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Complexity of Brassica oleracea-Alternaria brassicicola Susceptible Interaction Reveals Downregulation of Photosynthesis at Ultrastructural, Transcriptional, and Physiological Levels.

ABSTRACT: Black spot disease, caused by Alternaria brassicicola in Brassica species, is one of the most devastating diseases all over the world, especially since there is no known fully resistant Brassica cultivar. In this study, the visualization of black spot disease development on Brassica oleracea var. capitata f. alba (white cabbage) leaves and subsequent ultrastructural, molecular and physiological investigations were conducted. Inter- and intracellular hyphae growth within leaf tissues led to the loss of host cell integrity and various levels of organelle disintegration. Severe symptoms of chloroplast damage included the degeneration of chloroplast envelope and grana, and the loss of electron denseness by stroma at the advanced stage of infection. Transcriptional profiling of infected leaves revealed that photosynthesis was the most negatively regulated biological process. However, in infected leaves, chlorophyll and carotenoid content did not decrease until 48 hpi, and several chlorophyll a fluorescence parameters, such as photosystem II quantum yield (Fv/Fm), non-photochemical quenching (NPQ), or plant vitality parameter (Rdf) decreased significantly at 24 and 48 hpi compared to control leaves. Our results indicate that the initial stages of interaction between B. oleracea and A. brassicicola are not uniform within an inoculation site and show a complexity of host responses and fungal attempts to overcome host cell defense mechanisms. The downregulation of photosynthesis at the early stage of this susceptible interaction suggests that it may be a part of a host defense strategy, or, alternatively, that chloroplasts are targets for the unknown virulence factor(s) of A. brassicicola. However, the observed decrease of photosynthetic efficiency at the later stages of infection is a result of the fungus-induced necrotic lesion expansion.

SUBMITTER: Macioszek VK

PROVIDER: S-EPMC7593931 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Complexity of Brassica oleracea-Alternaria brassicicola Susceptible Interaction Reveals Downregulation of Photosynthesis at Ultrastructural, Transcriptional, and Physiological Levels.

Macioszek Violetta Katarzyna VK Gapińska Magdalena M Zmienko Agnieszka A Sobczak Mirosław M Skoczowski Andrzej A Oliwa Jakub J Kononowicz Andrzej Kiejstut AK

Cells 20201020 10

Black spot disease, caused by Alternaria brassicicola in Brassica species, is one of the most devastating diseases all over the world, especially since there is no known fully resistant Brassica cultivar. In this study, the visualization of black spot disease development on Brassica oleracea var. capitata f. alba (white cabbage) leaves and subsequent ultrastructural, molecular and physiological investigations were conducted. Inter- and intracellular hyph ...[more]

PMID: 33092216

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Project description:Alternaria blight is a devastating disease that causes significant crop losses in oilseed Brassicas every year. Adoption of conventional breeding to generate disease-resistant varieties has so far been unsuccessful due to the lack of suitable resistant source germplasms of cultivated Brassica spp. A thorough understanding of the molecular basis of resistance, as well as the identification of defense-related genes involved in resistance responses in closely related wild germplasms, would substantially aid in disease management. In the current study, a comparative transcriptome profiling was performed using Illumina based RNA-seq to detect differentially expressed genes (DEGs) specifically modulated in response to Alternaria brassicicola infection in resistant Sinapis alba, a close relative of Brassicas, and the highly susceptible Brassica rapa. The analysis revealed that, at 48 hpi (hours post inoculation), 3396 genes were upregulated and 23239 were downregulated, whereas at 72 hpi, 4023 genes were upregulated and 21116 were downregulated. Furthermore, a large number of defense response genes were detected to be specifically regulated as a result of Alternaria infection. The transcriptome data was validated using qPCR-based expression profiling for selected defense-related DEGs, that revealed significantly higher fold change in gene expression in S. alba when compared to B. rapa. Expression of most of the selected genes was elevated across all the time points under study with significantly higher expression towards the later time point of 72 hpi in the resistant germplasm. S. alba activates a stronger defense response reaction against the disease by deploying an array of genes and transcription factors involved in a wide range of biological processes such as pathogen recognition, signal transduction, cell wall modification, antioxidation, transcription regulation, etc. Overall, the study provides new insights on resistance of S. alba against A. brassicicola, which will aid in devising strategies for breeding resistant varieties of oilseed Brassica.

