Pub Date : 2025-02-10Epub Date: 2024-12-02DOI: 10.1016/j.xplc.2024.101200
Chao-Feng Huang, Yingtang Ma
Aluminum (Al) toxicity poses a significant challenge for plant production on acidic soils, which constitute approximately 30% of the world's ice-free land. To combat Al toxicity, plants have evolved both external and internal detoxification mechanisms. The zinc-finger transcription factor STOP1 (SENSITIVE TO PROTON RHIZOTOXICITY 1) plays a critical and conserved role in Al resistance by inducing genes involved in both external exclusion and internal detoxification mechanisms. Recent studies have uncovered multiple layers of post-transcriptional regulation of STOP1 and have elucidated mechanisms by which plants sense Al and activate signaling cascades that regulate STOP1 function. This review offers a comprehensive overview of the mechanisms through which STOP1 and its homologs confer Al resistance in plants, with a particular focus on Arabidopsis thaliana and rice. Additionally, we discuss recent advances and future perspectives in understanding the post-transcriptional regulation of STOP1, as well as the Al sensing and signaling pathways upstream of STOP1.
{"title":"Aluminum resistance in plants: A critical review focusing on STOP1.","authors":"Chao-Feng Huang, Yingtang Ma","doi":"10.1016/j.xplc.2024.101200","DOIUrl":"10.1016/j.xplc.2024.101200","url":null,"abstract":"<p><p>Aluminum (Al) toxicity poses a significant challenge for plant production on acidic soils, which constitute approximately 30% of the world's ice-free land. To combat Al toxicity, plants have evolved both external and internal detoxification mechanisms. The zinc-finger transcription factor STOP1 (SENSITIVE TO PROTON RHIZOTOXICITY 1) plays a critical and conserved role in Al resistance by inducing genes involved in both external exclusion and internal detoxification mechanisms. Recent studies have uncovered multiple layers of post-transcriptional regulation of STOP1 and have elucidated mechanisms by which plants sense Al and activate signaling cascades that regulate STOP1 function. This review offers a comprehensive overview of the mechanisms through which STOP1 and its homologs confer Al resistance in plants, with a particular focus on Arabidopsis thaliana and rice. Additionally, we discuss recent advances and future perspectives in understanding the post-transcriptional regulation of STOP1, as well as the Al sensing and signaling pathways upstream of STOP1.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101200"},"PeriodicalIF":9.4,"publicationDate":"2025-02-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142774622","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}
Convergent and parallel evolution occur more frequently than previously thought. Here, we focus on the evolutionary adaptations of angiosperms at sub-zero temperatures. We begin by introducing the history of research on convergent and parallel evolution, defining all independent similarities as convergent evolution. Our analysis reveals that frost zones (periodic or constant), which cover 49.1% of Earth's land surface, host 137 angiosperm families, with over 90% of their species thriving in these regions. In this context, we revisit the global biogeography and evolutionary trajectories of plant traits, such as herbaceous form and deciduous leaves, that are thought to be evasion strategies for frost adaptation. At the physiological and molecular levels, many angiosperms have independently evolved cold acclimation mechanisms through multiple pathways in addition to the well-characterized C-repeat binding factor/dehydration-responsive element binding protein 1 (CBF/DREB1) regulatory pathway. These convergent adaptations have occurred across various molecular levels, including amino acid substitutions and changes in gene duplication and expression within the same or similar functional pathways; however, identical amino acid changes are rare. Our results also highlight the prevalence of polyploidy in frost zones and the occurrence of paleopolyploidization events during global cooling. These patterns suggest repeated evolution in cold climates. Finally, we discuss plant domestication and predict climate zone shifts due to global warming and their effects on plant migration and in situ adaptation. Overall, the integration of ecological and molecular perspectives is essential for understanding and forecasting plant responses to climate change.
