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

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 evolutio...

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Main Authors: Radha Sivarajan Sajeevan, Ingi Abdelmeguid, Ganapathi Varma Saripella, Marit Lenman, Erik Alexandersson
Format: Article
Language:English
Published: BMC 2023-03-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04135-9
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author Radha Sivarajan Sajeevan
Ingi Abdelmeguid
Ganapathi Varma Saripella
Marit Lenman
Erik Alexandersson
author_facet Radha Sivarajan Sajeevan
Ingi Abdelmeguid
Ganapathi Varma Saripella
Marit Lenman
Erik Alexandersson
author_sort Radha Sivarajan Sajeevan
collection DOAJ
description 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.
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spelling doaj.art-8f59ae624f8a4f229688f1b9d3fe07e12023-03-22T10:50:07ZengBMCBMC Plant Biology1471-22292023-03-0123112210.1186/s12870-023-04135-9Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solaniRadha Sivarajan Sajeevan0Ingi Abdelmeguid1Ganapathi Varma Saripella2Marit Lenman3Erik Alexandersson4Department of Plant Protection Biology, Swedish University of Agricultural SciencesDepartment of Plant Protection Biology, Swedish University of Agricultural SciencesDepartment of Plant Breeding, Swedish University of Agricultural SciencesDepartment of Plant Protection Biology, Swedish University of Agricultural SciencesDepartment of Plant Protection Biology, Swedish University of Agricultural SciencesAbstract 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.https://doi.org/10.1186/s12870-023-04135-9PotatoEarly blightAlternaria solaniTranscriptomeTranscription factorsJasmonic acid
spellingShingle Radha Sivarajan Sajeevan
Ingi Abdelmeguid
Ganapathi Varma Saripella
Marit Lenman
Erik Alexandersson
Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
BMC Plant Biology
Potato
Early blight
Alternaria solani
Transcriptome
Transcription factors
Jasmonic acid
title Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
title_full Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
title_fullStr Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
title_full_unstemmed Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
title_short Comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by Alternaria solani
title_sort comprehensive transcriptome analysis of different potato cultivars provides insight into early blight disease caused by alternaria solani
topic Potato
Early blight
Alternaria solani
Transcriptome
Transcription factors
Jasmonic acid
url https://doi.org/10.1186/s12870-023-04135-9
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