PECULIARITIES OF THE REPRODUCTIVE PROCESSES IN THE GYMNOSPERMS.
GAMETOPHYTES’ DEVELOPMENT, POLLINATION AND FERTILIZATION

A. Odintsova, A. Rugusova


DOI: http://dx.doi.org/10.30970/sbi.0702.296

Abstract


The review contains the analysis of the latest literature sourses reproductive processes in gymnosperms, namely gametophytes development, рollination, fertilization. The peculiarities of these processes in the various classes of gymnosperms as also differences and similarities with the Angiosperms are noted. It was shown that male and female gametophyte development goes according to the common plan. Deep adaptations for zoophyly were revealed in Cycadopsida and Gnetopsida, and confirmed with paleontological data in fossil Gymnosperms. Anemophyly in Ginkgo and Pinopsida revealed the high specialized pollination mechanisms. The penetration of the male gametophyte to the female after pollination (post-pollinative stage of the reproductive cycle) reveals a great variability as also fertilization process does. The described facts confirm that differences between the classes of Gymnosperms are comparable with the differences between Gymnosperms and Angiosperms. From another side, common adaptive features between all classes of seed plants exist, and they are connected with seed reproduction. Most specific reproductive processes are typical for Gnetopsida. They tetrasporic female gametophyte, absence of archegonia and differentiated egg cells, “double fertilization”.


Keywords


Gymnosperms, gametophytes, рollination, fertilization, pollen grain, ovule, anemophyly, zoophyly, post-pollinational phase

References


1. Бобров А.В. Филогения хвойных (анализ современных представлений) / под ред. А.П. Меликяна. М. 2002. 194 с.

2. Камелина О.П. Пыльник. Эмбриология цветковых растений. Терминология и концепции: в 3 т. / ред. Т.Б. Батыгина. Т. 1. Генеративные органы цветка. СПб: Мир и семья, 1994. С. 39-40.

3. Козубов Г.М. Генеративные органы голосеменных // Репродуктивные структуры голосеменных (сравнительное описание). Л.: Наука, 1982. С. 7-43.

4. Козубов Г.М., Муратова Е.Н. Современные голосеменные (морфолого-систематический обзор и кариология) / под ред. А.А. Яценко-Хмелевского. Л.: Наука, 1986. 193 с.

5. Мошкович А.М. Эмбриология хвойных (Pinales, Cupressales, Taxales). Под ред. А.А. Чеботаря. Кишинев: Штиинца, 1992. 250 с.

6. Наумова Т.Н. Порогамия. Халазогамия. Эмбриология цветковых растений. Терминология и концепции: в 3 т. / ред. Т.Б. Батыгина. Т. 2. Семя. СПб: Мир и семья, 1997. С. 136-139.

7. Поддубная-Арнольди В.А. Цитоэмбриология покрытосеменных растений. М.: Наука, 1976. 507 с.

8. Ругузов И.А. О двух способах доставки пыльцевого зерна на нуцелусы семяпочек хвойных. Бюлл. ГНБС, 1975; 2(27): 48-50.

9. Ругузов И.А., Склонная Л.У., Ругузова А.И. Новые данные по репродуктивной биологии некоторых хвойных растений. Бюлл. ГБС, 2003; 185: 148-159.

10. Ругузова А.И. Закономерности развития мужской генеративной сферы у некоторых видов голосеменных растений. Вісник КНУ ім. Т.Шевченка. Інтродукція та збереження рослинного різноманіття, 2007; 12-14: 82-88.

11. Ругузова А.И. Репродуктивный цикл Ephedra distachya L. в условиях Крыма: матер. Междунар. научн. конф. "Ученые ботаники Таврического университета: вклад в науку, идеи и их развитие" (Симферополь, 20 мая 2008 г.). Симферополь: ТНУ, 2008. С. 133-137.

12. Ругузова А.И. Формирование мужских репродуктивных структур у трех интродуцированных видов рода Ephedra L. в условиях Южного берега Крыма. Вісник КНУ ім. Т. Шевченка, 2009; 27: 140-143.

13. Тахтаджян А.Л. Высшие растения. Т.1. От псилофитовых до хвойных. М.;Л.: Изд-во АН СССР. 1956. 488 с.

14. Терехин Э.С. Семя и семенное размножение. СПб.: Мир и семья - 95, 1996. 377 с.

15. Тимонин А.К. Низшие Spermatophyta - Низшие семенные растения. Тимонин А.К., Соколов Д.Д., Шипунов А.Б. Ботаника: в 4 т. Т. 4, кн. 2. Систематика высших растений: учебник для студ. высш. учеб. заведений. М.: Изд. центр «Академия», 2009. 352 с.

