Alexis Riché, Louis Dumas, Soazig Malesinski, Guillaume Bossan, Céline Madigou, Francesca Zito, Jean Alric
In oxygenic photosynthesis, state transitions distribute light energy between PSI and PSII. This regulation involves reduction of the plastoquinone pool, activation of the state transitions 7 (STT7) protein kinase by the cytochrome (cyt) b6f complex, and phosphorylation and migration of light harvesting complexes II (LHCII). In this study, we show that in Chlamydomonas reinhardtii, the C-terminus of the cyt b6 subunit PetB acts on phosphorylation of STT7 and state transitions. We used site-directed mutagenesis of the chloroplast petB gene to truncate (remove L215b6) or elongate (add G216b6) the cyt b6 subunit. Modified complexes are devoid of heme ci and degraded by FTSH protease, revealing that salt bridge formation between cyt b6 (PetB) and Subunit IV (PetD) is essential to the assembly of the complex. In double mutants where FTSH is inactivated, modified cyt b6f accumulated but the phosphorylation cascade was blocked. We also replaced the arginine interacting with heme ci propionate (R207Kb6). In this modified complex, heme ci is present but the kinetics of phosphorylation are slower. We show that highly phosphorylated forms of STT7 accumulated transiently after reduction of the PQ pool and represent the active forms of the protein kinase. The phosphorylation of the LHCII targets is favored at the expense of the protein kinase, and the migration of LHCII toward PSI is the limiting step for state transitions.
在含氧光合作用中,状态转换在光系统 I 和光系统 II 之间分配光能。这种调节涉及质醌池的减少、细胞色素 b6f 复合物对状态转换 7(STT7)蛋白激酶的激活以及光收集复合物 II(LHCII)的磷酸化和迁移。在这里,我们发现在莱茵衣藻中,细胞色素 b6 亚基 PetB 的 C 端作用于 STT7 的磷酸化和状态转换。我们利用叶绿体 petB 基因的定点突变来截短(去除 L215b6)或延长(添加 G216b6)细胞 b6 亚基。改造后的复合物不含血红素 ci,并被 FTSH 蛋白酶降解,这表明细胞 b6(PetB)和亚基 IV(PetD)之间形成的盐桥是复合物组装的关键。在 FTSH 失活的双突变体中,修饰的细胞 b6f 积累,但磷酸化级联被阻断。我们还替换了与血红素 ci 丙酸盐(R207Kb6)相互作用的精氨酸。在这种经过修饰的复合物中,血红素 ci 存在,但磷酸化的动力学过程较慢。我们的研究表明,高磷酸化形式的 STT7 在 PQ 池减少后瞬时积累,代表了蛋白激酶的活性形式。LHCII 目标的磷酸化以牺牲蛋白激酶为代价,LHCII 向 PSI 的迁移是状态转换的限制步骤。
{"title":"The stromal side of the cytochrome b6f complex regulates state transitions.","authors":"Alexis Riché, Louis Dumas, Soazig Malesinski, Guillaume Bossan, Céline Madigou, Francesca Zito, Jean Alric","doi":"10.1093/plcell/koae190","DOIUrl":"10.1093/plcell/koae190","url":null,"abstract":"<p><p>In oxygenic photosynthesis, state transitions distribute light energy between PSI and PSII. This regulation involves reduction of the plastoquinone pool, activation of the state transitions 7 (STT7) protein kinase by the cytochrome (cyt) b6f complex, and phosphorylation and migration of light harvesting complexes II (LHCII). In this study, we show that in Chlamydomonas reinhardtii, the C-terminus of the cyt b6 subunit PetB acts on phosphorylation of STT7 and state transitions. We used site-directed mutagenesis of the chloroplast petB gene to truncate (remove L215b6) or elongate (add G216b6) the cyt b6 subunit. Modified complexes are devoid of heme ci and degraded by FTSH protease, revealing that salt bridge formation between cyt b6 (PetB) and Subunit IV (PetD) is essential to the assembly of the complex. In double mutants where FTSH is inactivated, modified cyt b6f accumulated but the phosphorylation cascade was blocked. We also replaced the arginine interacting with heme ci propionate (R207Kb6). In this modified complex, heme ci is present but the kinetics of phosphorylation are slower. We show that highly phosphorylated forms of STT7 accumulated transiently after reduction of the PQ pool and represent the active forms of the protein kinase. The phosphorylation of the LHCII targets is favored at the expense of the protein kinase, and the migration of LHCII toward PSI is the limiting step for state transitions.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4234-4244"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448884/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141535075","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}
