Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.)

Abstract

Abstract Background Fusarium oxysporum f. sp. vasinfectum (FOV) race 4 (FOV4) is a highly pathogenic soil-borne fungus responsible for Fusarium wilt in cotton (Gossypium spp.) and represents a continuing threat to cotton production in the southwest states of the U.S., including California, New Mexico, and Texas. Even though the Pima (G. barbadense L.) cotton gene pool shows more susceptibility to this pathogen than Upland (G. hirsutum L.) cotton, fortunately, some Pima cultivars present resistance to FOV4 infection, like Pima-S6. To gain insights into the mechanism underlying FOV4 resistance, we performed comparative transcriptional and metabolomic profiling of FOV4-resistant Pima-S6 and FOV4-susceptible Pima S-7 and Pima 3–79 cotton. Results Comparative analysis of transcriptional FOV4 infection responses on these genotypes indicated a differential response between resistant Pima-S6 and susceptible Pima S-7 and 3–79. GO-enriched analysis found clusters related to various biological processes, including transmembrane transport, glycoside hydrolysis, metabolism of small molecules, and phenylpropanoid metabolism. Arabidopsis ortholog genes comparison with categories significantly enriched in Pima-S6 resulted in multiple categories clustered to similar biological processes such as the metabolism of small molecules, regulation of enzymatic activity, diterpenoid biosynthetic processes, and phytohormone signaling-related processes, being phenylpropanoid biosynthesis and metabolism highly enriched. These results correlated with the accumulation of secondary metabolites in Pima-S6 roots, specifically esculetin, a coumarin that inhibits the growth of Fusarium. Transcriptomic profiling enabled the identification of candidate genes potentially involved in the resistance mechanism of FOV4-resistance in protecting the Pima-S6 cotton cultivar from this pathogenic fungus. Some genes of this pathway were found to be in chromosome-QTL regions linked with resistance to FOV4. Conclusions Our results highlight an essential role for the phenylpropanoid synthesis pathway in FOV4 resistance and create opportunities for gene discovery and SNP development for marker-associated selection (MAS) for breeding for FOV4 resistance.