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Global analysis of gene expression in flower buds of Ms-cd1 Brassica oleracea conferring male sterility by using an Arabidopsis microarray

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Abstract

The dominant male sterility gene Ms-cd1 is identified in Brassica oleracea. Electron microscopical observations revealed that abortion of pollen development starts after tetrad formation. This important male sterility phenotype is characterized by lack of degradation of the primary pollen mother cell (PMC) wall and delayed degradation of callose surrounding the tetrads and thus arrest of microspore release. Gene expression of the male sterile and fertile buds was analyzed by heterologous hybridization of Brassica oleracea cRNA onto an Arabidopsis whole genome oligonucleotide microarray. A total of 277 suppressed genes including 40 kinase-, 32 cell wall modification and 29 transport related genes were found to be significantly down regulated >3-fold in the male sterile mutant. The vast majority of the differentially expressed transcripts are found to present late pollen stage specific genes. Kinase genes, cell wall modification genes and ion transport genes were greatly over-represented when compared to their percentage of all flower bud expressed genes and represent 36.5% of the genes suppressed by Ms-cd1. Our results also suggest that Ms-cd1 may blocks an anther developmental pathway with a small number of genes suppressed in tapetum cells which prevent the degradation of callose and PMC wall, which further leads to the suppression of a large number of genes involved in signaling pathways, cell wall modification and ion transport in pollen grains.

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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  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. Sexual Plant Reproduction 15:213–220

    CAS  Google Scholar 

  • Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168

    Article  PubMed  CAS  Google Scholar 

  • Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226

    Article  PubMed  CAS  Google Scholar 

  • Brandes A, Heslop-Harrison JS, Kamm A, Kubis S, Doudrick RL, Schmidt T (1997) Comparative analysis of the chromosomal and genomic organization of Ty1-copia-like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol Biol 33:11–21

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J, Lagercrantz U, Sundstrom 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. The Plant Journal 49:452–462

    Article  PubMed  CAS  Google Scholar 

  • Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    Article  PubMed  CAS  Google Scholar 

  • Franklin-Tong VE (1999) Signaling and the modulation of pollen tube growth. Plant Cell 11:727–738

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hepler PK (1997) Tip growth in pollen tubes: calcium leads the way. Trend Plant Sci 2:79–80

    Article  Google Scholar 

  • Hird DL, Worrall D, Hodge R, Smartt S, Paul W, Scott R (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to beta-1,3-glucanases. Plant J 4:1023–1033

    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 S, McDowell JM, Weise MJ, Meagher RB (1996) The Arabidopsis profilin gene family. Evidence for an ancient split between constitutive and pollen-specific profilin genes. Plant Physiol 111:115–126

    Article  PubMed  CAS  Google Scholar 

  • Jakobsen MK, Poulsen LR, Schulz A, Fleurat-Lessard P, Moller A, Husted S, Schiott M, Amtmann A, Palmgren MG (2005) Pollen development and fertilization in Arabidopsis is dependent on the MALE GAMETOGENESIS IMPAIRED ANTHERS gene encoding a Type V P-type ATPase. Genes Dev 19:2757–2769

    Article  PubMed  CAS  Google Scholar 

  • Jiang L, Yang S, Xie L, Puah C, Zhang X, Yang W, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596

    Article  PubMed  CAS  Google Scholar 

  • Lee HS, Karunanandaa B, McCubbin A, Gilroy S, Kao TH (1996) PRK1, a receptor-like kinase of petunia inflata, is essential for postmeiotic development of pollen. Plant J 9:613–624

    Article  CAS  Google Scholar 

  • Lee HS, Wang J, Tian L, Jiang H, Black MA, Madlung A, Watson B, Lukens L, Pires JC, Wang JJ, Comai L, Osborn TC, Doerge RW, Chen ZJ (2004) Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotechnol J 2:45–57

    Article  PubMed  CAS  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 H (2005) Molecular gentic analysis of microsporogenesis and microgametogenesis in flowering plants Ann Rev Plant Biol 56:393–434

    Article  CAS  Google Scholar 

  • McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275

    Article  PubMed  Google Scholar 

  • Neelam A, Sexton R (1995) Cellulase (endo b-1,4-glucanase) and cell wall breakdown during anther development in the sweet pea (Lathyrus odoratus L.): isolation and characterization of partial cDNA clones. J Plant Physiol 146:622–628

    CAS  Google Scholar 

  • Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460

    Article  PubMed  CAS  Google Scholar 

  • Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133:1170–1180

    Article  PubMed  CAS  Google Scholar 

  • Rhee SY, Somerville CR (1998) Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J 15:79–88

    Article  PubMed  CAS  Google Scholar 

  • Rigola D, Fiers M, Vurro E, Aarts MG (2006) The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis. New Phytol 170:753–765

    Article  PubMed  CAS  Google Scholar 

  • Roberts MR, Foster GD, Blundell RP, Robinson SW, Kumar A, Draper J, Scott R (1993) Gametophytic and sporophytic expression of an anther-specific Arabidopsis thaliana gene. Plant J 3:111–120

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sexton R, Campillo ED, Duncan D, Lewis LN (1990) The purification of an anther cellulase (b(1:4)4-glucan hydrolase) from Lathyrus odoratus L. and its relationship to the similar enzyme found in abscission zones. Plant Sci 67:169–176

    Article  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early Flower Development in Arabidopsis. Plant Cell 2:755–767

    Article  PubMed  CAS  Google Scholar 

  • Taylor AA, Horsch A, Rzepczyk A, Hasenkampf CA, Riggs CD (1997) Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis. Plant J 12:1261–1271

    Article  PubMed  CAS  Google Scholar 

  • Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Lou P, Bonnema G, Yang B, He H, Zhang Y, Fang Z (2005) Linkage mapping of a dominant male sterility gene Ms-cd1 in Brassica oleracea. Genome 48:848–854

    PubMed  CAS  Google Scholar 

  • Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326

    Article  PubMed  CAS  Google Scholar 

  • Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett 555:551–555

    Article  PubMed  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  CAS  Google Scholar 

  • Yang Y, Dudoit S, Luu P, Speed T (2001) Normalization for cDNA microarray. Society for Optical Engineering, San Jose, CA

    Google Scholar 

  • Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58:401–419

    Article  PubMed  CAS  Google Scholar 

  • Zik M, Irish VF (2003) Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15:207–222

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was conducted at the Key Opening Laboratory of Vegetable Genetics and Physiology funded by the Chinese Ministry of Agriculture and the Sino-Dutch Joint Plant Genome Analysis Laboratory at the Institute of Vegetables and Flowers (CAAS). The work was supported by National Natural Science Foundation projects 30370981, 30471188, 30400298 and partly supported by “863” program 2006AA100108.

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Correspondence to Xiaowu Wang.

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Kang, J., Zhang, G., Bonnema, G. et al. Global analysis of gene expression in flower buds of Ms-cd1 Brassica oleracea conferring male sterility by using an Arabidopsis microarray. Plant Mol Biol 66, 177–192 (2008). https://doi.org/10.1007/s11103-007-9261-9

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  • DOI: https://doi.org/10.1007/s11103-007-9261-9

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