Plant Molecular Biology

, Volume 63, Issue 1, pp 109–123 | Cite as

Self-compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species

  • Ryutaro Tao
  • Akiko Watari
  • Toshio Hanada
  • Tsuyoshi Habu
  • Hideaki Yaegaki
  • Masami Yamaguchi
  • Hisayo Yamane
Article

Abstract

This study demonstrates that self-compatible (SC) peach has mutant versions of S haplotypes that are present in self-incompatible (SI) Prunus species. All three peach S haplotypes, S1, S2, and S2m, found in this study encode mutated pollen determinants, SFB, while only S2m has a mutation that affects the function of the pistil determinant S-RNase. A cysteine residue in the C5 domain of the S2m-RNase is substituted by a tyrosine residue, thereby reducing RNase stability. The peach SFB mutations are similar to the SFB mutations found in SC haplotypes of sweet cherry (P. avium) and Japanese apricot (P. mume). SFB1 of the S1 haplotype, a mutant version of almond (P. dulcis) Sk haplotype, encodes truncated SFB due to a 155 bp insertion. SFB2 of the S2 and S2m haplotypes, both of which are mutant versions of the Sa haplotype in Japanese plum (P. salicina), encodes a truncated SFB due to a 5 bp insertion. Thus, regardless of the functionality of the pistil determinant, all three peach S haplotypes are SC haplotypes. Our finding that peach has mutant versions of S haplotypes that function in almond and Japanese plum, which are phylogenetically close and remote species, respectively, to peach in the subfamily Prunoideae of the Roasaceae, provides insight into the SC/SI evolution in Prunus. We discuss the significance of SC pollen part mutation in peach with special reference to possible differences in the SI mechanisms between Prunus and Solanaceae.

Keywords

Self-incompatibility SFB·S-RNase Pistil part mutations Pollen part mutations F-box protein 

