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Transcriptomic Analysis Reveals Candidate Genes Responding Maize Gray Leaf Spot Caused by Cercospora zeina.

ABSTRACT: Gray leaf spot (GLS), caused by the fungal pathogen Cercospora zeina (C. zeina), is one of the most destructive soil-borne diseases in maize (Zea mays L.), and severely reduces maize production in Southwest China. However, the mechanism of resistance to GLS is not clear and few resistant alleles have been identified. Two maize inbred lines, which were shown to be resistant (R6) and susceptible (S8) to GLS, were injected by C. zeina spore suspensions. Transcriptome analysis was carried out with leaf tissue at 0, 6, 24, 144, and 240 h after inoculation. Compared with 0 h of inoculation, a total of 667 and 419 stable common differentially expressed genes (DEGs) were found in the resistant and susceptible lines across the four timepoints, respectively. The DEGs were usually enriched in 'response to stimulus' and 'response to stress' in GO term analysis, and 'plant-pathogen interaction', 'MAPK signaling pathways', and 'plant hormone signal transduction' pathways, which were related to maize's response to GLS, were enriched in KEGG analysis. Weighted-Genes Co-expression Network Analysis (WGCNA) identified two modules, while twenty hub genes identified from these indicated that plant hormone signaling, calcium signaling pathways, and transcription factors played a central role in GLS sensing and response. Combing DEGs and QTL mapping, five genes were identified as the consensus genes for the resistance of GLS. Two genes, were both putative Leucine-rich repeat protein kinase family proteins, specifically expressed in R6. In summary, our results can provide resources for gene mining and exploring the mechanism of resistance to GLS in maize.

SUBMITTER: He W

PROVIDER: S-EPMC8625984 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Gray leaf spot (GLS) is a globally important foliar disease of maize. Cercospora zeina, one of the two fungal species that cause the disease, is prevalent in southern Africa, China, Brazil and the eastern corn belt of the USA. Identification of QTL for GLS resistance in subtropical germplasm is important to support breeding programmes in developing countries where C.?zeina limits production of this staple food crop. RESULTS: A maize RIL population (F7:S6) from a cross between CML444 and SC Malawi was field-tested under GLS disease pressure at five field sites over three seasons in KwaZulu-Natal, South Africa. Thirty QTL identified from eleven field trials (environments) were consolidated to seven QTL for GLS resistance based on their expression in at least two environments and location in the same core maize bins. Four GLS resistance alleles were derived from the more resistant parent CML444 (bin 1.10, 4.08, 9.04/9.05, 10.06/10.07), whereas the remainder were from SC Malawi (bin 6.06/6.07, 7.02/7.03, 9.06). QTLs in bin 4.08 and bin 6.06/6.07 were also detected as joint QTLs, each explained more than 11% of the phenotypic variation, and were identified in four and seven environments, respectively. Common markers were used to allocate GLS QTL from eleven previous studies to bins on the IBM2005 map, and GLS QTL "hotspots" were noted. Bin 4.08 and 7.02/7.03 GLS QTL from this study overlapped with hotspots, whereas the bin 6.06/6.07 and bin 9.06 QTLs appeared to be unique. QTL for flowering time (bin 1.07, 4.09) in this population did not correspond to QTL for GLS resistance. CONCLUSIONS: QTL mapping of a RIL population from the subtropical maize parents CML444 and SC Malawi identified seven QTL for resistance to gray leaf spot disease caused by C.?zeina. These QTL together with QTL from eleven studies were allocated to bins on the IBM2005 map to provide a basis for comparison. Hotspots of GLS QTL were identified on chromosomes one, two, four, five and seven, with QTL in the current study overlapping with two of these. Two QTL from this study did not overlap with previously reported QTL.

