Key message: SiDVLs inhibit auxin signaling to regulate root growth by enhancing the expression of Aux/IAAs and reducing the protein accumulation of PINs. The DEVIL/ ROTUNDIFOLIA (DVL/RTFL), a small polypeptide family, is conserved in seed plants and important in regulating plant growth and development. However, the molecular mechanisms remain largely unknown. Here, 27 SiDVLs were identified in foxtail millet genome. Overexpression of three SiDVLs in Arabidopsis (Arabidopsis thaliana) strongly repressed the plant growth, especially the root growth. We demonstrate that overexpression of SiDVLs enhances Auxin/Indole-3-Acetic Acids (Aux/IAAs) transcription, thereby weakening auxin signaling in the roots. Furthermore, SiDVLs reduced the protein levels of the auxin transporters PIN-formed 1 (PIN1), PIN2, and PIN7 in the roots. The impaired auxin signaling reduces the cell division and elongation. In conclusion, SiDVLs suppress cell division and elongation in root by inhibiting auxin signaling and transport, which lead to the reduced root growth.
{"title":"Small peptide SiDVL/RTFLs from foxtail millet inhibit root growth through repressing auxin signaling in transgenic Arabidopsis.","authors":"Chunyan Wang, Tongtong Wang, Miao Liu, Shizhong Zhang, Changai Wu","doi":"10.1007/s00299-024-03360-2","DOIUrl":"10.1007/s00299-024-03360-2","url":null,"abstract":"<p><strong>Key message: </strong>SiDVLs inhibit auxin signaling to regulate root growth by enhancing the expression of Aux/IAAs and reducing the protein accumulation of PINs. The DEVIL/ ROTUNDIFOLIA (DVL/RTFL), a small polypeptide family, is conserved in seed plants and important in regulating plant growth and development. However, the molecular mechanisms remain largely unknown. Here, 27 SiDVLs were identified in foxtail millet genome. Overexpression of three SiDVLs in Arabidopsis (Arabidopsis thaliana) strongly repressed the plant growth, especially the root growth. We demonstrate that overexpression of SiDVLs enhances Auxin/Indole-3-Acetic Acids (Aux/IAAs) transcription, thereby weakening auxin signaling in the roots. Furthermore, SiDVLs reduced the protein levels of the auxin transporters PIN-formed 1 (PIN1), PIN2, and PIN7 in the roots. The impaired auxin signaling reduces the cell division and elongation. In conclusion, SiDVLs suppress cell division and elongation in root by inhibiting auxin signaling and transport, which lead to the reduced root growth.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"268"},"PeriodicalIF":5.3,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472870","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Key message: A plant growth regulator, 5-aminolevulinic acid, enhanced the saline-alkali tolerance via photosynthetic, oxidative-reduction, and glutathione metabolism pathways in pepper seedlings. Saline-alkali stress is a prominent environmental problem, hindering growth and development of pepper. 5-Aminolevulinic acid (ALA) application effectively improves plant growth status under various abiotic stresses. Here, we evaluated morphological, physiological, and transcriptomic differences in saline-alkali-stressed pepper seedlings after ALA application to explore the impact of ALA on saline-alkali stress. The results indicated that saline-alkali stress inhibited plant growth, decreased biomass and photosynthesis, altered the osmolyte content and antioxidant system, and increased reactive oxygen species (ROS) accumulation and proline content in pepper seedlings. Conversely, the application of exogenous ALA alleviated this damage by increasing the photosynthetic rate, osmolyte content, antioxidant enzyme activity, and antioxidants, including superoxide dismutase, catalase, glutathione reductase, and glutathione peroxidase, and reducing glutathione to reduce ROS accumulation and malonaldehyde content. Moreover, the transcriptomic analysis revealed the differentially expressed genes were mainly associated with photosynthesis, oxidation-reduction process, and glutathione metabolism in saline-alkali stress + ALA treatment compared to saline-alkali treatment. Among them, the change in expression level in CaGST, CaGR, and CaGPX was close to the variation of corresponding enzyme activity. Collectively, our findings revealed the alleviating effect of ALA on saline-alkali stress in pepper seedlings, broadening the application of ALA and providing a feasible strategy for utilize saline-alkali soil.
