The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula

doi:10.1016/j.pld.2025.10.004

Plant Diversity ›› 2026, Vol. 48 ›› Issue (03): 529-543.DOI: 10.1016/j.pld.2025.10.004

• Articles • Previous Articles Next Articles

The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula

Qing Wu^a,b, Ruoruo Wang^c, Yawen Mao^a,b, Liling Yang^a, Weiyue Zhao^a, Liangliang He^a,b, Shaoli Zhou^a, Jia Luo^a,b, Hailong Zhang^a, Hanyan Feng^d, Yuqi Fang^d, Mingli Liu^e, Yu Liu^a, Jianghua Chen^a,b,d, Baolin Zhao^a,b

a State Key Laboratory of Plant Diversity and Specialty Crops, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China;
b University of Chinese Academy of Sciences, Beijing 100049, China;
c Guizhou Key Laboratory of Agricultural Biotechnology, Biotechnology Institute of Guizhou Province, Guizhou Academy of Agricultural Sciences, Guiyang 550006, China;
d College of Biological Science and Food Engineering, Southwest Forestry University, Kunming 650224, China;
e School of Agriculture, Yunnan University, Kunming 650504, China

Received:2025-07-21 Revised:2025-10-03 Online:2026-06-10 Published:2026-05-25
Contact: Qing Wu,E-mail:wuqing18@mails.ucas.ac.cn;Ruoruo Wang,E-mail:ruozhu_w@163.com;Yawen Mao,E-mail:maoyawen16@mails.ucas.ac.cn;Liling Yang,E-mail:llyang1211@163.com;Weiyue Zhao,E-mail:zhaoweiyue@xtbg.ac.cn;Liangliang He,E-mail:heliangliang@xtbg.ac.cn;Shaoli Zhou,E-mail:zhoushaoli@xtbg.ac.cn;Jia Luo,E-mail:luojia@xtbg.ac.cn;Hailong Zhang,E-mail:zhanghailong0311@163.com;Hanyan Feng,E-mail:fenghanyan0923@163.com;Yuqi Fang,E-mail:fangyuqi@xtbg.ac.cn;Mingli Liu,E-mail:liumingli08@163.com;Yu Liu,E-mail:oklahomaliu@163.com;Jianghua Chen,E-mail:jhchen@xtbg.ac.cn;Baolin Zhao,E-mail:zhaobaolin@xtbg.ac.cn
Supported by:
This research was supported by National Natural Science Foundation of China (32170360, 32470334, 32200681, 32570980, and 32200290), Strategic Priority Research Programs of the Chinese Academy of Sciences (XDA26030301), Yunnan Revitalization Talent Support Program (Yunling Scholar Project to J.C., XDYCQNRC-2022-0179, and XDYC-QNRC-2022-0335), the Youth Innovation Promotion Association CAS (2021395), and the Caiyun Postdoctoral Funding (to S.Z.).

The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula

a State Key Laboratory of Plant Diversity and Specialty Crops, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China;
b University of Chinese Academy of Sciences, Beijing 100049, China;
c Guizhou Key Laboratory of Agricultural Biotechnology, Biotechnology Institute of Guizhou Province, Guizhou Academy of Agricultural Sciences, Guiyang 550006, China;
d College of Biological Science and Food Engineering, Southwest Forestry University, Kunming 650224, China;
e School of Agriculture, Yunnan University, Kunming 650504, China

通讯作者: Qing Wu,E-mail:wuqing18@mails.ucas.ac.cn;Ruoruo Wang,E-mail:ruozhu_w@163.com;Yawen Mao,E-mail:maoyawen16@mails.ucas.ac.cn;Liling Yang,E-mail:llyang1211@163.com;Weiyue Zhao,E-mail:zhaoweiyue@xtbg.ac.cn;Liangliang He,E-mail:heliangliang@xtbg.ac.cn;Shaoli Zhou,E-mail:zhoushaoli@xtbg.ac.cn;Jia Luo,E-mail:luojia@xtbg.ac.cn;Hailong Zhang,E-mail:zhanghailong0311@163.com;Hanyan Feng,E-mail:fenghanyan0923@163.com;Yuqi Fang,E-mail:fangyuqi@xtbg.ac.cn;Mingli Liu,E-mail:liumingli08@163.com;Yu Liu,E-mail:oklahomaliu@163.com;Jianghua Chen,E-mail:jhchen@xtbg.ac.cn;Baolin Zhao,E-mail:zhaobaolin@xtbg.ac.cn
基金资助:
This research was supported by National Natural Science Foundation of China (32170360, 32470334, 32200681, 32570980, and 32200290), Strategic Priority Research Programs of the Chinese Academy of Sciences (XDA26030301), Yunnan Revitalization Talent Support Program (Yunling Scholar Project to J.C., XDYCQNRC-2022-0179, and XDYC-QNRC-2022-0335), the Youth Innovation Promotion Association CAS (2021395), and the Caiyun Postdoctoral Funding (to S.Z.).