Meiotic recombination is a key biological process in plant evolution and breeding, as it generates genetic diversity in each generation through the formation of crossovers (COs). However, due to their importance in genome stability, COs are highly regulated in frequency and distribution. We previously demonstrated that this strict regulation of COs can be modified, both in terms of CO frequency and distribution, in allotriploid Brassica hybrids (2n = 3x = 29; AAC) resulting from a cross between Brassica napus (2n = 4x = 38; AACC) and Brassica rapa (2n = 2x = 20; AA). Using the recently updated B. napus genome now including pericentromeres, we demonstrated that COs occur in these cold regions in allotriploids, as close as 375 kb from the centromere. Reverse transcription quantitative PCR (RT-qPCR) of various meiotic genes indicated that Class I COs are likely involved in the increased recombination frequency observed in allotriploids. We also demonstrated that this modified recombination landscape can be maintained via successive generations of allotriploidy (odd ploidy level). This deregulated meiotic behavior reverts to strict regulation in allotetraploid (even ploidy level) progeny in the second generation. Overall, we provide an easy way to manipulate tight recombination control in a polyploid crop.
减数分裂重组是植物进化和育种中的一个关键生物过程,因为它通过形成交叉(COs)在每一代中产生遗传多样性。然而,由于 COs 在基因组稳定性中的重要性,它们的频率和分布受到了严格的调控。我们之前证明,在由甘蓝(2n = 4x = 38; AACC)和芸苔(2n = 2x = 20; AA)杂交产生的异源三倍体芸苔杂交种(2n = 3x = 29; AAC)中,COs 的这种严格调控可以在 CO 频率和分布方面得到改变。我们利用最近更新的油菜基因组(现在包括中心粒)证明,在异源三倍体的这些冷区,离中心粒最接近的地方有 375 kb 的 CO。各种减数分裂基因的反转录定量 PCR(RT-qPCR)表明,异源三倍体中观察到的重组频率增加可能与 I 类 COs 有关。我们还证明,通过连续几代的异源三倍体(奇数倍性水平),可以维持这种改变了的重组景观。这种失调的减数分裂行为在第二代异源四倍体(偶倍性水平)后代中恢复到严格的调节状态。总之,我们提供了一种在多倍体作物中进行严格重组控制的简便方法。
{"title":"Alternating between even and odd ploidy levels switches on and off the recombination control, even near the centromeres.","authors":"Franz Boideau, Virginie Huteau, Loeiz Maillet, Anael Brunet, Olivier Coriton, Gwenaëlle Deniot, Gwenn Trotoux, Maryse Taburel-Lodé, Frédérique Eber, Marie Gilet, Cécile Baron, Julien Boutte, Gautier Richard, Jean-Marc Aury, Caroline Belser, Karine Labadie, Jérôme Morice, Cyril Falentin, Olivier Martin, Matthieu Falque, Anne-Marie Chèvre, Mathieu Rousseau-Gueutin","doi":"10.1093/plcell/koae208","DOIUrl":"10.1093/plcell/koae208","url":null,"abstract":"<p><p>Meiotic recombination is a key biological process in plant evolution and breeding, as it generates genetic diversity in each generation through the formation of crossovers (COs). However, due to their importance in genome stability, COs are highly regulated in frequency and distribution. We previously demonstrated that this strict regulation of COs can be modified, both in terms of CO frequency and distribution, in allotriploid Brassica hybrids (2n = 3x = 29; AAC) resulting from a cross between Brassica napus (2n = 4x = 38; AACC) and Brassica rapa (2n = 2x = 20; AA). Using the recently updated B. napus genome now including pericentromeres, we demonstrated that COs occur in these cold regions in allotriploids, as close as 375 kb from the centromere. Reverse transcription quantitative PCR (RT-qPCR) of various meiotic genes indicated that Class I COs are likely involved in the increased recombination frequency observed in allotriploids. We also demonstrated that this modified recombination landscape can be maintained via successive generations of allotriploidy (odd ploidy level). This deregulated meiotic behavior reverts to strict regulation in allotetraploid (even ploidy level) progeny in the second generation. Overall, we provide an easy way to manipulate tight recombination control in a polyploid crop.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4472-4490"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449113/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141910031","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}
Xuening Liu, Mingzheng Han, Tianhua Jiang, Lei Liu, Jiayi Luo, Ying Lu, Yafei Zhao, Cai-Zhong Jiang, Junping Gao, Bo Hong, Chao Ma