关键信息植物生长调节剂5-氨基乙酰丙酸可通过光合作用、氧化还原和谷胱甘肽代谢途径增强辣椒幼苗的耐盐碱能力。盐碱胁迫是阻碍辣椒生长发育的一个突出环境问题。施用 5-氨基乙酰丙酸(ALA)能有效改善各种非生物胁迫下的植物生长状况。在此,我们评估了施用ALA后盐碱胁迫辣椒幼苗的形态、生理和转录组差异,以探讨ALA对盐碱胁迫的影响。结果表明,盐碱胁迫抑制了辣椒幼苗的生长,降低了生物量和光合作用,改变了渗透溶质含量和抗氧化系统,增加了活性氧(ROS)积累和脯氨酸含量。相反,施用外源 ALA 可通过提高光合速率、渗透压含量、抗氧化酶活性和抗氧化剂(包括超氧化物歧化酶、过氧化氢酶、谷胱甘肽还原酶和谷胱甘肽过氧化物酶)以及还原谷胱甘肽来减少 ROS 积累和丙二醛含量,从而减轻这种损害。此外,转录组分析表明,与盐碱胁迫处理相比,盐碱胁迫+ALA处理的差异表达基因主要与光合作用、氧化还原过程和谷胱甘肽代谢有关。其中,CaGST、CaGR和CaGPX的表达水平变化与相应酶活性的变化接近。综上所述,我们的研究结果揭示了ALA对辣椒幼苗盐碱胁迫的缓解作用,拓宽了ALA的应用范围,为盐碱地的利用提供了可行的策略。
{"title":"Exogenous 5-aminolevulinic acid enhanced saline-alkali tolerance in pepper seedlings by regulating photosynthesis, oxidative damage, and glutathione metabolism.","authors":"Xueting Wang, Sizhen Yang, Baixue Li, Chunlin Chen, Jinling Li, Yichao Wang, Qingjie Du, Meng Li, Hu Wang, Juanqi Li, Jiqing Wang, HuaiJuan Xiao","doi":"10.1007/s00299-024-03352-2","DOIUrl":"10.1007/s00299-024-03352-2","url":null,"abstract":"<p><strong>Key message: </strong>A plant growth regulator, 5-aminolevulinic acid, enhanced the saline-alkali tolerance via photosynthetic, oxidative-reduction, and glutathione metabolism pathways in pepper seedlings. Saline-alkali stress is a prominent environmental problem, hindering growth and development of pepper. 5-Aminolevulinic acid (ALA) application effectively improves plant growth status under various abiotic stresses. Here, we evaluated morphological, physiological, and transcriptomic differences in saline-alkali-stressed pepper seedlings after ALA application to explore the impact of ALA on saline-alkali stress. The results indicated that saline-alkali stress inhibited plant growth, decreased biomass and photosynthesis, altered the osmolyte content and antioxidant system, and increased reactive oxygen species (ROS) accumulation and proline content in pepper seedlings. Conversely, the application of exogenous ALA alleviated this damage by increasing the photosynthetic rate, osmolyte content, antioxidant enzyme activity, and antioxidants, including superoxide dismutase, catalase, glutathione reductase, and glutathione peroxidase, and reducing glutathione to reduce ROS accumulation and malonaldehyde content. Moreover, the transcriptomic analysis revealed the differentially expressed genes were mainly associated with photosynthesis, oxidation-reduction process, and glutathione metabolism in saline-alkali stress + ALA treatment compared to saline-alkali treatment. Among them, the change in expression level in CaGST, CaGR, and CaGPX was close to the variation of corresponding enzyme activity. Collectively, our findings revealed the alleviating effect of ALA on saline-alkali stress in pepper seedlings, broadening the application of ALA and providing a feasible strategy for utilize saline-alkali soil.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"267"},"PeriodicalIF":5.3,"publicationDate":"2024-10-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472867","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Key message: Desiccation-stage transcription factors perform similar functions, with early ones focused on desiccation tolerance and later ones on development. Gene networks governing late embryo development diverge between soybean and Arabidopsis. To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis. Our studies provide new information on the biological processes and gene networks underlying development from embryonic morphogenesis to post-germination.
{"title":"Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination.","authors":"Yen-Ching Wang, Wei-Hsun Hsieh, Liang-Peng Lin, Meng-Hsun He, Ya-Ting Jhan, Chu-Jun Huang, Junpeng Zhan, Ching-Chun Chang, Tzung-Fu Hsieh, Jer-Young Lin","doi":"10.1007/s00299-024-03354-0","DOIUrl":"10.1007/s00299-024-03354-0","url":null,"abstract":"<p><strong>Key message: </strong>Desiccation-stage transcription factors perform similar functions, with early ones focused on desiccation tolerance and later ones on development. Gene networks governing late embryo development diverge between soybean and Arabidopsis. To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis. Our studies provide new information on the biological processes and gene networks underlying development from embryonic morphogenesis to post-germination.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"266"},"PeriodicalIF":5.3,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11489296/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472866","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-17DOI: 10.1007/s00299-024-03353-1
Shixiong Lu, Min Li, Yongjuan Cheng, Huimin Gou, Lili Che, Guoping Liang, Juan Mao
Key message: Twenty-five VvIAA genes and eighteen VaIAA genes were identified from Pinot Noir and Shanputao, respectively. The overexpression of VaIAA3 in transgenic Arabidopsis increased cold tolerance by regulating auxin, ABA and ethylene signaling. Aux/IAA genes are key genes involved in regulating auxin signal transduction in plants. Although IAA genes have been characterized in various plant species, the role of IAA genes in grape cold resistance is unclear. To further explore the members of the Aux/IAA gene family in grape and their functions, in this study, using genomic data for Pinot Noir (Vitis vinifera cv. 'Pinot Noir') and Shanputao (Vitis amurensis), 25 VvIAA genes and 18 VaIAA genes were identified. The VaIAA genes presented different expression patterns at five different temperatures (28 ± 1 °C, 5 ± 1 °C, 0 ± 1 °C, -5 ± 1 °C, and -10 ± 1 °C) according to qRT‑PCR results. VaIAA3 was selected as a candidate gene for further functional analysis because of its high expression level under low-temperature stress. Subcellular localization experiments revealed that VaIAA3 was localized in the nucleus. Additionally, under 4 °C treatment for 24 h, relative expression level of VaIAA3, antioxidant enzyme activity, survival rate, and cold-responsive gene expression in three transgenic lines (OE-1, OE-2, OE-3) were greater, whereas relative electrolytic conductivity (REC), malondialdehyde (MDA) content and hydrogen peroxide (H2O2) content were lower than those of the wild type (WT). Transcriptome sequencing analysis revealed that VaIAA3 regulated cold stress resistance in Arabidopsis thaliana (Arabidopsis) through pathways involving auxin, ABA, JA, or ethylene. Importantly, heterologous overexpression of VaIAA3 increased the resistance of Arabidopsis to cold stress, which provides a theoretical basis for the further use of VaIAA3 to improve cold resistance in grape.
