Constitutive and herbivore‐induced plant defences regulate herbivore population processes

Abstract

Herbivore‐induced plant defences regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) are predicted to influence herbivore population dynamics, in part because they can operate in a density‐dependent manner. While there is ample evidence that herbivore‐induced plant responses affect individual performance and growth of herbivores, whether they scale‐up to regulate herbivore population dynamics is still unclear. We evaluated the consequences of variation in plant defences and herbivore density on herbivore development, reproduction and density‐dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density‐dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones JA and SA and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defences by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate‐dependent defences. Jasmonate‐insensitive plants cannot induce the defences regulated by the JA pathway, while jasmonate‐overexpressing plants constitutively express jasmonate‐dependent defences. We found that jasmonate defences provided resistance against aphids and influenced density‐dependent processes. Jasmonate‐overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities and caused density‐independent aphid population growth. Jasmonate‐overexpressing plants showed high JA‐dependent constitutive levels of resistance and were unable to activate the SA pathway in response to aphid feeding. In contrast, jasmonate‐insensitive plants increased aphid reproduction, shortened developmental time, reduced population growth only at high initial densities and promoted strong negative density‐dependent population growth. Aphid feeding on jasmonate‐insensitive plants did not induce jasmonate‐dependent defences, but induced the SA pathway in a density‐dependent manner, which resulted in negative density‐dependent aphid population growth. Aphid feeding on jasmonate‐insensitive and jasmonate‐overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones JA and SA. By muting or enhancing jasmonate‐mediated responses and quantifying SA phytohormone induction, we demonstrated that plant defences are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores.

Aphid-Responsive Defense Networks in Hybrid Switchgrass

“…ABA and SA are also important hormones impacting plant responses (Hillwig et al, 2016;Kersch-Becker and Thaler, 2019;Yang et al, 2019). ABA was induced early in response to GB and later in response to YSA, while SA was induced solely in response to YSA.…”

Asexual reproduction of a few genotypes favored the invasion of the cereal aphidRhopalosiphum padiin Chile

“…The reproductive success was estimated by calculating daily per capita growth rate of aphids (PGR = d N / N d t ) as (ln( N f ) – ln( N i ))/(( t f – t i )). Here, N i and N f indicate the initial and final number of individuals, respectively, while t f – t i correspond to the difference in days from the beginning to the end of the experiment (Kersch‐Becker & Thaler, 2019). Five replicates were included for each host.…”

Plant defences for enhanced integrated pest management in tomato

“…Constitutive defences include products, structures and compounds of the primary and secondary metabolism that are involved in plant defences regardless of the threat of an herbivore (Bar & Shtein, 2019; Hanley, Lamont, Fairbanks, & Rafferty, 2007). By contrast, induced defences are activated following an herbivore attack, or other biotic and abiotic stresses, and include products, structures and compounds of the secondary metabolism of the plants subsequently primed (Arimura, Kost, & Boland, 2005; Kersch‐Becker & Thaler, 2019). The response of plants to stresses is a combination of many reactions and mechanisms that indirectly and directly influence their interactions with the ecosystem, even at the multitrophic level and often with long‐term consequences (Mithöfer & Boland, 2012; Stam et al, 2014).…”