Nancy A Eckardt, Yagut Allahverdiyeva, Clarisa E Alvarez, Claudia Büchel, Adrien Burlacot, Tanai Cardona, Emma Chaloner, Benjamin D Engel, Arthur R Grossman, Dvir Harris, Nicolas Herrmann, Michael Hodges, Jan Kern, Tom Dongmin Kim, Veronica G Maurino, Conrad W Mullineaux, Henna Mustila, Lauri Nikkanen, Gabriela Schlau-Cohen, Marcos A Tronconi, Wojciech Wietrzynski, Vittal K Yachandra, Junko Yano
Photosynthesis-the conversion of energy from sunlight into chemical energy-is essential for life on Earth. Yet there is much we do not understand about photosynthetic energy conversion on a fundamental level: how it evolved and the extent of its diversity, its dynamics, and all the components and connections involved in its regulation. In this commentary, researchers working on fundamental aspects of photosynthesis including the light-dependent reactions, photorespiration, and C4 photosynthetic metabolism pose and discuss what they view as the most compelling open questions in their areas of research.
{"title":"Lighting the way: Compelling open questions in photosynthesis research.","authors":"Nancy A Eckardt, Yagut Allahverdiyeva, Clarisa E Alvarez, Claudia Büchel, Adrien Burlacot, Tanai Cardona, Emma Chaloner, Benjamin D Engel, Arthur R Grossman, Dvir Harris, Nicolas Herrmann, Michael Hodges, Jan Kern, Tom Dongmin Kim, Veronica G Maurino, Conrad W Mullineaux, Henna Mustila, Lauri Nikkanen, Gabriela Schlau-Cohen, Marcos A Tronconi, Wojciech Wietrzynski, Vittal K Yachandra, Junko Yano","doi":"10.1093/plcell/koae203","DOIUrl":"10.1093/plcell/koae203","url":null,"abstract":"<p><p>Photosynthesis-the conversion of energy from sunlight into chemical energy-is essential for life on Earth. Yet there is much we do not understand about photosynthetic energy conversion on a fundamental level: how it evolved and the extent of its diversity, its dynamics, and all the components and connections involved in its regulation. In this commentary, researchers working on fundamental aspects of photosynthesis including the light-dependent reactions, photorespiration, and C4 photosynthetic metabolism pose and discuss what they view as the most compelling open questions in their areas of research.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3914-3943"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449116/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748880","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}
Identifying the essential factors and underlying mechanisms regulating plant heat stress (HS) responses is crucial for mitigating the threat posed by HS on plant growth, development, distribution, and productivity. In this study, we found that the Arabidopsis (Arabidopsis thaliana) super-killer2 (ski2) dicer-like4 (dcl4) mutant, characterized by RNA processing defects and the accumulation of abundant 22-nt small interfering RNAs derived from protein-coding transcripts, displayed significantly increased expression levels of HS-responsive genes and enhanced thermotolerance. These traits primarily resulted from the suppression of SMAX1-LIKE4 (SMXL4) and SMXL5, which encode 2 putative transcriptional regulators that belong to the SMXL protein family. While smxl4 and smxl5 single mutants were similar to wild type, the smxl4 smxl5 double mutant displayed substantially heightened seedling thermotolerance. Further investigation demonstrated that SMXL4 and SMXL5 repressed the transcription of HEAT-SHOCK TRANSCRIPTION FACTOR A2 (HSFA2), encoding a master regulator of thermotolerance, independently of ethylene-response factor-associated amphiphilic repression motifs. Moreover, SMXL4 and SMXL5 interacted with HSFA1d and HSFA1e, central regulators sensing and transducing HS stimuli, and antagonistically affected their transactivation activity. In addition, HSFA2 directly bound to the SMXL4 and SMXL5 promoters, inducing their expression during recovery from HS. Collectively, our findings elucidate the role of the SMXL4/SMXL5-HSFA2 regulatory module in orchestrating plant thermotolerance under HS.
