Lignification of the cell wall in pear (Pyrus) fruit results in the formation of stone cells, which affects the texture and quality of the fruit. However, it is still unclear that how different transcription factors (TFs) work together to coordinate the synthesis and deposition of lignin. Here, we examined the transcriptome of pear varieties with different stone cell contents and found a key TF (PbAGL7) that can promote the increase of stone cell contents and secondary cell wall thicknesses. In addition, PbAGL7 can facilitate the expression level of lignin biosynthesis-related genes and accelerate the lignin biosynthesis in pear fruit and Arabidopsis. However, PbAGL7 did not directly bind to the promoters of PbC3H1 and PbHCT17 which are crucial genes involved in lignin biosynthesis. On the other hand, yeast two-hybrid (Y2H) library showed that PbNAC47 and PbMYB73 interacted with PbAGL7 in the nucleus. PbNAC47 and PbMYB73 also increased the stone cell and lignin contents, and upregulated the expressions of PbC3H1 and PbHCT17 by binding to the SNBE and AC elements, respectively. Moreover, PbNAC47 also interacted with PbMYB73 to form PbAGL7-PbNAC47-PbMYB73 complex. This complex significantly activated the expression levels of PbC3H1 and PbHCT17 and promoted lignin biosynthesis to form stone cells in pear fruit. Overall, our study provides new insights into the molecular mechanism of TFs that coordinately regulate the stone cell formation in pear fruit and extend our knowledge to understand cell wall lignification in plants.
{"title":"PbAGL7-PbNAC47-PbMYB73 complex coordinately regulates PbC3H1 and PbHCT17 to promote the lignin biosynthesis in stone cells of pear fruit.","authors":"Xin Gong, Kaijie Qi, Liangyi Zhao, Zhihua Xie, Jiahui Pan, Xin Yan, Katsuhiro Shiratake, Shaoling Zhang, Shutian Tao","doi":"10.1111/tpj.17090","DOIUrl":"https://doi.org/10.1111/tpj.17090","url":null,"abstract":"<p><p>Lignification of the cell wall in pear (Pyrus) fruit results in the formation of stone cells, which affects the texture and quality of the fruit. However, it is still unclear that how different transcription factors (TFs) work together to coordinate the synthesis and deposition of lignin. Here, we examined the transcriptome of pear varieties with different stone cell contents and found a key TF (PbAGL7) that can promote the increase of stone cell contents and secondary cell wall thicknesses. In addition, PbAGL7 can facilitate the expression level of lignin biosynthesis-related genes and accelerate the lignin biosynthesis in pear fruit and Arabidopsis. However, PbAGL7 did not directly bind to the promoters of PbC3H1 and PbHCT17 which are crucial genes involved in lignin biosynthesis. On the other hand, yeast two-hybrid (Y2H) library showed that PbNAC47 and PbMYB73 interacted with PbAGL7 in the nucleus. PbNAC47 and PbMYB73 also increased the stone cell and lignin contents, and upregulated the expressions of PbC3H1 and PbHCT17 by binding to the SNBE and AC elements, respectively. Moreover, PbNAC47 also interacted with PbMYB73 to form PbAGL7-PbNAC47-PbMYB73 complex. This complex significantly activated the expression levels of PbC3H1 and PbHCT17 and promoted lignin biosynthesis to form stone cells in pear fruit. Overall, our study provides new insights into the molecular mechanism of TFs that coordinately regulate the stone cell formation in pear fruit and extend our knowledge to understand cell wall lignification in plants.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491826","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sivakumar Swaminathan, Corrinne E Grover, Alither S Mugisha, Lauren E Sichterman, Youngwoo Lee, Pengcheng Yang, Eileen L Mallery, Josef J Jareczek, Alexis G Leach, Jun Xie, Jonathan F Wendel, Daniel B Szymanski, Olga A Zabotina
Cotton fiber is the most valuable naturally available material for the textile industry and the fiber length and strength are key determinants of its quality. Dynamic changes in the pectin, xyloglucan, xylan, and cellulose polysaccharide epitope content during fiber growth contribute to complex remodeling of fiber cell wall (CW) and quality. Detailed knowledge about polysaccharide compositional and structural alteration in the fiber during fiber elongation and strengthening is important to understand the molecular dynamics of fiber development and improve its quality. Here, large-scale glycome profiling coupled with fiber phenotype and transcriptome profiling was conducted on fiber collected daily covering the most critical window of fiber development. The profiling studies with high temporal resolution allowed us to identify specific polysaccharide epitopes associated with distinct