From trade-off to synergy: how nutrient status modulates plant resistance to herbivorous insects?

Abstract

The principle of the "growth-defense trade-off" governs how plants adjust their growth and defensive strategies in response to external factors, impacting interactions among plants, herbivorous insects, and their natural enemies. Mineral nutrients are crucial in modulating plant growth and development through their bottom-up effects. Emerging evidence has revealed complex regulatory networks that link mineral nutrients to plant defense responses, influencing the delicate balance between growth and defense against herbivores. This review aims to summarize recent advances that elucidate the impact of nutrient availability on plant defense responses. Particularly, we focus on how nutrient status shapes plant resistance to herbivores, delving into the molecular mechanisms underlying this physiological process. Moreover, the interplay between mineral nutrients and various herbivore defense mechanisms, including physical protection, plant hormone signaling, defensive metabolite production, and volatile organic compound emissions that deter herbivores or attract their natural enemies, are discussed. This comprehensive review sets the stage for future investigations into the intricate crosstalk between nutrient signaling and plant defense responses, which serves as a central mechanism to guide sustainable pest management approaches, thereby promoting balanced agroecosystem health and enhancing plant ecosystem productivity and resilience.

Keywords: Growth-defense trade-off; Integrated pest management; Mineral nutrients; Plant–insect interaction; Volatile organic compounds.

Fig. 1

Nutrient cues modulate VOC formation and crosstalk with hormone signaling. On the left are the VOC biosynthetic pathways. The pathways involved include the shikimate/phenylalanine, mevalonic acid (MVA), methylerythritol phosphate (MEP), and the lipoxygenase (LOX) pathways. These pathways involve multiple enzymatic reactions, as depicted by stacked arrows. VOCs encompass a diverse array of compounds such as including benzenoids/phenylpropanoids, sesquiterpenes, monoterpenes, hemiterpenes, diterpenes, volatile carotenoid derivatives, and methyl jasmonate/green leaf volatiles, all set against a purple cloud backdrop. The effects of VOCs on herbivorous insects, I, deter herbivores; II, predation by natural enemies. Key acronyms include PEP (phosphoenolpyruvate), E4P (erythrose 4-phosphate), DAHP (3-deoxy-D-arabinoheptulosonate-7 phosphate), DMAPP (dimethylallyl pyrophosphate), IPP (isopentenyl pyrophosphate), GPP (geranyl pyrophosphate), NPP (neryl pyrophosphate), GGPP (geranylgeranyl pyrophosphate), and FPP (farnesyl pyrophosphate). On the right is a schematic illustration of the synthetic mechanisms of the JA signaling and phenylpropanoid pathways affected by nutrient availability. Abbreviations: High-N, high nitrogen; High-P, high phosphorus; High-K, high potassium; High-Si, high silicon; Low-N, low nitrogen; Low-P, low phosphorus; JA-Ile, jasmonic acid isoleucine; JAZ, jasmonate-zim; SCF, SKP1–CUL1–F-box protein E3 ubiquitin ligase

Fig. 2

Nutrient-mediated growth-defense trade-off strategies. The three solid circles show the reported functions of mineral nutrients on plant herbivores, including modulation of physical defense, hormonal response, and defensive metabolites. The concentric circles in the middle indicate other defenses mediated by the activation of defense-related genes. The circles of different colors at the plant root represent distinct nutrient elements. VOCs, volatile organic compounds; JA, jasmonic acid; SA, salicylic acid