Skip to main content
SpringerLink
Log in

Extracellular Guidance Cues and Intracellular Signaling Pathways that Direct Pollen Tube Growth

  • Chapter
  • First Online:
The Pollen Tube

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

Abstract

Fertilization in flowering plants requires that a pollen tube deliver two sperm to the female gametes, which develop in ovules buried deep within floral tissues. The tube germinates on a receptive stigma and enters the style where it grows rapidly in a nutrient-rich extracellular matrix secreted by cells of the transmitting tract (Lord 2003). Subsequently, it enters the ovary where it continues to grow on the surface of cells while targeting an individual ovule. Inside the ovule, the pollen tube immediately encounters the haploid synergid cells and continues to grow through the filiform apparatus, a specialized cell wall that forms at the basal junction of the two synergids. The journey ends when the tip enters one of the two synergids and bursts.

How does the pollen tube navigate these diverse environments within the pistil to reach a precise cellular target? Recently a great deal of progress has been made toward defining the sources of signals that direct specific stages of the pollen tube journey and toward identifying molecules that direct tube growth. However, our understanding of how the tube changes direction of growth in response to signals presented by floral cells along its path is still limited. For example, no pollen tube receptors have been identified for any of the extracellular guidance cues identified thus far and consequently, it has not been possible to assign specific signal transduction pathways linking the floral environment to changes within the pollen tube that cause reorientation of the tip. Here we review the recent progress toward identification of extracellular guidance cues and highlight efforts to understand how the tube perceives and transduces these signals into changes in the direction of its growth.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, Gasser CS (1997) Interactions among genes regulating ovule development in Arabidopsis thaliana. Genetics 145:1109–1124

    CAS  Google Scholar 

  2. Baltazar BM, Sanchez-Gonzalez JD, de la Cruz-Larios L, Schoper JB (2005) Pollination between maize and teosinte: an important determinant of gene flow in Mexico. Theor Appl Genetics 110:519-526

    Article  PubMed  Google Scholar 

  3. Cheung AY, Wang H, Wu HM (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393

    Article  CAS  PubMed  Google Scholar 

  4. Ding JP, Pickard BG (1993) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3:83–110

    Article  CAS  Google Scholar 

  5. Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138:778–789

    Article  CAS  PubMed  Google Scholar 

  6. Elleman CJ, Franklin Tong V, Dickinson HG (1992) Pollination In Species With Dry Stigmas the Nature Of the Early Stigmatic Response and the Pathway Taken By Pollen Tubes. New Phytol 121:413–424

    Article  Google Scholar 

  7. Geitmann A, Cresti M (1998) Ca2+channels control the rapid expansions in pulsating growth of Petunia hybrida pollen tubes. J Plant Physiol 152:439–447

    CAS  Google Scholar 

  8. Goubet F, Misrahi A, Park SK, Zhang ZN, Twell D, Dupree P (2003) AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol 131:547–557

    Article  CAS  PubMed  Google Scholar 

  9. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169:127–138

    Article  CAS  PubMed  Google Scholar 

  10. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103

    Article  CAS  PubMed  Google Scholar 

  11. Heslop-Harrison J (1986) Pollen-Tube Chemotropism: Fact or Delusion. In: Cresti M, Dallai R (eds) Biol of reproduction and cell motility in plants and animals. Siena: University of Siena Press, Italy, p 169–174

    Google Scholar 

  12. Heslop-Harrison J (1987) Pollen germination and pollen-tube growth. Int Rev Cytol 107:1–78

    Article  Google Scholar 

  13. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (1998) Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 10:2019–2032

    Article  CAS  PubMed  Google Scholar 

  14. Higashiyama T, Kuroiwa H, Kuroiwa T (2003) Pollen-tube guidance: beacons from the female gametophyte. Curr Opin Plant Biol 6:36–41

    Article  PubMed  Google Scholar 

  15. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 293:1480–1483

    Article  CAS  PubMed  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. Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–2159

    Article  CAS  PubMed  Google Scholar 

  18. Hülskamp M, Schneitz K, Pruitt RE (1995) Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7:57–64

    Article  PubMed  Google Scholar 

  19. Johnson MA, Preuss D (2002) Plotting a course: multiple signals guide pollen tubes to their targets. Dev Cell 2:273–281

    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. Kandasamy MK, Nasrallah JB, Nasrallah ME (1994) Pollen-pistil interactions and developmental regulation of pollen tube growth in Arabidopsis. Development 120:3405–3418

    CAS  Google Scholar 

  22. Kaothien P, Ok SH, Shuai B, Wengier D, Cotter R, Kelley D, Kiriakopolos S, Muschietti J, McCormick S (2005) Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant J 42:492–503

    Article  CAS  PubMed  Google Scholar 

  23. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17(11):2981–2992

    Article  CAS  PubMed  Google Scholar 

  24. Kim S, Dong J, Lord EM (2004) Pollen tube guidance: the role of adhesion and chemotropic molecules. Curr Top Dev Biol 61:61–79

