Molecular and genetic characterization of novel S-RNases from a natural population of Nicotiana alata

Plant Cell Reports

Volumn 29, Issue 7, 2010, Pages 735-746

  Roldán, Juan A ^a   Quiroga, Rodrigo ^a   Goldraij, Ariel ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Natural populations; Nicotiana alata; S Haplotype; S RNase; Self incompatibility; Transgeneric S lineages

Indexed keywords

PLANT RNA; RIBONUCLEASE;

ALLELE; ANGIOSPERM; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLOTYPE; METABOLISM; PLANT MORPHOLOGY; SELF FERTILIZATION; TOBACCO; TRANSGENIC PLANT;

ALLELES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENETIC VARIATION; HAPLOTYPES; PLANT STRUCTURES; PLANTS, GENETICALLY MODIFIED; RIBONUCLEASES; RNA, PLANT; SELF-FERTILIZATION; SOLANACEAE; TOBACCO;

MAGNOLIOPHYTA; NICOTIANA ALATA; SOLANACEAE;

EID: 77955697142     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-010-0860-6     Document Type: Article

References (58)

1. Anderson AG, McFadden I, Bernatzky R, Atkinson A, Orpin T et al (1989) Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1: 483-491.
2. de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin.
3. Dodds PN, Clarke AE, Newbigin E (1996) Molecular characterisation of an S-like RNase of Nicotiana alata that is induced by phosphate starvation. Plant Mol Biol 31: 227-238.
4. East E, Yarnell SH (1929) Studies on self-sterility VIII. Self-sterility allelomorphs. Genetics 14: 455-487.
5. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vázquez-Santana S, Kim S, Phillips TE, Cruz-García F, McClure BA (2006) S-RNase compartmentalization and HT-B degradation in self-incompatible Nicotiana. Nature 439: 805-810.
6. Golz JF, Clarke AE, Newbigin E, Anderson M (1998) A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. The Plant J 16: 591-599.
7. Goodspeed TH (1954) The genus Nicotiana. Origins, relationships and evolution of its species in the light of their distribution, morphology and cytogenetics. Chronica Botanica Company, Waltham, MA, pp 389-405.
8. Green PJ (1994) The ribonucleases of higher plants. Ann Rev of Plant Physiol Plant Mol Biol 45: 421-445.
9. Hancock CN, Kent L, McClure B (2005) The stylar 120 k glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43: 716-723.
10. Hauck NR, Yamane H, Tao R, Iezzoni AF (2006) Accumulation of non-functional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172: 1191-1198.
11. Hua Z, Kao T-h (2006) Identification and characterization of components of a putative PetuniaS-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18: 2531-2553.
12. Huang S, Lee HS, Karunandaa B, Kao T-h (1994) Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell 6: 1021-1028.
13. Hugot K, Ponchet M, Marais A, Ricci P, Galiana E (2002) A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol Plant Microbe Int 15: 243-250.
14. Igic B, Smith WA, Robertson KA, Schaal BA, Kohn JR (2007) Studies of self-incompatibility in wild tomatoes: I. S-allele diversity in Solanum chilense Dun. (Solanaceae). Heredity 99: 553-561.
15. Ioerger TR, Clarke AE, Kao T-h (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Nat Acad Sci USA 87: 9732-9735.
16. Ioerger TR, Gohlke JR, Xu B, Kao T-h (1991) Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4: 81-87.
17. Ippolito A, Fernandes GW, Holtsford TP (2004) Pollinator preferences for Nicotiana alata, N. forgetiana, and their F1 hybrids. Evolution 58: 2634-2644.
18. Kao T-h, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16: S72-S83.
19. Kokubun H, Nakano M, Tsukamoto T, Watanabe H, Hashimoto G, Marchesi E, Bullrich L, Basualdo IL, Kao TH, Ando T (2006) Distribution of self-compatible and self-incompatible populations of Petunia axillaris (Solanaceae) outside Uruguay. J Plant Res 5: 419-430.
20. Kuroda S, Norioka S, Mitta M, Kato I, Sakiyama F (1994) Primary structure of a novel stylar RNase unassociated with self-incompatibility in tobacco plant Nicotiana alata. J Prot Chem 13: 438-439.
21. Lee HS, Singh A, Kao T-h (1992) RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol 20: 1131-1141.
22. Lee HS, Huang S, Kao T-h (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367: 560-563.
23. Lee CB, Page LE, McClure BA, Holtsford TP (2008) Post-pollination hybridization barriers in Nicotiana section Alatae. Sex Plant Reprod 21: 183-195.
24. Liang L, Lai Z, Ma W, Zhang Y, Xue Y (2002) AhSL28, a senescence- and phosphate starvation-induced S-like RNase gene in Antirrhinum. Biochem Biophys Acta 17: 5964-5971.
25. Liang L, Huang J, Xue Y (2003) Identification and evolutionary analysis of a relic S-RNase in Antirrhinum. Sex Plant Reprod 16: 17-22.
26. Lu Y (2006) Historical events and allelic polymorphism at the gametophytic self-incompatibility locus in Solanaceae. Heredity 96: 22-28.
