Skip to main content
SpringerLink
Log in

Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

A global view of differential expression of genes in CMS-D8 of cotton was presented in this study which will facilitate the understanding of cytoplasmic male sterility in cotton.

Abstract

Cytoplasmic male sterility (CMS) is a maternally inherited trait in higher plants which is incapable of producing functional pollen. However, the male fertility can be restored by one or more nuclear-encoded restorer genes. A genome-wide transcriptome analysis of CMS and restoration in cotton is currently lacking. In this study, Affymetrix GeneChips© Cotton Genome Array containing 24,132 transcripts was used to compare differentially expressed (DE) genes of flower buds at the meiosis stage between CMS and its restorer cotton plants conditioned by the D8 cytoplasm. A total of 458 (1.9 %) of DE genes including 127 up-regulated and 331 down-regulated ones were identified in the CMS-D8 line. Quantitative RT-PCR was used to validate 10 DE genes selected from seven functional categories. The most frequent DE gene group was found to encode putative proteins involved in cell wall expansion, such as pectinesterase, pectate lyase, pectin methylesterase, glyoxal oxidase, polygalacturonase, indole-3-acetic acid-amino synthetase, and xyloglucan endo-transglycosylase. Genes in cytoskeleton category including actin, which plays a key role in cell wall expansion, cell elongation and cell division, were also highly differentially expressed between the fertile and CMS plants. This work represents the first study in utilizing microarray to identify CMS-related genes by comparing overall DE genes between fertile and CMS plants in cotton. The results provide evidence that many CMS-associated genes are mainly involved in cell wall expansion. Further analysis will be required to elucidate the molecular mechanisms of male sterility which will facilitate the development of new hybrid cultivars in cotton.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmed FE, Hall AE, DeMason DA (1992) Heat injury during floral development in cowpea (Vigna unguiculata, Fabaceae). Am J Bot 79:784–791

    Article  Google Scholar 

  • Aitken A (2006) 14–3-3 proteins: a historic overview. Semin Cancer Biol 16:162–172

    Article  PubMed  CAS  Google Scholar 

  • Amagai M, Ariizumi T, Endo M, Hatakeyama K, Kuwata C, Shibata D, Toriyama K, Watanabe M (2003) Identification of anther-specific genes in a cruciferous model plant, Arabidopsis thaliana, by using a combination of Arabidopsis macroarray and mRNA derived from Brassica oleracea. Sex Plant Reprod 15:213–220

    CAS  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD et al (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    Article  PubMed  CAS  Google Scholar 

  • Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725

    Article  PubMed  CAS  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174:483–498

    Article  PubMed  CAS  Google Scholar 

  • Blanchoin L, Boujemaa-Paterski R, Henty JL, Khurana P, Staiger CJ (2010) Actin dynamics in plant cells: a team effort from multiple proteins orchestrates this very fast-paced game. Curr Opin Plant Biol 13:714–723

    Article  PubMed  CAS  Google Scholar 

  • Bourquin V, Nishikubo N, Abe H, Brumer H, Denman S, Eklund M, Christiernin M, Teeri TT, Sundberg B, Mellerowicz EJ (2002) Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell 2002:3073–3088

    Google Scholar 

  • Bunney TD, van Walraven HS, de Boer AH (2001) 14–3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proc Natl Acad Sci USA 98:4249–4254

    Article  PubMed  CAS  Google Scholar 

  • Campbell P, Braam J (1999) Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. Trends Plant Sci 4:361–366

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J, Lagercrantz U, Sundstro J, Teixeira R, 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  PubMed  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Cecchetti V, Altamura M, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799

    Article  PubMed  CAS  Google Scholar 

  • De Rienzo F, Gabdoulline RR, Menziani MC, Wade RC (2000) Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci 9:1439–1454

    Article  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  PubMed  CAS  Google Scholar 

  • Dieterich JH, Braun HP, Schmitz UK (2003) Alloplasmic male sterility in Brassica napus (CMS ‘Tournefortii-Stiewe’) is associated with a special gene arrangement around a novel atp9 gene. Mol Genet Genomics 269:723–731

    Article  PubMed  CAS  Google Scholar 

  • Dong X, Kim WK, Lim YP, Kim YK, Hur Y (2013) Ogura-CMS in Chinese cabbage (Brassica rapa ssp. pekinensis) causes delayed expression of many nuclear genes. Plant Sci 199–200:7–17