{"title":"Suppression of SMXL4 and SMXL5 confers enhanced thermotolerance through promoting HSFA2 transcription in Arabidopsis.","authors":"Yajie Pan, Bofan Yu, Xin Wei, Yuping Qiu, Xin Mao, Yuelin Liu, Wei Yan, Qianyan Linghu, Wenyang Li, Hongwei Guo, Zhonghua Tang","doi":"10.1093/plcell/koae224","DOIUrl":"10.1093/plcell/koae224","url":null,"abstract":"<p><p>Identifying the essential factors and underlying mechanisms regulating plant heat stress (HS) responses is crucial for mitigating the threat posed by HS on plant growth, development, distribution, and productivity. In this study, we found that the Arabidopsis (Arabidopsis thaliana) super-killer2 (ski2) dicer-like4 (dcl4) mutant, characterized by RNA processing defects and the accumulation of abundant 22-nt small interfering RNAs derived from protein-coding transcripts, displayed significantly increased expression levels of HS-responsive genes and enhanced thermotolerance. These traits primarily resulted from the suppression of SMAX1-LIKE4 (SMXL4) and SMXL5, which encode 2 putative transcriptional regulators that belong to the SMXL protein family. While smxl4 and smxl5 single mutants were similar to wild type, the smxl4 smxl5 double mutant displayed substantially heightened seedling thermotolerance. Further investigation demonstrated that SMXL4 and SMXL5 repressed the transcription of HEAT-SHOCK TRANSCRIPTION FACTOR A2 (HSFA2), encoding a master regulator of thermotolerance, independently of ethylene-response factor-associated amphiphilic repression motifs. Moreover, SMXL4 and SMXL5 interacted with HSFA1d and HSFA1e, central regulators sensing and transducing HS stimuli, and antagonistically affected their transactivation activity. In addition, HSFA2 directly bound to the SMXL4 and SMXL5 promoters, inducing their expression during recovery from HS. Collectively, our findings elucidate the role of the SMXL4/SMXL5-HSFA2 regulatory module in orchestrating plant thermotolerance under HS.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4557-4575"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449109/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141894017","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}
Yanzhi Yang, Lei Xu, Chen Hao, Miaomiao Wan, Yihan Tao, Yan Zhuang, Yanning Su, Lei Li
The conserved microRNA (miRNA) miR408 enhances photosynthesis and compromises stress tolerance in multiple plants, but the cellular mechanism underlying its function remains largely unclear. Here, we show that in Arabidopsis (Arabidopsis thaliana), the transcript encoding the blue copper protein PLANTACYANIN (PCY) is the primary target for miR408 in vegetative tissues. PCY is preferentially expressed in the guard cells, and PCY is associated with the endomembrane surrounding individual chloroplasts. We found that the MIR408 promoter is suppressed by multiple abscisic acid (ABA)-responsive transcription factors, thus allowing PCY to accumulate under stress conditions. Genetic analysis revealed that PCY elevates reactive oxygen species (ROS) levels in the guard cells, promotes stomatal closure, reduces photosynthetic gas exchange, and enhances drought resistance. Moreover, the miR408-PCY module is sufficient to rescue the growth and drought tolerance phenotypes caused by gain- and loss-of-function of MYB44, an established positive regulator of ABA responses, indicating that the miR408-PCY module relays ABA signaling for regulating ROS homeostasis and drought resistance. These results demonstrate that miR408 regulates stomatal movement to balance growth and drought resistance, providing a mechanistic understanding of why miR408 is selected during land plant evolution and insights into the long-pursued quest of breeding drought-tolerant and high-yielding crops.
