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Comparative Analysis of Biological Models used in the Study of Pollen Tube Growth

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Book cover The Pollen Tube

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

Abstract

The mechanisms of pollen tube growth have been studied in a wide variety of plant species. Since the 1990s, with the explosion of molecular genetic analyses in Arabidopsis thaliana, most studies started to focus on this model plant. However, because of their particular characteristics, plant species other than Arabidopsis are still used to reveal physiological mechanisms and identify novel molecules relating to pollen tube growth, including, for example, lily, tobacco, Nicotiana alata, tomato, rice, maize, Brassica spp., corn poppy and Torenia (Table 1). Here, we designate all of these relatively common experimental plants as “biological models” for the study of pollen tube growth. These models sometimes provide a good first step in the identification of novel physiological mechanisms and molecules. As genome sequencing technologies become more advanced, the difficulty of performing molecular analyses in these biological models will decrease. Thus, a better understanding of these biological models will allow researchers to perform unique studies of pollen tube growth. In this chapter, we compare the characteristics of biological models, focusing on in vitro systems, to facilitate the use of these biological models for in vitro analyses.

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References

  1. Aida R, Yoshida K, Kondo T, Kishimoto S, Shibata M (2000) Copigmentation gives bluer flowers on transgenic torenia plants with the antisense dihydroflavonol-4-reductase gene. Plant Sci 160:49–56

    Article  CAS  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. Barinova I, Zhexembekova M, Barsova E, Lukyanov S, Heberle-Bors E, Touraev A (2002) Antirrhinum majus microspore maturation and transient transformation in vitro. J Exp Bot 53:1119–1129

    Article  CAS  PubMed  Google Scholar 

  4. Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    Article  CAS  PubMed  Google Scholar 

  5. Brewbaker JL (1967) The distribution and phylogenetic significance of binucleate and trinucleate pollen grains in the angiosperms. Am J Bot 54:1069–1083

    Article  Google Scholar 

  6. Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865

    Article  CAS  Google Scholar 

  7. Chen YF, Matsubayashi Y, Sakagami Y (2000) Peptide growth factor phytosulfokine-alpha contributes to the pollen population effect. Planta 211:752–755

    Article  CAS  PubMed  Google Scholar 

  8. Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK, Wu HM, Cheung AY (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14:2175–2190

    Article  CAS  PubMed  Google Scholar 

  9. 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 

  10. Cheung AY, Chen CYH, Glaven RH, de Graaf BHJ, Vidali L, Hepler PK, Wu HM (2002) Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to ddpollen tube growth. Plant Cell 14:945–962

    Article  CAS  PubMed  Google Scholar 

  11. Derksen J, Knuiman B, Hoedemaekers K, Guyon A, Bonhomme S, Pierson ES (2002) Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sex Plant Reprod 15:133–139

    Article  Google Scholar 

  12. 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 

  13. Engel ML, Chaboud A, Dumas C, McCormick S (2003) Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 34:697–707

    Article  CAS  PubMed  Google Scholar 

  14. Fauré S, Noyer JL, Carreel F, Horry JP, Bakry F, Lanaud C (1994) Maternal inheritance of chloroplast genome and paternal inheritance of mitochondrial genome in bananas (Musa acuminata). Curr Genet 25:265–269

    Article  PubMed  Google Scholar 

  15. Faure JE, Rotman N, Fortune P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–488

    Article  PubMed  Google Scholar 

  16. Forsthoefel NR, Bohnert HJ, Smith SE (1992) Discordant inheritance of mitochondrial and plastid DNA in diverse alfalfa genotypes. J Hered 83:342–345

    Google Scholar 

  17. Franklin-Tong VE, Lawrence MJ, Franklin FCH (1988) An in vitro bioassay for the stigmatic product of the self-incompatibility gene in Papaver rhoeas L. New Phytol 110:109–118

    Article  Google Scholar 

  18. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2001) A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159:883–892

    CAS  Google Scholar 

  19. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2002) Diverse variation of reproductive barriers in three intraspecific rice crosses. Genetics 160:313–322

    Google Scholar 

  20. Heslop-Harrison J, Heslop-Harrison Y (1986) Pollen-tube chemotropism: fact or delusion? In: Cresti M, Dallai R (eds) Biology of reproduction and cell motility in plant and animals. University of Siena, Siena, Italy, p 169–174

    Google Scholar 

  21. Heslop-Harrison Y, Shivanna KR (1977) Receptive surface of angiosperm stigma. Ann Bot 41:1233–1258

    Google Scholar 

  22. Higashiyama T (2002) The synergid cell: attractor and acceptor of the pollen tube for double fertilization. J Plant Res 115:149–160

    Article  PubMed  Google Scholar 

  23. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (1997) Kinetics of double fertilization in Torenia fournieri based on direct observations of the naked embryo sac. Planta 203:101–110

    Article  CAS  Google Scholar 

  24. 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 

  25. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (2000) Explosive discharge of pollen tube contents in Torenia fournieri. Plant Physiol 122:11–14