    Article  PubMed  Google Scholar 

  • Dzeja P, Terzic A (2009) Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci 10:1729–1772

    Article  PubMed  CAS  Google Scholar 

  • Endo M, Matsubara H, Kokubuna T, Masuko H, Takahata Y, Tsuchiya T, Fukuda H, Demura T, Watanabe M (2002) The advantages of cDNA microarray as an effective tool for identification of reproductive organ-specific genes in a model legume, Lotus japonicas. FEBS Lett 514:229–237

    Article  PubMed  CAS  Google Scholar 

  • Feng C, Wilson HL, Hurley JK et al (2003) Essential role of conserved arginine 160 in intramolecular electron transfer in human sulfite oxidase. Biochemistry 42:12235–12242

    Article  PubMed  CAS  Google Scholar 

  • Fujii S, Toriyama K (2008) DCW11, down-regulated gene 11 in CW-type cytoplasmic male sterile rice, encoding mitochondrial protein phosphatase 2c is related to cytoplasmic male sterility. Plant Cell Physiol 49:633–640

    Article  PubMed  CAS  Google Scholar 

  • Fujii S, Komatsu S, Toriyama K (2007) Retrograde regulation of nuclear gene expression in CW-CMS of rice. Plant Mol Biol 63:405–417

    Article  PubMed  CAS  Google Scholar 

  • Fujii S, Yamada M, Toriyama K (2009) Cytoplasmic male sterility-related protein kinase, OsNek3, is regulated downstream of mitochondrial protein phosphatase 2C, DCW11. Plant Cell Physiol 50:828–837

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337–343

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85

    Article  PubMed  Google Scholar 

  • Huang J, Lee SH, Lin C, Medici R, Hack E, Myers AM (1990) Expression in yeast of the T-urf13 protein from Texas male-sterile maize mitochondria confers sensitivity to methomyl and to Texascytoplasm-specific fungal toxins. EMBO J 9:339–347

    PubMed  CAS  Google Scholar 

  • Huang S, Cerny RE, Qi Y, Bhat D, Aydt CM, Hanson DD, Malloy KP, Ness LA (2003) Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282

    Article  PubMed  CAS  Google Scholar 

  • Jiang CZ, Lu F, Imsabai W (2008) Silencing polygalacturonase expression inhibits tomato petiole abscission. J Exp Bot 59:973–979

    Article  PubMed  CAS  Google Scholar 

  • Kieber J, Rothenberg M, Roman G, Feldmann K, Ecker J (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72:427–441

    Article  PubMed  CAS  Google Scholar 

  • Klinman JP (1996) Mechanisms whereby mononuclear copper proteins functionalize organic substrates. Chemical Rev 96:2541–2562

    Article  CAS  Google Scholar 

  • Knox RB (1984) The pollen grain. In: Johri BM (ed) Embryology of angiosperms. Springer-Verlag, Berlin

    Google Scholar 

  • Lee HF, Mak BS, Chi CS et al (2002) A novel mutation in neonatal isolated sulphite oxidase deficiency. Neuropediatrics 33:174–179

    Article  PubMed  CAS  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  PubMed  CAS  Google Scholar 

  • Mayfield JA, Fiebig A, Johnstone SE, Preuss D (2001) Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292:2482–2485

    Article  PubMed  CAS  Google Scholar 

  • Murray JAH, Crockett N (1992) In: Murray JAH (ed) Antisense RNA and DNA. Wiley-Liss, New York, pp 1–49

  • Pacini E (1990) Tapetum and microspore function. In: Blackmore S, Knox RB (eds) Microspores: evolution and ontogeny. Academic, London, pp 213–237

  • Pang M, Stewart JMcD, Zhang J (2011) A mini-scale hot borate method for the isolation of total RNA from a large number of cotton tissue samples. Afr J Biotechnol 10:15430–15437

    Article  CAS  Google Scholar 

  • Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12

    Article  PubMed  Google Scholar 

  • Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001) Changes in the structure of xyloglucan during cell elongation. Planta 212:842–850

    Article  PubMed  CAS  Google Scholar 

  • Pelletier G, Budar F (2007) The molecular biology of cytoplasmically inherited male sterility and prospects for its engineering. Curr Opin Biotechnol 18:121–125

