Characterization of self-incompatibility in Campanula rapunculoides (Campanulaceae) through genetic analyses and microscopy

Botany

Volumn 86, Issue 1, 2008, Pages 1-13

  Good Avila, S V ^a   Majumder, D ^a   Amos, H ^a   Stephenson, A G ^b  

^a ACADIA UNIVERSITY   (Canada)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Breeding system; Coefficient of crossability; Diallel; Partial self incompatibility; S RNase; Self incompatibility

Indexed keywords

BIODIVERSITY; GENE EXPRESSION; PROTEINS;

BREEDING SYSTEM; PARTIAL SELF-INCOMPATIBILITY; S-RNASE;

PLANTS (BOTANY);

ANGIOSPERM; GAMETOPHYTE; GENETIC ANALYSIS; MICROSCOPY; POLLINATION; PROTEIN; REPRODUCTIVE STRATEGY; SELF INCOMPATIBILITY;

CAMPANULA RAPUNCULOIDES; CAMPANULACEAE; MAGNOLIOPHYTA; SOLANACEAE;

EID: 40449102965     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/B07-100     Document Type: Article

References (70)

1. Anderson, N.O., Liedl, B.E., Ascher, P.D., and Desborough, S.L. 1989. Distinguishing between self-incompatibility and other reproductive barriers in plants using male (MCC) and female (FCC) coefficient of crossability. Sex. Plant Reprod. 2: 116-126.
2. Bielawska, H. 1964. Self fertilization in Campanula rotundifolia L.S. 1. group. Acta Soc. Bot. Polon. 42.
3. Bredemeijer, G.M.M., and Blaas, J. 1981. S-specific proteins in styles of self-iincompatible Nicotiana alata. Theor. Appl. Genet. 59: 185-190. doi:10.1007/BF00264974.
4. Brewbaker, J.L. 1967. The distribution and phylogenetic significance of binucleate and trinucleate pollen grains in the angiosperms. Am. J. Bot. 54: 1069-1083. doi:10.2307/2440530.
5. Burgos, L., Perez-Tornero, O., and Olmos, E. 1998. Detection and inheritance of stylar ribonucleases associated with incompatibility alleles in apricot. Sex. Plant Reprod. 11: 153-158. doi:10.1007/s004970050133.
6. Dafni, A., Kevan, P.G., and Husband, B.C. 2005. Practical pollination biology. Enviroquest, Ltd., Cambridge, Ont.
7. de Nettancourt, D. 2001. Incompatibility and incongruity in wild and cultivated plants. 2nd ed. Springer-Verlag, Berlin, Germany.
8. East, E.M. 1940. The distribution of sterility in flowering plants. Proc. Am. Philos. Soc. 82: 449-518.
9. East, E.M., and Magelsdorf, A.J. 1925. A new interpretation of the hereditary behaviour of self-sterile plants. Proc. Natl. Acad. Sci. U.S.A. 11: 166-171. doi:10.1073/pnas.11.2.166.
10. Faivre, A.E. 2002. Variation in pollen tube inhibition sites within and among three heterostylous species of Rubiaceae. Int. J. Plant Sci. 163: 783-794. doi:10.1086/341230.
11. Franklin, F.C.H., Lawrence, M.J., and Franklin-Tong, V.E. 1995. Cell and molecular biology of self-incompatiblity in flowering plants. Int. Rev. Cytol. 158: 1-64.
12. Franklin-Tong, V.E., and Franklin, F.C.H. 2003. The different mechanisms of gametophytic self-incompatibility. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 1025-1032.
13. Ganders, F.R. 1979. The biology of heterostyly. N.Z. J. Bot. 17: 605-635.
14. Golz, J.F., Clarke, A.E., and Newbigin, E. 2000. Mutational approaches to the study of self-incompatibility revisiting the pollenpart mutants. Ann. Bot. (Lond.), 85: 95-103. doi:10.1006/anbo.1999.1060.
15. Golz, J.F., Oh, H.-Y., Su, V., Kusaba, M., and Newbigin, E. 2001. Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S-locus. Proc. Natl. Acad. Sci. U.S.A. 98: 15372-15376. doi:10.1073/pnas.261571598.
