Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice
Abstract Background Due to rising costs, water shortages, and labour shortages, farmers across the globe now prefer a direct seeding approach. However, submergence stress remains a major bottleneck limiting the success of this approach in rice cultivation. The merger of accumulated rice genetic reso...
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BMC
2024-04-01
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Series: | BMC Genomics |
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Online Access: | https://doi.org/10.1186/s12864-024-10219-z |
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author | Kelvin Dodzi Aloryi Nnaemeka Emmanuel Okpala Hong Guo Benjamin Karikari Aduragbemi Amo Semiu Folaniyi Bello Dinesh Kumar Saini Selorm Akaba Xiaohai Tian |
author_facet | Kelvin Dodzi Aloryi Nnaemeka Emmanuel Okpala Hong Guo Benjamin Karikari Aduragbemi Amo Semiu Folaniyi Bello Dinesh Kumar Saini Selorm Akaba Xiaohai Tian |
author_sort | Kelvin Dodzi Aloryi |
collection | DOAJ |
description | Abstract Background Due to rising costs, water shortages, and labour shortages, farmers across the globe now prefer a direct seeding approach. However, submergence stress remains a major bottleneck limiting the success of this approach in rice cultivation. The merger of accumulated rice genetic resources provides an opportunity to detect key genomic loci and candidate genes that influence the flooding tolerance of rice. Results In the present study, a whole-genome meta-analysis was conducted on 120 quantitative trait loci (QTL) obtained from 16 independent QTL studies reported from 2004 to 2023. These QTL were confined to 18 meta-QTL (MQTL), and ten MQTL were successfully validated by independent genome-wide association studies from diverse natural populations. The mean confidence interval (CI) of the identified MQTL was 3.44 times narrower than the mean CI of the initial QTL. Moreover, four core MQTL loci with genetic distance less than 2 cM were obtained. By combining differentially expressed genes (DEG) from two transcriptome datasets with 858 candidate genes identified in the core MQTL regions, we found 38 common differentially expressed candidate genes (DECGs). In silico expression analysis of these DECGs led to the identification of 21 genes with high expression in embryo and coleoptile under submerged conditions. These DECGs encode proteins with known functions involved in submergence tolerance including WRKY, F-box, zinc fingers, glycosyltransferase, protein kinase, cytochrome P450, PP2C, hypoxia-responsive family, and DUF domain. By haplotype analysis, the 21 DECGs demonstrated distinct genetic differentiation and substantial genetic distance mainly between indica and japonica subspecies. Further, the MQTL7.1 was successfully validated using flanked marker S2329 on a set of genotypes with phenotypic variation. Conclusion This study provides a new perspective on understanding the genetic basis of submergence tolerance in rice. The identified MQTL and novel candidate genes lay the foundation for marker-assisted breeding/engineering of flooding-tolerant cultivars conducive to direct seeding. |
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issn | 1471-2164 |
language | English |
last_indexed | 2024-04-24T12:43:02Z |
publishDate | 2024-04-01 |
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series | BMC Genomics |
spelling | doaj.art-d04087b7a5144e49a5dadabdc6ac9b452024-04-07T11:09:23ZengBMCBMC Genomics1471-21642024-04-0125111810.1186/s12864-024-10219-zIntegrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in riceKelvin Dodzi Aloryi0Nnaemeka Emmanuel Okpala1Hong Guo2Benjamin Karikari3Aduragbemi Amo4Semiu Folaniyi Bello5Dinesh Kumar Saini6Selorm Akaba7Xiaohai Tian8Hubei Collaborative Innovation Centre for Grain Industry, College of Agriculture, Yangtze UniversityHubei Collaborative Innovation Centre for Grain Industry, College of Agriculture, Yangtze UniversityUniversity of Chinese Academy of SciencesDépartement de phytologie, Université LavalDepartment of Horticultural Sciences, Texas A&M UniversityDepartment of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural UniversityDepartment of Plant Breeding and Genetics, Punjab Agricultural UniversitySchool of Agriculture, University of Cape CoastHubei Collaborative Innovation Centre for Grain Industry, College of Agriculture, Yangtze UniversityAbstract Background Due to rising costs, water shortages, and labour shortages, farmers across the globe now prefer a direct seeding approach. However, submergence stress remains a major bottleneck limiting the success of this approach in rice cultivation. The merger of accumulated rice genetic resources provides an opportunity to detect key genomic loci and candidate genes that influence the flooding tolerance of rice. Results In the present study, a whole-genome meta-analysis was conducted on 120 quantitative trait loci (QTL) obtained from 16 independent QTL studies reported from 2004 to 2023. These QTL were confined to 18 meta-QTL (MQTL), and ten MQTL were successfully validated by independent genome-wide association studies from diverse natural populations. The mean confidence interval (CI) of the identified MQTL was 3.44 times narrower than the mean CI of the initial QTL. Moreover, four core MQTL loci with genetic distance less than 2 cM were obtained. By combining differentially expressed genes (DEG) from two transcriptome datasets with 858 candidate genes identified in the core MQTL regions, we found 38 common differentially expressed candidate genes (DECGs). In silico expression analysis of these DECGs led to the identification of 21 genes with high expression in embryo and coleoptile under submerged conditions. These DECGs encode proteins with known functions involved in submergence tolerance including WRKY, F-box, zinc fingers, glycosyltransferase, protein kinase, cytochrome P450, PP2C, hypoxia-responsive family, and DUF domain. By haplotype analysis, the 21 DECGs demonstrated distinct genetic differentiation and substantial genetic distance mainly between indica and japonica subspecies. Further, the MQTL7.1 was successfully validated using flanked marker S2329 on a set of genotypes with phenotypic variation. Conclusion This study provides a new perspective on understanding the genetic basis of submergence tolerance in rice. The identified MQTL and novel candidate genes lay the foundation for marker-assisted breeding/engineering of flooding-tolerant cultivars conducive to direct seeding.https://doi.org/10.1186/s12864-024-10219-zMeta-analysisMQTLSubmergence toleranceHaplotype analysisDifferentially expressed candidate genes (DECGs)Marker-assisted breeding |
spellingShingle | Kelvin Dodzi Aloryi Nnaemeka Emmanuel Okpala Hong Guo Benjamin Karikari Aduragbemi Amo Semiu Folaniyi Bello Dinesh Kumar Saini Selorm Akaba Xiaohai Tian Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice BMC Genomics Meta-analysis MQTL Submergence tolerance Haplotype analysis Differentially expressed candidate genes (DECGs) Marker-assisted breeding |
title | Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
title_full | Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
title_fullStr | Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
title_full_unstemmed | Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
title_short | Integrated meta-analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
title_sort | integrated meta analysis and transcriptomics pinpoint genomic loci and novel candidate genes associated with submergence tolerance in rice |
topic | Meta-analysis MQTL Submergence tolerance Haplotype analysis Differentially expressed candidate genes (DECGs) Marker-assisted breeding |
url | https://doi.org/10.1186/s12864-024-10219-z |
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