Wentao Li and Roger T. Chetelat

Significance

Self-incompatibility (SI) in plants prevents inbreeding by rejection of pollen from closely related individuals of the same species. Unilateral interspecific incompatibility (UI) blocks cross-hybridization between related species, typically when the pollen donor is self-compatible and the pistil parent is self-incompatible. In this study, we show that ui1.1, a pollen UI factor in tomato, encodes an S-locus F-box protein that is homologous to an SI gene that in Petunia determines pollen specificity. We previously showed that another pollen factor, ui6.1, encodes a Cullin1 protein that functions in both UI and SI. Cullin1 and F-box proteins are components of SCF-type (Skp1, Cullin1, F-box) ubiquitin ligase complexes. The results provide further evidence that pollen rejection in UI involves biochemical mechanisms related to SI.

Abstract

Unilateral interspecific incompatibility (UI) is a postpollination, prezygotic reproductive barrier that prevents hybridization between related species when the female parent is self-incompatible (SI) and the male parent is self-compatible (SC). In tomato and related Solanum species, two genes, ui1.1 and ui6.1, are required for pollen compatibility on pistils of SI species or hybrids. We previously showed that ui6.1 encodes a Cullin1 (CUL1) protein. Here we report that ui1.1 encodes an S-locus F-box (SLF) protein. The ui1.1 gene was mapped to a 0.43-cM, 43.2-Mbp interval at the S-locus on chromosome 1, but positional cloning was hampered by low recombination frequency. We hypothesized that ui1.1 encodes an SLF protein(s) that interacts with CUL1 and Skp1 proteins to form an SCF-type (Skp1, Cullin1, F-box) ubiquitin E3 ligase complex. We identified 23 SLF genes in the S. pennellii genome, of which 19 were also represented in cultivated tomato (S. lycopersicum). Data from recombination events, expression analysis, and sequence annotation highlighted 11 S. pennellii genes as candidates. Genetic transformations demonstrated that one of these, SpSLF-23, is sufficient for ui1.1 function. A survey of cultivated and wild tomato species identified SLF-23 orthologs in each of the SI species, but not in the SC species S. lycopersicum, S. cheesmaniae, and S. galapagense, pollen of which lacks ui1.1 function. These results demonstrate that pollen compatibility in UI is mediated by protein degradation through the ubiquitin–proteasome pathway, a mechanism related to that which controls pollen recognition in SI.

See: http://www.pnas.org/content/112/14/4417.figures-only

PNAS April 7, 2015 vol. 112 no. 14 4417-4422

Fig. 1.

Genetic and physical maps of the ui1.1 region, showing positions of SLF genes in S. lycopersicum and S. pennellii. (A) Genetic map of the S-locus region on chromosome 1, from the EXPEN 2000 interspecific mapping population. (B) Genetic map of the ui1.1 region from a BC mapping population of 1,632 individuals. Recombination suppression reduced the genetic distance of this region to less than 25% of the reference map. (C) Physical map of markers based on the Tomato WGS Chromosomes (ver. SL2.31). (D) Physical map of SLF genes identified in the Tomato WGS Chromosomes. Note: 19 SLF genes were found this region, of which 4 were ruled out as ui1.1 candidates based on the positions of flanking markers. Open ovals, genes with likely loss-of-function mutations; shaded ovals, putative functional genes. (E) SLF genes identified in the S. pennellii genome. Hatched ovals, four S. pennellii SLF genes not present in S. lycopersicum.