fiber phenotypes that might contribute to fiber quality. This study revealed the critical role of highly branched RG-I pectin epitopes such as β-1,4-linked-galactans, β-1,6-linked-galactans, and arabinogalactans, in addition to earlier reported homogalacturonans and xyloglucans in the formation of cotton fiber middle lamella and contributing to fiber plasticity and elongation. We also propose the essential role of heteroxylans (Xyl-MeGlcA and Xyl-3Ar), as a guiding factor for secondary CW cellulose microfibril arrangement, thus contributing to fiber strength. Correlation analysis of profiles of polysaccharide epitopes from glycome data and expression profiles of glycosyltransferase-encoding genes from transcriptome data identified several key putative glycosyltransferases that are potentially involved in synthesizing the critical polysaccharide epitopes. The findings of this study provide a foundation to identify molecular factors that dictate important fiber traits.
{"title":"Daily glycome and transcriptome profiling reveals polysaccharide structures and correlated glycosyltransferases critical for cotton fiber growth.","authors":"Sivakumar Swaminathan, Corrinne E Grover, Alither S Mugisha, Lauren E Sichterman, Youngwoo Lee, Pengcheng Yang, Eileen L Mallery, Josef J Jareczek, Alexis G Leach, Jun Xie, Jonathan F Wendel, Daniel B Szymanski, Olga A Zabotina","doi":"10.1111/tpj.17084","DOIUrl":"https://doi.org/10.1111/tpj.17084","url":null,"abstract":"<p><p>Cotton fiber is the most valuable naturally available material for the textile industry and the fiber length and strength are key determinants of its quality. Dynamic changes in the pectin, xyloglucan, xylan, and cellulose polysaccharide epitope content during fiber growth contribute to complex remodeling of fiber cell wall (CW) and quality. Detailed knowledge about polysaccharide compositional and structural alteration in the fiber during fiber elongation and strengthening is important to understand the molecular dynamics of fiber development and improve its quality. Here, large-scale glycome profiling coupled with fiber phenotype and transcriptome profiling was conducted on fiber collected daily covering the most critical window of fiber development. The profiling studies with high temporal resolution allowed us to identify specific polysaccharide epitopes associated with distinct fiber phenotypes that might contribute to fiber quality. This study revealed the critical role of highly branched RG-I pectin epitopes such as β-1,4-linked-galactans, β-1,6-linked-galactans, and arabinogalactans, in addition to earlier reported homogalacturonans and xyloglucans in the formation of cotton fiber middle lamella and contributing to fiber plasticity and elongation. We also propose the essential role of heteroxylans (Xyl-MeGlcA and Xyl-3Ar), as a guiding factor for secondary CW cellulose microfibril arrangement, thus contributing to fiber strength. Correlation analysis of profiles of polysaccharide epitopes from glycome data and expression profiles of glycosyltransferase-encoding genes from transcriptome data identified several key putative glycosyltransferases that are potentially involved in synthesizing the critical polysaccharide epitopes. The findings of this study provide a foundation to identify molecular factors that dictate important fiber traits.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491806","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
<p>Rice (<i>Oryza sativa</i>) is the staple crop for more than half the world's population, making yield improvements a critical goal for current breeding efforts. One approach focuses on improving plant architecture, and the tiller angle is a promising trait in this context: a large angle results in a spread-out growth habit that enhances light capture and helps outcompete weeds, while an erect growth habit with a smaller tiller angle allows for dense planting, efficient harvesting and reduces competition between individual plants (Wang et al., 2022). Domestication of wild rice has favoured an erect growth habit, which can be largely attributed to selection for specific alleles of several C2H2 zinc finger transcription factor genes, including <i>PROSTRATE GROWTH 1</i> (<i>PROG1</i>) (Tan et al., <span>2008</span>), <i>PROG7</i> (Hu et al., <span>2018</span>) and <i>RICE PLANT ARCHITECTURE DOMESTICATION</i> (<i>RPAD</i>) (Wu et al., <span>2018</span>).