Changes in leaf economic trait relationships across a precipitation gradient are related to differential gene expression in a C4 perennial grass

Authors: HECKMAN, ROBERT - Forest Service (FS); ASPINWALL, M. - Formation Environmental Llc; TAYLOR, SAMUEL - Lancaster University; LOWRY, DAVID - Michigan State University; KHASANOVA, ALBINA - University Of Texas At Austin; BONNETTE, JASON - University Of Texas At Austin; RAZZAQUE, SAMSAD - Salk Institute Of Biological Studies; Fay, Philip; JUENGER, THOMAS - University Of Texas At Austin

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/23/2025
Publication Date: 3/28/2025
Citation: Heckman, R.A., Aspinwall, M.J., Taylor, S.H., Lowry, D.B., Khasanova, A., Bonnette, J.E., Razzaque, S., Fay, P.A., Juenger, T.E. 2025. Changes in leaf economic trait relationships across a precipitation gradient are related to differential gene expression in a C4 perennial grass. New Phytologist. https://doi.org/10.1111/nph.70089.
DOI: https://doi.org/10.1111/nph.70089

Interpretive Summary: The leaf economics spectrum results from a trade-off between resource acquisition and conservation. Yet, despite strong evidence for the presence of the leaf economics spectrum at broad geographic and taxonomic scales, few studies have examined the major drivers of the leaf economics spectrum within species—phenotypic plasticity and standing genetic variation. In the candidate bioenergy species, switchgrass, we show that both phenotypic plasticity—changes in leaf economics traits in response to the environment—and standing genetic variation—differences in the genetic basis of leaf economics traits among plants—contribute to leaf economics strategies. Moreover, leaf economics strategies were more consistently expressed when plants received ample water than when they were subjected to drought: selection favored particular trait combinations (e.g., low nitrogen content and high leaf structural costs) in wetter environments; in drier environments, selection favored only individual traits (e.g., higher photosynthetic rates) rather than trait combinations. This suggests that some aspects of leaf economics strategies are more drought-sensitive than others, leading to a break-down of the leaf economics spectrum in more stressful environments. Understanding how switchgrass varieties with different leaf economics trait combinations perform in various environments may improve our ability to breed more productive biofuel crops.

Technical Abstract: The leaf economics spectrum (LES) describes a suite of functional traits that consistently covary at large spatial and taxonomic scales. Despite its importance at these larger scales, few studies have examined the major drivers of intraspecific variation in the LES—phenotypic plasticity and standing genetic variation. Using experimental precipitation manipulations, we examined whether correlations among leaf economics traits change as diverse genotypes of the widespread perennial C4 grass Panicum virgatum become increasingly water-limited and whether these relationships can be explained by changes in gene expression. We found that water limitation had important impacts on leaf economics trait covariation—covariation between individual traits and selection on leaf economics trait covariation tended to be strongest at high precipitation and break down at low precipitation when water was most limiting. Gene expression was also most strongly related to traits and pairs of traits at higher precipitation. Better understanding how within-species leaf economics strategies change with precipitation can improve our knowledge of LES evolution across broader scales.