16. Good, S.V. 2000. Partial self-incompatibility in Campanula rapunculoides L. (Campanulaceae): genetic and molecular bases, parental effects and the influence of pollinator availability on the selfing rate. Ph.D. thesis. Pennsylvania State University, Pa.
17. Good-Avila, S.V., and Stephenson, A. 2002. The inheritance of modifiers conferring self-fertility in Campanula rapunculoides L. (Campanulaceae). Evolution, 56: 263-272.
18. Good-Avila, S.V., and Stephenson, A.G. 2003. Parental effects in a partially self-incompatible herb: influence of variation in the strength of self-incompatibility on seed set and progeny performance. Am. Nat. 161: 615-630. doi:10.1086/368290.
19. Good-Avila, S.V., Frey, F., and Stephenson, A.G. 2001. The effect of partial self-incompatibility on the breeding system of Campanula rapunculoides L. (Campanulaceae) under conditions of natural pollination. Int. J. Plant Sci. 162: 1081-1087. doi:10.1086/321928.
20. Good-Avila, S.V., Nagel, T., Vogler, D.W., and Stephenson, A.G. 2003. Effects of inbreeding on male function and self-fertility in the partially self-incompatible herb Campanula rapunculoides (Campanulaceae). Am. J. Bot. 90: 1736-1745.
21. Goodwillie, C. 1997. The genetic control of self-incompatibility in Linanthus parviflorus (Polemoniaceae). Heredity, 79: 424-432. doi:10.1038/sj.hdy.6882030.
22. Heslop-Harrison, Y., and Shivanna, K.R. 1977. The receptive surface of the angiosperm stigma. Ann. Bot. (Lond.), 41: 1233-1258.
23. Hiscock, S.J. 2000. Self-incompatibility in Senecio squalidus L. (Asteraceae). Ann. Bot. (Lond.), 85: 181-190. doi:10.1006/anbo.1999.1058.
24. Hiscock, S.J., and Kües, U. 1999. Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int. Rev. Cytol. 193: 165-295.
25. Hiscock, S.J., and Tabah, D.A. 2003. The different methods of sporophytic self-incompatibility. Philos. Trans. Roy. Soc. Lond. B, 358: 1037-1045.
26. Hiscock, S.J., Hoedemaekers, K., Friedman, W.E., and Dickinson, H.G. 2002. The stigma surface and pollen-stigma interactions in Senecio squalidus L. (Asteraceae) following cross (compatible) and self (incompatible) pollinations. Int. J. Plant Sci. 163: 1-16. doi:10.1086/324530.
27. Hiscock, S.J., McInnis, S.M., Tabah, D.A., Henderson, C.A., and Brennan, A.C. 2003. Sporophytic self-incompatibility in Senecio squalidus L (asteraceae) - the search for S. J. Exp. Bot. 54: 169-174. doi:10.1093/jxb/54.380.169.
28. Igic, B., and Kohn, J.R. 2001. Evolutionary relationships among self-incompatibility RNases. Proc. Natl. Acad. Sci. U.S.A. 98: 13167-13171. doi:10.1073/pnas.231386798.
29. Ikeda, K., Igic, B., Ushijima, K., Yamane, H., Hauck, N.R., Nakano, R., Sassa, H., Iezzoni, A.F., Kohn, J.R., and Tao, R. 2004. Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus. Sex. Plant Reprod. 16: 235-243. doi:10.1007/s00497-003-0200-x.
30. Inoue, K. 1990. Dichogamy, sex allocation, and mating system of Campanula microdonta and C. punctata. Plant Species Biol. 5: 197-203. doi:10.1111/j.1442-1984.1990.tb00179.x.
31. James, S.H. 1979. Chromosome numbers and genetic systems in the trigger plants of western Australia (Stylidium; Stylidiaceae). Aust. J. Bot. 27: 17-25. doi:10.1071/BT9790017.
32. Kovanda, M. 1977. Polyploidy and variation in the Campanula rotundifolia complex. Part II (Taxonomic). 2. Revision of the groups Vulgares and Scheuchzerianae in Czechoslovakia and adjacent regions. Folia Geobot. Phytotax. 5: 171-208.
33. Kowyama, Y., Tsuchiya, T., and Kakeda, K. 2000. Sporophytic self-incompatibility in Ipomoea trifida, a close relative of sweet potato. Ann. Bot. (Lond.), 85: 191-202. doi:10.1006/anbo.1999.1036.