{"title":"Genome-wide identification of Aux/IAA gene family members in grape and functional analysis of VaIAA3 in response to cold stress.","authors":"Shixiong Lu, Min Li, Yongjuan Cheng, Huimin Gou, Lili Che, Guoping Liang, Juan Mao","doi":"10.1007/s00299-024-03353-1","DOIUrl":"10.1007/s00299-024-03353-1","url":null,"abstract":"<p><strong>Key message: </strong>Twenty-five VvIAA genes and eighteen VaIAA genes were identified from Pinot Noir and Shanputao, respectively. The overexpression of VaIAA3 in transgenic Arabidopsis increased cold tolerance by regulating auxin, ABA and ethylene signaling. Aux/IAA genes are key genes involved in regulating auxin signal transduction in plants. Although IAA genes have been characterized in various plant species, the role of IAA genes in grape cold resistance is unclear. To further explore the members of the Aux/IAA gene family in grape and their functions, in this study, using genomic data for Pinot Noir (Vitis vinifera cv. 'Pinot Noir') and Shanputao (Vitis amurensis), 25 VvIAA genes and 18 VaIAA genes were identified. The VaIAA genes presented different expression patterns at five different temperatures (28 ± 1 °C, 5 ± 1 °C, 0 ± 1 °C, -5 ± 1 °C, and -10 ± 1 °C) according to qRT‑PCR results. VaIAA3 was selected as a candidate gene for further functional analysis because of its high expression level under low-temperature stress. Subcellular localization experiments revealed that VaIAA3 was localized in the nucleus. Additionally, under 4 °C treatment for 24 h, relative expression level of VaIAA3, antioxidant enzyme activity, survival rate, and cold-responsive gene expression in three transgenic lines (OE-1, OE-2, OE-3) were greater, whereas relative electrolytic conductivity (REC), malondialdehyde (MDA) content and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) content were lower than those of the wild type (WT). Transcriptome sequencing analysis revealed that VaIAA3 regulated cold stress resistance in Arabidopsis thaliana (Arabidopsis) through pathways involving auxin, ABA, JA, or ethylene. Importantly, heterologous overexpression of VaIAA3 increased the resistance of Arabidopsis to cold stress, which provides a theoretical basis for the further use of VaIAA3 to improve cold resistance in grape.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"265"},"PeriodicalIF":5.3,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472869","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Reactive oxygen species (ROS) and reactive nitrogen species (RNS) are critical for plant development as well as for its stress response. They can function as signaling molecules to orchestrate a well-defined response of plants to biotic stress. These responses are further fine-tuned by phytohormones, such as salicylic acid, jasmonic acid, and ethylene, to modulate immune response. In the past decades, the intricacies of redox and phytohormonal signaling have been uncovered during plant-pathogen interactions. This review explores the dynamic interplay of these components, elucidating their roles in perceiving biotic threats and shaping the plant's defense strategy. Molecular regulators and sites of oxidative burst have been explored during pathogen perception. Further, the interplay between various components of redox and phytohormonal signaling has been explored during bacterial, fungal, viral, and nematode infections as well as during insect pest infestation. Understanding these interactions highlights gaps in the current knowledge and provides insights into engineering crop varieties with enhanced resistance to pathogens and pests. This review also highlights potential applications of manipulating regulators of redox signaling to bolster plant immunity and ensure global food security. Future research should explore regulators of these signaling pathways as potential target to develop biotic stress-tolerant crops. Further insights are also needed into roles of endophytes and host microbiome modulating host ROS and RNS pool for exploiting them as biocontrol agents imparting resistance against pathogens in plants.