During the floral transition, many plant species including chrysanthemum (Chrysanthemum morifolium) require continuous photoperiodic stimulation for successful anthesis. Insufficient photoperiodic stimulation results in flower bud arrest or even failure. The molecular mechanisms underlying how continuous photoperiodic stimulation promotes anthesis are not well understood. Here, we reveal that in wild chrysanthemum (Chrysanthemum indicum), an obligate short-day (SD) plant, floral evocation is not limited to SD conditions. However, SD signals generated locally in the inflorescence meristem (IM) play a vital role in ensuring anthesis after floral commitment. Genetic analyses indicate that the florigen FLOWERING LOCUS T-LIKE3 (CiFTL3) plays an important role in floral evocation, but a lesser role in anthesis. Importantly, our data demonstrate that AGAMOUS-LIKE 24 (CiAGL24) is a critical component of SD signal perception in the IM to promote successful anthesis, and that floral evocation and anthesis are two separate developmental events in chrysanthemum. We further reveal that the central circadian clock component PSEUDO-RESPONSE REGULATOR 7 (CiPRR7) in the IM activates CiAGL24 expression in response to SD conditions. Moreover, our findings elucidate a negative feedback loop in which CiAGL24 and SUPPRESSOR OF OVEREXPRESSION OF CO 1 (CiSOC1) modulate LEAFY (CiLFY) expression. Together, our results demonstrate that the CiPRR7-CiAGL24 module is vital for sustained SD signal perception in the IM to ensure successful anthesis in chrysanthemum.
在花期过渡期间,包括菊花(Chrysanthemum morifolium)在内的许多植物物种都需要持续的光周期刺激才能成功开花。光周期刺激不足会导致花芽停止甚至失败。连续光周期刺激如何促进开花的分子机制尚不十分清楚。在这里,我们揭示了在野菊花(C. indicum)这种必须生长在短日照(SD)条件下的植物中,花的萌发并不局限于 SD 条件。然而,花序分生组织(IM)局部产生的短日照信号在确保花期承诺后的开花方面起着至关重要的作用。遗传分析表明,花原基 FLOWERING LOCUS T-LIKE3 (CiFTL3)在花唤醒中起着重要作用,但在开花中作用较小。重要的是,我们的数据证明 AGAMOUS-LIKE 24(CiAGL24)是 IM 中 SD 信号感知的关键组成部分,可促进成功开花,而且菊花的花唤醒和开花是两个独立的发育事件。我们还进一步揭示了昼夜节律时钟中枢元件 PSEUDO-RESPONSE REGULATOR 7(CiPRR7)可激活 CiAGL24 的表达,以应对自毁条件。此外,我们的研究结果还阐明了 CiAGL24 和 CO 1 过度表达抑制因子(CiSOC1)调节 LEAFY(CiLFY)表达的负反馈回路。总之,我们的研究结果表明,CiPRR7-CiAGL24 模块对于在 IM 中持续感知 SD 信号以确保菊花成功开花至关重要。
{"title":"AGAMOUS-LIKE 24 senses continuous inductive photoperiod in the inflorescence meristem to promote anthesis in chrysanthemum.","authors":"Xuening Liu, Mingzheng Han, Tianhua Jiang, Lei Liu, Jiayi Luo, Ying Lu, Yafei Zhao, Cai-Zhong Jiang, Junping Gao, Bo Hong, Chao Ma","doi":"10.1093/plcell/koae235","DOIUrl":"10.1093/plcell/koae235","url":null,"abstract":"<p><p>During the floral transition, many plant species including chrysanthemum (Chrysanthemum morifolium) require continuous photoperiodic stimulation for successful anthesis. Insufficient photoperiodic stimulation results in flower bud arrest or even failure. The molecular mechanisms underlying how continuous photoperiodic stimulation promotes anthesis are not well understood. Here, we reveal that in wild chrysanthemum (Chrysanthemum indicum), an obligate short-day (SD) plant, floral evocation is not limited to SD conditions. However, SD signals generated locally in the inflorescence meristem (IM) play a vital role in ensuring anthesis after floral commitment. Genetic analyses indicate that the florigen FLOWERING LOCUS T-LIKE3 (CiFTL3) plays an important role in floral evocation, but a lesser role in anthesis. Importantly, our data demonstrate that AGAMOUS-LIKE 24 (CiAGL24) is a critical component of SD signal perception in the IM to promote successful anthesis, and that floral evocation and anthesis are two separate developmental events in chrysanthemum. We further reveal that the central circadian clock component PSEUDO-RESPONSE REGULATOR 7 (CiPRR7) in the IM activates CiAGL24 expression in response to SD conditions. Moreover, our findings elucidate a negative feedback loop in which CiAGL24 and SUPPRESSOR OF OVEREXPRESSION OF CO 1 (CiSOC1) modulate LEAFY (CiLFY) expression. Together, our results demonstrate that the CiPRR7-CiAGL24 module is vital for sustained SD signal perception in the IM to ensure successful anthesis in chrysanthemum.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4658-4671"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11448879/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142005007","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}
