Nature: Revealing the Molecular Mechanism of Plant Airborne Immunity Mediated by Methyl Salicylate and the Anti-defense Mechanism of Viruses

Yulie Liu's team from the School of Life Sciences at Tsinghua University has made research progress in the molecular mechanisms of plant airborne immunity and the anti-defense mechanisms of viruses. The research results have been published in the Nature (IF=64.8).

Plants produce volatile organic compounds (VOCs) when they feel environmental stimuli, which can act as aerial cues and be perceived by neighboring receiving plants to trigger defense. This phenomenon is called airborne defense (AD). Although plant-to-plant communication (PPC) has been observed in many species for decades and its important biological and ecological significance has been recognized, the molecular genetic framework of VOCs mediated PPC (including AD) remains largely unclear. In addition, receptors for plant perception of other VOCs have not been identified, except for ethylene receptors.

Aphids are the most destructive agricultural and horticultural pests worldwide, feeding on the phloem and causing widespread damage to crop production. The attack of aphids can induce plants to release VOCs, the main component of which is methyl salicylate (MeSA). MeSA helps plants resist the invasion of herbivorous insects (including aphids), such as driving away, attracting natural enemies, or reducing the survival ability of these insects. However, how MeSA can serve as a communication signal between plants to activate the anti-aphid defense function of adjacent receiving plants is a long-standing unsolved problem. For example, it is currently unclear whether plants have a receptor system for sensing MeSA in the air. The mechanism by which MeSA generation is initiated during aphid invasion is also unclear. In addition, although there have been reports that MeSA can mediate resistance to tobacco mosaic virus (TMV), it remains to be elucidated whether and how aphids and viruses regulate resistance.

In this study, Yulie Liu's team found that after aphids bite plants, they produce MeSA, which can be sensed and bound by the nearby MeSA receptor protein SA-binding protein-2 (SABP2) in the air and converted into salicylic acid (SA). SA activates transcription factor NAC2 and upregulates the expression of SA-carboxylmethyltransferase-1 (SAMT1) gene, resulting in more MeSA and inducing plant anti aphid immunity, thereby reducing virus transmission.

In addition, Yulie Liu 's team also found that some aphid borne viruses can encode proteins containing the helicase domain and interact with NAC2 protein, altering the subcellular nuclear localization of NAC2 protein to the cytoplasm, promoting the degradation of NAC2 by 26S proteasomes in the cytoplasm, thereby negatively regulating the NAC2-SAMT1 pathway, inhibiting the synthesis and volatilization of MeSA in plants bitten by aphids, and blocking inter plant "warning" communication, Promote aphid infestation of neighboring plants and the spread of viruses. This discovery reveals the molecular mechanism of plant airborne immunity and the anti defense mechanism of viruses, as well as a novel reciprocal way of coevolution between aphids and viruses.

Figure 1: Schematic diagram of the molecular mechanism of plant airborne immunity 

In the article, Biolight Biotechnology’s Plantview100 in vivo plant imaging system was used to detect luciferase activity in the complementary image technology (LCI) for firefly luciferase fragments detection.

LCI assay to show that CMV1a helicase domain (1a-H), but not methyltransferase domain (1a-M), interacts with NAC2

Reference：

Gong, Q., Wang, Y., He, L. et al. Molecular basis of methyl-salicylate-mediated plant airborne defence. Nature 622, 139–148 (2023). https://doi.org/10.1038/s41586-023-06533-3