Comparative transcriptomics and genomics patterns of discordance in Capsiceae (Solanaceae)

Authors: SPALINK, DANIEL - University Of Utah; STOFFEL, KEVIN - University Of California; HILL, THERESA - University Of California; Hulse-Kemp, Amanda; WALDEN, GENEVIEVE - University Of Utah; VAN DEYNZE, ALLEN - University Of California; BOHS, LYNN - University Of Utah

Submitted to: Systematic Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/20/2018
Publication Date: 4/25/2018
Citation: Spalink, D., Stoffel, K., Hill, T.A., Hulse-Kemp, A.M., Walden, G., Van Deynze, A., Bohs, L. 2018. Comparative transcriptomics and genomics patterns of discordance in Capsiceae (Solanaceae). Systematic Biology. 126(2018):293-302. https://doi: 10.1016/j.ympev.2018.04.030.
DOI: https://doi.org/10.1016/j.ympev.2018.04.030

Interpretive Summary: Understanding the relationships between our crops and their close relatives is important to know how different desirable traits have evolved through time, particularly for breeding, and the diversity of genes that confer these traits. Pepper is a crop of world-wide importance used for food as well as medicine. The genus Lycianthes is a very closely related to the pepper genus, Capsicum. The actual relationship between Lycianthes and Capsicum is not well known, and clarifying their relationship will help us to breed more nutritious, disease resistant, sustainable peppers. To determine the relationship of these two genera, we investigated the sequences for the genes in seven different species. Using these sequence data for computational analysis, we could see that the different genes provided evidence for multiple different relationships, but most of the evidence supported a relationship where Capsicum and Lycianthes may actually form a single genus, as opposed to the two distinct genera as they are currently classified. These findings go against prior assumptions, so this will call for additional studies with large numbers of individuals to ensure these findings are correct. We also found that the physical location of the genes on chromosomes used as evidence can affect the estimated relationships among species, so this study provides a warning for scientists performing these additional studies. We were able to find 787 genes that have a signature showing that they’ve been important for our current peppers in the market, so these can be used in targeted future studies to look how these genes function to make a great pepper for consumers.

Technical Abstract: The genus Capsicum L. (peppers; Solanaceae) forms the foundation of a multibillion-dollar industry, has transformed global culinary cultures for hundreds of years, and serves as a model system for ecological, genomic, and developmental evolution [1-10]. Reflecting its global importance, abundant genetic resources, including both transcriptome and genome sequences, are available for multiple species in the genus [2,4,7,11-15]. Capsicum is one of only 13 genera of land plants for which full genomes have been assembled and annotated for more than one species, and Solanaceae ranks 4th among land plant families for the total number of individual genomes assembled. Given this abundance of genomic resources and the cultural, scientific, and economic importance of Capsicum, it is perhaps surprising that very little is known about the evolutionary diversification of Capsicum beyond the few species that have been cultivated, or within the broader context of Solanaceae. Indeed, the relationship between Capsicum and its closest relative, Lycianthes Hassl. (Dunal), remains unresolved, with phylogenetic evidence suggesting that Capsicum may be imbedded within Lycianthes [16]. Thus, even the taxonomic validity of Capsicum and its relatives is problematic. Resolving these relationships has far-reaching implications for understanding the diversification of the clade and the evolution and ecology of pungency, and could provide resources for improving crop diversity and agricultural sustainability [10,15,17]. Capsicum and Lycianthes together comprise the tribe Capsiceae, but the two genera have remained taxonomically separated because of their geographical, ecological, and morphological distinctiveness. With ca. 35 species of annual and perennial herbs and shrubs, Capsicum is native only to Central and South America. The capsaicinoids that result in fruit pungency are expressed to varying degrees in all but 7 species, though only five species have been domesticated [18]. Pungency appears to be genetically correlated to stomatal density [8]; thus, while the anti-fungal properties of pungency [5,19] are thought to confer an advantage in high moisture conditions, the high stomatal density of pungent individuals are conversely disadvantageous in water-stressed conditions [8], a trade-off with important implications in cultivation. In comparison, pungency is lacking altogether in Lycianthes. With ca. 250 species, Lycianthes is one of the largest genera in Solanaceae and is native to Central and South America, Asia, and the South Pacific. All species are perennial, and exhibit a diversity of habits including small trees, vines, shrubs, herbs, and epiphytes. Lycianthes species remain undomesticated, though some produce edible berries and others are grown as ornamental shrubs [20]. Capsicum flowers have stamens that dehisce along longitudinal slits, and offer an energy-intensive nectar reward to primarily bee pollinators [21-25]. Lycianthes stamens, on the other hand, dehisce by terminal pores and are buzz-pollinated exclusively by bees, which receive pollen as their only reward [26]. Many Lycianthes species are nocturnal or crepuscular bloomers, which may offer a competitive advantage by allowing access to a wider diversity of pollinators [27]. Attempts to resolve the Capsiceae phylogeny have relied exclusively on a few plastid and nuclear ribosomal genes, or at most, these in combination with a single low-copy nuclear gene [16,18,28]. Support for the paraphyly of Lycianthes with respect to Capsicum is weak in these published studies, suggesting that additional data are necessary to more fully understand the evolutionary processes involved in the diversification of this clade. Several such processes could be involved. For example, rapid diversification along the backbone of the phylogeny could simply require more informative characters to provide be