechanism by which HopF2Pto employs QSK1 to desensitize plants to pathogen attack.
{"title":"The leucine-rich repeat receptor kinase QSK1 regulates PRR-RBOHD complexes targeted by the bacterial effector HopF2Pto.","authors":"Yukihisa Goto, Yasuhiro Kadota, Malick Mbengue, Jennifer D Lewis, Hidenori Matsui, Noriko Maki, Bruno Pok Man Ngou, Jan Sklenar, Paul Derbyshire, Arisa Shibata, Yasunori Ichihashi, David S Guttman, Hirofumi Nakagami, Takamasa Suzuki, Frank L H Menke, Silke Robatzek, Darrell Desveaux, Cyril Zipfel, Ken Shirasu","doi":"10.1093/plcell/koae267","DOIUrl":"https://doi.org/10.1093/plcell/koae267","url":null,"abstract":"<p><p>Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) such as ELONGATION Factor-TU (EF-TU) RECEPTOR (EFR) and FLAGELLIN SENSING 2 (FLS2), which recognize bacterial EF-Tu and flagellin, respectively. These PRRs belong to the leucine-rich repeat receptor kinase (LRR-RK) family and activate the production of reactive oxygen species via the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD). The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogen effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative coimmunoprecipitation analysis using EFR, FLS2, and RBOHD in Arabidopsis thaliana. We identified QIAN SHOU KINASE 1 (QSK1), an LRR-RK, as a PRR-RBOHD complex-associated protein. QSK1 downregulated FLS2 and EFR abundance, functioning as a negative regulator of PRR-triggered immunity (PTI). QSK1 was targeted by the bacterial effector HopF2Pto, a mono-ADP ribosyltransferase, reducing FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2Pto transcriptionally downregulated PROSCOOP genes encoding important stress-regulated phytocytokines and their receptor MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2. Importantly, HopF2Pto requires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide insights into the mechanism by which HopF2Pto employs QSK1 to desensitize plants to pathogen attack.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472550","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}
Qi He, Hao Wu, Longjun Zeng, Caiyun Yin, Li Wang, Yiqing Tan, Wanqing Lv, Zhiqiang Liao, Xuelian Zheng, Shuting Zhang, Qinqin Han, Danning Wang, Yong Zhang, Guosheng Xiong, Quan Wang
Plant height is an important agronomic characteristic of rice (Oryza sativa L.). Map-based cloning analyses of a natural semi-dwarf rice mutant with inwardly curled leaves found in the field revealed that the defects were due to a mutation of a SHAQKYF-class MYB family transcription factor, OsKANADI1 (OsKAN1). OsKAN1 directly bound to the OsYABBY5 (OsYAB5) promoter to repress its expression and interacted with OsYAB5 to form a functional OsKAN1-OsYAB5 complex. GIBERELLIN 2-OXIDASE6 (OsGA2ox6), encoding an enzyme in the gibberellin (GA) catabolic pathway, was activated by OsYAB5. Furthermore, the OsKAN1-OsYAB5 complex suppressed the inhibitory effect of OsKAN1 toward OsYAB5 and inhibited OsYAB5-induced OsGA2ox6 expression. The proOsKAN1:OsYAB5 transgenic plants were taller than wild-type plants, whereas oskan1 proOsKAN1:OsYAB5 plants exhibited a severe dwarf phenotype due to the absence of the OsKAN1-OsYAB5 complex. The OsKAN1-OsYAB5 complex modulated OsGA2ox6 expression, thereby regulating the levels of bioactive gibberellins and, consequently, plant height. This study elucidated the mechanism underlying the effect of the OsKAN1-OsYAB5-OsGA2ox6 regulatory pathway on plant height at different positions in rice stems and provided insights on stem development and candidate genes for the aerial architecture improvement of crop plants.
