Plant Systematics and Evolution

, Volume 210, Issue 1–2, pp 113–139 | Cite as

Pollen morphology and functional dioecy inSolanum (Solanaceae)

  • Sandra Knapp
  • Viveca Persson
  • Stephen Blackmore


Dioecy has evolved independently several times in the large, mostly tropical genusSolanum. In all cases of dioecy inSolanum functionally male flowers have normal anthers, normal pollen and reduced stigmas while functionally female flowers have stigmas and anthers that appear normal but contain non-functional, usually inaperturate pollen. The inaperturate pollen has living cytoplasm, but apparently never germinates and it has been hypothesised that the pollen in these functionally female flowers is retained as a pollinator reward. Pollen morphology is compared in twelve of the thirteen known dioecious species ofSolanum, and some stages in the the development of inaperturate pollen in the anthers of functionally female flowers ofSolanum confertiseriatum of Western Ecuador are examined. Observations on the development and morphology of inaperturate pollen in functionally female flowers ofSolanum are related to hypotheses about the evolution of dioecy in the genus.

Key words

Solanaceae Solanum Evolution male sterility breeding system dioecy inaperturate pollen pollen development palynology plant reproduction 


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  1. Anderson, G. J., 1977: The variation and evolution ofSolanum sectionBasarthrum. II. — Brittonia29: 116–128.Google Scholar
  2. —, 1979: DioeciousSolanum species of hermaphroditic origin is an example of broad convergence. — Nature282: 836–838.Google Scholar
  3. —, 1982: Three taxa constitute the sexes of a single species of dioeciousSolanum. — Taxon81: 667–672.Google Scholar
  4. —, 1989: Functional dioecy and andromonoecy inSolanum. — Evolution43: 204–219.Google Scholar
  5. Baker, H., 1959: Reproductive methods as factors in speciation in flowering plants. — Cold Spring Harbor Symp. Quant. Biol.24: 177–191.PubMedGoogle Scholar
  6. Baker, H. G., 1976: “Mistake” pollination as a reproductive system with special reference to the Caricaceae. — InBurley, J., Styles, B. T., (Eds): Tropical trees: variation, breeding and conservation, pp. 161–169. — London: Academic Press.Google Scholar
  7. Bawa, J. S., 1980: Evolution of dioecy in flowering plants. — Annual Rev. Ecol. Syst.11: 15–39.Google Scholar
  8. —, 1994: Pollination of tropical dioecious angiosperms: a reassessment? No, not yet. — Amer. J. Bot.81: 456–460.Google Scholar
  9. Bawa, K. S., Beach, J. H., 1981: Evolution of sexual systems in flowering plants. — Ann. Missouri Bot. Gard.68: 254–274.Google Scholar
  10. —, 1975: Dioecism in tropical forest trees. — Evolution29: 167–179.Google Scholar
  11. Beach, J. H., Bawa, K. S., 1980: Role of pollinators in the evolution of dioecy from distyly. — Evolution34: 1138–1142.Google Scholar
  12. Bitter, G., 1913: LXXVII. Solana nova vel minus cognita. VII. XVII. Solana diversa. — Repert. Spec. Nov. Regni Veg.11: 481–491.Google Scholar
  13. Blackmore, S., 1990: Sporoderm homologies and morphogenesis in land plants, with a discussion ofEchinops sphaerocephala (Compositae). — Pl. Syst. Evol., Suppl.5: 1–12.Google Scholar
  14. —, 1990: Angiosperm pollen wall ontogeny. — InBlackmore, S., Knox, R. B., (Eds): Microsporogenesis: ontogeny and evolution, pp. 173–192. — London: Academic Press.Google Scholar
  15. McConchie, C. A., Knox, R. B., 1988: Phylogenetic analysis of the male ontogenetic programme in aquatic and terrestrial monocotyledons. — Cladistics3: 333–347.Google Scholar
  16. Charlesworth, D., 1981: A further study of the problem of the maintenance of females in gynodioecious species. — Heredity46: 27–39.Google Scholar