David Rolo, Mark A Schöttler, Omar Sandoval-Ibáñez, Ralph Bock
The photosynthetic apparatus is formed by thylakoid membrane-embedded multiprotein complexes that carry out linear electron transport in oxygenic photosynthesis. The machinery is largely conserved from cyanobacteria to land plants, and structure and function of the protein complexes involved are relatively well studied. By contrast, how the machinery is assembled in thylakoid membranes remains poorly understood. The complexes participating in photosynthetic electron transfer are composed of many proteins, pigments, and redox-active cofactors, whose temporally and spatially highly coordinated incorporation is essential to build functional mature complexes. Several proteins, jointly referred to as assembly factors, engage in the biogenesis of these complexes to bring the components together in a step-wise manner, in the right order and time. In this review, we focus on the biogenesis of the terminal protein supercomplex of the photosynthetic electron transport chain, PSI, in vascular plants. We summarize our current knowledge of the assembly process and the factors involved and describe the challenges associated with resolving the assembly pathway in molecular detail.
{"title":"Structure, function, and assembly of PSI in thylakoid membranes of vascular plants.","authors":"David Rolo, Mark A Schöttler, Omar Sandoval-Ibáñez, Ralph Bock","doi":"10.1093/plcell/koae169","DOIUrl":"10.1093/plcell/koae169","url":null,"abstract":"<p><p>The photosynthetic apparatus is formed by thylakoid membrane-embedded multiprotein complexes that carry out linear electron transport in oxygenic photosynthesis. The machinery is largely conserved from cyanobacteria to land plants, and structure and function of the protein complexes involved are relatively well studied. By contrast, how the machinery is assembled in thylakoid membranes remains poorly understood. The complexes participating in photosynthetic electron transfer are composed of many proteins, pigments, and redox-active cofactors, whose temporally and spatially highly coordinated incorporation is essential to build functional mature complexes. Several proteins, jointly referred to as assembly factors, engage in the biogenesis of these complexes to bring the components together in a step-wise manner, in the right order and time. In this review, we focus on the biogenesis of the terminal protein supercomplex of the photosynthetic electron transport chain, PSI, in vascular plants. We summarize our current knowledge of the assembly process and the factors involved and describe the challenges associated with resolving the assembly pathway in molecular detail.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4080-4108"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449065/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141288442","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 respond to cold stress at multiple levels, including increasing cytosolic calcium (Ca2+) influx and triggering the expression of cold-responsive genes. In this study, we show that the Ca2+-permeable channel CYCLIC NUCLEOTIDE-GATED CHANNEL20 (CNGC20) positively regulates freezing tolerance in Arabidopsis (Arabidopsis thaliana) by mediating cold-induced Ca2+ influx. Moreover, we demonstrate that the leucine-rich repeat receptor-like kinase PLANT PEPTIDE CONTAINING SULFATED TYROSINE1 RECEPTOR (PSY1R) is activated by cold, phosphorylating and enhancing the activity of CNGC20. The psy1r mutant exhibits decreased cold-evoked Ca2+ influx and freezing tolerance. Conversely, COLD-RESPONSIVE PROTEIN KINASE1 (CRPK1), a protein kinase that negatively regulates cold signaling, phosphorylates and facilitates the degradation of CNGC20 under prolonged periods of cold treatment, thereby attenuating freezing tolerance. This study thus identifies PSY1R and CRPK1 kinases that regulate CNGC20 activity and stability, respectively, thereby antagonistically modulating freezing tolerance in plants.