{"title":"Convergent evolution in angiosperms adapted to cold climates.","authors":"Shuo Wang, Jing Li, Ping Yu, Liangyu Guo, Junhui Zhou, Jian Yang, Wenwu Wu","doi":"10.1016/j.xplc.2025.101258","DOIUrl":"10.1016/j.xplc.2025.101258","url":null,"abstract":"<p><p>Convergent and parallel evolution occur more frequently than previously thought. Here, we focus on the evolutionary adaptations of angiosperms at sub-zero temperatures. We begin by introducing the history of research on convergent and parallel evolution, defining all independent similarities as convergent evolution. Our analysis reveals that frost zones (periodic or constant), which cover 49.1% of Earth's land surface, host 137 angiosperm families, with over 90% of their species thriving in these regions. In this context, we revisit the global biogeography and evolutionary trajectories of plant traits, such as herbaceous form and deciduous leaves, that are thought to be evasion strategies for frost adaptation. At the physiological and molecular levels, many angiosperms have independently evolved cold acclimation mechanisms through multiple pathways in addition to the well-characterized C-repeat binding factor/dehydration-responsive element binding protein 1 (CBF/DREB1) regulatory pathway. These convergent adaptations have occurred across various molecular levels, including amino acid substitutions and changes in gene duplication and expression within the same or similar functional pathways; however, identical amino acid changes are rare. Our results also highlight the prevalence of polyploidy in frost zones and the occurrence of paleopolyploidization events during global cooling. These patterns suggest repeated evolution in cold climates. Finally, we discuss plant domestication and predict climate zone shifts due to global warming and their effects on plant migration and in situ adaptation. Overall, the integration of ecological and molecular perspectives is essential for understanding and forecasting plant responses to climate change.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101258"},"PeriodicalIF":9.4,"publicationDate":"2025-02-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143030316","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}
Pub Date : 2025-01-31DOI: 10.1016/j.xplc.2025.101265
Jiawei Pei, Zheng Wang, Yanfang Heng, Zhuo Chen, Ke Wang, Qingmeng Xiao, Jian Li, Zhaorong Hu, Hang He, Ying Cao, Xingguo Ye, Xing Wang Deng, Zhijin Liu, Ligeng Ma
Grain color is a key agronomic trait that greatly determines food quality. Elucidating the molecular and evolutionary mechanism underlying grain color regulation is also an important question in evolutionary biology and crop breeding. Here, we confirm that both bHLH and MYB play a critical role in controlling grain color evolution in Triticeae. Blue grain is the ancestral trait, while white grain caused by dysfunctions of bHLH or MYB is the derived trait in Triticeae. HvbHLH1 and HvMYB1 are the targets of selection in barley, and dysfunctionalized by deletion(s), insertion(s) and point mutation(s) in vast majority of Triticeae species accompanied by the alteration from blue grain to white grain. Wheat with white grain exhibits high seed vigor under stresses. Artificial co-expressions of ThbHLH1 and ThMYB1 in grain endosperm and aleurone layer generates color grains with health benefits and is used in a new hybrid breeding technology in wheat, respectively. Therefore, our study reveals that white grain might be a favorable derived trait and kept through natural/artificial selection in Triticeae, and ancient blue grain could be regained and reused in the modern technology of molecular breeding in modern wheat.
