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Proc Natl Acad Sci U S A. 2018 May 22;115(21):5606-5611. doi: 10.1073/pnas.1722068115. Epub 2018 May 7.

Diurnal down-regulation of ethylene biosynthesis mediates biomass heterosis.

Song Q1, Ando A1, Xu D1, Fang L1,2, Zhang T2, Huq E1, Qiao H1, Deng XW3,4,5,6, Chen ZJ7,2.

Author information

1
Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, Center for Computational Biology and Bioinformatics, The University of Texas at Austin, Austin, TX 78712.
2
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 210095 Nanjing, China.
3
State Key Laboratory of Protein and Plant Gene Research, Peking University, 100871 Beijing, China; deng@pku.edu.cn zjchen@austin.utexas.edu.
4
Peking-Tsinghua Center for Life Sciences, Peking University, 100871 Beijing, China.
5
School of Advanced Agriculture Sciences, Peking University, 100871 Beijing, China.
6
School of Life Sciences, Peking University, 100871 Beijing, China.
7
Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, Center for Computational Biology and Bioinformatics, The University of Texas at Austin, Austin, TX 78712; deng@pku.edu.cn zjchen@austin.utexas.edu.

Abstract

Heterosis is widely applied in agriculture; however, the underlying molecular mechanisms for superior performance are not well understood. Ethylene biosynthesis and signaling genes are shown to be down-regulated in Arabidopsis interspecific hybrids. Ethylene is a plant hormone that promotes fruit ripening and maturation but inhibits hypocotyl elongation. Here we report that application of exogenous ethylene could eliminate biomass vigor in Arabidopsis thaliana F1 hybrids, suggesting a negative role of ethylene in heterosis. Ethylene biosynthesis is mediated by the rate-limiting enzyme, 1-aminocyclopropane-1-carboxylate synthase (ACS). Down-regulation of ACS genes led to the decrease of ethylene production, which was associated with the high-vigor F1 hybrids, but not with the low-vigor ones. At the mechanistic level, expression of ACS genes was down-regulated diurnally and indirectly by Circadian Clock Associated 1 (CCA1) during the day and directly by Phyotochrome-Interacting Factor 5 (PIF5) at night. Consistent with the negative role of ethylene in plant growth, biomass vigor was higher in the acs mutants than in wild-type plants, while increasing endogenous ethylene production in the hybridizing parents reduced growth vigor in the hybrids. Thus, integrating circadian rhythms and light signaling into ethylene production is another regulatory module of complex biological networks, leading to biomass heterosis in plants.

KEYWORDS:

ACS; PIF; circadian clock; epigenetics; hybrid vigor

PMID:
29735680
DOI:
10.1073/pnas.1722068115
[Indexed for MEDLINE]
Free PMC Article

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