{"title":"The molecular dynamics between reactive oxygen species (ROS), reactive nitrogen species (RNS) and phytohormones in plant's response to biotic stress.","authors":"Krishna Gogoi, Hunmoyna Gogoi, Manashi Borgohain, Ratul Saikia, Channakeshavaiah Chikkaputtaiah, Shridhar Hiremath, Udita Basu","doi":"10.1007/s00299-024-03343-3","DOIUrl":"10.1007/s00299-024-03343-3","url":null,"abstract":"<p><p>Reactive oxygen species (ROS) and reactive nitrogen species (RNS) are critical for plant development as well as for its stress response. They can function as signaling molecules to orchestrate a well-defined response of plants to biotic stress. These responses are further fine-tuned by phytohormones, such as salicylic acid, jasmonic acid, and ethylene, to modulate immune response. In the past decades, the intricacies of redox and phytohormonal signaling have been uncovered during plant-pathogen interactions. This review explores the dynamic interplay of these components, elucidating their roles in perceiving biotic threats and shaping the plant's defense strategy. Molecular regulators and sites of oxidative burst have been explored during pathogen perception. Further, the interplay between various components of redox and phytohormonal signaling has been explored during bacterial, fungal, viral, and nematode infections as well as during insect pest infestation. Understanding these interactions highlights gaps in the current knowledge and provides insights into engineering crop varieties with enhanced resistance to pathogens and pests. This review also highlights potential applications of manipulating regulators of redox signaling to bolster plant immunity and ensure global food security. Future research should explore regulators of these signaling pathways as potential target to develop biotic stress-tolerant crops. Further insights are also needed into roles of endophytes and host microbiome modulating host ROS and RNS pool for exploiting them as biocontrol agents imparting resistance against pathogens in plants.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"263"},"PeriodicalIF":5.3,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-16DOI: 10.1007/s00299-024-03356-y
Guofang Zhang, Zhuang Yang, Shen Zhou, Jinjin Zhu, Xianqing Liu, Jie Luo
Key message: Cellulose synthase-like OsCSLD4 plays a pivotal role in regulating diverse agronomic traits, enhancing resistance against bacterial leaf blight, and modulating metabolite indices based on the multi-omics analysis in rice. To delve deeper into this complex network between agronomic traits and metabolites in rice, we have compiled a dataset encompassing genome, phenome, and metabolome, including 524 diverse accessions, 11 agronomic traits, and 841 metabolites, enabling us to pinpoint eight hotspots through GWAS. We later discovered four distinct metabolite categories, encompassing 15 metabolites that are concurrently present on the QTL qC12.1, associated with leaf angle of flag and spikelet length, and finally focused the cellulose synthase-like OsCSLD4, which was pinpointed through a rigorous process encompassing sequence variation, haplotype, ATAC, and differential expression across diverse tissues. Compared to the wild type, csld4 exhibited significant reductions in the plant height, flag leaf length, leaf width, spikelet length, 1000-grain weight, grain width, grain thickness, fertility, yield per plant, and bacterial blight resistance. However, there were significant increase in tiller numbers, degree of leaf rolling, flowering period, growth period, grain length, and empty kernel rate. Furthermore, the content of four polyphenol metabolites, excluding metabolite N-feruloyltyramine (mr1268), notably rose, whereas the levels of the other three polyphenol metabolites, smiglaside C (mr1498), 4-coumaric acid (mr1622), and smiglaside A (mr1925) decreased significantly in mutant csld4. The content of amino acid L-tyramine (mr1446) exhibited a notable increase, whereas the alkaloid trigonelline (mr1188) displayed a substantial decrease among the mutants. This study offered a comprehensive multi-omics perspective to analyze the genetic mechanism of OsCSLD4, and breeders can potentially enhance rice's yield, bacterial leaf blight resistance, and metabolite content, leading to more sustainable and profitable rice production.