{"title":"Selection of dysfunctional alleles of bHLH1 and MYB1 genes produces white grain in the tribe Triticeae.","authors":"Jiawei Pei, Zheng Wang, Yanfang Heng, Zhuo Chen, Ke Wang, Qingmeng Xiao, Jian Li, Zhaorong Hu, Hang He, Ying Cao, Xingguo Ye, Xing Wang Deng, Zhijin Liu, Ligeng Ma","doi":"10.1016/j.xplc.2025.101265","DOIUrl":"https://doi.org/10.1016/j.xplc.2025.101265","url":null,"abstract":"<p><p>Grain color is a key agronomic trait that greatly determines food quality. Elucidating the molecular and evolutionary mechanism underlying grain color regulation is also an important question in evolutionary biology and crop breeding. Here, we confirm that both bHLH and MYB play a critical role in controlling grain color evolution in Triticeae. Blue grain is the ancestral trait, while white grain caused by dysfunctions of bHLH or MYB is the derived trait in Triticeae. HvbHLH1 and HvMYB1 are the targets of selection in barley, and dysfunctionalized by deletion(s), insertion(s) and point mutation(s) in vast majority of Triticeae species accompanied by the alteration from blue grain to white grain. Wheat with white grain exhibits high seed vigor under stresses. Artificial co-expressions of ThbHLH1 and ThMYB1 in grain endosperm and aleurone layer generates color grains with health benefits and is used in a new hybrid breeding technology in wheat, respectively. Therefore, our study reveals that white grain might be a favorable derived trait and kept through natural/artificial selection in Triticeae, and ancient blue grain could be regained and reused in the modern technology of molecular breeding in modern wheat.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101265"},"PeriodicalIF":9.4,"publicationDate":"2025-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143076555","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}
Pub Date : 2025-01-28DOI: 10.1016/j.xplc.2025.101264
Siyuan Liu, Qiongli Wang, Ming Zhong, Guifang Lin, Meiling Ye, Youren Wang, Jing Zhang, Qin Wang
High-temperature stress, also referred to as heat stress, often has detrimental effects on plant growth and development. Phytochromes have been implicated in regulating plant heat stress responses, but the role of blue-light receptors, such as cryptochromes, in plant blue light-dependent heat stress response has remained unclear. We found that the blue light receptor cryptochrome 1 (CRY1) negatively regulates heat stress tolerance (thermotolerance) in Arabidopsis. Heat stress represses CRY1 phosphorylation. Unphosphorylated CRY1 exhibits decreased activity suppressing CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) and ELONGATED HYPOCOTYL 5 (HY5) interaction, leading to the excessive degradation of HY5 under heat stress in blue light. This reduction in HY5 protein levels subsequently relieves its repression on the transcription of HY5 target genes, especially the heat shock transcription factors (HSFs). Our study unveils a novel mechanism by which CRY1-mediated blue-light signaling suppresses plant thermotolerance and highlights the dual function of CRY1-COP1-HY5 module in both light and heat stress signaling, providing insights on how heat stress and light signals integrate to optimize plant survival under heat stress.
{"title":"The CRY1-COP1-HY5 axis mediates blue-light regulation of Arabidopsis thermotolerance.","authors":"Siyuan Liu, Qiongli Wang, Ming Zhong, Guifang Lin, Meiling Ye, Youren Wang, Jing Zhang, Qin Wang","doi":"10.1016/j.xplc.2025.101264","DOIUrl":"https://doi.org/10.1016/j.xplc.2025.101264","url":null,"abstract":"<p><p>High-temperature stress, also referred to as heat stress, often has detrimental effects on plant growth and development. Phytochromes have been implicated in regulating plant heat stress responses, but the role of blue-light receptors, such as cryptochromes, in plant blue light-dependent heat stress response has remained unclear. We found that the blue light receptor cryptochrome 1 (CRY1) negatively regulates heat stress tolerance (thermotolerance) in Arabidopsis. Heat stress represses CRY1 phosphorylation. Unphosphorylated CRY1 exhibits decreased activity suppressing CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) and ELONGATED HYPOCOTYL 5 (HY5) interaction, leading to the excessive degradation of HY5 under heat stress in blue light. This reduction in HY5 protein levels subsequently relieves its repression on the transcription of HY5 target genes, especially the heat shock transcription factors (HSFs). Our study unveils a novel mechanism by which CRY1-mediated blue-light signaling suppresses plant thermotolerance and highlights the dual function of CRY1-COP1-HY5 module in both light and heat stress signaling, providing insights on how heat stress and light signals integrate to optimize plant survival under heat stress.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101264"},"PeriodicalIF":9.4,"publicationDate":"2025-01-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143069608","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}
