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

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 chilense naturally 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 within S. 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 in S. chilense by adaptive changes core genes with substantial network rewiring and subsequently by smaller changes at peripheral genes.