Journal Article

Major Signaling Pathways Modulate Arabidopsis Glucosinolate Accumulation and Response to Both Phloem-Feeding and Chewing Insects

Hom, Amanda, Schultz, Jack C, Appel, Heidi M, Raina, Ramesh, Mewis, Inga

2005

Overview

Plant responses to enemies are coordinated by several interacting signaling systems. Molecular and genetic studies with mutants and exogenous signal application suggest that jasmonate (JA)-, salicylate (SA)-, and ethylene (ET)-mediated pathways modulate expression of portions of the defense phenotype in Arabidopsis (Arabidopsis thaliana), but have not yet linked these observations directly with plant responses to insect attack. We compared the glucosinolate (GS) profiles of rosette leaves of 4-week-old mutant and transgenic Arabidopsis (Columbia) plants compromised in these three major signaling pathways, and characterized responses by those plants to feeding by two phloem-feeding aphids (generalist Myzus persicae and specialist Brevicoryne brassicae) and one generalist caterpillar species (Spodoptera exigua Hubner). Blocked JA signaling in coronatine-insensitive (coi1) and enhanced expression of SA-signaled disease resistance in hypersensitive response-like (hrl1) mutants reduced constitutive GS concentrations, while blocking SA signaling at the mediator protein npr1 mutant (NPR) increased them. There was no significant impact on constitutive GS contents of blocking ET signaling (at ET resistant [etr1]) or reducing SA concentrations (nahG transgene). We found increased GS accumulation in response to insect feeding, which required functional NPR1 and ETR1 but not COI1 or SA. Insect feeding caused increases primarily in short-chain aliphatic methylsulfinyl GS. By contrast, responses to exogenous JA, a frequent experimental surrogate for insect attack, were characterized by an increase in indolyl GS. Insect performance, measured as population increase or weight increase, was negatively related to GS levels, but we found evidence that other, ET-regulated factors may also be influential. Plant resistance to (consumption by) S. exigua was not related to insect growth because some plant chemistries inhibited growth while others inhibited feeding. These major signaling pathways modulate Arabidopsis GS accumulation and response to both phloem-feeding and chewing insects, often antagonistically; NPR appears to be central to these interactions. Our results indicate that exogenous signal application and plant consumption measures may not provide useful measures of plant responses to actual insect feeding.

• Publisher: American Society of Plant Biologists,American Society of Plant Physiologists
• Subject: Animals / Aphididae / Arabidopsis / Arabidopsis - genetics / Arabidopsis - metabolism / Arabidopsis - parasitology / Arabidopsis - physiology / Arabidopsis thaliana / bioaccumulation / Biological and medical sciences / Brevicoryne brassicae / Caterpillars / Cell physiology / coronatine-insensitive prtoein / Cyclopentanes / ethylene / Feeding Behavior / Feeding Behavior - physiology / Fundamental and applied biological sciences. Psychology / genetics / Genotype / Genotypes / Glucosinolates / Glucosinolates - metabolism / Herbivores / hypersensitive response-like protein / Insect genetics / Insect pests / Insecta / Insecta - physiology / jasmonic acid / Leaves / metabolism / Molecular and cellular biology / Myzus persicae / Oxylipins / parasitology / physiology / Phytophagous insects / plant biochemistry / plant response / plant-insect relations / Plants / Plants Interacting with Other Organisms / salicylic acid / Signal Transduction / Spodoptera exigua / Transgenic insects / transgenic plants