Sexual Plant Reproduction

, Volume 24, Issue 3, pp 171–187 | Cite as

Interspecific reproductive barriers in the tomato clade: opportunities to decipher mechanisms of reproductive isolation

  • Patricia A. BedingerEmail author
  • Roger T. Chetelat
  • Bruce McClure
  • Leonie C. Moyle
  • Jocelyn K. C. Rose
  • Stephen M. Stack
  • Esther van der Knaap
  • You Soon Baek
  • Gloria Lopez-Casado
  • Paul A. Covey
  • Aruna Kumar
  • Wentao Li
  • Reynaldo Nunez
  • Felipe Cruz-Garcia
  • Suzanne Royer


The tomato clade within the genus Solanum has numerous advantages for mechanistic studies of reproductive isolation. Its thirteen closely related species, along with four closely allied Solanum species, provide a defined group with diverse mating systems that display complex interspecific reproductive barriers. Several kinds of pre- and postzygotic barriers have already been identified within this clade. Well-developed genetic maps, introgression lines, interspecific bridging lines, and the newly available draft genome sequence of the domesticated tomato (Solanum lycopersicum) are valuable tools for the genetic analysis of interspecific reproductive barriers. The excellent chromosome morphology of these diploid species allows detailed cytological analysis of interspecific hybrids. Transgenic methodologies, well developed in the Solanaceae, allow the functional testing of candidate reproductive barrier genes as well as live imaging of pollen rejection events through the use of fluorescently tagged proteins. Proteomic and transcriptomics approaches are also providing new insights into the molecular nature of interspecific barriers. Recent progress toward understanding reproductive isolation mechanisms using these molecular and genetic tools is assessed in this review.


Reproductive barriers Section Lycopersicon Interspecific pollination 







Unilateral incongruity





This work was supported by the National Science Foundation, grant number DBI-0605200. We thank Ms. Ashley Denney and Ms. Margaret Fleming for helpful editing.


