Population Genomics of the “Arcanum” Species Group in Wild Tomatoes: Evidence for Separate Origins of Two Self-Compatible Lineages

Abstract

Given their diverse mating systems and recent divergence, wild tomatoes (Solanum section Lycopersicon) have become an attractive model system to study ecological divergence, the build-up of reproductive barriers, and the causes and consequences of the breakdown of self-incompatibility. Here we report on a lesser-studied group of species known as the “Arcanum” group, comprising the nominal species Solanum arcanum, Solanum chmielewskii, and Solanum neorickii. The latter two taxa are self-compatible but are thought to self-fertilize at different rates, given their distinct manifestations of the morphological “selfing syndrome.” Based on experimental crossings and transcriptome sequencing of a total of 39 different genotypes from as many accessions representing each species’ geographic range, we provide compelling evidence for deep genealogical divisions within S. arcanum; only the self-incompatible lineage known as “var. marañón” has close genealogical ties to the two self-compatible species. Moreover, there is evidence under multiple inference schemes for different geographic subsets of S. arcanum var. marañón being closest to S. chmielewskii and S. neorickii, respectively. To broadly characterize the population-genomic consequences of these recent mating-system transitions and their associated speciation events, we fit demographic models indicating strong reductions in effective population size, congruent with reduced nucleotide and S-locus diversity in the two independently derived self-compatible species.

S-RNase Alleles Associated With Self-Compatibility in the Tomato Clade: Structure, Origins, and Expression Plasticity

“…In addition to the four red/orange fruited tomato species, there are two additional SC species that group within a subclade known as the Arcanum group, which contains three species: SI S. arcanum , SC S. chmielewskii and SC S. neorickii . Recent data have shown that while both SC species are derived from SI S. arcanum , they are independently derived from distinct geographical subsets of S. arcanum ( Florez-Rueda et al, 2021 ). The single known S-RNase allele in S. chmielewskii , LcwSRN-1 (after the previous species name, Lycopersicum chmielewskii ), is not expressed at the RNA level ( Kondo et al, 2002a ), and the transition from SI to SC in S. chmielewskii likely followed the typical pistil first pattern with a loss of S-RNase function ( Markova et al, 2017 ).…”

The role of hybrid seed inviability in angiosperm speciation

“…Hanneman, 1980, 1982;Dinu et al, 2005); Div: (Särkinen et al, 2013;Fumia, 2021;Tang et al, 2022) Solanum sect. Lycopersicon celluar several instances; often complete or strongly asymmetric crown age ~1.2-2.6MY, incidences in species pairs <1MY diverged Both (Rick, 1963;Ehlenfeldt and Hanneman, 1992;Ehlenfeldt and Ortiz, 1995;Baek et al, 2016;Roth et al, 2018a;Florez-Rueda et al, 2021b)Div: (Särkinen et al, 2013;Pease et al, 2016) Brassica nuclear several instances; often strong earliest incidences between species ~2MY diverged Both (Nishiyama et al, 1991); Div: (Li et al, 2017) Nicotiana celluar several instances; often complete or strongly asymmetric crown age ~10-13MYA; few crosses made between recently diverged species Both (McCray, 1932;East, 1935;Cooper and Brink, 1940); Div (Clarkson et al, 2017; Triticum nuclear strong HSI between T. boeoticum and T. urartu ~1MY divergd Both (Gill and Waines, 1978); Div (Huynh et al, 2019) Aegilops nuclear strong HSI between Ae. tauschii (Ae.…”

Hormonal Signaling during dPCD: Cytokinin as the Determinant of RNase-Based Self-Incompatibility in Solanaceae

“…The SI of tomatoes is of an S-RNase type which is characteristic of Solanaceae [10]. The study of SI in tomatoes has been ongoing for a long time [17] and is still in progress [18][19][20]. Tomatoes are a popular object in the studies of SI evolution and variation in the S locus [18,21,22].…”