Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus

Abstract

The transition from self-incompatibility (SI) to self-compatibility (SC) is regarded as one of the most prevalent transitions in Angiosperm evolution, having profound impacts on the genetic structure of populations. Yet, the identity and function of mutations that result in the breakdown of SI in nature are not well understood. This work provides the first detailed genetic description of the breakdown of S-RNase-mediated gametophytic self-incompatibility (GSI) in a polyploid species that exhibits genotype-dependent loss of SI. Genetic analyses of six natural sour cherry (Rosaceae, Prunus cerasus) selections identified seven independent, nonfunctional S-haplotypes with disrupted pistil component (stylar-S) and/or pollen component (pollen-S) function. A genetic model demonstrating that the breakdown of SI in sour cherry is due to the accumulation of a minimum of two nonfunctional S-haplotypes within a single individual is developed and validated. Our finding that sour cherry is SI when only one nonfunctional S-haplotype is present has significant evolutionary implications since nonfunctional S-haplotypes would be maintained in the population without causing an abrupt shift to SC. Furthermore, we demonstrate that heteroallelic sour cherry pollen is self-incompatible, which is counter to the well-documented phenomenon in the Solanaceae where SC accompanying polyploidization is frequently due to the SC of heteroallelic pollen.

Figure 1.

Schematics of the interspecific crosses between RS (S₆S_13′ S₂₆S_a) and Gold (S₃S₆) and the self-pollination of RS. (A) Pollination of RS styles with Gold pollen results in the rejection of all pollen containing the S₆-haplotype. Pollen containing the S₃-haplotype is successful. (B) Pollination of Gold styles with RS pollen results in the rejection of all pollen containing the S₆-haplotype. Any pollen that does not contain the S₆-haplotype is successful. Because sour cherry exhibits homologous and occasional nonhomologous pairing (Beaver and Iezzoni 1993), all possible chromosome-pairing configurations are considered. Pollen types formed by homologous pairing are shaded. (C) Self-pollination of RS results in rejection of all pollen containing either S₆ or S₂₆ or both. The only successful pollen is S_13′S_a.

Figure 2.

Schematic of the affects of polyploidy on GSI in (A) the Solanaceae and (B) Prunus. In the Solanaceae, polyploidy directly causes the conversion from SI to SC due to the compatibility of heteroallelic pollen. In Prunus, polyploidy does not directly result in a breakdown of SI. Rather, SC requires the loss-of-function for a minimum of two S-haplotype-specificity components. Polyploidization creating tetraploid sour cherry presumably resulted from the mating of a 2n gamete from sweet cherry and an n gamete from tetraploid ground cherry (Iezzoni and Hancock 1984).