Quantitative proteomics analysis reveals resistance differences of banana cultivar 'Brazilian' to Fusarium oxysporum f. sp. cubense races 1 and 4.

Banana Fusarium wilt, caused by Fusarium oxysporum f. sp. cubense (Foc), is one of the most devastating diseases in banana production. Foc is classified into three physiological races. However, the resistance mechanisms of banana against different Foc races are poorly understood. In this study, we performed a comparative proteomics analysis to investigate the resistance mechanisms of 'Brazilian' against Foc1 and Foc4. The proteomes of 'Brazilian' roots inoculated with Foc1 and Foc4 and mock inoculated control at 48 h were analyzed using TMT based quantitative analysis technique. A total of 7325 unique protein species were identified, of which 689, 744, and 1222 protein species were differentially accumulated in Foc1 vs. CK, Foc4 vs. CK, and Foc1 vs. Foc4, respectively. The differential accumulations of candidate protein species were further confirmed by RT-qPCR, PRM, and physiological and biochemical assays. Bioinformatics analysis revealed that the differentially abundance protein species (DAPS) related to pattern recognition receptors, plant cell wall modification, redox homeostasis, and defense responses were differentially accumulated after Foc1 and Foc4 infection, suggesting that 'Brazilian' differed in resistance to the two Foc races. Our study lay the foundation for an in-depth understanding of the interaction between bananas and Foc at the proteome level. SIGNIFICANCE: The banana fusarium wilt disease is one of the most destructive disease of banana and is caused by Fusarium oxysporum f. sp. cubense (Foc). Foc is classified into three physiological races, namely, Foc1, Foc2, and Foc4. Among these races, Foc1 and Foc4 are widely distributed in south China and significantly lose yield. Although both physiological races (Foc1 and Foc4) can invade the Cavendish banana cultivar 'Brazilian', they have significant pathogenicity differences. Unfortunately, how the resistance differences are produced between two races is still largely unclear to date. In this study, we addressed this issue by performing TMT-based comparative quantitative proteomics analysis of 'Brazilian' roots after inoculation with Foc1 and Foc4 as well as sterile water as the control. We revealed that the series of protein species associated with pattern recognition receptors, plant cell wall modification, redox homeostasis, pathogenesis, phytohormones and signal transduction, plant secondary metabolites and programmed cell death etc. were involved in the response to Foc infection. Notably, the potential role of lipid signaling in banana defense against Foc are not reported previously but rather unveiled for the first time in this study. The current study represents the most extensive analysis of the protein profile of 'Brazilian' in response to Foc inoculation and includes for the first time the results from comparison quantitative proteomics analysis between plants inoculated with a pathogenic strain Foc4 and a nonpathogenic strain Foc1 of 'Brazilian', which will lay the foundation for an in-depth understanding of the interaction between bananas and Foc at the proteome level.

Histological and Gene Expression Analyses in Banana Reveals the Pathogenic Differences between Races 1 and 4 of Banana Fusarium Wilt Pathogen.

Fusarium oxysporum f. sp. cubense, the causative agent of Panama disease, is classified into three races: Foc1, Foc2, and Foc4. However, the histological characteristics, the accumulation of fusaric acid (FA), and resistant gene expression in banana infected with different races remain unclear. In this study, we compared the infection processes, FA contents, and gene expression levels in a Cavendish banana cultivar (Musa AAA Brazilian) inoculated with Foc1 and Foc4. Results showed that Foc4 can rapidly extend from the roots to the leaves, whereas Foc1 expands slowly from the roots to the rhizomes but cannot expand further upward. In addition, the colonization of plants by Foc4 was significantly higher compared with Foc1, as was the content of FA in those infected plant tissues. We observed that a large amount of starch granules was produced in the rhizomes and the number of starch granules was significantly higher after infection with Foc1 than after infection with Foc4. We further found that starch has an important inhibitory effect on the phytotoxicity induced by FA, thus leading to more resistance to the pathogens in the plants with high amounts of starch accumulation than in those with a low amount of starch accumulation. Moreover, the expression levels of 10 defense-related genes were analyzed and the results showed that the induction levels of those genes were higher after infection with Foc1 than after infection with Foc4. These results suggest that the observed differences in the invasion of host tissues and FA accumulation, and the number of starch granules and expression of defense-related genes, may contribute to a difference in virulence between the two races and the resulting difference in host resistance response, respectively.