    Article  PubMed  CAS  Google Scholar 

  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104:15566–15571

    Article  PubMed  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control and gene expression regulation. Plant Physiol 138:744–756

    Article  PubMed  CAS  Google Scholar 

  • Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492

    PubMed  CAS  Google Scholar 

  • Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran S, Christensen HE, Ishimaru Y, Dong CH, Chao-Ming W, Cleary AL, Chua NH (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124:1637–1647

    Article  PubMed  CAS  Google Scholar 

  • Sanders P, Bui A, Weterings K, McIntire K, Hsu YC, Lee P, Truong M, Beals T, Goldberg R (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS ONE 2:e648

    Article  PubMed  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506

    Article  PubMed  CAS  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:S46–S60

    Article  PubMed  CAS  Google Scholar 

  • Singh D, Jermakow A, Swain S (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14:3133–3147

    Article  PubMed  CAS  Google Scholar 

  • Taylor PE, Glover JA, Lavithis M, Craig S, Singh MB, Knox RB, Dennis ES, Chaudhury AM (1998) Genetic control of male fertility in Arabidopsis thaliana: structural analyses of postmeiotic developmental mutants. Planta 205:492–505

    Article  PubMed  CAS  Google Scholar 

  • Theerakulpisut P, Xu H, Singh MB, Pettitt JM, Knox RB (1991) Isolation and developmental expression of Bcpl, an anther-specific cDNA clone in Brassica campestris. Plant Cell 3:1037–1084

    Google Scholar 

  • Tissier AF, Marillonnet S, Klimyuk V, Patel K, Torres MA, Murphy G, Jones JDG (1999) Multiple independent defective Suppressor-mutator transposon insertions in arabidopsis: a tool for functional genomics. Plant Cell 11:1841–1852

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu YG (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687

    Article  PubMed  CAS  Google Scholar 

  • Wilkins TA, Smart LB (1996) Isolation of RNA from plant tissue. In: Krieg PA (ed) A laboratory guide to RNA: isolation, analysis, and synthesis. Wiley-Liss, Inc., New York, pp 21–42

    Google Scholar 

  • Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  PubMed  CAS  Google Scholar 

  • Wise RP, Gobelman-Werner K, Pei D, Dill CL, Schnable PS (1999) Mitochondrial transcript processing and restoration of male fertility in T-cytoplasm maize. J Hered 90:380–385

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Knox RB, Taylor PE, Singh MB (1995) Bcpl, a gene required for male fertility in Arabidopsis. Proc Natl Acad Sci USA 92:2106–2110

    Article  PubMed  CAS  Google Scholar 

  • Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during Berry development in Vitis vinifera using RNA-seq. Plant Physiol 152:1787–1795

    Article  PubMed  CAS  Google Scholar 

  • Zhang JF, Stewart JMcD (2001) Inheritance and genetic relationships of the D8 and D2–2 restorer genes for cotton cytoplasmical male sterility. Crop Sci 41:289–294

    Article  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  PubMed  CAS  Google Scholar 

  • Zhang JF, Turley RB, Stewart JMcD (2008) Comparative analysis of gene expression between CMS-D8 restored plants and normal non-restoring fertile plants in cotton by differential display. Plant Cell Rep 27:553–561

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant and Environmental Sciences, New Mexico State University, Las Cruces, NM, 88003, USA

    Hideaki Suzuki, Laura Rodriguez-Uribe & Jinfa Zhang

  2. Molecular Genetics and Microbiology, University of New Mexico Health Sciences Center, Albuquerque, NM, 87131, USA

    Hideaki Suzuki

  3. Department of Biology, New Mexico State University, Las Cruces, NM, 88003, USA

    Jiannong Xu

Authors
  1. Hideaki Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Rodriguez-Uribe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiannong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinfa Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jinfa Zhang.

Additional information

Communicated by V. Srivastava.

This work is dedicated to the memory of Dr. James McD. Stewart (Department of Crop, Soil and Environmental Sciences, University of Arkansas, Fayetteville, AR, USA) as the developer of the CMS-D8 system in cotton and for his numerous contributions to genetic and genomic studies of the system.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, H., Rodriguez-Uribe, L., Xu, J. et al. Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton. Plant Cell Rep 32, 1531–1542 (2013). https://doi.org/10.1007/s00299-013-1465-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1465-7

Keywords

Search

Navigation