AUTHOR=Schuman Meredith C. , Meldau Stefan , Gaquerel Emmanuel , Diezel Celia , McGale Erica , Greenfield Sara , Baldwin Ian T. 

TITLE=The Active Jasmonate JA-Ile Regulates a Specific Subset of Plant Jasmonate-Mediated Resistance to Herbivores in Nature

JOURNAL=Frontiers in Plant Science

VOLUME=9

YEAR=2018

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2018.00787

DOI=10.3389/fpls.2018.00787

ISSN=1664-462X

ABSTRACT=<p>The jasmonate hormones are essential regulators of plant defense against herbivores and include several dozen derivatives of the oxylipin jasmonic acid (JA). Among these, the conjugate jasmonoyl isoleucine (JA-Ile) has been shown to interact directly with the jasmonate co-receptor complex to regulate responses to jasmonate signaling. However, functional studies indicate that some aspects of jasmonate-mediated defense are not regulated by JA-Ile. Thus, it is not clear whether JA-Ile is best characterized as the master jasmonate regulator of defense, or if it regulates more specific aspects. We investigated possible functions of JA-Ile in anti-herbivore resistance of the wild tobacco <italic>Nicotiana attenuata</italic>, a model system for plant-herbivore interactions. We first analyzed the soluble and volatile secondary metabolomes of ir<italic>JAR4</italic>xir<italic>JAR6</italic>, as<italic>LOX3</italic>, and WT plants, as well as an RNAi line targeting the jasmonate co-receptor CORONATINE INSENSITIVE 1 (ir<italic>COI1</italic>), following a standardized herbivory treatment. ir<italic>JAR4</italic>xir<italic>JAR6</italic> were the most similar to WT plants, having a ca. 60% overlap in differentially regulated metabolites with either asLOX3 or ir<italic>COI1</italic>. In contrast, while at least 25 volatiles differed between ir<italic>COI1</italic> or as<italic>LOX3</italic> and WT plants, there were few or no differences in herbivore-induced volatile emission between ir<italic>JAR4</italic>xir<italic>JAR6</italic> and WT plants, in glasshouse- or field-collected samples. We then measured the susceptibility of jasmonate-deficient vs. JA-Ile-deficient plants in nature, in comparison to wild-type (WT) controls, and found that JA-Ile-deficient plants (ir<italic>JAR4</italic>xir<italic>JAR6</italic>) are much better defended even than a mildly jasmonate-deficient line (as<italic>LOX3</italic>). The differences among lines could be attributed to differences in damage from specific herbivores, which appeared to prefer either one or the other jasmonate-deficient phenotype. We further investigated the elicitation of one herbivore-induced volatile known to be jasmonate-regulated and to mediate resistance to herbivores: (<italic>E</italic>)-α-bergamotene. We found that JA was a more potent elicitor of (<italic>E</italic>)-α-bergamotene emission than was JA-Ile, and when treated with JA, ir<italic>JAR4</italic>xir<italic>JAR6</italic> plants emitted 20- to 40-fold as much (<italic>E</italic>)-α-bergamotene than WT. We conclude that JA-Ile regulates specific aspects of herbivore resistance in <italic>N. attenuata</italic>. This specificity may allow plants flexibility in their responses to herbivores and in managing trade-offs between resistance, vs. growth and reproduction, over the course of ontogeny.</p>