  1. Aguilar R, Bernardello G, Galetto L (2002) Pollen–pistil relationships and pollen size-number trade-off in species of the tribe Lycieae (Solanaceae). J Plant Res 115:335–340PubMedCrossRefGoogle Scholar
  2. Albini SM (1988) Synaptonemal complex spreading in Allium cepa and Allium fistulosum. II. Pachytene observations: the SC karyotype and the correspondence of late recombination nodules and chiasmata. Genome 30:399–410CrossRefGoogle Scholar
  3. Albini SM, Jones GH (1984) Synaptonemal complex-associated centromeres and recombination nodules in plant meiocytes prepared by an improved surface-spreading technique. Exp Cell Res 155:589–592CrossRefGoogle Scholar
  4. Albini SM, Jones GH, Wallace BMN (1984) A method for preparing two-dimensional surface-spreads of synaptonemal complexes from plant meiocytes for light and electron microscopy. Exp Cell Res 152:280–285PubMedCrossRefGoogle Scholar
  5. Anderson LK, Covey PA, Larsen LR, Bedinger PA, Stack SM (2010) Structural differences in chromosomes distinguish species in the tomato clade. J Cytogen Genome Res (in press)Google Scholar
  6. Barton DW (1950) Pachytene morphology of the tomato chromosome complement. Am J Bot 37:639–643CrossRefGoogle Scholar
  7. Beecher B, McClure BA (2001) Expressing self-incompatibility RNases (S-RNases) in transgenic plants. In: Schein CH (ed) Nuclease methods and protocols. Humana Press, Totowa, pp 65–85CrossRefGoogle Scholar
  8. Beecher B, Murfett J, McClure BA (1998) RNaseI from Escherichia coli cannot substitute for S-RNase in rejection of Nicotiana plumbaginifolia pollen. Plant Mol Biol 36:553–563PubMedCrossRefGoogle Scholar
  9. Bernacchi D, Tanksley SD (1997) An interspecific backcross of Lycopersicon esculentum × L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147:861–877PubMedGoogle Scholar
  10. Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478Google Scholar
  11. Brown SW (1949) The structure and meiotic behavior of the differentiated chromosomes of tomato. Genetics 34:437–461Google Scholar
  12. Canady MA, Meglic V, Chetelat RT (2005) A library of Solanum lycopersicoides introgression lines in cultivated tomato. Genome 48:685–697PubMedCrossRefGoogle Scholar
  13. Chandler JM, Jan C-C, Beard BH (1986) Chromosomal differentiation among annual Helianthus species. Syst Botany 11:354–371CrossRefGoogle Scholar
  14. Chang S-B, Anderson LK, Sherman JD, Royer SM, Stack SM (2007) Predicting and testing physical locations of genetically mapped loci on tomato pachytene chromosome 1. Genetics 176:2131–2138PubMedCrossRefGoogle Scholar
  15. Chen K-Y, Cong B, Wing R, Vrebalov J, Tanksley SD (2007) Changes in regulation of a transcription factor lead to autogamy in cultivated tomatoes. Science 318:643–645PubMedCrossRefGoogle Scholar
  16. Chetelat RT, De Verna JW (1991) Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6, and 10. Theor Appl Genet 82:704–712CrossRefGoogle Scholar
  17. Chetelat RT, Pertuze RA, Faundez L, Graham EB, Jones CM (2009) Distribution, ecology and reproductive biology of wild tomatoes and related nightshades from the Atacama Desert region of northern Chile. Euphytica 167:77–93CrossRefGoogle Scholar
  18. Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572PubMedCrossRefGoogle Scholar
  19. Covey PA, KondoK, Welch L, Frank E, Kumar A, Knaap Evd, Nunez R, Lopez-Casado G, Rose JKC, McClure BA, Bedinger PA (2010) Multiple features that distinguish unilateral incongruity and self-incompatibility in the tomato clade. Plant J. doi: 10.1111/j.1365-313X.2010.04340.x
  20. Coyne JA, Aulard S, Berry A (1991) Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics 129:791–802PubMedGoogle Scholar
  21. Cruden R (2009) Pollen grain size, stigma depth, and style length: the relationships revisited. Plant Syst Evol 278:223–238CrossRefGoogle Scholar
  22. Cruden RW, Lyon DL (1985) Correlations among stigma depth, style length, and pollen grain size: do they reflect function or phylogeny? Botanical Gazette 146:143–149CrossRefGoogle Scholar
  23. Dai S, Wang T, Yan X, Chen S (2007) Proteomics of pollen development and germination. J Proteome Res 6:4556–4563Google Scholar
  24. Darwin C (1897) The different forms of flowers on plants of the same species. D. Appleton and Company, LondonGoogle Scholar
  25. Dawe RK (2005) Centromere renewal and replacement in the plant kingdom. Proc Natl Acad Sci USA 192:11573–11574CrossRefGoogle Scholar
  26. Delphino F (1867) Sull’opera, la distribuzione dei sessi nelle piante e la legge che osta alla perennita della fecundazione consanguinea. Atti Soc Itl Sci Natil 10:272–303Google Scholar
  27. Dobzhansky T (1936) Studies on hybrid sterility II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113–135PubMedGoogle Scholar
  28. Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162PubMedGoogle Scholar
