Evolutionary history of two pollen self-incompatibility factors reveals alternate routes to self-compatibility within Solanum.

PREMISE OF THE STUDY: Self-incompatibility (SI) prevents self-fertilization and reduces inbreeding. While SI is common in plants, transitions to self-compatibility (SC) occur frequently. Little is known about the genetic changes and evolutionary steps underlying these shifts. METHODS: In the Solanaceae, SI is gametophytic, with specificity determined by S-RNases in the pistil and S-locus F-box proteins (SLFs) in pollen. We examined the role of two pollen factors, Cullin1 (CUL1) and SLF-23, in SI → SC transitions in wild tomato species from the Arcanum species group (Solanum arcanum, S. neorickii, and S. chmielewskii). Pollen compatibility was assessed on tester lines that reject pollen lacking functional SLF-23 or CUL1. Complementation tests, gene sequencing, and phylogenetic analyses were used to characterize both functional and nonfunctional alleles. KEY RESULTS: We found evidence for multiple independent SI → SC transitions. In S. arcanum and S. chmielewskii, SC is caused by loss of pistil S-RNase activity, while in S. neorickii SC is associated with expression of a functional SLF-23 that recognizes the S9 type S-RNase expressed in its pistils. Interestingly, we found identical deletion mutations in CUL1 exon 7 of S. chmielewskii as previously seen in S. habrochaites. CONCLUSIONS: Mating system transitions in the Arcanum group have occurred via both pistil loss-of-function and pollen gain-of-function SC mutations. Mutations common to S. chmielewskii and S. habrochaites must have arisen in a common ancestor, possibly to the entire tomato clade, then became fixed in different lineages after loss of pistil-side SI function.

Mutations in two pollen self-incompatibility factors in geographically marginal populations of Solanum habrochaites impact mating system transitions and reproductive isolation.

PREMISE OF THE STUDY: Self-incompatibility (SI) is a mechanism that prevents inbreeding in many plant species. The mutational breakdown of SI occurs frequently, yet relatively little is known about the evolutionary steps involved in the progressive loss of pistil and pollen SI function. METHODS: In Solanaceae, SI is the S-RNase-based gametophytic type. We used SI and SC populations of the wild tomato species Solanum habrochaites to study natural variation for two pollen SI factors: a Cullin1 (CUL1) protein and an S-locus F-box protein (SLF-23). Pollen compatibility was assessed on an allotriploid tester line encoding an S-RNase recognized by SLF-23. Both pollen factors are required for compatibility on this tester line. Complementation tests and gene sequencing were used to identify mutations in CUL1 or SLF-23. KEY RESULTS: We detected loss-of-function mutations in CUL1 and/or SLF-23 in SC populations collected near the northern and southern geographic margins of this taxon's natural range. Nonmarginal SC and all SI accessions expressed mostly functional alleles of these pollen factors. Comparison of the CUL1 sequences identified several shared deletion mutations present in both northern and southern margin SC accessions. CONCLUSIONS: Loss-of-function mutations in CUL1 and SLF-23 likely became fixed relatively late during SI to SC transitions, after loss of pistil SI function. Mutations in CUL1 establish unilateral incompatibility with SI populations and strengthen reproductive isolation. Point mutations common to northern and southern SC biotypes likely derive from shared ancestral variants found in more central SI populations.

Testing the SI × SC rule: Pollen-pistil interactions in interspecific crosses between members of the tomato clade (Solanum section Lycopersicon, Solanaceae).

PREMISE OF THE STUDY: Interspecific reproductive barriers (IRBs) act to ensure species integrity by preventing hybridization. Previous studies on interspecific crosses in the tomato clade have focused on the success of fruit and seed set. The SI × SC rule (SI species × SC species crosses are incompatible, but the reciprocal crosses are compatible) often applies to interspecific crosses. Because SI systems in the Solanaceae affect pollen tube growth, we focused on this process in a comprehensive study of interspecific crosses in the tomato clade to test whether the SI × SC rule was always followed. METHODS: Pollen tube growth was assessed in reciprocal crosses between all 13 species of the tomato clade using fluorescence microscopy. KEY RESULTS: In crosses between SC and SI species, pollen tube growth follows the SI × SC rule: interspecific pollen tube rejection occurs when SI species are pollinated by SC species, but in the reciprocal crosses (SC × SI), pollen tubes reach ovaries. However, pollen tube rejection occurred in some crosses between pairs of SC species, demonstrating that a fully functional SI system is not necessary for pollen tube rejection in interspecific crosses. Further, gradations in the strength of both pistil and pollen IRBs were revealed in interspecific crosses using SC populations of generally SI species. CONCLUSION: The SI × SC rule explains many of the compatibility relations in the tomato clade, but exceptions occur with more recently evolved SC species and accessions, revealing differences in strength of both pistil and pollen IRBs.

Ten polymorphic microsatellite primers in the tropical tree caimito, Chrysophyllum cainito (Sapotaceae).

