Abstract
Pollen development in flowering plants is critical for male reproductive success. The pollen wall that protects the pollen from various environment stresses and bacterial infections plays an essential role in pollen development. The formation of pollen wall is associated with the biosynthesis and transport of sporopollenin components. ACOS5 in Arabidopsis encodes an acyl-CoA synthetase 5 required for sporopollenin biosynthesis. We identified the rice homolog of ACOS5 as OsACOS12. The CRISPR/Cas9-mediated OsACOS12 knockout mutant has complete male sterility due to a defect in pollen wall formation. β-Glucuronidase reporter gene analysis and RNA in situ hybridization indicated that OsACOS12 was specifically expressed in tapetum and microspores. The subcellular localization of OsACOS12-YFP demonstrated that OsACOS12 protein was primarily localized in the endoplasmic reticulum and nucleus. Our results suggest that OsACOS12 plays a critical and conserved role in pollen wall formation and pollen development and has implications in rice breeding.
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References
Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460. https://doi.org/10.1146/annurev-arplant-042809-112312
Aya K et al (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472. https://doi.org/10.1105/tpc.108.062935
Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4:879–887. https://doi.org/10.1105/tpc.4.8.879
Blackmore S et al (2007) Pollen wall development in flowering plants. New Phytologist 174:483–498. https://doi.org/10.1111/j.1469-8137.2007.02060.x
Chang Z et al (2016) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1613792113
Chen X et al (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094
Chen Y, Zou T, McCormick S (2016) S-adenosylmethionine synthetase 3 is important for pollen tube growth. Plant Physiol 172:244–253. https://doi.org/10.1104/pp.16.00774
de Azevedo Souza C et al (2009) A novel fatty acyl-CoA synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21:507–525. https://doi.org/10.1105/tpc.108.062513
Dobritsa AA et al (2009) CYP704B1 Is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589. https://doi.org/10.1104/pp.109.144469
Dobritsa AA et al (2010) LAP5 And LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153:937–955. https://doi.org/10.1104/pp.110.157446
Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16 Suppl:S84–S97. https://doi.org/10.1105/tpc.015800
Fellenberg C, Vogt T (2015) Evolutionarily conserved phenylpropanoid pattern on angiosperm pollen. Trends Plant Sci 20:212–218. https://doi.org/10.1016/j.tplants.2015.01.011
Fu Z et al (2014) The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26:1512–1524. https://doi.org/10.1105/tpc.114.123745
Gomez JF, Talle B, Wilson ZA (2015) Anther and pollen development: A conserved developmental pathway. J Integr Plant Biol 57:876–891. https://doi.org/10.1111/jipb.12425
Goujon M et al (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:W695–W699. https://doi.org/10.1093/nar/gkq313
He X et al (2012) Influence of an ER-retention signal on the N-glycosylation of recombinant human alpha-L-iduronidase generated in seeds of Arabidopsis. Plant Mol Biol 79:157–169. https://doi.org/10.1007/s11103-012-9902-5
Heslop-Harrison J (1968) Pollen Wall Dev Sci 161:230–237
Hiei Y et al (1994) Efficient transformation of rice (Oryza Sativa L.) mediated by agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J Cell Mol Biol 6:271–282
Jiang J, Zhang Z, Cao J (2013) Pollen wall development: the associated enzymes and metabolic pathways. Plant Biol 15:249–263. https://doi.org/10.1111/j.1438-8677.2012.00706.x
Jung KH et al (2005) Rice undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722. https://doi.org/10.1105/tpc.105.034090
Kim SS 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 22:4045–4066. https://doi.org/10.1105/tpc.110.080028
Ko SS et al (2014) The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26:2486–2504. https://doi.org/10.1105/tpc.114.126292
Lallemand B et al (2013) Sporopollenin biosynthetic enzymes interact and constitute a metabolon localized to the endoplasmic reticulum of tapetum cells. Plant Physiol 162:616–625. https://doi.org/10.1104/pp.112.213124
Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121
Li N et al (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014. https://doi.org/10.1105/tpc.106.044107
Li H et al (2010) Cytochrome P450 family member CYP704B2 catalyzes the {omega}-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190. https://doi.org/10.1105/tpc.109.070326
Li H et al (2011) Persistent tapetal cell1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630. https://doi.org/10.1104/pp.111.175760
Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, Zheng Y (2016a) Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. 遗传学报:英文版 43:415–419