  29. Garcia CC (2007) Pollen starch reserves in tomato relatives: ecophysiological implications. Grana 46:13–19Google Scholar
  30. Georgiady M, Lord S, Elizabeth M (2002) Evolution of the inbred flower form in the currant tomato, Lycopersicon pimpinellifolium. Int J Plant Sci 163:531–541CrossRefGoogle Scholar
  31. Gillies CB (1981) Electron microscopy of spread maize pachytene synaptonemal complexes. Chromosoma 83:575–591CrossRefGoogle Scholar
  32. Gottschalk W (1954) Die Chromosomenstruktur der Solanaceen unter Berücksichtigung (relation). Chromosoma 6:539–626PubMedCrossRefGoogle Scholar
  33. Graham EB, Shannon SM, Persrsen JP, Chetelat RT (2003) A self-compatible population of Lycopersicon peruvianum collected from N. Chile. Tomato Genet Coop 53:22–24Google Scholar
  34. Grobei MA, Qeli E, Brunner E, Rehrauer H, Zhang R, Roschitzki B, Basler K, Ahrens CH, Grossniklaus U (2009) Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Res 19:1786–1800Google Scholar
  35. Haerizadeh F, Wong C, Bhalla P, Gresshoff P, Singh M (2009) Genomic expression profiling of mature soybean (Glycine max) pollen. BMC Plant Biol 9:25Google Scholar
  36. Hancock CN, Kent L, McClure BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723PubMedCrossRefGoogle Scholar
  37. Hardon JJ (1967) Unilateral incompatibility between Solanum pennellii and Lycopersicon esculentum. Genetics 57:795–808PubMedGoogle Scholar
  38. Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49:1429–1450Google Scholar
  39. Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama, T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428Google Scholar
  40. Hogenboom NG (1972) Breaking breeding barriers in Lycopersicon. 5. The inheritance of the unilateral incongruity between L. peruvianum (L.) Mill. and L. esculentum Mill. and the genetics of its breakdown. Euphytica 21:405–414CrossRefGoogle Scholar
  41. Holle M, Rick CM, Hunt DG (1978–1979) Catalog of collections of green-fruited Lycopersicon species and Solanum pennellii found in watersheds of Peru. Tomato Genet Cooper 28–29, 49–78, 63–91Google Scholar
  42. Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884Google Scholar
  43. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85Google Scholar
  44. Kadej AJ, Wilms HJ, Willemse MTM (1985) Stigma and stigmatoid tissue of Lycopersicon esculentum MillerGoogle Scholar
  45. Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751Google Scholar
  46. Kondo K, Yamamoto M, Itahashi R, Sato T, Egashira H, Hattori T, Kowyama Y (2002) Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J 30:143–153PubMedCrossRefGoogle Scholar
  47. Lai Z, Nakazato T, Salmaso M, Burke JM, Tang S, Knapp SJ, Rieseberg LH (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303PubMedCrossRefGoogle Scholar
  48. Lee H-S, Huang S, Kao T-h (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563PubMedCrossRefGoogle Scholar
  49. Lee C, Page L, McClure B, Holtsford T (2008) Post-pollination hybridization barriers in Nicotiana section Alatae. Sex Plant Reprod 21:183–195CrossRefGoogle Scholar
  50. Lee CB, Kim S, McClure B (2009) A pollen protein, NaPCCP, that binds pistil arabinogalactan proteins also binds phosphatidylinositol 3-phosphate and associates with the pollen tube endomembrane system. Plant Physiol 149:791–802PubMedCrossRefGoogle Scholar
  51. Lewis D, Crowe L (1958) Unilateral interspecific incompatibility in flowering plants. Heredity 12:233–256CrossRefGoogle Scholar
  52. Li W, Royer S, Chetelat RT (2010) Fine mapping of ui6.1, a gametophytic factor controlling pollen-side unilateral incompatibility in interspecific Solanum hybrids. Genetics. doi:genetics.110.116343
  53. Liedl BE, McCormick S, Mutschler MA (1996) Unilateral incongruity in crosses involving Lycopersicon pennellii and L. esculentum is distinct from self-incompatibility in expression, timing and location. Sexual Plant Reprod 9:299–308CrossRefGoogle Scholar
  54. Linsley EG, Rick CM, Stephens SG (1966) Observations on the floral relationships of the Galapagos carpenter bee (Hymenoptera: Apidae). Pan-Pacific Entomol 42:1–18Google Scholar
  55. Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos Trans Royal Soc B Biol Sci 363:3009–3021CrossRefGoogle Scholar
  56. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen Y-J, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim J-B, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380 Google Scholar
  57. Martin FW (1961) The inheritance of self-incompatibility in hybrids of Lycopersicon Esculentum Mill. x L. Chilense Dun. Genetics 46:1443–1454PubMedGoogle Scholar
  58. Martin FW (1964) The inheritance of unilateral incompatibility in Lycopersicon hirsutum. Genetics 50:459–469PubMedGoogle Scholar
