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Molecular characterization of three non-functional S-haplotypes in sour cherry (Prunus cerasus)

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Abstract

Tetraploid sour cherry (Prunus cerasus) exhibits a genotype-dependent loss of gametophytic self-incompatibility that is caused by the accumulation of non-functional S-haplotypes with disrupted pistil component (stylar-S) and/or pollen component (pollen-S) function. Genetic studies using diverse sour cherry germplasm identified non-functional S-haplotypes for which an equivalent wild-type S-haplotype was present in sweet cherry (Prunus avium), a diploid progenitor of sour cherry. In all cases, the non-functional S-haplotype resulted from mutations affecting the stylar component S-RNase or Prunus pollen component S-haplotype-specific F-box protein (SFB). This study determines the molecular bases of three of these S-haplotypes that confer unilateral incompatibility, two stylar-part mutants (S 6m2 and S 13m ) and one pollen-part mutant (S 13 ′). Compared to their wild-type alleles, S 6m2 -RNase has a 1 bp deletion, S 13m -RNase has a 23 bp deletion and SFB 13 ′ has a 1 bp substitution that lead to premature stop codons. Transcripts were identified for these three alleles, S 6m2 -RNase, S 13m -RNase, and SFB 13 ′, however, these transcripts presumably result in altered proteins with a resulting loss of activity. Our characterization of natural pollen-part and stylar-part mutants in sour cherry along with other natural S-haplotype mutants identified in Prunus supports the view that loss of pollen specificity and stylar rejection evolve independently and are caused by structural alterations affecting the S-haplotype. The prevalence of non-functional S-haplotypes in sour cherry but not in sweet cherry (a diploid) suggests that polyploidization and gene duplication were indirectly responsible for the dysfunction of some S-haplotypes and the emergence of self-compatibility in sour cherry. This resembles the specific mode of evolution in yeast where accelerated evolution occurred to one member of the duplicated gene pair.

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Abbreviations

GSI:

Gametophytic self-incompatibility

RT-PCR:

Reverse transcriptase PCR

R:

Rheinische

SI:

Self-incompatible

SC:

Self-compatible

SFB:

S-haplotype-specific F-box protein

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Acknowledgments

This work was supported by a grant from the USDA Cooperative State Research, Education, and Extension Service—National Research Initiative—Plant Genome Program.

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Authors and Affiliations

  1. Department of Horticulture, Michigan State University, East Lansing, MI, 48824, USA

    Tatsuya Tsukamoto, Nathanael R. Hauck, Ning Jiang & Amy F. Iezzoni

  2. Laboratory of Pomology, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Ryutaro Tao

Authors
  1. Tatsuya Tsukamoto
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  2. Nathanael R. Hauck
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  3. Ryutaro Tao
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  4. Ning Jiang
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  5. Amy F. Iezzoni
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Corresponding author

Correspondence to Amy F. Iezzoni.

Additional information

The nucleotide sequences reported in this paper have been submitted to the GenBank/EMBL/DDBJ database under accession numbers: DQ385841 (S 6m2 -RNase), DQ385842 (S 13 -RNase), DQ385843 (S 13m -RNase), DQ385844 (SFB 13 ), and␣DQ385845 (SFB 13 ′)

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Tsukamoto, T., Hauck, N.R., Tao, R. et al. Molecular characterization of three non-functional S-haplotypes in sour cherry (Prunus cerasus). Plant Mol Biol 62, 371–383 (2006). https://doi.org/10.1007/s11103-006-9026-x

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  • DOI: https://doi.org/10.1007/s11103-006-9026-x

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