</p><p>These genes also affect shoot gravitropism (Wang, Gao, Liang, Li, & Wang, <span>2022</span>), a process more thoroughly studied in <i>Arabidopsis thaliana</i>. The starch-statolith hypothesis states that the direction of gravity is sensed by the sedimentation of starch-filled amyloplasts (Sack, <span>1997</span>). This sedimentation, possibly sensed by mechanosensitive membranes, activates a signal transduction cascade that results in the asymmetric distribution of the plant hormone auxin across the shoot. High auxin concentrations on the lower side lead to increased cell elongation, causing asymmetric growth and a bending of the shoot (Takahashi et al., <span>2021</span>). Roles for amyloplastic starch granules and asymmetric auxin distribution have also been established in the control of tiller angle in rice, but only a few genes involved in this process are known.</p><p>Lubin Tan's lab at China Agricultural University in Beijing studies the genetic regulation of rice agronomic traits; uncovering the signalling pathways underlying plant architecture thus remains a key area of the group's research. Through an EMS mutagenesis screen, PhD student Jinjian Fan, first author of the highlighted publication, and colleagues identified a mutant with a with a spread-out architecture they named <i>large tiller angle 1</i> (<i>lata1</i>). Throughout development, this mutant consistently exhibited larger tiller angles than the wild type, with the outermost tiller reaching a 25° angle at the heading stage, compared to an 11° angle in the wild type (Figure 1a). This phenotype was caused by reduced asymmetric growth at the tiller base. As for other tiller angle mutants, the change in angle was associated with altered shoot gravitropism: after rotating seedlings 90°, gravitropic bending was visibly delayed in <i>lata1</i> seedlings (Figure 1b).</p><p>Using bulk segregant analysis, the authors mapped the <i>lata1</i> phenotype to a single-nucleotide polymorphism (SNP) in a gene located on chromosome 5 tha
{"title":"A new angle for crop improvement? The RING E3 ubiquitin ligase LATA1 impacts tiller angle in rice","authors":"Martin Balcerowicz","doi":"10.1111/tpj.17069","DOIUrl":"10.1111/tpj.17069","url":null,"abstract":"<p>Rice (<i>Oryza sativa</i>) is the staple crop for more than half the world's population, making yield improvements a critical goal for current breeding efforts. One approach focuses on improving plant architecture, and the tiller angle is a promising trait in this context: a large angle results in a spread-out growth habit that enhances light capture and helps outcompete weeds, while an erect growth habit with a smaller tiller angle allows for dense planting, efficient harvesting and reduces competition between individual plants (Wang et al., 2022). Domestication of wild rice has favoured an erect growth habit, which can be largely attributed to selection for specific alleles of several C2H2 zinc finger transcription factor genes, including <i>PROSTRATE GROWTH 1</i> (<i>PROG1</i>) (Tan et al., <span>2008</span>), <i>PROG7</i> (Hu et al., <span>2018</span>) and <i>RICE PLANT ARCHITECTURE DOMESTICATION</i> (<i>RPAD</i>) (Wu et al., <span>2018</span>).</p><p>These genes also affect shoot gravitropism (Wang, Gao, Liang, Li, & Wang, <span>2022</span>), a process more thoroughly studied in <i>Arabidopsis thaliana</i>. The starch-statolith hypothesis states that the direction of gravity is sensed by the sedimentation of starch-filled amyloplasts (Sack, <span>1997</span>). This sedimentation, possibly sensed by mechanosensitive membranes, activates a signal transduction cascade that results in the asymmetric distribution of the plant hormone auxin across the shoot. High auxin concentrations on the lower side lead to increased cell elongation, causing asymmetric growth and a bending of the shoot (Takahashi et al., <span>2021</span>). Roles for amyloplastic starch granules and asymmetric auxin distribution have also been established in the control of tiller angle in rice, but only a few genes involved in this process are known.</p><p>Lubin Tan's lab at China Agricultural University in Beijing studies the genetic regulation of rice agronomic traits; uncovering the signalling pathways underlying plant architecture thus remains a key area of the group's research. Through an EMS mutagenesis screen, PhD student Jinjian Fan, first author of the highlighted publication, and colleagues identified a mutant with a with a spread-out architecture they named <i>large tiller angle 1</i> (<i>lata1</i>). Throughout development, this mutant consistently exhibited larger tiller angles than the wild type, with the outermost tiller reaching a 25° angle at the heading stage, compared to an 11° angle in the wild type (Figure 1a). This phenotype was caused by reduced asymmetric growth at the tiller base. As for other tiller angle mutants, the change in angle was associated with altered shoot gravitropism: after rotating seedlings 90°, gravitropic bending was visibly delayed in <i>lata1</i> seedlings (Figure 1b).</p><p>Using bulk segregant analysis, the authors mapped the <i>lata1</i> phenotype to a single-nucleotide polymorphism (SNP) in a gene located on chromosome 5 tha","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":"120 2","pages":"427-428"},"PeriodicalIF":6.2,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.17069","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491839","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}