  59. Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9:1757–1766PubMedCrossRefGoogle Scholar
  60. McClure B, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci USA 96:13548–13553PubMedCrossRefGoogle Scholar
  61. McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. Plant Tissue Cult Manual B6:1–9Google Scholar
  62. McGuire DC, Rick CM (1954) Self-Incompatibility in species of Lycopersicon sect. Eriopersicon and hybrids with L. esculentum. Hilgardia 23:101–124Google Scholar
  63. Moses M (1968) Synaptinemal complex. Ann Rev Genet 2:363–412CrossRefGoogle Scholar
  64. Moses M, Poorman P (1984) Synapsis, synaptic adjustment and DNA synthesis in mouse oocytes. Chromosom Today 8:99–103Google Scholar
  65. Moyle LC, Graham EB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169:355–373PubMedCrossRefGoogle Scholar
  66. Moyle LC, Nakazato T (2008) Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genetics 179:1437–1453PubMedCrossRefGoogle Scholar
  67. Moyle LC, Nakazato T (2009) Complex epistasis for Dobzhansky-Muller hybrid incompatibility in Solanum. Genetics 181:347–351PubMedCrossRefGoogle Scholar
  68. Moyle LC, Nakazato T (2010) Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521–1523Google Scholar
  69. Mueller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–125Google Scholar
  70. Murfett J, McClure BA (1998) Expressing foreign genes in the pistil: a comparison of S-RNase constructs in different Nicotiana backgrounds. Plant Mol Biol 37:561–569PubMedCrossRefGoogle Scholar
  71. Murfett J, Cornish EC, Ebert PR, Bonig I, McClure BA, Clarke AE (1992) Expression of a self-incompatibility glycoprotein (S2-Ribonuclease) from Nicotiana alata in Transgenic Nicotiana tabacum. Plant Cell 4:1063–1074PubMedCrossRefGoogle Scholar
  72. Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566PubMedCrossRefGoogle Scholar
  73. Murfett J, Strabala TJ, Zurek DM, Mou B, Beecher B, McClure BA (1996) S-RNase and interspecific pollen rejection in the Genus Nicotiana: multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8:943–958PubMedCrossRefGoogle Scholar
  74. Mutschler M, Liedl B (1994) Interspecific crossing barriers in Lycopersicon and their relationship to self-incompatibility. In: Williams E (ed) Genetic control of self-incompatibility and reproductive development in flowering plants. Kluwer Academic, Netherlands, pp 164–188Google Scholar
  75. Nasrallah JB (2002) Recognition and rejection of self in plant reproduction. Science 296:305–308PubMedCrossRefGoogle Scholar
  76. Nasrallah JB, Liu P, Sherman-Broyles S, Schmidt R, Nasrallah ME (2007) Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids. Genetics 175:1965–1973PubMedCrossRefGoogle Scholar
  77. Nesbitt TC, Tanksley SD (2002) Comparative sequencing in the genus Lycopersicon. Implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162:365–379Google Scholar
  78. Noor MAF, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. PNAS USA 98:12084–12088PubMedCrossRefGoogle Scholar
  79. O’Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP (2002) Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J 32:985–996PubMedCrossRefGoogle Scholar
  80. Peralta IE, Spooner DM, Knapp S (2008) Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae). Syst Botany Monogr 84:186Google Scholar
  81. Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004) The F-box protein AhSLFS2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595Google Scholar
  82. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5:e1000621Google Scholar
  83. Quiros C (1991) Lycopersicon cytogenetics. In: Tsuchiya T, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution (Part B). Elsevier Science Publishers, Amsterdam, pp 119–137Google Scholar
  84. Rick CM (1950) Pollination relations of Lycopersicon esculentum in native and foreign regions. Evolution 4:110–122CrossRefGoogle Scholar
  85. Rick MC (1988) Tomato-like nightshades: affinities, autoecology, and breeders’ opportunities. Econ Bot 42:145–154CrossRefGoogle Scholar
  86. Rick CM, Chetelat RT (1991) The breakdown of self-incompatibility in Lycopersicon hirsutum. In: Hawkes L, Nee E (eds) Solanaceae III: taxonomy, chemistry, evolution, Royal Botanical Gardens Kew and Linnean Society of London, pp 253–256Google Scholar
  87. Rick CM, Tanksley SD (1981) Genetic variation in Solanum pennellii: comparisons with two other sympatric tomato species. Plant Syst Evol 139:11–45CrossRefGoogle Scholar
  88. Rick CM, Holle M, Robbin TW (1978) Rates of cross-pollination in Lycopersicon pimpinellifolium: impact of genetic variation in floral characters. Plant Syst Evol 129:31–44CrossRefGoogle Scholar
  89. Rick CM, Fobes JF, Tanksley SD (1979) Evolution of mating systems in Lycopersicon hirsutum as deduced from genetic variation in electrophoretic and morphological characters. Plant Syst Evol 132:279–298CrossRefGoogle Scholar
