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

Ying-Bo Mao,Jia-Wei Wang,Dian-Yang Chen,Yao-Qian Liu,Gao-Jie Hong,Xiao-Ya Chen,Fang-Yan Chen,Ling-Jian Wang,Xin Fang

doi:10.1038/ncomms13925

Abstract

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.

Highlights

Immunity deteriorates with age in animals but comparatively little is known about the temporal regulation of plant resistance to herbivores
We demonstrate that the JA response declines with plant age. We show that this attenuated JA response is primarily regulated by the miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) proteins that can interact with certain JA ZIM-domain (JAZ) proteins, and appears to be independent of the GA signalling pathway
Diamondback moth (Plutella xylostella), is a specialist herbivore living on plants of Brassicaceae, and Arabidopsis thaliana can be used as a model host[37]

Summary

Introduction

Immunity deteriorates with age in animals but comparatively little is known about the temporal regulation of plant resistance to herbivores. As SPL9 levels gradually increase, JAZ3 accumulates and the JA response is attenuated. 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]. 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 proteasome[10], releasing transcription factors to activate downstream defense genes[11]. The molecular mechanisms underlying ARR and the Plant Vigour Hypothesis remain elusive

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