Soil salinization is becoming a great threat that reduces crop productivity worldwide. In this study, we found that rice allantoate amidohydrolase (OsAAH) expression was significantly upregulated by salt stress, and its overexpression conferred salt tolerance at the seedling stage. Compared to wild type (WT), the contents of ureides (allantoin and allantoate) were significantly increased in Osaah mutants and reduced in OsAAH overexpression lines both before and after salt treatments. Exogenous allantoin significantly promoted salt tolerance in OsAAH overexpression, but not in Osaah mutants. Subcellular localization showed that OsAAH was also localized to the peroxisomes in addition to the previously reported endoplasmic reticulum (ER). The differential expression of peroxisome-related genes was identified between Osaah mutants and WT. Furthermore, the contents of H2O2 and malondialdehyde (MDA) were significantly accumulated in Osaah mutants and reduced in OsAAH overexpression lines. The activities of antioxidant enzymes were significantly reduced in Osaah mutants and enhanced in OsAAH overexpression under NaCl treatment. The transcription factor OsABI5 could directly bind to OsAAH promoter and activate OsAAH expression. Our findings reveal that OsAAH could be induced by salt stress through the activation of OsABI5 and then confer salt tolerance by enhancing the scavenging capacity of reactive oxygen species (ROS), which contributes to rice breeding in salt tolerance.
{"title":"OsAAH confers salt tolerance in rice seedlings.","authors":"Ting Xie, Jiangyu Xu, Wenling Hu, Silvtu Shan, Haoming Gao, Jiaxin Shen, Xinyi Chen, Yanxiao Jia, Xiuying Gao, Ji Huang, Hongsheng Zhang, Jinping Cheng","doi":"10.1111/tpj.17091","DOIUrl":"https://doi.org/10.1111/tpj.17091","url":null,"abstract":"<p><p>Soil salinization is becoming a great threat that reduces crop productivity worldwide. In this study, we found that rice allantoate amidohydrolase (OsAAH) expression was significantly upregulated by salt stress, and its overexpression conferred salt tolerance at the seedling stage. Compared to wild type (WT), the contents of ureides (allantoin and allantoate) were significantly increased in Osaah mutants and reduced in OsAAH overexpression lines both before and after salt treatments. Exogenous allantoin significantly promoted salt tolerance in OsAAH overexpression, but not in Osaah mutants. Subcellular localization showed that OsAAH was also localized to the peroxisomes in addition to the previously reported endoplasmic reticulum (ER). The differential expression of peroxisome-related genes was identified between Osaah mutants and WT. Furthermore, the contents of H<sub>2</sub>O<sub>2</sub> and malondialdehyde (MDA) were significantly accumulated in Osaah mutants and reduced in OsAAH overexpression lines. The activities of antioxidant enzymes were significantly reduced in Osaah mutants and enhanced in OsAAH overexpression under NaCl treatment. The transcription factor OsABI5 could directly bind to OsAAH promoter and activate OsAAH expression. Our findings reveal that OsAAH could be induced by salt stress through the activation of OsABI5 and then confer salt tolerance by enhancing the scavenging capacity of reactive oxygen species (ROS), which contributes to rice breeding in salt tolerance.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491825","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Berenice Jiménez-Marín, José A Ortega-Escalante, Antariksh Tyagi, Jundhi Seah, Bradley J S C Olson, Stephen M Miller