{"title":"OsKANADI1 and OsYABBY5 regulate rice plant height by targeting GIBERELLIN 2-OXIDASE6.","authors":"Qi He, Hao Wu, Longjun Zeng, Caiyun Yin, Li Wang, Yiqing Tan, Wanqing Lv, Zhiqiang Liao, Xuelian Zheng, Shuting Zhang, Qinqin Han, Danning Wang, Yong Zhang, Guosheng Xiong, Quan Wang","doi":"10.1093/plcell/koae276","DOIUrl":"https://doi.org/10.1093/plcell/koae276","url":null,"abstract":"<p><p>Plant height is an important agronomic characteristic of rice (Oryza sativa L.). Map-based cloning analyses of a natural semi-dwarf rice mutant with inwardly curled leaves found in the field revealed that the defects were due to a mutation of a SHAQKYF-class MYB family transcription factor, OsKANADI1 (OsKAN1). OsKAN1 directly bound to the OsYABBY5 (OsYAB5) promoter to repress its expression and interacted with OsYAB5 to form a functional OsKAN1-OsYAB5 complex. GIBERELLIN 2-OXIDASE6 (OsGA2ox6), encoding an enzyme in the gibberellin (GA) catabolic pathway, was activated by OsYAB5. Furthermore, the OsKAN1-OsYAB5 complex suppressed the inhibitory effect of OsKAN1 toward OsYAB5 and inhibited OsYAB5-induced OsGA2ox6 expression. The proOsKAN1:OsYAB5 transgenic plants were taller than wild-type plants, whereas oskan1 proOsKAN1:OsYAB5 plants exhibited a severe dwarf phenotype due to the absence of the OsKAN1-OsYAB5 complex. The OsKAN1-OsYAB5 complex modulated OsGA2ox6 expression, thereby regulating the levels of bioactive gibberellins and, consequently, plant height. This study elucidated the mechanism underlying the effect of the OsKAN1-OsYAB5-OsGA2ox6 regulatory pathway on plant height at different positions in rice stems and provided insights on stem development and candidate genes for the aerial architecture improvement of crop plants.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142392432","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}
Nolwenn Guéguen, Yannick Sérès, Félix Cicéron, Valérie Gros, Grégory Si Larbi, Denis Falconet, Etienne Deragon, Siraba D Gueye, Damien Le Moigne, Marion Schilling, Mathilde Cussac, Dimitris Petroutsos, Hanhua Hu, Yangmin Gong, Morgane Michaud, Juliette Jouhet, Juliette Salvaing, Alberto Amato, Eric Maréchal
Diatoms derive from a secondary endosymbiosis event, which occurred when a eukaryotic host cell engulfed a red alga. This led to the formation of a complex plastid enclosed by four membranes: two innermost membranes originating from the red alga chloroplast envelope, and two additional peri- and epiplastidial membranes (PPM, EpM). The EpM is linked to the endoplasmic reticulum (ER). The most abundant membrane lipid in diatoms is monogalactosyldiacylglycerol (MGDG), synthesized by galactosyltransferases called MGDG synthases (MGDs), conserved in photosynthetic eukaryotes and considered to be specific to chloroplast membranes. Similar to angiosperms, a multigenic family of MGDs has evolved in diatoms, but through an independent process. We characterized MGDα, MGDβ and MGDγ in Phaeodactylum tricornutum, combining molecular analyses, heterologous expression in Saccharomyces cerevisiae, and studying overexpressing and CRISPR-Cas9-edited lines. MGDα localizes mainly to thylakoids, MGDβ to the PPM, and MGDγ to the ER and EpM. MGDs have distinct specificities for diacylglycerol, consistent with their localization. Results suggest that MGDα is required for thylakoid expansion under optimal conditions, while MGDβ and MGDγ play roles in plastid and non-plastid membranes and in response to environmental stress. Functional compensation among MGDs likely contributes to diatom resilience under adverse conditions and to their ecological success.
