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Regulation of mitochondrial NAD pool via NAD+ transporter 2 is essential for matrix NADH homeostasis and ROS production in Arabidopsis

  • Lilan Luo
  • Yajun He
  • Yannan Zhao
  • Qian Xu
  • Jian Wu
  • Haiyan Ma
  • Hongyan Guo
  • Lin Bai
  • Jianru Zuo
  • Jian-Min Zhou
  • Hong YuEmail author
  • Jiayang LiEmail author
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Abstract

Reactive oxygen species (ROS) play a crucial role in numerous biological processes in plants, including development, responses to environmental stimuli, and programmed cell death (PCD). Deficiency in MOSAIC DEATH 1 (MOD1), a plastid-localized enoyl-ACP reductase essential for de novo fatty acid biosynthesis in Arabidopsis thaliana, leads to the increased malate export from chloroplasts to mitochondria, and the subsequent accumulation of mitochondria-generated ROS and PCD. In this study, we report the identification and characterization of a mod1 suppressor, som592. SOM592 encodes mitochondrion-localized NAD+ transporter 2 (NDT2). We show that the mitochondrial NAD pool is elevated in the mod1 mutant. The som592 mutation fully suppressed mitochondrial NADH hyper-accumulation, ROS production, and PCD in the mod1 mutant, indicating a causal relationship between mitochondrial NAD accumulation and ROS/PCD phenotypes. We also show that in wild-type plants, the mitochondrial NAD+ uptake is involved in the regulation of ROS production in response to continuous photoperiod. Elevation of the alternative respiration pathway can suppress ROS accumulation and PCD in mod1, but leads to growth restriction. These findings uncover a regulatory mechanism for mitochondrial ROS production via NADH homeostasis in Arabidopsis thaliana that is likely important for growth regulation in response to altered photoperiod.

Keywords

mitochondrial NAD pool NAD+ transporter 2 mtROS 

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Notes

Acknowledgements

We thank Prof. Yu Fu and Dr. Huijun Xue (Institute of Microbiology, Chinese Academy of Sciences) for kindly providing the yeast cell strain BY4741 and assistance in yeast double mutant construction, and Nottingham Arabidopsis Stock Centre (NASC) for providing N648685 (som592-2), N450741 (ndt1-1), N423124 (ndt1-2). This work was supported by the National Natural Science Foundation of China (31521001, 91854103, 31661143025).

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Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lilan Luo
    • 1
  • Yajun He
    • 1
    • 2
  • Yannan Zhao
    • 1
  • Qian Xu
    • 1
    • 2
  • Jian Wu
    • 1
  • Haiyan Ma
    • 1
  • Hongyan Guo
    • 1
  • Lin Bai
    • 1
    • 2
  • Jianru Zuo
    • 1
    • 2
  • Jian-Min Zhou
    • 1
    • 2
  • Hong Yu
    • 1
    Email author
  • Jiayang Li
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed DesignChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

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