Volvox carteri is an excellent system for investigating the origins of cell differentiation because it possesses just two cell types, reproductive gonidia and motile somatic cells, which evolved relatively recently. The somatic phenotype depends on the regA gene, which represses cell growth and reproduction, preventing cells expressing it from growing large enough to become gonidia. regA encodes a putative transcription factor and was generated in an undifferentiated ancestor of V. carteri through duplication of a progenitor gene whose ortholog in V. carteri is named rlsD. Here we analyze the function of rlsD through knockdown, overexpression, and RNA-seq experiments, to gain clues into the function of a member of an understudied putative transcription factor family and to obtain insight into the origins of cell differentiation in the volvocine algae. rlsD knockdown was lethal, while rlsD overexpression dramatically reduced gonidial growth. rlsD overexpression led to differential expression of approximately one-fourth of the genome, with repressed genes biased for those typically overexpressed in gonidia relative to somatic cells, and upregulated genes biased toward expression in soma, where regA expression is high. Notably, rlsD overexpression affects accumulation of transcripts for genes/Pfam domains involved in ribosome biogenesis, photosynthetic light harvesting, and sulfate generation, functions related to organismal growth, and responses to resource availability. We also found that in the wild type, rlsD expression is induced by light deprivation. These findings are consistent with the idea that cell differentiation in V. carteri evolved when a resource-responsive, growth-regulating gene was amplified, and a resulting gene duplicate was co-opted to repress growth in a constitutive, spatial context.
{"title":"Functional analysis of regA paralog rlsD in Volvox carteri.","authors":"Berenice Jiménez-Marín, José A Ortega-Escalante, Antariksh Tyagi, Jundhi Seah, Bradley J S C Olson, Stephen M Miller","doi":"10.1111/tpj.17081","DOIUrl":"https://doi.org/10.1111/tpj.17081","url":null,"abstract":"<p><p>Volvox carteri is an excellent system for investigating the origins of cell differentiation because it possesses just two cell types, reproductive gonidia and motile somatic cells, which evolved relatively recently. The somatic phenotype depends on the regA gene, which represses cell growth and reproduction, preventing cells expressing it from growing large enough to become gonidia. regA encodes a putative transcription factor and was generated in an undifferentiated ancestor of V. carteri through duplication of a progenitor gene whose ortholog in V. carteri is named rlsD. Here we analyze the function of rlsD through knockdown, overexpression, and RNA-seq experiments, to gain clues into the function of a member of an understudied putative transcription factor family and to obtain insight into the origins of cell differentiation in the volvocine algae. rlsD knockdown was lethal, while rlsD overexpression dramatically reduced gonidial growth. rlsD overexpression led to differential expression of approximately one-fourth of the genome, with repressed genes biased for those typically overexpressed in gonidia relative to somatic cells, and upregulated genes biased toward expression in soma, where regA expression is high. Notably, rlsD overexpression affects accumulation of transcripts for genes/Pfam domains involved in ribosome biogenesis, photosynthetic light harvesting, and sulfate generation, functions related to organismal growth, and responses to resource availability. We also found that in the wild type, rlsD expression is induced by light deprivation. These findings are consistent with the idea that cell differentiation in V. carteri evolved when a resource-responsive, growth-regulating gene was amplified, and a resulting gene duplicate was co-opted to repress growth in a constitutive, spatial context.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491822","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Donka Teneva Koleva, Anthony W. Bengochea, Silas B. Mellor, Rocio Ochoa-Fernandez, David R. Nelson, Birger Lindberg Møller, Elizabeth M. J. Gillam, Mette Sørensen
Cytochrome P450 monooxygenases of the CYP79 family catalyze conversion of specific amino acids into oximes feeding into a variety of metabolic plant pathways. Here we present an extensive phylogenetic tree of the CYP79 family built on carefully curated sequences collected across the entire plant kingdom. Based on a monophyletic origin of the P450s, a set of evolutionarily distinct branches was identified. Founded on the functionally characterized CYP79 sequences, sequence features of the individual substrate recognition sites (SRSs) were analyzed. Co-evolving amino acid residues were identified using co-evolutionary sequence analysis. SRS4 possesses a specific sequence pattern when tyrosine is a substrate. Except for the CYP79Cs and CYP79Fs, substrate preferences toward specific amino acids could not be assigned to specific subfamilies. The highly diversified CYP79 tree, reflecting recurrent independent evolution of CYP79s, may relate to the different roles of oximes in different plant species. The sequence differences across individual