Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility
- 1k Downloads
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.
KeywordsAcyl-activating enzyme Anther cuticle Male sterility Oryza sativa Pollen exine
Flame ionization detector
Gas chromatography–mass spectrometry
Programmed cell death
High-performance liquid chromatography–mass spectrometer/mass spectrometry
Scanning electron microscopy
Transmission electron microscopy
Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling
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).
Compliance with ethical standards
Conflict of interest
The authors declare that there is no conflict of interest.
- Chen L, Chu H, Yuan Z, Pan A, Liang W, Huang H, Shen M, Zhang D, Chen L (2006) Isolation and genetic analysis for rice mutants treated with 60 Co γ-Ray. J Xiamen Univ 45:82–85Google Scholar
- de Azevedo Souza C, Barbazuk B, Ralph S, Bohlmann J, Hamberger B, Douglas C (2008) Genome-wide analysis of a land plant-specific acyl:coenzyme A synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytol 179:987–1003Google Scholar
- Dobritsa AA, Shrestha J, Morant M, Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Møller LB, Preuss D (2009) CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589CrossRefPubMedPubMedCentralGoogle Scholar
- Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, de Azevedo Souza C, Heitz T, Douglas CJ, Legrand M (2010) Analysis of TETRAKETIDE alpha-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Plant Cell 22:4067–4083CrossRefPubMedPubMedCentralGoogle Scholar
- Kim SS, Grienenberger E, Lallemand B et al (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl alpha-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 22:4045–4066CrossRefPubMedPubMedCentralGoogle Scholar
- Lin Y (2012) Functional analysis of anther-specific genes essential for pollen exine development and male fertility in tobacco. Ph. D thesis from The University of Hong KongGoogle Scholar
- Morant M, Jorgensen K, Schaller H, Pinot F, Moller BL, Werck-Reichhart D, Bak S (2007) CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19:1473–1487CrossRefPubMedPubMedCentralGoogle Scholar
- Qin M, Tian T, Xia S, Wang Z, Song L, Yi B, Wen J, Shen J, Ma C, Fu T, Tu J (2016) Heterodimer formation of BnPKSA or BnPKSB with BnACOS5 constitutes a multienzyme complex in tapetal cells and is involved in male reproductive development in Brassica napus. Plant Cell Physiol 57:1643–1656CrossRefPubMedGoogle Scholar
- Wallace S, Chater CC, Kamisugi Y, Cuming AC, Wellman CH, Beerling DJ, Fleming AJ (2015) Conservation of Male Sterility 2 function during spore and pollen wall development supports an evolutionarily early recruitment of a core component in the sporopollenin biosynthetic pathway. New Phytol 205:390–401CrossRefPubMedGoogle Scholar
- Yuan X, Wei J, Zhang F, Zhou S, Zhang W (2011) Expression analysis of anACOS5 rice homologue in floret. J Shanghai Norm Univ (Nat Sci) 40:244–248Google Scholar
- Zhang D, Shi J, Yang X (2016) Role of lipid metabolism in plant pollen exine development. In: Nakamura Y, Li-Beisson Y, eds. Lipids in plant and algae development. Springer, Geneva, pp 315–337Google Scholar