Skip to main content
Log in

Differential proteomic studies of the genic male-sterile line and fertile line anthers of upland cotton (Gossypium hirsutum L.)

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Pollen development is disturbed in the microspore development stage of the double-recessive nuclear male-sterile line ms5ms6 (Gossypium hirsutum L.). This study aimed to identify differentially expressed anther proteins and their potential roles in pollen development and male sterility. We compared the proteomes of sterile and fertile anthers of the double recessive nuclear male-sterile line ms5ms6. Approximately 1,390 protein spots were detected by two-dimensional differential gel electrophoresis. Proteins with altered accumulation levels in sterile anthers compared with fertile anthers were identified by mass spectrometry and the NCBInr and Viridiplantae EST databases. Down-regulated proteins in the sterile anthers included cytosolic ascorbate peroxidase 1 and glutaminyl-tRNA synthetase (glutamine-tRNA ligase). Several carbohydrate metabolism- and photosynthesis-related enzymes were also present at lower levels in the mutant anthers. By contrast, ATP-dependent RNA helicase eIF4A-13, NADH dehydrogenase subunit 1, enolase, gibberellin 20-oxidase, gibberellin 3-hydroxylase 1, alcohol dehydrogenase 2d, 3-ketoacyl-CoA synthase, and trehalose 6-phosphate synthase were expressed at higher levels in sterile anthers than in fertile anthers. The regulation of upland cotton pollen development involves a complex network of differentially expressed genes. This study provides the foundation for future investigations of gene function in upland cotton pollen development and male sterility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

GMS:

Genic male sterility

GS:

Genic male sterility

2-DE:

Two-dimensional electrophoresis

IPG:

pH gradient

MALDI-TOF–TOF:

Matrix-assisted laser desorption/ionization time-of-flight and time-of-flight

NCBI:

National Center for Biotechnology Information

PCD:

Programmed cell death

CMS:

Cytoplasmic male sterility

ORF:

Open reading frames

TCA:

Trichloroacetic acid

References

  • Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyama K (2003) A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine. Plant Mol Biol 53:107–116

    Article  CAS  PubMed  Google Scholar 

  • Carlsson J, Lagercrantz U, Sundstrom J, Teixeira R, Wellmer F, Wellmer F, Meyerowitz EM, Glimelius K (2007) Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J 49:452–462

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Yu XH, Zhang K, Shi J, De Oliveira S, Schreiber L, Shanklin J, Zhang D (2011) Male Sterile 2 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 

  • Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007) Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol Cell Proteomics 6:207–230

    Article  CAS  PubMed  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 Paepe R, Forchioni A, Chetrit P, Vedel F (1993) Specific mitochondrial proteins in pollen: presence of an additional ATP synthase beta subunit. Proc Natl Acad Sci USA 90:5934–5938

    Article  PubMed Central  PubMed  Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328

    Article  CAS  PubMed  Google Scholar 

  • Endo M, Tsuchiya T, Saito H, Matsubara H, Hakozaki H, Masuko H, Kamada M, Higashitani A, Takahashi H, Fukuda H et al (2004) Tification and molecular characterization of novel anther-specific genes in Oryza sativa L. by using cDNA microarray. Genes Genet Syst 79:213–226

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang R, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U (2009) Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Res 19:1786–1800

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884

    Article  CAS  PubMed  Google Scholar 

  • Hu SW, Fan YF, Zhao HX, Guo XL, Yu CY, Sun GL, Dong CH, Liu SY, Wang HZ (2006) Analysis of MS2Bnap genomic DNA homologous to MS2 gene from Arabidopsis thaliana in two dominant digenic male sterile accessions of oilseed rape (Brassica napus L.). Theor Appl Genet 113:397–406

    Article  CAS  PubMed  Google Scholar 

  • Imin N, Kerim T, Weinman JJ, Rolfe BG (2001) Characterisation of rice anther proteins expressed at the young microspore stage. Proteomics 1:1149–1161

    Article  CAS  PubMed  Google Scholar 

  • Imin N, Kerim T, Rolfe BG, Weinman JJ (2004) Effect of early cold stress on the maturation of rice anthers. Proteomics 4:1873–1882

    Article  CAS  PubMed  Google Scholar 

  • Kaul MLH (1987) Male sterility in higher plants, vol 1005. Springer, Berlin, pp 116–117