{"title":"The microRNA408-plantacyanin module balances plant growth and drought resistance by regulating reactive oxygen species homeostasis in guard cells.","authors":"Yanzhi Yang, Lei Xu, Chen Hao, Miaomiao Wan, Yihan Tao, Yan Zhuang, Yanning Su, Lei Li","doi":"10.1093/plcell/koae144","DOIUrl":"10.1093/plcell/koae144","url":null,"abstract":"<p><p>The conserved microRNA (miRNA) miR408 enhances photosynthesis and compromises stress tolerance in multiple plants, but the cellular mechanism underlying its function remains largely unclear. Here, we show that in Arabidopsis (Arabidopsis thaliana), the transcript encoding the blue copper protein PLANTACYANIN (PCY) is the primary target for miR408 in vegetative tissues. PCY is preferentially expressed in the guard cells, and PCY is associated with the endomembrane surrounding individual chloroplasts. We found that the MIR408 promoter is suppressed by multiple abscisic acid (ABA)-responsive transcription factors, thus allowing PCY to accumulate under stress conditions. Genetic analysis revealed that PCY elevates reactive oxygen species (ROS) levels in the guard cells, promotes stomatal closure, reduces photosynthetic gas exchange, and enhances drought resistance. Moreover, the miR408-PCY module is sufficient to rescue the growth and drought tolerance phenotypes caused by gain- and loss-of-function of MYB44, an established positive regulator of ABA responses, indicating that the miR408-PCY module relays ABA signaling for regulating ROS homeostasis and drought resistance. These results demonstrate that miR408 regulates stomatal movement to balance growth and drought resistance, providing a mechanistic understanding of why miR408 is selected during land plant evolution and insights into the long-pursued quest of breeding drought-tolerant and high-yielding crops.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4338-4355"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448907/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140897775","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}
Plants can perceive a slight upsurge in ambient temperature and respond by undergoing morphological changes, such as elongated hypocotyls and early flowering. The dynamic functioning of PHYTOCHROME INTERACTING FACTOR4 (PIF4) in thermomorphogenesis is well established, although the complete regulatory pathway involved in thermosensing remains elusive. We establish that an increase in temperature from 22 to 28 °C induces upregulation and activation of MITOGEN-ACTIVATED PROTEIN KINASE 4 (MPK4) in Arabidopsis (Arabidopsis thaliana), subsequently leading to the phosphorylation of PIF4. Phosphorylated PIF4 represses the expression of ACTIN-RELATED PROTEIN 6 (ARP6), which is required for mediating the deposition of histone variant H2A.Z at its target loci. Furthermore, we demonstrate that variations in ARP6 expression in PIF4 phosphor-null and phosphor-mimetic seedlings affect hypocotyl growth at 22 and 28 °C by modulating the regulation of ARP6-mediated H2A.Z deposition at the loci of genes involved in elongating hypocotyl cells. Interestingly, the expression of MPK4 is also controlled by H2A.Z deposition in a temperature-dependent manner. Taken together, these findings highlight the regulatory mechanism of thermosensing by which MPK4-mediated phosphorylation of PIF4 affects ARP6-mediated H2A.Z deposition at the genes involved in hypocotyl cell elongation.
