Testing the SI × SC rule: Pollen–pistil interactions in interspecific crosses between members of the tomato clade(Solanum section lycopersicon, Solanaceae)

American Journal of Botany

Volumn 102, Issue 2, 2015, Pages 302-311

  Baek, You Soon ^a   Covey, Paul A ^a   Petersen, Jennifer J ^b   Chetelat, Roger T ^b   McClure, Bruce ^c   Bedinger, Patricia A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Missouri   (United States)

Author keywords

Interspecific reproductive barriers; Pollen pistil interactions; Self incompatibility; SI SC rule; Solanaceae; Solanum; Tomato clade; Unilateral incompatibility; Unilateral incongruity; Wide hybridization; Wild tomato species

Indexed keywords

FRUIT; GROWTH RATE; HYBRIDIZATION; INTERSPECIFIC VARIATION; POLLEN; SEED;

LYCOPERSICON; LYCOPERSICON ESCULENTUM; SOLANACEAE; SOLANUM;

CROSS BREEDING; EVOLUTION; FLOWER; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; POLLEN; POLLEN TUBE; POLLINATION; REPRODUCTION; SOLANACEAE; SOLANUM; TOMATO;

BIOLOGICAL EVOLUTION; CROSSES, GENETIC; FLOWERS; FRUIT; HYBRIDIZATION, GENETIC; LYCOPERSICON ESCULENTUM; POLLEN; POLLEN TUBE; POLLINATION; REPRODUCTION; SOLANACEAE; SOLANUM;

EID: 84922433961     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1400484     Document Type: Article

References (58)

