Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence
Soybean is a globally important legume crop which is highly sensitive to drought. The identification of genes of particular relevance for drought responses provides an important basis to improve tolerance to environmental stress. Chloroplast Vesiculation (CV) genes have been characterized in Arabido...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-06-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1184020/full |
| _version_ | 1797810479776661504 |
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| author | Andrea Luciana Fleitas Alexandra Castro Eduardo Blumwald Sabina Vidal |
| author_facet | Andrea Luciana Fleitas Alexandra Castro Eduardo Blumwald Sabina Vidal |
| author_sort | Andrea Luciana Fleitas |
| collection | DOAJ |
| description | Soybean is a globally important legume crop which is highly sensitive to drought. The identification of genes of particular relevance for drought responses provides an important basis to improve tolerance to environmental stress. Chloroplast Vesiculation (CV) genes have been characterized in Arabidopsis and rice as proteins participating in a specific chloroplast-degradation vesicular pathway (CVV) during natural or stress-induced leaf senescence. Soybean genome contains two paralogous genes encoding highly similar CV proteins, CV1 and CV2. In this study, we found that expression of CV1 was differentially upregulated by drought stress in soybean contrasting genotypes exhibiting slow-wilting (tolerant) or fast-wilting (sensitive) phenotypes. CV1 reached higher induction levels in fast-wilting plants, suggesting a negative correlation between CV1 gene expression and drought tolerance. In contrast, autophagy (ATG8) and ATI-PS (ATI1) genes were induced to higher levels in slow-wilting plants, supporting a pro-survival role for these genes in soybean drought tolerance responses. The biological function of soybean CVs in chloroplast degradation was confirmed by analyzing the effect of conditional overexpression of CV2-FLAG fusions on the accumulation of specific chloroplast proteins. Functional specificity of CV1 and CV2 genes was assessed by analyzing their specific promoter activities in transgenic Arabidopsis expressing GUS reporter gene driven by CV1 or CV2 promoters. CV1 promoter responded primarily to abiotic stimuli (hyperosmolarity, salinity and oxidative stress), while the promoter of CV2 was predominantly active during natural senescence. Both promoters were highly responsive to auxin but only CV1 responded to other stress-related hormones, such as ABA, salicylic acid and methyl jasmonate. Moreover, the dark-induced expression of CV2, but not of CV1, was strongly inhibited by cytokinin, indicating similarities in the regulation of CV2 to the reported expression of Arabidopsis and rice CV genes. Finally, we report the expression of both CV1 and CV2 genes in roots of soybean and transgenic Arabidopsis, suggesting a role for the encoded proteins in root plastids. Together, the results indicate differential roles for CV1 and CV2 in development and in responses to environmental stress, and point to CV1 as a potential target for gene editing to improve crop performance under stress without compromising natural development. |
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| format | Article |
| id | doaj.art-3842406a332f462080392e3ebdb75701 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-13T07:08:29Z |
| publishDate | 2023-06-01 |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-3842406a332f462080392e3ebdb757012023-06-06T05:02:05ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11840201184020Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescenceAndrea Luciana Fleitas0Alexandra Castro1Eduardo Blumwald2Sabina Vidal3Laboratorio de Biología Molecular Vegetal, Instituto de Química Biológica, Facultad de Ciencias, Universidad de la República, Montevideo, UruguayLaboratorio de Biología Molecular Vegetal, Instituto de Química Biológica, Facultad de Ciencias, Universidad de la República, Montevideo, UruguayDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesLaboratorio de Biología Molecular Vegetal, Instituto de Química Biológica, Facultad de Ciencias, Universidad de la República, Montevideo, UruguaySoybean is a globally important legume crop which is highly sensitive to drought. The identification of genes of particular relevance for drought responses provides an important basis to improve tolerance to environmental stress. Chloroplast Vesiculation (CV) genes have been characterized in Arabidopsis and rice as proteins participating in a specific chloroplast-degradation vesicular pathway (CVV) during natural or stress-induced leaf senescence. Soybean genome contains two paralogous genes encoding highly similar CV proteins, CV1 and CV2. In this study, we found that expression of CV1 was differentially upregulated by drought stress in soybean contrasting genotypes exhibiting slow-wilting (tolerant) or fast-wilting (sensitive) phenotypes. CV1 reached higher induction levels in fast-wilting plants, suggesting a negative correlation between CV1 gene expression and drought tolerance. In contrast, autophagy (ATG8) and ATI-PS (ATI1) genes were induced to higher levels in slow-wilting plants, supporting a pro-survival role for these genes in soybean drought tolerance responses. The biological function of soybean CVs in chloroplast degradation was confirmed by analyzing the effect of conditional overexpression of CV2-FLAG fusions on the accumulation of specific chloroplast proteins. Functional specificity of CV1 and CV2 genes was assessed by analyzing their specific promoter activities in transgenic Arabidopsis expressing GUS reporter gene driven by CV1 or CV2 promoters. CV1 promoter responded primarily to abiotic stimuli (hyperosmolarity, salinity and oxidative stress), while the promoter of CV2 was predominantly active during natural senescence. Both promoters were highly responsive to auxin but only CV1 responded to other stress-related hormones, such as ABA, salicylic acid and methyl jasmonate. Moreover, the dark-induced expression of CV2, but not of CV1, was strongly inhibited by cytokinin, indicating similarities in the regulation of CV2 to the reported expression of Arabidopsis and rice CV genes. Finally, we report the expression of both CV1 and CV2 genes in roots of soybean and transgenic Arabidopsis, suggesting a role for the encoded proteins in root plastids. Together, the results indicate differential roles for CV1 and CV2 in development and in responses to environmental stress, and point to CV1 as a potential target for gene editing to improve crop performance under stress without compromising natural development.https://www.frontiersin.org/articles/10.3389/fpls.2023.1184020/fullsoybeandroughtchloroplast vesiculationsenescenceslow wilting |
| spellingShingle | Andrea Luciana Fleitas Alexandra Castro Eduardo Blumwald Sabina Vidal Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence Frontiers in Plant Science soybean drought chloroplast vesiculation senescence slow wilting |
| title | Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence |
| title_full | Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence |
| title_fullStr | Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence |
| title_full_unstemmed | Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence |
| title_short | Functional specialization of chloroplast vesiculation (CV) duplicated genes from soybean shows partial overlapping roles during stress-induced or natural senescence |
| title_sort | functional specialization of chloroplast vesiculation cv duplicated genes from soybean shows partial overlapping roles during stress induced or natural senescence |
| topic | soybean drought chloroplast vesiculation senescence slow wilting |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1184020/full |
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