The laccase gene MdLac18 decouples the growth-defense trade-off by orchestrating lignification to enhance aphid resistance and biomass accumulation in Nicotiana benthamiana

Enhancing resistance to piercing-sucking pests while preserving superior agronomic performance remains a key challenge in plant breeding, constrained by the classical “growth-defense trade-off”. Lignin, a core component of plant secondary cell walls, acts as a vital physical barrier against pest invasion, yet genetic regulators that simultaneously reinforce lignin-mediated defense and promote plant growth are rarely reported. Here, we cloned MdLac18 (GenBank Accession No.: PV341664), a laccase gene from the aphid-resistant apple cultivar ‘Starkrimson’, and heterologously expressed it in Nicotiana benthamiana via Agrobacterium-mediated transformation. Transgenic lines exhibited robust resistance to Myzus persicae : corrected aphid mortality reached 43.99% and fecundity decreased by 55.13% at 8 days post-inoculation. Electrical Penetration Graph (EPG) analysis revealed prolonged salivation (E1 wave) and shortened phloem ingestion (E2 wave) in aphids, reflecting impaired stylet penetration. MdLac18 overexpression increased laccase activity by 59.61% and lignin content by 47.40%, with enhanced vascular tissue lignification. GC-MS analysis confirmed a 176% increase in G-type lignin monomers (coniferyl alcohol derivatives), indicating specific promotion of G-type lignin biosynthesis. Notably, unlike typical defense-related genes, MdLac18 conferred dual benefits: transgenic tobacco showed improved agronomic traits (increased plant height, stem diameter at the early vegetative stage (30–60 days after transplantation), biomass, and early flowering). Our findings establish MdLac18 as a rare genetic resource that, by exerting its stress-regulatory function and enhancing plant adaptability to adverse environments, holds the potential to decouple the growth-defense trade-off under controlled suboptimal conditions, thus providing a novel strategy for breeding crops with durable aphid resistance and superior agronomic performance.