Infection of tomato plants by tomato yellow leaf curl virus (TYLCV) potentiates the ethylene and salicylic acid pathways to fend off root-knot nematode (Meloidogyne incognita) parasitism

Abstract

In nature, it is common for plants to be infected by multiple pathogens simultaneously, and deciphering the underlying mechanisms of such interactions has remained elusive. The occurrence of root-knot nematode (RKN), Meloidogyne incognita, and tomato yellow leaf curl virus (TYLCV; Begomovirus coheni) has been reported in most tomato cultivation areas. We investigated the interaction between RKN and TYLCV in tomato plants at phenotypic, biochemical, and gene expression levels. Several treatments were considered including mock inoculation, inoculation with TYLCV or RKN alone, simultaneous inoculation with both TYLCV and RKN, and sequential inoculations with a five-day interval. Among them, simultaneous inoculation showed the highest impact on RKN suppression compared to mock-inoculated plants. Biochemical assays in the time-point experiments demonstrated that the pick of defense capacity of plants occurs at 48- and 72-h post-inoculation. Gene expression analyses utilizing marker genes from main hormonal pathways involved in plant defense, including salicylic acid (SA), jasmonic acid (JA), and ethylene (ET), indicated that ET and SA are highly involved in the potentiation of TYLCV-induced defense against RKN. To validate the action of SA and ET in the induction of defense against RKN by TYLCV, transgenic lines deficient in SA (NahG) and ET (ACD) accumulation were co-inoculated with TYLCV and RKN. Both transgenic lines failed to express TYLCV-induced defense against RKN. These findings demonstrate an antagonistic effect of TYLCV against RKN in tomato plants, mediated by SA and ET signaling pathways.