Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana

Wall-Associated Kinase-like (WAKL) proteins play crucial roles in plant stress responses, but their evolutionary divergence and functions in kiwifruit remain unclear. In this study, we performed a genome-wide analysis of WAKL proteins in Actinidia chinensis and Actinidia eriantha. Our findings revea...

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Main Authors: Zupeng Wang, Zhenting Sun, Hui Pan, Caihong Zhong, Li Li
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Plant Stress
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667064X25001149
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author Zupeng Wang
Zhenting Sun
Hui Pan
Caihong Zhong
Li Li
author_facet Zupeng Wang
Zhenting Sun
Hui Pan
Caihong Zhong
Li Li
author_sort Zupeng Wang
collection DOAJ
description Wall-Associated Kinase-like (WAKL) proteins play crucial roles in plant stress responses, but their evolutionary divergence and functions in kiwifruit remain unclear. In this study, we performed a genome-wide analysis of WAKL proteins in Actinidia chinensis and Actinidia eriantha. Our findings reveal haploid-specific variations that contribute to kiwifruit resistance against bacterial canker. Significant structural and numerical differences in WAKL genes between haploids were identified, driven by genomic rearrangements and duplication events. Phylogenetic and motif analyses revealed functional specialization and evolutionary divergence within the WAKL family in kiwifruit. Expression analysis showed that key WAKL genes respond differently in resistant and susceptible kiwifruit during Psa infection. We validated nine AcWAKL genes in Nicotiana benthamiana. Four induced reactive oxygen species (ROS) accumulation and cell death, and three of these genes are found only on one haploid. Further investigation showed that these four AcWAKL genes triggered ROS accumulation and cell death by upregulating NbRBOHB expression. Our findings highlight the importance of haploid-specific variations and PAVs in shaping WAKL gene function, providing new insights into how these genomic features modulate immune responses and offering potential implications for enhancing disease resistance in kiwifruit breeding.
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issn 2667-064X
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publishDate 2025-06-01
publisher Elsevier
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series Plant Stress
spelling doaj-art-744ca425f17d48e7be44cb63d77131b32025-08-20T02:26:40ZengElsevierPlant Stress2667-064X2025-06-011610084910.1016/j.stress.2025.100849Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamianaZupeng Wang0Zhenting Sun1Hui Pan2Caihong Zhong3Li Li4Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China; Engineering Laboratory for Kiwifruit Industrial Technology, Chinese Academy of Sciences, Wuhan 430074, ChinaKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China; Engineering Laboratory for Kiwifruit Industrial Technology, Chinese Academy of Sciences, Wuhan 430074, ChinaKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China; Engineering Laboratory for Kiwifruit Industrial Technology, Chinese Academy of Sciences, Wuhan 430074, ChinaKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China; Engineering Laboratory for Kiwifruit Industrial Technology, Chinese Academy of Sciences, Wuhan 430074, China; Corresponding authors.Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China; Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China; Engineering Laboratory for Kiwifruit Industrial Technology, Chinese Academy of Sciences, Wuhan 430074, China; Corresponding authors.Wall-Associated Kinase-like (WAKL) proteins play crucial roles in plant stress responses, but their evolutionary divergence and functions in kiwifruit remain unclear. In this study, we performed a genome-wide analysis of WAKL proteins in Actinidia chinensis and Actinidia eriantha. Our findings reveal haploid-specific variations that contribute to kiwifruit resistance against bacterial canker. Significant structural and numerical differences in WAKL genes between haploids were identified, driven by genomic rearrangements and duplication events. Phylogenetic and motif analyses revealed functional specialization and evolutionary divergence within the WAKL family in kiwifruit. Expression analysis showed that key WAKL genes respond differently in resistant and susceptible kiwifruit during Psa infection. We validated nine AcWAKL genes in Nicotiana benthamiana. Four induced reactive oxygen species (ROS) accumulation and cell death, and three of these genes are found only on one haploid. Further investigation showed that these four AcWAKL genes triggered ROS accumulation and cell death by upregulating NbRBOHB expression. Our findings highlight the importance of haploid-specific variations and PAVs in shaping WAKL gene function, providing new insights into how these genomic features modulate immune responses and offering potential implications for enhancing disease resistance in kiwifruit breeding.http://www.sciencedirect.com/science/article/pii/S2667064X25001149KiwifruitWAKL genesBacterial cankerHaploid variationsGene duplicationROS accumulation
spellingShingle Zupeng Wang
Zhenting Sun
Hui Pan
Caihong Zhong
Li Li
Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
Plant Stress
Kiwifruit
WAKL genes
Bacterial canker
Haploid variations
Gene duplication
ROS accumulation
title Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
title_full Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
title_fullStr Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
title_full_unstemmed Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
title_short Haploid-specific variations of kiwifruit WAKL genes modulate immune-related responses in Nicotiana benthamiana
title_sort haploid specific variations of kiwifruit wakl genes modulate immune related responses in nicotiana benthamiana
topic Kiwifruit
WAKL genes
Bacterial canker
Haploid variations
Gene duplication
ROS accumulation
url http://www.sciencedirect.com/science/article/pii/S2667064X25001149
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