{"title":"Monogalactosyldiacylglycerol synthase isoforms play diverse roles inside and outside the diatom plastid.","authors":"Nolwenn Guéguen, Yannick Sérès, Félix Cicéron, Valérie Gros, Grégory Si Larbi, Denis Falconet, Etienne Deragon, Siraba D Gueye, Damien Le Moigne, Marion Schilling, Mathilde Cussac, Dimitris Petroutsos, Hanhua Hu, Yangmin Gong, Morgane Michaud, Juliette Jouhet, Juliette Salvaing, Alberto Amato, Eric Maréchal","doi":"10.1093/plcell/koae275","DOIUrl":"https://doi.org/10.1093/plcell/koae275","url":null,"abstract":"<p><p>Diatoms derive from a secondary endosymbiosis event, which occurred when a eukaryotic host cell engulfed a red alga. This led to the formation of a complex plastid enclosed by four membranes: two innermost membranes originating from the red alga chloroplast envelope, and two additional peri- and epiplastidial membranes (PPM, EpM). The EpM is linked to the endoplasmic reticulum (ER). The most abundant membrane lipid in diatoms is monogalactosyldiacylglycerol (MGDG), synthesized by galactosyltransferases called MGDG synthases (MGDs), conserved in photosynthetic eukaryotes and considered to be specific to chloroplast membranes. Similar to angiosperms, a multigenic family of MGDs has evolved in diatoms, but through an independent process. We characterized MGDα, MGDβ and MGDγ in Phaeodactylum tricornutum, combining molecular analyses, heterologous expression in Saccharomyces cerevisiae, and studying overexpressing and CRISPR-Cas9-edited lines. MGDα localizes mainly to thylakoids, MGDβ to the PPM, and MGDγ to the ER and EpM. MGDs have distinct specificities for diacylglycerol, consistent with their localization. Results suggest that MGDα is required for thylakoid expansion under optimal conditions, while MGDβ and MGDγ play roles in plastid and non-plastid membranes and in response to environmental stress. Functional compensation among MGDs likely contributes to diatom resilience under adverse conditions and to their ecological success.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142392431","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}
Xin Wang, Jiaxin Liu, Erlei Shang, Amangul Hawar, Toshiro Ito, Bo Sun
Brassinosteroid (BR) signaling and the C-class MADS-box gene AGAMOUS (AG) play important roles in ovule development in Arabidopsis (Arabidopsis thaliana). However, how BR signaling integrates with AG functions to control the female reproductive process remains elusive. Here, we showed that the regulatory role of BR signaling in proper ovule development is mediated by the transcriptional repressor gene ZINC FINGER PROTEIN 11 (ZFP11), which is a direct target of AG. ZFP11 expression initiates from the placenta upon AG induction and becomes prominent in the funiculus of ovule primordia. Plants harboring zfp11 mutations showed reduced placental length with decreased ovule numbers and some aborted ovules. During ovule development, the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1), which functions downstream of BR signaling, inhibits ZFP11 expression in the chalaza and nucellus. Weakened BR signaling leads to stunted integuments in ovules, resulting from the direct repression of INNER NO OUTER (INO) and WUSCHEL (WUS) by extended ZFP11 expression in the chalaza and nucellus, respectively. In addition, the zfp11 mutant shows reduced sensitivity to BR biosynthesis inhibitors and can rescue outer integument defects in brassinosteroid insensitive 1 (bri1) mutants. Thus, the precise spatial regulation of ZFP11, which is activated by AG in the placenta and suppressed by BR signaling in the central and distal regions of ovules, is essential for ensuring sufficient ovule numbers and proper ovule formation.
类芸香苷(BR)信号和 C 级 MADS-box 基因 AGAMOUS(AG)在拟南芥(Arabidopsis thaliana)胚珠发育过程中发挥着重要作用。然而,BR 信号如何与 AG 功能相结合以控制雌性生殖过程仍是一个未知数。在这里,我们发现,BR 信号在胚珠正常发育过程中的调控作用是由转录抑制基因 ZINC FINGER PROTEIN 11(ZFP11)介导的,而 ZFP11 是 AG 的直接靶标。ZFP11 的表达在 AG 诱导时从胎座开始,并在胚珠原基的漏斗部变得突出。携带 zfp11 基因突变的植株胎盘长度缩短,胚珠数量减少,部分胚珠流产。在胚珠发育过程中,BR 信号转导下游的转录因子 BRASSINAZOLE-RESISTANT 1(BZR1)会抑制 ZFP11 在子房和核部的表达。BR信号的减弱导致胚珠中的整粒发育不良,这是因为ZFP11在颖果和核果中的延长表达分别直接抑制了INNER NO OUTER(INO)和WUSCHEL(WUS)。此外,zfp11突变体对BR生物合成抑制剂的敏感性降低,并能挽救黄铜类固醇不敏感1(bri1)突变体的外被膜缺陷。因此,ZFP11在胎盘中被AG激活,在胚珠的中央和远端区域被BR信号抑制,其精确的空间调控对于确保足够的胚珠数量和适当的胚珠形成至关重要。
