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PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice

Plant leaf senescence, caused by multiple internal and environmental factors, has an important impact on agricultural production. The lectin receptor‐like kinase (LecRLK) family members participate in plant development and responses to biotic and abiotic stresses, but their roles in regulating leaf...

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Autores principales: Xu, Jiangmin, Wang, Chunlian, Wang, Fujun, Liu, Yapei, Li, Man, Wang, Hongjie, Zheng, Yuhan, Zhao, Kaijun, Ji, Zhiyuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651159/
https://www.ncbi.nlm.nih.gov/pubmed/37578160
http://dx.doi.org/10.1111/pbi.14150
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author Xu, Jiangmin
Wang, Chunlian
Wang, Fujun
Liu, Yapei
Li, Man
Wang, Hongjie
Zheng, Yuhan
Zhao, Kaijun
Ji, Zhiyuan
author_facet Xu, Jiangmin
Wang, Chunlian
Wang, Fujun
Liu, Yapei
Li, Man
Wang, Hongjie
Zheng, Yuhan
Zhao, Kaijun
Ji, Zhiyuan
author_sort Xu, Jiangmin
collection PubMed
description Plant leaf senescence, caused by multiple internal and environmental factors, has an important impact on agricultural production. The lectin receptor‐like kinase (LecRLK) family members participate in plant development and responses to biotic and abiotic stresses, but their roles in regulating leaf senescence remain elusive. Here, we identify and characterize a rice premature withered leaf 1 (pwl1) mutant, which exhibits premature leaf senescence throughout the plant life cycle. The pwl1 mutant displayed withered and whitish leaf tips, decreased chlorophyll content, and accelerated chloroplast degradation. Map‐based cloning revealed an amino acid substitution (Gly412Arg) in LOC_Os03g62180 (PWL1) was responsible for the phenotypes of pwl1. The expression of PWL1 was detected in all tissues, but predominantly in tillering and mature leaves. PWL1 encodes a G‐type LecRLK with active kinase and autophosphorylation activities. PWL1 is localized to the plasma membrane and can self‐associate, mainly mediated by the plasminogen‐apple‐nematode (PAN) domain. Substitution of the PAN domain significantly diminished the self‐interaction of PWL1. Moreover, the pwl1 mutant showed enhanced reactive oxygen species (ROS) accumulation, cell death, and severe DNA fragmentation. RNA sequencing analysis revealed that PWL1 was involved in the regulation of multiple biological processes, like carbon metabolism, ribosome, and peroxisome pathways. Meanwhile, interfering of biological processes induced by the PWL1 mutation also enhanced heat sensitivity and resistance to bacterial blight and bacterial leaf streak with excessive accumulation of ROS and impaired chloroplast development in rice. Natural variation analysis indicated more variations in indica varieties, and the vast majority of japonica varieties harbour the PWL1 ( Hap1 ) allele. Together, our results suggest that PWL1, a member of LecRLKs, exerts multiple roles in regulating plant growth and development, heat‐tolerance, and resistance to bacterial pathogens.
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spelling pubmed-106511592023-11-15 PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice Xu, Jiangmin Wang, Chunlian Wang, Fujun Liu, Yapei Li, Man Wang, Hongjie Zheng, Yuhan Zhao, Kaijun Ji, Zhiyuan Plant Biotechnol J Research Articles Plant leaf senescence, caused by multiple internal and environmental factors, has an important impact on agricultural production. The lectin receptor‐like kinase (LecRLK) family members participate in plant development and responses to biotic and abiotic stresses, but their roles in regulating leaf senescence remain elusive. Here, we identify and characterize a rice premature withered leaf 1 (pwl1) mutant, which exhibits premature leaf senescence throughout the plant life cycle. The pwl1 mutant displayed withered and whitish leaf tips, decreased chlorophyll content, and accelerated chloroplast degradation. Map‐based cloning revealed an amino acid substitution (Gly412Arg) in LOC_Os03g62180 (PWL1) was responsible for the phenotypes of pwl1. The expression of PWL1 was detected in all tissues, but predominantly in tillering and mature leaves. PWL1 encodes a G‐type LecRLK with active kinase and autophosphorylation activities. PWL1 is localized to the plasma membrane and can self‐associate, mainly mediated by the plasminogen‐apple‐nematode (PAN) domain. Substitution of the PAN domain significantly diminished the self‐interaction of PWL1. Moreover, the pwl1 mutant showed enhanced reactive oxygen species (ROS) accumulation, cell death, and severe DNA fragmentation. RNA sequencing analysis revealed that PWL1 was involved in the regulation of multiple biological processes, like carbon metabolism, ribosome, and peroxisome pathways. Meanwhile, interfering of biological processes induced by the PWL1 mutation also enhanced heat sensitivity and resistance to bacterial blight and bacterial leaf streak with excessive accumulation of ROS and impaired chloroplast development in rice. Natural variation analysis indicated more variations in indica varieties, and the vast majority of japonica varieties harbour the PWL1 ( Hap1 ) allele. Together, our results suggest that PWL1, a member of LecRLKs, exerts multiple roles in regulating plant growth and development, heat‐tolerance, and resistance to bacterial pathogens. John Wiley and Sons Inc. 2023-08-14 2023-12 /pmc/articles/PMC10651159/ /pubmed/37578160 http://dx.doi.org/10.1111/pbi.14150 Text en © 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Xu, Jiangmin
Wang, Chunlian
Wang, Fujun
Liu, Yapei
Li, Man
Wang, Hongjie
Zheng, Yuhan
Zhao, Kaijun
Ji, Zhiyuan
PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title_full PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title_fullStr PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title_full_unstemmed PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title_short PWL1, a G‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice
title_sort pwl1, a g‐type lectin receptor‐like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to xanthomonas oryzae in rice
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10651159/
https://www.ncbi.nlm.nih.gov/pubmed/37578160
http://dx.doi.org/10.1111/pbi.14150
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