16. Фегри К., Ван дер Пэйл Л. Основы экологии опыления. М.: Мир, 1982. 379 с.

17. Шевченко С.В. Кузьмина Т.Н., Марко Н.В. и др. Репродуктивная биология некоторых редких видов флоры Крыма. К.: Аграрна наука, 2010. 387 с.

18. Anderson E. D., Owens J. N. Microsporogenesis, pollination, pollen germination and male gametophyte development in Taxus brevifolia. Ann. Bot, 2000; 86: 1033-1042.
https://doi.org/10.1006/anbo.2000.1274

19. Brunsfeld S.J., Soltis P.E., Soltis D.E. et al. Phylogenetic relationships among the genera of Taxodiaceae and Cupressaceae: evidence from rbcL sequences. Syst. Bot, 1994; 19: 253-262.
https://doi.org/10.2307/2419600

20. Carmichael J. S. Gnetales. Encyclopedia of Life Sciences. 2002. Macmillan Publishers Ltd, Nature Publishing Group. 5 р.
https://doi.org/10.1038/npg.els.0003681

21. Chase, M.W. & 41 co-authors. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann. Missouri Bot. Gard,1993; 80: 528-580.

22. Chaw S.-M., Parkinson C.L., Cheng Y. et al. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natd. Acad. Sci. USA, 2000; 97: 4086-4086.
https://doi.org/10.1073/pnas.97.8.4086
PMid:10760277 PMCid:PMC18157

23. Chaw S.-M., Zharkikh A., Sung H.-M. et al. Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences. Mol. Biol. Evol, 1997; 14: 56-68.
https://doi.org/10.1093/oxfordjournals.molbev.a025702
PMid:9000754

24. Christenhusz M.J.M., Reveal J. L. et al. A new classification and linear sequence of extant gymnosperms. Phytotaxa, 2011; 19: 55-70.
https://doi.org/10.11646/phytotaxa.19.1.3

25. Cresswell J. E., Henning K., Pennel Ch. et al. Conifer ovulate cones accumulate pollen principally by simple impaction. Proc. Natd. Acad. Sci. USA, 2007; 104(46): 18141-18144.
https://doi.org/10.1073/pnas.0706434104
PMid:17986613 PMCid:PMC2084310

26. Donaldson J. S. Is there a floral parasite mutualism in Cycad pollination? The pollination biology of Encephalartos villosus (Zamiaceae). Am. J. Bot, 1997; 84(10): 1398-1406.
https://doi.org/10.2307/2446138

27. Doyle J. Developmental lines in pollination mechanisms in the Coniferales. Sci. Proc. R. Dublin Soc, 1945; 24: 43-62.

28. Doyle J.A. Phylogeny of Vascular plants. Ann. Rev. Ecol. Syst, 1998; 29: 567-599.
https://doi.org/10.1146/annurev.ecolsys.29.1.567

29. Doyle J., O' Leary M. Pollination in Pinus. Sci. Proc. R. Dublin Soc, 1935; 21: 180-190.

30. Farjon A.A. Handbook of the World's Conifers. 2010. E.J. Brill, Leiden/Boston.
https://doi.org/10.1163/9789047430629
PMid:20978281

31. Farjon A., Garcia S.O. Cone and ovule development in Cunninghamia аnd Taiwania (Cupressaceae sensu lato) and its significance for conifer evolution. Am. J. Bot, 2003; 90(1): 8-16.
https://doi.org/10.3732/ajb.90.1.8
PMid:21659075

32. Fernando D.D., Quinn C.R., Brenner E.D. et al. Male gametophyte development and evolution in extant Gymnosperms. Int. J. Plant Developmental Biology, 2010; 4 (Sp. іss. 1): 47-63.

33. Flores-Rentería L., Molina-Freaner F., Whipple A.V. et al. Sexual stability in the nearly dioecious Pinus johannis (Pinaceae) Am. J. Bot, 2013; 100(3): 602-612.
https://doi.org/10.3732/ajb.1200068
PMid:23445824

34. Friedman W.E. Double fertilization in Ephedra, a nonflowering seed plant: its bearing on the origin of Аngiosperms. Science. 1990; 247: 951-954.
https://doi.org/10.1126/science.247.4945.951
PMid:17776453

35. Friedman W.E. Developmental and evolutionary hypotheses for the origin of double fertilization and endosperm. C. R. Acad. Sci. III, 2001; 324(6): 559-567.
https://doi.org/10.1016/S0764-4469(01)01326-9

36. Friedman W.E., Carmichael J.S. Heterochrony and developmental innovation: evolution of female gametophyte ontogeny in Gnetum, a highly apomorphic seed plant. Evolution, 1998; 52(4): 1016-1030.
https://doi.org/10.1111/j.1558-5646.1998.tb01830.x
PMid:28565210

37. Friedman W.E., Floyd S.K. Perspective: the origin of flowering plants and their reproductive biology - a tale of two phylogenies. Evolution, 2001; 55(2): 217-231.
https://doi.org/10.1111/j.0014-3820.2001.tb01288.x
PMid:11308081

38. Gifford E.M., Foster A.S. Gnetophyta. Comparative morphology of vascular plants. San Francisco, CA: WH Freeman.1989: 455-483.

