Structural variation underlies functional diversity at methyl salicylate loci in tomato.

Methyl salicylate is an important inter- and intra-plant signaling molecule, but is deemed undesirable by humans when it accumulates to high levels in ripe fruits. Balancing the tradeoff between consumer satisfaction and overall plant health is challenging as the mechanisms regulating volatile levels have not yet been fully elucidated. In this study, we investigated the accumulation of methyl salicylate in ripe fruits of tomatoes that belong to the red-fruited clade. We determine the genetic diversity and the interaction of four known loci controlling methyl salicylate levels in ripe fruits. In addition to Non-Smoky Glucosyl Transferase 1 (NSGT1), we uncovered extensive genome structural variation (SV) at the Methylesterase (MES) locus. This locus contains four tandemly duplicated Methylesterase genes and genome sequence investigations at the locus identified nine distinct haplotypes. Based on gene expression and results from biparental crosses, functional and non-functional haplotypes for MES were identified. The combination of the non-functional MES haplotype 2 and the non-functional NSGT1 haplotype IV or V in a GWAS panel showed high methyl salicylate levels in ripe fruits, particularly in accessions from Ecuador, demonstrating a strong interaction between these two loci and suggesting an ecological advantage. The genetic variation at the other two known loci, Salicylic Acid Methyl Transferase 1 (SAMT1) and tomato UDP Glycosyl Transferase 5 (SlUGT5), did not explain volatile variation in the red-fruited tomato germplasm, suggesting a minor role in methyl salicylate production in red-fruited tomato. Lastly, we found that most heirloom and modern tomato accessions carried a functional MES and a non-functional NSGT1 haplotype, ensuring acceptable levels of methyl salicylate in fruits. Yet, future selection of the functional NSGT1 allele could potentially improve flavor in the modern germplasm.

Genetic diversity, gene flow, and differentiation among wild, semiwild, and landrace chile pepper (Capsicum annuum) populations in Oaxaca, Mexico.

PREMISE: Capsicum annuum (Solanaceae) was originally domesticated in Mexico, where wild (C. annuum var. glabriusculum) and cultivated (C. annuum var. annuum) chile pepper populations (>60 landraces) are common, and wild-resembling individuals (hereafter semiwild) grow spontaneously in anthropogenic environments. Here we analyze the role of elevation and domestication gradients in shaping the genetic diversity in C. annuum from the state of Oaxaca, Mexico. METHODS: We collected samples of 341 individuals from 28 populations, corresponding to wild, semiwild (C. annuum var. glabriusculum) and cultivated C. annuum, and closely related species Capsicum frutescens and C. chinense. From the genetic variation of 10 simple sequence repeat (SSR) loci, we assessed the population genetic structure, inbreeding, and gene flow through variance distribution analyses, genetic clustering, and connectivity estimations. RESULTS: Genetic diversity (HE ) did not differ across domestication levels. However, inbreeding coefficients were higher in semiwild and cultivated chiles than in wild populations. We found evidence for gene flow between wild populations and cultivated landraces along the coast. Genetic structure analysis revealed strong differentiation between most highland and lowland landraces. CONCLUSIONS: Gene flow between wild and domesticated populations may be mediated by backyards and smallholder farms, while mating systems may facilitate gene flow between landraces and semiwild populations. Domestication and elevation may overlap in their influence on genetic differentiation. Lowland Gui'ña dani clustered with highland landraces perhaps due to the social history of the Zapotec peoples. In situ conservation may play an important role in preserving semiwild populations and private alleles found in landraces.

Genetic Structure of Liriomyza trifolii (Diptera: Agromyzidae) Associated With Host Plants From Southeastern Mexico.

