SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration

During evolutionary adaptation, the mechanisms for self-regulation are established between the normal growth and development of plants and environmental stress. The phytohormone jasmonate (JA) is a key tie of plant defence and development, and JASMONATE-ZIM DOMAIN (JAZ) repressor proteins are key co...

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Main Authors: Boyan Tang, Tingting Tan, Yating Chen, Zongli Hu, Qiaoli Xie, Xiaohui Yu, Guoping Chen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-07-01
Series:PLoS Genetics
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9278786/?tool=EBI
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author Boyan Tang
Tingting Tan
Yating Chen
Zongli Hu
Qiaoli Xie
Xiaohui Yu
Guoping Chen
author_facet Boyan Tang
Tingting Tan
Yating Chen
Zongli Hu
Qiaoli Xie
Xiaohui Yu
Guoping Chen
author_sort Boyan Tang
collection DOAJ
description During evolutionary adaptation, the mechanisms for self-regulation are established between the normal growth and development of plants and environmental stress. The phytohormone jasmonate (JA) is a key tie of plant defence and development, and JASMONATE-ZIM DOMAIN (JAZ) repressor proteins are key components in JA signalling pathways. Here, we show that JAZ expression was affected by leaf senescence from the transcriptomic data. Further investigation revealed that SlJAZ10 and SlJAZ11 positively regulate leaf senescence and that SlJAZ11 can also promote plant regeneration. Moreover, we reveal that the SlJAV1-SlWRKY51 (JW) complex could suppress JA biosynthesis under normal growth conditions. Immediately after injury, SlJAZ10 and SlJAZ11 can regulate the activity of the JW complex through the effects of electrical signals and Ca2+ waves, which in turn affect JA biosynthesis, causing a difference in the regeneration phenotype between SlJAZ10-OE and SlJAZ11-OE transgenic plants. In addition, SlRbcs-3B could maintain the protein stability of SlJAZ11 to protect it from degradation. Together, SlJAZ10 and SlJAZ11 not only act as repressors of JA signalling to leaf senescence, but also regulate plant regeneration through coordinated electrical signals, Ca2+ waves, hormones and transcriptional regulation. Our study provides critical insights into the mechanisms by which SlJAZ11 can induce regeneration. Author summary In plants, senescence is the final stage of development, but regeneration can help them beyond the stage. Plants regeneration is essential for propagation, and in cultivated crops to maintain excellent traits as close as possible. JA signaling can sense environmental signals and integrate various regulatory mechanisms to ensure plants regeneration occurs under optimal conditions. In this work, the JAZ-JAV1-WRKY51 complexes with reported was further optimized, the function of SlJAZ10 and SlJAZ11 was identified to promote inhibitory activity of SlJAV1-SlWRKY51 complex which negatively regulated JA biosynthesis by direct binding of the W-box of the SlAOC promoter. The results of further investigation suggest that the differences in regulation of electrical signals, Ca2+ waves, hormones and transcriptional regulation are responsible for the regeneration between SlJAZ10 and SlJAZ11. In addition, we have found that SlRbcs-3B could maintain the protein stability of SlJAZ11 to protect it from degradation. In summary, despite both SlJAZ10 and SlJAZ11 can function as senescence, only SlJAZ11 has an important promoting function for regeneration.
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spelling doaj.art-ea48e7f30fdc4dfe8c69f7c880db672e2022-12-22T03:01:00ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042022-07-01187SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regenerationBoyan TangTingting TanYating ChenZongli HuQiaoli XieXiaohui YuGuoping ChenDuring evolutionary adaptation, the mechanisms for self-regulation are established between the normal growth and development of plants and environmental stress. The phytohormone jasmonate (JA) is a key tie of plant defence and development, and JASMONATE-ZIM DOMAIN (JAZ) repressor proteins are key components in JA signalling pathways. Here, we show that JAZ expression was affected by leaf senescence from the transcriptomic data. Further investigation revealed that SlJAZ10 and SlJAZ11 positively regulate leaf senescence and that SlJAZ11 can also promote plant regeneration. Moreover, we reveal that the SlJAV1-SlWRKY51 (JW) complex could suppress JA biosynthesis under normal growth conditions. Immediately after injury, SlJAZ10 and SlJAZ11 can regulate the activity of the JW complex through the effects of electrical signals and Ca2+ waves, which in turn affect JA biosynthesis, causing a difference in the regeneration phenotype between SlJAZ10-OE and SlJAZ11-OE transgenic plants. In addition, SlRbcs-3B could maintain the protein stability of SlJAZ11 to protect it from degradation. Together, SlJAZ10 and SlJAZ11 not only act as repressors of JA signalling to leaf senescence, but also regulate plant regeneration through coordinated electrical signals, Ca2+ waves, hormones and transcriptional regulation. Our study provides critical insights into the mechanisms by which SlJAZ11 can induce regeneration. Author summary In plants, senescence is the final stage of development, but regeneration can help them beyond the stage. Plants regeneration is essential for propagation, and in cultivated crops to maintain excellent traits as close as possible. JA signaling can sense environmental signals and integrate various regulatory mechanisms to ensure plants regeneration occurs under optimal conditions. In this work, the JAZ-JAV1-WRKY51 complexes with reported was further optimized, the function of SlJAZ10 and SlJAZ11 was identified to promote inhibitory activity of SlJAV1-SlWRKY51 complex which negatively regulated JA biosynthesis by direct binding of the W-box of the SlAOC promoter. The results of further investigation suggest that the differences in regulation of electrical signals, Ca2+ waves, hormones and transcriptional regulation are responsible for the regeneration between SlJAZ10 and SlJAZ11. In addition, we have found that SlRbcs-3B could maintain the protein stability of SlJAZ11 to protect it from degradation. In summary, despite both SlJAZ10 and SlJAZ11 can function as senescence, only SlJAZ11 has an important promoting function for regeneration.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9278786/?tool=EBI
spellingShingle Boyan Tang
Tingting Tan
Yating Chen
Zongli Hu
Qiaoli Xie
Xiaohui Yu
Guoping Chen
SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
PLoS Genetics
title SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
title_full SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
title_fullStr SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
title_full_unstemmed SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
title_short SlJAZ10 and SlJAZ11 mediate dark-induced leaf senescence and regeneration
title_sort sljaz10 and sljaz11 mediate dark induced leaf senescence and regeneration
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9278786/?tool=EBI
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AT qiaolixie sljaz10andsljaz11mediatedarkinducedleafsenescenceandregeneration
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