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Genome-Wide Identification and Characterization of RNA/DNA Differences Associated with Fusarium graminearum Infection in Wheat.

ABSTRACT: RNA/DNA difference (RDD) is a post-transcriptional modification playing a crucial role in regulating diverse biological processes in eukaryotes. Although it has been extensively studied in plant chloroplast and mitochondria genomes, RDDs in plant nuclear genomes are not well studied at present. Here, we investigated the RDDs associated with fusarium head blight (FHB) through a novel method by comparing the RNA-seq data between Fusarium-infected and control samples of four wheat genotypes. A total of 187 high-confidence unique RDDs in 36 genes were identified, representing the first landscape of the FHB-responsive RDD in wheat. The majority (26) of these 36 RDD genes were correlated either positively or negatively with FHB levels. Effects of these RDDs on RNA and protein sequences have been identified, their editing frequency and the expression level of the corresponding genes provided, and the prediction of the effect on the minimum folding free energy of mRNA, miRNA binding, and colocation of RDDs with conserved domains presented. RDDs were predicted to induce modifications in the mRNA and protein structures of the corresponding genes. In two genes, TraesCS1B02G294300 and TraesCS3A02G263900, editing was predicted to enhance their affinity with tae-miR9661-5p and tae-miR9664-3p, respectively. To our knowledge, this study is the first report of the association between RDD and FHB in wheat; this will contribute to a better understanding of the molecular basis underlying FHB resistance, and potentially lead to novel strategies to improve wheat FHB resistance through epigenetic methods.

SUBMITTER: Yang G

PROVIDER: S-EPMC9316857 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe mycotoxin producing fungal pathogen Fusarium graminearum is the causal agent of Fusarium head blight (FHB) of small grain cereals in fields worldwide. Although F. graminearum is highly investigated by means of molecular genetics, detailed studies about hyphal development during initial infection stages are rare. In addition, the role of mycotoxins during initial infection stages of FHB is still unknown. Therefore, we investigated the infection strategy of the fungus on different floral organs of wheat (Triticum aestivum L.) under real time conditions by constitutive expression of the dsRed reporter gene in a TRI5prom::GFP mutant. Additionally, trichothecene induction during infection was visualised with a green fluorescent protein (GFP) coupled TRI5 promoter. A tissue specific infection pattern and TRI5 induction were tested by using different floral organs of wheat. Through combination of bioimaging and electron microscopy infection structures were identified and characterised. In addition, the role of trichothecene production for initial infection was elucidated by a ΔTRI5-GFP reporter strain.ResultsThe present investigation demonstrates the formation of foot structures and compound appressoria by F. graminearum. All infection structures developed from epiphytic runner hyphae. Compound appressoria including lobate appressoria and infection cushions were observed on inoculated caryopses, paleas, lemmas, and glumes of susceptible and resistant wheat cultivars. A specific trichothecene induction in infection structures was demonstrated by different imaging techniques. Interestingly, a ΔTRI5-GFP mutant formed the same infection structures and exhibited a similar symptom development compared to the wild type and the TRI5prom::GFP mutant.ConclusionsThe different specialised infection structures of F. graminearum on wheat florets, as described in this study, indicate that the penetration strategy of this fungus is far more complex than postulated to date. We show that trichothecene biosynthesis is specifically induced in infection structures, but is neither necessary for their development nor for formation of primary symptoms on wheat.

Project description:BackgroundFusarium graminearum virus 1 strain-DK21 (FgV1-DK21) is a mycovirus that confers hypovirulence to F. graminearum, which is the primary phytopathogenic fungus that causes Fusarium head blight (FHB) disease in many cereals. Understanding the interaction between mycoviruses and plant pathogenic fungi is necessary for preventing damage caused by F. graminearum. Therefore, we investigated important cellular regulatory processes in a host containing FgV1-DK21 as compared to an uninfected parent using a transcriptional approach.ResultsUsing a 3'-tiling microarray covering all known F. graminearum genes, we carried out genome-wide expression analyses of F. graminearum at two different time points. At the early point of growth of an infected strain as compared to an uninfected strain, genes associated with protein synthesis, including ribosome assembly, nucleolus, and ribosomal RNA processing, were significantly up-regulated. In addition, genes required for transcription and signal transduction, including fungal-specific transcription factors and cAMP signaling, respectively, were actively up-regulated. In contrast, genes involved in various metabolic pathways, particularly in producing carboxylic acids, aromatic amino acids, nitrogen compounds, and polyamines, showed dramatic down-regulation at the early time point. Moreover, genes associated with transport systems localizing to transmembranes were down-regulated at both time points.ConclusionThis is the first report of global change in the prominent cellular pathways in the Fusarium host containing FgV1-DK21. The significant increase in transcripts for transcription and translation machinery in fungal host cells seems to be related to virus replication. In addition, significant down-regulation of genes required for metabolism and transporting systems in a fungal host containing the virus appears to be related to the host defense mechanism and fungal virulence. Taken together, our data aid in the understanding of how FgV1-DK21 regulates the transcriptional reprogramming of F. graminearum.

Project description:BackgroundFusarium head blight (FHB) of wheat caused by Fusarium graminearum species complex (FGSC) is a devastating disease worldwide. The pathogens not only reduce the yield of wheat, but also impact the quality of wheat by contamination with trichothecene mycotoxins. A systematic investigation on the pathogens of FHB in Taiwan is lacking. Here, molecular and morphological approaches were used to identify species of the Taiwanese FGSC isolates and determine their trichothecene genotypes.ResultsIn this study, a total of 195 isolates of FGSC from diseased wheat were collected from 8 areas of northern and central Taiwan. All isolates were subjected to seedling inoculation for verification of pathogenicity. The pathogenic isolates were genetically characterized by sequence characterized amplified region (SCAR), PCR- restriction fragment length polymorphism (RFLP), phylogenetic analysis and fixed nucleotides to clarify their phylogenetic species, and by PCR assays of TRI genes to determine trichothecene genotypes. They were identified as F. asiaticum, F. graminearum sensu stricto, F. meridionale and an unknown species. Isolates of F. asiaticum were the major causal agents (98%) in this investigated population and were comprised of SCAR type 5 (75%), SCAR type 4 (21%) and SCAR type 3 (2%). Their trichothecene genotypes were either 15-acetyl-deoxynivalenol (15-ADON) (83%) or nivalenol (NIV) genotype (17%). These genetic characterizations indicated that F. asiaticum (15-ADON SCAR type 5) accounts for 60% of this Taiwanese population. Virulence assay on wheat heads indicated virulence of F. asiaticum isolates in subpopulations divided by SCAR types or trichothecene genotypes were comparable, suggesting other factors influence the unequal subpopulation sizes.ConclusionsThis is the first study that FGSC isolates in Taiwan were systematically collected and characterized. In addition to F. graminearum sensu stricto and F. meridionale, F. asiaticum with 15-ADON genotype was identified as the predominate species in Taiwan. In contrast to Chinese and Japanese populations that F. asiaticum isolates were typically of 3-ADON or NIV genotype, the predominate 15-ADON genotype in Taiwanese population was unique among F. asiaticum populations and represented the southernmost 15-ADON genotype population in East Asia.

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Genome-Wide Identification and Characterization of RNA/DNA Differences Associated with Fusarium graminearum Infection in Wheat.

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