Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon

Drought stress has detrimental effects on crop productivity worldwide. A strong root system is crucial for maintaining water and nutrients uptake under drought stress. Wild watermelons possess resilient roots with excellent drought adaptability. However, the genetic factors controlling this trait re...

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Main Authors: Ahmed Mahmoud, Rui Qi, Xiaolu Chi, Nanqiao Liao, Guy Kateta Malangisha, Abid Ali, Mohamed Moustafa-Farag, Jinghua Yang, Mingfang Zhang, Zhongyuan Hu
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/1/65
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author Ahmed Mahmoud
Rui Qi
Xiaolu Chi
Nanqiao Liao
Guy Kateta Malangisha
Abid Ali
Mohamed Moustafa-Farag
Jinghua Yang
Mingfang Zhang
Zhongyuan Hu
author_facet Ahmed Mahmoud
Rui Qi
Xiaolu Chi
Nanqiao Liao
Guy Kateta Malangisha
Abid Ali
Mohamed Moustafa-Farag
Jinghua Yang
Mingfang Zhang
Zhongyuan Hu
author_sort Ahmed Mahmoud
collection DOAJ
description Drought stress has detrimental effects on crop productivity worldwide. A strong root system is crucial for maintaining water and nutrients uptake under drought stress. Wild watermelons possess resilient roots with excellent drought adaptability. However, the genetic factors controlling this trait remain uninvestigated. In this study, we conducted a bulk segregant analysis (BSA) on an F<sub>2</sub> population consisting of two watermelon genotypes, wild and domesticated, which differ in their lateral root development under drought conditions. We identified two quantitative trait loci (<i>qNLR_Dr. Chr01</i> and <i>qNLR_Dr. Chr02</i>) associated with the lateral root response to drought. Furthermore, we determined that a small region (0.93 Mb in <i>qNLR_Dr. Chr01</i>) is closely linked to drought adaptation through quantitative trait loci (QTL) validation and fine mapping. Transcriptome analysis of the parent roots under drought stress revealed unique effects on numerous genes in the sensitive genotype but not in the tolerant genotype. By integrating BSA, fine mapping, and the transcriptome, we identified six genes, namely L-Ascorbate Oxidase (AO), Cellulose Synthase-Interactive Protein 1 (CSI1), Late Embryogenesis Abundant Protein (LEA), Zinc-Finger Homeodomain Protein 2 (ZHD2), Pericycle Factor Type-A 5 (PFA5), and bZIP transcription factor 53-like (bZIP53-like), that might be involved in the drought adaptation. Our findings provide valuable QTLs and genes for marker-assisted selection in improving water-use efficiency and drought tolerance in watermelon. They also lay the groundwork for the genetic manipulation of drought-adapting genes in watermelon and other <i>Cucurbitacea</i> species.
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spelling doaj.art-0e6f87beba5c4c2d9b516812f5ffe45c2024-01-10T14:58:02ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-12-012516510.3390/ijms25010065Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild WatermelonAhmed Mahmoud0Rui Qi1Xiaolu Chi2Nanqiao Liao3Guy Kateta Malangisha4Abid Ali5Mohamed Moustafa-Farag6Jinghua Yang7Mingfang Zhang8Zhongyuan Hu9Institute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaHorticulture Research Institute, Agricultural Research Center, 9 Cairo University St, Giza 12619, EgyptInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaInstitute of Vegetable Science, Zhejiang University, Hangzhou 310058, ChinaDrought stress has detrimental effects on crop productivity worldwide. A strong root system is crucial for maintaining water and nutrients uptake under drought stress. Wild watermelons possess resilient roots with excellent drought adaptability. However, the genetic factors controlling this trait remain uninvestigated. In this study, we conducted a bulk segregant analysis (BSA) on an F<sub>2</sub> population consisting of two watermelon genotypes, wild and domesticated, which differ in their lateral root development under drought conditions. We identified two quantitative trait loci (<i>qNLR_Dr. Chr01</i> and <i>qNLR_Dr. Chr02</i>) associated with the lateral root response to drought. Furthermore, we determined that a small region (0.93 Mb in <i>qNLR_Dr. Chr01</i>) is closely linked to drought adaptation through quantitative trait loci (QTL) validation and fine mapping. Transcriptome analysis of the parent roots under drought stress revealed unique effects on numerous genes in the sensitive genotype but not in the tolerant genotype. By integrating BSA, fine mapping, and the transcriptome, we identified six genes, namely L-Ascorbate Oxidase (AO), Cellulose Synthase-Interactive Protein 1 (CSI1), Late Embryogenesis Abundant Protein (LEA), Zinc-Finger Homeodomain Protein 2 (ZHD2), Pericycle Factor Type-A 5 (PFA5), and bZIP transcription factor 53-like (bZIP53-like), that might be involved in the drought adaptation. Our findings provide valuable QTLs and genes for marker-assisted selection in improving water-use efficiency and drought tolerance in watermelon. They also lay the groundwork for the genetic manipulation of drought-adapting genes in watermelon and other <i>Cucurbitacea</i> species.https://www.mdpi.com/1422-0067/25/1/65drought tolerancegenetic resourceswild watermelonquantitative trait loci (QTL) mappingtranscriptomegenomics-assisted breeding
spellingShingle Ahmed Mahmoud
Rui Qi
Xiaolu Chi
Nanqiao Liao
Guy Kateta Malangisha
Abid Ali
Mohamed Moustafa-Farag
Jinghua Yang
Mingfang Zhang
Zhongyuan Hu
Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
International Journal of Molecular Sciences
drought tolerance
genetic resources
wild watermelon
quantitative trait loci (QTL) mapping
transcriptome
genomics-assisted breeding
title Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
title_full Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
title_fullStr Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
title_full_unstemmed Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
title_short Integrated Bulk Segregant Analysis, Fine Mapping, and Transcriptome Revealed QTLs and Candidate Genes Associated with Drought Adaptation in Wild Watermelon
title_sort integrated bulk segregant analysis fine mapping and transcriptome revealed qtls and candidate genes associated with drought adaptation in wild watermelon
topic drought tolerance
genetic resources
wild watermelon
quantitative trait loci (QTL) mapping
transcriptome
genomics-assisted breeding
url https://www.mdpi.com/1422-0067/25/1/65
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