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      Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani

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          Abstract

          Background

          Early blight, caused by the necrotrophic fungal pathogen Alternaria solani, is an economically important disease affecting the tuber yield worldwide. The disease is mainly controlled by chemical plant protection agents. However, over-using these chemicals can lead to the evolution of resistant A. solani strains and is environmentally hazardous. Identifying genetic disease resistance factors is crucial for the sustainable management of early blight but little effort has been diverted in this direction. Therefore, we carried out transcriptome sequencing of the A. solani interaction with different potato cultivars with varying levels of early blight resistance to identify key host genes and pathways in a cultivar-specific manner.

          Results

          In this study, we have captured transcriptomes from three different potato cultivars with varying susceptibility to A. solani,  namely Magnum Bonum, Désirée, and Kuras, at 18 and 36 h post-infection. We identified many differentially expressed genes (DEGs) between these cultivars, and the number of DEGs increased with susceptibility and infection time. There were 649 transcripts commonly expressed between the potato cultivars and time points, of which 627 and 22 were up- and down-regulated, respectively. Interestingly, overall the up-regulated DEGs were twice in number as compared to down-regulated ones in all the potato cultivars and time points, except Kuras at 36 h post-inoculation. In general, transcription factor families WRKY, ERF, bHLH, MYB, and C2H2 were highly enriched DEGs, of which a significant number were up-regulated. The majority of the key transcripts involved in the jasmonic acid and ethylene biosynthesis pathways were highly up-regulated. Many transcripts involved in the mevalonate (MVA) pathway, isoprenyl-PP, and terpene biosynthesis were also up-regulated across the potato cultivars and time points. Compared to Magnum Bonum and Désirée, multiple components of the photosynthesis machinery, starch biosynthesis and degradation pathway were down-regulated in the most susceptible potato cultivar, Kuras.

          Conclusions

          Transcriptome sequencing identified many differentially expressed genes and pathways, thereby contributing to the improved understanding of the interaction between the potato host and A. solani. The transcription factors identified are attractive targets for genetic modification to improve potato resistance against early blight. The results provide important insights into the molecular events at the early stages of disease development, help to shorten the knowledge gap, and support potato breeding programs for improved early blight disease resistance.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12870-023-04135-9.

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          Most cited references82

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          Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

          In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
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            Trimmomatic: a flexible trimmer for Illumina sequence data

            Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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              KEGG: kyoto encyclopedia of genes and genomes.

              M Kanehisa (2000)
              KEGG (Kyoto Encyclopedia of Genes and Genomes) is a knowledge base for systematic analysis of gene functions, linking genomic information with higher order functional information. The genomic information is stored in the GENES database, which is a collection of gene catalogs for all the completely sequenced genomes and some partial genomes with up-to-date annotation of gene functions. The higher order functional information is stored in the PATHWAY database, which contains graphical representations of cellular processes, such as metabolism, membrane transport, signal transduction and cell cycle. The PATHWAY database is supplemented by a set of ortholog group tables for the information about conserved subpathways (pathway motifs), which are often encoded by positionally coupled genes on the chromosome and which are especially useful in predicting gene functions. A third database in KEGG is LIGAND for the information about chemical compounds, enzyme molecules and enzymatic reactions. KEGG provides Java graphics tools for browsing genome maps, comparing two genome maps and manipulating expression maps, as well as computational tools for sequence comparison, graph comparison and path computation. The KEGG databases are daily updated and made freely available (http://www. genome.ad.jp/kegg/).
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                Author and article information

                Contributors
                sajeevan.radha.sivarajan@slu.se
                erik.alexandersson@slu.se
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                8 March 2023
                8 March 2023
                2023
                : 23
                : 130
                Affiliations
                [1 ]GRID grid.6341.0, ISNI 0000 0000 8578 2742, Department of Plant Protection Biology, , Swedish University of Agricultural Sciences, ; 23422 Lomma, Sweden
                [2 ]GRID grid.412093.d, ISNI 0000 0000 9853 2750, Department of Botany and Microbiology, Faculty of Science, , Helwan University, ; Cairo, EG-11795 Egypt
                [3 ]GRID grid.6341.0, ISNI 0000 0000 8578 2742, Department of Plant Breeding, , Swedish University of Agricultural Sciences, ; 23422 Lomma, Sweden
                [4 ]GRID grid.4514.4, ISNI 0000 0001 0930 2361, CropTailor AB, Department of Chemistry, Division of Pure and Applied Biochemistry, , Lund University, ; Lund, Sweden
                Author information
                http://orcid.org/0000-0002-8671-4981
                http://orcid.org/0000-0001-6320-2492
                Article
                4135
                10.1186/s12870-023-04135-9
                9993742
                36882678
                0345781c-fa73-42e2-b357-203e7ceef767
                © The Author(s) 2023

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 15 September 2022
                : 22 February 2023
                Funding
                Funded by: Swedish University of Agricultural Sciences
                Categories
                Research
                Custom metadata
                © The Author(s) 2023

                Plant science & Botany
                potato,early blight,alternaria solani,transcriptome,transcription factors,jasmonic acid,ethylene,photosynthesis,starch metabolism,terpenes

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