{"title":"Cellulose synthase-like OsCSLD4: a key regulator of agronomic traits, disease resistance, and metabolic indices in rice.","authors":"Guofang Zhang, Zhuang Yang, Shen Zhou, Jinjin Zhu, Xianqing Liu, Jie Luo","doi":"10.1007/s00299-024-03356-y","DOIUrl":"10.1007/s00299-024-03356-y","url":null,"abstract":"<p><strong>Key message: </strong>Cellulose synthase-like OsCSLD4 plays a pivotal role in regulating diverse agronomic traits, enhancing resistance against bacterial leaf blight, and modulating metabolite indices based on the multi-omics analysis in rice. To delve deeper into this complex network between agronomic traits and metabolites in rice, we have compiled a dataset encompassing genome, phenome, and metabolome, including 524 diverse accessions, 11 agronomic traits, and 841 metabolites, enabling us to pinpoint eight hotspots through GWAS. We later discovered four distinct metabolite categories, encompassing 15 metabolites that are concurrently present on the QTL qC12.1, associated with leaf angle of flag and spikelet length, and finally focused the cellulose synthase-like OsCSLD4, which was pinpointed through a rigorous process encompassing sequence variation, haplotype, ATAC, and differential expression across diverse tissues. Compared to the wild type, csld4 exhibited significant reductions in the plant height, flag leaf length, leaf width, spikelet length, 1000-grain weight, grain width, grain thickness, fertility, yield per plant, and bacterial blight resistance. However, there were significant increase in tiller numbers, degree of leaf rolling, flowering period, growth period, grain length, and empty kernel rate. Furthermore, the content of four polyphenol metabolites, excluding metabolite N-feruloyltyramine (mr1268), notably rose, whereas the levels of the other three polyphenol metabolites, smiglaside C (mr1498), 4-coumaric acid (mr1622), and smiglaside A (mr1925) decreased significantly in mutant csld4. The content of amino acid L-tyramine (mr1446) exhibited a notable increase, whereas the alkaloid trigonelline (mr1188) displayed a substantial decrease among the mutants. This study offered a comprehensive multi-omics perspective to analyze the genetic mechanism of OsCSLD4, and breeders can potentially enhance rice's yield, bacterial leaf blight resistance, and metabolite content, leading to more sustainable and profitable rice production.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"264"},"PeriodicalIF":5.3,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472865","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-15DOI: 10.1007/s00299-024-03357-x
Rong Wang, Yang-Cao Shi, Bo Zhang, Wan-Rong Liu, Feng-Quan Tan, Fang Lu, Nan Jiang, Lai-Chao Cheng, Kai-Dong Xie, Xiao-Meng Wu, Wen-Wu Guo
Key message: Abnormal expression of genes regulating anther and pollen development and insufficient accumulation of male sterility (MS)- related metabolites lead to MS in cybrid pummelo Male sterility (MS) is a major cause of seedlessness in citrus, which is an important trait for fresh fruit. Understanding the mechanism of MS is important for breeding seedless citrus cultivars. In this study, we dissected the transcriptional, metabolic and physiological mechanisms of MS in somatic cybrid of pummelo (G1 + HBP). G1 + HBP exhibited severe male sterility, manifesting as retarded anther differentiation, abnormal anther wall development (especially tapetum and endothecium), and deficient pollen wall formation. In the anthers of G1 + HBP, the expression of genes regulating anther differentiation and tapetum development was abnormal, and the expression of genes regulating endothecium secondary lignification thickening and pollen wall formation was down-regulated. The transcription of genes involved in MS-related biological processes, such as jasmonic acid (JA) signaling pathway, primary metabolism, flavonoid metabolism, and programmed cell death, was altered in G1 + HBP anthers, and the accumulation of MS-associated metabolites, including fatty acids, amino acids, sugars, ATP, flavonols and reactive oxygen species (ROS), was down-regulated in G1 + HBP anthers. In summary, abnormal expression of key genes regulating anther and pollen development, altered transcription of key genes involved in MS-related metabolic pathways, and insufficient accumulation of MS-related metabolites together lead to MS in G1 + HBP. The critical genes and the metabolism pathways identified herein provide new insights into the formation mechanism of MS in citrus and candidate genes for breeding seedless citrus.
关键信息:调控花药和花粉发育的基因表达异常以及雄性不育(MS)相关代谢物积累不足导致杂交柚的雄性不育 雄性不育(MS)是柑橘无籽的主要原因,而无籽是新鲜水果的重要性状。了解 MS 的机理对于培育无籽柑橘栽培品种非常重要。本研究剖析了柚子体细胞杂交种(G1 + HBP)的转录、代谢和生理机制。G1 + HBP表现出严重的雄性不育,具体表现为花药分化迟缓、花药壁发育异常(尤其是叶柄和内皮)以及花粉壁形成不足。在 G1 + HBP 的花药中,调控花药分化和叶舌发育的基因表达异常,调控内皮层次生木质化增厚和花粉壁形成的基因表达下调。在 G1 + HBP 花药中,参与 MS 相关生物学过程(如茉莉酸(JA)信号通路、初级代谢、类黄酮代谢和细胞程序性死亡)的基因转录发生了改变,MS 相关代谢产物(包括脂肪酸、氨基酸、糖类、ATP、黄酮醇和活性氧(ROS))的积累在 G1 + HBP 花药中下调。总之,调控花药和花粉发育的关键基因表达异常、参与 MS 相关代谢途径的关键基因转录改变以及 MS 相关代谢物积累不足共同导致了 G1 + HBP 的 MS。本文鉴定的关键基因和代谢途径为了解柑橘 MS 的形成机制和培育无籽柑橘的候选基因提供了新的视角。
