From ancient genes to modern communities: the cellular stress response and the evolution of plant strategies

1. Two major plant strategy theories attempt to explain how phenotype determines community structure. Crucially, CSR plant strategy theory suggests that stress and sporadic resource availability favour conservative phenotypes, whereas the resource-ratio hypothesis views the spatial heterogeneity of resources as selecting for optimal foraging in chronically unproductive habitats. Which view is most realistic? 2. The ecophysiology literature demonstrates that stress is comprised of two processes: (1) limitation of resource supply to metabolism; and (2) damage to biomembranes, proteins and genetic material (chronic stress). Thus stress is defined mechanistically as the suboptimal performance of metabolism. 3. Adaptations to limitation buffer metabolism against variability in external resource supply; internal storage pools are more consistent. Chronic stress elicits the same ancient cellular stress response in all cellular life: investment in stress metabolites that preserve the integrity and compartmentalization of metabolic components in concert with molecular damage-repair mechanisms. 4. The cellular stress response was augmented by morphological innovations during the Silurian-Devonian terrestrial radiation, during which nutrient limitation appears to have been a principal selection pressure (sensu CSR theory). 5. The modern stress-tolerator syndrome is conservative and supports metabolism in limiting or fluctuating environmental conditions: standing resource pools with high investment/maintenance costs impose high internal diffusion resistances and limit inherent growth rate (sensu CSR theory). 6. The resource-ratio hypothesis cannot account for the cellular stress response or the crucial role of ombrotrophy in primary succession. CSR theory agrees with current understanding of the cellular stress response, terrestrial radiation and modern adaptations recorded in chronically unproductive habitats, and is applicable as CSR classification.