A positive feedback loop mediated by CsERF31 initiates female cucumber flower development
Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber (Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropan...
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Published in | Plant physiology (Bethesda) Vol. 186; no. 2; pp. 1088 - 1100 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Oxford University Press
21.03.2021
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Abstract | Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber (Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropane-1-carboxylic acid synthases (CsACSs). However, the regulatory mechanism of these synthases remains elusive. Here, we used gene expression analysis, protein-DNA interaction assays, and transgenic plants to study the function of a gynoecium-specific gene, ETHYLENE RESPONSE FACTOR31 (CsERF31), in female flower differentiation. We found that in a predetermined female flower, ethylene signaling activates CsERF31 by CsEIN3, and then CsERF31 stimulates CsACS2, which triggers a positive feedback loop to ensure female rather than bisexual flower development. A similar interplay is functionally conserved in melon (Cucumis melo L.). Knockdown of CsERF31 by RNAi causes defective bisexual flowers to replace female flowers. Ectopic expression of CsERF31 suppresses stamen development and promotes pistil development in male flowers, demonstrating that CsERF31 functions as a sex switch. Taken together, our data confirm that CsERF31 represents the molecular link between female-male determination and female-bisexual determination, and provide mechanistic insight into how ethylene promotes female flowers, rather than bisexual flowers, in cucumber sex determination. |
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AbstractList | Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber (Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropane-1-carboxylic acid synthases (CsACSs). However, the regulatory mechanism of these synthases remains elusive. Here, we used gene expression analysis, protein-DNA interaction assays, and transgenic plants to study the function of a gynoecium-specific gene, ETHYLENE RESPONSE FACTOR31 (CsERF31), in female flower differentiation. We found that in a predetermined female flower, ethylene signaling activates CsERF31 by CsEIN3, and then CsERF31 stimulates CsACS2, which triggers a positive feedback loop to ensure female rather than bisexual flower development. A similar interplay is functionally conserved in melon (Cucumis melo L.). Knockdown of CsERF31 by RNAi causes defective bisexual flowers to replace female flowers. Ectopic expression of CsERF31 suppresses stamen development and promotes pistil development in male flowers, demonstrating that CsERF31 functions as a sex switch. Taken together, our data confirm that CsERF31 represents the molecular link between female-male determination and female-bisexual determination, and provide mechanistic insight into how ethylene promotes female flowers, rather than bisexual flowers, in cucumber sex determination. Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber ( Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropane-1-carboxylic acid synthases ( CsACSs ). However, the regulatory mechanism of these synthases remains elusive. Here, we used gene expression analysis, protein–DNA interaction assays, and transgenic plants to study the function of a gynoecium-specific gene, ETHYLENE RESPONSE FACTOR31 ( CsERF31 ), in female flower differentiation. We found that in a predetermined female flower, ethylene signaling activates CsERF31 by CsEIN3 , and then CsERF31 stimulates CsACS2 , which triggers a positive feedback loop to ensure female rather than bisexual flower development. A similar interplay is functionally conserved in melon ( Cucumis melo L.). Knockdown of CsERF31 by RNAi causes defective bisexual flowers to replace female flowers. Ectopic expression of CsERF31 suppresses stamen development and promotes pistil development in male flowers, demonstrating that CsERF31 functions as a sex switch. Taken together, our data confirm that CsERF31 represents the molecular link between female–male determination and female–bisexual determination, and provide mechanistic insight into how ethylene promotes female flowers, rather than bisexual flowers, in cucumber sex determination. A key regulator promotes female flower development by triggering a positive feedback loop during cucumber sex determination. Abstract Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber (Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropane-1-carboxylic acid synthases (CsACSs). However, the regulatory mechanism of these synthases remains elusive. Here, we used gene expression analysis, protein–DNA interaction assays, and transgenic plants to study the function of a gynoecium-specific gene, ETHYLENE RESPONSE FACTOR31 (CsERF31), in female flower differentiation. We found that in a predetermined female flower, ethylene signaling activates CsERF31 by CsEIN3, and then CsERF31 stimulates CsACS2, which triggers a positive feedback loop to ensure female rather than bisexual flower development. A similar interplay is functionally conserved in melon (Cucumis melo L.). Knockdown of CsERF31 by RNAi causes defective bisexual flowers to replace female flowers. Ectopic expression of CsERF31 suppresses stamen development and promotes pistil development in male flowers, demonstrating that CsERF31 functions as a sex switch. Taken together, our data confirm that CsERF31 represents the molecular link between female–male determination and female–bisexual determination, and provide mechanistic insight into how ethylene promotes female flowers, rather than bisexual flowers, in cucumber sex determination. |
Author | Pan, Jian Lin, Wen-Hui Lian, Hongli Wang, Gang Wen, Haifan Du, Hui Pan, Junsong Chen, Guanqun Chen, Yue Zhang, Leyu Cai, Run |
AuthorAffiliation | 1 School of Agriculture and Biology, Shanghai Jiao Tong University , Shanghai, China 2 School of Design, Shanghai Jiao Tong University , Shanghai, China 3 School of Life Sciences and Biotechnology, The Joint International Research Laboratory of Metabolic and Developmental Sciences, Joint Center for Single Cell Biology, Shanghai Jiao Tong University , Shanghai, China |
AuthorAffiliation_xml | – name: 3 School of Life Sciences and Biotechnology, The Joint International Research Laboratory of Metabolic and Developmental Sciences, Joint Center for Single Cell Biology, Shanghai Jiao Tong University , Shanghai, China – name: 1 School of Agriculture and Biology, Shanghai Jiao Tong University , Shanghai, China – name: 2 School of Design, Shanghai Jiao Tong University , Shanghai, China |
Author_xml | – sequence: 1 givenname: Jian surname: Pan fullname: Pan, Jian organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 2 givenname: Haifan surname: Wen fullname: Wen, Haifan organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 3 givenname: Guanqun surname: Chen fullname: Chen, Guanqun organization: School of Design, Shanghai Jiao Tong University, Shanghai, China – sequence: 4 givenname: Wen-Hui surname: Lin fullname: Lin, Wen-Hui organization: School of Life Sciences and Biotechnology, The Joint International Research Laboratory of Metabolic and Developmental Sciences, Joint Center for Single Cell Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 5 givenname: Hui surname: Du fullname: Du, Hui organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 6 givenname: Yue surname: Chen fullname: Chen, Yue organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 7 givenname: Leyu surname: Zhang fullname: Zhang, Leyu organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 8 givenname: Hongli surname: Lian fullname: Lian, Hongli organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 9 givenname: Gang surname: Wang fullname: Wang, Gang organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 10 givenname: Run surname: Cai fullname: Cai, Run organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China – sequence: 11 givenname: Junsong surname: Pan fullname: Pan, Junsong organization: School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China |
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Title | A positive feedback loop mediated by CsERF31 initiates female cucumber flower development |
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