{"title":"Gene expression profiles and metabolic pathways responsible for male sterility in cybrid pummelo.","authors":"Rong Wang, Yang-Cao Shi, Bo Zhang, Wan-Rong Liu, Feng-Quan Tan, Fang Lu, Nan Jiang, Lai-Chao Cheng, Kai-Dong Xie, Xiao-Meng Wu, Wen-Wu Guo","doi":"10.1007/s00299-024-03357-x","DOIUrl":"10.1007/s00299-024-03357-x","url":null,"abstract":"<p><strong>Key message: </strong>Abnormal expression of genes regulating anther and pollen development and insufficient accumulation of male sterility (MS)- related metabolites lead to MS in cybrid pummelo Male sterility (MS) is a major cause of seedlessness in citrus, which is an important trait for fresh fruit. Understanding the mechanism of MS is important for breeding seedless citrus cultivars. In this study, we dissected the transcriptional, metabolic and physiological mechanisms of MS in somatic cybrid of pummelo (G1 + HBP). G1 + HBP exhibited severe male sterility, manifesting as retarded anther differentiation, abnormal anther wall development (especially tapetum and endothecium), and deficient pollen wall formation. In the anthers of G1 + HBP, the expression of genes regulating anther differentiation and tapetum development was abnormal, and the expression of genes regulating endothecium secondary lignification thickening and pollen wall formation was down-regulated. The transcription of genes involved in MS-related biological processes, such as jasmonic acid (JA) signaling pathway, primary metabolism, flavonoid metabolism, and programmed cell death, was altered in G1 + HBP anthers, and the accumulation of MS-associated metabolites, including fatty acids, amino acids, sugars, ATP, flavonols and reactive oxygen species (ROS), was down-regulated in G1 + HBP anthers. In summary, abnormal expression of key genes regulating anther and pollen development, altered transcription of key genes involved in MS-related metabolic pathways, and insufficient accumulation of MS-related metabolites together lead to MS in G1 + HBP. The critical genes and the metabolism pathways identified herein provide new insights into the formation mechanism of MS in citrus and candidate genes for breeding seedless citrus.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"262"},"PeriodicalIF":5.3,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472868","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Key message: Platanus acerifolia AIL genes PaAIL5a/b and PaAIL6b participate in FT-AP1/FUL-AIL pathways to regulate bud dormancy. In addition, PaAIL6a/b can promote flowering, and PaAIL5b and PaAIL6b affect floral development. Bud dormancy and floral induction are essential processes for perennial plants, they are both regulated by photoperiod, temperature, and hormones, indicating the existence of common regulators for both processes. AINTEGUMENTA-LIKE (AIL) genes regulate reproductive growth of annual plants, including floral induction and flower development, and their homologs in poplar and grape act downstream of the florigen gene FT and the floral meristem identity genes AP1/FUL and function to maintain growth and thus inhibit dormancy induction. However, it is not known whether AIL homologs participate in the reproduction processes in perennials and whether the Platanus acerifolia AIL genes are involved in dormancy. P. acerifolia is a perennial woody plant whose reproductive growth is strongly associated with dormancy. Here, we isolated four AIL homologs from P. acerifolia, PaAIL5a, PaAIL5b, PaAIL6a, and PaAIL6b, and systematically investigated their functions by ectopic-overexpression in tobacco. The findings demonstrate that PaAIL5a/b and PaAIL6b respond to short day, low temperature, and hormone signals and act as the components of the FT-AP1/FUL-AIL pathway to regulate the bud dormancy in P. acerifolia. Notably, PaAIL5a/b and PaAIL6b function downstream of PaFTL-PaFUL1/2/3 to inhibit the dormancy induction and downstream of PaFT-PaFUL2/3 to promote the dormancy release. In addition, PaAIL6a/b were found to accelerate flowering in transgenic tobacco, whereas PaAIL5b and PaAIL6b affected the flower development. Together, our results suggest that PaAIL genes may act downstream of different PaFT/PaFTL and PaFUL proteins to fulfill conservative and diverse roles in floral initiation, floral development, and dormancy regulation in P. acerifolia.
