UvSorA and UvSorB Involved in Sorbicillinoid Biosynthesis Contribute to Fungal Development, Stress Response and Phytotoxicity in Ustilaginoidea virens

Abstract

Ustilaginoidea virens (teleomorph: Villosiclava virens) is an important fungal pathogen that causes a devastating rice disease. It can produce mycotoxins including sorbicillinoids. The biosynthesis and biological functions of sorbicillinoids have not been reported in U. virens. In this study, we identified a sorbicillinoid biosynthetic gene cluster in which two polyketide synthase genes UvSorA and UvSorB were responsible for sorbicillinoid biosynthesis in U. virens. In ∆UvSorA and ∆UvSorB mutants, the mycelial growth, sporulation and hyphal hydrophobicity were increased dramatically, while the resistances to osmotic pressure, metal cations, and fungicides were reduced. Both phytotoxic activity of rice germinated seeds and cell wall integrity were also reduced. Furthermore, mycelia and cell walls of ∆UvSorA and ∆UvSorB mutants showed alterations of microscopic and submicroscopic structures. In addition, feeding experiment showed that sorbicillinoids could restore mycelial growth, sporulation, and cell wall integrity in ∆UvSorA and ∆UvSorB mutants. The results demonstrated that both UvSorA and UvSorB were responsible for sorbicillinoid biosynthesis in U. virens, and contributed to development (mycelial growth, sporulation, and cell wall integrity), stress responses, and phytotoxicity through sorbicillinoid mediation. It provides an insight into further investigation of biological functions and biosynthesis of sorbicillinoids.

UvHOS3‐mediated histone deacetylation is essential for virulence and negatively regulates ustilaginoidin biosynthesis in Ustilaginoidea virens

“…The culture of U. virens generates multiple types of mycotoxins, such as ustilaginoidins and sorbicillinoids (Liu, Wang, et al., 2023 ; Zhang, Xu, et al., 2022 ). The mycotoxin biosynthesis‐related genes in DEGs are summarized in Table S7 .…”

“…The mycotoxin biosynthesis‐related genes in DEGs are summarized in Table S7 . Interestingly, the sorbicillinoid biosynthesis genes UV8b_03315 ( UvSorC ), UV8b_03319 ( UvSorT ), UV8b_03320 ( UvSorR2 ), UV8b_03321 ( UvSorA ) and UV8b_03322 ( UvSorB ) (Lai et al., 2019 ; Zhang, Xu, et al., 2022 ), isoquinoline alkaloid biosynthesis genes UV8b_06024 and UV8b_06025 and ustilaginoidin biosynthesis‐related genes UV8b_01133 ( UV_2085 ), UV8b_01134 ( UvPKS1 ), UV8b_01135 ( UgsZ ), UV8b_01136 ( UgsT ), UV8b_01137 ( UgsH ), UV8b_01138 ( UgsJ ) and UV8b_01139 ( UgsL ) (Li et al., 2019 ) were significantly upregulated in the Δ Uvhos3‐ 1 mutant (Figure 6c ). Elevated expression of ustilaginoidin biosynthesis genes explains why the Δ Uvhos3 mutant generates more ustilaginoidins.…”

“…(UvSorB) (Lai et al, 2019;Zhang, Xu, et al, 2022), isoquinoline alkaloid biosynthesis genes UV8b_06024 and UV8b_06025 and ustilaginoidin biosynthesis-related genes UV8b_01133 (UV_2085),…”

Activation of Ustilaginoidin Biosynthesis Gene uvpks1 in Villosiclava virens Albino Strain LN02 Influences Development, Stress Responses, and Inhibition of Rice Seed Germination

“…The conidia were obtained via the filtration of the culture broths after the fungal strains were cultured in PSB medium at 28 • C for 7 days. The conidia quantity and germination rates were determined with an optical microscope and a hemocytometer according to previously described methods [12][13][14].…”

A Berberine Bridge Enzyme-like Oxidase Mediates the Cage-like Acresorbicillinol C Biosynthesis

“…Structurally various sorbicillinoids are synthesized from the key monomeric sorbicillinol ( 1 ), which can react with itself and other compounds on the basis of its dienophile and dual diene character, and these dimers are classified as bisvertinols, cage-like, and bridged bicycle-like sorbicillinoids according to the connectivity of the dual reactivity of 1 (Figure A). The biosynthesis of sorbicillinoids starts with the cooperation of hrPKS (highly reducing iterative polyketide synthase, SorA) and nrPKS (nonreducing iterative polyketide synthase, SorB) to form the core backbone of sorbicillin and dihydrosorbicillin ( 2a and 2b , respectively), and then oxidative dearomatization is mediated by a FAD-dependent monooxygenase (FMO) SorC to synthesize 1 or dihydrosorbicillinol ( 1a ). − …”