  17. —, 1984: Androdioecy and the evolution of dioecy. — Biol. J. Linn. Soc.23: 333–348.Google Scholar
  18. Chaudhury, A. M., Lavithis, M., Taylor, P. E., Craig, S., Singh, M. B., Knox, R. B., Dennis, E. S., 1994: Genetic control of male fertility inArabidopsis thaliana: structural analysis of premeiotic developmental mutants. — Sexual Pl. Reprod.7: 17–28.Google Scholar
  19. Clark, A. G., 1996: Population genetic aspects of gametophytic self-incompatibility. — Pl. Spec. Biol.11: 13–21.Google Scholar
  20. Cox, P. A., 1982: Vertebrate pollination and the maintenance of dioecism inFreycinetia. — Amer. Naturalist120: 65–80.Google Scholar
  21. —, 1990: Pollination and the evolution of breeding systems inPandanaceae. — Ann. Missouri Bot. Gard.77: 816–840.Google Scholar
  22. —, 1993: Hydrophilous pollination and breeding system evolution in seagrasses: a phylogenetic approach to the evolutionary ecology ofCymodoceaceae. — Bot. J. Linn. Soc.113: 217–226.Google Scholar
  23. D'Arcy, W. G., 1972:Solanaceae studies II. Typification of the subdivisions ofSolanum. — Ann. Missouri Bot. Gard.59: 262–278.Google Scholar
  24. —, 1974 [1973]:Solanaceae. — InWoodson, R. E., Schery, R. W. Jr., (Eds): Flora of Panama. — Ann. Missouri Bot. Gard.60: 573–780.Google Scholar
  25. Darwin, C., 1876: The effects of cross and self fertilization of plants. — London: Murray.Google Scholar
  26. —, 1877: On different forms of flowers on plants of the same species. — London: Murray.Google Scholar
  27. Dickinson, H. G., 1976: Common factors in exine deposition. — InFerguson, I. K., Muller, J., (Eds): The evolutionary significance of the exine, pp. 67–89. — London: Academic Press.Google Scholar
  28. Bell, P. R., 1972: The identification of sporopollenin in sections of resin embedded tissues by controlled acetolysis. — Stain Technol.48: 17–22.Google Scholar
  29. Diggle, P. K., 1991: Labile sex expression in andromonoeciousSolanum hirtum: floral development and sex determination. — Amer. J. Bot.78: 377–393.Google Scholar
  30. —, 1993: Developmental plasticity, genetic variation, and the evolution of andromonoecy inSolanum hirtum (Solanaceae). — Amer. J. Bot.80: 967–973.Google Scholar
  31. —, 1994: The expression of andromonoecy inSolanum hirtum (Solanaceae): phenotypic plasticity and ontogenetic contingency. — Amer. J. Bot.81: 1354–1365.Google Scholar
  32. Donoghue, M. J., 1989: Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. — Evolution43: 1137–1156.Google Scholar
  33. Dover, G. A., 1972: The organisation and polarity of pollen mother cells ofTriticum aestivum. — J. Cell. Sci.11: 699–711.PubMedGoogle Scholar
  34. Drahowzal, G., 1936: Beiträge zur Morphologie und Entwicklungsgeschichte der Pollenkörner. — Oesterr. Bot. Z.85: 241–269.Google Scholar
  35. Erdtman, G., 1960: The acetolysis technique, a revised description. — Svensk Bot. Tidskr.54: 561–564.Google Scholar
  36. Fox, J. F., 1985: Incidence of dioecy in relation to growth form, pollination and dispersal. — Oecologia67: 244–249.Google Scholar
  37. Freeman, D. C., Harper, K. T., Ostler, W. K., 1980: Ecology of plant dioecy in the intermountain region of Western North America and California. — Oecologia67: 244–249.Google Scholar
  38. Givnish, T. J., 1980: Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. — Evolution34: 959–972.Google Scholar
  39. —, 1982: Outcrossing versus ecological constraints in the evolution of dioecy. — Amer. Naturalist119: 849–865.Google Scholar
  40. Godward, M. B. E., Pell, K., 1994: Inheritance of exine pattern inNicotiana ×sanderae (Solanaceae). — Bot. J. Linn. Soc.115: 145–159.Google Scholar
  41. Heslop-Harrison, J., 1968: The pollen grain wall. — Science161: 230–237.PubMedGoogle Scholar
  42. —, 1971: Wall pattern formation in angiosperm microsporogenesis. — Symp. Soc. Exp. Biol.25: 277–300.PubMedGoogle Scholar
