Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling

IntroductionWaterlogging is a major stress that severely affects onion cultivation worldwide, and developing stress-tolerant varieties could be a valuable measure for overcoming its adverse effects. Gathering information regarding the molecular mechanisms and gene expression patterns of waterlogging...

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Main Authors: Pranjali A. Gedam, Kiran Khandagale, Dhananjay Shirsat, A. Thangasamy, Onkar Kulkarni, Abhijeet Kulkarni, Swaranjali S. Patil, Vitthal T. Barvkar, Vijay Mahajan, Amar Jeet Gupta, Kiran P. Bhagat, Yogesh P. Khade, Major Singh, Suresh Gawande
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1150909/full
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author Pranjali A. Gedam
Kiran Khandagale
Dhananjay Shirsat
A. Thangasamy
Onkar Kulkarni
Abhijeet Kulkarni
Swaranjali S. Patil
Vitthal T. Barvkar
Vijay Mahajan
Amar Jeet Gupta
Kiran P. Bhagat
Yogesh P. Khade
Major Singh
Suresh Gawande
author_facet Pranjali A. Gedam
Kiran Khandagale
Dhananjay Shirsat
A. Thangasamy
Onkar Kulkarni
Abhijeet Kulkarni
Swaranjali S. Patil
Vitthal T. Barvkar
Vijay Mahajan
Amar Jeet Gupta
Kiran P. Bhagat
Yogesh P. Khade
Major Singh
Suresh Gawande
author_sort Pranjali A. Gedam
collection DOAJ
description IntroductionWaterlogging is a major stress that severely affects onion cultivation worldwide, and developing stress-tolerant varieties could be a valuable measure for overcoming its adverse effects. Gathering information regarding the molecular mechanisms and gene expression patterns of waterlogging-tolerant and sensitive genotypes is an effective method for improving stress tolerance in onions. To date, the waterlogging tolerance-governing molecular mechanism in onions is unknown.MethodsThis study identified the differentially expressed genes (DEGs) through transcriptome analysis in leaf tissue of two onion genotypes (Acc. 1666; tolerant and W-344; sensitive) presenting contrasting responses to waterlogging stress.ResultsDifferential gene expression analysis revealed that in Acc. 1666, 1629 and 3271 genes were upregulated and downregulated, respectively. In W-344, 2134 and 1909 genes were upregulated and downregulated, respectively, under waterlogging stress. The proteins coded by these DEGs regulate several key biological processes to overcome waterlogging stress such as phytohormone production, antioxidant enzymes, programmed cell death, and energy production. The clusters of orthologous group pathway analysis revealed that DEGs contributed to the post-translational modification, energy production, and carbohydrate metabolism-related pathways under waterlogging stress. The enzyme assay demonstrated higher activity of antioxidant enzymes in Acc. 1666 than in W-344. The differential expression of waterlogging tolerance related genes, such as those related to antioxidant enzymes, phytohormone biosynthesis, carbohydrate metabolism, and transcriptional factors, suggested that significant fine reprogramming of gene expression occurs in response to waterlogging stress in onion. A few genes such as ADH, PDC, PEP carboxylase, WRKY22, and Respiratory burst oxidase D were exclusively upregulated in Acc. 1666.DiscussionThe molecular information about DEGs identified in the present study would be valuable for improving stress tolerance and for developing waterlogging tolerant onion varieties.
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spelling doaj.art-b63cbe37e78943c49a985f3b2affdc612023-08-08T09:43:19ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.11509091150909Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profilingPranjali A. Gedam0Kiran Khandagale1Dhananjay Shirsat2A. Thangasamy3Onkar Kulkarni4Abhijeet Kulkarni5Swaranjali S. Patil6Vitthal T. Barvkar7Vijay Mahajan8Amar Jeet Gupta9Kiran P. Bhagat10Yogesh P. Khade11Major Singh12Suresh Gawande13Indian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaBioinformatics Centre, Savitribai Phule Pune University, Pune, IndiaBioinformatics Centre, Savitribai Phule Pune University, Pune, IndiaDepartment of Botany, Savitribai Phule Pune University, Pune, IndiaDepartment of Botany, Savitribai Phule Pune University, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Floriculture Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIndian Council of Agricultural Research (ICAR)-Directorate of Onion and Garlic Research, Pune, IndiaIntroductionWaterlogging is a major stress that severely affects onion cultivation worldwide, and developing stress-tolerant varieties could be a valuable measure for overcoming its adverse effects. Gathering information regarding the molecular mechanisms and gene expression patterns of waterlogging-tolerant and sensitive genotypes is an effective method for improving stress tolerance in onions. To date, the waterlogging tolerance-governing molecular mechanism in onions is unknown.MethodsThis study identified the differentially expressed genes (DEGs) through transcriptome analysis in leaf tissue of two onion genotypes (Acc. 1666; tolerant and W-344; sensitive) presenting contrasting responses to waterlogging stress.ResultsDifferential gene expression analysis revealed that in Acc. 1666, 1629 and 3271 genes were upregulated and downregulated, respectively. In W-344, 2134 and 1909 genes were upregulated and downregulated, respectively, under waterlogging stress. The proteins coded by these DEGs regulate several key biological processes to overcome waterlogging stress such as phytohormone production, antioxidant enzymes, programmed cell death, and energy production. The clusters of orthologous group pathway analysis revealed that DEGs contributed to the post-translational modification, energy production, and carbohydrate metabolism-related pathways under waterlogging stress. The enzyme assay demonstrated higher activity of antioxidant enzymes in Acc. 1666 than in W-344. The differential expression of waterlogging tolerance related genes, such as those related to antioxidant enzymes, phytohormone biosynthesis, carbohydrate metabolism, and transcriptional factors, suggested that significant fine reprogramming of gene expression occurs in response to waterlogging stress in onion. A few genes such as ADH, PDC, PEP carboxylase, WRKY22, and Respiratory burst oxidase D were exclusively upregulated in Acc. 1666.DiscussionThe molecular information about DEGs identified in the present study would be valuable for improving stress tolerance and for developing waterlogging tolerant onion varieties.https://www.frontiersin.org/articles/10.3389/fpls.2023.1150909/fullwaterloggingoniontranscriptomeRNA-sequencingdifferential gene expression
spellingShingle Pranjali A. Gedam
Kiran Khandagale
Dhananjay Shirsat
A. Thangasamy
Onkar Kulkarni
Abhijeet Kulkarni
Swaranjali S. Patil
Vitthal T. Barvkar
Vijay Mahajan
Amar Jeet Gupta
Kiran P. Bhagat
Yogesh P. Khade
Major Singh
Suresh Gawande
Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
Frontiers in Plant Science
waterlogging
onion
transcriptome
RNA-sequencing
differential gene expression
title Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
title_full Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
title_fullStr Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
title_full_unstemmed Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
title_short Elucidating the molecular responses to waterlogging stress in onion (Allium cepa L.) leaf by comparative transcriptome profiling
title_sort elucidating the molecular responses to waterlogging stress in onion allium cepa l leaf by comparative transcriptome profiling
topic waterlogging
onion
transcriptome
RNA-sequencing
differential gene expression
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1150909/full
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