{"title":"Differential phosphorylation of Ca2+-permeable channel CYCLIC NUCLEOTIDE-GATED CHANNEL20 modulates calcium-mediated freezing tolerance in Arabidopsis.","authors":"Yue Peng, Yuhang Ming, Bochen Jiang, Xiuyue Zhang, Diyi Fu, Qihong Lin, Xiaoyan Zhang, Yi Wang, Yiting Shi, Zhizhong Gong, Yanglin Ding, Shuhua Yang","doi":"10.1093/plcell/koae177","DOIUrl":"10.1093/plcell/koae177","url":null,"abstract":"<p><p>Plants respond to cold stress at multiple levels, including increasing cytosolic calcium (Ca2+) influx and triggering the expression of cold-responsive genes. In this study, we show that the Ca2+-permeable channel CYCLIC NUCLEOTIDE-GATED CHANNEL20 (CNGC20) positively regulates freezing tolerance in Arabidopsis (Arabidopsis thaliana) by mediating cold-induced Ca2+ influx. Moreover, we demonstrate that the leucine-rich repeat receptor-like kinase PLANT PEPTIDE CONTAINING SULFATED TYROSINE1 RECEPTOR (PSY1R) is activated by cold, phosphorylating and enhancing the activity of CNGC20. The psy1r mutant exhibits decreased cold-evoked Ca2+ influx and freezing tolerance. Conversely, COLD-RESPONSIVE PROTEIN KINASE1 (CRPK1), a protein kinase that negatively regulates cold signaling, phosphorylates and facilitates the degradation of CNGC20 under prolonged periods of cold treatment, thereby attenuating freezing tolerance. This study thus identifies PSY1R and CRPK1 kinases that regulate CNGC20 activity and stability, respectively, thereby antagonistically modulating freezing tolerance in plants.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4356-4371"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449002/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141321350","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}
PROTON GRADIENT REGULATION5 (PGR5) is thought to promote cyclic electron flow, and its deficiency impairs photosynthetic control and increases photosensitivity of photosystem (PS) I, leading to seedling lethality under fluctuating light (FL). By screening for Arabidopsis (Arabidopsis thaliana) suppressor mutations that rescue the seedling lethality of pgr5 plants under FL, we identified a portfolio of mutations in 12 different genes. These mutations affect either PSII function, cytochrome b6f (cyt b6f) assembly, plastocyanin (PC) accumulation, the CHLOROPLAST FRUCTOSE-1,6-BISPHOSPHATASE1 (cFBP1), or its negative regulator ATYPICAL CYS HIS-RICH THIOREDOXIN2 (ACHT2). The characterization of the mutants indicates that the recovery of viability can in most cases be explained by the restoration of PSI donor side limitation, which is caused by reduced electron flow to PSI due to defects in PSII, cyt b6f, or PC. Inactivation of cFBP1 or its negative regulator ACHT2 results in increased levels of the NADH dehydrogenase-like complex. This increased activity may be responsible for suppressing the pgr5 phenotype under FL conditions. Plants that lack both PGR5 and DE-ETIOLATION-INDUCED PROTEIN1 (DEIP1)/NEW TINY ALBINO1 (NTA1), previously thought to be essential for cyt b6f assembly, are viable and accumulate cyt b6f. We suggest that PGR5 can have a negative effect on the cyt b6f complex and that DEIP1/NTA1 can ameliorate this negative effect.