{"title":"MPK4-mediated phosphorylation of PHYTOCHROME INTERACTING FACTOR4 controls thermosensing by regulating histone variant H2A.Z deposition.","authors":"Neetu Verma, Dhanraj Singh, Lavanya Mittal, Gopal Banerjee, Stanzin Noryang, Alok Krishna Sinha","doi":"10.1093/plcell/koae223","DOIUrl":"10.1093/plcell/koae223","url":null,"abstract":"<p><p>Plants can perceive a slight upsurge in ambient temperature and respond by undergoing morphological changes, such as elongated hypocotyls and early flowering. The dynamic functioning of PHYTOCHROME INTERACTING FACTOR4 (PIF4) in thermomorphogenesis is well established, although the complete regulatory pathway involved in thermosensing remains elusive. We establish that an increase in temperature from 22 to 28 °C induces upregulation and activation of MITOGEN-ACTIVATED PROTEIN KINASE 4 (MPK4) in Arabidopsis (Arabidopsis thaliana), subsequently leading to the phosphorylation of PIF4. Phosphorylated PIF4 represses the expression of ACTIN-RELATED PROTEIN 6 (ARP6), which is required for mediating the deposition of histone variant H2A.Z at its target loci. Furthermore, we demonstrate that variations in ARP6 expression in PIF4 phosphor-null and phosphor-mimetic seedlings affect hypocotyl growth at 22 and 28 °C by modulating the regulation of ARP6-mediated H2A.Z deposition at the loci of genes involved in elongating hypocotyl cells. Interestingly, the expression of MPK4 is also controlled by H2A.Z deposition in a temperature-dependent manner. Taken together, these findings highlight the regulatory mechanism of thermosensing by which MPK4-mediated phosphorylation of PIF4 affects ARP6-mediated H2A.Z deposition at the genes involved in hypocotyl cell elongation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4535-4556"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449107/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141894016","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}
Symbiotic nitrogen fixation within nitrogen-fixing clade (NFC) plants is thought to have arisen from a single gain followed by massive losses in the genomes of ancestral non-nodulating plants. However, molecular evidence supporting this model is limited. Here, we confirm through bioinformatic analysis that NODULES WITH ACTIVATED DEFENSE1 (NAD1) is present only in NFC plants and is thus an NFC-specific gene. Moreover, NAD1 was specifically expressed in nodules. We identified three conserved nodulation-associated cis-regulatory elements (NACE1-3) in the promoter of LjNAD1 from Lotus japonicus that are required for its nodule specific expression. A survey of NFC plants revealed that NACE1 and NACE2 are specific to the Fabales and Papilionoideae, respectively, while NACE3 is present in all NFC plants. Moreover, we found that nodule inception (NIN) directly binds to all three NACEs to activate NAD1 expression. Mutation of L. japonicus LjNAD1 resulted in the formation of abnormal symbiosomes with enlarged symbiosome space and frequent breakdown of bacteroids in nodules, resembling phenotypes reported for Medicago truncatula Mtnad1 and Mtnin mutants. These data point to NIN-NAD1 as an important module regulating rhizobial accommodation in nodules. The regulation of NAD1 by NIN in the NFC ancestor represent an important evolutionary adaptation for nodulation.
{"title":"Conserved cis-elements enable NODULES WITH ACTIVATED DEFENSE1 regulation by NODULE INCEPTION during nodulation.","authors":"Haixiang Yu, Aifang Xiao, Zhongmin Zou, Qiujin Wu, Lin Chen, Dandan Zhang, Yuzhang Sun, Chao Wang, Jianbo Cao, Hui Zhu, Zhongming Zhang, Yangrong Cao","doi":"10.1093/plcell/koae229","DOIUrl":"10.1093/plcell/koae229","url":null,"abstract":"<p><p>Symbiotic nitrogen fixation within nitrogen-fixing clade (NFC) plants is thought to have arisen from a single gain followed by massive losses in the genomes of ancestral non-nodulating plants. However, molecular evidence supporting this model is limited. Here, we confirm through bioinformatic analysis that NODULES WITH ACTIVATED DEFENSE1 (NAD1) is present only in NFC plants and is thus an NFC-specific gene. Moreover, NAD1 was specifically expressed in nodules. We identified three conserved nodulation-associated cis-regulatory elements (NACE1-3) in the promoter of LjNAD1 from Lotus japonicus that are required for its nodule specific expression. A survey of NFC plants revealed that NACE1 and NACE2 are specific to the Fabales and Papilionoideae, respectively, while NACE3 is present in all NFC plants. Moreover, we found that nodule inception (NIN) directly binds to all three NACEs to activate NAD1 expression. Mutation of L. japonicus