  90. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914PubMedCrossRefGoogle Scholar
  91. Rieseberg LH, Linder CR, Seiler GJ (1995) Chromosomal and genic barriers to introgression in helianthus. Genetics 141:1163–1171PubMedGoogle Scholar
  92. Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between Two sunflower species. Genetics 152:713–727PubMedGoogle Scholar
  93. Rodriguez F, Wu F, Ane C, Tanksley S, Spooner D (2009) Do potatoes and tomatoes have a single evolutionary history, and what proportion of the genome supports this history? BMC Evol Biology 9:191CrossRefGoogle Scholar
  94. Sassa H, Hirano H (2006) Identification of a new class of pistil-specific proteins of Petunia inflata that is structurally similar to, but functionally distinct from, the self-incompatibility factor HT. Mol Gen Genomics 275:97–104CrossRefGoogle Scholar
  95. Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700PubMedCrossRefGoogle Scholar
  96. Sheoran IS, Ross AR, Olson DJ, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535Google Scholar
  97. Sherman JD, Stack SM (1992) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. Genome 35:354–359CrossRefGoogle Scholar
  98. Sherman JD, Stack SM (1995) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141:686–708Google Scholar
  99. Stack SM (1982) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. I. The technique. Stain Technol 57:265–272PubMedGoogle Scholar
  100. Stack SM, Anderson LK (1986a) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. II. Synapsis in Lycopersicon esculentum. Am J Botany 73:264–281CrossRefGoogle Scholar
  101. Stack SM, Anderson LK (1986b) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. III. Recombination nodules and crossing over in Lycopersicon esculentum (tomato). Chromosoma 94:253–258CrossRefGoogle Scholar
  102. Stack SM, Anderson LK (2009) Electron microscopic immunogold localization of recombination-related proteins in spreads of synaptonemal complexes from tomato microsporocytes. In: Keeney S (ed) Meiosis. Humana Press, Inc, Totowa, pp 147–169CrossRefGoogle Scholar
  103. Stack SM, Royer SM, Shearer LA, Chang SB, Giovannoni JJ, Westfall DH, White RA, Anderson LK (2009) Role of fluorescence in situ hybridization in sequencing the tomato genome. Cytogenet Genome Res 124:339–350PubMedCrossRefGoogle Scholar
  104. Swanson C (1957) Cytology and cytogenetics. Printice-Hall, Inc), Englewood CliffsGoogle Scholar
  105. Szinay D (2010) The development of FISH tools for genetic, phylogenetic and breeding studies in tomato (Solanum lycopersicum). Wageningen University, The NetherlandsGoogle Scholar
  106. Torres C (2000) Pollen size evolution: correlation between pollen volume and pistil length in Asteraceae. Sex Plant Reprod 12:365–370CrossRefGoogle Scholar
  107. von Wagenheim K-H (1957) Das Pachytan und der weiter Ablauf der meiose in diploiden Solanum-Arten und–Bastarden. Chromosoma 8:671–690CrossRefGoogle Scholar
  108. von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Ann Rev Genet 18:331–413CrossRefGoogle Scholar
  109. Widmer A, Lexer C, Cozzolino S (2008) Evolution of reproductive isolation in plants. Heredity 102:31–38PubMedCrossRefGoogle Scholar
  110. Williams EG, Rouse JL (1990) Relationships of pollen size, pistil length and pollen tube growth rates in Rhododendron and their influence on hybridization. Sex Plant Reprod 3:7–17CrossRefGoogle Scholar
  111. Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821PubMedCrossRefGoogle Scholar
  112. Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003) A pollen-expressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium. Plant Cell Physiol 44:764–769Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Patricia A. Bedinger
    • 1
    Email author
  • Roger T. Chetelat
    • 2
  • Bruce McClure
    • 3
  • Leonie C. Moyle
    • 4
  • Jocelyn K. C. Rose
    • 5
  • Stephen M. Stack
    • 1
  • Esther van der Knaap
    • 6
  • You Soon Baek
    • 1
  • Gloria Lopez-Casado
    • 5
  • Paul A. Covey
    • 1
  • Aruna Kumar
    • 3
  • Wentao Li
    • 2
  • Reynaldo Nunez
    • 6
  • Felipe Cruz-Garcia
    • 7
  • Suzanne Royer
    • 1
  1. 1.Department of BiologyColorado State UniversityFort CollinsUSA
  2. 2.Department of Plant SciencesUniversity of California DavisDavisUSA
  3. 3.Department of BiochemistryUniversity of MissouriColumbiaUSA
  4. 4.Department of BiologyUniversity of IndianaBloomingtonUSA
  5. 5.Department of Plant BiologyCornell UniversityIthacaUSA
  6. 6.Department of Horticulture and Crop ScienceThe Ohio State University/OARDCWoosterUSA
  7. 7.Departmento de Bioquímica, Facultad de QuímicaUniversidad Nacional Autónoma de MéxicoMexico CityMexico

Personalised recommendations