Evolution of two gene networks underlying adaptation to drought stress in the wild tomatoSolanum chilense

Abstract

Drought stress is a key factor limiting plant growth and the colonization of arid habitats by plants. Here, we study the evolution of gene expression response to drought stress in a wild tomato,Solanum chilensenaturally occurring around the Atacama Desert in South America. We conduct a transcriptome analysis of plants under standard and drought experimental conditions to understand the evolution of drought-response gene networks. We identify two main regulatory networks corresponding to two typical drought-responsive strategies: cell cycle and fundamental metabolic processes. We estimate the age of the genes in these networks and the age of the gene expression network, revealing that the metabolic network has a younger origin and more variable transcriptome than the cell-cycle network. Combining with analyses of population genetics, we found that a higher proportion of the metabolic network genes show signatures of recent positive selection underlying recent adaptation withinS. chilense, while the cell-cycle network appears of ancient origin and is more conserved. For both networks, however, we find that genes showing older age of selective sweeps are the more connected in the network. Adaptation to southern arid habitats over the last 50,000 years occurred inS. chilenseby adaptive changes core genes with substantial network rewiring and subsequently by smaller changes at peripheral genes.

Copy number variations shape genomic structural diversity underpinning ecological adaptation in the wild tomatoSolanum chilense

“…Eleven genes are also found to belong to the drought-responsive metabolism gene network previous studied (26), these genes showing significantly higher expression in drought than normal conditions (Fig. S8; t-test, P=2.68e-05) based on the data in (26). In addition, the number of DEL and DUP genes which are linked to response to water deprivation are similar across all populations (Fig.…”

“…S11B and S11C). These physiological processes (ABA signaling pathway, root hair differentiation) have been found to be important responses to drought stress using transcriptome and genome analysis (18,26). This confirms that drought tolerance is likely is the main driving environmental pressure driving CNV evolution across the different populations.…”

“…The populations currently occurring in the SC and SH habitats have been shown to exhibit signatures of past positive selection for adaptation to cold, drought, light (photoperiod), heat and biotic stresses (17,18,(22)(23)(24)(25). These events of recent positive selection at a cohesive set of genes and drought-responsive gene networks suggest the occurrence of genetic underpinnings to adaptation of novel habitats, during the southward expansion of S. chilense populations towards arid areas around the Atacama desert (26).…”

Patterns of presence-absence variation of NLRs across populations ofSolanum chilenseare clade-dependent and mainly shaped by past demographic history

“…It exhibits high local effective population sizes, due to the seed banks (Tellier et al, 2011) and mild bottlenecks of colonisation, and thus high genetic diversity at the SNP level. Selection occurring at genes for abiotic adaptation has been documented at SNP (Mboup et al, 2012;Böndel et al, 2015;Wei et al, 2023a) and PAV levels (Fischer et al, 2011;Wei et al, 2023b). We previously found a few NLRs under positive selection for local adaptation based on SNPs (Stam et al, 2019b), on a subset recovered through a PoolSeq method and a draft genome assembly of S. chilense (Stam et al, 2019a).…”

“…It exhibits high local effective population sizes, due to the seed banks 32 and mild bottleneck of colonisation, and thus high genetic diversity at the SNP level. Selection occurring at genes for abiotic adaptation has been documented at SNP 30,31,33 and PAV levels 34,35 . We previously found few NLRs under positive selection for local adaptation based on SNPs 8 .…”