Induced post-invasive defenses in the nonhost plant Parthenium hysterophorus L. prevent root cortical colonization by Macrophomina phaseolina and impart resistance to dry root rot

Abstract

Dry root rot (DRR) of chickpea is caused by the broad-range necrotrophic fungus Macrophomina phaseolina. Chickpea germplasm does not provide durable resistance to DRR, which is particularly devastating under drought. Even moderately resistant chickpea varieties become susceptible under combined stress. We hypothesized that nonhost resistance (NHR) is durable even under combined stress. Using the blotter paper assay and stereomicroscopic observations, we identified the asterid weed Parthenium hysterophorus as a potential nonhost of M. phaseolina among 82 potential nonhosts. Epidermal necrotic lesions were prevented in P. hysterophorus. In planta fungal load was 0.195 and 0.007 ng/ng total DNA in chickpea and P. hysterophorus, respectively. M. phaseolina could not colonize the P. hysterophorus root while up to 6 cortical cell layers were colonized in chickpea. Further, NHR was durable under combined stress. Dual RNA sequencing revealed that M. phaseolina actively attempted to infect the nonhost and activated specific genes in the xenobiotics degradation pathway. P. hysterophorus also showed an active defense response with1958 and 2294 differentially expressed genes at 2 and 4 DAI, respectively, with 363 upregulated at both time points. Differential expression of cell wall synthesis, phytohormone signaling, and other defense response pathways likely contributes to NHR. Few genes in the phenylpropanoid biosynthesis pathways in P. hysterophorus were also upregulated, possibly because these metabolites are linked to the distinct changes in the fungus during nonhost infection. We therefore conclude that P. hysterophorus exhibits post-invasive NHR to M. phaseolina and that general defense, phytohormone signaling and secondary metabolic pathways contribute to NHR.