Dataset Information

Tandem gene duplication and recombination at the AT3 locus in the Solanaceae, a gene essential for capsaicinoid biosynthesis in Capsicum.

ABSTRACT: Capsaicinoids are compounds synthesized exclusively in the genus Capsicum and are responsible for the burning sensation experienced when consuming hot pepper fruits. To date, only one gene, AT3, a member of the BAHD family of acyltransferases, is currently known to have a measurable quantitative effect on capsaicinoid biosynthesis. Multiple AT3 paralogs exist in the Capsicum genome, but their evolutionary relationships have not been characterized well. Recessive alleles at this locus result in absence of capsaicinoids in pepper fruit. To explore the evolution of AT3 in Capsicum and the Solanaceae, we sequenced this gene from diverse Capsicum genotypes and species, along with a number of representative solanaceous taxa. Our results revealed that the coding region of AT3 is highly conserved throughout the family. Further, we uncovered a tandem duplication that predates the diversification of the Solanaceae taxa sampled in this study. This pair of tandem duplications were designated AT3-1 and AT3-2. Sequence alignments showed that the AT3-2 locus, a pseudogene, retains regions of amino acid conservation relative to AT3-1. Gene tree estimation demonstrated that AT3-1 and AT3-2 form well supported, distinct clades. In C. rhomboideum, a non-pungent basal Capsicum species, we describe a recombination event between AT3-1 and AT3-2 that modified the putative active site of AT3-1, also resulting in a frame-shift mutation in the second exon. Our data suggest that duplication of the original AT3 representative, in combination with divergence and pseudogene degeneration, may account for the patterns of sequence divergence and punctuated amino acid conservation observed in this study. Further, an early rearrangement in C. rhomboidium could account for the absence of pungency in this Capsicum species.

SUBMITTER: Egan AN

PROVIDER: S-EPMC6343889 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Tandem gene duplication and recombination at the AT3 locus in the Solanaceae, a gene essential for capsaicinoid biosynthesis in Capsicum.

Egan Ashley N AN Moore Shanna S Stellari Giulia Marina GM Kang Byoung-Cheorl BC Jahn Molly M MM

PloS one 20190123 1

Capsaicinoids are compounds synthesized exclusively in the genus Capsicum and are responsible for the burning sensation experienced when consuming hot pepper fruits. To date, only one gene, AT3, a member of the BAHD family of acyltransferases, is currently known to have a measurable quantitative effect on capsaicinoid biosynthesis. Multiple AT3 paralogs exist in the Capsicum genome, but their evolutionary relationships have not been characterized well. Recessive alleles at this locus result in a ...[more]

PMID: 30673734

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Project description:BACKGROUND: The Potato type II (Pot II) family of proteinase inhibitors plays critical roles in the defense system of plants from Solanaceae family against pests. To better understand the evolution of this family, we investigated the correlation between sequence and structural repeats within this family and the evolution and molecular adaptation of Pot II genes through computational analysis, using the putative ancestral domain sequence as the basic repeat unit. RESULTS: Our analysis discovered the following interesting findings in Pot II family. (1) We classified the structural domains in Pot II family into three types (original repeat domain, circularly permuted domain, the two-chain domain) according to the existence of two linkers between the two domain components, which clearly show the circular permutation relationship between the original repeat domain and circularly permuted domain. (2) The permuted domains appear more stable than original repeat domain, from available structural information. Therefore, we proposed a multiple-repeat sequence is likely to adopt the permuted domain from contiguous sequence segments, with the N- and C-termini forming a single non-contiguous structural domain, linking the bracelet of tandem repeats. (3) The analysis of nonsynonymous/synonymous substitution rates ratio in Pot II domain revealed heterogeneous selective pressures among amino acid sites: the reactive site is under positive Darwinian selection (providing different specificity to target varieties of proteinases) while the cysteine scaffold is under purifying selection (essential for maintaining the fold). (4) For multi-repeat Pot II genes from Nicotiana genus, the proteolytic processing site is under positive Darwinian selection (which may improve the cleavage efficiency). CONCLUSION: This paper provides comprehensive analysis and characterization of Pot II family, and enlightens our understanding on the strategies (Gene and domain duplication, structural circular permutation and molecular adaptation) of Solanaceae plants for defending pathogenic attacks through the evolution of Pot II genes.

