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Evaluation of candidate F-box genes for the pollen S of gametophytic self-incompatibility in the Pyrinae (Rosaceae) on the basis of their phylogenomic context

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Abstract

The recent analysis of the S-locus region of apple and Japanese pear, two species of Pyrinae (Rosaceae), suggested multiple and different F-box genes (called SFBBs) as candidates for the male determinant (pollen S) of RNase-based gametophytic self-incompatibility in these two species. Here, we followed a phylogenetic approach to take advantage of the pattern of molecular evolution of the S-locus of Pyrinae in characterizing SFBB homologs belonging to S-haplotypes of apple and three species of Pyrus (European, Japanese, and Chinese pears). Our results suggested that the S-locus region of Pyrinae contains no less than six SFBB members and that its structure seems to be rather conserved between apple and pear species. In accordance with the prevailing theory on S-haplotype evolution, the pollen S is expected to have coevolved with the S-RNase and to show some common features derived from the long-term evolution under frequency-dependent balancing selection, i.e., high sequence diversity, evidence of positive selection, and shared ancestral polymorphisms. Using this conceptual framework, we present evidence that some SFBB genes may be better candidates for pollen S in Pyrinae than others. Overall, the SFBB genes analyzed exhibited much lower sequence diversity than their associated S-RNases; likewise, they showed little or no evidence of positive selection. However, evidence of coevolution with the S-RNase clearly emerged for two of them. Altogether our results suggested different evolutionary histories for different SFBBs putatively derived from their distinct involvement in self-incompatibility.

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Acknowledgments

This work was supported by project grants from the “Ministerio de Ciencia e Innovación de España”–EU-FEDER (CICYT AGL2006-13529-CO2-02 and AGL2009-12621-C02-02) and “Gobierno de Aragón” (Grupo de Excelencia de Aragón A-43) and by the PRIN project (MIUR, Rome) 2007 “The productive process in fruit tree species: molecular, physiological and agronomical aspects of floral incompatibility and strategies for its control”. JS acknowledges “Instituto de Investigación y Tecnología Agroalimentaria”–INIA_CCAA Program and “Ministerio de Ciencia e Innovación de España”–I3 Program for financial support.

Ethical standards and conflict of interest declaration

The authors declare that all the experiments comply with the current laws of the country in which they were performed (Italy, Spain) and that they have no conflicts of interest.

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Authors and Affiliations

  1. Dipartimento di Colture Arboree (DCA), Università degli Studi di Bologna, Via Giuseppe Fanin 46, 40127, Bologna, Italy

    Paolo De Franceschi, Luca Pierantoni, Luca Dondini, Marco Grandi & Silviero Sansavini

  2. Unidad de Fruticultura, Centro de Investigación y Tecnología Agroalimentaria de Aragón (CITA), Avenida de Montañana 930, 50059, Zaragoza, Spain

    Javier Sanzol

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  1. Paolo De Franceschi
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  2. Luca Pierantoni
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  3. Luca Dondini
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  5. Silviero Sansavini
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  6. Javier Sanzol
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Correspondence to Paolo De Franceschi or Javier Sanzol.

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Communicated by A. Abbott

Electronic supplementary material

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ESM 1

Accession numbers of 64 Pyrinae S-RNases and ten SFBB sequences from apple and three species of Pyrus, downloaded from GenBank. (PDF 62 kb)

ESM 2

Sequence distances calculated among the S-RNase alleles present in the cultivars analyzed in this study. (PDF 45 kb)

ESM 3

Alignment between the putative pseudogene SFBBβ-Wild1, characterized in the European pear ‘Wilder’, and the functional genes PpSFBB 4-β and PpSFBB 5-β. (PDF 76 kb)

ESM 4

Evaluation of positive selection on the S-RNase and SFBB genes with PAML 4 using site models. (PDF 61 kb)

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De Franceschi, P., Pierantoni, L., Dondini, L. et al. Evaluation of candidate F-box genes for the pollen S of gametophytic self-incompatibility in the Pyrinae (Rosaceae) on the basis of their phylogenomic context. Tree Genetics & Genomes 7, 663–683 (2011). https://doi.org/10.1007/s11295-011-0365-7

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