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Emerging data on pollen tube growth and fertilization in flowering plants, 1990–1995

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Summary

Since its discovery at the end of the last century, double fertilization remains of central interest in plant reproductive biology research. Although the sequence of events leading to fertilization is well known from cytological studies, the underlying mechanisms remain to be elucidated. This now seems feasible by the diversification and refinement of recently developed technologies presented in this review. The progress made during the last five years in understanding pollen tube guidance, discharge into the embryo sac, and gametic fusion are described. Future directions are also discussed.

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References

  • Almeida EAC, Huovila A-PJ, Sutherland AE, Stephens LE, Calarco PG, Shaw LM, Mercurio AM, Sonnenberg A, Primakoff P, Myles D, White JM (1995) Mouse egg integrin α6β1 functions as a sperm receptor. Cell 81: 1095–1104

    PubMed  Google Scholar 

  • Blobel CP, Wolfsberg TG, Turk CW, Myles DG, Primakoff P, White JM (1992) A potential fusion peptide and integrin ligand domain in a protein active in sperm-egg fusion. Nature 356: 248–252

    PubMed  Google Scholar 

  • Brawley SH (1990) The fast block against polyspermy in fucoid algae is an electrical block. Dev Biol 144: 94–106

    Google Scholar 

  • Breton C, Faure J-E, Dumas C (1995) From in vitro fertilization to early embryogenesis in maize. Protoplasma 187: 3–12

    Google Scholar 

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

    Google Scholar 

  • Campenot MK, Zhang G, Cutler AJ, Cass DD (1992)Zea mays embryo sacs in culture. I. Plant regeneration from 1 day after pollination embryos. Am J Bot 79: 1368–1373

    Google Scholar 

  • Capus MG (1878) Anatomie du tissu conducteur. Ann Sci Nat 7: 207–291

    Google Scholar 

  • Chaboud A, Perez R (1992) Generative cells and male gametes: isolation, physiology, and biochemistry. Int Rev Cytol 140: 205–232

    Google Scholar 

  • Chasan R (1992) Frontiers in fertilization. Plant Cell 4: 369–371

    PubMed  Google Scholar 

  • Chaubal R, Reger BJ (1990) Relatively high calcium is localized in synergid cells of wheat ovaries. Sex Plant Reprod 3: 98–102

    Google Scholar 

  • — — (1992a) Calcium in the synergid cells and other regions of pearl millet ovaries. Sex Plant Reprod 5: 34–46

    Google Scholar 

  • — — (1992b) The dynamics of calcium distribution in the synergid cells of wheat after pollination. Sex Plant Reprod 5: 206–213

    Google Scholar 

  • — — (1993) Prepollination degeneration in mature synergids of pearl millet: an examination using antimonate fixation to localize calcium. Sex Plant Reprod 6: 225–238

    Google Scholar 

  • Cheung AY (1995) Pollen-pistil interactions in compatible pollination. Proc Natl Acad Sci USA 92: 3077–3080

    PubMed  Google Scholar 

  • —, Wang H, Wu H-M (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82: 381–393

    Google Scholar 

  • Dresselhaus T, Lörz H, Kranz E (1994) Representative cDNA libraries from few plant cells. Plant J 5: 605–610

    PubMed  Google Scholar 

  • Dumas C, Faure J-E (1995) Use of in vitro fertilization and zygote culture in crop improvement. Curr Opin Biotech 6: 183–188

    Google Scholar 

  • —, Mogensen HL (1993) Gametes and fertilization: maize as a model system for experimental embryogenesis in flowering plants. Plant Cell 5: 1337–1348

    PubMed  Google Scholar 

  • Dupuis I (1992) In vitro pollination: a new tool for analysing environmental stress. Int Rev Cytol 140: 391–405

    Google Scholar 

  • —, Dumas C (1990) Biochemical markers of female receptivity in maize (Zea mays L.) assessed using in vitro fertilization. Plant Sci 70: 11–19

    Google Scholar 

  • Faure J-E, Mogensen HL, Kranz E, Digonnet C, Dumas C (1992) Ultrastructural characterization and three-dimensional reconstruction of isolated maize (Zea mays L.) egg cell protoplasts. Protoplasma 171: 97–103