Li Y et al (2016b) OsACOS12, an orthologue of Arabidopsis acyl-CoA synthetase5, plays an important role in pollen exine formation and anther development in rice BMC. Plant Biol 16:256. https://doi.org/10.1186/s12870-016-0943-9
Liang W, Zhang D (2016) Improving food security: using male fertility for hybrid seed breeding pushing the boundaries of scientific research: 120 years of addressing global issues doi:http://science.Imirus.Com/Mpowered/book/vscim16/i1/p45
Morant M et al (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 19:1473–1487. https://doi.org/10.1105/tpc.106.045948
Niu N et al (2013) EAT1 Promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4:1445. https://doi.org/10.1038/ncomms2396
Qin P et al (2013) ABCG15 Encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in rice. Plant Cell Physiol 54:138–154. https://doi.org/10.1093/pcp/pcs162
Quilichini TD, Douglas CJ, Samuels AL (2014) New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann Bot 114:1189–1201. https://doi.org/10.1093/aob/mcu042
Quilichini TD, Grienenberger E, Douglas CJ (2015) The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113:170–182. https://doi.org/10.1016/j.phytochem.2014.05.002
Shan Q et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688. https://doi.org/10.1038/nbt.2650
Shi J et al (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23:2225–2246. https://doi.org/10.1105/tpc.111.087528
Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20:741–753. https://doi.org/10.1016/j.tplants.2015.07.010
Souza Cde A et al (2008) Genome-wide analysis of a land plant-specific acyl:coenzyme a synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytologist 179:987–1003. https://doi.org/10.1111/j.1469-8137.2008.02534.x
Tamura K et al (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Wang Y et al (2013) Conserved metabolic steps for sporopollenin precursor formation in tobacco and rice. Physiol Plant 149:13–24
Wang W et al (2014) Crystallization and preliminary crystallographic analysis of defective pollen wall (DPW) protein from Oryza sativa Acta crystallographica section F. Struct Biol Commun 70:758–760. https://doi.org/10.1107/S2053230X14008486
Wu L et al (2014) OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice. Plant Cell Rep 33:1881–1899
Wu Y et al (2016) Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J 14:1046
Xu D et al (2016) Defective pollen wall 2 (DPW2) encodes an acyl transferase required for rice pollen development. Plant Physiol. https://doi.org/10.1104/pp.16.00095
Yang X et al (2014) Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J Integr Plant Biol 56:979–994. https://doi.org/10.1111/jipb.12212
Yang X et al (2017) Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility. Planta 11(2017):1–18
Zhang D (2011) Cytological analysis and genetic control of rice anther development. J Genet Genom 38:379
Zhang D, Li H (2014) Exine export in pollen. Plant ABC Transp 2014:49–62
Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54:2342–2353. https://doi.org/10.1007/s11434-009-0348-3
Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55. https://doi.org/10.1016/j.pbi.2013.11.001
Zhang D et al (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162. https://doi.org/10.1104/pp.110.158865
Zhang D, Shi J, Yang X (2016) Role of lipid metabolism in plant pollen exine development. Subcell Biochem 86:315–337. https://doi.org/10.1007/978-3-319-25979-6_13
Zhao G et al (2015) Two ATP binding cassette G (ABCG) transporters, OsABCG26 and OsABCG15, collaboratively regulate rice male reproduction. Plant Physiol 169:2064–2079
Zhou H et al (2016) Development of commercial Thermo-sensitive genic male sterile Rice accelerates hybrid Rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep 6:37395
Acknowledgements
We thank Dr. Yuan Chen at UC Berkeley for the editing and comments on the manuscript.
Funding
This work was supported by the National Natural Science Foundation of China (91435102 and 31570004), the Sichuan provincial funding for distinguished young scholars (2015JQ0048), and the Open Research Fund of State Key Laboratory of Hybrid Rice (Hunan Hybrid Rice Research Center, 2016KF10).
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S.L. and P. L. designed and directed the experiments. D.C. and Yanling L. performed the expression analysis and tissue localization and subcellular localization. Jun Z., Q.D., and S.W. performed the genetic transformations. M.L., T.W., and Q.X. performed the phenotypic characterization of the mutant and the transgenic plants. Yueyang L., A.Z., and L.W. constructed all the vectors. T.Z., Jing Z., Z.H., and L.Q. performed the cloning and functional analysis and collected almost all the data. T.Z. analyzed the data and wrote the main manuscript.
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Zou, T., He, Z., Qu, L. et al. Knockout of OsACOS12 caused male sterility in rice. Mol Breeding 37, 126 (2017). https://doi.org/10.1007/s11032-017-0722-9
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DOI: https://doi.org/10.1007/s11032-017-0722-9