  43. Holmgren, P. K., Holmgren, N. H., Barnett, L. C., (Eds), 1990: Index herbariorum. 8th edn. — Regnum Veg.120.Google Scholar
  44. Huyhn, K. L., 1976: Arrangement of some monosulcate, disulcate, trisulcate, and tricolpate pollen types in the tetrads, and some aspects of evolution in the angiosperms. — InFerguson, I. K., Muller, J., (Eds): The evolutionary significance of the exine, pp. 101–124. — London: Academic Press.Google Scholar
  45. Kaplan, S. M., Mulcahy, D. L., 1971: Mode of pollination and floral sexuality inThalictrum. — Evolution25: 659–688.Google Scholar
  46. Knapp, S., 1986: A revision ofSolanum sectionGeminata (G. Don)Walpers. — Ph.D. Dissertation, Cornell University, Ithaca, NY.Google Scholar
  47. —, 1991: A revision of theSolanum sessile species group (sectionGeminata pro parte:Solanaceae). — Bot. J. Linn. Soc.105: 179–210.Google Scholar
  48. —, 1997: A revision ofSolanum sectionPteroidea Dunal (Solanaceae). — Bull. Nat. Hist. Mus. London (Bot.)27: 31–73.Google Scholar
  49. Knox, R. B., 1984: The pollen grain. — InJohri, B. M., (Ed.): Embryology of angiosperms, pp. 197–271. — Berlin, Heidelberg, New York: Springer.Google Scholar
  50. Lahav-Ginott, S., Cronk, Q. C. B., 1993: The mating system ofElatostema (Urticaceae) in relation to morphology: a comparative study. — Pl. Syst. Evol.186: 135–145.Google Scholar
  51. Levine, D. A., Anderson, G. J., 1986: Evolution of dioecy in an AmericanSolanum. — InD'Arcy, W. G., (Ed.):Solanaceae: biology and systematics, pp. 264–273. — New York: Columbia University Press.Google Scholar
  52. Linnaeus, C., 1753: Species plantarum. — Stockholm: Salvivs.Google Scholar
  53. Lloyd, D. G., 1975: The maintenance of gynodioecy and androdioecy in angiosperms. — Genetica45: 325–339.Google Scholar
  54. —, 1976: The transmission of genes via pollen and ovules in gynodioecious angiosperms. — Theor. Populat. Biol.9: 299–316.Google Scholar
  55. —, 1982: Selection of combined versus separate sexes in seed plants. — Amer. Naturalist120: 571–585.Google Scholar
  56. Muenchow, G. E., 1987: Is dioecy associated with fleshy fruit? — Amer. J. Bot.74: 287–293.Google Scholar
  57. Nettancourt, D. de, 1977: Incompatibility in angiosperms. — Berlin, Heidelberg, New York: Springer.Google Scholar
  58. Owens, S., Sheldon, J. M., Dickinson, H. G., 1990: The microtubular cytoskeleton during pollen development. — Pl. Syst. Evol., Suppl.5: 31–37.Google Scholar
  59. Peirson, B. N., Owen, H. A., Feldmann, K. A., Makaroff, C. A., 1996: Characterization of three male-sterile mutants ofArabidopsis thaliana exhibiting alterations in meiosis. — Sexual Pl. Reprod.9: 1–16.Google Scholar
  60. Peloquin, S. J., 1983: Genetic engineering with meiotic mutants. — InMulcahy, D. L., Ottaviano, E., (Eds): Pollen: biology and implications for plant breeding, pp. 311–316. — New York: Elsevier.Google Scholar
  61. Persson, V., Knapp, S., Blackmore, S., 1994: Pollen morphology and systematics of tribeJuanulloaeae A. T. Huntziker (Solanaceae). — Rev. Palaeobot. Palynol.83: 1–30.Google Scholar
  62. Preuss, D., Rhee, S. H., Davis, R. W., 1994: Tetrad analysis inArabidopsis with mutation of the QUARTET (QRT) genes. — Science264: 1458–1460.PubMedGoogle Scholar
  63. Punt, W., Monna-Brands, M., 1980: The Northwest European pollen flora, 8.Solanaceae. — InPunt, W., Clarke, G. C. S., (Eds): The Northwest European pollen floraII. pp. 1–30. — Amsterdam: Elsevier.Google Scholar
  64. —, 1994: Glossary of pollen and spore terminology. — Utrecht: L. P. P. Foundation.Google Scholar
  65. Quiros, C. F., 1975: Exine pattern of a hybrid betweenLycopersicon esculentum andSolanum penellii. — J. Heredity66: 45–47.Google Scholar
  66. Renner, S. S., Feil, J. P., 1993: Pollinators of tropical dioecious angiosperms. — Amer. J. Bot.80: 1100–1107.Google Scholar