    Google Scholar 

  • Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751

    Article  CAS  PubMed  Google Scholar 

  • Kim OK, Jung JH, Park CM (2010) An Arabidopsis F-box protein regulates tapetum degeneration and pollen maturation during anther development. Planta 232:353–366

    Article  CAS  PubMed  Google Scholar 

  • Kyo M, Harada H (1986) Control of the developmental pathway of tobacco pollen in vitro. Planta 168:427–432

    Article  CAS  PubMed  Google Scholar 

  • Laver H, Reynolds S, Moneger F, Leaver C (1991) Mitochondrial genome organization and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J 1:185–193

    Article  CAS  PubMed  Google Scholar 

  • Levings CS (1993) Thoughts on cytoplasmic male sterility in cms-T maize. Plant Cell 5:1285–1290

    Article  PubMed Central  PubMed  Google Scholar 

  • Linke B, Börner T (2005) Mitochondrial effects on flower and pollen development. Mitochondrion 5(6):389–402

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Qu LJ (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1:564–574

    Article  CAS  PubMed  Google Scholar 

  • Lou P, Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2007) Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119

    Article  CAS  Google Scholar 

  • Ma XD, Xing CZ, Guo LP, Gong YC, Wang HL, Zhao YL, Wu JY (2007) Analysis of differentially expressed genes in genic male sterility cotton (Gossypium hirsutum L.) using cDNA-AFLP. J Genet Genom 34(6):536–554

    Article  CAS  Google Scholar 

  • Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatoutd C, Duboisc F, Balliaue T, Valote B, Davanture M et al (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585–598

    Article  CAS  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142–S153

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McNeil KJ, Smith AG (2005) An anther-specific cysteine-rich protein of tomato localized to the tapetum and microspores. J Plant Physiol 162:457–464

    Article  CAS  PubMed  Google Scholar 

  • McNeil KJ, Smith AG (2010) A glycine-rich protein that facilitates exine formation during tomato pollen development. Planta 231:793–808

    Article  CAS  PubMed  Google Scholar 

  • Mihr C, Baumgartner M, Dieterich J-H, Schmitz UK, Braun H-P (2001) Proteomic approach for investigation of cytoplasmic male sterility (CMS) in Brassica. J Plant Physiol 158:787–794

    Article  CAS  Google Scholar 

  • Nakajima Y, Yamamoto T, Muranaka T, Oeda K (2001) A novel orfB-related gene of carrot mitochondrial genomes that is associated with homeotic cytoplasmic male sterility (CMS). Plant Mol Biol 46:99–107

    Article  CAS  PubMed  Google Scholar 

  • Noir S, Brautigam A, Colby T, Schmidt J, Panstruga R (2005) A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem Biophys Res Commun 337:1257–1266

    Article  CAS  PubMed  Google Scholar 

  • Pacini EFG, Hesse M (1985) The tapetum: its form, function and possible phylogeny in embryophyta. Plant Syst Evol 149:155–185

    Article  Google Scholar 

  • Ribarits A, Mamun A, Li S, Resch T, Fiers M, Heberle-Bors E, Liu CM, Touraev A (2007) Combination of reversible male sterility and doubled haploid production by targeted inactivation of cytoplasmic glutamine synthetase in developing anthers and pollen. Plant Biotech J 5:483–494

    Article  CAS  Google Scholar 

  • Ribarits A, Mamun A, Li S, Resch T, Fiers M, Heberle-Bors E, Liu CM, Touraev A (2009) A novel and reversible male sterility system using targeted inactivation of glutamine synthetase and doubled haploidy. In: Advances in Haploid Production in Higher Plants, Springer, Berlin, pp 285–294

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Scott R, Hodge R, Paul W, Draper J (1991) The molecular biology of anther differentiation. Plant Sci 80:167–191

    Article  CAS  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl):S46–S60

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheoran IS, Sawhney VK (2010) Proteome analysis of the normal and Ogura (ogu) CMS anthers of Brassica napus to identify proteins associated with male sterility. Botany 88:217–230

    Article  CAS  Google Scholar 

  • Sheoran IS, Ross AR, Olson DJ, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535

    Article  CAS  PubMed  Google Scholar 

  • Sheoran IS, Pedersen EJ, Ross AR, Sawhney VK (2009a) Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230:779–793

    Article  CAS  PubMed  Google Scholar 

  • Sheoran IS, Ross AR, Olson DJ, Sawhney VK (2009b) Differential expression of proteins in the wild type and 7B-1 male-sterile mutant anthers of tomato (Solanum lycopersicum): a proteomic analysis. J Proteomics 71:624–636