{"title":"A pgr5 suppressor screen uncovers two distinct suppression mechanisms and links cytochrome b6f complex stability to PGR5.","authors":"Jan-Ferdinand Penzler, Belén Naranjo, Sabrina Walz, Giada Marino, Tatjana Kleine, Dario Leister","doi":"10.1093/plcell/koae098","DOIUrl":"10.1093/plcell/koae098","url":null,"abstract":"<p><p>PROTON GRADIENT REGULATION5 (PGR5) is thought to promote cyclic electron flow, and its deficiency impairs photosynthetic control and increases photosensitivity of photosystem (PS) I, leading to seedling lethality under fluctuating light (FL). By screening for Arabidopsis (Arabidopsis thaliana) suppressor mutations that rescue the seedling lethality of pgr5 plants under FL, we identified a portfolio of mutations in 12 different genes. These mutations affect either PSII function, cytochrome b6f (cyt b6f) assembly, plastocyanin (PC) accumulation, the CHLOROPLAST FRUCTOSE-1,6-BISPHOSPHATASE1 (cFBP1), or its negative regulator ATYPICAL CYS HIS-RICH THIOREDOXIN2 (ACHT2). The characterization of the mutants indicates that the recovery of viability can in most cases be explained by the restoration of PSI donor side limitation, which is caused by reduced electron flow to PSI due to defects in PSII, cyt b6f, or PC. Inactivation of cFBP1 or its negative regulator ACHT2 results in increased levels of the NADH dehydrogenase-like complex. This increased activity may be responsible for suppressing the pgr5 phenotype under FL conditions. Plants that lack both PGR5 and DE-ETIOLATION-INDUCED PROTEIN1 (DEIP1)/NEW TINY ALBINO1 (NTA1), previously thought to be essential for cyt b6f assembly, are viable and accumulate cyt b6f. We suggest that PGR5 can have a negative effect on the cyt b6f complex and that DEIP1/NTA1 can ameliorate this negative effect.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4245-4266"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449078/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141088130","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}
Microalgae contribute to about half of global net photosynthesis, which converts sunlight into the chemical energy (ATP and NADPH) used to transform CO2 into biomass. Alternative electron pathways of photosynthesis have been proposed to generate additional ATP that is required to sustain CO2 fixation. However, the relative importance of each alternative pathway remains elusive. Here, we dissect and quantify the contribution of cyclic, pseudo-cyclic, and chloroplast-to-mitochondrion electron flows for their ability to sustain net photosynthesis in the microalga Chlamydomonas reinhardtii. We show that (i) each alternative pathway can provide sufficient additional energy to sustain high CO2 fixation rates, (ii) the alternative pathways exhibit cross-compensation, and (iii) the activity of at least one of the three alternative pathways is necessary to sustain photosynthesis. We further show that all pathways have very different efficiencies at energizing CO2 fixation, with the chloroplast-mitochondrion interaction being the most efficient. Overall, our data lay bioenergetic foundations for biotechnological strategies to improve CO2 capture and fixation.
