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Pollen Development, a Genetic and Transcriptomic View

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The Pollen Tube

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 3))

Abstract

The haploid gametophyte generation occupies a short but vital phase in the life cycle of flowering plants. The male gametophyte consists of just two or three cells when shed from the anthers as pollen grains. It is this functional specialization that is thought to be a key factor in the evolutionary success of flowering plants. Moreover, pollen development offers an excellent model system to study many fundamentally important biological processes such as polarity, cell fate determination, cell cycle regulation, cell signaling and mechanisms of gene regulation.

In the first part of this chapter we review the progress achieved through genetic analysis in identifying gametophytic mutants and genes required for key aspects of male gametogenesis. In the second part we discuss recent advances in genome-wide transcriptomic studies of haploid gene expression and a critical evaluation of data treatment methods. Finally we provide a perspective of the impact of these data on future strategies for understanding the gametophytic control of pollen development.

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References

  1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Bonhomme S, Horlow C, Vezon D, de Laissardiere S, Guyon A, Ferault M, Marchand M, Bechtold N, Pelletier G (1998) T-DNA mediated disruption of essential gametophytic genes in Arabidopsis is unexpectedly rare and cannot be inferred from segregation distortion alone. Mol Gen Genet 129:444–452

    Google Scholar 

  5. Chen Y-C, McCormick S (1996) sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122:3243–3253

    CAS  PubMed  Google Scholar 

  6. Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S (2004) NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32 Database issue: D575–577

    Google Scholar 

  7. Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis Gene Regulatory Information Server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4:25

    Article  PubMed  Google Scholar 

  8. Dettmer J, Schubert D, Calvo-Weimar O, Stierhof YD, Schmidt R, Schumacher K (2005) Essential role of the V-ATPase in male gametophyte development. Plant J 41:117–124

    Article  CAS  PubMed  Google Scholar 

  9. Dumas C, Berger F, Faure J-E, Matthys-Rochon E (1998) Gametes, fertilization and early embryogenesis in flowering plants. Adv Bot Res 28:231–261

    Article  Google Scholar 

  10. Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis: duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137:297–307

    Article  CAS  PubMed  Google Scholar 

  11. Eady C, Lindsey K, Twell D (1995) The Significance of Microspore Division and Division Symmetry for Vegetative Cell-Specific Transcription and Generative Cell Differentiation. Plant Cell 7:65–74

    Article  CAS  PubMed  Google Scholar 

  12. Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138:2124–2133

    Article  CAS  PubMed  Google Scholar 

  13. Grini PE, Schnittger A, Schwarz H, Zimmermann I, Schwab B, Jurgens G, Hulskamp M (1999) Isolation of ethyl methanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1. Genetics 151:849–863

    CAS  Google Scholar 

  14. Gupta R, Ting JT, Sokolov LN, Johnson SA, Luan S (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 14:2495–2507

    Article  CAS  PubMed  Google Scholar 

  15. Honys D, Combe JP, Twell D, čapková V (2000) The translationally repressed pollen-specific ntp303 mRNA is stored in nonpolysomal mRNPs during pollen maturation. Sex Plant Reprod 13:135–144

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  18. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D (1998) Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149:621–631

    CAS  Google Scholar 

  19. Johnson SA, McCormick S (2001) Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol 126:685–695

    Article  CAS  PubMed  Google Scholar 

  20. Johnson MA, von Besser K, Zhou Q, Smith E, Aux G, Patton D, Levin JZ, Preuss D (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168:971–982

    Article  CAS  Google Scholar 

  21. Johnson-Brousseau SA, McCormick S (2004) A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J 39:761–775

    Article  CAS  PubMed  Google Scholar 

  22. Kang BH, Rancour DM, Bednarek SY (2003) The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation. Plant J 35:1–15

    Article  CAS  PubMed  Google Scholar 

  23. Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290

    Article  CAS  PubMed  Google Scholar 

  24. Lalanne E, Twell D (2002) Genetic control of male germ unit organization in Arabidopsis. Plant Physiol 129:865–875

    Article  CAS  PubMed  Google Scholar 

  25. Lalanne E, Honys D, Johnson A, Borner GHH, Lilley KS, Dupree P, Grossniklaus U, Twell D (2004a) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16:229–240

    Google Scholar 

  26. Lalanne E, Michaelidis C, Moore JM, Gagliano W, Johnson A, Patel R, Howden R, Vielle-Calzada J-P, Grossniklaus U, Twell D (2004b) Analysis of transposon insertion mutants highlights the diversity of mechanisms underlying male progamic development in Arabidopsis. Genetics 167:1975–1986

    Google Scholar 

  27. Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529

    Article  CAS  PubMed  Google Scholar 

  28. Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36

    Article  CAS  PubMed  Google Scholar 

  29. Lum L, Beachy PA (2004) The Hedgehog response network: sensors, switches, and routers. Science 304:1755–1759

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  31. Mascarenhas JP (1990) Gene activity during pollen development. Annu Rev Plant Physiol Plant Mol Biol 41:317–338

    Article  Google Scholar 

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

    Google Scholar 

  33. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flugge UI, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17:760–775