1. AFLITOS, S., E. SCHIJLEN, H. DE JONG, D. DE RIDDER, S. SMIT, R. FINKERS, J. WANG, ET AL. 2014. Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant Journal 80: 136-148.
2. BEDINGER, P. A., R. T. CHETELAT, B. MCCLURE, L. C. MOYLE, J. K. ROSE, S. M. STACK, E. VAN DER KNAAP, ET AL. 2011. Interspecific reproductive barriers in the tomato clade: Opportunities to decipher mechanisms of reproductive isolation. Sexual Plant Reproduction 24: 171-187.
3. BEECHER, B., D. ZUREK, AND B. MCCLURE. 2001. Effects of RNases on rejection of pollen from Nicotiana tabacum and N. plumbaginifolia. Sexual Plant Reproduction 14: 69-76.
4. BERNACCHI, D., AND S. D. TANKSLEY. 1997. An interspecific backcross of Lycopersicon esculentum × L. hirsutum: Linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147: 861-877.
5. BRUKHIN, V., M. HERNOULD, N. GONZALEZ, C. CHEVALIER, AND A. MOURAS. 2003. Flower development schedule in tomato Lycopersicon esculentum cv. Sweet Cherry. Sexual Plant Reproduction 15: 311-320.
6. CHALIVENDRA, S. C., G. LOPEZ-CASADO, A. KUMAR, A. R. KASSENBROCK, S. ROYER, A. TOVAR-MÉNDEZ, P. A. COVEY, ET AL. 2013. Developmental onset of reproductive barriers and associated proteome changes in stigma/styles of Solanum pennellii. Journal of Experimental Botany 64: 265-279.
7. CHETELAT, R. T., AND J. W. DEVERNA. 1991. Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10. Theoretical and Applied Genetics 82: 704-712.
8. CHEUNG, A. Y. 1996. Pollen-pistil interactions during pollen tube growth. Trends in Plant Science 1: 45-51.
9. CHMIELEWSKI, T. 1962. Cytogenetical and taxonomical studies on a new tomato form. Genetica Polonica 3: 253-264.
10. CHMIELEWSKI, T. 1966. An exception to the unidirectional crossability pattern in the genus Lycopersicon. Genetica Polonica 7: 31-39.
11. COVEY, P. A., K. KONDO, L. WELCH, E. FRANK, S. SIANTA, A. KUMAR, R. NUÑEZ, ET AL. 2010. Multiple features that distinguish unilateral incongruity and self-incompatibility in the tomato clade. Plant Journal 64: 367-378.
12. DRESSELHAUS, T., AND N. FRANKLIN-TONG. 2013. Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. M olecular Plant 6: 1018-1036.
13. GOODWILLIE, C., R. D. SARGENT, C. G. ECKERT, E. ELLE, M. A. GEBER, M. O. JOHNSTON, S. KALISZ, ET AL. 2010. Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phytologist 185: 311-321.
14. GRANT, V. 1981. Plant speciation, 2nd ed. Columbia University, New York, New York, USA.
15. HANCOCK, C. N., K. KONDO, B. BEECHER, AND B. MCCLURE. 2003. The S-locus and unilateral incompatibility. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 358: 1133-1140.
16. HARDER, L. D. 1993. Unilateral incompatibility and the effects of interspecific pollination for Erythronium americanum and Erythronium albidum (Liliaceae). Canadian Journal of Botany 71: 353-358.
17. HARDON, J. J. 1967. Unilateral incompatibility between Solanum pennellii and Lycopersicon esculentum. Genetics 57: 795-808.
18. HARRISON, J. J., AND L. A. DARBY. 1955. Unilateral hybridization. Nature 176: 982.
19. HISCOCK, S. J., AND H. G. DICKINSON. 1993. Unilateral incompatibility within the Brassicaceae: Further evidence for the involvement of the self-incompatibility (S)-locus. Theoretical and Applied Genetics 86: 744-753.
20. HOGENBOOM, N. G. 1973. A model for incongruity in intimate partner relationships. E uphytica 22: 219-233.
21. HOGENBOOM, N. G. 1984. Incongruity: Non-functioning of intercellular and intracellular partner relationships through non-matching information. In H. Linskens and J. Heslop-Harrison [eds.], Cellular interactions, vol. 17, Encyclopedia of plant physiology, 640-654. Springer, Berlin, Germany.
22. HUA, Z., AND T. H. KAO. 2006. Identification and characterization of components of a Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18: 2531-2553.
23. KAO, T. H., AND T. TSUKAMOTO. 2004. The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16: S72-S83.
24. KONDO, K., M. YAMAMOTO, R. ITAHASHI, T. SATO, H. EGASHIRA, T. HATTORI, AND Y. KOWYAMA. 2002a. Insights into the evolution of selfcompatibility in Lycopersicon from a study of stylar factors. Plant Journal 30: 143-153.
25. KONDO, K., M. YAMAMOTO, D. P. MATTON, T. SATO, M. HIRAI, S. NORIOKA, T. HATTORI, AND Y. KOWYAMA. 2002b. Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of selfincompatibility. P lant Journal 29: 627-636.
26. KOWYAMA, Y., C. KUNZ, I. LEWIS, E. NEWBIGIN, A. E. CLARKE, AND M. A. ANDERSON. 1994. Self-compatibility in a Lycopersicon peruvianum variant (LA2157) is associated with a lack of style S-RNase activity. Theoretical and Applied Genetics 88: 859-864.
27. KUBO, K., T. ENTANI, A. TAKARA, N. WANG, A. M. FIELDS, Z. HUA, M. TOYODA, ET AL. 2010. Collaborative non-self recognition system in S-RNasebased self-incompatibility. Science 330: 796-799.
28. LEVIN, D. A. 1971. The origin of reproductive isolating mechanisms in flowering plants. Taxon 20: 91-113.
29. LEWIS, D., AND L. K. CROWE. 1958. Unilateral interspecific incompatibility in flowering plants. Heredity 12: 233-256.
