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...

Full description

Bibliographic Details
Main Authors: Kelvin Dodzi Aloryi, Nnaemeka Emmanuel Okpala, Hong Guo, Benjamin Karikari, Aduragbemi Amo, Semiu Folaniyi Bello, Dinesh Kumar Saini, Selorm Akaba, Xiaohai Tian
Format: Article
Language:English
Published: BMC 2024-04-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10219-z
_version_ 1797220029178052608
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.
first_indexed 2024-04-24T12:43:02Z
format Article
id doaj.art-d04087b7a5144e49a5dadabdc6ac9b45
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-04-24T12:43:02Z
publishDate 2024-04-01
publisher BMC
record_format Article
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
work_keys_str_mv AT kelvindodzialoryi integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT nnaemekaemmanuelokpala integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT hongguo integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT benjaminkarikari integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT aduragbemiamo integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT semiufolaniyibello integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT dineshkumarsaini integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT selormakaba integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice
AT xiaohaitian integratedmetaanalysisandtranscriptomicspinpointgenomiclociandnovelcandidategenesassociatedwithsubmergencetoleranceinrice