OsLAP6/OsPKS1, an orthologue of Arabidopsis PKSA/LAP6, is critical for proper pollen exine formation

Rice - Tập 10 - Trang 1-14 - 2017
Ting Zou1,2, Qiao Xiao1, Wenjie Li1, Tao Luo1, Guoqiang Yuan1, Zhiyuan He1, Mingxing Liu1, Qiao Li1,2, Peizhou Xu1, Jun Zhu1,3, Yueyang Liang1, Qiming Deng1, Shiquan Wang1, Aiping Zheng1, Lingxia Wang1, Ping Li1,3, Shuangcheng Li1,3
1State Key Laboratory of Hybrid Rice, Rice Research Institute, Sichuan Agricultural University, Chengdu, China
2Chongqing Key Laboratory of Economic Plant Biotechnology, Collaborative Innovation Center of Special Plant Industry in Chongqing, Institute of Special Plants, Chongqing University of Arts and Sciences, Yongchuan, China
3State Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, China

Tóm tắt

Male fertility is crucial for rice yield, and the improvement of rice yield requires hybrid production that depends on male sterile lines. Although recent studies have revealed several important genes in male reproductive development, our understanding of the mechanisms of rice pollen development remains unclear. We identified a rice mutant oslap6 with complete male sterile phenotype caused by defects in pollen exine formation. By using the MutMap method, we found that a single nucleotide polymorphism (SNP) variation located in the second exon of OsLAP6/OsPKS1 was responsible for the mutant phenotype. OsLAP6/OsPKS1 is an orthologous gene of Arabidopsis PKSA/LAP6, which functions in sporopollenin metabolism. Several other loss-of-function mutants of OsLAP6/OsPKS1 generated by the CRISPR/Cas9 genomic editing tool also exhibited the same phenotype of male sterility. Our cellular analysis suggested that OsLAP6/OsPKS1 might regulate pollen exine formation by affecting bacula elongation. Expression examination indicated that OsLAP6/OsPKS1 is specifically expressed in tapetum, and its product is localized to the endoplasmic reticulum (ER). Protein sequence analysis indicated that OsLAP6/OsPKS1 is conserved in land plants. OsLAP6/OsPKS1 is a critical molecular switch for rice male fertility by participating in a conserved sporopollenin precursor biosynthetic pathway in land plants. Manipulation of OsLAP6/OsPKS1 has potential for application in hybrid rice breeding.