PREMISE OF THE STUDY: We developed microsatellite primers for the tropical tree Chrysophyllum cainito (Sapotaceae) to determine the native range of the species, investigate the origin of cultivated populations, and examine the partitioning of genetic diversity in wild and cultivated populations. • METHODS AND RESULTS: We developed 10 polymorphic primers from C. cainito genomic DNA libraries enriched for di-, tri-, and tetranucleotide repeat motifs. The loci amplified were polymorphic in samples collected from Jamaica and Panama. The number of alleles per locus ranged from two to 10 and three to 12, while observed heterozygosities ranged from 0.074 to 0.704 and 0.407 to 0.852 in Jamaica and Panama, respectively. • CONCLUSIONS: The microsatellite primers will be useful in future population genetic studies as well as those aimed at understanding the geographic origin(s) of wild and cultivated populations.

Domestication of the neotropical tree Chrysophyllum cainito from a geographically limited yet genetically diverse gene pool in Panama.

Species in the early stages of domestication, in which wild and cultivated forms co-occur, provide important opportunities to develop and test hypotheses about the origins of crop species. Chrysophyllum cainito (Sapotaceae), the star apple or caimito, is a semidomesticated tree widely cultivated for its edible fruits; it is known to be native to the neotropics, but its precise geographic origins have not been firmly established. Here, we report results of microsatellite marker analyses supporting the hypothesis that the center of domestication for caimito was the Isthmus of Panama, a region in which few crop species are believed to have originated, despite its importance as a crossroads for the dispersal of domesticated plants between North and South America. Our data suggest that caimito was domesticated in a geographically restricted area while incorporating a diverse gene pool. These results refute the generally accepted Antillean origin of caimito, as well as alternative hypotheses that the species was domesticated independently in the two areas or over a broad geographic range including both. Human-mediated dispersal from Panama to the north and east was accompanied by strong reductions in both genotypic and phenotypic diversity. Within Panama, cultivated and wild trees show little neutral genetic divergence, in contrast to striking phenotypic differentiation in fruit and seed traits. In addition to providing a rare example of data that support the hypothesis of a narrow geographic origin on the Isthmus of Panama for a now widespread cultivated plant species, this study is one of the first investigations of the origins of an edible species of the large pantropical family Sapotaceae.

Origins and close relatives of a semi-domesticated neotropical fruit tree: Chrysophyllum cainito (Sapotaceae).

PREMISE OF THE STUDY: Understanding patterns and processes associated with domestication has implications for crop development and agricultural biodiversity conservation. Semi-domesticated crops provide excellent opportunities to examine the interplay of natural and anthropogenic influences on plant evolution. The domestication process has not been thoroughly examined in many tropical perennial crop species. Chrysophyllum cainito (Sapotaceae), the star apple or caimito, is a semi-domesticated species widely cultivated for its edible fruits. It is known to be native to the neotropics, but the precise geographic origins of wild and cultivated forms are unresolved. METHODS: We used nuclear ribosomal ITS sequences to infer phylogenetic relationships among C. cainito and close relatives (section Chrysophyllum). We employed phylogeographic approaches using ITS and plastid sequence data to determine geographic origins and center(s) of domestication of caimito. KEY RESULTS: ITS data suggest a close relationship between C. cainito and C. argenteum. Plastid haplotype networks reveal several haplotypes unique to individual taxa but fail to resolve distinct lineages for either C. cainito or C. argenteum. Caimito populations from northern Mesoamerica and the Antilles exhibit a subset of the genetic diversity found in southern Mesoamerica. In Panama, cultivated caimito retains high levels of the diversity seen in wild populations. CONCLUSIONS: Chrysophyllum cainito is most closely related to a clade containing Central and South American C. argenteum, including subsp. panamense. We hypothesize that caimito is native to southern Mesoamerica and was domesticated from multiple wild populations in Panama. Subsequent migration into northern Mesoamerica and the Antilles was mediated by human cultivation.

Domestication Syndrome in Caimito (Chrysophyllum cainito L.): Fruit and Seed Characteristics.

Domestication Syndrome in Caimito (Chrysophyllum cainitoL.): Fruit and Seed Characteristics: The process of domestication is understudied and poorly known for many tropical fruit tree crops. The star apple or caimito tree (Chrysophyllum cainito L., Sapotaceae) is cultivated throughout the New World tropics for its edible fruits. We studied this species in central Panama, where it grows wild in tropical moist forests and is also commonly cultivated in backyard gardens. Using fruits collected over two harvest seasons, we tested the hypothesis that cultivated individuals of C. cainito show distinctive fruit and seed characteristics associated with domestication relative to wild types. We found that cultivated fruits were significantly and substantially larger and allocated more to pulp and less to exocarp than wild fruits. The pulp of cultivated fruits was less acidic; also, the pulp had lower concentrations of phenolics and higher concentrations of sugar. The seeds were larger and more numerous and were less defended with phenolics in cultivated than in wild fruits. Discriminant Analysis showed that, among the many significant differences, fruit size and sugar concentration drove the great majority of the variance distinguishing wild from cultivated classes. Variance of pulp phenolics among individuals was significantly higher among wild trees than among cultivated trees, while variance of fruit mass and seed number was significantly higher among cultivated trees. Most traits showed strong correlations between years. Overall, we found a clear signature of a domestication syndrome in the fruits of cultivated caimito in Panama.