34. Levin, D.A. 1993. S-gene polymorphism in Phlox drummondii. Heredity, 71: 193-198.
35. Levin, D.A. 1996. The evolutionary significance of pseudo self-fertility. Am. Nat. 148: 321-332. doi:10.1086/285927.
36. Lewis, D. 1949. Competition and dominance of incompatibility alleles in diploid pollen. Heredity, 1: 85-108.
37. Lubliner, N., Singh-Cundy, D.T., and Singh-Cundy, A. 2003. Characterization of the pollen growth transition in self-incompatible Petunia inflata. Sex. Plant Reprod. 15: 243-253.
38. Lundquist, A. 1990. The complex S-gene system for control of self-incompatibility in the buttercup genus Ranunculus. Hereditas, 113: 29-46.
39. Lush, W.M., and Clarke, A.E. 1997. Observations of pollen tube growth in Nicotiana alata and their implications for the mechanism of self-incompatibility. Sex. Plant Reprod. 10: 27-35. doi:10.1007/ s004970050064.
40. Majumder, D. 2005. The genetic basis of self-incompatibility in Campanula rapunculoides (Campanulaceae). B.Sc. thesis, Acadia University, Wolfville, N.S.
41. Mau, S.L., Anderson, M.A., Heisler, M., Haring, V., McClure, B.A., and Clarke, A.E. 1991. Molecular and evolutionary aspects of self-incompatibility in flowering plants. In Molecular biology of plant development. Edited by G. Jenkins and W. Schuch. Company of Biologists Limited, Cambridge, UK. pp. 245-269.
42. McCubbin, A.G., Lee, C., and Hetrick, A. 2006. Identification of genes showing differential expression between morphs in developing flowers of Primula vulgaris. Sex Plant Reprod. 19: 63-72. doi:10.1007/s00497-006-0022-8.
43. Nyman, Y. 1992. Pollination mechanisms in six Campanula species (Campanulaceae). Plant Syst. Evol. 181: 97-108. doi:10.1007/BF00937589.
44. Nyman, Y. 1993. The pollen-collecting hairs of Campanula (Campanulaceae). II. Functional and adaptive significance in relation to pollination. Am. J. Bot. 80: 1437-1443. doi:10.2307/2445673.
45. Olmstead, R.G., Jansen, R.K., Kim, K.-J., and Wagstaff, S.J. 2000. The phylogeny of the Asteridae s.l. based on chloroplast ndhF sequences. Mol. Phylogenet. Evol. 16: 96-112. doi:10.1006/mpev.1999.0769.
46. Pandey, K.K. 1980. Evolution of incompatibility systems in plants: origin of 'independent' and 'complementary' control of incompatibility in angiosperms. New Phytol. 84: 381-400. doi:10.1111/j.1469-8137.1980.tb04438.x.
47. Qiao, H., Wang, H., Zhao, L., Zhou, J., Huang, J., Zhang, Y., and Xue, Y. 2004. The F-Box protein AhSLF-S2 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: 582-595. doi:10.1105/tpc.017673.
48. Richardson, T.E., and Stephenson, A.G. 1989. Pollen removal and pollen deposition affect the duration of the staminate and pistillate phases in Campanula rapunculoides. Am. J. Bot. 76: 532-538. doi:10.2307/2444347.
49. Richardson, T.E., and Stephenson, A.G. 1991. Effects of parentage, prior fruit set and pollen load on fruit and seed production in Campanula americana L. Oecology, 87: 80-95.
50. Richardson, T.E., Hrincevich, A., Kao, T.H., and Stephenson, A.G. 1990. Preliminary studies into age-dependent breakdown of self-incompatibility in Campanula rapunculoides: seed set, pollen tube growth, and molecular data. P. Cell Incompat. Newsl. 22: 41-47.
51. Richman, A.D., Broothaerts, W., and Kohn, J.R. 1997. Self-incompatibility RNases from three plant families: homology or convergence? Am. J. Bot. 84: 912-917. doi:10.2307/2446281.
52. Ridout, M.S., Xu, X.-M., and Tobutt, K.R. 2005. Single-locus gametophytic incompatibility in autotetraploids. J. Hered. 96: 430-433. doi:10.1093/jhered/esi063.
