Abstract
Non-self gametophytic self-incompatibility (GSI) recognition system is characterized by the presence of multiple F-box genes tandemly located in the S-locus, that regulate pollen specificity. This reproductive barrier is present in Solanaceae, Plantaginacea and Maleae (Rosaceae), but only in Petunia functional assays have been performed to get insight on how this recognition mechanism works. In this system, each of the encoded S-pollen proteins (called SLFs in Solanaceae and Plantaginaceae /SFBBs in Maleae) recognizes and interacts with a sub-set of non-self S-pistil proteins, called S-RNases, mediating their ubiquitination and degradation. In Petunia there are 17 SLF genes per S-haplotype, making impossible to determine experimentally each SLF specificity. Moreover, domain –swapping experiments are unlikely to be performed in large scale to determine S-pollen and S-pistil specificities. Phylogenetic analyses of the Petunia SLFs and those from two Solanum genomes, suggest that diversification of SLFs predate the two genera separation. Here we first identify putative SLF genes from nine Solanum and 10 Nicotiana genomes to determine how many gene lineages are present in the three genera, and the rate of origin of new SLF gene lineages. The use of multiple genomes per genera precludes the effect of incompleteness of the genome at the S-locus. The similar number of gene lineages in the three genera implies a comparable effective population size for these species, and number of specificities. The rate of origin of new specificities is one per 10 million years. Moreover, here we determine the amino acids positions under positive selection, those involved in SLF specificity recognition, using 10 Petunia S-haplotypes with more than 11 SLF genes. These 16 amino acid positions account for the differences of self-incompatible (SI) behavior described in the literature. When SLF and S-RNase proteins are divided according to the SI behavior, and the positively selected amino acids classified according to hydrophobicity, charge, polarity and size, we identified fixed differences between SI groups. According to the in silico 3D structure of the two proteins these amino acid positions interact. Therefore, this methodology can be used to infer SLF/S-RNase specificity recognition.
Highlights
To avoid self-fertilization and promote out-crossing, many Angiosperms have developed self-incompatible (SI) mechanisms, that allow the pistil to reject self-pollen and only nongenetically related pollen is allowed to effect fertilization (De Nettancourt, 1977)
The Bayesian phylogenetic tree obtained using the 29 Nicotiana and 75 Solanum SLF sequences obtained after using the Get open reading frames (ORFs) option of BDBM (Vázquez et al, 2019; using the nine available genomes for eight Solanum species, and the 10 available genomes for seven Nicotiana species; Table 1; see Material and Methods), together with one sequence of each Petunia gene, and the nine N. alata SLF sequences, revealed five gene lineages common to the three genera, six present in Petunia and Solanum (PS in Supplementary Figure S2), three in Petunia and Nicotiana (PN in Supplementary Figure S2), and three in Nicotiana and Solanum (NS in Supplementary Figure S2)
It is conceivable that the sequence we retrieved comes from a yet to be characterized S-haplotype, but it is possible that the observed differences are due to sequencing or assembly mistakes. This approach shows that the Petunia genomes here used either have a low coverage or the S-locus region is difficult to assemble in Petunia
Summary
To avoid self-fertilization and promote out-crossing, many Angiosperms have developed self-incompatible (SI) mechanisms, that allow the pistil to reject self-pollen and only nongenetically related pollen is allowed to effect fertilization (De Nettancourt, 1977). In the Rosaceae family, two gene lineages are determining Prunus (Amygdaleae) and Malus (Maleae) Spistil and S-pollen specificity (Aguiar et al, 2015) In these species a self- and non-self- recognition mechanisms is present, respectively. Only Prunus has an RNase based selfrecognition mechanism In this system, only one S-pollen gene (called SFB), is sufficient to account for the self-S-RNase inhibition (Entani et al, 2003; Ushijima et al, 2003; Ikeda et al, 2004; Tsukamoto et al, 2005, 2010; Nunes et al, 2006; Hua et al, 2007; Aguiar et al, 2015). A “general inhibitor,” such as the gene products of the F-box like genes in the vicinity of the S-locus region (Matsumoto and Tao, 2016; Chen et al, 2018), inactivate the cytotoxic effect of non-self S-RNases (Luu et al, 2001; Sonneveld et al, 2005)
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