{"title":"Alternative electron pathways of photosynthesis power green algal CO2 capture.","authors":"Gilles Peltier, Carolyne Stoffel, Justin Findinier, Sai Kiran Madireddi, Ousmane Dao, Virginie Epting, Amélie Morin, Arthur Grossman, Yonghua Li-Beisson, Adrien Burlacot","doi":"10.1093/plcell/koae143","DOIUrl":"10.1093/plcell/koae143","url":null,"abstract":"<p><p>Microalgae contribute to about half of global net photosynthesis, which converts sunlight into the chemical energy (ATP and NADPH) used to transform CO2 into biomass. Alternative electron pathways of photosynthesis have been proposed to generate additional ATP that is required to sustain CO2 fixation. However, the relative importance of each alternative pathway remains elusive. Here, we dissect and quantify the contribution of cyclic, pseudo-cyclic, and chloroplast-to-mitochondrion electron flows for their ability to sustain net photosynthesis in the microalga Chlamydomonas reinhardtii. We show that (i) each alternative pathway can provide sufficient additional energy to sustain high CO2 fixation rates, (ii) the alternative pathways exhibit cross-compensation, and (iii) the activity of at least one of the three alternative pathways is necessary to sustain photosynthesis. We further show that all pathways have very different efficiencies at energizing CO2 fixation, with the chloroplast-mitochondrion interaction being the most efficient. Overall, our data lay bioenergetic foundations for biotechnological strategies to improve CO2 capture and fixation.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4132-4142"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449004/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140916948","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}
As an essential intrinsic component of photosystem II (PSII) in all oxygenic photosynthetic organisms, heme-bridged heterodimer cytochrome b559 (Cyt b559) plays critical roles in the protection and assembly of PSII. However, the underlying mechanisms of Cyt b559 assembly are largely unclear. Here, we characterized the Arabidopsis (Arabidopsis thaliana) rph1 (resistance to Phytophthora1) mutant, which was previously shown to be susceptible to the oomycete pathogen Phytophthora brassicae. Loss of RPH1 leads to a drastic reduction in PSII accumulation, which can be primarily attributed to the defective formation of Cyt b559. Spectroscopic analyses showed that the heme level in PSII supercomplexes isolated from rph1 is significantly reduced, suggesting that RPH1 facilitates proper heme assembly in Cyt b559. Due to the loss of RPH1-mediated processes, a covalently bound PsbE-PsbF heterodimer is formed during the biogenesis of PSII. In addition, rph1 is highly photosensitive and accumulates elevated levels of reactive oxygen species under photoinhibitory-light conditions. RPH1 is a conserved intrinsic thylakoid protein present in green algae and terrestrial plants, but absent in Synechocystis, and it directly interacts with the subunits of Cyt b559. Thus, our data demonstrate that RPH1 represents a chloroplast acquisition specifically promoting the efficient assembly of Cyt b559, probably by mediating proper heme insertion into the apo-Cyt b559 during the initial phase of PSII biogenesis.
{"title":"RESISTANCE TO PHYTOPHTHORA1 promotes cytochrome b559 formation during early photosystem II biogenesis in Arabidopsis.","authors":"Li-Ping Che, Junxiang Ruan, Qiang Xin, Lin Zhang, Fudan Gao, Lujuan Cai, Jianing Zhang, Shiwei Chen, Hui Zhang, Jean-David Rochaix, Lianwei Peng","doi":"10.1093/plcell/koae196","DOIUrl":"10.1093/plcell/koae196","url":null,"abstract":"<p><p>As an essential intrinsic component of photosystem II (PSII) in all oxygenic photosynthetic organisms, heme-bridged heterodimer cytochrome b559 (Cyt b559) plays critical roles in the protection and assembly of PSII. However, the underlying mechanisms of Cyt b559 assembly are largely unclear. Here, we characterized the Arabidopsis (Arabidopsis thaliana) rph1 (resistance to Phytophthora1) mutant, which was previously shown to be susceptible to the oomycete pathogen Phytophthora brassicae. Loss of RPH1 leads to a drastic reduction in PSII accumulation, which can be primarily attributed to the defective formation of Cyt b559. Spectroscopic analyses showed that the heme level in PSII supercomplexes isolated from rph1 is significantly reduced, suggesting that RPH1 facilitates proper heme assembly in Cyt b559. Due to the loss of RPH1-mediated processes, a covalently bound PsbE-PsbF heterodimer is formed during the biogenesis of PSII. In addition, rph1 is highly photosensitive and accumulates elevated levels of reactive oxygen species under photoinhibitory-light conditions. RPH1 is a conserved intrinsic thylakoid protein present in green algae and terrestrial plants, but absent in Synechocystis, and it directly interacts with the subunits of Cyt b559. Thus, our data demonstrate that RPH1 represents a chloroplast acquisition specifically promoting the efficient assembly of Cyt b559, probably by mediating proper heme insertion into the apo-Cyt b559 during the initial phase of PSII biogenesis.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4143-4167"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449094/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141535074","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}
Alternative splicing (AS) plays crucial roles in regulating various biological processes in plants. However, the genetic mechanisms underlying AS and its role in controlling important agronomic traits in rice (Oryza sativa) remain poorly understood. In this study, we explored AS in rice leaves and panicles using the rice minicore collection. Our analysis revealed a high level of transcript isoform diversity, with approximately one-fifth of the potential isoforms acting as major transcripts in both tissues. Regarding the genetic mechanism of AS, we found that the splicing of 833 genes in the leaf and 1,230 genes in the panicle was affected by cis-genetic variation. Twenty-one percent of these AS events could only be explained by large structural variations. Approximately 77.5% of genes with significant splicing quantitative trait loci (sGenes) exhibited tissue-specific regulation, and AS can cause 26.9% (leaf) and 23.6% (panicle) of sGenes to have altered, lost, or gained functional domains. Additionally, through splicing-phenotype association analysis, we identified phosphate-starvation-induced RING-type E3 ligase (OsPIE1; LOC_Os01g72480), whose splicing ratio was significantly associated with plant height. In summary, this study provides an understanding of AS in rice and its contribution to the regulation of important agronomic traits.