    Article  CAS  PubMed  Google Scholar 

  34. Oh S-A, Park S-K, Jang I, Howden R, Moore JM, Grossniklaus U, Twell D (2003) halfman, an Arabidopsis male gametophytic mutant associated with a 150 kb chromosomal deletion at the site of transposon insertion. Sex Plant Reprod 16:99–102

    Article  CAS  Google Scholar 

  35. Oh S-A, Johnson JA, Smertenko A, Rahman D, Park S-K, Hussey PJ, Twell D (2005) A divergent cellular role for the FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr Biol 15:2107–2111

    Article  CAS  PubMed  Google Scholar 

  36. Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21

    Article  Google Scholar 

  37. Pacini E (1996) Types and meaning of pollen carbohydrate reserves. Sex Plant Reprod 9:362–366

    Article  CAS  Google Scholar 

  38. Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen 1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799

    CAS  PubMed  Google Scholar 

  39. Park SK, Rahman D, Oh SA, Twell D (2004) gemini pollen 2, a male and female gametophytic cytokinesis defective mutation. Sex Plant Reprod 17:63–70

    Article  CAS  PubMed  Google Scholar 

  40. Park SK, Twell D (2001) Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen 1 mutant. Plant Physiol 126:899–909

    Article  CAS  PubMed  Google Scholar 

  41. Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B et al. (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551

    Article  CAS  PubMed  Google Scholar 

  42. Pedersen S, Simonsen V, Loeschcke V (1987) Overlap of gametophytic and sporophytic gene expression in barley. Theor Appl Genet 75:200–206

    Article  Google Scholar 

  43. Procissi A, de Laissardiere S et al. (2001) Five gametophytic mutations affecting pollen development and pollen tube growth in Arabidopsis thaliana. Genetics 158:1773–1783

    CAS  Google Scholar 

  44. Pina C, Pinto F, Feijó 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  CAS  PubMed  Google Scholar 

  45. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  46. Robertson WR, Clark K, Young JC, Sussman MR (2004) An Arabidopsis thaliana plasma membrane proton pump is essential for pollen development. Genetics 168:1677–1687

    Article  CAS  Google Scholar 

  47. Rotman N, Durbarry A, Wardle A, Yang W-C, Chaboud A, Faure J-E, 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 

  48. Schoof H, Ernst R, Nazarov V, Pfeifer L, Mewes HW, Mayer KF (2004) MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource for plant genomics. Nucleic Acids Res 32(Database issue):D373–376

    Google Scholar 

  49. Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11:377–392

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  51. Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y, Muramatsu M, Hayashizaki Y, Kawai J, Carninci P, Itoh M, Ishii Y, Arakawa T, Shibata K, Shinagawa A, Shinozaki K (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145

    Article  PubMed  Google Scholar 

  52. Singh DP, Jermakow AM, Swain SM (2002) Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14:3133–3147

    Article  CAS  PubMed  Google Scholar 

  53. Stinson JR, Eisenberg AJ, Willing RP, Pe MP, Hanson DD, Mascarenhas JP (1987) Genes expressed in the male gametophyte of flowering plants and their isolation. Plant Physiol 83:442–447

    Article  CAS  PubMed  Google Scholar 

  54. Tanksley SD, Zamir D, Rick CM (1981) Evidence for extensive overlap of sporophytic and gametophytic gene expression in Lycopersicon esculentum. Science 213:454–455

    Article  Google Scholar 

  55. Tax FE, Vernon DM (2001) T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics. Plant Physiol 126:1527–1538

    Article  CAS  PubMed  Google Scholar 

  56. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770

    Article  CAS  PubMed  Google Scholar 

  57. Twell D (1992) Use of a nuclear-targeted β-glucuronidase fusion protein to demonstrate vegetative cell-specific gene expression in developing pollen. Plant J 2:887–892

    Article  CAS  Google Scholar 

  58. Twell D (1994) The diversity and regulation of gene expression in the pathway of male gametophyte development. In: Scott RJ, Stead AD (eds) Molecular and Cellular Aspects of Plant Reproduction. Cambridge University Press, Cambridge UK, p 83–135

    Google Scholar 

  59. Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  60. Twell D (2002) Pollen developmental biology. In: O'Neill SD, Roberts JA (eds) Plant Reproduction. Annual Plant Reviews, vol 6. Sheffield Academic Press, Sheffield UK, p 86–153

    Google Scholar 

  61. Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 plays an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4:711–714

    Article  CAS  PubMed  Google Scholar 

  62. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613

    Article  CAS  PubMed  Google Scholar 

  63. Willing RP, Bashe D, Mascarenhas JP (1988) An analysis of the quantity and diversity of messenger RNAs from pollen and shoots of Zea mays. Theor Appl Genet 75:751–753

    Article  CAS  Google Scholar 

  64. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44:1192–1201

    Article  CAS  Google Scholar 

  65. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

D.T. and D.H. gratefully acknowledge the financial support from the Royal Society. D.T. and S-A.O. were supported by BBSRC (91/18532) and D.H. by GAASCR (KJB6038409) and GACR (522/06/0896).

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Correspondence to David Twell .

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Rui Malhó

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Twell, D., Oh, SA., Honys, D. Pollen Development, a Genetic and Transcriptomic View. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_042

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