The GATA‐type IVb zinc‐finger transcription factor SsNsd1 regulates asexual–sexual development and appressoria formation in Sclerotinia sclerotiorum

Abstract

The sclerotium, a multicellular structure composed of the compact aggregation of vegetative hyphae, is critical for the long-term survival and sexual reproduction of the plant-pathogenic fungus Sclerotinia sclerotiorum. The development and carpogenic germination of sclerotia are regulated by integrating signals from both environmental and endogenous processes. Here, we report the regulatory functions of the S. sclerotiorum GATA-type IVb zinc-finger transcription factor SsNsd1 in these processes. SsNsd1 is orthologous to the Aspergillus nidulans NsdD (never in sexual development) and the Neurospora crassa SUB-1 (submerged protoperithecia-1) proteins. Ssnsd1 gene transcript accumulation remains relatively low, but variable, during vegetative mycelial growth and multicellular development. Ssnsd1 deletion mutants (Δnsd1-KOs) produce phialides and phialospores (spermatia) excessively in vegetative hyphae and promiscuously within the interior medulla of sclerotia. In contrast, phialospore development occurs only on the sclerotium surface in the wild-type. Loss of SsNsd1 function affects sclerotium structural integrity and disrupts ascogonia formation during conditioning for carpogenic germination. As a consequence, apothecium development is abolished. The Ssnsd1 deletion mutants are also defective in the transition from hyphae to compound appressorium formation, resulting in a loss of pathogenicity on unwounded hosts. In sum, our results demonstrate that SsNsd1 functions in a regulatory role similar to its ascomycete orthologues in regulating sexual and asexual development. Further, SsNsd1 appears to have evolved as a regulator of pre-penetration infectious development required for the successful infection of its many hosts.

Transcription Factor NsdD Regulates the Expression of Genes Involved in Plant Biomass-Degrading Enzymes, Conidiation, and Pigment Biosynthesis in Penicillium oxalicum

“…NsdD and its orthologues are identified as TFs with the conserved DNA-binding domain ZnF_GATA in many filamentous fungi (22)(23)(24)(25)(26)(27)(28)(29). Hitherto in the reported literature and this work, NsdD and its orthologues primarily played six roles, including (i) repressing asexual development in Aspergillus spp.…”

“…Hitherto in the reported literature and this work, NsdD and its orthologues primarily played six roles, including (i) repressing asexual development in Aspergillus spp. (25,29), F. fujikuroi (27), S. sclerotiorum (28), and P. oxalicum; (ii) activating sexual development in Aspergillus nidulans (22), S. sclerotiorum (28), and S. macrospora (24); (iii) affecting the production of secondary metabolites, such as the dark mycelial pigment and gliotoxin in Aspergillus spp., under specific conditions (25,29); synthesizing the polyketide synthase (PKS)derived pigments in F. fujikuroi (27) and P. oxalicum; (iv) regulating light responses in N. crassa (23) and B. cinerea (26); (v) regulating fungal virulence in the necrotrophic plant pathogen B. cinerea (26); and (vi) regulating the production of plant biomassdegrading enzymes and the expression of these enzyme genes in P. oxalicum, as identified previously (30) and in this study.…”

“…NsdD in Aspergillus spp. and its orthologs, such as Pro44 in Sordaria macrospora, Ltf1 in Botrytis cinerea, Csm1 in Fusarium fujikuroi, SUB-1 in Neurospora crassa, and SsNsd1 in Sclerotinia sclerotiorum, regulate development and/or biosynthesis of secondary metabolites (22)(23)(24)(25)(26)(27)(28). Additional functions involving stress tolerance, light response, and virulence have been observed in the plant pathogens B. cinerea, F. fujikuroi, and/or N. crassa (23,26,27).…”

Sclerotinia sclerotiorum Circumvents Flavonoid Defenses by Catabolizing Flavonol Glycosides and Aglycones

“…Relative quantification of wild-type and DSsQDO pathogenicity on Arabidopsis was also achieved through RT-qPCR of the fungal Histone gene (Li et al, 2018) against the Arabidopsis ACTIN gene (Czechowski et al, 2005; Supplemental Table S1). Plant inoculation, RNA isolation, cDNA synthesis, and RT-qPCR were conducted following the protocol described above.…”

Transcription Factor SsSte12 Was Involved in Mycelium Growth and Development in Sclerotinia sclerotiorum

“…For example, controlling the sclerotinia diseases by suppressing sclerotia formation could reduce new infections by interfering with the life cycle. Importantly, lost the capacity to produce normal sclerotia in these pathogens attenuate their virulence or the ability to cause disease ( Rollins, 2003 ; Erental et al, 2007 ; Li et al, 2017 ). Understanding the relationship between sclerotia development and pathogenicity may provide insights into the genetic links between fungal development and pathogenicity.…”