Project description:Indian mustard (Brassica juncea) is an important oilseed crop in India. Alternaria leaf spot (Alternaria blight) is incited by the fungus Alternaria brassicicola. It majorly affects crop production leading to a yield loss of up to 70%. To circumvent this problem, the study of the resistance mechanism and identification of biochemical markers is one of the important strategies for its management. In the present study, a total of 219 genotypes of Indian mustard with check were screened for Alternaria blight over two seasons. Based on the area under the disease progress curve (AUDPC) scores, ten consistently performing genotypes were selected for the screening of biochemical and yield attributes under artificial inoculated conditions of Alternaria brassicicola (Berk) Sacc. The result showed a negative correlation between disease and yield attributes. The catalase (CAT) activity was significantly increased in resistant genotypes compared to susceptible ones, indicating the crucial role of CAT in the resistance mechanism. Pathogen infection also increases the total protein content and the Alternaria-resistant genotype showed the highest total soluble protein while the susceptible genotype showed the lowest total soluble protein. The ten genotypes were categorized by SSI (stress susceptibility index) and Varuna was identified as a tolerant genotype and Giriraj as a susceptible genotype for Alternaria brassicicola (Berk) Sacc. Varuna and Giriraj were chosen for quantitative analysis of methionine and tryptophan amino acids from seeds using RP-HPLC (Reverse Phase-High Performance Liquid Chromatography) and there were significant differences in the levels of methionine and tryptophan between the Varuna and Giriraj genotypes. Varuna showed higher methionine and tryptophan content compared to the Giriraj genotype. Higher protein content demonstrated an increase in biotic stress-responsive amino acids, such as methionine and tryptophan, suggesting increased resistance to Alternaria diseases in these high-protein genotypes. These amino acids could be used as biochemical markers for Alternaria resistance of mustard.

Project description:BACKGROUND:Alternaria blight, a recalcitrant disease caused by Alternaria brassicae and Alternaria brassicicola, has been recognized for significant losses of oilseed crops especially rapeseed-mustard throughout the world. Till date, no resistance source is available against the disease; hence, plant breeding methods cannot be used to develop disease-resistant varieties. Therefore, in the present study, efforts have been made to identify resistance and defense-related genes as well as key components of JA-SA-ET-mediated pathway involved in resistance against Alternaria brasscicola through computational analysis of microarray data and network biology approach. Microarray profiling data from wild type and mutant Arabidopsis plants challenged with Alternaria brassicicola along with control plant were obtained from the Gene Expression Omnibus (GEO) database. The data analysis, including DEGs extraction, functional enrichment, annotation, and network analysis, was used to identify genes associated with disease resistance and defense response. RESULTS:A total of 2854 genes were differentially expressed in WT9C9; among them, 1327 genes were upregulated and 1527 genes were downregulated. A total of 1159 genes were differentially expressed in JAM9C9; among them, 809 were upregulated and 350 were downregulated. A total of 2516 genes were differentially expressed in SAM9C9; among them, 1355 were upregulated and 1161 were downregulated. A total of 1567 genes were differentially expressed in ETM9C9; among them, 917 were upregulated and 650 were downregulated. Besides, a total of 2965 genes were differentially expressed in contrast WT24C24; among them, 1510 genes were upregulated and 1455 genes were downregulated. A total of 4598 genes were differentially expressed in JAM24C24; among them, 2201 were upregulated and 2397 were downregulated. A total of 3803 genes were differentially expressed in SAM24C24; among them, 1819 were upregulated and 1984 were downregulated. A total of 4164 genes were differentially expressed in ETM24C24; among them, 1895 were upregulated and 2269 were downregulated. The upregulated genes of Arabidopsis thaliana were mapped and annotated with CDS sequences of Brassica rapa obtained from PlantGDB database. Additionally, PPI network of these genes were constructed to investigate the key components of hormone-mediated pathway involved in resistance during pathogenesis. CONCLUSION:The obtained information from present study can be used to engineer resistance to Alternaria blight caused by Alternaria brasscicola through molecular breeding or genetic manipulation-based approaches for improving Brassica oilseed productivity.

Dataset Information

Complexity of Brassica oleracea-Alternaria brassicicola Susceptible Interaction Reveals Downregulation of Photosynthesis at Ultrastructural, Transcriptional, and Physiological Levels.

Publications

Complexity of <i>Brassica oleracea</i>-<i>Alternaria brassicicola</i> Susceptible Interaction Reveals Downregulation of Photosynthesis at Ultrastructural, Transcriptional, and Physiological Levels.

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