Coordinated resource allocation to plant growth–defense tradeoffs

Abstract

Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G-D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed 'big data' resources including multiomic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi-omics biology to better understand how selection has shaped the mechanisms of G-D tradeoffs. Multi-omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G-D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G-D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply-and demand-side perspectives of previous G-D tradeoff theories.

Diversity and Divergence: Evolution of defense chemistry in the tropical tree genusInga

“…Our goal in laying out the above hypothesized mechanism for the generation of novel compounds and chemical profiles is to integrate the patterns we observed in our study of Inga metabolomes, with the growing body of literature on the underlying genetic and biochemical mechanisms for the evolution of plant secondary metabolism (20,50,72,73).…”

“…We look forward to this model being tested and updated by future studies using multiomics approaches (50).…”

“…Investment in structurally diverse defensive compounds is adaptive for protection against a broad suite of herbivores (8,11,12), yet investment in chemical defense comes at a cost (known as the 'growth-defense trade off') (48)(49)(50). We ask whether biosynthetic tradeoffs constrain a plant's ability to invest in structurally unrelated compounds (i.e., the cost of maintaining enzymes in multiple PSM pathways), or whether selection promotes investment in chemical diversity.…”

“…Comparative phylogenetic analyses of defense traits have revealed both trade-offs (negative correlations) (19,26,50,62,63) and positive correlations (63), providing evidence 12 for evolutionary integration and defense syndromes. For example, trade-offs between compound classes that share the same biosynthetic precursor are well supported in the literature (19,64,65).…”

Functional Traits 2.0: The power of the metabolome for ecology

“…However, although dynamic coupling between the plant metabolome and leaf traits has been found (Gargallo-Garriga et al, 2015;Monson et al, 2021;Rivas-Ubach et al, 2012), it does not follow that such plasticity in the metabolome is always evident in classical functional traits, for two reasons. First, while specialised metabolites are relatively rich in carbon or nitrogen (Züst & Agrawal, 2017), the number of carbon and nitrogen atoms allocated to such metabolites is several orders of magnitude lower than that allocated to morphological structures.…”