27. Luu DT, Qin XK, Morse D, Capadoccia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407: 649-651.
28. Matton DP, Maes C, Laublin G, Qin XK, Bertrand C, Morse D, Cappadoccia M (1997) Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9: 1757-1766.
29. McClure BA (2008) Comparing models for S-RNase-based self-incompatibility. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants. Evolution diversity and mechanisms. Springer, Berlin, pp 217-236.
30. McClure BA (2009) Darwin foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI. J Exp Bot 60: 1069-1081.
31. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342: 955-957.
32. McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347: 757-760.
33. McClure BA, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele specific pollen rejection in Nicotiana. Proc Nat Acad Sci USA 96: 13548-13553.
34. McClure BA, Cruz-García F, Beecher B, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Ann Bot 85: 113-123.
35. Mena-Alí JI, Stephenson AG (2007) Segregation analyses of partial self-incompatibility in self and cross progeny of Solanum carolinense reveal a leaky S-allele. Genetics 177: 501-510.
36. Miller JS, Levin RA, Feliciano NM (2008) A tale of two continents: Baker's rule and the maintenance of self-incompatibility in Lycium (Solanaceae). Evolution 5: 1052-1065.
37. 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: 563-566.
38. 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: 943-958.
39. O'Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP (2002) Molecular analysis of the stylar-expressed Solanumchacoense asparagine-rich protein family related to the HT modifier gametophytic self-incompatibility in Nicotiana. The Plant J 32: 1-12.
40. Pandey KK (1979) The genus Nicotiana: evolution of incompatibility in flowering plants. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic, London.
41. Puerta AR, Ushijima K, Koba T, Sassa H (2009) Identification and functional analysis of pistil self-incompatibility factor HT-B of Petunia. J Exp Bot 60: 1309-1318.
42. Richman A, Kohn JR (2000) Evolutionary genetics of self-incompatibility in the Solanaceae. Plant Mol Biol 42: 169-179.
43. Richman A, Kao T-h, Schaeffer SW, Uyenoyama MK (1995) S-allele sequence diversity in natural populations of Solanum carolinense (Horsenettle). Heredity 75: 405-415.
44. Richman AD, Uyenoyama MK, Kohn JR (1996) S-allele diversity in a natural population of Physalis crassifolia (Solanaceae) (ground cherry) assessed by RT-PCR. Heredity 76: 497-505.
45. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
46. Savage AE, Miller JS (2006) Gametophytic self-incompatibility in Lycium parishii (Solanaceae): allelic diversity, genealogical structure and patterns of molecular evolution. Heredity 96: 434-444.
47. Sijacic P, Wang X, Skirpan L, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao T-h (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429: 302-305.
48. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
49. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RaxML web servers. Syst Biol 57: 758-771.
50. Stone JL, Pierce S (2005) Rapid recent radiation of S-RNase lineages in Whiteringia solanaceae (Solanaceae). Heredity 94: 547-555.
51. Stone JL, Sasuclark MA, Blomberg C (2006) Variation in the self-incompatibility response within and among populations of the tropical shrub Witheringia solanaceae (Solanaceae). Am J Bot 93: 592-598.
52. Thompson JD, Gibson TJ, Plewniak F, Jeanmouguin F, Higgins DG (1997) The ClustalX window interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 24: 4876-4882.
53. Tsukamoto T, Ando T, Kokubun H, Watanabe H, Masada M, Zhu X, Marchesi E, T-h Kao (1999) Breakdown of self-incompatibility in a natural population of Petunia axillaris (Solanaceae) in Uruguay containing both self-incompatible and self-compatible plants. Sexual Plant Reprod 12: 6-13.
54. Tsukamoto T, Ando T, Kokubun H, Watanabe H, Sato T, Masada M, Marchesi E, Kao T-h (2003a) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by a modifier locus that suppresses the expression of an S-RNAse gene. Sexual Plant Reprod 15: 255-263.
55. Tsukamoto T, Ando T, Takahashi K, Omori T, Watanabe H, Kokubun H, Marchesi E, Kao T-h (2003b) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by loss of pollen function. Plant Physiol 131: 1903-1912.
56. Tsukamoto T, Potter V, Tao R, Vieira CP, Vieira J, Iezzoni AF (2008) Genetic and molecular characterization of three novel S-haplotypes in sour cherry (Prunus cerasus L.). J Exp Bot 59: 3169-3185.
57. Wang X, Tsukamoto T, Ando T, Kao T-h (2001) Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol 125: 1012-1022.
58. Wheeler D, Newbigin E (2007) Expression of 10 S-Class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics 177: 2171-2180.