    Google Scholar 

  • — —, Dumas C, Kranz E, Lörz H (1993) Karyogamy after electrofusion of single egg and sperm cell protoplast from maize (Zea mays L.): cytological evidences and time course. Plant Cell 5: 747–755

    PubMed  Google Scholar 

  • —, Digonnet C, Mól R, Matthys-Rochon E, Dumas C (1994a) In vitro pollination and fertilisation in maize (Zea mays L.): technical procedures and prospects for the dissection of the double fertilisation process. Plant Sci 104: 1–10

    Google Scholar 

  • — —, Dumas C (1994b) An in vitro system for adhesion and fusion of maize gametes. Science 263: 1598–1600

    Google Scholar 

  • Foltz KR, Partin JS, Lennarz WJ (1993) Molecular characterization of the sea urchin egg receptor for sperm. Science 259: 1421–1425

    PubMed  Google Scholar 

  • Friedman WE (1994) The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm. Am J Bot 81: 1468–1486

    Google Scholar 

  • Guǵuen MF (1901) Anatomie comparée du tissu conducteur de style et du stigmate des phanérogames. J Bot Paris 14: 140–300

    Google Scholar 

  • Guignard L (1899) Sur les anthérozoïdes et la double copulation sexuelle chez les végétaux angiospermes. Rev Gén Bot 11: 129–135

    Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y (1986) Pollen-tube chemotropism: fact or delusion? In: Cresti M, Romano D (eds) Biology of reproduction and cell motility in plants and animals. University of Siena Press, Siena, pp 169–174

    Google Scholar 

  • Holm PB, Knudsen S, Mouritzen P, Negri D, Olsen FL, Roué C (1994) Regeneration of fertile barley plants from mechanically isolated protoplasts of the fertilized egg cell. Plant Cell 6: 531–543

    PubMed  Google Scholar 

  • — — — — — — (1995) Regeneration of the barley zygote in ovule culture. Sex Plant Reprod 8: 49–59

    Google Scholar 

  • Huang B-Q, Russel SD (1992a) Female germ unit: organization, isolation, and function. Int Rev Cytol 140: 233–293

    Google Scholar 

  • — — (1992b) Synergid degeneration inNicotiana: a quantitative, fluorochromatic and chlorotetracycline study. Sex Plant Reprod 5: 151–155

    Google Scholar 

  • — — (1994) Fertilization inNicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration. Planta 194: 200–214

    Google Scholar 

  • —, Sheridan WF (1994) Female gametophyte development in maize: microtubular organization and embryo sac polarity. Plant Cell 6: 845–861

    PubMed  Google Scholar 

  • — —, Strout GW, Mao L-J (1990) Organization of isolated embryo sacs and eggs ofPlumbago zeylanica (Plumbaginaceae) before and after fertilization. Am J Bot 77: 1401–1410

    Google Scholar 

  • — —, Russell SD (1993a) Fertilization inNicotiana tabacum — ultrastructural organization of propane-jet-frozen embryo sacs in vivo. Planta 191: 256–264

    Google Scholar 

  • —, Pierson ES, Russell SD, Tiezzi A, Cresti M (1993b) Cytoskeletal organization and modification during pollen tube arrival, gamete delivery and fertilization inPlumbago zeylanica. Zygote 1: 143–154

    PubMed  Google Scholar 

  • Hülskamp M, Kopczak S, Horejsi TF, Kihl BK, Pruitt RE (1995a) Identification of genes required for pollen-stigma recognition inArabidopsis thaliana. Plant J 8: 703–714

    PubMed  Google Scholar 

  • —, Schneitz K, Pruitt RE (1995b) Genetic evidence for a long-range activity that directs pollen tube guidance inArabidopsis. Plant Cell 7: 57–64

    PubMed  Google Scholar 

  • Iwanami Y (1953) Physiological researches of pollen. 5. On the conductive tissue and the growth of the pollen tube in the style. Bot Mag Tokyo 66: 189–196

    Google Scholar 

  • Jaffe LA (1976) Fast block to polyspermy in sea urchin is electrically mediated. Nature 261: 68–71

    PubMed  Google Scholar 

  • Janson J, Willemse MTM (1995) Pollen tube penetration and fertilization inLilium longiflorum (Liliaceae). Am J Bot 82: 186–196

