Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers

Abstract Pumpkin rootstock is commonly used to graft cucurbit crops, improving their ability to withstand stress. While the significance of systemic signals from rootstocks to scions is recognized, the role of root-to-shoot transported mRNAs remains understudied. Cucumber plants often face growth an...

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Main Authors: Miao Zhang, Wenqian Liu, Cuicui Wang, Shujin Lin, Ying Chen, Heran Cui, Chenggang Xiang, Yujia Ma, Xiaojun Li, Yongzhen Lu, Xiao Han, Yihan Dong, Lihong Gao, Wenna Zhang
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-63228-1
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author Miao Zhang
Wenqian Liu
Cuicui Wang
Shujin Lin
Ying Chen
Heran Cui
Chenggang Xiang
Yujia Ma
Xiaojun Li
Yongzhen Lu
Xiao Han
Yihan Dong
Lihong Gao
Wenna Zhang
author_facet Miao Zhang
Wenqian Liu
Cuicui Wang
Shujin Lin
Ying Chen
Heran Cui
Chenggang Xiang
Yujia Ma
Xiaojun Li
Yongzhen Lu
Xiao Han
Yihan Dong
Lihong Gao
Wenna Zhang
author_sort Miao Zhang
collection DOAJ
description Abstract Pumpkin rootstock is commonly used to graft cucurbit crops, improving their ability to withstand stress. While the significance of systemic signals from rootstocks to scions is recognized, the role of root-to-shoot transported mRNAs remains understudied. Cucumber plants often face growth and productivity limitations due to low temperatures. To shed light on the enhancement of chilling tolerance in grafted cucumber scions by pumpkin-derived mRNAs, we revisit the metabolomic and transcriptomic dataset from the cucumber/pumpkin heterograft under chilling condition. We identify pumpkin Ketol-acid reductoisomerase 1 (CmoKARI1) as the key mobile mRNA that specifically travels from pumpkin rootstock to cucumber scion upon early chilling stress. Overexpressing CmoKARI1 results in increased isoleucine level and chilling tolerance in both cucumber and Arabidopsis. The increased isoleucine is further used to synthesize JA-Ile conjugates, activating JA-Ile signaling and enabling heterografts to weather low temperatures. This study represents the instance of a unidirectional mobile mRNA triggered by specific environmental cues.
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issn 2041-1723
language English
publishDate 2025-08-01
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spelling doaj-art-a4c71d01268746109be5181faab3e87d2025-08-24T11:39:28ZengNature PortfolioNature Communications2041-17232025-08-0116111610.1038/s41467-025-63228-1Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbersMiao Zhang0Wenqian Liu1Cuicui Wang2Shujin Lin3Ying Chen4Heran Cui5Chenggang Xiang6Yujia Ma7Xiaojun Li8Yongzhen Lu9Xiao Han10Yihan Dong11Lihong Gao12Wenna Zhang13Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityCollege of Biology Science and Engineering, Fuzhou UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityCollege of Life Science and Technology, Honghe UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityCollege of Biology Science and Engineering, Fuzhou UniversityInstitut de Biologie Moléculaire des Plantes, Centre National de la Recherche Scientifique, UPR 2357, Université de StrasbourgBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityBeijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural UniversityAbstract Pumpkin rootstock is commonly used to graft cucurbit crops, improving their ability to withstand stress. While the significance of systemic signals from rootstocks to scions is recognized, the role of root-to-shoot transported mRNAs remains understudied. Cucumber plants often face growth and productivity limitations due to low temperatures. To shed light on the enhancement of chilling tolerance in grafted cucumber scions by pumpkin-derived mRNAs, we revisit the metabolomic and transcriptomic dataset from the cucumber/pumpkin heterograft under chilling condition. We identify pumpkin Ketol-acid reductoisomerase 1 (CmoKARI1) as the key mobile mRNA that specifically travels from pumpkin rootstock to cucumber scion upon early chilling stress. Overexpressing CmoKARI1 results in increased isoleucine level and chilling tolerance in both cucumber and Arabidopsis. The increased isoleucine is further used to synthesize JA-Ile conjugates, activating JA-Ile signaling and enabling heterografts to weather low temperatures. This study represents the instance of a unidirectional mobile mRNA triggered by specific environmental cues.https://doi.org/10.1038/s41467-025-63228-1
spellingShingle Miao Zhang
Wenqian Liu
Cuicui Wang
Shujin Lin
Ying Chen
Heran Cui
Chenggang Xiang
Yujia Ma
Xiaojun Li
Yongzhen Lu
Xiao Han
Yihan Dong
Lihong Gao
Wenna Zhang
Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
Nature Communications
title Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
title_full Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
title_fullStr Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
title_full_unstemmed Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
title_short Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers
title_sort root to shoot mobile mrna cmokari1 promotes ja ile biosynthesis to confer chilling tolerance in grafted cucumbers
url https://doi.org/10.1038/s41467-025-63228-1
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