Gene family evolution and natural selection signatures in Datura spp. (Solanaceae)

Abstract

Elucidating the diversification process of congeneric species makes it necessary to identify the factors promoting species variation and diversification. Comparative gene family analysis allows us to elucidate the evolutionary history of species by identifying common genetic/genomic mechanisms underlying species responses to biotic and abiotic environments at the genomic level. In this study, we analyzed the high-quality transcriptomes of four Datura species, D. inoxia, D. pruinosa, D. stramonium, and D. wrightii. We performed a thorough comparative gene family analysis to infer the role of selection in molecular variation, changes in protein physicochemical properties, and gain/loss of genes during their diversification processes. The results revealed common and species-specific signals of positive selection, physicochemical divergence and/or expansion of metabolic genes (e.g., transferases and oxidoreductases) associated with terpene and tropane metabolism and some resistance genes (R genes). The gene family analysis presented here is a valuable tool for understanding the genome evolution of economically and ecologically significant taxa such as the Solanaceae family.

The chromosome-scale genome and the genetic resistance machinery against insect herbivores of the Mexican toloache,Datura stramonium

“…We obtained RNA sequences of D. stramonium from BioProject DDBJ/ENA/GenBank PRJNA669339. These sequences originated from an experiment involving D. stramonium plants exposed to the main folivore, L. daturaphila larvae (Coleoptera: Chrysomelidae) (E. Kariñho-Betancourt, N. Calderón Cortés, R. Tapia López, I. De-la-Cruz, J. Núñez-Farfán, K. Oyama, in preparation; De-la-Cruz et al 2022 ). In this experiment, seeds from 6 plants of the Ticumán population—where the highly resistant parent was selected—were germinated.…”

“…In this experiment, seeds from 6 plants of the Ticumán population—where the highly resistant parent was selected—were germinated. The seedlings were grown under controlled environmental conditions (16:8 light:dark and 25:20°C light:dark cycle) in the greenhouse of the Institute of Ecology, Universidad Nacional Autónoma de México (E. Kariñho-Betancourt, N. Calderón Cortés, R. Tapia López, I. De-la-Cruz, J. Núñez-Farfán, K. Oyama, in preparation; De-la-Cruz et al 2022 ). Each seedling was planted in a 150 mL pot filled with sterilized soil and watered as needed.…”

“…Each seedling was planted in a 150 mL pot filled with sterilized soil and watered as needed. Of these, 3 plants were designated for the damage treatment, exposed to feeding by L. daturaphila larvae, and 3 were maintained intact, representing the control treatment (E. Kariñho-Betancourt, N. Calderón Cortés, R. Tapia López, I. De-la-Cruz, J. Núñez-Farfán, K. Oyama, in preparation; De-la-Cruz et al 2022 ). For the damage treatment, 2 larvae in the second to 4th instar were randomly assigned to the adaxial side of 10 fully expanded leaves.…”

“…Simultaneously, 10 leaves from each control plant were also harvested. These leaves were immediately flash-frozen and stored at −80°C for subsequent RNA extraction and sequencing (E. Kariñho-Betancourt, N. Calderón Cortés, R. Tapia López, I. De-la-Cruz, J. Núñez-Farfán, K. Oyama, in preparation; De-la-Cruz et al 2022 ).…”

“…While tropane alkaloids are found across multiple Solanaceae species ( Huang et al 2021 ), limited research has investigated their ecological function as potential chemical defenses against pathogens and herbivores, with notable exceptions in the case of D. stramonium ( Shonle and Bergelson 2000 ; Castillo et al 2013 , 2014 ; Miranda-Peréz et al 2016 ; De-la-Cruz, Cruz, et al 2020 ; De-la-Cruz, Merilä, et al 2020 ). Prior ecological genetics studies focusing on defense mechanisms of D. stramonium against herbivores highlighted the genomic analysis of candidate genes ( De-la-Cruz et al 2021 , 2022 ). Our findings also revealed that resistance in D. stramonium is both inheritable and subject to positive selection ( De-la-Cruz, Merilä, et al 2020 ).…”