Project description:Background and aimsUnilateral incompatibility (UI) occurs when pollinations between species are successful in one direction but not in the other. Self-incompatible (SI) species frequently show UI with genetically related, self-compatible (SC) species, as pollen of SI species is compatible on the SC pistil, but not vice versa. Many examples of unilateral incompatibility, and all those which have been studied most intensively, are found in the Solanaceae, particularly Lycopersicon, Solanum, Nicotiana and Petunia. The genus Capsicum is evolutionarily somewhat distant from Lycopersicon and Solanum and even further removed from Nicotiana and Petunia. Unilateral incompatibility has also been reported in Capsicum; however, this is the first comprehensive study of crosses between all readily available species in the genus.MethodsAll readily available (wild and domesticated) species in the genus are used as plant material, including the three genera from the Capsicum pubescens complex plus eight other species. Pollinations were made on pot-grown plants in a glasshouse. The number of pistils pollinated per cross varied (from five to 40 pistils per plant), depending on the numbers of flowers available. Pistils were collected 24 h after pollination and fixed for 3-24 h. After staining, pistils were mounted in a drop of stain, squashed gently under a cover slip and examined microscopically under ultra-violet light for pollen tube growth.Key resultsUnilateral incompatibility is confirmed in the C. pubescens complex. Its direction conforms to that predominant in the Solanaceae and other families, i.e. pistils of self-incompatible species, or self-compatible taxa closely related to self-incompatible species, inhibit pollen tubes of self-compatible species.ConclusionsUnilateral incompatibility in Capsicum does not seem to have arisen to prevent introgression of self-compatibility into self-incompatible taxa, but as a by-product of divergence of the C. pubescens complex from the remainder of the genus.

Project description:Background and aimsCapsicum (Solanaceae), native to the tropical and temperate Americas, comprises the well-known sweet and hot chili peppers and several wild species. So far, only partial taxonomic and phylogenetic analyses have been done for the genus. Here, the phylogenetic relationships between nearly all taxa of Capsicum were explored to test the monophyly of the genus and to obtain a better knowledge of species relationships, diversification and expansion.MethodsThirty-four of approximately 35 Capsicum species were sampled. Maximum parsimony and Bayesian inference analyses were performed using two plastid markers (matK and psbA-trnH) and one single-copy nuclear gene (waxy). The evolutionary changes of nine key features were reconstructed following the parsimony ancestral states method. Ancestral areas were reconstructed through a Bayesian Markov chain Monte Carlo analysis.Key resultsCapsicum forms a monophyletic clade, with Lycianthes as a sister group, following both phylogenetic approaches. Eleven well-supported clades (four of them monotypic) can be recognized within Capsicum, although some interspecific relationships need further analysis. A few features are useful to characterize different clades (e.g. fruit anatomy, chromosome base number), whereas some others are highly homoplastic (e.g. seed colour). The origin of Capsicum is postulated in an area along the Andes of western to north-western South America. The expansion of the genus has followed a clockwise direction around the Amazon basin, towards central and south-eastern Brazil, then back to western South America, and finally northwards to Central America.ConclusionsNew insights are provided regarding interspecific relationships, character evolution, and geographical origin and expansion of Capsicum A clearly distinct early-diverging clade can be distinguished, centred in western-north-western South America. Subsequent rapid speciation has led to the origin of the remaining clades. The diversification of Capsicum has culminated in the origin of the main cultivated species in several regions of South to Central America.

Dataset Information

Tandem gene duplication and recombination at the AT3 locus in the Solanaceae, a gene essential for capsaicinoid biosynthesis in Capsicum.

Publications

Tandem gene duplication and recombination at the AT3 locus in the Solanaceae, a gene essential for capsaicinoid biosynthesis in Capsicum.

Similar Datasets

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