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Plants target gut microbes to reduce insect herbivore damage

Hannah M. McMillan

Published 2023 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Plants must constantly identify and respond to a variety of abiotic and biotic stress, and they must do so in ways that balance defense and stress responses with growth and reproduction. In agricultural settings, understanding the mechanisms behind plant growth and stress tradeoffs could facilitate identification and design of safe, effective treatments to improve plant performance, crop yield, and plant health. With respect to biotic threats such as bacteria, fungi, and insect herbivores, plants often produce specialized metabolites that act either directly to neutralize the attack or indirectly by activating various local and systemic responses (1). Many defensive plant metabolites have been identified; however, their mechanism of action is often unknown or poorly understood, especially for insect herbivores (2). Intriguingly, microbial endosymbionts can play important roles in plant–insect interactions (3–5), suggesting that previous research may have overlooked important multilevel interaction networks that determine the outcome of herbivore attack. In PNAS, Liu et al. explore one such network of interactions and show that a rice defense flavonoid, sakuranetin, targets and reduces the abundance of yeastlike beneficial endosymbionts in brown planthoppers (BPHs), thereby reducing BPH performance and improving plant health (Fig. 1) (6). The brown planthopper Nilaparvata lugens is a destructive phloemfeeding herbivore that causes hundreds of millions of US dollars in rice crop losses annually (7, 8). Indeed, BPH damage leads to 20 to 80% yield loss, and in areas with heavy infestations, BPH damage can result in neartotal crop failure (9). While chemical insecticides effectively control BPHs, application poses significant risks for human health and eliminates natural BPH predators. Without predators, BPH populations increase unchecked, which can lead to greater plant damage during outbreaks and in subsequent years (7, 9). Further, BPHs display high levels of resistance to many insecticides (7). Safer, more effective BPH treatments are clearly needed to address these issues. The main driver of plant immune responses to insect herbivores is the phytohormone jasmonate, which is induced upon insect attack and regulates the biosynthesis of many downstream defense proteins and metabolites (10). Some of these metabolites, such as the alkaloid nicotine and volatile terpenes, have broad impacts on insect pests including neuromuscular impairment and repellent effects (11, 12). In response to BPH attack, jasmonate signaling in rice plants regulates genes in the phenylpropanoid pathway, strongly increasing expression of flavonoid biosynthetic genes (13). This signaling network increases levels of the defense metabolite sakuranetin and subsequently reduces BPH performance; however, the precise mechanism of action for sakuranetin is unknown (13). One unexplored target for plant defense metabolites like sakuranetin is the insect microbiome (14). Microbial endosymbionts play many beneficial roles for their insect hosts, including essential roles in growth, development, reproduction, stress resilience, and insect–plant interactions (5). In BPHs, yeastlike symbionts (YLSs) are the most abundant endosymbionts, are transmitted via eggs, and are found in every developmental stage of BPHs (15, 16). Critically, YLSs provide essential amino acids and sterol precursors for BPHs and aid in nitrogen recycling (17–19). These microbes play such an important role that depleting YLSs by heat treatment reduces growth of BPHs, resulting in lower body weight and delayed emergence (18). In light of previous data showing that sakuranetin has broad antifungal activity (20), Liu et al. hypothesized that this defense metabolite may reduce BPH performance by targeting YLSs. As expected, Liu et al. show that BPH nymph survival decreased when fed an artificial diet with sakuranetin (6).

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