Divergent geographic variation in above- versus belowground secondary metabolites of Reynoutria japonica

Abstract

Secondary metabolites play an important role in plant adaptation because they can mitigate biotic and abiotic environmental stresses. However, their production and allocation incur different costs and benefits and are therefore subject to trade-offs, which are less studied.

To understand large-scale geographic patterns of secondary metabolites, and their environmental drivers and trade-offs, we studied 39 natural populations of the perennial herb Japanese knotweed (Reynoutria japonica) along a large latitudinal gradient in China. We measured the concentrations of six polyphenols in leaves and rhizomes of R. japonica and associated the variation in these metabolites with biotic and abiotic environmental factors as well as with functional plant traits and putative costs of secondary metabolites.

We found that climate was an important driver of variation in secondary metabolites, both above- and belowground. Remarkably, the patterns of association differed between leaves and rhizomes, as well as between putative low-cost vs. high-cost compounds. While annual mean temperature was a stronger predictor of aboveground metabolites, annual precipitation was more frequently associated with variation in belowground metabolites. Moreover, annual temperature was positively associated with high-cost metabolites, but negatively with low-cost metabolites. Aboveground secondary metabolites were generally more strongly associated with functional traits (e.g., specific leaf area) than belowground metabolites, and in all cases, the directions of correlation were opposite for low-cost versus high-cost metabolites aboveground. The patterns of association also varied with latitude such that leaf concentrations of low-cost metabolites (quercetin) increased but those of high-cost metabolites (resveratrol, piceid and emodin) decreased at higher latitudes. In rhizomes, in contrast, the concentrations of high-cost metabolites (piceid and emodin) increased with latitude.

Synthesis. Our findings indicate that allocation strategies differ between above- and belowground tissues of R. japonica. As latitude increases, R. japonica invests relatively more into belowground metabolites. We propose that reduced high-cost metabolites in the leaves at higher latitudes may help to conserve nutrients after defoliation, while maintaining high-cost metabolites in rhizomes may be important for persistent allelopathic effects and resource conservation belowground. The divergent patterns of above- and belowground metabolite allocation thus likely reflect the multiple functions of metabolites and the plants’ adaptation to different environments.