    Article  CAS  PubMed  Google Scholar 

  • Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Hu C, Hu J, Li S, Zhu Y (2009) Quantitative proteomic analysis of CMS-related changes in Honglian CMS rice anther. Protein J 28:341–348

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi M, Sugiyama K, Ishiyama K, Inoue E, Sato T, Takahashi H, Yamaya T (2005) Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1; 1. Plant J 42:641–651

    Article  CAS  PubMed  Google Scholar 

  • Vizcay-Barrena G, Wilson ZA (2006) Altered tapetal PCD and pollen walldevelopment in the Arabidopsis ms1 mutant. J Exp Bot 57:2709–2717

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Zha W, Cheng X, Liu C, Lv L, Liu C, Wang Z, Du B, Chen R, Zhu L, He G (2011) A rice beta-1, 3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233:309–323

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Scali M, Vignani R, Milanesi C, Petersen A, Sari-Gorla M, Cresti M (2004) Male-sterilemutation alters Zea m 1 (b-expansin 1) accumulation in a maize mutant. Sex Plant Reprod 17:41–47

    Article  CAS  Google Scholar 

  • Wang D, Oses-Prieto JA, Li KH, Fernandes JF, Burlingame AL, Walbot V (2010) The male sterile 8 mutation of maize disrupts the temporal progression of the transcriptome and results in the mis-regulation of metabolic functions. Plant J 63:939–951

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang DX, Adams CM, Fernandes JF, Egger RL, Walbot V (2012) A low molecular weight proteome comparison of fertile and male sterile 8 anthers of Zea mays. Plant Biotechnol J 10:925–935

    Article  PubMed Central  PubMed  Google Scholar 

  • Warmke H, Overman M Ann (1972) Cytoplasmic male sterility in Sorghum I. Gallose behavior in fertile and sterile anthers. J Hered 63:103–108

    Google Scholar 

  • Wei L, Fei Z, Wu X, Dong H, Zhou P, Zhang J (2010) Mitochondrial comparative proteomic analysis of sterile line and its maintain line of purple cytoplasmic rice (Oryza sativa). Adv Biosci Biotechnol 1:145–151

    Article  CAS  Google Scholar 

  • Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4:759–771

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu HM, Cheun AY (2000) Programmed cell death in plant reproduction. Plant Mol Biol 44:267–281

    Article  PubMed  Google Scholar 

  • Wu S, O’Leary SJ, Gleddie S, Eudes F, Laroche A, Robert LS (2008) A chalcone synthase-like gene is highly expressed in the tapetum of both wheat (Triticum aestivum L.) and triticale (xTriticosecale Wittmack). Plant Cell Rep 27:1441–1449

    Article  CAS  PubMed  Google Scholar 

  • Yao DX, Zhang XY, Xinhua Zhao XH, Liu CL, Wang CC, Zhang ZH, Zhang CJ, Wei Q, Wang QH, Yan H, Li FG, Su Z (2011) Transcriptome analysis reveals salt-stress-regulated biological processes and key pathways in roots of cotton (Gossypium hirsutum L.). Genomics 98(1):47–55

    Article  CAS  PubMed  Google Scholar 

  • Zheng R, Yue SJ, Xu XY, Liu JY, Xu Q, Wang XL, Han L, Yu DY (2012) Proteome analysis of the wild and YX-1 male sterile mutant anthers of wolfberry (Lycium barbarum L.). PLoS One 7(7):e41861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the other members of our laboratory for help in the research and for insightful remarks. This work was supported by the Natural Science Foundation of Tianjin (12JCQNJC09700, 12JCZDJC23000), the Science and Technology Development Foundation Program of the University in Tianjin (20100606), Doctoral Fund of Tianjin Normal University (52XB1105), Henry Fok Education Fund (20111203210002), and Open Fund of Tianjin Key Laboratory of Animal and Plant Resistance (52XS1210). Thank the referees for helpful comments.

Conflict of interest

The authors declared that they have no conflicts of interest to this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Canming Tang.

Additional information

Yan Ren is the co-first author.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yue, J., Ren, Y., Wu, S. et al. Differential proteomic studies of the genic male-sterile line and fertile line anthers of upland cotton (Gossypium hirsutum L.). Genes Genom 36, 415–426 (2014). https://doi.org/10.1007/s13258-014-0176-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-014-0176-y

Keywords

Navigation