Pub Date : 2025-01-27DOI: 10.1016/j.xplc.2025.101262
Andrea Lepri, Hira Kazmi, Gaia Bertolotti, Chiara Longo, Sara Occhigrossi, Luca Quattrocchi, Mirko De Vivo, Daria Scintu, Noemi Svolacchia, Danuse Tarkowska, Veronika Tureckova, Miroslav Strnad, Marta Del Bianco, Riccardo di Mambro, Paolo Costantino, Sabrina Sabatini, Raffaele Dello Ioio, Paola Vittorioso
Plants evolved several strategies to cope with the ever-changing environment. One example of this is given by seed germination, which must occur when environmental conditions are suitable for plant life. In the model system Arabidopsis thaliana seed germination is induced by light; however in nature, seeds of several plant species can germinate regardless of this stimulus. Whereas the molecular mechanisms triggered by light for seed germination are well understood, the ones permitting plants to germinate in the dark are still vague mostly due to the lack of suitable model systems. Here we employ Cardamine hirsuta, a close Arabidopsis relative, as a powerful model system to uncover the molecular mechanisms underlying light-independent germination. Comparing Cardamine and Arabidopsis we show that the maintenance of the pro-germination hormone Gibberellin (GA) levels prompt Cardamine seeds to germinate in dark and light conditions. Via genetic and molecular biology experiments, we show that the Cardamine DOF transcriptional repressor DOF AFFECTING GERMINATION 1 (ChDAG1), homologous to the Arabidopsis DAG1 transcription factor, is involved in this process functioning to mitigate GA levels via negative regulation of ChGA3OX1 and ChGA3OX2 gibberellin biosynthetic genes, independently of light conditions. We also demonstrate that this mechanism is likely to be conserved in other Brassica species capable of germinating in dark conditions, such as Lepidium sativum and Camelina sativa. Our data support the proposal that Cardamine is a new model system suitable for light-independent germination studies. Exploiting this system we also resolved a long-time question about the mechanisms controlling the light-independent germination in plants, opening new frontiers for future studies.
{"title":"A DOF transcriptional repressor-gibberellin feedback loop plays a crucial role in modulating light-independent seed germination.","authors":"Andrea Lepri, Hira Kazmi, Gaia Bertolotti, Chiara Longo, Sara Occhigrossi, Luca Quattrocchi, Mirko De Vivo, Daria Scintu, Noemi Svolacchia, Danuse Tarkowska, Veronika Tureckova, Miroslav Strnad, Marta Del Bianco, Riccardo di Mambro, Paolo Costantino, Sabrina Sabatini, Raffaele Dello Ioio, Paola Vittorioso","doi":"10.1016/j.xplc.2025.101262","DOIUrl":"https://doi.org/10.1016/j.xplc.2025.101262","url":null,"abstract":"<p><p>Plants evolved several strategies to cope with the ever-changing environment. One example of this is given by seed germination, which must occur when environmental conditions are suitable for plant life. In the model system Arabidopsis thaliana seed germination is induced by light; however in nature, seeds of several plant species can germinate regardless of this stimulus. Whereas the molecular mechanisms triggered by light for seed germination are well understood, the ones permitting plants to germinate in the dark are still vague mostly due to the lack of suitable model systems. Here we employ Cardamine hirsuta, a close Arabidopsis relative, as a powerful model system to uncover the molecular mechanisms underlying light-independent germination. Comparing Cardamine and Arabidopsis we show that the maintenance of the pro-germination hormone Gibberellin (GA) levels prompt Cardamine seeds to germinate in dark and light conditions. Via genetic and molecular biology experiments, we show that the Cardamine DOF transcriptional repressor DOF AFFECTING GERMINATION 1 (ChDAG1), homologous to the Arabidopsis DAG1 transcription factor, is involved in this process functioning to mitigate GA levels via negative regulation of ChGA3OX1 and ChGA3OX2 gibberellin biosynthetic genes, independently of light conditions. We also demonstrate that this mechanism is likely to be conserved in other Brassica species capable of germinating in dark conditions, such as Lepidium sativum and Camelina sativa. Our data support the proposal that Cardamine is a new model system suitable for light-independent germination studies. Exploiting this system we also resolved a long-time question about the mechanisms controlling the light-independent germination in plants, opening new frontiers for future studies.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101262"},"PeriodicalIF":9.4,"publicationDate":"2025-01-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143061451","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}
