Wheat (Triticum aestivum L.) spike development is tightly regulated by genetic and metabolic programs that drive organ growth and morphological changes. However, the dynamic interplay between metabolic shifts, gene expression patterns, and their regulatory roles during spike development, remains poorly characterized. To address this knowledge gap, we performed integrated metabolomic and transcriptomic profiling across 12 stages of wheat spike organ development. Our analysis detected 1,105 metabolites in 233 spike, spikelet, and floret samples, uncovering an uneven distribution of phytohormone-related metabolites. The exogenous phytohormone treatments validated the regulatory roles of phytohormones in spike morphogenesis. High-resolution spatiotemporal data from carpel organs enabled the reconstruction of a regulatory network, identifying key genes (including 12-oxo-phytodienoic acid reductase3 (TaOPR3), Grain Length1 (GL1), and Grain Length2 (GL2)) as critical determinants of grain size. Genomic analyses revealed geographical differentiation in gene haplotypes and their selective retention during breeding, with superior alleles associated with increased grain size. This comprehensive dataset provides a valuable resource for understanding the molecular basis of wheat grain yield and offers potential targets for crop improvement.
{"title":"Multi-omics identifies key genetic and metabolic networks regulating spike organ development in wheat","authors":"Yangyang Liu, Lili Zhang, Anting Zhu, Liping Shen, Jiaqi Zhang, Jun Chen, Guowei Chang, Changbin Yin, Ziying Wang, Zhiwen Sun, Kuocheng Shen, Xiaowan Xu, Mengjing Sun, Mingming Xin, Jianhui Wu, Zefu Lu, Yiping Tong, Zhonghu He, Fei Lu, Yuanfeng Hao, Wei Chen, Zifeng Guo","doi":"10.1093/plcell/koaf250","DOIUrl":"https://doi.org/10.1093/plcell/koaf250","url":null,"abstract":"Wheat (Triticum aestivum L.) spike development is tightly regulated by genetic and metabolic programs that drive organ growth and morphological changes. However, the dynamic interplay between metabolic shifts, gene expression patterns, and their regulatory roles during spike development, remains poorly characterized. To address this knowledge gap, we performed integrated metabolomic and transcriptomic profiling across 12 stages of wheat spike organ development. Our analysis detected 1,105 metabolites in 233 spike, spikelet, and floret samples, uncovering an uneven distribution of phytohormone-related metabolites. The exogenous phytohormone treatments validated the regulatory roles of phytohormones in spike morphogenesis. High-resolution spatiotemporal data from carpel organs enabled the reconstruction of a regulatory network, identifying key genes (including 12-oxo-phytodienoic acid reductase3 (TaOPR3), Grain Length1 (GL1), and Grain Length2 (GL2)) as critical determinants of grain size. Genomic analyses revealed geographical differentiation in gene haplotypes and their selective retention during breeding, with superior alleles associated with increased grain size. This comprehensive dataset provides a valuable resource for understanding the molecular basis of wheat grain yield and offers potential targets for crop improvement.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"102 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145314590","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Two to tango: DTT1 regulates barley tapetum transition as part of a paired key.","authors":"Julie Robinson","doi":"10.1093/plcell/koaf249","DOIUrl":"https://doi.org/10.1093/plcell/koaf249","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"46 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145305582","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Fruit weight and size are fundamental traits in tomato breeding and critical determinants of yield. Although several histone-modifying enzymes have been implicated in tomato fruit ripening, the role of histone arginine methylation in fruit development remains unknown. Here, we identify the histone H3R2me2a demethylase Jumonji C-domain-containing proteins 10 (JMJ10) as a key regulator of fruit size in tomato (Solanum lycopersicum). Loss of JMJ10 function reduces fruit size, whereas JMJ10 overexpression enhances fruit growth, primarily by promoting pericarp cell expansion. JMJ10 specifically demethylates H3R2me2a at key fruit size-associated genes, including FW11.3, CDF4, EXP2, EXP5, XTH8, and PRE2, thereby promoting their transcription. Furthermore, we show that JMJ10 physically interacts with the transcription factor Brassinazole-Resistant 1.3 (BZR1.3), which recruits JMJ10 to its target genes. The jmj10 bzr1.3 double mutants exhibit a more severe reduction in fruit size compared to either single mutant, confirming a synergistic interaction between JMJ10 and BZR1.3. ChIP-qPCR analysis showed that JMJ10 occupancy at its target loci is significantly reduced in the bzr1.3 mutant, suggesting that JMJ10 binding is BZR1.3-dependent. Additionally, BZR1.3 recruits JMJ10 to enhance the expression of these genes by facilitating H3R2me2a removal. Collectively, our findings reveal a mechanism by which BZR1.3 recruits JMJ10, a H3R2me2a demethylase, to coordinate the epigenetic regulation of fruit size in tomato.
