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Transcriptome Analysis of Early Anther Development of Cotton Revealed Male Sterility Genes for Major Metabolic Pathways

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Abstract

Anther development in flowering plants is critical for plant breeding and reproduction and is regulated by elaborate coordination of many genes. However, the functions of most genes related to this developmental process remain unknown and understanding of the molecular mechanism of cotton (Gossypium hirsutum L.) genetic male sterility (GMS) is still scant. To better understand the functions of genes related to anther development, we performed a digital gene expression (DGE) analysis between an upland cotton GMS line and its maintainer line. Compared with the maintainer line, we identified 916 up-regulated and 826 down-regulated genes in the GMS line, including 12 transcription factors. Transcriptome profiling analysis showed that many key genes were involved in pentose and glucuronate interconversions, starch and sucrose metabolism, galactose metabolism, alpha-linolenic acid metabolism, peroxisome, monoterpenoid biosynthesis, and sesquiterpenoid biosynthesis. Our analysis provides comprehensive gene expression information at the transcriptional level and lays the foundation1s for further functional analysis of candidate genes required for anther development, and will help understand the molecular mechanism of GMS in cotton.

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References

  • Aarts MG, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira A (1997) The arabidopsis male sterility 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12:615–623

    Article  CAS  PubMed  Google Scholar 

  • Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in arabidopsis. Proc Natl Acad Sci 92:8675–8679

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Changbao L, Jiaqiang S, Hongling J, Xiaoyan W, Chuanyou L (2005) Systemic defense signaling in tomato. Chin Sci Bull 50:1817–1822

    Article  Google Scholar 

  • Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. The Plant Cell Online 19:847–861

    Article  CAS  Google Scholar 

  • Chen W, Yu X-H, Zhang K, Shi J, De Oliveira S, Schreiber L, Shanklin J, Zhang D (2011) Male sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in arabidopsis. Plant Physiol 157:842–853

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Biol 48:355–381

    Article  CAS  Google Scholar 

  • Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130:1645–1656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • de Groot P, Weterings K, de Been M, Wittink F, Hulzink R, Custers J, van Herpen M, Wullems G (2004) Silencing of the pollen-specific gene NTP303 and its family members in tobacco affects in vivo pollen tube growth and results in male sterile plants. Plant Mol Biol 55:715–726

    Article  PubMed  Google Scholar 

  • Deveshwar P, Bovill WD, Sharma R, Able JA, Kapoor S (2011) Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice. BMC Plant Biol 11:78–97

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. The Plant Cell Online 4:129–134

    Article  CAS  Google Scholar 

  • Feng X, Liu F, Liu Y, Yin Z, Han X, Shen F (2010) Studies of new genic male sterility cotton named “21A” in upland cotton (Gossypium hirsutum L.). J Plant Genet Resour 11:433–438

    Google Scholar 

  • Fulda M, Shockey J, Werber M, Wolter FP, Heinz E (2002) Two long-chain acyl-CoA synthetases from arabidopsis thaliana involved in peroxisomal fatty acid β-oxidation. Plant J 32:93–103

    Article  CAS  PubMed  Google Scholar 

  • Goetz M, Godt DE, Guivarc’h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci 98:6522–6527

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hennig L, Gruissem W, Grossniklaus U, Köhler C (2004) Transcriptional programs of early reproductive stages in arabidopsis. Plant Physiol 135:1765–1775

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hruba P, Honys D, Twell D, Čapková V, Tupý J (2005) Expression of β-galactosidase and β-xylosidase genes during microspore and pollen development. Planta 220:931–940

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. The Plant Cell Online 24:2279–2303

    Article  CAS  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in arabidopsis. The Plant Cell Online 13:2191–2209

    Article  CAS  Google Scholar 

  • Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein agamous controls microsporogenesis by regulation of sporocyteless. Nature 430:356–360

    Article  CAS  PubMed  Google Scholar 

  • Klinghammer M, Tenhaken R (2007) Genome-wide analysis of the UDP-glucose dehydrogenase gene family in arabidopsis, a key enzyme for matrix polysaccharides in cell walls. J Exp Bot 58:3609–3621

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Jiang J, Du M-L, Li L, Wang X-L, Li X-B (2013) A cotton gene encoding MYB-like transcription factor is specifically expressed in pollen and is involved in regulation of late anther/pollen development. Plant Cell Physiol 54:893–906

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo X, Sun X, Liu B, Zhu D, Bai X, Cai H, Ji W, Cao L, Wu J, Wang M (2013) Ectopic expression of a WRKY homolog from glycine soja alters flowering time in arabidopsis. PLoS ONE 8:e73295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma J, Skibbe DS, Fernandes J, Walbot V (2008) Male reproductive development: gene expression profiling of maize anther and pollen ontogeny. Genome Biol 9:R18