UDP-glycosyltransferases (UGTs) constitute the largest glycosyltransferase family in the plant kingdom. They are responsible for transferring sugar moieties onto various small molecules to control many metabolic processes. However, their physiological significance in plants is largely unknown. Here, we revealed the function and mechanism of two Arabidopsis UGT genes, UGT73C3 and UGT73C4, which can be strongly induced by Pseudomonas syringae pv. tomato DC3000. Their overexpression significantly enhanced plant immune response, while the loss of their functions in double mutants resulted in the more sensitive phenotype to pathogen infection, although their single mutants had no obvious alteration in pathogen resistance. To understand the regulatory mechanism of UGT3C3/C4 in plant immunity, a completely secondary metabolome analysis and glycoside quantification were conducted. More accumulation of pinoresinol diglucosides was revealed in the UGT73C3 and UGT73C4 overexpression lines than that in wild-type plants whether before or after Pst DC3000 treatment, whereas the double mutants accumulated less pinoresinol diglucosides. Further, the in vitro and in vivo experiments demonstrated that UGT73C3 and UGT73C4 were capable of glycosylating pinoresinol to form pinoresinol monoglucoside and diglucoside. Moreover, we found that pinoresinol glycosylation promoted plant immune response by enhancing ROS production and callose deposition. Additionally, the transcriptional factor HB34 was identified to be responsible for the activation of UGT73C3 and UGT73C4 transcription and play a key role in plant immune responses. Overall, this study revealed a new pathway of plant immune responses via UGT73C3/C4 mediated pinoresinol glycosylation under the HB34 regulation.
{"title":"Two pathogen-inducible UDP-glycosyltransferases, UGT73C3 and UGT73C4, catalyze the glycosylation of pinoresinol to promote plant immunity in Arabidopsis.","authors":"Shuman Zhao, Guangrui Dong, Chonglin Liu, Yi Ding, Yuqing Ma, Xinmei Ma, Xianqin Yang, Lijing Liu, Bingkai Hou","doi":"10.1016/j.xplc.2025.101261","DOIUrl":"https://doi.org/10.1016/j.xplc.2025.101261","url":null,"abstract":"<p><p>UDP-glycosyltransferases (UGTs) constitute the largest glycosyltransferase family in the plant kingdom. They are responsible for transferring sugar moieties onto various small molecules to control many metabolic processes. However, their physiological significance in plants is largely unknown. Here, we revealed the function and mechanism of two Arabidopsis UGT genes, UGT73C3 and UGT73C4, which can be strongly induced by Pseudomonas syringae pv. tomato DC3000. Their overexpression significantly enhanced plant immune response, while the loss of their functions in double mutants resulted in the more sensitive phenotype to pathogen infection, although their single mutants had no obvious alteration in pathogen resistance. To understand the regulatory mechanism of UGT3C3/C4 in plant immunity, a completely secondary metabolome analysis and glycoside quantification were conducted. More accumulation of pinoresinol diglucosides was revealed in the UGT73C3 and UGT73C4 overexpression lines than that in wild-type plants whether before or after Pst DC3000 treatment, whereas the double mutants accumulated less pinoresinol diglucosides. Further, the in vitro and in vivo experiments demonstrated that UGT73C3 and UGT73C4 were capable of glycosylating pinoresinol to form pinoresinol monoglucoside and diglucoside. Moreover, we found that pinoresinol glycosylation promoted plant immune response by enhancing ROS production and callose deposition. Additionally, the transcriptional factor HB34 was identified to be responsible for the activation of UGT73C3 and UGT73C4 transcription and play a key role in plant immune responses. Overall, this study revealed a new pathway of plant immune responses via UGT73C3/C4 mediated pinoresinol glycosylation under the HB34 regulation.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101261"},"PeriodicalIF":9.4,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143043330","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}