果实重量和大小是番茄育种的基本性状，也是决定产量的关键因素。虽然有几种组蛋白修饰酶与番茄果实成熟有关，但组蛋白精氨酸甲基化在果实发育中的作用尚不清楚。本研究发现组蛋白H3R2me2a去甲基化酶Jumonji c -domain containing proteins 10 （JMJ10）是番茄果实大小的关键调控因子。JMJ10功能缺失会降低果实大小，而JMJ10过表达则主要通过促进果皮细胞扩张来促进果实生长。JMJ10特异性地使H3R2me2a在果实大小相关的关键基因上去甲基化，包括FW11.3、CDF4、EXP2、EXP5、XTH8和PRE2，从而促进它们的转录。此外，我们发现JMJ10与转录因子Brassinazole-Resistant 1.3 （BZR1.3）发生物理相互作用，从而将JMJ10招募到其靶基因。与单突变体相比，jmj10 bzr1.3双突变体表现出更严重的果实大小减少，证实了jmj10和bzr1.3之间的协同相互作用。ChIP-qPCR分析显示，在bzr1.3突变体中，JMJ10在其靶位点的占用率显著降低，表明JMJ10的结合依赖于bzr1.3。此外，BZR1.3招募JMJ10通过促进H3R2me2a的去除来增强这些基因的表达。总之，我们的研究结果揭示了BZR1.3招募H3R2me2a去甲基化酶JMJ10来协调番茄果实大小表观遗传调控的机制。
{"title":"The H3R2me2a demethylase JMJ10 regulates tomato fruit size through its interaction with the transcription factor BZR1.3.","authors":"Jing Zeng,Zhiwei Li,Xiaochun Ding,Hanzhi Liang,Keqiang Wu,Yueming Jiang,Xuewu Duan,Guoxiang Jiang","doi":"10.1093/plcell/koaf251","DOIUrl":"https://doi.org/10.1093/plcell/koaf251","url":null,"abstract":"Fruit weight and size are fundamental traits in tomato breeding and critical determinants of yield. Although several histone-modifying enzymes have been implicated in tomato fruit ripening, the role of histone arginine methylation in fruit development remains unknown. Here, we identify the histone H3R2me2a demethylase Jumonji C-domain-containing proteins 10 (JMJ10) as a key regulator of fruit size in tomato (Solanum lycopersicum). Loss of JMJ10 function reduces fruit size, whereas JMJ10 overexpression enhances fruit growth, primarily by promoting pericarp cell expansion. JMJ10 specifically demethylates H3R2me2a at key fruit size-associated genes, including FW11.3, CDF4, EXP2, EXP5, XTH8, and PRE2, thereby promoting their transcription. Furthermore, we show that JMJ10 physically interacts with the transcription factor Brassinazole-Resistant 1.3 (BZR1.3), which recruits JMJ10 to its target genes. The jmj10 bzr1.3 double mutants exhibit a more severe reduction in fruit size compared to either single mutant, confirming a synergistic interaction between JMJ10 and BZR1.3. ChIP-qPCR analysis showed that JMJ10 occupancy at its target loci is significantly reduced in the bzr1.3 mutant, suggesting that JMJ10 binding is BZR1.3-dependent. Additionally, BZR1.3 recruits JMJ10 to enhance the expression of these genes by facilitating H3R2me2a removal. Collectively, our findings reveal a mechanism by which BZR1.3 recruits JMJ10, a H3R2me2a demethylase, to coordinate the epigenetic regulation of fruit size in tomato.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"8 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145305583","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
M Fenech, J Brumos, A Pěnčík, B Edwards, S Belcapo, J DeLacey, A Patel, M M Kater, X Li, K Ljung, O Novak, J M Alonso, A N Stepanova
The auxin indole-3-acetic acid (IAA) governs plant development and environmental responses. Although the indole-3-pyruvic acid (IPyA) pathway is the predominant route for IAA biosynthesis, other pathways have been proposed, such as the indole-3-acetaldoxime (IAOx) pathway. The IAOx pathway has garnered attention due to its supposed activation in auxin-overproducing mutants (e.g., sur1, sur2, ugt74b1) and the auxin-like responses triggered by exogenous application of its proposed intermediates IAOx, indole-3-acetonitrile (IAN), and indole-3-acetamide (IAM). However, despite the supporting evidence for individual steps of the IAOx pathway, its overall physiological relevance remains inconclusive. Here, using a comprehensive genetic approach combined with metabolic and phenotypic profiling, we demonstrate that mutating gene families proposed to function in the IAOx pathway in Arabidopsis (Arabidopsis thaliana) does not result in prominent auxin-deficient phenotypes, nor are these genes required for the high auxin production in the sur2 mutant. Our findings also challenge the previously postulated linear IAOx pathway. Exogenously provided IAOx, IAN, and IAM can be converted to IAA in vivo, but they do not act as precursors for each other. Finally, our findings question the physiological relevance of IAM and IAN as IAA precursors in plants and suggest the existence of a yet-uncharacterized route for IAA production in the sur2 mutant, likely involving IAOx as an intermediate. The identification of the metabolic steps and the corresponding genes in this pathway may uncover another IAA biosynthesis route in plants.