CYP79 subfamilies may facilitate the in vivo orchestration of channeled metabolic pathways based on altered surface charge domains of the CYP79 protein. Alternatively, they may serve to optimize dynamic interactions with oxime metabolizing enzymes to enable optimal ecological interactions. The outlined detailed curation of the CYP79 sequences used for building the phylogenetic tree made it appropriate to make a conservative phylogenetic tree-based revision of the naming of the sequences within this highly complex cytochrome P450 family. The same approach may be used in other complex P450 subfamilies. The detailed phylogeny of the CYP79 family will enable further exploration of the evolution of function in these enzymes.
{"title":"Sequence diversity in the monooxygenases involved in oxime production in plant defense and signaling: a conservative revision in the nomenclature of the highly complex CYP79 family","authors":"Donka Teneva Koleva, Anthony W. Bengochea, Silas B. Mellor, Rocio Ochoa-Fernandez, David R. Nelson, Birger Lindberg Møller, Elizabeth M. J. Gillam, Mette Sørensen","doi":"10.1111/tpj.17044","DOIUrl":"10.1111/tpj.17044","url":null,"abstract":"<p>Cytochrome P450 monooxygenases of the CYP79 family catalyze conversion of specific amino acids into oximes feeding into a variety of metabolic plant pathways. Here we present an extensive phylogenetic tree of the CYP79 family built on carefully curated sequences collected across the entire plant kingdom. Based on a monophyletic origin of the P450s, a set of evolutionarily distinct branches was identified. Founded on the functionally characterized CYP79 sequences, sequence features of the individual substrate recognition sites (SRSs) were analyzed. Co-evolving amino acid residues were identified using co-evolutionary sequence analysis. SRS4 possesses a specific sequence pattern when tyrosine is a substrate. Except for the CYP79Cs and CYP79Fs, substrate preferences toward specific amino acids could not be assigned to specific subfamilies. The highly diversified CYP79 tree, reflecting recurrent independent evolution of CYP79s, may relate to the different roles of oximes in different plant species. The sequence differences across individual CYP79 subfamilies may facilitate the <i>in vivo</i> orchestration of channeled metabolic pathways based on altered surface charge domains of the CYP79 protein. Alternatively, they may serve to optimize dynamic interactions with oxime metabolizing enzymes to enable optimal ecological interactions. The outlined detailed curation of the CYP79 sequences used for building the phylogenetic tree made it appropriate to make a conservative phylogenetic tree-based revision of the naming of the sequences within this highly complex cytochrome P450 family. The same approach may be used in other complex P450 subfamilies. The detailed phylogeny of the CYP79 family will enable further exploration of the evolution of function in these enzymes.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":"120 3","pages":"1236-1256"},"PeriodicalIF":6.2,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.17044","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142491827","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}
Hongyue Zu, Jing Zhang, Weiwei Bai, Peng Kuai, Jingli Cheng, Jing Lu, Yonggen Lou, Ran Li
Polyamines (PAs) along with their conjugated forms, are important mediators of plant defense mechanisms against both biotic and abiotic stresses. Flavin-containing polyamine oxidases (PAOs) regulate PA levels through terminal oxidation. To date, the role of PAOs in plant-herbivore interaction remains poorly understood. We discovered that infestation by the brown planthopper (BPH) disrupts PA homeostasis within the leaf sheaths of rice plants, which co-occurs with the upregulation of OsPAO6, a tissue-specific inducible, apoplast-localized enzyme that regulates the terminal catabolism of spermidine (Spd) and spermine. Functional analysis using CRISPR-Cas9 genome-edited plants revealed that pao6 mutants accumulated significantly higher levels of Spd and phenylpropanoid-conjugated Spd in response to BPH infestation compared to wild-type controls. In addition, BPH feeding on pao6 mutants led to increased honeydew excretion and plant damage by female adults, consistent with in vitro experiments in which Spd enhanced BPH feeding. Furthermore, OsPAO6 transcription is regulated by jasmonate (JA) signaling, and it is dependent on MYC2, which directly binds to the G-box-like motif in the OsPAO6 promoter. Our findings reveal an important role of OsPAO6 in regulating polyamine catabolism in JA-induced responses triggered by herbivore attacks in rice.
