Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Abstract

Self-incompatibility (SI) systems in flowering plants distinguish self-and non-self pollen to prevent inbreeding. While other SI systems rely on the self-recognition between specific male-and femaledeterminants, the Solanaceae family has a non-self recognition system resulting in the detoxification of female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen. It is not known how many SLF components of this non-self recognition system there are in Solanaceae species, or how they evolved. We identified 16-20 SLFs in each S-haplotype in SI Petunia, from a total of 168 SLF sequences using large-scale nextgeneration sequencing and genomic polymerase chain reaction (PCR) techniques. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated these predictions by transformation experiments. A simple mathematical model confirmed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to the constitution of a non-self recognition system and also contribute to self-compatible mutations. Self-incompatibility (SI) systems in flowering plants distinguish self and non-self pollen to prevent inbreeding. While all other SI systems studied to date rely on the self-recognition between each single male-and female-determinants, the Solanaceae plants has a non-self recognition system that functions through the detoxification of non-self female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen.However, little is known about how many SLF components constitute such a non-self recognition system and how they evolve. Here we conducted large-scale next-generation sequencing and genomic PCR and identified 16-20 SLFs in each S-haplotype in SI Petunia, for a total of 168 SLF sequences. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated them by transformation experiments. A simple mathematical model showed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to constitute a non-self recognition system and as well as contributed to self-compatible mutations.SI is a genetically controlled reproductive barrier in angiosperms that allows the pistil to reject self (genetically-related) pollen and accept non-self (genetically-unrelated) pollen [1][2][3][4] . In most cases, this self/non-self discrimination is controlled by male-and

Pollen-Pistil Interactions and Their Role in Mate Selection

“…Recent transcriptome studies suggest that an array of 16 to 20 SLF genes function in SI in Petunia spp. (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).…”

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

“…Therefore, if any of the SLF genes expressed in S. lycopersicum pollen (SlSLF-2, -3, -4, and -14) were functional, then at least some F 1 interspecific hybrids with SI species are predicted to be partially SC, but this has not been reported. The collaborative non-self-recognition model (6,34) predicts that each functional SLF protein recognizes one to two different S-RNase alleles; therefore, if the four genes in S. lycopersicum are functional, the expectation is that they should be compatible on four to eight S-haplotypes. However, only 25% of the pollen from the interspecific F 1 hybrids would contain both a functional CUL1 gene (from the SI parent) and the S c allele, including SlSLF genes, from S. lycopersicum.…”

DNA Markers and the Molecular Mechanism of Self-(in)compatibility in Japanese Pear (<i>Pyrus pyrifolia</i> Nakai)

“…Similarly, 16-20 S-locus F-box (SLF) genes were identified in each S-haplotype in Petunia, a member of the Solanaceae family that exhibits the same S-RNasebased GSI as Japanese pear (Hua et al, 2007;Kubo et al, 2010Kubo et al, , 2015McCubbin et al, 2000;Wang et al, 2003Wang et al, , 2004Williams et al, 2014a). These SLFs were classified into 18 types (SLF1-SLF18) based on their phylogenetic relationships (Kubo et al, 2015).…”

“…These SLFs were classified into 18 types (SLF1-SLF18) based on their phylogenetic relationships (Kubo et al, 2015). Transformation experiments showed that at least eight of the SLFs (SLF1-SLF6, SLF8, and SLF9) were involved in pollen specificity (Kubo et al, 2010(Kubo et al, , 2015Sijacic et al, 2004;Williams et al, 2014b).…”