Project description:BackgroundCercospora zeina is a foliar pathogen responsible for maize grey leaf spot in southern Africa that negatively impacts maize production. Plants use a variety of chemical and structural mechanisms to defend themselves against invading pathogens such as C. zeina, including the production of secondary metabolites with antimicrobial properties. In maize, a variety of biotic and abiotic stressors induce the accumulation of the terpenoid phytoalexins, zealexins and kauralexins.ResultsC. zeina-susceptible line displayed pervasive rectangular grey leaf spot lesions, running parallel with the leaf veins in contrast to C. zeina-resistant line that had restricted disease symptoms. Analysis of the transcriptome of both lines indicated that genes involved in primary and secondary metabolism were up-regualted, and although different pathways were prioritized in each line, production of terpenoid compounds were common to both. Targeted phytoalexin analysis revealed that C. zeina-inoculated leaves accumulated zealexins and kauralexins. The resistant line shows a propensity toward accumulation of the kauralexin B series metabolites in response to infection, which contrasts with the susceptible line that preferentially accumulates the kauralexin A series. Kauralexin accumulation was correlated to expression of the kauralexin biosynthetic gene, ZmAn2 and a candidate biosynthetic gene, ZmKSL2. We report the expression of a putative copalyl diphosphate synthase gene that is induced by C. zeina in the resistant line exclusively.DiscussionThis study shows that zealexins and kauralexins, and expression of their biosynthetic genes, are induced by C. zeina in both resistant and susceptible germplasm adapted to the southern African climate. The data presented here indicates that different forms of kauralexins accumulate in the resistant and susceptible maize lines in response to C. zeina, with the accumulation of kauralexin B compounds in a resistant maize line and kauralexin A compounds accumulating in the susceptible line.

Project description:BackgroundGray leaf spot (GLS), which is caused by the necrotrophic fungi Cercospora zeae-maydis and Cercospora zeina, is one of the most impactful diseases in maize worldwide. The aim of the present study is to identify the resistance genes and understand the molecular mechanisms for GLS resistance.ResultsTwo cultivars, 'Yayu889' and 'Zhenghong532,' which are distinguished as resistant and susceptible cultivars, respectively, were challenged with the GLS disease and a RNA-seq experiment was conducted on infected plants at 81, 89, 91, and 93 days post planting (dap). Compared with the beginning stage at 81 dap, 4666, 1733, and 1166 differentially expressed genes (DEGs) were identified at 89, 91, and 93 dap, respectively, in 'Yayu889,' while relatively fewer, i.e., 4713, 881, and 722 DEGs, were identified in 'Zhenghong532.' Multiple pathways involved in the response of maize to GLS, including 'response to salicylic acid,' 'protein phosphorylation,' 'oxidation-reduction process,' and 'carotenoid biosynthetic process,' were enriched by combining differential expression analysis and Weighted Gene Co-expression Network Analysis (WGCNA). The expression of 12 candidate resistance proteins in these pathways were quantified by the multiple reaction monitoring (MRM) method. This approach identified two candidate resistance proteins, a calmodulin-like protein and a leucine-rich repeat receptor-like protein kinase with SNPs that were located in QTL regions for GLS resistance. Metabolic analysis showed that, compared with 'Zhenghong532,' the amount of salicylic acid (SA) and total carotenoids in 'Yayu889' increased, while peroxidase activity decreased during the early infection stages, suggesting that increased levels of SA, carotenoids, and reactive oxygen species (ROS) may enhance the defense response of 'Yayu889' to GLS.ConclusionBy combining transcriptome and proteome analyses with comparisons of resistance QTL regions, calmodulin-like protein and leucine-rich repeat receptor-like protein kinase were identified as candidate GLS resistance proteins. Moreover, we found that the metabolic pathways for ROS, SA, and carotenoids are especially active in the resistant cultivar. These findings could lead to a better understanding of the GLS resistance mechanisms and facilitate the breeding of GLS-resistant maize cultivars.

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Transcriptomic Analysis Reveals Candidate Genes Responding Maize Gray Leaf Spot Caused by Cercospora zeina.

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