替代剪接(AS)在调控植物的各种生物过程中发挥着至关重要的作用。然而,人们对替代剪接的遗传机制及其在控制水稻(Oryza sativa)重要农艺性状中的作用仍然知之甚少。在本研究中,我们利用水稻微型核心集探索了水稻叶片和圆锥花序中的AS。我们的分析揭示了转录本同工酶的高度多样性,约五分之一的潜在同工酶在这两种组织中充当主要转录本。关于AS的遗传机制,我们发现叶片中833个基因和圆锥花序中1230个基因的剪接受到顺式遗传变异的影响。在这些AS事件中,有21%只能通过较大的结构变异来解释。约77.5%的具有显著剪接数量性状位点(sGenes)的基因表现出组织特异性调控,AS可导致26.9%(叶片)和23.6%(圆锥花序)的sGenes改变、丢失或获得功能域。此外,通过剪接-表型关联分析,我们发现磷酸盐饥饿诱导的RING型E3连接酶(OsPIE1;LOC_Os01g72480)的剪接比率与植株高度显著相关。总之,本研究有助于了解水稻中的 AS 及其对重要农艺性状调控的贡献。
{"title":"Population-level exploration of alternative splicing and its unique role in controlling agronomic traits of rice.","authors":"Hong Zhang, Wu Chen, De Zhu, Bintao Zhang, Qiang Xu, Chuanlin Shi, Huiying He, Xiaofan Dai, Yilin Li, Wenchuang He, Yang Lv, Longbo Yang, Xinglan Cao, Yan Cui, Yue Leng, Hua Wei, Xiangpei Liu, Bin Zhang, Xianmeng Wang, Mingliang Guo, Zhipeng Zhang, Xiaoxia Li, Congcong Liu, Qiaoling Yuan, Tianyi Wang, Xiaoman Yu, Hongge Qian, Qianqian Zhang, Dandan Chen, Guanjing Hu, Qian Qian, Lianguang Shang","doi":"10.1093/plcell/koae181","DOIUrl":"10.1093/plcell/koae181","url":null,"abstract":"<p><p>Alternative splicing (AS) plays crucial roles in regulating various biological processes in plants. However, the genetic mechanisms underlying AS and its role in controlling important agronomic traits in rice (Oryza sativa) remain poorly understood. In this study, we explored AS in rice leaves and panicles using the rice minicore collection. Our analysis revealed a high level of transcript isoform diversity, with approximately one-fifth of the potential isoforms acting as major transcripts in both tissues. Regarding the genetic mechanism of AS, we found that the splicing of 833 genes in the leaf and 1,230 genes in the panicle was affected by cis-genetic variation. Twenty-one percent of these AS events could only be explained by large structural variations. Approximately 77.5% of genes with significant splicing quantitative trait loci (sGenes) exhibited tissue-specific regulation, and AS can cause 26.9% (leaf) and 23.6% (panicle) of sGenes to have altered, lost, or gained functional domains. Additionally, through splicing-phenotype association analysis, we identified phosphate-starvation-induced RING-type E3 ligase (OsPIE1; LOC_Os01g72480), whose splicing ratio was significantly associated with plant height. In summary, this study provides an understanding of AS in rice and its contribution to the regulation of important agronomic traits.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":" ","pages":"4372-4387"},"PeriodicalIF":10.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449091/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141446768","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}