Abstract

Abstract: Reactive oxygen species (ROS) play an important role as a key signal in plant adaptation to environment stresses, and the stress-induced anthocyanins accumulation are also critical for plant adaptation; however, molecular mechanisms coordinating these processes remain poorly understood in legumes. Here, we identified a novel player in the ROS-anthocyanin crosstalk signal in the model plant Medicago truncatula. Using the forward-genetic approach, we isolated a leaves with more ROS and anthocyanin1 (lma1) mutant, which exhibits ROS hyperaccumulation in its leaves. The LMA1 gene was then cloned by a whole genome resequencing assay and was found to encode a conserved mitochondria-localized type A DnaJ (DnaJA) protein. Loss of LMA1 function additionally induced ectopic anthocyanin accumulation in their small leaves, supported by upregulation of genes involved in the anthocyanin biosynthesis. The transcriptomic analysis also uncovered the mitochondrial dysfunction in lma1-1, as evidenced by further ultrastructural and physiological analyses showing severe mitochondrial defects and reduced activity of mitochondrial respiratory chain complex I in lma1. Treatment with exogenous H₂O₂ and the ROS scavenger N, N'-dimethylthiourea (DMTU) significantly exacerbated and inhibited ROS as well as anthocyanin accumulation in lma1 mutants, respectively, correlating with the expression dynamics of anthocyanin biosynthetic genes. Overall, we establish that LMA1 maintains mitochondrial integrity to influence ROS and anthocyanin accumulation, revealing a potential mechanism by which DnaJA proteins orchestrate the ROS-driven anthocyanin homeostasis in plants.

Key words: LMA1, DnaJ, ROS, Mitochondria, Anthocyanin, Medicago truncatula

摘要： Reactive oxygen species (ROS) play an important role as a key signal in plant adaptation to environment stresses, and the stress-induced anthocyanins accumulation are also critical for plant adaptation; however, molecular mechanisms coordinating these processes remain poorly understood in legumes. Here, we identified a novel player in the ROS-anthocyanin crosstalk signal in the model plant Medicago truncatula. Using the forward-genetic approach, we isolated a leaves with more ROS and anthocyanin1 (lma1) mutant, which exhibits ROS hyperaccumulation in its leaves. The LMA1 gene was then cloned by a whole genome resequencing assay and was found to encode a conserved mitochondria-localized type A DnaJ (DnaJA) protein. Loss of LMA1 function additionally induced ectopic anthocyanin accumulation in their small leaves, supported by upregulation of genes involved in the anthocyanin biosynthesis. The transcriptomic analysis also uncovered the mitochondrial dysfunction in lma1-1, as evidenced by further ultrastructural and physiological analyses showing severe mitochondrial defects and reduced activity of mitochondrial respiratory chain complex I in lma1. Treatment with exogenous H₂O₂ and the ROS scavenger N, N'-dimethylthiourea (DMTU) significantly exacerbated and inhibited ROS as well as anthocyanin accumulation in lma1 mutants, respectively, correlating with the expression dynamics of anthocyanin biosynthetic genes. Overall, we establish that LMA1 maintains mitochondrial integrity to influence ROS and anthocyanin accumulation, revealing a potential mechanism by which DnaJA proteins orchestrate the ROS-driven anthocyanin homeostasis in plants.

关键词: LMA1, DnaJ, ROS, Mitochondria, Anthocyanin, Medicago truncatula

Qing Wu, Ruoruo Wang, Yawen Mao, Liling Yang, Weiyue Zhao, Liangliang He, Shaoli Zhou, Jia Luo, Hailong Zhang, Hanyan Feng, Yuqi Fang, Mingli Liu, Yu Liu, Jianghua Chen, Baolin Zhao. The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula[J]. Plant Diversity, 2026, 48(03): 529-543.

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The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula

The mitochondrial DnaJA protein LMA1 regulates reactive oxygen species homeostasis and anthocyanin biosynthesis in Medicago truncatula

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