    Article  CAS  PubMed  Google Scholar 

  26. 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 

  27. 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 

  28. Hodgkin T (1983) A medium for germinating Brassica pollen in vitro. Cruciferae Newslett 8:62–63

    Google Scholar 

  29. Holdaway-Clarke TL, Weddle NM, Kim S, Robi A, Parris C, Kunkel JG, Hepler PK (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J Exp Bot 54:65–72

    Article  CAS  PubMed  Google Scholar 

  30. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  31. 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 

  32. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  33. Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  CAS  Google Scholar 

  34. Jahnen W, Lush WM, Clarke AE (1989) Inhibition of in vitro pollen tube growth by isolated S-glycoproteins of Nicotiana alata. Plant Cell 1:501–510

    Article  CAS  PubMed  Google Scholar 

  35. Janson J (1993) Placental pollination in Lilium longiflorum thunb. Plant Sci 90:105–115

    Article  Google Scholar 

  36. Kao TH, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16:S72–83

    Article  CAS  PubMed  Google Scholar 

  37. Kariya K (1989) Sterility caused by cooling treatment at the flowering stage in rice plants. 3. Establishment of a method of in vitro pollen germination. Japanese J Crop Sci 58:96–102

    Google Scholar 

  38. 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 17:2981–2992

    Article  CAS  PubMed  Google Scholar 

  39. Khatun S, Flowers TJ (1995) The estimation of pollen viability in rice. J Exp Bot 46:151–154

    Article  CAS  Google Scholar 

  40. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2004) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16125–16130

    Article  Google Scholar 

  41. Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1742

    Article  CAS  PubMed  Google Scholar 

  42. Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  44. Lush WM, Grieser F, Wolters-Arts M (1998) Directional guidance of Nicotiana alata pollen tubes in vitro and on the stigma. Plant Physiol 118:733–741

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  47. Mascarenhas JP, Machlis L (1962a) Chemotropic response of Antirrhinum majus pollen to calcium. Nature 196:292–293

    Google Scholar 

  48. Mascarenhas JP, Machlis L (1962b) The hormonal control of the directional growth of pollen tubes. Vitamins and Hormones 20:347–372

    Google Scholar 

  49. Mascarenhas JP, Machlis L (1962c) The pollen-tube chemotropic factor from Antirrhinum majus: bioassay, extraction, and partial purification. Am J Bot 49:482–489

    Google Scholar 

  50. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957

    Article  CAS  PubMed  Google Scholar 

  51. McCormick S, Yang H (2005) Is there more than one way to attract a pollen tube? Trends Plant Sci 10:260–263

    Article  CAS  PubMed  Google Scholar 

  52. Miki H (1954) A study of tropism of pollen tubes to the pistil. I. Tropism in Lilium. Bot Mag Tokyo 67:143–147

    Google Scholar 

  53. Mòl R, Matthys-Rochon E, Dumas C (1994) The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5:197–206

    Article  Google Scholar 

  54. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2003) Identification of higher plant GlsA, a putative morphogenesis factor of gametic cells. Biochem Biophys Res Commun 306:564–569

    Article  CAS  PubMed  Google Scholar 

  55. Negre F, Kish CM, Boatright J, Underwood B, Shibuya K, Wagner C, Clark DG, Dudareva N (2003) Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell 15:2992–3006

    Article  CAS  PubMed  Google Scholar 

  56. Nitsch JP (1951) Growth and development in vitro of excised ovaries. Am J Bot 38:566–577

    Article  CAS  Google Scholar 

  57. 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 

  58. Preuss D, Lemieux B, Yen G, Davis RW (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev 7:974–985

    Article  CAS  PubMed  Google Scholar 

  59. Raghavan V (2003) Some reflections on double fertilization, from its discovery to the present. New Phytologist 159:565–583

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  61. Read M, Bacic A, Clarke AE (1992) Pollen tube growth in culture. I. Control of morphology and generative cell division in cultured pollen tubes of Nicotiana. In: Ottaviano E, Mulcahy DL, Sari Gorla M, Bergamini Mulcahy G (eds) Angiosperm pollen and ovules. Springer-Verlag, New York, p 162–167

    Google Scholar 

  62. Read SM, Clarke AE, Bacic A (1993) Requirements for division of the generative nucleus in cultured pollen tubes of Nicotiana. Protoplasma 174:101–115

    Article  Google Scholar 

  63. Romagnoli S, Cai G, Cresti M (2003) In vitro assays demonstrate that pollen tube organelles use kinesin-related motor proteins to move along microtubules. Plant Cell 15:251–269

    Article  CAS  PubMed  Google Scholar 

  64. Rudd JJ, Franklin-Tong VE (2003) Signals and targets of the self-incompatibility response in pollen of Papaver rhoeas. J Exp Bot 54:141–148

    Article  CAS  PubMed  Google Scholar 

  65. Russell SD (1984) Ultrastructure of the sperm of Plumbago zeylanica: 2. Quantitative cytology and 3-dimensional organization. Planta 162:385–391

    Article  Google Scholar 

  66. Russell SD (1985) Preferential fertilization in Plumbago zeylanica: ultrastructural evidence for gamete-level recognition in an angiosperm. Proc Natl Acad Sci USA 82:6129–6132