53. Rosatti, T.J. 1986. The genera of Sphenocleaceae and Campanulaceae in the southeastern United States. J. Arnold Arbor. Harv. Univ. 67: 1-64.
54. Sage, T.L., Pontieri, V., and Christopher, R. 2000. Incompatibility and mate recognition in monocotyledons. In Monocots systematics and evolution. Proceedings of the 2nd International Conference on the Comparative Biology of Monocots. Aust. J. Bot. 2: 268-275.
55. Sassa, H., Hirano, H., and Ikehashi, H. 1992. Self-incompatibility- related RNases in styles of Japanese pear (Pyrus serotina Rehd.). Plant Cell Physiol. 33: 811-814.
56. Shetler, S. 1979. Pollen-collecting hairs of Campanula (Campanulaceae), I: Historical review. Taxon, 28: 205-215. doi:10.2307/1219578.
57. Shore, J.S., Arbo, M.M., and Fenández, A. 2006. Breeding system variation, genetics and evolution in the Turneraceae. New Phytol. 171: 539-551.
58. Sijacic, P., Wang, X., Skirpan, A.L., Wang, Y., Dowd, P.E., McCubbin, A.G., Huang, S., and Kao, T.-H. 2004. Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature (London), 429: 302-305. doi:10.1038/nature02523.
59. Silva, N.F., and Goring, D.R. 2001. Mechanisms of self-incompatibility in flowering plants. Cell. Mol. Life Sci. 58: 1988-2007. doi:10.1007/PL00000832.
60. Singh, A., Ai, Y., and Kao, T.-H. 1991. Characterization of ribonuclease activity of three S-allele-associated proteins of Petunia inflata. Plant Physiol. 96: 61-68.
61. Soltis, D.E., Soltis, P.S., Chase, M.W., Mort, M.E., Albach, D.C., Zanis, M., Savolainen, V., Hahn, W.H., Hoot, S.B., Fay, M.F., Axtell, M., Swensen, S.M., Prince, L.M., Kress, W.J., Nixon, K.C., and Farris, J.S. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL and atpB sequences. Bot. J. Linn. Soc. 133: 381-461. doi:10.1006/bojl.2000.0380.
62. Stephenson, A.G., Good, S.V., and Vogler, D.W. 2000. Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the breeding system of Campanula rapunculoides L. (Campanulaceae). Ann. Bot. (Lond.), 85: 211-220. doi:10.1006/anbo.1999.1033.
63. Stone, J.L. 2002. Molecular mechanisms underlying the breakdown of gametophytic self-incompatibility. Q. Rev. Biol. 77: 17-32. doi:10.1086/339200.
64. Sugiura, R. 1942. Studies on the chromosome numbers in Campanulaceae I. Campanuloideae-Campanuleae. Cytologia (Tokyo), 12: 418-434.
65. Talavera, S., Gibbs, P.E., Fernadez-piedra, M.P., and Herrera, M.A. 2001. Genetic control of self-incompatibility in Anagallis monelli (Primulaceae: Mursinaceae). Heredity, 87: 589-597. doi:10.1046/j.1365- 2540.2001.00951.x.
66. Vogler, D.W., and Stephenson, A. 2001. The potential for a mixed mating system Campanula. Int. J. Plant Sci. 162: 801-805. doi:10.1086/320787.
67. Vogler, D.W., Das, C., and Stephenson, A.G. 1998. Phenotypic plasticity in the expression of self-incompatibility in Campanula rapunculoides. Heredity, 81: 546-555. doi:10.1046/j.1365-2540.1998.00417.x.
68. Vogler, D.W., Filmore, K., and Stephenson, A.G. 1999. Inbreeding depression in Campanula rapunculoides L. I. A comparison of inbreeding depression in plants derived from strong and weak self-incompatibility phenotypes. J. Evol. Ecol. 12: 483-494.
69. Weller, S.G., Donoghue, M.J., and Charlesworth, D. 1995. The evolution of self-incompatibility in flowering plants: a phylogenetic approach. Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis, Mo. pp. 355-382.
70. Willis, A.J., and Ash, J.E. 1990. The breeding systems of Stylidium graminifolium and S. productum (Stylidiaceae). Aust. J. Bot. 38: 217-227. doi:10.1071/BT9900217.