LjNAD1 resulted in the formation of abnormal symbiosomes with enlarged symbiosome space and frequent breakdown of bacteroids in nodules, resembling phenotypes reported for Medicago truncatula Mtnad1 and Mtnin mutants. These data point to NIN-NAD1 as an important module regulating rhizobial accommodation in nodules. The regulation of NAD1 by NIN in the NFC ancestor represent an important evolutionary adaptation for nodulation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4622-4636"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448908/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141971633","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}
Weiyuan Song, Yang Xie, Bin Liu, Yuxiang Huang, Zhihua Cheng, Zilong Zhao, Di Tian, Yan Geng, Jingyu Guo, Chuang Li, Daixi She, Yanting Zhong, Min Li, Liu Liu, Jiacai Chen, Chengzhen Sun, Xuejun Zhang, Zhaoyang Zhou, Jinsheng Lai, Ming Xin, Liying Yan, Jianyu Zhao, Xiaolan Zhang
Complete disruption of critical genes is generally accompanied by severe growth and developmental defects, which dramatically hinder its utilization in crop breeding. Identifying subtle changes, such as single-nucleotide polymorphisms (SNPs), in critical genes that specifically modulate a favorable trait is a prerequisite to fulfill breeding potential. Here, we found 2 SNPs in the E-class floral organ identity gene cucumber (Cucumis sativus) SEPALLATA2 (CsSEP2) that specifically regulate fruit length. Haplotype (HAP) 1 (8G2667A) and HAP2 (8G2667T) exist in natural populations, whereas HAP3 (8A2667T) is induced by ethyl methanesulfonate mutagenesis. Phenotypic characterization of 4 near-isogenic lines and a mutant line showed that HAP2 fruits are significantly longer than those of HAP1, and those of HAP3 are 37.8% longer than HAP2 fruit. The increasing fruit length in HAP1-3 was caused by a decreasing inhibitory effect on CRABS CLAW (CsCRC) transcription (a reported positive regulator of fruit length), resulting in enhanced cell expansion. Moreover, a 7638G/A-SNP in melon (Cucumis melo) CmSEP2 modulates fruit length in a natural melon population via the conserved SEP2-CRC module. Our findings provide a strategy for utilizing essential regulators with pleiotropic effects during crop breeding.
{"title":"Single nucleotide polymorphisms in SEPALLATA 2 underlie fruit length variation in cucurbits.","authors":"Weiyuan Song, Yang Xie, Bin Liu, Yuxiang Huang, Zhihua Cheng, Zilong Zhao, Di Tian, Yan Geng, Jingyu Guo, Chuang Li, Daixi She, Yanting Zhong, Min Li, Liu Liu, Jiacai Chen, Chengzhen Sun, Xuejun Zhang, Zhaoyang Zhou, Jinsheng Lai, Ming Xin, Liying Yan, Jianyu Zhao, Xiaolan Zhang","doi":"10.1093/plcell/koae228","DOIUrl":"10.1093/plcell/koae228","url":null,"abstract":"<p><p>Complete disruption of critical genes is generally accompanied by severe growth and developmental defects, which dramatically hinder its utilization in crop breeding. Identifying subtle changes, such as single-nucleotide polymorphisms (SNPs), in critical genes that specifically modulate a favorable trait is a prerequisite to fulfill breeding potential. Here, we found 2 SNPs in the E-class floral organ identity gene cucumber (Cucumis sativus) SEPALLATA2 (CsSEP2) that specifically regulate fruit length. Haplotype (HAP) 1 (8G2667A) and HAP2 (8G2667T) exist in natural populations, whereas HAP3 (8A2667T) is induced by ethyl methanesulfonate mutagenesis. Phenotypic characterization of 4 near-isogenic lines and a mutant line showed that HAP2 fruits are significantly longer than those of HAP1, and those of HAP3 are 37.8% longer than HAP2 fruit. The increasing fruit length in HAP1-3 was caused by a decreasing inhibitory effect on CRABS CLAW (CsCRC) transcription (a reported positive regulator of fruit length), resulting in enhanced cell expansion. Moreover, a 7638G/A-SNP in melon (Cucumis melo) CmSEP2 modulates fruit length in a natural melon population via the conserved SEP2-CRC module. Our findings provide a strategy for utilizing essential regulators with pleiotropic effects during crop breeding.