{"title":"Brassinosteroid signaling represses ZINC FINGER PROTEIN11 to regulate ovule development in Arabidopsis.","authors":"Xin Wang, Jiaxin Liu, Erlei Shang, Amangul Hawar, Toshiro Ito, Bo Sun","doi":"10.1093/plcell/koae273","DOIUrl":"https://doi.org/10.1093/plcell/koae273","url":null,"abstract":"<p><p>Brassinosteroid (BR) signaling and the C-class MADS-box gene AGAMOUS (AG) play important roles in ovule development in Arabidopsis (Arabidopsis thaliana). However, how BR signaling integrates with AG functions to control the female reproductive process remains elusive. Here, we showed that the regulatory role of BR signaling in proper ovule development is mediated by the transcriptional repressor gene ZINC FINGER PROTEIN 11 (ZFP11), which is a direct target of AG. ZFP11 expression initiates from the placenta upon AG induction and becomes prominent in the funiculus of ovule primordia. Plants harboring zfp11 mutations showed reduced placental length with decreased ovule numbers and some aborted ovules. During ovule development, the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1), which functions downstream of BR signaling, inhibits ZFP11 expression in the chalaza and nucellus. Weakened BR signaling leads to stunted integuments in ovules, resulting from the direct repression of INNER NO OUTER (INO) and WUSCHEL (WUS) by extended ZFP11 expression in the chalaza and nucellus, respectively. In addition, the zfp11 mutant shows reduced sensitivity to BR biosynthesis inhibitors and can rescue outer integument defects in brassinosteroid insensitive 1 (bri1) mutants. Thus, the precise spatial regulation of ZFP11, which is activated by AG in the placenta and suppressed by BR signaling in the central and distal regions of ovules, is essential for ensuring sufficient ovule numbers and proper ovule formation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142381491","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}
Noah Sprent, C Y Maurice Cheung, Sanu Shameer, R George Ratcliffe, J Lee Sweetlove, Nadine Töpfer
Guard cell metabolism is crucial for stomatal dynamics, but a full understanding of its role is hampered by experimental limitations and the flexible nature of the metabolic network. To tackle this challenge, we constructed a time-resolved stoichiometric model of guard cell metabolism that accounts for energy and osmolyte requirements and which is integrated with the mesophyll. The model resolved distinct roles for starch, sugars, and malate in guard cell metabolism and revealed several unexpected flux patterns in central metabolism. During blue light-mediated stomatal opening, starch breakdown was the most efficient way to generate osmolytes with downregulation of glycolysis allowing starch-derived glucose to accumulate as a cytosolic osmolyte. Maltose couldalso accumulate as a cytosolic osmoticum, although this made the metabolic system marginally less efficient. The metabolic energy for stomatal opening was predicted to be derived independently of starch, using nocturnally accumulated citrate which was metabolised in the tricarboxylic acid cycle to malate to provide mitochondrial reducing power for ATP synthesis. In white light-mediated stomatal opening, malate transferred reducing equivalents from guard cell photosynthesis to mitochondria for ATP production. Depending on the capacity for guard cell photosynthesis, glycolysis showed little flux during the day but was crucial for energy metabolism at night. In summary, our analyses have corroborated recent findings in Arabidopsis guard cell research, resolved conflicting observations by highlighting the flexibility of guard cell metabolism, and proposed new metabolic flux modes for further experimental testing.
保卫细胞的新陈代谢对气孔动力学至关重要,但实验的局限性和新陈代谢网络的灵活性阻碍了对其作用的全面了解。为了应对这一挑战,我们构建了一个时间分辨的护卫细胞新陈代谢化学计量模型,该模型考虑了能量和渗透溶质的需求,并与叶肉结合在一起。该模型解决了淀粉、糖类和苹果酸盐在保卫细胞代谢中的不同作用,并揭示了中央代谢中几种意想不到的通量模式。在蓝光介导的气孔开放过程中,淀粉分解是产生渗透溶质的最有效方式,糖酵解的下调使淀粉衍生的葡萄糖作为细胞膜渗透溶质积累。麦芽糖也可以作为细胞膜渗透质积累,尽管这使得代谢系统的效率略低。据预测,气孔打开所需的代谢能不依赖于淀粉,而是利用夜间积累的柠檬酸,在三羧酸循环中代谢成苹果酸,为线粒体合成 ATP 提供还原力。在白光介导的气孔打开过程中,苹果酸将还原当量从保卫细胞的光合作用转移到线粒体,以产生 ATP。根据保卫细胞光合作用的能力,糖酵解在白天的通量很小,但在夜间对能量代谢至关重要。总之,我们的分析证实了拟南芥保卫细胞研究的最新发现,通过强调保卫细胞代谢的灵活性解决了相互矛盾的观察结果,并提出了新的代谢通量模式供进一步实验测试。
