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Research Article

Mitochondrial small heat shock protein mediates seed germination via thermal sensing

Wei Ma, Xueying Guan, Jie Li, Ronghui Pan, Luyao Wang, Fengjun Liu, Hongyu Ma, Shuijin Zhu, Jin Hu, Yong-Ling Ruan, Xiaoya Chen, and View ORCID ProfileTianzhen Zhang
  1. aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
  2. bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
  3. cDepartment of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China;
  4. dSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia;
  5. eInstitute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 200032 Shanghai, China

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PNAS March 5, 2019 116 (10) 4716-4721; first published February 14, 2019; https://doi.org/10.1073/pnas.1815790116
Wei Ma
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
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Xueying Guan
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
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Jie Li
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
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Ronghui Pan
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
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Luyao Wang
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
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Fengjun Liu
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
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Hongyu Ma
cDepartment of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China;
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Shuijin Zhu
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
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Jin Hu
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
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Yong-Ling Ruan
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
dSchool of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia;
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Xiaoya Chen
eInstitute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 200032 Shanghai, China
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Tianzhen Zhang
aZhejiang Provincial Key Laboratory of Crop Genetic Resources, Institute of Crop Science, Zhejiang University, 310029 Zhejiang, China;
bState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China;
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  • ORCID record for Tianzhen Zhang
  • For correspondence: cotton@zju.edu.cn
  1. Edited by Maarten Koornneef, Max Planck Institute for Plant Breeding Research, Cologne, Germany, and approved January 18, 2019 (received for review September 19, 2018)

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Significance

The propagation of most flowering plant species is determined by the success of seed germination, which is of both economic and ecologic importance. Mitochondria are the energy resource and crucial organelles for plant seed germination. Studying the underlying mechanism is important for us to understand the basic principles of plant development and improve crop yields. Here we identify HSP24.7 as a central activator for temperature-dependent seed germination. HSP24.7 modulates cytochrome C/C1 production in the mitochondrial electron transport chain and induces the generation of reactive oxygen species, which accelerates seed germination. Our work provides a comprehensive framework of how mitochondria regulate seed germination in response to the dynamics of environmental temperature.

Abstract

Seed germination is an energy demanding process that requires functional mitochondria upon imbibition. However, how mitochondria fine tune seed germination, especially in response to the dynamics of environmental temperature, remains largely unknown at the molecular level. Here, we report a mitochondrial matrix-localized heat shock protein GhHSP24.7, that regulates seed germination in a temperature-dependent manner. Suppression of GhHSP24.7 renders the seed insensitive to temperature changes and delays germination. We show that GhHSP24.7 competes with GhCCMH to bind to the maturation subunit protein GhCcmFc to form cytochrome C/C1 (CytC/C1) in the mitochondrial electron transport chain. GhHSP24.7 modulates CytC/C1 production to induce reactive oxygen species (ROS) generation, which consequently accelerates endosperm rupture and promotes seed germination. Overexpression of GhHSP24.7’s homologous genes can accelerate seed germination in Arabidopsis and tomato, indicating its conserved function across plant species. Therefore, HSP24.7 is a critical factor that positively controls seed germination via temperature-dependent ROS generation.

  • seed germination
  • mitochondria
  • ROS
  • temperature
  • HSP

Footnotes

  • ↵1W.M. and X.G. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: cotton{at}zju.edu.cn.
  • Author contributions: W.M., X.G., J.L., R.P., and T.Z. designed research; W.M., J.L., L.W., F.L., and H.M. performed research; W.M., X.G., R.P., Y.-L.R., X.C., and T.Z. analyzed data; and W.M., X.G., R.P., S.Z., J.H., Y.-L.R., X.C., and T.Z. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1815790116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Mitochondrial small heat shock protein mediates seed germination via thermal sensing
Wei Ma, Xueying Guan, Jie Li, Ronghui Pan, Luyao Wang, Fengjun Liu, Hongyu Ma, Shuijin Zhu, Jin Hu, Yong-Ling Ruan, Xiaoya Chen, Tianzhen Zhang
Proceedings of the National Academy of Sciences Mar 2019, 116 (10) 4716-4721; DOI: 10.1073/pnas.1815790116

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Mitochondrial small heat shock protein mediates seed germination via thermal sensing
Wei Ma, Xueying Guan, Jie Li, Ronghui Pan, Luyao Wang, Fengjun Liu, Hongyu Ma, Shuijin Zhu, Jin Hu, Yong-Ling Ruan, Xiaoya Chen, Tianzhen Zhang
Proceedings of the National Academy of Sciences Mar 2019, 116 (10) 4716-4721; DOI: 10.1073/pnas.1815790116
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