{"title":"The CYP71A, NIT, AMI, and IAMH gene families are dispensable for indole-3-acetaldoxime-mediated auxin biosynthesis in Arabidopsis","authors":"M Fenech, J Brumos, A Pěnčík, B Edwards, S Belcapo, J DeLacey, A Patel, M M Kater, X Li, K Ljung, O Novak, J M Alonso, A N Stepanova","doi":"10.1093/plcell/koaf242","DOIUrl":"https://doi.org/10.1093/plcell/koaf242","url":null,"abstract":"The auxin indole-3-acetic acid (IAA) governs plant development and environmental responses. Although the indole-3-pyruvic acid (IPyA) pathway is the predominant route for IAA biosynthesis, other pathways have been proposed, such as the indole-3-acetaldoxime (IAOx) pathway. The IAOx pathway has garnered attention due to its supposed activation in auxin-overproducing mutants (e.g., sur1, sur2, ugt74b1) and the auxin-like responses triggered by exogenous application of its proposed intermediates IAOx, indole-3-acetonitrile (IAN), and indole-3-acetamide (IAM). However, despite the supporting evidence for individual steps of the IAOx pathway, its overall physiological relevance remains inconclusive. Here, using a comprehensive genetic approach combined with metabolic and phenotypic profiling, we demonstrate that mutating gene families proposed to function in the IAOx pathway in Arabidopsis (Arabidopsis thaliana) does not result in prominent auxin-deficient phenotypes, nor are these genes required for the high auxin production in the sur2 mutant. Our findings also challenge the previously postulated linear IAOx pathway. Exogenously provided IAOx, IAN, and IAM can be converted to IAA in vivo, but they do not act as precursors for each other. Finally, our findings question the physiological relevance of IAM and IAN as IAA precursors in plants and suggest the existence of a yet-uncharacterized route for IAA production in the sur2 mutant, likely involving IAOx as an intermediate. The identification of the metabolic steps and the corresponding genes in this pathway may uncover another IAA biosynthesis route in plants.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"16 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145295587","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Beyond the PEL surveyance: Genome editing of the OsPEL family enhances photosynthesis efficiency in Rice.","authors":"Christian Damian Lorenzo","doi":"10.1093/plcell/koaf247","DOIUrl":"https://doi.org/10.1093/plcell/koaf247","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"119 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296049","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Whispers in the Genome: The Hidden Grammar of Tomato Fruit Development.","authors":"Andrea Gómez-Felipe","doi":"10.1093/plcell/koaf248","DOIUrl":"https://doi.org/10.1093/plcell/koaf248","url":null,"abstract":"","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"33 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296050","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gene and genome duplications expand genetic repertoires and facilitate functional innovation. Segmental or whole-genome duplications generate duplicates with similar and somewhat redundant expression profiles across multiple tissues, while other modes of duplication create genes that show increased divergence, leading to functional innovations. How duplicates diverge in expression across cell types in a single tissue remains elusive. Here, we used high-resolution spatial transcriptomic data from Arabidopsis thaliana, Glycine max, Phalaenopsis aphrodite, Zea mays, and Hordeum vulgare to investigate the evolution of gene expression following gene duplication. We found that genes originating from segmental or whole-genome duplications display increased expression levels, expression breadths, spatial variability, and number of coexpression partners. Duplication mechanisms that preserve cis-regulatory landscapes typically generate paralogs with more preserved expression profiles, but such differences generated by mode of duplication fade or disappear over time. Paralogs originating from large-scale (including whole-genome) duplications display redundant or overlapping expression profiles, indicating functional redundancy or subfunctionalization, while most small-scale duplicates diverge asymmetrically, consistent with neofunctionalization. Expression divergence also depends on gene functions, with dosage-sensitive genes displaying highly preserved expression profiles, and genes involved in more specialized processes diverging more rapidly. Our findings offer a spatially resolved view of expression divergence following duplication, elucidating the tempo and mode of gene expression evolution, and helping understand how gene and genome duplications shape cell identities.