关键信息:Platanus acerifolia AIL 基因 PaAIL5a/b 和 PaAIL6b 参与 FT-AP1/FUL-AIL 途径,调节花芽休眠。此外,PAAIL6a/b 能促进开花,PAAIL5b 和 PaAIL6b 影响花的发育。芽休眠和花诱导是多年生植物的重要过程,它们都受光周期、温度和激素的调控,表明这两个过程存在共同的调控因子。AINTEGUMENTA-LIKE(AIL)基因调控一年生植物的生殖生长,包括花的诱导和花的发育,其在杨树和葡萄中的同源物作用于花源基因 FT 和花分生组织特征基因 AP1/FUL 的下游,具有维持生长的功能,从而抑制休眠的诱导。然而,AIL 同源基因是否参与多年生植物的繁殖过程,以及皂荚属植物的 AIL 基因是否参与休眠,目前尚不清楚。桔梗是一种多年生木本植物,其生殖生长与休眠密切相关。在此,我们从桔梗中分离出了四个 AIL 同源物:PaAIL5a、PaAIL5b、PaAIL6a 和 PaAIL6b,并通过在烟草中异位表达系统地研究了它们的功能。研究结果表明,PaAIL5a/b和PaAIL6b能响应短日照、低温和激素信号,并作为FT-AP1/FUL-AIL通路的组分调控P.acerifolia的花蕾休眠。值得注意的是,PaAIL5a/b 和 PaAIL6b 在 PaFTL-PaFUL1/2/3 的下游起抑制休眠诱导的作用,在 PaFT-PaFUL2/3 的下游起促进休眠解除的作用。此外,我们还发现 PaAIL6a/b 能加速转基因烟草的开花,而 PaAIL5b 和 PaAIL6b 则影响花的发育。总之,我们的研究结果表明,PaAIL基因可能作用于不同的PaFT/PaFTL和PaFUL蛋白的下游,在P. acerifolia的花萌发、花发育和休眠调控中发挥保守而多样的作用。
{"title":"AINTEGUMENTA-LIKE genes regulate reproductive growth and bud dormancy in Platanus acerifolia.","authors":"Fangfang Cai, Xin Jin, Linshan Han, Hui Chen, Changsheng Shao, Gehui Shi, Manzhu Bao, Yuqiang Sun, Jiaqi Zhang","doi":"10.1007/s00299-024-03349-x","DOIUrl":"10.1007/s00299-024-03349-x","url":null,"abstract":"<p><strong>Key message: </strong>Platanus acerifolia AIL genes PaAIL5a/b and PaAIL6b participate in FT-AP1/FUL-AIL pathways to regulate bud dormancy. In addition, PaAIL6a/b can promote flowering, and PaAIL5b and PaAIL6b affect floral development. Bud dormancy and floral induction are essential processes for perennial plants, they are both regulated by photoperiod, temperature, and hormones, indicating the existence of common regulators for both processes. AINTEGUMENTA-LIKE (AIL) genes regulate reproductive growth of annual plants, including floral induction and flower development, and their homologs in poplar and grape act downstream of the florigen gene FT and the floral meristem identity genes AP1/FUL and function to maintain growth and thus inhibit dormancy induction. However, it is not known whether AIL homologs participate in the reproduction processes in perennials and whether the Platanus acerifolia AIL genes are involved in dormancy. P. acerifolia is a perennial woody plant whose reproductive growth is strongly associated with dormancy. Here, we isolated four AIL homologs from P. acerifolia, PaAIL5a, PaAIL5b, PaAIL6a, and PaAIL6b, and systematically investigated their functions by ectopic-overexpression in tobacco. The findings demonstrate that PaAIL5a/b and PaAIL6b respond to short day, low temperature, and hormone signals and act as the components of the FT-AP1/FUL-AIL pathway to regulate the bud dormancy in P. acerifolia. Notably, PaAIL5a/b and PaAIL6b function downstream of PaFTL-PaFUL1/2/3 to inhibit the dormancy induction and downstream of PaFT-PaFUL2/3 to promote the dormancy release. In addition, PaAIL6a/b were found to accelerate flowering in transgenic tobacco, whereas PaAIL5b and PaAIL6b affected the flower development. Together, our results suggest that PaAIL genes may act downstream of different PaFT/PaFTL and PaFUL proteins to fulfill conservative and diverse roles in floral initiation, floral development, and dormancy regulation in P. acerifolia.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"261"},"PeriodicalIF":5.3,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472864","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-10DOI: 10.1007/s00299-024-03345-1
Imtiaz Ahmad, András Kis, Radhika Verma, István Szádeczky-Kardoss, Henrik Mihály Szaker, Aladár Pettkó-Szandtner, Dániel Silhavy, Zoltán Havelda, Tibor Csorba
Key message: Barley reproductive fitness and efficient heat stress adaptation requires the activity of TFIIS, the elongation cofactor of RNAPII. Regulation of transcriptional machinery and its adaptive role under different stress conditions are studied extensively in the dicot model plant Arabidopsis, but our knowledge on monocot species remains elusive. TFIIS is an RNA polymerase II-associated transcription elongation cofactor. Previously, it was shown that TFIIS ensures efficient transcription elongation that is necessary for heat stress survival in A. thaliana. However, the function of TFIIS has not been analysed in monocots. In the present work, we have generated and studied independent tfIIs-crispr-mutant barley lines. We show that TFIIS is needed for reproductive development and heat stress survival in barley. The molecular basis of HS-sensitivity of tfIIs mutants is the retarded expression of heat stress protein transcripts, which leads to late accumulation of HSP chaperones, enhanced proteotoxicity and ultimately to lethality. We also show that TFIIS is transcriptionally regulated in response to heat, supporting a conserved adaptive function of these control elements for plant thermal adaptation. In sum, our results are a step forward for the better understanding of transcriptional machinery regulation in monocot crops.