30. LI, W., AND R. T. CHETELAT. 2010. A pollen factor linking inter-and intraspecific pollen rejection in tomato. Science 330: 1827-1830.
31. LI, W., AND R. T. CHETELAT. 2014. The role of a pollen-expressed Cullin1 protein in gametophytic self-incompatibility in Solanum. Genetics 196: 439-442.
32. LIEDL, B. E., S. MCCORMICK, AND M. A. MUTSCHLER. 1996. Unilateral incongruity in crosses involving Lycopersicon pennellii and L. esculentum is distinct from self-incompatibility in expression, timing and location. Sexual Plant Reproduction 9: 299-308.
33. LIN, T., G. ZHU, J. ZHANG, X. XU, Q. YU, Z. ZHENG, Z. ZHANG, ET AL. 2014. Genomic analyses provide insights into the history of tomato breeding. Nature Genetics 10. 1038/ng. 3117.
34. MARTIN, F. W. 1961a. Complex unilateral hybridization in Lycopersicon hirsutum. Proceedings of the National Academy of Sciences, USA 47: 855-857.
35. MARTIN, F. W. 1961b. The inheritance of self-incompatibility in hybrids of Lycopersicon eculentum Mill. × L. chilense Dun. Genetics 46: 1443-1454.
36. MARTIN, F. W. 1964. The inheritance of unilateral incompatibility in Lycopersicon hirsutum. Genetics 50: 459-469.
37. MARTIN, F. W. 1967. The genetic control of unilateral incompatibility between two tomato species. Genetics 56: 391-398.
38. MCCLURE, B. 2004. S-RNase and SLF determine S-haplotype-specific pollen recognition and rejection. Plant Cell 16: 2840-2847.
39. MCCLURE, B., F. CRUZ-GARCIA, B. BEECHER, AND W. SULAMAN. 2000. Factors affecting inter-and intra specific pollen rejection in Nicotiana. Annals of Botany 85: 113-123.
40. MCCLURE, B., F. CRUZ-GARCIA, AND C. ROMERO. 2011. Compatibility and incompatibility in S-RNase-based systems. Annals of Botany 108: 647-658.
41. MCCLURE, B., AND V. FRANKLIN-TONG. 2006. Gametophytic selfincompatibility: Understanding the cellular mechanisms involved in "self" pollen tube inhibition. Planta 224: 233-245.
42. MURFETT, J., T. J. STRABALA, D. M. ZUREK, B. MOU, B. BEECHER, AND B. A. MCCLURE. 1996. S-RNase and interspecific pollen rejection in the genus Nicotiana: Multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and selfcompatible species. Plant Cell 8: 943-958.
43. MUTSCHLER, M., AND B. LIEDL. 1994. Interspecific crossing barriers in Lycopersicon and their relationship to self-incompatibility. In E. Williams [ed.], Genetic control of self-incompatibility and reproductive development in flowering plants, 164-188. Klewer, Dordrecht, Netherlands.
44. ONUS, A. N., AND B. PICKERSGILL. 2004. Unilateral incompatibility in Capsicum (Solanaceae): Occurrence and taxonomic distribution. Annals of Botany 94: 289-295.
45. ORNDUFF, R. 1969. Reproductive biology in relation to systematics. Taxon 18: 121-133.
46. PERALTA, I. E., D. M. SPOONER, AND S. KNAPP. 2008. Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae). Systematic Botany Monographs 84.
47. RICK, C. M. 1956. Genetic and systematic studies on accessions of Lycopersicon from the Gal ápagos island tomato. American Journal of Botany 43: 687-696.
48. RICK, C. M. 1967. Fruit and pedicel characters derived from Gal ápagos tomatoes. E conomic Botany 21: 171-184.
49. RICK, C. M. 1979. Biosystematic studies in Lycopersicon and closely related species of Solanum. In J. G. Hawkes, R. N. Lester, and A. D. Skelding [ed.], The biology and taxonomy of the Solanaceae, 667-679. Academic Press, New York, New York, USA.
50. RICK, C. M. 1986. Reproductive isolation in the Lycopersicon peruvianum complex. Columbia University Press, New York, New York, USA.
51. RICK, C. M., J. F. FOBES, AND S. D. TANKSLEY. 1979. Evolution of mating systems in Lycopersicon hirsutum as deduced from genetic variation in electrophoretic and morphological characters. Plant Systematics and Evolution 132: 279-298.
52. RICK, C. M., E. KESICKI, J. F. FOBES, AND M. HOLLE. 1976. Genetic and biosystematic studies on two new sibling species of Lycopersicon from interandean Perú. Theoretical and Applied Genetics 47: 55-68.
53. RODRIGUEZ, F., F. WU, C. ANÉ, S. TANKSLEY, AND D. M. SPOONER. 2009. Do potatoes and tomatoes have a single evolutionary history, and what proportion of the genome supports this history? BMC Evolutionary Biology 9: 191.
54. ROYO, J., C. KUNZ, Y. KOWYAMA, AND M. ANDERSON. A. E. CLARK, AND E. NEWBIGIN. 1994. Loss of a histidine residue at the active site of S-locus ribonuclease is associated with self-compatibility in Lycopersicon peruvianum. Proceedings of the National Academy of Sciences, USA 91: 6511-6514.
55. SICARD, A., AND M. LENHARD. 2011. The selfing syndrome: A model for studying the genetic and evolutionary basis of morphological adaptation in plants. Annals of Botany 107: 1433-1443.
56. SIMS, T. L., A. PATEL, AND P. SHRESTHA. 2010. Protein interactions and subcellular localization in S-RNase-based self-incompatibility. Biochemical Society Transactions 38: 622-626.
57. TOMATO GENOME CONSORTIUM. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
58. TOVAR-MÉNDEZ, A., A. KUMAR, K. KONDO, A. ASHFORD, Y. S. BAEK, L. WELCH, P. A. BEDINGER, AND B. A. MCCLURE. 2014. Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species. Plant Journal 77: 727-736.