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

Authors: OJEDA-RIVERA, JONATHAN - Texas Tech University; Ulloa, Mauricio; NAJERA GONZALEZ, R - Texas Tech University; ROBERTS, A - Texas Tech University; CHAVEZ MONTES, RICARDO - Texas Tech University; HERRERA-ESTRELLA, LUIS - Texas Tech University; LOPEZ-ARRENDONDO, DAMAR - Texas Tech University

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/24/2023
Publication Date: 1/8/2024
Citation: Ojeda-Rivera, J., Ulloa, M., Najera Gonzalez, R.H., Roberts, A.P., Chavez Montes, R., Herrera-Estrella, L., Lopez-Arrendondo, D. 2024. Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.). Frontiers in Genetics. 14. https://doi.org/10.3389/fgene.2023.1271200.
DOI: https://doi.org/10.3389/fgene.2023.1271200

Interpretive Summary: Fusarium oxysporum f. sp. vasinfectum (FOV) race 4 (FOV4) is a highly pathogenic soil-borne fungus responsible for Fusarium wilt disease in cotton and represents a continuing threat to cotton production in the southwest states of the U.S., including California, New Mexico, and Texas. This plant-root fungal disease results in plant death or significant yield loss. FOV4 enters the plant through root system. Plant cell wall forms the primary barrier against pathogen infection in addition to providing the mechanical support. Plants have several mechanisms, both physical and chemical, to prevent FOV4 infection. While plant cell walls are well-studied, their specific role in FOV4 infection-interaction in cotton is unknown. ARS scientists with university cooperators examined the genes/proteins in FOV4 infected roots and uninfected roots of known resistant and susceptible cotton plants and found biochemical and root cell wall component differences between susceptible and resistant cotton. Resistant cotton plants were able to have fortified roots preventing less or no infection of FOV4. Our results highlight an essential role of certain genes/proteins and create opportunities for gene discovery and the development molecular markers such as SNP for marker-associated selection (MAS) for breeding for FOV4 resistance. This is the first comprehensive report describing the possible fortification of the roots against the attack of FOV4 in resistant cotton. Additionally, this information can be used by researchers involved in developing Pima and Upland cotton resistant to Fusarium wilt or FOV4.

Technical Abstract: 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. 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, phenylpropanoid biosynthesis and metabolism, ABC-type transporter activity, lipid metabolism, regulation of enzymatic activity, diterpenoid biosynthetic processes, and phytohormone signaling-related processes. 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. The MS Peak-to-Pathway analysis identified differences related to secondary metabolism, specifically to the phenylpropanoid pathway, in which enhanced levels of a set of metabolites for plant development and environmental adaptation are present in resistant Pima-S6 compared to susceptible genotypes (Pima S-7 and 3-79). Some genes of this pathway were found to be in chromosome-QTL regions linked with resistance to FOV4. Our results highlight an essential role for the phenylpropanoid synthesis pathway and create opportunities for gene discovery and SNP development for marker-associated selection (MAS) for breeding for FOV4 resistance.