Host-associated differentiation (HAD) has played a major role in insect diversification at both macroevolutionary and microevolutionary scales. This evolutionary process has been reported in insects associated with wild and domesticated plant species. In particular, domesticated species harbor large genetic and phenotypic diversity associated with traits of human interest, including variation in nutrition, phenology, fruit, and leaf shape. This diversity may alter selection regimes affecting insect evolution and host specialization. The genus Liriomyza includes highly polyphagous species that are characterized for living and feeding inside plant leaves. Ecological and genetic data suggest the presence of cryptic species within this genus. Moreover, there is evidence of HAD in a group of populations of Liriomyza trifolii (Burgess) associated with Capsicum annum L. (Solanaceae). In this work, we explored HAD in L. trifolii populations from southeastern Mexico, and inquire into differentiation specific to peppers based on cytochrome oxidase I. We also evaluated the relationship between the genetic structure of leafminers and the different types of C. annuum. Our main results did not support previous findings of specialization of L. trifolli on C. annuum. Nevertheless, we found a divergent group of haplotypes associated to Allium cepa (Aspargales: Amaryllidaceae) in sympatric condition to Physalis philadelphica Lam. (Solanales: Solanaceae) and C. annum, suggesting the presence of HAD, as well as significant genetic differentiation of L. trifolii associated to peppers from Oaxaca and Yucatán.

Genome-wide genotyping of a novel Mexican Chile Pepper collection illuminates the history of landrace differentiation after Capsicum annuum L. domestication.

Studies of genetic diversity among phenotypically distinct crop landraces improve our understanding of fruit evolution and genome structure under domestication. Chile peppers (Capsicum spp. L.) are economically valuable and culturally important species, and extensive phenotypic variation among landraces exists in southern Mexico, a center of C. annuum diversity. We collected 103 chile pepper seed accessions from 22 named landraces across 27 locations in southern Mexico. We genotyped these accessions with genotyping by sequencing (GBS), yielding 32,623 filtered single-nucleotide polymorphisms. Afterward, we genotyped 32 additional C. annuum accessions from a global collection for comparison to the Mexican collection. Within the Mexican collection, genetic assignment analyses showed clear genetic differentiation between landraces and clarified the unique nature of the Tusta landrace. Further clustering analyses indicated that the largest fresh-use Chile de Agua and dry-use Costeño landraces were part of separate clades, indicating that these two landraces likely represent distinct populations. The global accessions showed considerable admixture and limited clustering, which may be due to the collapse of use-type divisions outside of Central America. The separation of the Mexican landraces in part by fruit morphology related to use highlights the relevance of this use-type morphological diversity for plant breeders and the utility of fruit development variation for evolutionary biologists.

Interspecific reproductive barriers between sympatric populations of wild tomato species (Solanum section Lycopersicon).

PREMISE OF THE STUDY: Interspecific reproductive barriers (IRBs) often prevent hybridization between closely related species in sympatry. In the tomato clade (Solanum section Lycopersicon), interspecific interactions between natural sympatric populations have not been evaluated previously. In this study, we assessed IRBs between members of the tomato clade from nine sympatric sites in Peru. METHODS: Coflowering was assessed at sympatric sites in Peru. Using previously collected seeds from sympatric sites in Peru, we evaluated premating prezygotic (floral morphology), postmating prezygotic (pollen-tube growth), and postzygotic barriers (fruit and seed development) between sympatric species in common gardens. Pollen-tube growth and seed development were examined in reciprocal crosses between sympatric species. KEY RESULTS: We confirmed coflowering of sympatric species at five sites in Peru. We found three types of postmating prezygotic IRBs during pollen-pistil interactions: (1) unilateral pollen-tube rejection between pistils of self-incompatible species and pollen of self-compatible species; (2) potential conspecific pollen precedence in a cross between two self-incompatible species; and (3) failure of pollen tubes to target ovules. In addition, we found strong postzygotic IRBs that prevented normal seed development in 11 interspecific crosses, resulting in seed-like structures containing globular embryos and aborted endosperm and, in some cases, overgrown endothelium. Viable seed and F1 hybrid plants were recovered from three of 19 interspecific crosses. CONCLUSIONS: We have identified diverse prezygotic and postzygotic IRBs that would prevent hybridization between sympatric wild tomato species, but interspecific hybridization is possible in a few cases.