39. Hart J.A. A cladistic analisys of conifers: preliminary results. J. Arnold Arb, 1987; 68: 269-307.

40. Haycraft C.J., Carmichael J.S. Development of sterile ovules on bisexual cones of Gnetum gnemon (Gnetaceae). Am. J. Bot, 2001; 88(7): 1326-1330.
https://doi.org/10.2307/3558344

41. Hill K. Diversity and evolution of gymnosperms. Plant diversity and evolution: genotypic and phenotypic variation in higher plants / R. J. Henry - CABI Publishing. 2005: 25-45.
https://doi.org/10.1079/9780851999043.0025
PMCid:PMC1084246

42. Huang J.-C., Chang L.-C., Wang M.-L. et al. Identification and exploration of pollen tube small proteins encoded by pollination-induced transcripts. Plant Cell Physiol, 2011; 52(9): 1546-1559.
https://doi.org/10.1093/pcp/pcr095
PMid:21771867

43. Jin B., Jiang X., Wang D. et al. The behavior of pollination drop secretion in Ginkgo biloba L. Plant Signal Behav, 2012; 7(9): 1168-1176.
https://doi.org/10.4161/psb.21122
PMid:22899081 PMCid:PMC3489653

44. Jin B., Zhang L., Lu Y., et al. The mechanism of pollination drop withdrawal in Ginkgo biloba L. BMC Plant Biol, 2012; 12: 59. (http://www.biomedcentral.com/1471-2229/12/59).
https://doi.org/10.1186/1471-2229-12-59
PMid:22548734 PMCid:PMC3403970

45. Johnson L.A.S., Wilson K.L. General traits of the Cycadales. In: K. Kubitzki et al. (ed.). The families and genera of vascular plants. I. Pteridophytes and Gymnosperms. Springer, 1990: 363-368.
https://doi.org/10.1007/978-3-662-02604-5_63
PMCid:PMC269609

46. Kubitzki K. Gnetatae. In: K. Kubitzki et al. (ed.). The families and genera of vascular plants. I. Pteridophytes and Gymnosperms. Springer, 1990: 378-391.
https://doi.org/10.1007/978-3-662-02604-5_69

47. Leslie A.B. Flotation preferentially selects saccate pollen during conifer pollination. New Phytol, 2010; 188(1): 273-279.
https://doi.org/10.1111/j.1469-8137.2010.03356.x
PMid:20579290

48. Martens P. Les Gnetophytes / Handbuch der Pflanzenanatomie, Bd. 12, Teil 2. Berlin, Stuttgart: Borntraeger. 1971.

49. Mill R.R., Möller M., Christie F. et al. Morphology, anatomy and ontogeny of female cones in Acmopyle pancheri (Brongn. et Gris) Pilg. (Podocarpaceae). Ann. Bot, 2001; 88: 55-67.
https://doi.org/10.1006/anbo.2001.1426

50. Möller M., Mill R.R., Glidewell S.M. et al. Comparative biology of the pollination mechanisms in Acmopyle pancheri and Phyllocladus hypophyllus (Podocarpaceae s. l.). Ann. Bot, 2000; 86: 149-158.
https://doi.org/10.1006/anbo.2000.1167

51. Mugnaini S., Nepi M., Guarnieri M. et al. Pollination drop in Juniperus communis: response to deposited material. Ann. Bot, 2007; 100: 1475-1481.
https://doi.org/10.1093/aob/mcm253
PMid:17942592 PMCid:PMC2759232

52. Nepi M, Aderkas P, Wagner R, et al. Nectar and pollination drops: how different are they? Ann. Bot, 2009; 104: 205-219.
https://doi.org/10.1093/aob/mcp124
PMid:19477895 PMCid:PMC2710891

53. Niklas K. J. Simulated wind pollination and airflow around ovules of some early seed plants. Science, 1981; 211(4479): 275-277.
https://doi.org/10.1126/science.211.4479.275
PMid:17748024

