Systems analysis of long-term heat stress responses in the C4 grass Setaria viridis

Abstract

A substantial number of C4 plants are utilized as food and fodder crops and often display improved resource use efficiency compared to C3 counterparts. However, their response to future extreme climates such as heatwaves is less understood. Setaria viridis, an emerging C4 model grass closely related to important C4 crops, was grown under high temperature for two weeks (42{degrees}C as compared to 28{degrees}C). High temperature resulted in stunted growth, but surprisingly had little impact on leaf area based photosynthetic rates. Rates of dark respiration significantly increased and there were major alterations in carbon and nitrogen metabolism in the heat-stressed plants, including reduced starch levels, accumulation of soluble sugars and an increase in leaf nitrogen content. Measurements of major phytohormones revealed a dramatic increase in abscisic acid in the heat-stressed plants. Leaf transcriptomics, proteomics and metabolomics analyses were carried out and mapped onto metabolic pathways of photosynthesis, respiration, carbon/nitrogen metabolism and hormone synthesis and signaling. Overall, upregulation of a number of stress-signaling pathways was observed, consistent with multiple potent signals leading to reduced plant growth. A systems model of plant response is presented based on oxidative stress, hormone and sugar signaling pathways.