Interspecific reproductive barriers in the tomato clade: opportunities to decipher mechanisms of reproductive isolation
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Abstract
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.
Keywords
Reproductive barriers Section Lycopersicon Interspecific pollinationAbbreviations
- SC
Self-compatible
- SI
Self-incompatible
- UI
Unilateral incongruity
- cv
Cultivar
Notes
Acknowledgments
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.
References
- 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
- 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
- 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
- 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
- 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
- Barton DW (1950) Pachytene morphology of the tomato chromosome complement. Am J Bot 37:639–643CrossRefGoogle Scholar
- 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
- 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
- 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
- Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478Google Scholar
- Brown SW (1949) The structure and meiotic behavior of the differentiated chromosomes of tomato. Genetics 34:437–461Google Scholar
- Canady MA, Meglic V, Chetelat RT (2005) A library of Solanum lycopersicoides introgression lines in cultivated tomato. Genome 48:685–697PubMedCrossRefGoogle Scholar
- Chandler JM, Jan C-C, Beard BH (1986) Chromosomal differentiation among annual Helianthus species. Syst Botany 11:354–371CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Cruden R (2009) Pollen grain size, stigma depth, and style length: the relationships revisited. Plant Syst Evol 278:223–238CrossRefGoogle Scholar
- 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
- Dai S, Wang T, Yan X, Chen S (2007) Proteomics of pollen development and germination. J Proteome Res 6:4556–4563Google Scholar
- Darwin C (1897) The different forms of flowers on plants of the same species. D. Appleton and Company, LondonGoogle Scholar
- Dawe RK (2005) Centromere renewal and replacement in the plant kingdom. Proc Natl Acad Sci USA 192:11573–11574CrossRefGoogle Scholar
- 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
- Dobzhansky T (1936) Studies on hybrid sterility II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113–135PubMedGoogle Scholar
- 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
- Garcia CC (2007) Pollen starch reserves in tomato relatives: ecophysiological implications. Grana 46:13–19Google Scholar
- 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
- Gillies CB (1981) Electron microscopy of spread maize pachytene synaptonemal complexes. Chromosoma 83:575–591CrossRefGoogle Scholar
- Gottschalk W (1954) Die Chromosomenstruktur der Solanaceen unter Berücksichtigung (relation). Chromosoma 6:539–626PubMedCrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- Hardon JJ (1967) Unilateral incompatibility between Solanum pennellii and Lycopersicon esculentum. Genetics 57:795–808PubMedGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85Google Scholar
- Kadej AJ, Wilms HJ, Willemse MTM (1985) Stigma and stigmatoid tissue of Lycopersicon esculentum MillerGoogle Scholar
- Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751Google Scholar
- 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
- 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
- Lee H-S, Huang S, Kao T-h (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563PubMedCrossRefGoogle Scholar
- Lee C, Page L, McClure B, Holtsford T (2008) Post-pollination hybridization barriers in Nicotiana section Alatae. Sex Plant Reprod 21:183–195CrossRefGoogle Scholar
- 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
- Lewis D, Crowe L (1958) Unilateral interspecific incompatibility in flowering plants. Heredity 12:233–256CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- Martin FW (1961) The inheritance of self-incompatibility in hybrids of Lycopersicon Esculentum Mill. x L. Chilense Dun. Genetics 46:1443–1454PubMedGoogle Scholar
- Martin FW (1964) The inheritance of unilateral incompatibility in Lycopersicon hirsutum. Genetics 50:459–469PubMedGoogle Scholar
- 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
- 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
- McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. Plant Tissue Cult Manual B6:1–9Google Scholar
- McGuire DC, Rick CM (1954) Self-Incompatibility in species of Lycopersicon sect. Eriopersicon and hybrids with L. esculentum. Hilgardia 23:101–124Google Scholar
- Moses M (1968) Synaptinemal complex. Ann Rev Genet 2:363–412CrossRefGoogle Scholar
- Moses M, Poorman P (1984) Synapsis, synaptic adjustment and DNA synthesis in mouse oocytes. Chromosom Today 8:99–103Google Scholar
- Moyle LC, Graham EB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169:355–373PubMedCrossRefGoogle Scholar
- Moyle LC, Nakazato T (2008) Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genetics 179:1437–1453PubMedCrossRefGoogle Scholar
- Moyle LC, Nakazato T (2009) Complex epistasis for Dobzhansky-Muller hybrid incompatibility in Solanum. Genetics 181:347–351PubMedCrossRefGoogle Scholar
- Moyle LC, Nakazato T (2010) Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521–1523Google Scholar
- Mueller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–125Google Scholar
- 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
- 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
- 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
- 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
- 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
- Nasrallah JB (2002) Recognition and rejection of self in plant reproduction. Science 296:305–308PubMedCrossRefGoogle Scholar
- 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
- 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
- Noor MAF, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. PNAS USA 98:12084–12088PubMedCrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- Rick CM (1950) Pollination relations of Lycopersicon esculentum in native and foreign regions. Evolution 4:110–122CrossRefGoogle Scholar
- Rick MC (1988) Tomato-like nightshades: affinities, autoecology, and breeders’ opportunities. Econ Bot 42:145–154CrossRefGoogle Scholar
- 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
- Rick CM, Tanksley SD (1981) Genetic variation in Solanum pennellii: comparisons with two other sympatric tomato species. Plant Syst Evol 139:11–45CrossRefGoogle Scholar
- 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
- 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
- Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914PubMedCrossRefGoogle Scholar
- Rieseberg LH, Linder CR, Seiler GJ (1995) Chromosomal and genic barriers to introgression in helianthus. Genetics 141:1163–1171PubMedGoogle Scholar
- 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
- 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
- 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
- Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700PubMedCrossRefGoogle Scholar
- Sheoran IS, Ross AR, Olson DJ, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535Google Scholar
- Sherman JD, Stack SM (1992) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. Genome 35:354–359CrossRefGoogle Scholar
- 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
- Stack SM (1982) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. I. The technique. Stain Technol 57:265–272PubMedGoogle Scholar
- 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
- 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
- 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
- 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
- Swanson C (1957) Cytology and cytogenetics. Printice-Hall, Inc), Englewood CliffsGoogle Scholar
- Szinay D (2010) The development of FISH tools for genetic, phylogenetic and breeding studies in tomato (Solanum lycopersicum). Wageningen University, The NetherlandsGoogle Scholar
- Torres C (2000) Pollen size evolution: correlation between pollen volume and pistil length in Asteraceae. Sex Plant Reprod 12:365–370CrossRefGoogle Scholar
- von Wagenheim K-H (1957) Das Pachytan und der weiter Ablauf der meiose in diploiden Solanum-Arten und–Bastarden. Chromosoma 8:671–690CrossRefGoogle Scholar
- von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Ann Rev Genet 18:331–413CrossRefGoogle Scholar
- Widmer A, Lexer C, Cozzolino S (2008) Evolution of reproductive isolation in plants. Heredity 102:31–38PubMedCrossRefGoogle Scholar
- 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
- Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821PubMedCrossRefGoogle Scholar
- 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