    Google Scholar 

  • Jauh GY, Lord EM (1995) Movement of the tube cell in the lily style in the absence of the pollen grain and the spent pollen tube. Sex Plant Reprod 8: 168–172

    Google Scholar 

  • Jensen WA (1964) Observations on the fusion of nuclei in plants. J Cell Biol 23: 669–672

    PubMed  Google Scholar 

  • —, Fisher DB (1968) Cotton embryogenesis: the entrance and discharge of the pollen tube in the embryo sac. Planta 78: 158–183

    Google Scholar 

  • Keijzer CJ, Reinders MC, Leferinkten Klooster HB (1988) A micromanipulation method for artificial fertilization inTorenia. In: Cresti M, Gori P, Pacini E (eds) Sexual reproduction in higher plants. Springer, Berlin Heidelberg New York Tokyo, pp 119–124

    Google Scholar 

  • Knox RB (1994) 13th International Congress on Sexual Plant Reproduction 1994 — frontiers in sexual plant reproduction research. Sex Plant Reprod 7: 363–365

    Google Scholar 

  • Koornneef M, Hanhart CJ, Thiel F (1989) A genetic and phenotypic description ofEceriferum (cer) mutants inArabidopsis thaliana. J Hered 80: 118–122

    Google Scholar 

  • Kovacs M, Barnabas B, Kranz E (1994) The isolation of viable egg cells of wheat (Triticum aestivum L.). Sex Plant Reprod 7: 311–312

    Google Scholar 

  • Kranz E, Lörz H (1993) In vitro fertilization with isolated, single gametes results in zygotic embryogenesis and fertile maize plants. Plant Cell 5: 739–746

    PubMed  Google Scholar 

  • — — (1994) In vitro fertilization of maize by single egg and sperm cell protoplast fusion mediated by high calcium and high pH. Zygote 2: 125–128

    PubMed  Google Scholar 

  • —, Bautor J, Lörz H (1991a) In vitro fertilization of single isolated gametes by electrofusion. Sex Plant Reprod 4: 12–16

    Google Scholar 

  • — — — (1991b) Electrofusion-mediated transmission of cytoplasmic organelles through the in vitro fertilization process, fusion of sperm cells with synergids and central cells, and cell reconstruction in maize. Sex Plant Reprod 4: 17–21

    Google Scholar 

  • —, Lörz H, Digonnet C, Faure J-E (1992) In vitro fusion of gametes and production of zygotes. Int Rev Cytol 140: 407–423

    Google Scholar 

  • —, Von Wiegen P, Lörz H (1995) Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes. Plant J 8: 9–23

    Google Scholar 

  • Leduc N, Matthys-Rochon E, Dumas C (1995) Deleterious effect of minimal enzymatic treatments on the development of isolated maize embryo sacs in culture. Sex Plant Reprod 8: 313–317

    Google Scholar 

  • Lord EM, Sanders LC (1992) Roles for the extracellular matrix in plant development and pollination: a special case of cell movement in plants. Dev Biol 153: 16–28

    PubMed  Google Scholar 

  • Malhó R, Read ND, Pais MS, Trewavas AJ (1994) Role of cytosolic free calcium in the reorientation of pollen tube growth. Plant J 5: 331–341

    Google Scholar 

  • — —, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7: 1173–1184

    PubMed  Google Scholar 

  • Mascarenhas JP (1993) Molecular mechanisms of pollen tube growth and differentiation. Plant Cell 5: 1303–1314

    PubMed  Google Scholar 

  • —, Machlis L (1964) Chemotropic response of the pollen tube ofAntirrhinum to calcium. Plant Physiol 39: 70–77

    Google Scholar 

  • Matthys-Rochon E, Mòl R, Heizmann P, Dumas C (1994) Isolation and microinjection of active sperm nuclei into egg cells and central cells of isolated maize embryo sac. Zygote 2: 29–35

    PubMed  Google Scholar 

  • Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes ofLilium. J Cell Sci 101: 7–12

    Google Scholar 

  • Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci USA 89: 7213–7217

    PubMed  Google Scholar 

  • Modrusan Z, Reiser L, Feldman KA, Fisher RL, Haughn GW (1994) Homeotic transformation of ovules into carpelle-like structures inArabidopsis. Plant Cell 6: 333–349