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4607-4621"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448892/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141971634","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":"Decoding the role of flavonoids in ROS management during heat stress in tomato pollen.","authors":"Nitin Uttam Kamble","doi":"10.1093/plcell/koae234","DOIUrl":"10.1093/plcell/koae234","url":null,"abstract":"","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4285-4286"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449077/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142005008","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}
Colleen Drapek, Annalisa Rizza, Nadiatul A Mohd-Radzman, Katharina Schiessl, Fabio Dos Santos Barbosa, Jiangqi Wen, Giles E D Oldroyd, Alexander M Jones
During nutrient scarcity, plants can adapt their developmental strategy to maximize their chance of survival. Such plasticity in development is underpinned by hormonal regulation, which mediates the relationship between environmental cues and developmental outputs. In legumes, endosymbiosis with nitrogen-fixing bacteria (rhizobia) is a key adaptation for supplying the plant with nitrogen in the form of ammonium. Rhizobia are housed in lateral root-derived organs termed nodules that maintain an environment conducive to Nitrogenase in these bacteria. Several phytohormones are important for regulating the formation of nodules, with both positive and negative roles proposed for gibberellin (GA). In this study, we determine the cellular location and function of bioactive GA during nodule organogenesis using a genetically encoded second-generation GA biosensor, GIBBERELLIN PERCEPTION SENSOR 2 in Medicago truncatula. We find endogenous bioactive GA accumulates locally at the site of nodule primordia, increasing dramatically in the cortical cell layers, persisting through cell divisions, and maintaining accumulation in the mature nodule meristem. We show, through misexpression of GA-catabolic enzymes that suppress GA accumulation, that GA acts as a positive regulator of nodule growth and development. Furthermore, increasing or decreasing GA through perturbation of biosynthesis gene expression can increase or decrease the size of nodules, respectively. This is unique from lateral root formation, a developmental program that shares common organogenesis regulators. We link GA to a wider gene regulatory program by showing that nodule-identity genes induce and sustain GA accumulation necessary for proper nodule formation.
在养分匮乏的情况下,植物可以调整其发育策略,以最大限度地提高生存机会。这种发育可塑性的基础是激素调节,它介导了环境线索与发育产出之间的关系。在豆科植物中,与固氮菌(根瘤菌)的内共生是为植物提供铵态氮的主要适应方式。根瘤菌寄生在侧根衍生的器官中,这些器官被称为 "结节",可维持有利于这些细菌的氮酶的环境。有几种植物激素对调节结核的形成很重要,其中赤霉素(GA)被认为具有积极和消极的作用。在本研究中,我们利用遗传编码的第二代 GA 生物传感器--赤霉素感知传感器 2(GIBBERELLIN PERCEPTION SENSOR 2),确定了在美智子(Medicago truncatula)的结核器官形成过程中生物活性 GA 的细胞位置和功能。我们发现内源生物活性 GA 在结节原基部位局部积累,在皮层细胞层中急剧增加,在细胞分裂过程中持续存在,并在成熟的结节分生组织中保持积累。我们通过抑制 GA 积累的 GA 分解酶的错误表达表明,GA 对结核的生长和发育起着积极的调节作用。此外,通过扰乱生物合成基因的表达来增加或减少 GA,可分别增加或减少结核的大小。这与侧根的形成不同,侧根的形成是一种发育程序,而侧根的形成具有共同的器官发生调控因子。我们将 GA 与更广泛的基因调控程序联系起来,证明了结核特征基因诱导并维持适当的结核形成所需的 GA 积累。
{"title":"Gibberellin dynamics governing nodulation revealed using GIBBERELLIN PERCEPTION SENSOR 2 in Medicago truncatula lateral organs.","authors":"Colleen Drapek, Annalisa Rizza, Nadiatul A Mohd-Radzman, Katharina Schiessl, Fabio Dos Santos Barbosa, Jiangqi Wen, Giles E D Oldroyd, Alexander M Jones","doi":"10.1093/plcell/koae201","DOIUrl":"10.1093/plcell/koae201","url":null,"abstract":"<p><p>During nutrient scarcity, plants can adapt their developmental strategy to maximize their chance of survival. Such plasticity in development is underpinned by hormonal regulation, which mediates the relationship between environmental cues and developmental outputs. In legumes, endosymbiosis with nitrogen-fixing bacteria (rhizobia) is a key adaptation for supplying the plant with nitrogen in the form of ammonium. Rhizobia are housed in lateral root-derived organs termed nodules