Cis- and Trans-Regulatory Variations in the Domestication of the Chili Pepper Fruit

Abstract

The process of domestication requires the rapid transformation of the wild morphology into the cultivated forms that humans select for. This process often takes place through changes in the regulation of genes, yet, there is no definite pattern on the role of cis- and trans-acting regulatory variations in the domestication of the fruit among crops. Using allele-specific expression and network analyses, we characterized the regulatory patterns and the inheritance of gene expression in wild and cultivated accessions of chili pepper, a crop with remarkable fruit morphological variation. We propose that gene expression differences associated to the cultivated form are best explained by cis-regulatory hubs acting through trans-regulatory cascades. We show that in cultivated chili, the expression of genes associated with fruit morphology is partially recessive with respect to those in the wild relative, consistent with the hybrid fruit phenotype. Decreased expression of fruit maturation and growth genes in cultivated chili suggest that selection for loss-of-function took place in its domestication. Trans-regulatory changes underlie the majority of the genes showing regulatory divergence and had larger effect sizes on gene expression than cis-regulatory variants. Network analysis of selected cis-regulated genes, including ARP9 and MED25, indicated their interaction with many transcription factors involved in organ growth and fruit ripening. Differentially expressed genes linked to cis-regulatory variants and their interactions with downstream trans-acting genes have the potential to drive the morphological differences observed between wild and cultivated fruits and provide an attractive mechanism of morphological transformation during the domestication of the chili pepper.

Transcriptome Analyses Throughout Chili Pepper Fruit Development Reveal Novel Insights into the Domestication Process

“…This percentage can be considered to be high, given the dissimilarities of the above-mentioned factors (plots and results available upon request). On the other hand, Díaz-Valenzuela et al [ 41 ] reported results from the analyses of one cultivated accession, one wild accession, and their only at 40 DAA. Given that this study does not include gene expression measurements at different times of fruit development, it is impossible to examine their findings in the framework of our work.…”

“…In particular, the authors of [ 36 ] provided insights in order to evaluate the adaptive landscape of cultivated peppers [ 40 ] and reported a set of 511 genes that have a strong genomic domestication footprint. On the other hand, using allele-specific expression and network analyses from one domesticated and one wild chili pepper accession, as well as their cross, at 40 days after anthesis (DAA), the authors of [ 41 ] proposed that gene expression differences associated with the cultivated form could be explained by cis -regulatory hubs acting through trans -regulatory cascades.…”

Domestication of Crop Metabolomes: Desired and Unintended Consequences

“…In recent years transcriptomics has been used to study the effect of domestication on a wide range of species including the major cereals rice [47,48], maize [49,50], wheat (Triticum aestivum) [51], and barley [52], as well as cotton (Gossypium hirsutum) [53], tomato [54,55], eggplant (Solanum melongena) [56,57], peppers [58], sunflower (Helianthus annuus) [59], common bean (Phaseolus vulgaris) [60], curcubita [61], and a range of more other crops including chickpea (Cicer arietinum) [62], lupin (Lupinus albus) [63], pistachio (Pistacia vera) [64], spinach (Spinacia oleracea) [65], lettuce (Lactuca sativa) [66], and jujube (Ziziphus jujube) [67]. A common theme that emerges from these studies is that domestication is associated with a large reduction in allelic diversity, with estimates suggesting that our current crops contain on average only 6% of the allelic diversity present in wild species gene pools [68].…”

Genomic, Transcriptomic and Epigenomic Tools to Study the Domestication of Plants and Animals: A Field Guide for Beginners

“…Hybrid studies have been performed between maize and teosinte, suggesting potential selection on cis regulatory elements associated with changes in ear tissue and previously reported candidate genes (Lemmon et al, 2014). Another hybrid study in Capsicum annuum using network analyses revealed that loss of function in cis regulatory sequences lead to transcriptional changes in trans elements that are associated with fruit morphology (Díaz-Valenzuela et al, 2020).…”