Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance

By Ying-bo Mao | January 9, 2017

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Immunity deteriorates with age in animals but comparatively little is known about the temporal regulation of plant resistance to herbivores. The phytohormone jasmonate (JA) is a key regulator of plant insect defense. Here, we show that the JA response decays progressively in Arabidopsis. We show that this decay is regulated by the miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE9 (SPL9) group of proteins, which can interact with JA ZIM-domain (JAZ) proteins, including JAZ3. As SPL9 levels gradually increase, JAZ3 accumulates and the JA response is attenuated. We provide evidence that this pathway contributes to insect resistance in young plants. Interestingly however, despite the decay in JA response, older plants are still comparatively more resistant to both the lepidopteran generalist Helicoverpa armigera and the specialist Plutella xylostella, along with increased accumulation of glucosinolates. We propose a model whereby constitutive accumulation of defense compounds plays a role in compensating for age-related JA-response attenuation during plant maturation.


As sessile organisms, plants have evolved complex defense systems against herbivores for successful survival and reproduction. Induced defense response refers to immune responses elicited by specific stimuli whereas constitutive defense refers to the accumulation of insecticidal components in plant tissues during the course of normal growth and development1. Plants of Arabidopsis thaliana produce glucosinolates (GLSs), which function as defense metabolites against insect herbivores and pathogens2.

In plants, JA is the major defense hormone in activating defense reactions against herbivorous insects and necrotrophic pathogens, and in Arabidopsis most responses are regulated by the JA-amino acid conjugate jasmonoyl-L-isoleucine (JA-Ile)3,4. JA ZIM-domain (JAZ) proteins, which are the repressors of JA signalling, have two conserved domains: the N-terminal ZIM domain and the C-terminal Jas domain5,6. The Jas domain is a protein–protein interaction surface required for binding to either transcription factors such as MYC2, or CORONATINE INSENSITIVE1 (COI1), a component of the ubiquitin E3 ligase SCFCOI1 and the JA-Ile receptor7,8,9. In normal conditions, the relatively high levels of JAZ proteins repress the activity of transcription factors. External stimuli, such as wounding or insect attack, cause JA-Ile concentration to rapidly rise in plant cells, which triggers COI1-JAZ interaction and degradation of JAZs by the 26S proteasome10, releasing transcription factors to activate downstream defense genes11. Therefore, the abundance of JAZ proteins in cells, determined largely by the rates of protein degradation, controls the output of JA response12. Interestingly, protein stability of MYC transcription factors is also involved in JA response13,14.

Plant defense involves a metabolic cost, where a tradeoff occurs between defense and growth15. In animals immunosenescence is a common phenomenon16. In plants, immunity is also associated with age, as old plants may display increased resistance to pathogens, which is referred to as age-related resistance17. For plant-herbivore interactions, the Plant Vigour Hypothesis is based on observations that many herbivores attack young and vigorous plants more frequently than old and mature plants18. However, the molecular mechanisms underlying ARR and the Plant Vigour Hypothesis remain elusive.

In plants, miR156 functions as an important regulator of age-dependent development through targeting a group of transcription factors called SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL)19. The level of miR156 is high during the juvenile stage and steadily decreases during later plant growth and development, leading to a progressive increase in the level of SPLs, which regulate a broad range of processes including flowering20,21, secondary metabolite production22,23, trichome initiation24,25,26, vernalization27,28 and shoot regeneration29. The phytohormone gibberellin (GA) plays an important role in regulating diverse aspects of plant growth and development30,31. Similar to JAZ proteinss in the JA signalling pathway, DELLAs, a group of GRAS family proteins, function as repressors to control GA signal output. When the level of bioactive GAs increases, DELLAs are subject to ubiquitination and degradation30. Recent investigations revealed that GA signalling cross-talks with both the JA response and the miR156-SPL mediated aging pathways. DELLAs directly bind to SPL proteins and interfere with their transcriptional activity32, and they also interact with JAZ proteins or MYC2 to modulate the JA response33,34.

Here we demonstrate that the JA response declines with plant age. We show that this attenuated JA response is primarily regulated by the miR156-targeted SPL proteins that can interact with certain JAZ proteins, and appears to be independent of the GA signalling pathway. We propose a model whereby accumulation of GLS in older plants accumulates for attenuated JA response.