Tài liệu tham khảo

Aarts MG et al (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12(3):615 Abe A et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30(2):174 Aldemita RR, Hodges TK (1996) Agrobacterium tumefaciens-mediated transformation of japonica and indica rice varieties. Planta 199(4):612–617 Ariizumi T, Toriyama K (2010) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62(1):437–460 Ariizumi T et al (2003) A novel male-sterile mutant of Arabidopsis Thaliana, faceless pollen-1, produces pollen with a smooth and an acetolysis-sensitive exine. Plant Mol Biol 53(1–2):107–116 Atanassov I et al (1998) Expression of an anther-specific chalcone synthase-like gene is correlated with uninucleate microspore development in Nicotiana Sylvestris. Plant Mol Biol 38(6):1169–1178 Blackmore S et al (2007) Pollen wall development in flowering plants. New Phytol 174(3):483–498. doi: 10.1111/j.1469-8137.2007.02060.x Cai DT et al (2001) A new strategy of rice breeding in the 21st century. Searching a new pathway of rice breeding by utilization of double heterosis of wide cross and polyploidization. Acta Agron Sin 27:110–116 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. doi: 10.1073/pnas.1613792113 Chen L et al (2010) Thoughts and practice of some problems about research and application of two-line hybrid rice. Chin J Rice Sci 24(6):641–646. doi: 10.3969/j.issn.1001-7216.2010.06.013 Chen W et al (2011) Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in arabidopsis. Plant Physiol 157(2):842 Chen Y et al (2016) S-adenosylmethionine synthetase 3 is important for pollen tube growth. Plant Physiol 172(1):244–253. doi: 10.1104/pp.16.00774 Cheng S-H et al (2007) Super hybrid rice breeding in China: achievements and prospects. J Integr Plant Biol 49(6):805–810. doi: 10.1111/j.1744-7909.2007.00514.x Colpitts CC et al (2011) PpASCL, a moss ortholog of anther-specific chalcone synthase-like enzymes, is a hydroxyalkylpyrone synthase involved in an evolutionarily conserved sporopollenin biosynthesis pathway. New Phytol 192(4):855–868 Daku RM et al (2016) PpASCL, the Physcomitrella Patens anther-specific chalcone synthase-like enzyme implicated in sporopollenin biosynthesis, is needed for integrity of the moss spore wall and spore viability. PLoS One 11(1):e0146817. doi: 10.1371/journal.pone.0146817 Dar SH et al. (2013) Advances in hybrid rice technology through applications of novel technologies. Crop Improvement: An Integrated Approach. Publisher: MD Publications Pvt Ltd New Delhi. 2013:61–67. de Azevedo Souza et al (2009) A novel fatty Acyl-CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21(2):507–525. doi:10.1105/tpc.108.062513 De CM et al (2011) Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant J 65(2):295–308 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(2):574–589. doi: 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(3):937–955. doi: 10.1104/pp.110.157446 Domínguez E et al (1999) Pollen sporopollenin: degradation and structural elucidation. Sex Plant Reprod 12(3):171–178 Dumas C et al (1998) Gametes, fertilization and early embryogenesis in flowering plants. Adv Bot Res 28(08):231–261 Fan F et al (2017) Development of elite BPH-resistant wide-spectrum restorer lines for three and two line hybrid rice. Front Plant Sci 8:986 Galambosi B et al (2009) Effects of plant sex on the biomass production and secondary metabolites in roseroot (Rhodiola Rosea L.) from the aspect of cultivation. Z ARZNEI- GEWURZPFLA 14(3):114–121 Gershenzon J (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress, vol 18. Recent Advances in Phytochemistry, Springer, US Gnanasekaran M, Vivekanandan PM,S (2008) Correlation & path analysis in two line rice hybrids. Adv Pl Sci 21(2):689–692 Godwin H (1968) Pollen exine formation. Nature 220(5165):389–389 Gomez JF et al (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57(11):876–891. doi: 10.1111/jipb.12425 Goujon M et al (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic acids res 38 (web server issue):W695-699. doi: 10.1093/nar/gkq313 Hafidh S et al (2016) Male gametophyte development and function in angiosperms: a general concept. Plant Reprod 29(1–2):31–51. doi: 10.1007/s00497-015-0272-4 Huang MD, Huang AHC (2009) Analyses of advanced rice anther transcriptomes reveal global tapetum secretory functions and potential proteins for lipid exine formation. Plant Physiol 149(2):694 Jiang J et al (2013) Pollen wall development: the associated enzymes and metabolic pathways. Plant Biol (Stuttg) 15(2):249–263 Joshi SP et al (2001) Use of DNA markers in prediction of hybrid performance and heterosis for a three-line hybrid system in rice. Biochem Genet 39(5–6):179–200 Jung KH et al (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18(11):3015–3032. doi: 10.1105/tpc.106.042044 Khush GS (2013) Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breed 132(5):433–436 Kim SS et al (2010) LAP6/POLYKETIDE SYNTHASE a and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl α-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis Thaliana. Plant Cell 22(12):4045 Kliebenstein DJ (2004) Secondary metabolites and plant/environment interactions: a view through Arabidopsis Thaliana tinged glasses. Plant Cell Environ 27(6):675–684 Lallemand B et al (2013) Sporopollenin biosynthetic enzymes interact and constitute a metabolon localized to the endoplasmic reticulum of tapetum cells. Plant Physiol 162(2):616–625. doi: 10.1104/pp.112.213124 Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44(Web Server issue):W242–W245 Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5(9):1121–1123 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(1):173–190. doi: 10.1105/tpc.109.070326 Li Q et al (2016a) Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genomics 43(6):415–419 Li S et al (2012) Identification of genome-wide variations among three elite restorer lines for hybrid-Rice. PLoS One 7(2):e30952 Li S et al (2016b) The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J 14(11):2134 Li Y et al (2016c) 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(1):256. doi: 10.1186/s12870-016-0943-9 Liu L, Fan XD (2013) Tapetum: regulation and role in sporopollenin biosynthesis in Arabidopsis. Plant Mol Biol 83(3):165–175 Lopez MT, Virmani SS (2000) Development of TGMS lines for developing two-line rice hybrids for the tropics. Euphytica 114(3):211–215 Lu Y et al (2002) Ultrastructural studies on the developmental process of pollen and anther in rice (Oryza Sativa L.) Chin J Rice Sci 16(1):29–37 Mccormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142 McCormick S (2013) Pollen. Curr Biol 23(22):R988–R990. doi: 10.1016/j.cub.2013.08.016 Michel V et al (2009) Improvement of cropping systems by integration of rice breeding: a novel genetic improvement strategy. Euphytica 167(2):161–164 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(5):1473–1487. doi: 10.1105/tpc.106.045948 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(1):138–154. doi: 10.1093/pcp/pcs162 Quanlin et al (2016) Development of japonica photo-sensitive Genic male sterile Rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genomics 43(6):415–419 Rao GM (1977) Efficiency and ffectiveness of gmma rys and EMS in rce. Cytologia 42(3–4):443–450 Rowley JR et al (1981) A model of exine substructure based on dissection of pollen and spore exines. Palynology 5(1):107–152 Shi J et al (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20(11):741–753. doi: 10.1016/j.tplants.2015.07.010 Takagi H et al (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33(5):445–449. doi: 10.1038/nbt.3188 Tamura K et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi: 10.1093/molbev/msr121 Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites [review]. Int J Plant Sci 164(S3):93–102 Virmani SS (1994) Heterosis and hybrid Rice breeding. Monographs on Theoretical & Applied Genetics. Springer, Berlin, Heidelberg. 115(5):301–4. Wallace S et al (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(1):390–401. doi: 10.1111/nph.13012 Wang Y et al (2013) Conserved metabolic steps for sporopollenin precursor formation in tobacco and rice. Physiol Plant 149(1):13–24 Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60(5):1479 Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor App Genet 75(2):225–233 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(3):1046 Xie L et al (2016) Phylogeny and expression analyses reveal important roles for plant PKS III family during the conquest of land by plants and angiosperm diversification. Front Plant Sci 7(136):1312 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(10):979–994 Yang X et al (2017) Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility. Planta 11:1–18 Yi B et al (2010) Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica Napus. Plant J 63(6):925–938. doi: 10.1111/j.1365-313X.2010.04289.x Zhang D, Li H (2014) Exine export in pollen. In: Geisler M (ed) Plant ABC transporters. Springer International Publishing, Cham, pp 49–62. doi: 10.1007/978-3-319-06511-3_4 Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54(14):2342–2353. doi: 10.1007/s11434-009-0348-3 Zhang D et al (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38(9):379–390 Zhang D et al (2016) Role of lipid metabolism in plant pollen Exine development. Subcell Biochem 86:315–337. doi: 10.1007/978-3-319-25979-6_13 Zhang D et al (2017) Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnol J. doi: 10.1111/pbi.12786 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. doi: 10.1038/srep37395 Zhu X et al (2017) The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice. J Integr Plant Biol 59(9):612–628. doi: 10.1111/jipb.12574 Zou T et al (2017a) Knockout of OsACOS12 caused male sterility in rice. Mol Breed 37(10):126 Zou T et al (2017b) An atypical strictosidine synthase, OsSTRL2, plays key roles in anther development and pollen wall formation in rice. Sci Rep 7(1):6863. doi: 10.1038/s41598-017-07064-4