{"title":"Gene expression divergence following gene and genome duplications in spatially resolved plant transcriptomes","authors":"Fabricio Almeida-Silva, Yves Van de Peer","doi":"10.1093/plcell/koaf243","DOIUrl":"https://doi.org/10.1093/plcell/koaf243","url":null,"abstract":"Gene and genome duplications expand genetic repertoires and facilitate functional innovation. Segmental or whole-genome duplications generate duplicates with similar and somewhat redundant expression profiles across multiple tissues, while other modes of duplication create genes that show increased divergence, leading to functional innovations. How duplicates diverge in expression across cell types in a single tissue remains elusive. Here, we used high-resolution spatial transcriptomic data from Arabidopsis thaliana, Glycine max, Phalaenopsis aphrodite, Zea mays, and Hordeum vulgare to investigate the evolution of gene expression following gene duplication. We found that genes originating from segmental or whole-genome duplications display increased expression levels, expression breadths, spatial variability, and number of coexpression partners. Duplication mechanisms that preserve cis-regulatory landscapes typically generate paralogs with more preserved expression profiles, but such differences generated by mode of duplication fade or disappear over time. Paralogs originating from large-scale (including whole-genome) duplications display redundant or overlapping expression profiles, indicating functional redundancy or subfunctionalization, while most small-scale duplicates diverge asymmetrically, consistent with neofunctionalization. Expression divergence also depends on gene functions, with dosage-sensitive genes displaying highly preserved expression profiles, and genes involved in more specialized processes diverging more rapidly. Our findings offer a spatially resolved view of expression divergence following duplication, elucidating the tempo and mode of gene expression evolution, and helping understand how gene and genome duplications shape cell identities.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"10 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145295586","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Deng-Pan Zuo,Bin Wang,Yu-Zi Liu,Zheng-Song Chen,Ru-Jian Hu,Meng-Jun He,Zong-Ying Zhang,Ying Wang,Cheng-Gui Han
Chloroplasts play a crucial role in plant immunity against invading microbes. However, whether photosynthetic metabolites from chloroplasts participate directly in host defenses remains poorly understood. Here, we uncovered that an Arabidopsis thaliana triose phosphate/phosphate translocator (TPT) in the inner membrane of the chloroplast envelope suppresses viral infection and evokes defense responses. AtTPT overexpression impairs virus accumulation in plants, and loss-of-function tpt-3 mutants exhibit an increased viral load. The antiviral activity of AtTPT requires its metabolite transport capacity, implying that it indeed functions through its metabolite(s). To this end, we found that glyceraldehyde 3-phosphate (GAP), one the metabolites translocated by AtTPT, drastically enhances the expression of defense-related genes and induces defense signaling pathways. Moreover, AtTPT or GAP robustly impairs the proliferation of diverse phytopathogens. Therefore, we propose that AtTPT exports GAP to mediate broad-spectrum pathogen resistance, which provides insights into the mechanisms underlying chloroplast-mediated immunity induced by a photosynthetic metabolite.