    PubMed  Google Scholar 

  • Mogensen HL (1988) Exclusion of male mitochondria and plastids during syngamy in barley as a basis for maternal inheritance. Proc Natl Acad Sci USA 85: 2594–2597

    Google Scholar 

  • — (1990) Fertilization and early embryogenesis. In: Chapman CP (ed) Reproductive versatility in the grasses. Cambridge University Press, New York, pp 76–99

    Google Scholar 

  • — (1992) The male germ unit: concept, composition, and significance. Int Rev Cytol 140: 129–147

    Google Scholar 

  • — (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83: 383–404

    Google Scholar 

  • —, Holm PB (1995) Dynamics of nuclear DNA quantities during zygote development in barley. Plant Cell 7: 487–494

    PubMed  Google Scholar 

  • —, Leduc N, Matthys-Rochon E, Dumas C (1995) Nuclear DNA amounts in the egg and zygote of maize (Zea mays L.). Planta 197: 641–645

    Google Scholar 

  • Mól R, Matthys-Rochon E, Dumas C (1993) In vitro culture of fertilized embryo sacs of maize: zygotes and two-celled proembryos can develop into plants. Planta 189: 213–217

    Google Scholar 

  • — — — (1994) The kinetics of cytological events during double fertilization inZea mays L. Plant J 5: 197–206

    Google Scholar 

  • Murgia M, Huang B-Q, Tucker SC, Musgrave ME (1993) Embryo sac lacking antipodal cells inArabidopsis thaliana (Brassicaceae). Am J Bot 80: 824–838

    Google Scholar 

  • Nawaschin SG (1898) Resultate einer Revision der Befruchtungs-vorgänge beiLilium martagon undFritillaria tenella. Bull Acad Imp Sci St Petersburg 33: 39–47

    Google Scholar 

  • O'Driscoll D, Kann C, Read SM, Steer MW (1993) Endocytotic uptake of fluorescent dextrans by pollen tubes grown in vitro. Protoplasma 175: 126–130

    Google Scholar 

  • Obermeyer G, Weisenseel MH (1991) Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56: 319–327

    PubMed  Google Scholar 

  • Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6: 1815–1828

    PubMed  Google Scholar 

  • Pollak PE, Hansen K, Astwood JD, Taylor LP (1995) Conditional male fertility in maize. Sex Plant Reprod 8: 231–241

    Google Scholar 

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

    PubMed  Google Scholar 

  • Rathore KS, Cork RJ, Robinson KR (1991) A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol 148: 612–619

    PubMed  Google Scholar 

  • Reger BJ. Chaubal R, Pressey R (1992a) Chemotropic responses by pearl millet pollen tubes. Sex Plant Reprod 5: 47–56

    Google Scholar 

  • —, Pressey R, Chaubal R (1992b) In vitro chemotropism of pearl millet pollen tubes to stigma tissue: a response to glucose produced in the medium by tissue-bound invertase. Sex Plant Reprod 5: 201–205

    Google Scholar 

  • Reiser L, Fisher RL (1993) The ovule and the embryo sac. Plant Cell 5: 1291–1301

    PubMed  Google Scholar 

  • Robinson-Beers K, Pruitt RE, Gasser CS (1992) Ovule development in wild-typeArabidopsis and two female-sterile mutants. Plant Cell 4: 1237–1249

    PubMed  Google Scholar 

  • Roeckel P, Dumas C (1993) Survival at 20 °C and cryopreservation of isolated sperm cells fromZea mays pollen grains. Sex Plant Reprod 6: 212–216

    Google Scholar 

  • Russell SD (1991) Isolation and characterization of sperm cells in flowering plants. Annu Rev Plant Physiol 42: 189–204

    Google Scholar 

  • — (1992) Double fertilization. Int Rev Cytol 140: 357–388

    Google Scholar 

  • — (1993) The egg cell: development and role in fertilization and early embryogenesis. Plant Cell 5: 1349–1359

    PubMed  Google Scholar 

  • —, Rougier M, Dumas C (1990) Organization of the early post-fertilization megagametophyte ofPopulus deltoides: ultrastructure and implications for male cytoplasmic transmission. Protoplasma 155: 153–165

    Google Scholar 

  • Sanders LC, Lord EM (1989) Directed movement of latex particles in the gynoecia of three species of flowering plants. Science 243: 1606–1608

