Diversification and distinctive structural features of S-RNase alleles in the genus Solanum

Abstract

The multigenic and multiallelic S-locus in plants is responsible for the gametophytic self-incompatibility system, which is important to prevent the detrimental effects of self-fertilization and inbreeding depression. Several studies have discussed the importance of punctual mutations, recombination, and natural selection in the generation of allelic diversity in the S-locus. However, there has been no wide-ranging study correlating the molecular evolution and structural aspects of the corresponding proteins in Solanum. Therefore, we evaluated the molecular evolution of one gene in this locus and generated a statistically well-supported phylogenetic tree, as well as evidence of positive selection, helping us to understand the diversification of S alleles in Solanum. The three-dimensional structures of some of the proteins corresponding to the major clusters of the phylogenetic tree were constructed and subsequently submitted to molecular dynamics to stabilize the folding and obtain the native structure. The positively selected amino acid residues were predominantly located in the hyper variable regions and on the surface of the protein, which appears to be fundamental for allele specificity. One of the positively selected residues was identified adjacent to a conserved strand that is crucial for enzymatic catalysis. Additionally, we have shown significant differences in the electrostatic potential among the predicted molecular surfaces in S-RNases. The structural results indicate that local changes in the three-dimensional structure are present in some regions of the molecule, although the general structure seems to be conserved. No previous study has described such structural variations in S-RNases.

Overcoming Self-Incompatibility in Diploid Potato Using CRISPR-Cas9

“…Amino acid sequence variation within S-RNase was observed among S. tub _S p5 , S. tub _S t5 , and S. tub _S t6 alleles (Figure 1A). Nearly half of these variants were within the hypervariable domains (HVa and HVb) and not in conserved domains (C1-5) consistent with data that show the S-RNase variable regions are the determinants for allele specificity in different Solanum species (Matton et al, 1997, 1999; Brisolara-Corrêa et al, 2015). Specifically, four amino acids within these variable regions (T74, N76, Y77, and R101) have been reported as the sole factors for allele conversion of the pollen rejection phenotype in S. chacoense (Matton et al, 1997).…”

Electrostatic potentials of the S‐locus F‐box proteins contribute to the pollen S specificity in self‐incompatibility in Petunia hybrida

“…Recently, a ‘collaborative non‐self recognition’ system of S‐RNase‐based SI in Solanaceae was proposed, in which the product of each SLF interacts with a subset of non‐self S‐RNases, and the products of multiple SLF types are required for the entire collection of non‐self S‐RNases to be collectively recognized (Kubo et al ., ). Recent studies have shown two hypervariable regions of S‐RNases, named HVa and HVb, are involved in their specificity and both regions are exposed on the protein surface (Matton et al ., , ; Ida et al ., ; Matsuura et al ., ), and most positively selected sites are located in the HV regions of S‐RNase of the Solanaceae, supporting an important role of the HV regions in their specific recognition (Vieira et al ., ; Brisolara‐Correa et al ., ). SLF is an F‐box protein with a conserved F‐box domain at the N terminus.…”

Predicting Specificities Under the Non-self Gametophytic Self-Incompatibility Recognition Model

“…Domain-swapping transgenic experiments with similar S-RNase alleles have showed that the two hypervariable regions of S-RNases , are involved in specificity determination (Ide et al, 1991; Matton et al, 1997, 1999; Matsuura et al, 2001). Although there are positively selected amino acid sites in these regions, there are other amino acid sites in other regions of the S -pistil gene, that may be involved in recognition of the S -pollen gene(s) (Vieira et al, 2007; Brisolara-Correa et al, 2015). To address S -pollen specificity, Petunia SLF1 gene has been divided into three functional domains (FD1 from amino acid position 1 to 110; FD2, from amino acid position 110 to 260, and FD3 from amino acid position 260 to 389), and in vivo assays performed.…”