Pub Date : 2025-01-21DOI: 10.1016/j.xplc.2025.101257
Chen-Xiao Zhao, Yuan-Feng Yan, Li-Xiao Zhao, Xue Tang, Yue-Gui Chen, Wen-Jun Song, Li-Ping Long, Jing Chen, Chun-Lin Tan, Qiao-Zhuo Zhang, Xiu-Lan Pu, Qin-Qin Shen, Yu-Zhou Fan, Yang Tao, Xiao Ye, Sheng-Hong Li, Yan Liu
Steroidal saponins in Paris polyphylla featuring complicated sugar chains exhibit notable biological activities, but the sugar chain biosynthesis is still not fully understood. Here, we identified a 4'-O-rhamnosyltransferase (UGT73DY2) from P. polyphylla, which catalyzes the 4'-O-rhamnosylation of polyphyllins V and VI, producing dioscin and pennogenin 3-O-β-chacotrioside, respectively. UGT73DY2 exhibits strict substrate specificity towards steroidal diglycosides and UDP-Rha, and a new steroidal triglycoside was synthesized through enzyme catalysis. A mutation library was generated based on semi-rational design, identifying three mutants, I358T, A342V, and A132T, which displayed approximately two-fold enhanced enzyme activity. Molecular dynamics simulations revealed that shortened distances between the 4'-OH group of sugar acceptor and either the crucial residue H20 or the donor UDP-Rha contributed to the enhanced enzyme activity. Moreover, subcellular localization analysis of UGT73DY2 and other biosynthetic enzymes indicated that dioscin biosynthesis predominantly occurred in the endoplasmic reticulum of plant cells. By co-expressing 14 biosynthetic genes in Nicotiana benthamiana, optimizing HMGR subcellular localization and CYP450 gene sets, and engineering UGT73DY2, we successfully established a dioscin biosynthesis system with a yield of 3.12 ± 0.11 μg/g dry weight. This study not only uncovers the 4'-O-rhamnosylation process in steroidal saponin biosynthesis, but also presents an alternative approach for the production of steroidal saponins in P. polyphylla through synthetic biology and metabolic engineering.
{"title":"Characterization of a 4'-O-rhamnosyltransferase and de novo biosynthesis of bioactive steroidal triglycosides from Paris polyphylla.","authors":"Chen-Xiao Zhao, Yuan-Feng Yan, Li-Xiao Zhao, Xue Tang, Yue-Gui Chen, Wen-Jun Song, Li-Ping Long, Jing Chen, Chun-Lin Tan, Qiao-Zhuo Zhang, Xiu-Lan Pu, Qin-Qin Shen, Yu-Zhou Fan, Yang Tao, Xiao Ye, Sheng-Hong Li, Yan Liu","doi":"10.1016/j.xplc.2025.101257","DOIUrl":"https://doi.org/10.1016/j.xplc.2025.101257","url":null,"abstract":"<p><p>Steroidal saponins in Paris polyphylla featuring complicated sugar chains exhibit notable biological activities, but the sugar chain biosynthesis is still not fully understood. Here, we identified a 4'-O-rhamnosyltransferase (UGT73DY2) from P. polyphylla, which catalyzes the 4'-O-rhamnosylation of polyphyllins V and VI, producing dioscin and pennogenin 3-O-β-chacotrioside, respectively. UGT73DY2 exhibits strict substrate specificity towards steroidal diglycosides and UDP-Rha, and a new steroidal triglycoside was synthesized through enzyme catalysis. A mutation library was generated based on semi-rational design, identifying three mutants, I358T, A342V, and A132T, which displayed approximately two-fold enhanced enzyme activity. Molecular dynamics simulations revealed that shortened distances between the 4'-OH group of sugar acceptor and either the crucial residue H20 or the donor UDP-Rha contributed to the enhanced enzyme activity. Moreover, subcellular localization analysis of UGT73DY2 and other biosynthetic enzymes indicated that dioscin biosynthesis predominantly occurred in the endoplasmic reticulum of plant cells. By co-expressing 14 biosynthetic genes in Nicotiana benthamiana, optimizing HMGR subcellular localization and CYP450 gene sets, and engineering UGT73DY2, we successfully established a dioscin biosynthesis system with a yield of 3.12 ± 0.11 μg/g dry weight. This study not only uncovers the 4'-O-rhamnosylation process in steroidal saponin biosynthesis, but also presents an alternative approach for the production of steroidal saponins in P. polyphylla through synthetic biology and metabolic engineering.</p>","PeriodicalId":52373,"journal":{"name":"Plant Communications","volume":" ","pages":"101257"},"PeriodicalIF":9.4,"publicationDate":"2025-01-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143025742","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}