Histone acetylation, balanced by histone acetyltransferase (HAT) and histone deacetylase (HDAC) complexes, affects dynamic transitions of chromatin structure to regulate transcriptional accessibility. However, little is known about the interplay between HAT and HDAC complexes in Fusarium graminearum, a causal agent of Fusarium Head Blight (FHB) that uniquely contains chromosomal regions enriched for house-keeping or infection-related genes. In this study, we identified the ortholog of the human inhibitor of growth (ING1) gene in F. graminearum (FNG1) and found that it specifically interacts with the FgEsa1 HAT of the NuA4 complex. Deletion of FNG1 led to severe growth defects and blocked conidiation, sexual reproduction, DON production, and plant infection. The fng1 mutant was normal in H3 acetylation but significantly reduced in H4 acetylation. A total of 34 spontaneous suppressors of fng1 with faster growth rate were isolated. Most of them were still defective in sexual reproduction and plant infection. Thirty two of them had mutations in orthologs of yeast RPD3, SIN3, and SDS3, three key components of the yeast Rpd3L HDAC complex. Four mutations in these three genes were verified to suppress the defects of fng1 mutant in growth and H4 acetylation. The rest two suppressor strains had a frameshift or nonsense mutation in a glutamine-rich hypothetical protein that may be a novel component of the FgRpd3 HDAC complex in filamentous fungi. FgRpd3, like Fng1, localized in euchromatin. Deletion of FgRPD3 resulted in severe growth defects and elevated H4 acetylation. In contract, the Fgsds3 deletion mutant had only a minor reduction in growth rate but FgSIN3 appeared to be an essential gene. RNA-seq analysis revealed that 48.1% and 54.2% of the genes with altered expression levels in the fng1 mutant were recovered to normal expression levels in two suppressor strains with mutations in FgRPD3 and FgSDS3, respectively. Taken together, our data showed that Fng1 is important for H4 acetylation as a component of the NuA4 complex and functionally related to the FgRpd3 HDAC complex for transcriptional regulation of genes important for growth, conidiation, sexual reproduction, and plant infection in F. graminearum.

Maize (Zea mays L.) is one of the most important food and feed crops in China, with a cultivation area of more than 40 million hectares (http://www.fao.org/faostat/en/#data/QC). In July 2021, a serious maize seeding blight occurred in Changjia Town, Gaoqing Country, Zibo City, Shandong Province, China, and the disease incidence was up to 50% in some fields. The root system of infected plants displayed poor development. The primary roots were brown and rotted. The leaves at the base of the plants were drying up, then the whole plant withered. To determine the cause agent of the disease, symptomatic roots of diseased seedlings were collected and surface-sterilized (70% ethanol for 30 s and 3% sodium hypochlorite (NaClO) for 90 s), subsequently rinsed three times with sterile distilled water, placed on potato dextrose agar (PDA), then incubated at 25°C for 2 days. Two cultures with similar morphological characteristics were purified through single-spore isolation technique and identified by morphology and molecular methods as Fusarium pseudograminearum O'Donnell & T. Aoki 1999. Plentiful macroconidia formed in 5-day-old carboxymethyl cellulose (CMC) cultures; microconidia were absent. Macroconidia were thick-walled and curved, usually 3- to 5- septa, 31.6 ± 0.6 μm × 4.8 ± 0.1 μm (n = 50). Colony pigmentation on PDA was pink to red, with white to pink aerial mycelia on PDA cultures was abundant and filled the petri dishes. For molecular identification, the rDNA internal transcribed spacer (ITS) gene and translation elongation factor 1 alpha (TEF-1α) gene of two isolates (SAIA41B and SAIA41C) were amplified with ITS1/ITS4 (White et al., 1990) and EF-1/EF-2 (O'Donnell et al., 1998), respectively. Blastn analysis of both the ITS sequence (accession numbers OM108101 and OM108102) and TEF-1α sequence (accession numbers OM142205 and OM142206) revealed 100% (481/481 bp for ITS and 637/637 bp for TEF-1α) sequence identity with the sequences of F. pseudograminearum reported in GenBank (MW699613 for ITS and JN862232 for TEF-1α). The molecular identification was further confirmed by the F. pseudograminearum species-specific PCR primers Fp1-1/Fp1-2 (Aoki and O'Donnell 1999). The expected 523-bp fragments were obtained for isolates SAIA41B and SAIA41C. In the pathogenicity test, healthy germinating maize roots (Zhengdan958) were inoculated with PDA culture blocks of isolate SAIA41C. Plants inoculated only with PDA culture blocks served as controls. Maize plants were put in petri dishes and placed in an incubator with a 12-h photoperiod at 25 oC and 100% relative humidity. Seven days later, roots of the plants inoculated with isolate SAIA41C were poorly developed and became brown necrotic and rotted, which were identical to the symptoms observed in the fields, whereas the roots of control plants were developed normally. The pathogen was re-isolated from the necrotic tissue of the inoculated roots but not from the control plants, and its identity was confirmed by PCR with the primes Fp1-1/Fp1-2 described above, fulfilling Koch's Postulates. To our knowledge, this is the first report of maize seedling blight caused by F. pseudograminearum in China. Our finding indicates the potential spread of F. pseudograminearum on maize, and more attention should be paid to prevention and control of maize seedling blight caused by F. pseudograminearum. The author(s) declare no conflict of interest. Acknowledgements: This research was supported by National Natural Science Foundation of China (No. 32102181), Shandong Provincial Natural Science Foundation (No. ZR2021QC059), Wheat Industry Technology System of Shandong Province (No. SDAIT-01-10), and Agricultural Science and Technology Innovation Project of SAAS (No. CXGC2021A38 and CXGC2021A33).