多胺(PA)及其共轭形式是植物抵御生物和非生物胁迫的防御机制的重要介质。含黄素的多胺氧化酶(PAOs)通过末端氧化作用调节多胺的水平。迄今为止,人们对 PAOs 在植物与食草动物相互作用中的作用仍知之甚少。我们发现,褐飞虱(BPH)的侵袭破坏了水稻叶鞘内的 PA 平衡,这与 OsPAO6 的上调同时发生,OsPAO6 是一种组织特异性诱导型、定位在叶绿体的酶,可调节亚精胺(Spd)和精胺的末端分解代谢。利用 CRISPR-Cas9 基因组编辑植物进行的功能分析显示,与野生型对照组相比,pao6 突变体在应对 BPH 侵染时积累的 Spd 和苯丙酮结合的 Spd 水平明显更高。此外,BPH 在 pao6 突变体上的取食会导致雌性成虫排出更多的蜜露和对植物的损害,这与 Spd 会增强 BPH 取食的体外实验是一致的。此外,OsPAO6 的转录受茉莉酸盐(JA)信号的调控,并且依赖于 MYC2,后者直接与 OsPAO6 启动子中的 G-box-like motif 结合。我们的研究结果揭示了 OsPAO6 在调节 JA 诱导的水稻多胺分解反应中的重要作用。
{"title":"Jasmonate-mediated polyamine oxidase 6 drives herbivore-induced polyamine catabolism in rice.","authors":"Hongyue Zu, Jing Zhang, Weiwei Bai, Peng Kuai, Jingli Cheng, Jing Lu, Yonggen Lou, Ran Li","doi":"10.1111/tpj.17094","DOIUrl":"https://doi.org/10.1111/tpj.17094","url":null,"abstract":"<p><p>Polyamines (PAs) along with their conjugated forms, are important mediators of plant defense mechanisms against both biotic and abiotic stresses. Flavin-containing polyamine oxidases (PAOs) regulate PA levels through terminal oxidation. To date, the role of PAOs in plant-herbivore interaction remains poorly understood. We discovered that infestation by the brown planthopper (BPH) disrupts PA homeostasis within the leaf sheaths of rice plants, which co-occurs with the upregulation of OsPAO6, a tissue-specific inducible, apoplast-localized enzyme that regulates the terminal catabolism of spermidine (Spd) and spermine. Functional analysis using CRISPR-Cas9 genome-edited plants revealed that pao6 mutants accumulated significantly higher levels of Spd and phenylpropanoid-conjugated Spd in response to BPH infestation compared to wild-type controls. In addition, BPH feeding on pao6 mutants led to increased honeydew excretion and plant damage by female adults, consistent with in vitro experiments in which Spd enhanced BPH feeding. Furthermore, OsPAO6 transcription is regulated by jasmonate (JA) signaling, and it is dependent on MYC2, which directly binds to the G-box-like motif in the OsPAO6 promoter. Our findings reveal an important role of OsPAO6 in regulating polyamine catabolism in JA-induced responses triggered by herbivore attacks in rice.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454418","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Priyanka Gupta, Anuj Sharma, N R Kiran, T K Pranav Raj, Ram Krishna, Dinesh A Nagegowda
Citral, a naturally occurring acyclic monoterpene aldehyde, is present in the essential oils of various plants, but only a few produce it in abundance. Despite its importance as a key aroma molecule, knowledge regarding the in-planta biosynthesis of citral and its metabolic origin remains limited. Here, we have elucidated the functions of an alcohol dehydrogenase (CfADH1) and an aldoketo-reductase (CfAKR2b) in citral biosynthesis in lemongrass (Cymbopogon flexuosus), one of the most cultivated aromatic crops for its citral-rich essential oil. Expression of both CfADH1 and CfAKR2b showed correlation with citral accumulation in different developmental stages. Recombinant CfADH1 and CfAKR2b, despite their sequence unrelatedness, catalyzed citral formation from geraniol with NADP cofactor. Virus-induced gene silencing in lemongrass and transient expression