that maintain an environment conducive to Nitrogenase in these bacteria. Several phytohormones are important for regulating the formation of nodules, with both positive and negative roles proposed for gibberellin (GA). In this study, we determine the cellular location and function of bioactive GA during nodule organogenesis using a genetically encoded second-generation GA biosensor, GIBBERELLIN PERCEPTION SENSOR 2 in Medicago truncatula. We find endogenous bioactive GA accumulates locally at the site of nodule primordia, increasing dramatically in the cortical cell layers, persisting through cell divisions, and maintaining accumulation in the mature nodule meristem. We show, through misexpression of GA-catabolic enzymes that suppress GA accumulation, that GA acts as a positive regulator of nodule growth and development. Furthermore, increasing or decreasing GA through perturbation of biosynthesis gene expression can increase or decrease the size of nodules, respectively. This is unique from lateral root formation, a developmental program that shares common organogenesis regulators. We link GA to a wider gene regulatory program by showing that nodule-identity genes induce and sustain GA accumulation necessary for proper nodule formation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4442-4456"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449112/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141627407","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}
The growth of plants, algae, and cyanobacteria relies on the catalytic activity of the oxygen-evolving PSII complex, which uses solar energy to extract electrons from water to feed into the photosynthetic electron transport chain. PSII is proving to be an excellent system to study how large multi-subunit membrane-protein complexes are assembled in the thylakoid membrane and subsequently repaired in response to photooxidative damage. Here we summarize recent developments in understanding the biogenesis of PSII, with an emphasis on recent insights obtained from biochemical and structural analysis of cyanobacterial PSII assembly/repair intermediates. We also discuss how chlorophyll synthesis is synchronized with protein synthesis and suggest a possible role for PSI in PSII assembly. Special attention is paid to unresolved and controversial issues that could be addressed in future research.
植物、藻类和蓝藻的生长依赖于氧发生光系统二(PSII)复合物的催化活性,该复合物利用太阳能从水中提取电子,然后输入光合作用电子传递链。事实证明,PSII 是研究大型多亚基膜蛋白复合物如何在类木质膜中组装并在光氧化损伤后进行修复的绝佳系统。在此,我们总结了了解 PSII 生物发生过程的最新进展,重点是蓝藻 PSII 组装/修复中间体的生化和结构分析所获得的最新见解。我们还讨论了叶绿素合成如何与蛋白质合成同步,并提出了光系统 I 在 PSII 组装中可能扮演的角色。我们还特别关注了一些尚未解决和有争议的问题,这些问题可在今后的研究中加以解决。
{"title":"The biogenesis and maintenance of PSII: Recent advances and current challenges.","authors":"Josef Komenda, Roman Sobotka, Peter J Nixon","doi":"10.1093/plcell/koae082","DOIUrl":"10.1093/plcell/koae082","url":null,"abstract":"<p><p>The growth of plants, algae, and cyanobacteria relies on the catalytic activity of the oxygen-evolving PSII complex, which uses solar energy to extract electrons from water to feed into the photosynthetic electron transport chain. PSII is proving to be an excellent system to study how large multi-subunit membrane-protein complexes are assembled in the thylakoid membrane and subsequently repaired in response to photooxidative damage. Here we summarize recent developments in understanding the biogenesis of PSII, with an emphasis on recent insights obtained from biochemical and structural analysis of cyanobacterial PSII assembly/repair intermediates. We also discuss how chlorophyll synthesis is synchronized with protein synthesis and suggest a possible role for PSI in PSII assembly. Special attention is paid to unresolved and controversial issues that could be addressed in future research.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"3997-4013"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449106/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140132352","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}