Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

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 ubiquitinproteasome pathway, a mechanism related to that which controls pollen recognition in SI.interspecific incompatibility | self-incompatibility | Solanum lycopersicum | Solanum pennellii | S-locus F-box protein

Pollen-Pistil Interactions and Their Role in Mate Selection

“…(Box 2; Williams et al, 2014a;Kubo et al, 2015). Consistent with this finding, the genome sequence of SC Solanum pennellii LA0716 (a recently derived SC accession of an otherwise SI species) contains an array of 23 SLF genes, while the SC tomato genome shows, at most, four intact genes (Bolger et al, 2014;Li and Chetelat, 2015).…”

“…A loss-of-function study showed that CUL1 also functions in SI (Li and Chetelat, 2014). Recently, the ui1.1 factor was identified as a single SLF gene, SLF-23 (Li and Chetelat, 2015). Thus, SI and UI utilize shared factors for both the pollen-and pistil-side functions and are characterized by a pistil-barrier/pollen-resistance architecture.…”

Evaluation of crossability studies between selected eggplant accessions with wild relatives S. torvum, S. anguivi and S. aethopicum (Shum group)

“…McClure et al (1989) and Sijacic et al (2004) also attributed unilateral incompatibility in Solanum and other Solanaceae to the S-RNase-based, gametophytic type, in which S-specificity is determined by S-RNases in the pistil and S-locus F-box proteins (SLFs) in pollen. Li and Chetelat (2014) further emphasized that pollen rejection in UI involves biochemical mechanisms related to SI (self-incompatibility). According to Li and Chetelat (2014), ui1.1, a pollen UI factor in tomato, encodes an S-locus Fbox protein that is homologous to an SI gene that in Petunia determines pollen specificity.…”

“…Li and Chetelat (2014) further emphasized that pollen rejection in UI involves biochemical mechanisms related to SI (self-incompatibility). According to Li and Chetelat (2014), ui1.1, a pollen UI factor in tomato, encodes an S-locus Fbox protein that is homologous to an SI gene that in Petunia determines pollen specificity. Thus, pollen rejection in UI involves biochemical mechanisms related to SI.…”

Correlated evolution of self and interspecific incompatibility across the range of a Texas wildflower

“…This co‐variation between SI and II has been termed the SI × SC rule, and results in an asymmetric barrier to hybridization called ‘unilateral incompatibility’. In some systems, such as Solanum (de Nettancourt, ; Hancock et al ., ; Li & Chetelat, , , ) and Nicotiana (Murfett et al ., ), unilateral incompatibility arises because the genes causing SI also cause II. A pleiotropic link between SI and II implies that if selection acts on one incompatibility, the other type of incompatibility will show a correlated response to selection.…”