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Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility

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Abstract

Main Conclusion

Loss of function mutation of rice OsACOS12 impairs lipid metabolism-mediated anther cuticle and pollen wall formation, and interferes with tapetum programmed cell death, leading to male sterility.

Acyl-CoA Synthetase (ACOS) is one of the enzymes activating fatty acids for various metabolic functions in plants. Here, we show that OsACOS12, an orthologue of Arabidopsis ACOS5 in rice, is crucial for rice fertility. Similar to acos5, osaocs12 mutant had no mature pollen. But unlike acos5, osaocs12 produced defective anthers lacking cutin and Ubisch bodies on the epidermal and inner surfaces, respectively, and delayed programmed cell death (PCD)-induced tapetum degradation. Those phenotypic changes were evident at stage 10, during which OsACOS12 had its maximum expression in tapetal cells and microspores. Chemical analysis revealed that the levels of anther cuticular lipid components (wax and cutin monomers) were significantly reduced in osaocs12, while the expression levels of three known lipid biosynthetic genes were unchanged. Recombinant OsACOS12 enzyme was shown to catalyze the conversion of C18:1 fatty acid to C18:1 CoA in vitro. Phylogenetic analysis indicated that OsACOS12 is an ancient and conserved enzyme associated with the plant’s colonization to earth. Collectively, our study suggests that OsACOS12 is an ancient enzyme participating in a conserved metabolic pathway for diversified biochemical functions to secure male reproduction in plants.

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Abbreviations

FID:

Flame ionization detector

GC–MS:

Gas chromatography–mass spectrometry

GUS:

β-Glucuronidase

PCD:

Programmed cell death

HPLC–MS/MS:

High-performance liquid chromatography–mass spectrometer/mass spectrometry

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscopy

TUNEL:

Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling

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Acknowledgements

We thank Lu Zhu (Shanghai Jiao Tong University, SJTU) for help in electron microscopy, Dr. Guorun Qu and Ms. Qian Luo (SJTU) for help in wax and cutin analysis. We appreciate very much to Dr. Sheng Quan (from the SJTU-Metabolon Joint Metabolomics Laboratory) for his critical reading and editing of the Manuscript. This work was supported by funds from the National Key Research and Development Program of China (2016YFD0101107); National Key Technologies Research and Development Program of China (2016YFD0100804); China Innovative Research Team, Ministry of Education, and the Programme of Introducing Talents of Discipline to Universities (111 Project, B14016); The Science and Technology Commission of Shanghai Municipality (13JC1408200).

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Authors and Affiliations

  1. Joint International Research Laboratory of Metabolic and Developmental Sciences, Shanghai Jiao Tong University–University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Xijia Yang, Wanqi Liang, Minjiao Chen, Dabing Zhang & Jianxin Shi

  2. Plant Genomics Center, School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA, 5064, Australia

    Dabing Zhang

  3. Key Laboratory of Crop Marker-Assisted Breeding of Huaian Municipality, Jiangsu Collaborative Innovation Center of Regional Modern Agriculture and Environmental Protection, Huaian, 223300, China

    Dabing Zhang, Xiangxiang Zhao & Jianxin Shi

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  1. Xijia Yang
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  2. Wanqi Liang
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Correspondence to Jianxin Shi.

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Yang, X., Liang, W., Chen, M. et al. Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility. Planta 246, 105–122 (2017). https://doi.org/10.1007/s00425-017-2691-y

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