    Google Scholar 

  • — — (1992) A dynamic role for the stylar matrix in pollen tube extension. Int Rev Cytol 140: 297–318

    Google Scholar 

  • —, Wang C-S, Walling LL, Lord EM (1991) A homolog of the substrate adhesion molecule, vitronectin, occurs in four species of flowering plants. Plant Cell 3: 629–635

    PubMed  Google Scholar 

  • Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165: 299–335

    PubMed  Google Scholar 

  • Strasburger E (1884) Neue Untersuchungen über den Befruchtungsvorgang bei den Phanerogamen. G Fischer, Jena

    Google Scholar 

  • Swope RE, Kropf DL (1993) Pronuclear positioning and migration during fertilization inPelvetia. Dev Biol 157: 269–276

    PubMed  Google Scholar 

  • Tirlapur UK, Van Went JL, Cresti M (1993) Visualization of membrane calcium and calmodulin in embryo sacs in situ and isolated fromPetunia hybrida L. andNicotiana tabacum L. Ann Bot 71: 161–167

    Google Scholar 

  • —, Scali M, Moscatelli A, Del Casino C, Cai G, Tiezzi A, Cresti M (1994) Confocal image analysis of spatial variations in immunocytochemically identified calmodulin during pollen hydration, germination and pollen tube tip growth inNicotiana tabacum L. Zygote 2: 63–68

    PubMed  Google Scholar 

  • —, Kranz E, Cresti M (1995) Characterisation of isolated egg cells, in vitro fusion products and zygotes ofZea mays L. using the technique of image analysis and confocal laser microscopy. Zygote 3: 57–64

    PubMed  Google Scholar 

  • Ueda K, Tanaka I (1994) The basic proteins for male gametic nuclei isolated from pollen grains ofLilium longiflorum. Planta 192: 446–452

    Google Scholar 

  • Van der Maas HM, Zaal MACM, De Jong ER, Van Went JL (1993a) Optimization of isolation and storage of sperm cells from the pollen of perennial ryegrass (Lolium perenne L.). Sex Plant Reprod 6: 64–70

    Google Scholar 

  • — — —, Krens FA, Van Went JL (1993b) Isolation of viable egg cells of perennial ryegrass (Lolium perenne L.). Protoplasma 173: 86–89

    Google Scholar 

  • Webb MC, Gunning BES (1994) Embryo sac development inArabidopsis thaliana. II. The cytoskeleton during megagametogenesis. Sex Plant Reprod 7: 153–163.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Yanagimachi R (1978) Calcium requirement for sperm-egg fusion in mammals. Biol Reprod 19: 949–958

    PubMed  Google Scholar 

  • Yu H-S, Russell SD (1994) Occurrence of mitochondria in the nuclei of tobacco sperm cells. Plant Cell 6: 1477–1484

    PubMed  Google Scholar 

  • —, Huang B-Q, Russell SD (1994) Transmission of male cytoplasm during fertilization inNicotiana tabacum. Sex Plant Reprod 7: 313–323

    Google Scholar 

  • Zhang G, Campenot MK, McGann LE, Cass DD (1992a) Flow cytometric characteristics of sperm cells isolated from pollen ofZea mays L. Plant Physiol 99: 54–59

    Google Scholar 

  • —, Williams CM, Campenot MK, McGann LE, Cass DD (1992b) Improvement of longevity and viability of sperm cells isolated from pollen ofZea mays L. Plant Physiol 100: 47–53

    Google Scholar 

  • —, Gifford DJ, Cass DD (1993) RNA and protein synthesis in sperm cells isolated fromZea mays L. Pollen. Sex Plant Reprod 6: 239–243

    Google Scholar 

  • - Williams CM, Campenot MK, McGann LE, Cutler AJ, Cass DD (1995) Effects of calcium, magnesium, potassium, and boron on sperm cells isolated from pollen ofZea mays L. Sex Plant

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Dedicated to Prof. Dr. Dr. h.c. Eberhard Schnepf on the occasion of his retirement

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Faure, J.E., Aldon, D., Rougier, M. et al. Emerging data on pollen tube growth and fertilization in flowering plants, 1990–1995. Protoplasma 193, 132–143 (1996). https://doi.org/10.1007/BF01276641

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