At Long Last, Pathologists Hear Plants' Cry For Help

Abstract

PLANT BIOLOGY![Figure][1] Silent scream. Tobacco leaves scarred by the tobacco mosaic virus emit a signal that boosts resistance in the rest of the plant. CREDIT: COURTESY H. D. SHEW. REPRINTED BY PERMISSION FROM COMPENDIUM OF TOBACCO DISEASES, 1991, AMERICAN PHYTOPATHOLOGICAL SOCIETY, ST. PAUL, MINNESOTA A sick plant has something in common with an athlete who slathers on stinky sports balms. Both are counting on the salutary effects of methyl salicylate, the pungent oil of wintergreen. This compound turns out to be a long-sought distress call that rouses plant resistance against disease, researchers report on page 113. “Finally, we've been able to identify a signal that activates this plant-wide defense,” says co-author and plant pathologist Daniel Klessig of the Boyce Thompson Institute for Plant Research in Ithaca, New York. Unlike animals, plants can't mobilize a cadre of targeted immune cells to fight infection. But that doesn't mean that they just stand there and take it. When a pathogen infects one part of the plant, say a leaf, that tissue sounds the alarm, and other parts beef up their defenses, not only to that pathogen but also to other potential attackers. Some evidence even indicates that nearby plants can heed the alert. For more than 50 years, scientists have pursued the so-called mobile signal that wends through the plant's phloem, or food-transporting tissue, and spreads the alarm. In the 1990s, they thought they had nabbed this molecular messenger: salicylic acid, a key plant hormone and a close relative of the main ingredient in aspirin. However, grafting experiments proved them wrong: The graft still exhibited systemic resistance even if the infected part of the plant lacked the supposed messenger. Klessig and colleagues came upon what seems to be a real messenger while chasing the receptor for salicylic acid. The team's experiments eliminated one candidate receptor, the enzyme SABP2. However, they discovered that SABP2 transforms methyl salicylate into salicylic acid and that the enzyme is necessary for systemic resistance, suggesting that methyl salicylate might be the signal. To determine whether methyl salicylate indeed delivers a warning from the site of an infection to the rest of the plant, the team performed grafting experiments on tobacco plants and then exposed the graft recipient, or rootstock, to tobacco mosaic virus. Systemic resistance still occurred when the graft was missing an enzyme that makes methyl salicylate, but not if this protein was absent from the rootstock, indicating a need for methyl salicylate only where the infection occurred. The researchers engineered plants to make an overactive form of SABP2 that uses up methyl salicylate. When they used those plants as rootstock, no systemic resistance developed after the rootstock was infected. But if the graft alone manufactured this unstoppable enzyme, resistance appeared, again arguing for the need for methyl salicylate at the infection site. The scientists also used RNAi to banish SABP2 from the graft or the rootstock. After infection of the rootstock, the graft developed resistance only if it could make SABP2. It didn't matter whether the rootstock could produce the enzyme. Overall, the experiments indicate that the infected tissue requires the ability to make methyl salicylate, whereas the target tissue needs to be able to break it down. “I'd say we were quite confident that methyl salicylate is a signal [for resistance],” says Klessig. “It's a pretty persuasive series of experiments,” says molecular plant pathologist Terrence Delaney of the University of Vermont, Burlington. Raising the alarm probably involves two steps, Klessig says. The tissue under attack first produces methyl salicylate and releases it into the phloem for distribution. When this messenger arrives in target tissues, SABP2 converts it into salicylic acid, which triggers systemic resistance. The work is “an elegant solution” to the question of how to reconcile earlier evidence implicating salicylic acid in systemic resistance, says plant pathologist Luis Mur of the University of Wales in Aberystwyth, U. K. Agriculture could benefit from the discovery, says Klessig. Fine-tuning methyl salicylate levels—either through genetic engineering or selective breeding—might fortify crop defenses and reduce the amount of pesticides farmers need to apply. However, the methyl salicylate pathway may not be the whole story. Some data suggest that the signal is a lipid—methyl salicylate is not—and that a lipid called jasmonic acid might serve as an independent signal or as a partner. “The key question is, are we looking at a parallel system?” Mur asks. Klessig doesn't have an answer, at least not yet. “It's quite possible, even likely,” he notes, “that there are multiple signals.” [1]: pending:yes