54. Niklas K. J. Simulated and empiric wind pollination patterns of conifer ovulate cones. Proc. NatL Acad. Sci. USA, 1982; 79: 510-514.
https://doi.org/10.1073/pnas.79.2.510
PMid:16593147 PMCid:PMC345773

55. Niklas K. J., Paw U K. Th. Pollination and airflow patterns around conifer ovulate cones. Science, 1982; 217(4558): 442-444.
https://doi.org/10.1126/science.217.4558.442
PMid:17782978

56. Owens J.N., Takaso T., Runions C.J. Pollination in conifers. Trends Plant Sci. 1998; 3: 479-485.
https://doi.org/10.1016/S1360-1385(98)01337-5

57. Page C.N. General traits of Conifers. In: K. Kubitzki et al. (ed.). The families and genera of vascular plants. I. Pteridophytes and Gymnosperms. Springer, 1990: 290-292.
https://doi.org/10.1007/978-3-662-02604-5_51

58. Page C.N. Ginkgoaceae. In: K. Kubitzki et al. (ed.). The families and genera of vascular plants. I. Pteridophytes and Gymnosperms. Springer, 1990: 284-289.
https://doi.org/10.1007/978-3-662-02604-5_50

59. Palmer J. D., Soltis D.E., Chase M.W. The plant tree of life: an overview and some points of view. Am. J. Bot, 2004; 91(10): 1437-1445.
https://doi.org/10.3732/ajb.91.10.1437
PMid:21652302

60. Peñalvera E., Labandeirab C. C., Barróna E. et al. Thrips pollination of Mesozoic gymnosperms. Proc. Natd. Acad. Sci. USA. 2012; 109(22): 8623-8628.
https://doi.org/10.1073/pnas.1120499109
PMid:22615414 PMCid:PMC3365147

61. Pettitt J. M. The megaspore wall in Gymnosperms: ultrastructure in some zooidogamous forms. Proc. R. Soc. Lond. B, 1977; 195(1121): 497-515.
https://doi.org/10.1098/rspb.1977.0023

62. Pettitt J. M. Ultrastructural and immunocytochemical demonstration of gametophytic proteins in the pollen tube wall of the primitive gymnosperm Cycas. J. Cell Sci, 1982; 57: 189-313.

63. Price R.A., Thomas J., Strauss S.H. et al. Familia relationships of the conifers from rbcL sequence data. Am. J. Bot, 1993; 80: 172.
https://doi.org/10.2307/2399852

64. Proche Ş., Johnson S. D. Beetle pollination of the fruit-scented cones of the South African cycad Stangeria eriopus. Am. J. Bot, 2009; 96(9): 1722-1730.
https://doi.org/10.3732/ajb.0800377
PMid:21622358

65. Quan Z., Sodmergen, Yu-Shi H., et al. Female Cone Development in Fokienia, Cupressus, Chamaecyparis and Juniperus (Cupressaceae). Acta Botanica Sinica, 2004; 46(9): 1075-1082.

66. Ran J.-H., Gao H., Wang, X.-Q. Fast evolution of the retroprocessed mitochondrial rps3 gene in conifer II and further evidence for the phylogeny of gymnosperms. Molecular Phylogenetics and Evolution. 2010; 54: 136-149.
https://doi.org/10.1016/j.ympev.2009.09.011
PMid:19761858

67. Runions C. J., Rensing K. H., Takaso T. et al. Pollination of Picea orientalis (Pinaceae): Saccus morphology governs pollen buoyancy. Am. J. Bot, 1999; 86(2): 190-197.
https://doi.org/10.2307/2656936

68. Salter J., Murray B. G., Braggins J. E. Wettable and unsinkable: the hydrodynamics of saccate pollen grains in relation to the pollination mechanism in the two New Zealand species of Prumnopitys Phil. (Podocarpaceae). Ann. Bot, 2002; 89: 133-144.
https://doi.org/10.1093/aob/mcf019
PMid:12099344 PMCid:PMC4233786

69. Saxton W. T. Notes on Conifers: VI. Pollination in the Pinaceae, with special reference to Cedrus atlantica, Manetti. Ann. Bot, 1930; 44: 419-421.
https://doi.org/10.1093/oxfordjournals.aob.a090227

70. Schneider D., Wink M., Sporer F. et al. Cycads: their evolution, toxins, herbivores and insect pollinators. - Naturwissenschaften, 2002; 89(7): 281-294.
https://doi.org/10.1007/s00114-002-0330-2
PMid:12216856

