Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores

Abstract

Plants generally respond to herbivore attack by increasing resistance and decreasing growth. This prioritization is achieved through the regulation of phytohormonal signaling networks. However, it remains unknown how this prioritization affects resistance against non-target herbivores. In this study, we identify WRKY70 as a specific herbivore-induced, mitogen-activated protein kinase-regulated rice transcription factor that physically interacts with W-box motifs and prioritizes defence over growth by positively regulating jasmonic acid (JA) and negatively regulating gibberellin (GA) biosynthesis upon attack by the chewing herbivore Chilo suppressalis. WRKY70-dependent JA biosynthesis is required for proteinase inhibitor activation and resistance against C. suppressalis. In contrast, WRKY70 induction increases plant susceptibility against the rice brown planthopper Nilaparvata lugens. Experiments with GA-deficient rice lines identify WRKY70-dependent GA signaling as the causal factor in N. lugens susceptibility. Our study shows that prioritizing defence over growth leads to a significant resistance trade-off with important implications for the evolution and agricultural exploitation of plant immunity.

DOI: http://dx.doi.org/10.7554/eLife.04805.001

eLife digest

Many different animals feed on plants, including almost half of all known insect species. Some herbivores—like caterpillars for example—feed by chewing. Others, such as aphids and planthoppers, use syringe-like mouthparts to pierce plants and then feed on the fluids within.

To minimize the damage caused by these herbivores, plants activate specific defenses upon attack, including proteins that can inhibit the insect's digestive enzymes. The inhibitors are effective against chewing herbivores but seem to have little or no effect on some insects that feed by the ‘pierce-and-suck’ method.

Investing in defense requires energy, and so plants attacked by herbivores actively slow their growth to meet this demand. Plants achieve this trade-off by changing the levels of different plant hormones. These hormones can control the expression of thousands of genes and have widespread effects throughout the plant. However, little is known about how prioritizing defense overgrowth in response to an attack by one herbivore affects the plant's ability to defend itself against other herbivores.

Transcription factors are proteins that control which genes inside a cell are active or inactive. Li et al. searched for a transcription factor in rice plants that was specifically triggered in response to an attack by the caterpillars of a moth called the rice striped stem borer. This search identified a protein called WRKY70 as a transcription factor that prioritizes defense overgrowth. WRKY70 achieves this by increasing the levels of a defensive plant hormone (called jasmonic acid) while reducing the levels of a growth hormone (called gibberellin). Further experiments show that the increase in jasmonic acid production is required to activate the enzyme inhibitors and for resistance against these caterpillars.

Li et al. then found that increased WRKY70 activity makes rice plants more susceptible to attack by a second herbivore, a piercing-sucking insect called the rice brown planthopper. Further experiments revealed that this is due to the reduced levels of gibberillin. These findings show that while prioritizing defense overgrowth is effective against some insect herbivores, it comes with a cost as it makes the plants more susceptible to attack by other herbivores. This trade-off has important implications for both the evolution of plant immunity, and efforts to exploit plant immunity to help protect crops from herbivore attack.

DOI: http://dx.doi.org/10.7554/eLife.04805.002