{"title":"TFIIS is required for reproductive development and thermal adaptation in barley.","authors":"Imtiaz Ahmad, András Kis, Radhika Verma, István Szádeczky-Kardoss, Henrik Mihály Szaker, Aladár Pettkó-Szandtner, Dániel Silhavy, Zoltán Havelda, Tibor Csorba","doi":"10.1007/s00299-024-03345-1","DOIUrl":"10.1007/s00299-024-03345-1","url":null,"abstract":"<p><strong>Key message: </strong>Barley reproductive fitness and efficient heat stress adaptation requires the activity of TFIIS, the elongation cofactor of RNAPII. Regulation of transcriptional machinery and its adaptive role under different stress conditions are studied extensively in the dicot model plant Arabidopsis, but our knowledge on monocot species remains elusive. TFIIS is an RNA polymerase II-associated transcription elongation cofactor. Previously, it was shown that TFIIS ensures efficient transcription elongation that is necessary for heat stress survival in A. thaliana. However, the function of TFIIS has not been analysed in monocots. In the present work, we have generated and studied independent tfIIs-crispr-mutant barley lines. We show that TFIIS is needed for reproductive development and heat stress survival in barley. The molecular basis of HS-sensitivity of tfIIs mutants is the retarded expression of heat stress protein transcripts, which leads to late accumulation of HSP chaperones, enhanced proteotoxicity and ultimately to lethality. We also show that TFIIS is transcriptionally regulated in response to heat, supporting a conserved adaptive function of these control elements for plant thermal adaptation. In sum, our results are a step forward for the better understanding of transcriptional machinery regulation in monocot crops.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"260"},"PeriodicalIF":5.3,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11467006/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142401043","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-10DOI: 10.1007/s00299-024-03348-y
Zhenghong Han, Yuanyuan Qiu, Ting Pan, Longjie Wang, Jing Wang, Kang Liu
Key message: GhMAC3e expression was induced by various stresses and hormones. GhMAC3e may regulate plant growth by influencing auxin distribution, and play important roles in Verticillium wilt resistance via mediating SA signaling. The MOS4-Associated Complex (MAC) is a highly conserved protein complex involved in pre-mRNA splicing and spliceosome assembly, which plays a vital role in plant immunity. It comprises key components such as MOS4, CDC5, and PRL1. MAC3A/B, as U-box E3 ubiquitin ligases, are crucial for various plant processes including development, stress responses, and disease resistance. However, their roles in cotton remain largely unknown. In this study, we first cloned the GhMAC3e gene from cotton and explored its biological functions by using virus-induced gene silencing (VIGS) in cotton and transgenic overexpression in Arabidopsis. The results showed that GhMAC3e is ubiquitously expressed in cotton tissues and could be induced by salt stress, Verticillium dahliae (VD) infection, PEG, ABA, ETH, GA3, MeJA, and SA. Silencing GhMAC3e retarded primary stem growth and reduced biomass of cotton coupled with the reduced auxin content in the petioles and veins. Silencing GhMAC3e up-regulated expression of cell growth-related genes GhXTH16 and Gh3.6, while down-regulated GhSAUR12 expression. Ectopic expression of GhMAC3e in Arabidopsis significantly enhanced its resistance to Verticillium wilt (VW) in terms of decreased pathogen biomass and lowered plant mortality. Overexpression of GhMAC3e dramatically upregulated AtPR1 by around 15 fold and more than 262 fold under basal and VD inoculation condition, respectively. This change was not associated with the expression of GhNPR1. In conclusion, GhMAC3e may not only regulate plant growth by influencing auxin distribution and growth-related gene expression, but also play important roles in VW resistance via mediating SA signaling independent of NPR1 transcription level.
{"title":"GhMAC3e is involved in plant growth and defense response to Verticillium dahliae.","authors":"Zhenghong Han, Yuanyuan Qiu, Ting Pan, Longjie Wang, Jing Wang, Kang Liu","doi":"10.1007/s00299-024-03348-y","DOIUrl":"10.1007/s00299-024-03348-y","url":null,"abstract":"<p><strong>Key message: </strong>GhMAC3e expression was induced by various stresses and hormones. GhMAC3e may regulate plant growth by influencing auxin distribution, and play important roles in Verticillium wilt resistance via mediating SA signaling. The MOS4-Associated Complex (MAC) is a highly conserved protein complex involved in pre-mRNA splicing and spliceosome assembly, which plays a vital role in plant immunity. It comprises key components such as MOS4, CDC5, and PRL1. MAC3A/B, as U-box E3 ubiquitin ligases, are crucial for various plant processes including development, stress responses, and disease resistance. However, their roles in cotton remain largely unknown. In this study, we first cloned the GhMAC3e gene from cotton and explored its biological functions by using virus-induced gene silencing (VIGS) in cotton and transgenic overexpression in Arabidopsis. The results showed that GhMAC3e is ubiquitously expressed in cotton tissues and could be induced by salt stress, Verticillium dahliae (VD) infection, PEG, ABA, ETH, GA3, MeJA, and SA. Silencing GhMAC3e retarded primary stem growth and reduced biomass of cotton coupled with the reduced auxin content in the petioles and veins. Silencing GhMAC3e up-regulated expression of cell growth-related genes GhXTH16 and Gh3.6, while down-regulated GhSAUR12 expression. Ectopic expression of GhMAC3e in Arabidopsis significantly enhanced its resistance to Verticillium wilt (VW) in terms of decreased pathogen biomass and lowered plant mortality. Overexpression of GhMAC3e dramatically upregulated AtPR1 by around 15 fold and more than 262 fold under basal and VD inoculation condition, respectively. This change was not associated with the expression of GhNPR1. In conclusion, GhMAC3e may not only regulate plant growth by influencing auxin distribution and growth-related gene expression, but also play important roles in VW resistance via mediating SA signaling independent of NPR1 transcription level.</p>","PeriodicalId":20204,"journal":{"name":"Plant Cell Reports","volume":"43 11","pages":"259"},"PeriodicalIF":5.3,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142401042","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}