{"title":"A triose phosphate/phosphate translocator triggers antimicrobial immunity by exporting glyceraldehyde 3-phosphate from chloroplasts.","authors":"Deng-Pan Zuo,Bin Wang,Yu-Zi Liu,Zheng-Song Chen,Ru-Jian Hu,Meng-Jun He,Zong-Ying Zhang,Ying Wang,Cheng-Gui Han","doi":"10.1093/plcell/koaf245","DOIUrl":"https://doi.org/10.1093/plcell/koaf245","url":null,"abstract":"Chloroplasts play a crucial role in plant immunity against invading microbes. However, whether photosynthetic metabolites from chloroplasts participate directly in host defenses remains poorly understood. Here, we uncovered that an Arabidopsis thaliana triose phosphate/phosphate translocator (TPT) in the inner membrane of the chloroplast envelope suppresses viral infection and evokes defense responses. AtTPT overexpression impairs virus accumulation in plants, and loss-of-function tpt-3 mutants exhibit an increased viral load. The antiviral activity of AtTPT requires its metabolite transport capacity, implying that it indeed functions through its metabolite(s). To this end, we found that glyceraldehyde 3-phosphate (GAP), one the metabolites translocated by AtTPT, drastically enhances the expression of defense-related genes and induces defense signaling pathways. Moreover, AtTPT or GAP robustly impairs the proliferation of diverse phytopathogens. Therefore, we propose that AtTPT exports GAP to mediate broad-spectrum pathogen resistance, which provides insights into the mechanisms underlying chloroplast-mediated immunity induced by a photosynthetic metabolite.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296051","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Dawei Ma,Harley Gordon,Rashid Nazir,Jeremy E Wulff,C Peter Constabel
Salicylic acid (SA) biosynthesis in plants occurs via the isochorismate synthase (ICS) and phenylalanine ammonia-lyase (PAL) pathways. The critical steps from benzyl-CoA to SA in the PAL-mediated pathway remain unknown. To probe benzenoid metabolism, we generated CRISPR/Cas9-mediated knockouts of benzaldehyde synthase in poplar. These plants produce less benzyl benzoate, benzyl salicylate and SA, yet accumulate more benzoic acid. We show that HSR203J encodes a carboxylesterase that specifically hydrolyzes benzyl salicylate. Virus-induced gene silencing (VIGS) of HSR203J in Nicotiana benthamiana led to reduced benzyl salicylate hydrolysis to SA. Based on these data, we propose a biosynthesis model and provide evidence that benzoyl-CoA is esterified to benzyl benzoate and converted to benzyl salicylate, which then releases SA. In addition, we identified a pathogen-induced cytochrome P450 encoded by HSR515 as a putative benzyl benzoate 2-hydroxylase. VIGS-mediated suppression of HSR515 in N. benthamiana reduced the conversion of benzyl benzoate to SA. Phylogenetic analyses indicated that Brassicaceae genomes do not contain HSR203J and HSR515 orthologs, whereas these genes are present in other vascular plants. These findings represent an important advance in our understanding of SA biosynthesis and identify missing steps in the PAL-mediated SA biosynthetic pathway.
{"title":"Salicylic acid biosynthesis via the PAL pathway requires benzaldehyde synthase and a benzyl salicylate-specific esterase.","authors":"Dawei Ma,Harley Gordon,Rashid Nazir,Jeremy E Wulff,C Peter Constabel","doi":"10.1093/plcell/koaf241","DOIUrl":"https://doi.org/10.1093/plcell/koaf241","url":null,"abstract":"Salicylic acid (SA) biosynthesis in plants occurs via the isochorismate synthase (ICS) and phenylalanine ammonia-lyase (PAL) pathways. The critical steps from benzyl-CoA to SA in the PAL-mediated pathway remain unknown. To probe benzenoid metabolism, we generated CRISPR/Cas9-mediated knockouts of benzaldehyde synthase in poplar. These plants produce less benzyl benzoate, benzyl salicylate and SA, yet accumulate more benzoic acid. We show that HSR203J encodes a carboxylesterase that specifically hydrolyzes benzyl salicylate. Virus-induced gene silencing (VIGS) of HSR203J in Nicotiana benthamiana led to reduced benzyl salicylate hydrolysis to SA. Based on these data, we propose a biosynthesis model and provide evidence that benzoyl-CoA is esterified to benzyl benzoate and converted to benzyl salicylate, which then releases SA. In addition, we identified a pathogen-induced cytochrome P450 encoded by HSR515 as a putative benzyl benzoate 2-hydroxylase. VIGS-mediated suppression of HSR515 in N. benthamiana reduced the conversion of benzyl benzoate to SA. Phylogenetic analyses indicated that Brassicaceae genomes do not contain HSR203J and HSR515 orthologs, whereas these genes are present in other vascular plants. These findings represent an important advance in our understanding of SA biosynthesis and identify missing steps in the PAL-mediated SA biosynthetic pathway.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"25 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296066","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jiuwei Lu, Xinyi Chen, Jian Fang, Daniel Li, Huy Le, Xuehua Zhong, Jikui Song