{"title":"Metabolic modelling reveals distinct roles of sugars and carboxylic acids in stomatal opening and uncovers unexpected carbon fluxes.","authors":"Noah Sprent, C Y Maurice Cheung, Sanu Shameer, R George Ratcliffe, J Lee Sweetlove, Nadine Töpfer","doi":"10.1093/plcell/koae252","DOIUrl":"https://doi.org/10.1093/plcell/koae252","url":null,"abstract":"<p><p>Guard cell metabolism is crucial for stomatal dynamics, but a full understanding of its role is hampered by experimental limitations and the flexible nature of the metabolic network. To tackle this challenge, we constructed a time-resolved stoichiometric model of guard cell metabolism that accounts for energy and osmolyte requirements and which is integrated with the mesophyll. The model resolved distinct roles for starch, sugars, and malate in guard cell metabolism and revealed several unexpected flux patterns in central metabolism. During blue light-mediated stomatal opening, starch breakdown was the most efficient way to generate osmolytes with downregulation of glycolysis allowing starch-derived glucose to accumulate as a cytosolic osmolyte. Maltose couldalso accumulate as a cytosolic osmoticum, although this made the metabolic system marginally less efficient. The metabolic energy for stomatal opening was predicted to be derived independently of starch, using nocturnally accumulated citrate which was metabolised in the tricarboxylic acid cycle to malate to provide mitochondrial reducing power for ATP synthesis. In white light-mediated stomatal opening, malate transferred reducing equivalents from guard cell photosynthesis to mitochondria for ATP production. Depending on the capacity for guard cell photosynthesis, glycolysis showed little flux during the day but was crucial for energy metabolism at night. In summary, our analyses have corroborated recent findings in Arabidopsis guard cell research, resolved conflicting observations by highlighting the flexibility of guard cell metabolism, and proposed new metabolic flux modes for further experimental testing.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142381501","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 glycosyltransferases (UGTs) play a key role in plant growth and metabolism. Here, we examined the evolutionary landscape among UGTs in 28 fully sequenced species from early algae to angiosperms. Our findings revealed a distinctive expansion and contraction of UGTs in the G and H groups in tea (Camellia sinensis), respectively. Whole-genome duplication and tandem duplication events jointly drove the massive expansion of UGTs, and the interplay of natural and artificial selection has resulted in marked functional divergence within the G group of the sinensis-type tea population. In Cluster II of group G, differences in substrate selection (e.g., Abscisic Acid) of the enzymes encoded by UGT genes led to their functional diversification, and these genes influence tolerance to abiotic stresses such as low temperature and drought via different modes of positive and negative regulation, respectively. UGTs in Cluster III of the G group have diverse aroma substrate preferences, which contributes a diverse aroma spectrum of the sinensis-type tea population. All Cluster III genes respond to low-temperature stress, whereas UGTs within Cluster III-1, shaped by artificial selection, are unresponsive to drought. This suggests that artificial selection of tea plants focused on improving quality and cold tolerance as primary targets.
植物糖基转移酶(UGTs)在植物生长和新陈代谢中发挥着关键作用。在这里,我们研究了从早期藻类到被子植物的 28 个完全测序物种中 UGTs 的进化情况。我们的研究结果表明,茶叶(Camellia sinensis)中 G 组和 H 组的 UGTs 分别出现了明显的扩张和收缩。全基因组复制和串联复制事件共同推动了UGTs的大规模扩增,自然选择和人工选择的相互作用导致了中华茶树种群G群内部明显的功能分化。在G群的簇II中,UGT基因编码的酶在底物(如脱落酸)选择上的差异导致了其功能的多样化,这些基因分别通过不同的正负调控模式影响对低温和干旱等非生物胁迫的耐受性。G 组第 III 群组中的 UGTs 对香气底物的偏好各不相同,从而形成了多种多样的中茶香气谱。所有簇 III 基因都对低温胁迫有反应,而人工选择形成的簇 III-1 内的 UGTs 对干旱无反应。这表明,茶树的人工选择以提高品质和耐寒性为主要目标。
{"title":"Evolution and functional divergence of glycosyltransferase genes shaped the quality and cold tolerance of tea plants.","authors":"Jingming Wang, Yutong Hu, Danyang Guo, Ting Gao, Tianqi Liu, Jieyang Jin, Mingyue Zhao, Keke Yu, Wei Tong, Honghua Ge, Yuting Pan, Mengting Zhang, Mengqian Lu, Tingting Jing, Wenkai Du, Xiaoyan Tang, Chenjie Zhao, Wei Zhao, Zhijie Bao, Wilfried Schwab, Enhua Xia, Chuankui Song","doi":"10.1093/plcell/koae268","DOIUrl":"https://doi.org/10.1093/plcell/koae268","url":null,"abstract":"<p><p>Plant glycosyltransferases (UGTs) play a key role in plant growth and metabolism. Here, we examined the evolutionary landscape among UGTs in 28 fully sequenced species from early algae to angiosperms. Our findings revealed a distinctive expansion and contraction of UGTs in the G and H groups in tea (Camellia sinensis), respectively. Whole-genome duplication