    Article  CAS  PubMed  Google Scholar 

  25. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16125–16130

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Lord EM (2003) Adhesion and guidance in compatible pollination. J Exp Bot 54:47–54

    Article  CAS  PubMed  Google Scholar 

  28. Lush WM (1999) Whither chemotropism and pollen tube guidance? Trends Plant Sci 4:413–418

    Article  PubMed  Google Scholar 

  29. Malhó R, Camacho L, Moutinho A (2000) Signalling pathways in pollen tube growth and reorientation. Ann Bot 85(suppl A):59–68

    Google Scholar 

  30. Malhó R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173–1184

    Article  PubMed  Google Scholar 

  31. Malhó R, Trewavas AJ (1996) Localised apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935–1949

    Article  PubMed  Google Scholar 

  32. Marton ML, Cordts S, Broadhvest J, Dresselhaus T (2005) Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307:573–576

    Article  CAS  PubMed  Google Scholar 

  33. Mascarenhas JP (1975) The biochemistry of angiosperm pollen development. Botanical Rev 41:259–314

    Article  CAS  Google Scholar 

  34. Mollet JC, Kim S, Jauh GY, Lord EM (2002) Arabinogalactan proteins, pollen tube growth, and the reversible effects of Yariv phenylglycoside. Protoplasma 219:89–98

    Article  CAS  PubMed  Google Scholar 

  35. Mollet JC, Park SY, Nothnagel EA, Lord EM (2000) A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12:1737–1750

    Article  CAS  PubMed  Google Scholar 

  36. Mouline K, Very AA, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. Genes Dev 16:339–350

    Article  CAS  PubMed  Google Scholar 

  37. Moutinho A, Hussey PJ, Trewavas AJ, Malhó R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci USA 98:10481–10486

    Article  CAS  PubMed  Google Scholar 

  38. Muschietti J, Eyal Y, McCormick S (1998) Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 10:319–330

    Article  CAS  PubMed  Google Scholar 

  39. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603–614

    Article  CAS  PubMed  Google Scholar 

  40. Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59

    Article  CAS  PubMed  Google Scholar 

  41. Pinal CS, Tobin AJ (1998) Uniqueness and redundancy in GABA production. Perspect Dev Neurobiol 5:109–118

    Google Scholar 

  42. Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714

    Article  CAS  PubMed  Google Scholar 

  43. Ray SM, Park SS, Ray A (1997) Pollen tube guidance by the female gametophyte. Development 124:2489–2498

    CAS  PubMed  Google Scholar 

  44. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13:432–436

    Article  CAS  PubMed  Google Scholar 

  45. Sanders L, Lord E (1989) Directed movement of latex particles in the gynoecia of three species of flowering plant. Science 243:1606–1608

    Article  CAS  PubMed  Google Scholar 

  46. Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507

    Article  CAS  PubMed  Google Scholar 

  47. Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127:4511–4518

    CAS  PubMed  Google Scholar 

  48. Swanson R, Edlund AF, Preuss D (1994) Species specificity in pollen-pistil interactions. Annu Rev Genet 38:793–818

    Article  Google Scholar 

  49. Tang W, Ezcurra I, Muschietti J, McCormick S (2002) A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14:2277–2287

    Article  CAS  PubMed  Google Scholar 

  50. Tang W, Kelley D, Ezcurra I, Cotter R, McCormick S (2004) LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J 39:343–353

    Article  CAS  PubMed  Google Scholar 

  51. Wengier D, Valsecchi I, Cabanas ML, Tang WH, McCormick S, Muschietti J (2003) The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc Natl Acad Sci USA 100:6860–6865

    Article  CAS  PubMed  Google Scholar 

  52. Wilhelmi LK, Preuss D (1996) Self-sterility in Arabidopsis due to defective pollen tube guidance. Science 274:1535–1537

    Article  CAS  PubMed  Google Scholar 

  53. Williams EG, Kaul V, Rouse JL, Palser BF (1986) Overgrowth of pollen tubes in embryo sacs of Rhododendron following interspecific pollinations. Aust J Bot 34:413–423

    Article  Google Scholar 

  54. Wu HM, Wang H, Cheung AY (1995) A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82:395–403

    Article  CAS  PubMed  Google Scholar 

  55. Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16:S133–141

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Rebecca Lesiak for creating the figures, Adisorn Chaibang for the micrograph of pollen tubes growing in an Arabidopsis pistil, and Ravishankar Palanivelu for comments on the manuscript.

Author information

Authors and Affiliations

  1. Dept. of Molecular Biology, Cell Biology, and Biochemistry, Brown University, 69 Brown St., 02912, Providence, RI, USA

    Mark A. Johnson

  2. Department of Botany and Plant Sciences, University of California, Riverside, 92521-0124, Berkeley, CA, USA

    Elizabeth Lord

Authors
  1. Mark A. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth Lord
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark A. Johnson .

Editor information

Rui Malhó

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Johnson, M.A., Lord, E. Extracellular Guidance Cues and Intracellular Signaling Pathways that Direct Pollen Tube Growth. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_051

Download citation

Publish with us

Policies and ethics

Search

Navigation