Fusarium head blight (FHB), caused by the fungal pathogen Fusarium graminearum, is a destructive disease worldwide. Ascospores are the primary inoculum of F. graminearum, and sexual reproduction is a critical step in its infection cycle. In this study, we characterized the functions of FgCsn12. Although the ortholog of FgCsn12 in budding yeast was reported to have a direct interaction with Csn5, which served as the core subunit of the COP9 signalosome, the interaction between FgCsn12 and FgCsn5 was not detected through the yeast two-hybrid assay. The deletion of FgCSN12 resulted in slight defects in the growth rate, conidial morphology, and pathogenicity. Instead of forming four-celled, uninucleate ascospores, the Fgcsn12 deletion mutant produced oval ascospores with only one or two cells and was significantly defective in ascospore discharge. The 3′UTR of FgCsn12 was dispensable for vegetative growth but essential for sexual reproductive functions. Compared with those of the wild type, 1204 genes and 2240 genes were up- and downregulated over twofold, respectively, in the Fgcsn12 mutant. Taken together, FgCsn12 demonstrated an important function in the regulation of ascosporogenesis in F. graminearum.

Wheat is a vital global food crop, yet it faces challenges in saline–alkali soils where Fusarium crown rot significantly impacts growth. Variations in wheat growth across regions are often attributed to uneven terrain. To explore these disparities, we examined well-growing and poorly growing wheat samples and their rhizosphere soils. Measurements included wheat height, root length, fresh weight, and Fusarium crown rot severity. Well-growing wheat exhibited greater height, root length, and fresh weight, with a lower Fusarium crown rot disease index compared to poorly growing wheat. Analysis of rhizosphere soil revealed higher alkalinity; lower nutrient levels; and elevated Na, K, and Ca levels in poorly growing wheat compared to well-growing wheat. High-throughput sequencing identified a higher proportion of unique operational taxonomic units (OTUs) in poorly growing wheat, suggesting selection for distinct fungal species under stress. FUNGuild analysis indicated a higher prevalence of pathogenic microbial communities in poorly growing wheat rhizosphere soil. This study underscores how uneven terrains in saline–alkali soils affect pH, nutrient dynamics, mineral content, wheat health, and rhizosphere fungal community structure.