An eco-evo-devo genetic network model of stress response

The capacity of plants to resist abiotic stresses is of great importance to agricultural, ecological and environmental sustainability, but little is known about its genetic underpinnings. Existing genetic tools can identify individual genetic variants mediating biochemical, physiological, and cellular defenses, but fail to chart an overall genetic atlas behind stress resistance. We view stress response as an eco-evo-devo process by which plants adaptively respond to stress through complex interactions of developmental canalization, phenotypic plasticity, and phenotypic integration. As such, we define and quantify stress response as the developmental change of adaptive traits from stress-free to stress-exposed environments. We integrate composite functional mapping and evolutionary game theory to reconstruct omnigenic, information-flow interaction networks for stress response. Using desert-adapted Euphrates poplar as an example, we infer salt resistance-related genome-wide interactome networks and trace the roadmap of how each SNP acts and interacts with any other possible SNPs to mediate salt resistance. We characterize the previously unknown regulatory mechanisms driving trait variation; i.e. the significance of a SNP may be due to the promotion of positive regulators, whereas the insignificance of a SNP may result from the inhibition of negative regulators. The regulator-regulatee interactions detected are not only experimentally validated by two complementary experiments, but also biologically interpreted by their encoded protein-protein interactions. Our eco-evo-devo model of genetic interactome networks provides an approach to interrogate the genetic architecture of stress response and informs precise gene editing for improving plants' capacity to live in stress environments.

Automated summary

The genetic basis of plants' ability to resist abiotic stresses is not well understood. Current genetic tools can identify individual genetic variants involved in defense mechanisms, but lack a comprehensive understanding of the overall genetic atlas behind stress resistance. This study takes a holistic eco-evo-devo approach to stress response, integrating functional mapping and evolutionary game theory to reconstruct genetic interaction networks. Using the example of salt resistance in desert-adapted Euphrates poplar, the researchers infer genome-wide interactome networks and trace the regulatory mechanisms and interactions involved in mediating stress resistance. The study provides insights into the genetic architecture of stress response and informs gene editing strategies for improving plants' ability to thrive in stressful environments.