Plant DNA METHYLTRANSFERASE 1 (MET1) is responsible for maintaining genome-wide CG methylation. Its dysregulation has been linked to profound biological disruptions, including genomic instability and developmental defects. However, the exact mechanism by which MET1 orchestrates these vital functions and coordinates its various domains to shape the plant-specific epigenome remains unknown. Here, we report the cryo-EM structure of Arabidopsis thaliana MET1 (AtMET1), revealing an autoinhibitory mechanism that governs its DNA methylation activity. Between the two replication-foci-target sequence (RFTS) domains in AtMET1, the second RFTS domain (RFTS2) directly associates with the methyltransferase (MTase) domain, thereby inhibiting substrate-binding activity. Compared to DNMT1, AtMET1 lacks the CXXC domain and its downstream autoinhibitory linker, featuring only limited RFTS2-MTase interactions, resulting in a much-reduced autoinhibitory contact. In line with this difference, the DNA methylation activity of AtMET1 displays less temperature dependence than that of DNMT1, potentially allowing MET1 to maintain its activity across diverse temperature conditions. We further report the structure of AtMET1 bound to hemimethylated CG (hmCG) DNA, unveiling the molecular basis for substrate binding and CG recognition by AtMET1, and an activation mechanism that involves a coordinated conformational shift between two structural elements of its active site. In addition, our combined structural and biochemical analysis highlights distinct functionalities between the two RFTS domains of AtMET1, unraveling their evolutionary divergence from the DNMT1 RFTS domain. Together, this study offers a framework for understanding the structure and mechanism of AtMET1, with profound implications for the maintenance of CG methylation in plants.
{"title":"Structure and autoinhibitory regulation of MET1 in the maintenance of plant CG methylation","authors":"Jiuwei Lu, Xinyi Chen, Jian Fang, Daniel Li, Huy Le, Xuehua Zhong, Jikui Song","doi":"10.1093/plcell/koaf246","DOIUrl":"https://doi.org/10.1093/plcell/koaf246","url":null,"abstract":"Plant DNA METHYLTRANSFERASE 1 (MET1) is responsible for maintaining genome-wide CG methylation. Its dysregulation has been linked to profound biological disruptions, including genomic instability and developmental defects. However, the exact mechanism by which MET1 orchestrates these vital functions and coordinates its various domains to shape the plant-specific epigenome remains unknown. Here, we report the cryo-EM structure of Arabidopsis thaliana MET1 (AtMET1), revealing an autoinhibitory mechanism that governs its DNA methylation activity. Between the two replication-foci-target sequence (RFTS) domains in AtMET1, the second RFTS domain (RFTS2) directly associates with the methyltransferase (MTase) domain, thereby inhibiting substrate-binding activity. Compared to DNMT1, AtMET1 lacks the CXXC domain and its downstream autoinhibitory linker, featuring only limited RFTS2-MTase interactions, resulting in a much-reduced autoinhibitory contact. In line with this difference, the DNA methylation activity of AtMET1 displays less temperature dependence than that of DNMT1, potentially allowing MET1 to maintain its activity across diverse temperature conditions. We further report the structure of AtMET1 bound to hemimethylated CG (hmCG) DNA, unveiling the molecular basis for substrate binding and CG recognition by AtMET1, and an activation mechanism that involves a coordinated conformational shift between two structural elements of its active site. In addition, our combined structural and biochemical analysis highlights distinct functionalities between the two RFTS domains of AtMET1, unraveling their evolutionary divergence from the DNMT1 RFTS domain. Together, this study offers a framework for understanding the structure and mechanism of AtMET1, with profound implications for the maintenance of CG methylation in plants.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"52 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145282733","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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