Heat stress resistance drives coordination of emissions of suites of volatiles after severe heat stress and during recovery in five tropical crops

Abstract

Severe heat stress leads to a major reduction in foliage photosynthetic characteristics and the initial reduction and degree of recovery depend on species heat resistance. However, how the emissions of biogenic volatile organic compounds (BVOC) from different biochemical pathways are coordinated with photosynthetic modifications from the initial stress response through recovery are poorly understood, and the data are especially limited for short-living tropical crop species. We exposed leaves of five tropical crop species (A. cruentus, A. hybridus, S. aethiopicum, T. occidentalis and V. unguiculata) to severe heat treatment of 49 °C and a control treatment of 25 °C for 5 min and studied the modifications in foliage photosynthetic characteristics and constitutive BVOC emissions and elicitation of stress-induced volatiles through a 48 h recovery period upon return to non-stressed conditions. Overall, heat shock application resulted in a major inhibition of net assimilation rate similarly in all species indicating cellular damage and photosynthetic decay. However, species strongly varied in photosynthetic recovery with A. hybridus recovering the most and S. aethiopicum the least. Heat shock stress led to enhancement of emissions characterizing increased leaf oxidative status, in particular to enhanced emissions of lipoxygenase pathway volatiles (LOX). Surprisingly, LOX emissions were not associated with species heat resistance, but were greater in physiologically more active species with greater photosynthetic capacity. Species with greater constitutive isoprenoid emission capacity were generally more heat resistant, but terpenoid emissions were induced to a greater degree in less heat resistant species that likely suffered the most from the applied level of stress. Heat stress affected different groups of terpenoids - isoprene, monoterpenes and sesquiterpenes - to a different degree in different species, resulting in unique species-specific emission blends at different times of recovery. Heat stress had relatively minor effects on benzenoid emissions with moderately enhanced emissions primarily in V. unguiculata that differed from the other species by lower constitutive terpenoid emissions correspondent to its relatively high heat resistance. The results collectively demonstrate that species heat resistance is associated with the quantitative and qualitative characteristics of heat stress-dependent volatile emissions in different tropical crop species. We argue that these species-specific patterns need consideration in simulating volatile emissions under heat stress.