The Verticillium dahliae Sho1‐MAPK pathway regulates melanin biosynthesis and is required for cotton infection

Abstract

Summary Verticillium dahliae is a soil‐borne fungus that causes vascular wilt on numerous plants worldwide. The fungus survives in the soil for up to 14 years by producing melanized microsclerotia. The protective function of melanin in abiotic stresses is well documented. Here, we found that the V. dahliae tetraspan transmembrane protein VdSho1, a homolog of the Saccharomyces cerevisiae Sho1, acts as an osmosensor, and is required for plant penetration and melanin biosynthesis. The deletion mutant ΔSho1 was incubated on a cellophane membrane substrate that mimics the plant epidermis, revealing that the penetration of ΔSho1 strain was reduced compared to the wild‐type strain. Furthermore, VdSho1 regulates melanin biosynthesis by a signalling mechanism requiring a kinase‐kinase signalling module of Vst50‐Vst11‐Vst7. Strains, ΔVst50, ΔVst7 and ΔVst11 also displayed defective penetration and melanin production like the ΔSho1 strain. Defects in penetration and melanin production in ΔSho1 were restored by overexpression of Vst50, suggesting that Vst50 lies downstream of VdSho1 in the regulatory pathway governing penetration and melanin biosynthesis. Data analyses revealed that the transmembrane portion of VdSho1 was essential for both membrane penetration and melanin production. This study demonstrates that Vst50‐Vst11‐Vst7 module regulates VdSho1‐mediated plant penetration and melanin production in V. dahliae, contributing to virulence.

Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.

“…The perception of external signals and an adequate fungal response requires intracellular signaling pathways, which have important functions in development and virulence of Verticillium spp. ( Rauyaree et al, 2005 ; Qi et al, 2016 ; Li et al, 2019 ; Yu et al, 2019 ; Starke et al, 2021 ). Transcriptional changes of the fungus caused during bacterial co-cultivation with P_DAPG in liquid medium revealed that transcripts encoding proteins required for the degradation of pectin as main carbon source of the co-culture medium were among the most down-regulated transcripts within 120 min ( Supplementary Table 5 ).…”

Opportunities and Challenges in Studies of Host-Pathogen Interactions and Management of Verticillium dahliae in Tomatoes

“…Functional studies of the components of different MAP kinase pathways have confirmed the role of these proteins in the pathogenesis in V . dahliae, including a surface sensor (VdMsb) [ 74 ], an osmosensor (VdSho1) in the high osmolarity glycerol (HOG)-MAP kinase signaling pathway [ 75 , 76 ], a Hog1 MAP kinase (VdHog1) [ 77 ], VdPbs2, an upstream component of VdHog1 [ 78 ], Verticillium MAP Kinase 1 (Vmk1) [ 79 ], and MAPKKKs (VdSsk1, VdSsk2, and VdSte11) [ 80 , 81 ]. The deletion of these genes has shown that these MAP kinase cascades are involved in stress adaptation, plant root penetration, and microsclerotia formation in V. dahliae .…”

“…The phylogenetic and comparative genomic analysis suggested clusters in V. dahliae are involved in the biosynthesis of two putative siderophores, ferricrocin and triacetylfusarinine C (TAFC), 1,8-dihydroxynaphthalene (DHN)-melanin and fujikurin [ 90 ]. Melanin, a polyketide, is one of the most thoroughly studied SMs because it is directly linked to fungal cell wall stability and pathogenicity [ 75 , 81 , 91 , 92 , 93 ]. In V. dahliae , black melanin granules are heavily deposited in the cell wall of the survival structure, the microsclerotia [ 94 ].…”

Unfolded Protein Response and Scaffold Independent Pheromone MAP Kinase Signaling Control Verticillium dahliae Growth, Development, and Plant Pathogenesis

“…The pheromone response MAPK pathway plays an important role in the pathogenicity of numerous filamentous fungi [ 51 ]. The V. dahliae pheromone response MAPK pathway includes orthologues to the yeast pathway components (Adapter: Vst50; MAP3K: Vst11; MAP2K: Mek2/Vst7; MAPK: Vmk1; Ste12-like transcription factor: Vph1) and is essential for pathogenicity [ 52 , 53 , 54 , 55 , 56 ]. Vmk1, Mek2, Vst11, and Vst50-deficient mutants display defects in microsclerotia development, whereas resting structure formation is unaffected in a VPH1 deletion strain [ 52 , 53 , 54 , 55 , 56 ].…”