71. Schwendemann A. B., Wang G., Mertz M. L. et al. Aerodynamics of saccate pollen and its implications for wind pollination. Am. J. Bot, 2007; 94(8): 1371-1381.
https://doi.org/10.3732/ajb.94.8.1371
PMid:21636505

72. Singh H. Embryology of Gymnosperms. Berlin-Stuttgart. Gebrüder Borntraeger. 1978. 304 p.

73. Stefanovic S., Jager M., Deutsch J., et al. Phylogenetic relationships of conifers inferred from partial 28S rRNA gene sequences. Am. J. Bot,1998; 85: 688-697.
https://doi.org/10.2307/2446539

74. Sterling C. Structure of the male gametophyte in gymnosperms. Biol. Rev, 1963; 38: 167-203.
https://doi.org/10.1111/j.1469-185X.1963.tb00782.x
PMid:4873456

75. Stützel Th., Röwekamp I. Bestäubungsbiologie bei Nacktsamern (Gymnospermen). Blütenökologie - Faszinierendes Miteinander von Pflanzen und Tieren / Hrsg.: Zizka G., Schneckenburger S. Kleine Senckenberg-Reihe N 33. - Palmengarten Sonderheft № 31. Frankfurt am Main: Kramer, 1999: 107-117.

76. Takaso T., Owens J.N. Significance of exine shedding in Cupressaceae-type pollen. J. Plant Res. 2008; 121(1): 83-85.
https://doi.org/10.1007/s10265-007-0135-7
PMid:18058189

77. Taylor E. L., Taylor T. N. Reproductive biology of the Permian Glossopteridales and their suggested relationship to flowering plants. Proc. Natd. Acad. Sci. USA, 1992; 89: 11495-11497.
https://doi.org/10.1073/pnas.89.23.11495
PMid:11607341 PMCid:PMC50578

78. Terry l. I., Walter G. H., Donaldson J. S. et al. Pollination of australian Macrozamia cycads (Zamiaceae): effectiveness and behavior of specialist vectors in a dependent mutualism. Am. J. Bot, 2005; 92(6): 931-940.
https://doi.org/10.3732/ajb.92.6.931
PMid:21652476

79. Terry I., Walter G. H., Moore C. et al. Odor-mediated "push-pull" pollination in cycads. Science, 2007; 318: 70.
https://doi.org/10.1126/science.1145147
PMid:17916726

80. Tomlinson P.B. Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae. Int. J. Plant Science, 1994; 155: 699-715.
https://doi.org/10.1086/297209

81. Tomlinson P.B., Braggins J.E., Rattenbury J.A. Pollination drop in relation to cone morphology in Podocarpaceae: a novel reproductive mechanism. Am. J. Bot, 1991; 78: 1289-1303.
https://doi.org/10.1002/j.1537-2197.1991.tb11421.x

82. Tomlinson P.B., Braggins J.E., Rattenbury J.A. Contrasted pollen capture mechanisms іn Phyllocladaceae аnd сertain Podocarpaceae (Coniferales). Am. J. Bot, 1997; 84(2): 214-223.
https://doi.org/10.2307/2446083

83. Tomlinson P.B., Takaso T. Seed cone structure in conifers in relation to development and pollination: a biological approach. Can. J. Bot, 2002; 80: 1250-1273.
https://doi.org/10.1139/b02-112

84. Villar M., Knox R. B., Dumas C. Effective pollination period and nature of pollen-collecting apparatus in the Gymnosperm, Larix leptolepis. Ann. Bot, 1984; 53: 279-284.
https://doi.org/10.1093/oxfordjournals.aob.a086689

85. Wagner R.E., Mugnaini S., Sniezko R. et al. Proteomic evaluation of gymnosperm pollination drop proteins indicates highly conserved and complex biological functions. Sexual Plant Reprod, 2007; 20: 181-189.
https://doi.org/10.1007/s00497-007-0054-8

86. Wetschnig W., Depisch B. Pollination biology of Welwitschia mirabilis Hook. f. (Welwitschiaceae, Gnetopsida). Phyton, 1999; 39: 167-183.

87. Whitelock L.M. The Cycads. Portland: Timber Press. 2002. 374 p.

88. Williams C.G. Conifer reproductive biology. Berlin: Springer. 2009. 172 p.
https://doi.org/10.1007/978-1-4020-9602-0

89. Williams C.G. Long-distance pine pollen still germinates after meso-scale dispersal. Am. J. Bot, 2010; 97(5): 846-855.
https://doi.org/10.3732/ajb.0900255
PMid:21622450

90. Willemese M.T.M. Plant sexual reproduction: aspects of interaction, history and regulation. Act. Biol. Cracovien. Ser. Bot, 2003; 45(1): 19-26.


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