  67. Rick, C. M., 1948: Genetics and the development of nine male-sterile tomato mutants. — Hilgardia18: 599–633.Google Scholar
  68. Ricklefs, R. E., 1995: Dioecy and its correlates in flowering plants. — Amer. J. Bot.82: 596–606.Google Scholar
  69. Ross, M. D., 1978: The evolution of gynodioecy and subdioecy. — Evolution32: 174–188.Google Scholar
  70. —, 1982: Five evolutionary pathways to subdioecy. — Amer. Naturalist119: 297–318.Google Scholar
  71. Sakai, A. K., Karoly, K., Weller, S. G., 1989: Inbreeding depression inSchiedea globosa andS. salicaria (Caryophyllaceae), subdioecious and gynodioceious Hawaiian species. — Amer. J. Bot.76: 437–444.Google Scholar
  72. Schultz, S. T., 1994: Nucleo-cytoplasmic sterility and alternative routes to dioecy. — Evolution48: 1933–1945.Google Scholar
  73. Sheldon, J. M., Dickinson, H. G., 1983: Determination of patterning in the pollen wall ofLilium henryi. — J. Cell. Sci.63: 191–208.PubMedGoogle Scholar
  74. Spooner, D. M., Anderson, G. J., Jansen, R. K., 1993: Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes and pepinos (Solanaceae). — Amer. J. Bot.80: 676–688.Google Scholar
  75. Symon, D. E., 1970: Dioecious solanums. — Taxon19: 909–910.Google Scholar
  76. —, 1979: Sex forms inSolanum (Solanaceae) and the role of pollen collecting insects. — InHawkes, J. G., Lester, R. N., Skelding, A. D., (Eds): The biology and taxonomy of theSolanaceae, pp. 385–397. — London: Academic Press.Google Scholar
  77. —, 1981: A revision of the genusSolanum in Australia. — J. Adelaide Bot. Gard.4: 1–367.Google Scholar
  78. Thomson, J. D., Brunet, J., 1990: Hypotheses for the evolution of dioecy in seed plants. — Trends Ecol. Evol.5: 11–16.Google Scholar
  79. Theerakulpisut, P., Singh, M. B., Knox, R. B., 1991: Molecular aspects of the development of reproductive cells. — InHarding, J., Singh, F., Mol, J. N. M., (Eds): Genetics and breeding of ornamental species, pp. 333–366. — Dordrecht: Kluwer Academic Press.Google Scholar
  80. Trass, J. A., Burgain, S., Dumas De Vaulx, R., 1989: The organisation of the cytoskeleton during meiosis in eggplant (Solanum melongena L.): microtubules and F-actin are both necessary for coordinated meiotic division. — J. Cell Sci.92: 541–550.Google Scholar
  81. Weber, C. A., 1928:Georg Bitter. — Ber. Deutsch. Bot. Ges.46: 148–156.Google Scholar
  82. Weller, S. G., Sakai, A. K., 1991: The genetic basis of male sterility inSchiedea (Caryophyllaceae), an endemic Hawaiian genus. — Heredity67: 265–273.Google Scholar
  83. —, 1995: The evolution of self-incompatibility in flowering plants: a phylogenetic approach. — InHoch, P. C., Stephenson, A. G., (Eds): Experimental and molecular approaches to plant biosystematics, pp. 355–382. — St. Louis: Missouri Botanical Garden.Google Scholar
  84. Whalen, M. D., 1984: Conspectus of species groups inSolanum subgenusLeptostemonum. — Gentes Herb.12: 179–282.Google Scholar
  85. —, 1981: Distribution of gametophytic self-incompatibility and infrageneric classification inSolanum. — Taxon30: 761–767.Google Scholar
  86. —, 1986: Andromonoecy inSolanum. — InD'Arcy, W. G., (Ed.):Solanaceae: Biology and systematics, pp. 284–302. — New York: Columbia University Press.Google Scholar
  87. —,Heiser, C. B. Jr., 1981: Taxonomy ofSolanum sectionLasiocarpa. — Gentes Herb.12: 41–129.Google Scholar
  88. Yampolsky, C., Yampolsky, H., 1922: Distribution of sex forms in the phanerogamic flora. — Biblioth. Genet.3: 1–62.Google Scholar

Copyright information

© Springer-Verlag 1998

Authors and Affiliations

  • Sandra Knapp
    • 1
  • Viveca Persson
    • 1
  • Stephen Blackmore
    • 1
  1. 1.Department of BotanyThe Natural History MuseumLondonUnited Kingdom

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