Cargando…

Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions

Brown planthopper (BPH, Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remai...

Descripción completa

Detalles Bibliográficos
Autores principales: Dai, Yang‐Shuo, Liu, Di, Guo, Wuxiu, Liu, Zhi‐Xuan, Zhang, Xue, Shi, Li‐Li, Zhou, De‐Mian, Wang, Ling‐Na, Kang, Kui, Wang, Feng‐Zhu, Zhao, Shan‐Shan, Tan, Yi‐Fang, Hu, Tian, Chen, Wu, Li, Peng, Zhou, Qing‐Ming, Yuan, Long‐Yu, Zhang, Zhenfei, Chen, Yue‐Qin, Zhang, Wen‐Qing, Li, Juan, Yu, Lu‐Jun, Xiao, Shi
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/PMC10214751/
https://www.ncbi.nlm.nih.gov/pubmed/36952539
http://dx.doi.org/10.1111/pbi.14038
_version_ 1785047902670815232
author Dai, Yang‐Shuo
Liu, Di
Guo, Wuxiu
Liu, Zhi‐Xuan
Zhang, Xue
Shi, Li‐Li
Zhou, De‐Mian
Wang, Ling‐Na
Kang, Kui
Wang, Feng‐Zhu
Zhao, Shan‐Shan
Tan, Yi‐Fang
Hu, Tian
Chen, Wu
Li, Peng
Zhou, Qing‐Ming
Yuan, Long‐Yu
Zhang, Zhenfei
Chen, Yue‐Qin
Zhang, Wen‐Qing
Li, Juan
Yu, Lu‐Jun
Xiao, Shi
author_facet Dai, Yang‐Shuo
Liu, Di
Guo, Wuxiu
Liu, Zhi‐Xuan
Zhang, Xue
Shi, Li‐Li
Zhou, De‐Mian
Wang, Ling‐Na
Kang, Kui
Wang, Feng‐Zhu
Zhao, Shan‐Shan
Tan, Yi‐Fang
Hu, Tian
Chen, Wu
Li, Peng
Zhou, Qing‐Ming
Yuan, Long‐Yu
Zhang, Zhenfei
Chen, Yue‐Qin
Zhang, Wen‐Qing
Li, Juan
Yu, Lu‐Jun
Xiao, Shi
author_sort Dai, Yang‐Shuo
collection PubMed
description Brown planthopper (BPH, Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remains largely unknown. Here, we discovered a Poaceae‐specific metabolite, mixed‐linkage β‐1,3;1,4‐d‐glucan (MLG), which contributes to jasmonate‐mediated BPH resistance. MLG levels in rice significantly increased upon BPH attack. Overexpressing OsCslF6, which encodes a glucan synthase that catalyses MLG biosynthesis, significantly enhanced BPH resistance and cell wall thickness in vascular bundles, whereas knockout of OsCslF6 reduced BPH resistance and vascular wall thickness. OsMYC2, a master transcription factor of jasmonate signalling, directly controlled the upregulation of OsCslF6 in response to BPH feeding. The AT‐rich domain of the OsCslF6 promoter varies in rice varieties from different locations and natural variants in this domain were associated with BPH resistance. MLG‐derived oligosaccharides bound to the plasma membrane‐anchored LECTIN RECEPTOR KINASE1 OsLecRK1 and modulated its activity. Thus, our findings suggest that the OsMYC2‐OsCslF6 module regulates pest resistance by modulating MLG production to enhance vascular wall thickness and OsLecRK1‐mediated defence signalling during rice‐BPH interactions.
format Online
Article
Text
id pubmed-10214751
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-102147512023-05-27 Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions Dai, Yang‐Shuo Liu, Di Guo, Wuxiu Liu, Zhi‐Xuan Zhang, Xue Shi, Li‐Li Zhou, De‐Mian Wang, Ling‐Na Kang, Kui Wang, Feng‐Zhu Zhao, Shan‐Shan Tan, Yi‐Fang Hu, Tian Chen, Wu Li, Peng Zhou, Qing‐Ming Yuan, Long‐Yu Zhang, Zhenfei Chen, Yue‐Qin Zhang, Wen‐Qing Li, Juan Yu, Lu‐Jun Xiao, Shi Plant Biotechnol J Research Articles Brown planthopper (BPH, Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remains largely unknown. Here, we discovered a Poaceae‐specific metabolite, mixed‐linkage β‐1,3;1,4‐d‐glucan (MLG), which contributes to jasmonate‐mediated BPH resistance. MLG levels in rice significantly increased upon BPH attack. Overexpressing OsCslF6, which encodes a glucan synthase that catalyses MLG biosynthesis, significantly enhanced BPH resistance and cell wall thickness in vascular bundles, whereas knockout of OsCslF6 reduced BPH resistance and vascular wall thickness. OsMYC2, a master transcription factor of jasmonate signalling, directly controlled the upregulation of OsCslF6 in response to BPH feeding. The AT‐rich domain of the OsCslF6 promoter varies in rice varieties from different locations and natural variants in this domain were associated with BPH resistance. MLG‐derived oligosaccharides bound to the plasma membrane‐anchored LECTIN RECEPTOR KINASE1 OsLecRK1 and modulated its activity. Thus, our findings suggest that the OsMYC2‐OsCslF6 module regulates pest resistance by modulating MLG production to enhance vascular wall thickness and OsLecRK1‐mediated defence signalling during rice‐BPH interactions. John Wiley and Sons Inc. 2023-03-23 2023-06 /pmc/articles/PMC10214751/ /pubmed/36952539 http://dx.doi.org/10.1111/pbi.14038 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
Dai, Yang‐Shuo
Liu, Di
Guo, Wuxiu
Liu, Zhi‐Xuan
Zhang, Xue
Shi, Li‐Li
Zhou, De‐Mian
Wang, Ling‐Na
Kang, Kui
Wang, Feng‐Zhu
Zhao, Shan‐Shan
Tan, Yi‐Fang
Hu, Tian
Chen, Wu
Li, Peng
Zhou, Qing‐Ming
Yuan, Long‐Yu
Zhang, Zhenfei
Chen, Yue‐Qin
Zhang, Wen‐Qing
Li, Juan
Yu, Lu‐Jun
Xiao, Shi
Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title_full Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title_fullStr Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title_full_unstemmed Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title_short Poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to OsLecRK1‐mediated defence response during rice‐brown planthopper interactions
title_sort poaceae‐specific β‐1,3;1,4‐d‐glucans link jasmonate signalling to oslecrk1‐mediated defence response during rice‐brown planthopper interactions
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10214751/
https://www.ncbi.nlm.nih.gov/pubmed/36952539
http://dx.doi.org/10.1111/pbi.14038
work_keys_str_mv AT daiyangshuo poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT liudi poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT guowuxiu poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT liuzhixuan poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhangxue poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT shilili poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhoudemian poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT wanglingna poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT kangkui poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT wangfengzhu poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhaoshanshan poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT tanyifang poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT hutian poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT chenwu poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT lipeng poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhouqingming poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT yuanlongyu poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhangzhenfei poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT chenyueqin poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT zhangwenqing poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT lijuan poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT yulujun poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions
AT xiaoshi poaceaespecificb1314dglucanslinkjasmonatesignallingtooslecrk1mediateddefenceresponseduringricebrownplanthopperinteractions