    Article  CAS  PubMed  Google Scholar 

  67. Saito C, Nagata N, Sakai A, Mori K, Kuroiwa H, Kuroiwa T (2002) Angiosperm species that produce sperm cell pairs or generative cells with polarized distribution of DNA-containing organelles. Sex Plant Reprod 15:167–178

    Article  CAS  Google Scholar 

  68. Schreiber DN, Dresselhaus T (2003) In vitro pollen germination and transient transformation of Zea mays and other plant species. Plant Mol Biol Rep 21:31–41

    Article  Google Scholar 

  69. 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 

  70. Shimizu KK, Cork JM, Caicedo AL, Mays CA, Moore RC, Olsen KM, Ruzsa S, Coop G, Bustamante CD, Awadalla P, Purugganan MD (2004) Darwinian selection on a selfing locus. Science 306:2081–2084

    Article  CAS  PubMed  Google Scholar 

  71. Shirasaki R, Katsumata R, Murakami F (1998) Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 279:105–107

    Article  CAS  PubMed  Google Scholar 

  72. Sodmergen, Suzuki T, Kawano S, Nakamura S, Tano S, Kuroiwa T (1992) Behaviour of organelle nuclei (nucleoids) in generative and vegetative cells during maturation of pollen in Lilium longiflorum and Pelargonium zonale. Protoplasma 168:73–82

    Article  Google Scholar 

  73. Sodmergen, Chen GH, Hu ZM, Guo FL, Guan XL (1995) Male gametophyte development in Plumbago zeylanica: cytoplasm localization and cell determination in the early generative cells. Protoplasma 186:79–86

    Article  Google Scholar 

  74. Sogo A, Tobe H (2005) Intermittent pollen-tube growth in pistils of alders (Alnus). Proc Natl Acad Sci USA 102:8770–8775

    Article  CAS  PubMed  Google Scholar 

  75. Stern H (1985) Initiation of meiosis in lily and mouse: some molecular considerations. Arch Anat Microsc Morphol Exp 74:10–13

    CAS  PubMed  Google Scholar 

  76. Takayama S, Isogai A (2003) Molecular mechanism of self-recognition in Brassica self-incompatibility. J Exp Bot 54:149–156

    Article  CAS  PubMed  Google Scholar 

  77. 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 

  78. Tansengco ML, Imaizumi-Anraku H, Yoshikawa M, Takagi S, Kawaguchi M, Hayashi M, Murooka Y (2004) Pollen development and tube growth are affected in the symbiotic mutant of Lotus japonicus, crinkle. Plant Cell Physiol 45:511–520

    Article  CAS  Google Scholar 

  79. Tupy J, Rihova L (1984) Changes and growth effect of pH in pollen-tube culture. J Plant Physiol 115:1–10

    Google Scholar 

  80. Twell D, Klein TM, Fromm ME, McCormick S (1989) Transient expression of chimeric genes delivered into pollen by microprojectile bombardment. Plant Physiol 91:1270–1274

    Article  CAS  PubMed  Google Scholar 

  81. Ueda K, Tanaka I (1994) The basic-proteins of male gametic nuclei isolated from pollen grains of Lilium longiflorum. Planta 192:446–452

    Article  CAS  Google Scholar 

  82. Van Tieghem MP (1869) Végétation libre du pollen et de l'ovule. Ann Sci Nat Botan 12:312–328

    Google Scholar 

  83. Van Went JL, Willemse MTM (1984) Fertilization. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, p 273–317

    Google Scholar 

  84. Vasil IK (1987) Physiology and culture of pollen. Int Rev Cytol 107:127–174

    Article  Google Scholar 

  85. Vervaeke I, Parton E, Maene L, Deroose R, De Proft MP (2002) Pollen tube growth and fertilization after different in vitro pollination techniques of Aechmea fasciata. Euphytica 124:75–83

    Article  Google Scholar 

  86. Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12:2534–2545

    CAS  PubMed  Google Scholar 

  87. Walden DB (1993) In vitro pollen germination. In: Freeling M, Walbot V (eds) The maize hand book. Springer-Verlag, New York, p 723–724

    Google Scholar 

  88. Welk SM, Millington WF, Rosen WG (1965) Chemotropic activity and the pathway of the pollen tube in lily. Am J Bot 52:774–781

    Article  Google Scholar 

  89. Weterings K, Russell SD (2004) Experimental analysis of the fertilization process. Plant Cell 16:S107–118

    Article  CAS  PubMed  Google Scholar 

  90. Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821

    CAS  Google Scholar 

  91. Zhang HQ, Croes AF (1982) A new medium for pollen germination in vitro. Acta Bot Neerl 31:113–119

    Google Scholar 

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  1. Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo, 113-0033, Tokyo; CREST, JST, Japan

    Tetsuya Higashiyama & Rie Inatsugi

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  1. Tetsuya Higashiyama
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  2. Rie Inatsugi
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Correspondence to Tetsuya Higashiyama .

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Rui Malhó

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Higashiyama, T., Inatsugi, R. Comparative Analysis of Biological Models used in the Study of Pollen Tube Growth. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_053

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