Fungal symbionts generate water-saver and water-spender plant drought strategies via diverse effects on host gene expression

Abstract

Foliar fungal endophytes are known to alter plant physiology, but the mechanisms by which they do so remain poorly understood. We focused on how plant gene expression was altered by six fungal strains that generated "water-saver" and "water-spender" drought physiologies in a C4 grass, Panicum hallii. Water-saver physiologies have lower plant water loss, improved wilt resistance, and higher survival compared to water-spender strategies. We expected fungi within each functional group would have similar effects on P. hallii, and this was largely true for plant physiology, but not for plant gene expression. When we focused only on genes that were differentially expressed relative to fungus-free controls, we found surprisingly little overlap in plant differentially expressed genes or gene regulatory pathways across the fungal treatments, including within and between the water-saver and water-spender strategies. Nevertheless, using lasso regression we identified a small subset of genes that predicted 39% and 53% of the variation in plant wilt resistance and water loss, respectively. These results suggest that fungal effects on plant transcription may identify how they extend the plant phenotype, and the comparison across multiple fungi allows us to differentiate broadly fungal-responsive plant genes vs. those plant genes that respond only to single fungal taxa. The genes identified here could be targeted for future study to understand their function and, ultimately, represent candidates for precision breeding efforts to increase plant drought tolerance.