and tandem duplication events jointly drove the massive expansion of UGTs, and the interplay of natural and artificial selection has resulted in marked functional divergence within the G group of the sinensis-type tea population. In Cluster II of group G, differences in substrate selection (e.g., Abscisic Acid) of the enzymes encoded by UGT genes led to their functional diversification, and these genes influence tolerance to abiotic stresses such as low temperature and drought via different modes of positive and negative regulation, respectively. UGTs in Cluster III of the G group have diverse aroma substrate preferences, which contributes a diverse aroma spectrum of the sinensis-type tea population. All Cluster III genes respond to low-temperature stress, whereas UGTs within Cluster III-1, shaped by artificial selection, are unresponsive to drought. This suggests that artificial selection of tea plants focused on improving quality and cold tolerance as primary targets.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142375792","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}
Rui Lu, Shaoqiang Hu, Jia Feng, Zhongchi Liu, Chunying Kang
During flower development, different floral organs are formed to ensure fertilization and fruit set. Although the genetic networks underlying flower development are increasingly well understood, less is known about the mechanistic basis in different species. Here, we identified a mutant of woodland strawberry (Fragaria vesca), bare receptacle (bre), which produces flowers with greatly reduced carpels and other floral organs. Genetic analysis revealed that BRE encodes an APETALA2 (AP2) transcription factor. BRE was highly expressed in floral meristems and floral organ primordia. BRE could directly bind the GCC-box motif in the YUCCA (YUC) auxin biosynthesis genes FveYUC4 and FveYUC2 and promote their expression. The yuc4 mutant had fewer floral organs, and the bre yuc4 double mutant had similar numbers of petals and carpels to bre. Auxin homeostasis and distribution were severely disrupted in bre. Although auxin application or FveYUC4 overexpression did not rescue the bre phenotypes, bre was hypersensitive to treatment with the polar auxin transport inhibitor N-1-naphthylphthalamic acid (NPA). In addition, BRE was able to directly bind and regulate the expression of five other auxin pathway genes. Overall, these results demonstrate that BRE is required for floral organogenesis, particularly carpel initiation, and acts through the auxin pathway in strawberry.
{"title":"The AP2 transcription factor BARE RECEPTACLE regulates floral organogenesis via auxin pathways in woodland strawberry.","authors":"Rui Lu, Shaoqiang Hu, Jia Feng, Zhongchi Liu, Chunying Kang","doi":"10.1093/plcell/koae270","DOIUrl":"https://doi.org/10.1093/plcell/koae270","url":null,"abstract":"<p><p>During flower development, different floral organs are formed to ensure fertilization and fruit set. Although the genetic networks underlying flower development are increasingly well understood, less is known about the mechanistic basis in different species. Here, we identified a mutant of woodland strawberry (Fragaria vesca), bare receptacle (bre), which produces flowers with greatly reduced carpels and other floral organs. Genetic analysis revealed that BRE encodes an APETALA2 (AP2) transcription factor. BRE was highly expressed in floral meristems and floral organ primordia. BRE could directly bind the GCC-box motif in the YUCCA (YUC) auxin biosynthesis genes FveYUC4 and FveYUC2 and promote their expression. The yuc4 mutant had fewer floral organs, and the bre yuc4 double mutant had similar numbers of petals and carpels to bre. Auxin homeostasis and distribution were severely disrupted in bre. Although auxin application or FveYUC4 overexpression did not rescue the bre phenotypes, bre was hypersensitive to treatment with the polar auxin transport inhibitor N-1-naphthylphthalamic acid (NPA). In addition, BRE was able to directly bind and regulate the expression of five other auxin pathway genes. Overall, these results demonstrate that BRE is required for floral organogenesis, particularly carpel initiation, and acts through the auxin pathway in strawberry.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":""},"PeriodicalIF":10.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142375793","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}