Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato

Abstract

As global climate change brings elevated average temperatures and more frequent and extreme weather events, pressure from biotic stresses will become increasingly compounded by harsh abiotic stress conditions. The plant hormone jasmonate (JA) promotes resilience to many environmental stresses, including attack by arthropod herbivores whose feeding activity is often stimulated by rising temperatures. How wound-induced JA signaling affects plant adaptive responses to elevated temperature (ET), however, remains largely unknown. In this study, we used the commercially important crop plant Solanum lycopersicum (cultivated tomato) to investigate the interaction between simulated heat waves and wound-inducible JA responses. We provide evidence that the heat shock protein HSP90 enhances wound responses at ET by increasing the accumulation of the JA receptor, COI1. Wound-induced JA responses directly interfered with short-term adaptation to ET by blocking leaf hyponasty and evaporative cooling. Specifically, leaf damage inflicted by insect herbivory or mechanical wounding at ET resulted in COI1-dependent stomatal closure, leading to increased leaf temperature, lower photosynthetic carbon assimilation rate, and growth inhibition. Pharmacological inhibition of HSP90 reversed these effects to recapitulate the phenotype of a JA-insensitive mutant lacking the COI1 receptor. As climate change is predicted to compound biotic stress with larger and more voracious arthropod pest populations, our results suggest that antagonistic responses resulting from a combination of insect herbivory and moderate heat stress may exacerbate crop losses.

Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway

“…Although we did not observe significant effects of ET on the capacity of Arabidopsis (a winter annual) to deploy JA-mediated defenses, it is possible that plants in warmer native environments have experienced selective pressure from temperature-stimulated insect outbreaks and therefore, possess temperature-sensitive mechanisms to enhance resistance to insect herbivores. This hypothesis is consistent with the variable effects of rising temperature on different insect herbivoreplant pairs [31], as well as the recent finding that temperature-dependent accumulation of HSP90 enhances JA-dependent wound responses by a mechanism likely involving COI1 stabilization [37]. Although ET conditions greatly stimulated the feeding activity of T. ni larvae, additional studies are Figure 6.…”

“…In showing that elevated temperature can supersede the protective effects of JA, our findings highlight the importance of temperature as a dominant factor in determining the outcome of the T. ni-Arabidopsis interaction. Similar results were reported in a recent study that examined the effects of elevated temperature on the interaction between Manduca sexta (tobacco hornworm) and a JA perception mutant of cultivated tomato [37]. These collective findings suggest that projected increases in average global temperature [38] have the potential to disrupt plant-herbivore relationships that have co-evolved over the millennia and to tip the balance of these adversarial relationships toward the side of increased herbivory and greater plant damage.…”

Insect chemical ecology: chemically mediated interactions and novel applications in agriculture

“…Similarly, in several plant species, an increase in temperature triggers the release of higher amounts of volatiles, for instance, terpenoids and phenolics (Kleist et al 2012 ; Holopainen et al 2018 ). On the other hand, an increase in temperatures can accelerate insect metabolism and hence promote more feeding and herbivory (Havko et al 2019 ). Based on the above examples on the impact of temperature on the plant’s chemistry and insect metabolism, it can be expected that more voracious arthropods pest populations will emerge (Havko et al 2019 ).…”

“…On the other hand, an increase in temperatures can accelerate insect metabolism and hence promote more feeding and herbivory (Havko et al 2019 ). Based on the above examples on the impact of temperature on the plant’s chemistry and insect metabolism, it can be expected that more voracious arthropods pest populations will emerge (Havko et al 2019 ). However, more studies are needed to provide details on how variations in temperature affect insect population dynamics and levels of plant damage or herbivory.…”

The Heat is On: How Crops Respond to High Temperature

“…maize, rice, tomato and soybean) generally have a higher optimum temperature from emergence to the vegetative growth and development than those crops from temperate zones (e.g. wheat and barley), which are in the range of 25-32°C and 15-25°C, respectively (Ali Tahir, Nakata, Yamaguchi, Nakano, & Mukhtar Ali, 2015;Alsajri et al, 2019;Cannell, 1969;Chavan, Duursma, Tausz, & Ghannoum, 2019;Ford et al, 2016;Friend, 1965;Garmash, 2005;Hakim, Hossain, Teixeira da Silva, Zvolinsky, & Khan, 2012;Havko et al, 2020;Hemming, Walford, Fieg, Dennis, & Trevaskis, 2012;Jumrani & Bhatia, 2018;Krishnan, Ramakrishnan, Reddy, & Reddy, 2011;Liu et al, 2020;T. Lu et al, 2017;Lyu et al, 2020;Singh, Reddy, Reddy, & Gao, 2014;Tsai, Weng, Chen, Lin, & Tsai, 2019;Yoshida, 1973) ( Figure 2B and Table 1 ).…”