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Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response

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Abstract

Despite being the major dietary source for countless insects, plants have not only survived but thrived on earth and represent arguably the largest terrestrial biomass. This is because plants, instead of falling passive victims to the insects, have come to possess numerous defense strategies including production of insect poisons, deterrents, and other anti-nutritive compounds. A significant part of these built-in defenses are inducible and tactfully coordinated with plant growth in a manner that maximizes return on investment. The lipid-derived signal jasmonate (JA) orchestrates many of these inducible defense responses. JA has a similar evolutionary origin as eicosanoids which play critical roles in mammalian wound and inflammatory responses indicating cross-kingdom adoption of lipid-derived signals for use against tissue injuries. The molecular perception and signaling mechanism of JA indicates that the intracellular concentration of a derivative, jasmonoyl-l-isoleucine (JA-Ile), is the major determinant factor for the dynamic regulation of the JA signaling system. Interdisciplinary methods including recombinant enzyme assays, mass spectrometry based hormone profiling, genetics, genomics, and the model plant Arabidopsis thaliana have assisted in elucidating metabolic pathways controlling JA-Ile homeostasis. Along with the relatively well established biosynthetic enzymes, more recently discovered catabolic pathways as well as areas that need new discoveries are discussed herein. Knowledge obtained from the JA-dependent stress adaptive responses are expected to have agricultural and industrial impact in the future toward the development of environmentally friendly ways of managing pests and tapping into a largely unexplored treasure trove of plant-derived specialized metabolites for human use.

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Abbreviations

α-LA:

α-Linolenic acid

12COOH-JA-Ile:

12-Carboxy-JA-Ile

COI1:

CORONATINE INSENSITIVE 1

CYP:

Cytochrome P450

dnOPDA:

Dinor-OPDA

ER:

Endoplasmic reticulum

12,13-EOT:

12,13(S)-epoxy-octadecatrienoic acid

FA:

Fatty acid

13-HPOT:

13(S)-hydroperoxylinolenic acid

12HSO4-JA:

12-Hydroxyjasmonic acid sulfate

IAA:

Indole-3-acetic acid

IAH:

ILR1-like amidohydrolase

JA:

Jasmonate

JA-Ile:

Jasmonoyl-l-isoleucine

JAR1:

JASMONATE RESISTANT 1

JAZ:

JASMONATE-ZIM domain

MeJA:

Methyl-JA

OGA:

Oligosaccharides

12OH-JA:

12-Hydroxy-jasmonic acid

12OH-JA-Ile:

12-Hydroxy-JA-Ile

OPC-8:

0: 3-Oxo-2-(2′-[Z]-pentenyl)-cyclopentane-1-octanoic acid

OPDA:

12-Oxo-phytodienoic acid

ROS:

Reactive oxygen species

SCF:

Skip1-Cul1-F-box protein

TF:

Transcription factor

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Acknowledgements

I appreciate helpful comments and discussions by Tong Zhang, Arati Poudel, and Athen Kimberlin. Supports for research on jasmonate in my laboratory are from the National Science Foundation (IOS-1557439), the UM System Research Board, and the Food for the twentyfirst Century Program at the University of Missouri.

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Correspondence to Abraham J. Koo.

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Koo, A.J. Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response. Phytochem Rev 17, 51–80 (2018). https://doi.org/10.1007/s11101-017-9510-8

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