in lemon balm (Melissa officinalis) demonstrated the in-planta involvement of CfADH1 and CfAKR2b in citral biosynthesis. While CfADH1 exhibited a dual cytosolic/plastidial localization, CfAKR2b was localized to the cytosol. This was supported by higher citral-forming activity in the cytosolic fraction than in the chloroplast fraction of lemongrass leaf extract. Moreover, feeding lemongrass seedlings with inhibitors specific to the cytosolic mevalonate pathway and the plastidial methylerythritol phosphate pathway, combined with volatile profiling, supported the involvement of both pathways in citral formation. Taken together, our results indicate that high citral production has evolved in lemongrass through the recruitment of phylogenetically distant enzymes localized in both the cytosol and plastids.
{"title":"Phylogenetically distant enzymes localized in cytosol and plastids drive citral biosynthesis in lemongrass.","authors":"Priyanka Gupta, Anuj Sharma, N R Kiran, T K Pranav Raj, Ram Krishna, Dinesh A Nagegowda","doi":"10.1111/tpj.17086","DOIUrl":"https://doi.org/10.1111/tpj.17086","url":null,"abstract":"<p><p>Citral, a naturally occurring acyclic monoterpene aldehyde, is present in the essential oils of various plants, but only a few produce it in abundance. Despite its importance as a key aroma molecule, knowledge regarding the in-planta biosynthesis of citral and its metabolic origin remains limited. Here, we have elucidated the functions of an alcohol dehydrogenase (CfADH1) and an aldoketo-reductase (CfAKR2b) in citral biosynthesis in lemongrass (Cymbopogon flexuosus), one of the most cultivated aromatic crops for its citral-rich essential oil. Expression of both CfADH1 and CfAKR2b showed correlation with citral accumulation in different developmental stages. Recombinant CfADH1 and CfAKR2b, despite their sequence unrelatedness, catalyzed citral formation from geraniol with NADP cofactor. Virus-induced gene silencing in lemongrass and transient expression in lemon balm (Melissa officinalis) demonstrated the in-planta involvement of CfADH1 and CfAKR2b in citral biosynthesis. While CfADH1 exhibited a dual cytosolic/plastidial localization, CfAKR2b was localized to the cytosol. This was supported by higher citral-forming activity in the cytosolic fraction than in the chloroplast fraction of lemongrass leaf extract. Moreover, feeding lemongrass seedlings with inhibitors specific to the cytosolic mevalonate pathway and the plastidial methylerythritol phosphate pathway, combined with volatile profiling, supported the involvement of both pathways in citral formation. Taken together, our results indicate that high citral production has evolved in lemongrass through the recruitment of phylogenetically distant enzymes localized in both the cytosol and plastids.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":" ","pages":""},"PeriodicalIF":6.2,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454419","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eugene A. Arifulin, Dmitry V. Sorokin, Nadezhda A. Anoshina, Maria A. Kuznetsova, Anna A. Valyaeva, Daria M. Potashnikova, Denis O. Omelchenko, Veit Schubert, Tatyana D. Kolesnikova, Eugene V. Sheval