    Article  Google Scholar 

  • Ma J, Wei H, Song M, Pang C, Liu J, Wang L, Zhang J, Fan S, Yu S (2012) Transcriptome profiling analysis reveals that flavonoid and ascorbate-glutathione cycle are important during anther development in upland cotton. PLoS ONE 7:e49244

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mamun E, Alfred S, Cantrill L, Overall R, Sutton B (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int 30:583–591

    Article  CAS  PubMed  Google Scholar 

  • Mandaokar A, Thines B, Shin B, Markus Lange B, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G (2006) Transcriptional regulators of stamen development in arabidopsis identified by transcriptional profiling. Plant J 46:984–1008

    Article  CAS  PubMed  Google Scholar 

  • Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in arabidopsis. Plant Mol Biol 55:853–867

    Article  CAS  PubMed  Google Scholar 

  • Mu H, Ke J, Liu W, Zhuang C, Yip W (2009) UDP-glucose pyrophosphorylase2 (OsUgp2), a pollen-preferential gene in rice, plays a critical role in starch accumulation during pollen maturation. Chin Sci Bull 54:234–243

    Article  CAS  Google Scholar 

  • Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Richmond TA, Bleecker AB (1999) A defect in β-oxidation causes abnormal inflorescence development in arabidopsis. The Plant Cell Online 11:1911–1923

    CAS  Google Scholar 

  • Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–1149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire K, Hsu Y-C, Lee PY, Truong MT, Beals T, Goldberg R (1999) Anther developmental defects in arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Schneider K, Kienow L, Schmelzer E, Colby T, Bartsch M, Miersch O, Wasternack C, Kombrink E, Stuible H-P (2005) A new type of peroxisomal acyl-coenzyme a synthetase from arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J Biol Chem 280:13962–13972

    Article  CAS  PubMed  Google Scholar 

  • Stintzi A, Browse J (2000) The arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Till A, Lakhani R, Burnett SF, Subramani S (2012) Pexophagy: the selective degradation of peroxisomes. Int J Cell Biol 2012:512721

  • von Malek B, van der Graaff E, Schneitz K, Keller B (2002) The arabidopsis male-sterile mutant dde2-2 is defective in the allene oxide synthase gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216:187–192

    Article  Google Scholar 

  • Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12

    Article  CAS  PubMed  Google Scholar 

  • Wang XL, Li XB (2009) The GhACS1 gene encodes an acyl-CoA synthetase which is essential for normal microsporogenesis in early anther development of cotton. Plant J 57:473–486

    Article  CAS  PubMed  Google Scholar 

  • Wei M, Song M, Fan S, Yu S (2013) Transcriptomic analysis of differentially expressed genes during anther development in genetic male sterile and wild type cotton by digital gene-expression profiling. BMC Genom 14:97

    Article  CAS  Google Scholar 

  • Weterings K, Reijnen W, van Aarssen R, Kortstee A, Spijkers J, van Herpen M, Schrauwen J, Wullems G (1992) Characterization of a pollen-specific cDNA clone from nicotiana tabacum expressed during microgametogenesis and germination. Plant Mol Biol 18:1101–1111

    Article  CAS  PubMed  Google Scholar 

  • Yang S-L, Xie L-F, Mao H-Z, San Puah C, Yang W-C, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the arabidopsis anther. The Plant Cell Online 15:2792–2804

    Article  CAS  Google Scholar 

  • Yang S-L, Jiang L, San Puah C, Xie L-F, Zhang X-Q, Chen L-Q, Yang W-C, Ye D (2005) Overexpression of tapetum determinant1 alters the cell fates in the arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells. Plant Physiol 139:186–191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007a) Male sterility1 is required for tapetal development and pollen wall biosynthesis. The Plant Cell Online 19:3530–3548

    Article  CAS  Google Scholar 

  • Yang X, Li J, Pei M, Gu H, Chen Z, Qu L-J (2007b) Over-expression of a flower-specific transcription factor gene AtMYB24 causes aberrant anther development. Plant Cell Rep 26:219–228

    Article  CAS  PubMed  Google Scholar 

  • Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107:6100–6105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of arabidopsis tapetum development and function by Dysfunctional tapetum1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in arabidopsis. Plant J 52:528–538

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. The Plant Cell Online 22:672–689

    Article  CAS  Google Scholar 

  • Zhao D-Z, Wang G-F, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the arabidopsis anther. Genes Dev 16:2021–2031

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the China Major Projects for Transgenic Breeding (Grant Nos. 2013ZX08005-002 and 2013ZX005-004), and the China Key Development Project for Basic Research (973) (Grant No. 2012CB116208).

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Correspondence to Fafu Shen.

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Zhang, Y., Chen, J., Liu, J. et al. Transcriptome Analysis of Early Anther Development of Cotton Revealed Male Sterility Genes for Major Metabolic Pathways. J Plant Growth Regul 34, 223–232 (2015). https://doi.org/10.1007/s00344-014-9458-5

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  • DOI: https://doi.org/10.1007/s00344-014-9458-5

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