Abbreviations

GSI

gametophytic self-incompatibility

Pollen component

pollen S

SC

self-compatibility

SFB

S-haplotype-specific F-box gene

SI

self-incompatibility

SLFL

S locus F-box genes with the low allelic sequence polymorphism

S-RNase

self-incompatibility RNase

Stylar component

pistil S

References

  1. Brown PH, Ho T-HD (1986) Barley aleurone layers secrete a nuclease in response to gibberellic acid: Purification and partial characterization of the associated ribonuclease, deoxyribonuclease, and 3’-nucleotidase activities. Plant Physiol 82:801–806PubMedGoogle Scholar
  2. Channuntapipat C, Sedgley M, Collins G (2001) Sequences of the cDNAs and genomic DNAs encoding the S1, S7, S8, and Sf alleles from almond, Prunus dulcis. Theor. Appl. Genet 103:1115–1122CrossRefGoogle Scholar
  3. Chase MW, Soltis DE, Olmestead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hils HG, Qiu YL, Kron LA, Retting JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Herdren M, Gaut BS, Jansen RK, Kim KJ, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang QY, Plunkett CJ, Eguiarte LE, Golenberg E, Learn GH, Graham SW, Barett SCH, Dayanandan S,Albert VA (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann. Mo. Bot. Gard 80:528–580CrossRefGoogle Scholar
  4. de Nettancourt D (2001) Incompatibility and Incongruity in Wild and Cultivated Plants. Springer-Verlag, Berlin Google Scholar
  5. Dirlewanger ED, Graziano E, Joobeur T, Garriga-Calderé F Cosson P, Howad W, Arús P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc. Natl. Sci. USA 101:9891–9896CrossRefGoogle Scholar
  6. Faust M, Timon B (1995) Origin and dissemination of peach. Hort. Rev 17:331–379Google Scholar
  7. Entani T, Iwono M, Shiba H, Che FS, Isogai A,Takayama S (2003) Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213CrossRefPubMedGoogle Scholar
  8. Entani T, Takayama S, Iwano M, Shiba H, Ches FS, Isogai A (1999) Relationship between polyploidy and pollen self-incompatibility phenotype in Petunia hybrida Vilm. Bios. Biotech. Biochem 63:1882–1888CrossRefGoogle Scholar
  9. Golz JF, Oh H-Y, Su V, Kusaba M, 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. Soc. Sci. USA 98:15372–15376CrossRefGoogle Scholar
  10. Hancock CN, Kent L, McClure BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant. J 43:716–723CrossRefPubMedGoogle Scholar
  11. Hauck, N.R., Ikeda, K., Tao, R., Iezzoni, A. (2006a) The mutated S 1-haplotype in sour cherry has an altered S-haplotype specific F-box pretein gene. J. Hered. (in press)Google Scholar
  12. Hauck NR, Yamane H, Tao R, Iezzoni A (2006b) Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172:1191–1198CrossRefGoogle Scholar
  13. Hesse CO (1975) Peaches. In: Janick J, Moore JN (Eds.), Advances in Fruit Breeding. Purdue Univ. Press, West Lafayette, pp. 285–335 Google Scholar
  14. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc. Natl. Acad. Sci. USA 98:13167–13171CrossRefPubMedGoogle Scholar
  15. Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R, Sassa H, Iezzoni A, Kohon JR,Tao R (2004) Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus. Sex. Plant Reprod 16:235–243CrossRefGoogle Scholar
  16. Ikeda K, Ushijima K, Yamane H, Tao R, Hauck NR, Sebolt AM, Iezzoni AF (2005) Linkage and physical distances between the S-haplotype S-RNase and SFB genes in sweet cherry. Sex. Plant Reprod 17:289–296CrossRefGoogle Scholar
  17. Kester DE, Asay R (1975) Almonds. In: Janick J, Moore JN (Eds.), Advances in Fruit Breeding. Purdue Univ. Press, West Lafayette, pp. 387–419Google Scholar
  18. Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol. Biol 50:29–42CrossRefPubMedGoogle Scholar
  19. Lewis D, Crowe LK (1954) Structure of the incompatibility gene. IV. Types of mutations in Prunus avium L. Heredity 8:357–363Google Scholar
  20. Lewis D, Modlibowska I (1942) Genetical studies in pears. IV. Pollen-tube growth and incompatibility. J. Genet 43:211–222CrossRefGoogle Scholar
  21. Matsuura T, Sakai H, Unno M, Ida K, Sato M, Sakiyama F, Norioka S (2001) Crystal structure at 1.5-Å resolution of Pyrus pyrifolia pistil ribonuclease responsible for gametophytic self-incompatibility. J. Boiol. Chem 48:45261–45269CrossRefGoogle Scholar
  22. McClure BA, 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 96:13548–13553CrossRefPubMedGoogle Scholar
  23. Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB (2004) Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the evolution of selfing. Proc. Natl. Acad. Sci. USA 45:16070–16074CrossRefGoogle Scholar
  24. Porcher E, Lande R (2005) Loss of gametophytic self-incompatibility with evolution of inbreeding depression. Evolution 59:46–60CrossRefPubMedGoogle Scholar
  25. Qin S, Soulard J, Laublin G, Morse D, Cappadocia M (2005) Molecular analysis of the conserved C4 region of the S11-RNase of Solanum chacoense. Planta 221:531–537CrossRefPubMedGoogle Scholar
  26. Romero C, Vilanova S, Burgos L, Martínez-Calvo J, Vicente M, Llácer G, Madenes ML (2004) Analysis of S-locus structure in Prunus armeniaca L: identification of S-haplotype specific S-RNase and F-box genes. Plant Mol. Biol 56:145–157CrossRefPubMedGoogle Scholar
  27. Shimizu KK, Cork JM, Caicedo AL, Mays CA, Moore RC, Olsen KM, Ruzza S Coop G, Bustamante CD, Awadalla P, Purugganan MD (2004) Darwinian selection on a selfing locus. Science 306:2081–2084CrossRefPubMedGoogle Scholar
  28. Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao T (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305CrossRefPubMedGoogle Scholar
  29. Sonneveld T, Tobutt KR, Vaughan SP, Robbins TP (2005) Loss of pollen-S function in two self-compatible selections of Prunus avium is associated with deletion/mutation of an S haplotype-specific F-box gene. Plant Cell 17:37–51CrossRefPubMedGoogle Scholar
  30. Tao R, Yamane H, Sassa H, Mori H, Gradziel TM, Dandekar AM, Sugiura A (1997) Identification of stylar RNases associated with gametophytic self-incompatibility in almond (Prunus dulcis). Plant Cell Physiol 38:304–311PubMedGoogle Scholar
  31. Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999) Molecular typing of S-alleles through identification, characterization and cDNA cloning for S-RNases in sweet cherry. J. Am. Soc. Hort. Sci (124):224–233Google Scholar
  32. Tsukamoto, T, Hauck, NR, Tao, R, Jiang, N, Iezzoni, AF (2006) Molecular characterization of three non-functional S-haplotypes in sour cherry (Prunus cerasus). Plant Mol. Biol. (in press)Google Scholar
  33. Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781CrossRefPubMedGoogle Scholar
  34. Ushijima K, Sassa H, Tamura M, Kusaba M, Tao R, Gradziel TM, Dandekar AM, Hirano H (2001) Characterization of the S-locus region of almond (Prunus dulcis): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. Genetics 158:379–386PubMedGoogle Scholar
  35. Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol. Gen. Genet 260:261–268CrossRefPubMedGoogle Scholar
  36. Ushijima K, Yamane H, Watari A, Kakehi E, Hauck NR, Iezzoni AF, Tao R (2004) The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J 39:573–586CrossRefPubMedGoogle Scholar
  37. Wünsch A, Hormaza JI (2004) Genetic and molecular analysis in Cristobalina sweet cherry, a spontaneous self-compatible mutant. Sex. Plant Reprod 17:203–210CrossRefGoogle Scholar
  38. Yamane H, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2003a) Self-incompatibility (S) locus region of the mutated S 6-haplotype of sour cherry (Prunus cerasus) contains a functional pollen S allele and a non-functional pistil S allele. J. Exp. Bot 54:2431–2437CrossRefGoogle Scholar
  39. Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003b) 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 44:764–769CrossRefGoogle Scholar
  40. Yamane H, Tao R, Mori H, Sugiura A (2003c) Identification of a non-S RNase, a possible ancestral form of S-RNases, in Prunus. Mol. Gen. Genomics 269:90–100Google Scholar
  41. Yamane H, Ushijima K, Sassa H, Tao R, 2003d. The use of S haplotype-specific F-box protein gene, SFB, as a molecular marker for S-haplotypes and self-compatibility in Japanese apricot (Prunus mume). Theor. Appl. Genet 107:1357–1361CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Ryutaro Tao
    • 1
  • Akiko Watari
    • 1
  • Toshio Hanada
    • 1
  • Tsuyoshi Habu
    • 2
  • Hideaki Yaegaki
    • 3
  • Masami Yamaguchi
    • 3
  • Hisayo Yamane
    • 1
  1. 1.Laboratory of Pomology, Graduate School of AgricultureKyoto UniversityKyoto Japan
  2. 2.Experimental Farm, Graduate School of AgricultureKyoto UniversityTakatsuki Japan
  3. 3.National Institute of Fruit Tree ScienceTsukuba Japan

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