Abstract

Banana Fusarium wilt (BFW), which is one of the most important banana diseases worldwide, is mainly caused by Fusarium oxysporum f. sp. cubense tropic race 4 (Foc TR4). In this study, we conducted secretome analysis of Foc R1 and Foc TR4 and discovered a total of 120 and 109 secretory proteins (SPs) from Foc R1 cultured alone or with banana roots, respectively, and 129 and 105 SPs respectively from Foc TR4 cultured under the same conditions. Foc R1 and Foc TR4 shared numerous SPs associated with hydrolase activity, oxidoreductase activity, and transferase activity. Furthermore, in culture with banana roots, Foc R1 and Foc TR4 secreted many novel SPs, of which approximately 90% (Foc R1; 57/66; Foc TR4; 50/55) were unconventional SPs without signal peptides. Comparative analysis of SPs in Foc R1 and Foc TR4 revealed that Foc TR4 not only generated more specific SPs but also had a higher proportion of SPs involved in various metabolic pathways, such as phenylalanine metabolism and cysteine and methionine metabolism. The cysteine biosynthesis enzyme O-acetylhomoserine (thiol)-lyase (OASTL) was the most abundant root inducible Foc TR4-specific SP. In addition, knockout of the OASTL gene did not affect growth of Foc TR4; but resulted in the loss of pathogenicity in banana ‘Brazil’. We speculated that OASTL functions in banana by interfering with the biosynthesis of cysteine, which is the precursor of an enormous number of sulfur-containing defense compounds. Overall, our studies provide a basic understanding of the SPs in Foc R1 and Foc TR4; including a novel effector in Foc TR4.

Highlights

  • During the last century, the banana crop industry has experienced dramatic losses due to an epidemic of banana Fusarium wilt (BFW), caused by Fusarium oxysporum f. sp. cubense race 1 (Foc R1), which has more recently been intensified by Foc tropical race 4 (Foc TR4) in Cavendish banana [1]

  • We identified the secretory proteins (SPs) produced by Foc R1 and Foc TR4, and expected to find out some relationships between the SPs and the pathogenicity of Foc TR4

  • Pectin esterase (PE), endoglucanase (BG), arabinase, and a group of glycosidases, such as galactosidase, glucosidase, and arabinofuranosidase were identified among the SPs of both Foc R1 and Foc TR4 (Supplementary Table S1)

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Summary

Introduction

The banana crop industry has experienced dramatic losses due to an epidemic of banana Fusarium wilt (BFW), caused by Fusarium oxysporum f. sp. cubense race 1 (Foc R1), which has more recently been intensified by Foc tropical race 4 (Foc TR4) in Cavendish banana [1]. The mechanism underlying BFW resistance in Cavendish banana at the genetic level is unclear, and biological control remains the mainstream to method of control [2]. Pathogens generate secretory proteins (SPs) that are critical for infection of the host and function in processes including degradation of the cell wall and biomacromolecules as well as contributing to modulation of metabolic processes and immune responses [3,4]. AvrE-family Type-III effector proteins (T3Es) contribute to the virulence of multiple plant-pathogenic species by disturbing pathogen-associated molecular pattern-triggered immunity (PTI) via direct interaction with the B’ regulatory subunits of phosphatase 2A (PP2A) heterotrimeric enzyme complexes [5]. Avr3a-like effectors from Phytophthora spp. were shown to target the plant cinnamyl alcohol dehydrogenase 7 (CAD7) subfamily members to enhance the suppression of PTI functions, including callose deposition, reactive oxygen species burst, and WRKY33 expression [7]. The secreted fungal chorismate mutase, Cmu, is thought to affect biosynthesis of the plant immune signal salicylic acid by channeling chorismate into the phenylpropanoid pathway, and a maize-encoded kiwellin, ZmKWL1, targets and blocks the catalytic activity of Cmu1 [9]

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