Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (21): 4091-4103.doi: 10.3864/j.issn.0578-1752.2022.21.001

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Genome-Wide Association Study of Cold Tolerance at the Germination Stage of Rice

PANG HongBo1(),CHENG Lu1,YU MingLan1,CHEN Qiang2,LI YueYing1,WU LongKun3,WANG Ze1,PAN XiaoWu4,ZHENG XiaoMing5,6()   

  1. 1College of Life Science, Shenyang Normal University, Shenyang 110034
    2Experiment Teaching Center, Shenyang Normal University, Shenyang 110034
    3College of Grain Science and Technology, Shenyang Normal University, Shenyang 110034
    4Rice Research Institute, Hunan Academy of Agricultural Sciences, Changsha 410125
    5Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081
    6Sanya National Research Institute of Breeding in Hainan, Chinese Academy of Agricultural Sciences, Sanya 571700, Hainan
  • Received:2022-07-15 Accepted:2022-08-17 Online:2022-11-01 Published:2022-11-09
  • Contact: HongBo PANG,XiaoMing ZHENG E-mail:panghb@synu.edu.cn;zhengxiaoming@caas.cn

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Abstract:

【Objective】Rice is an important food crop, and its growth and development are most vulnerable at the germination stage. Under cold stress, direct-seeded rice exhibited significantly reduced germination rates (GRs) and yield compared with normally grown plants. Thus, a better understanding of genetic mechanisms regulating cold tolerance will enable to develop rice varieties with improved tolerance during germination. 【Method】238 representative rice germplasm resources from 14 countries worldwide were tested in phenotypic identification in Shenyang in 2021 and 2022; the low-temperature germination rate and relative low-temperature germination rate (LTGR and relative LTGR; 1-10 days under 15℃) were evaluated in an artificial climate incubator, and a 5-10 day LTGR histogram was constructed using R. The day suitable for GWAS was determined by phenotypic variation (Hill) and a mixed linear model combining LTGR and relative LTGR phenotype data with resequencing data. 【Result】LTGR histogram and phenotypic variation showed optimal GR on day 8 (Hill=0.84), i.e., it was higher than on other days (Hill=0.48-0.83), which could be used for GWAS. The principal component analysis results divided all germplasms into five groups—indica, aus, temperate japonica, tropical japonica, and aromatic. GWAS analysis of two indicators detected three identical significant single nucleotide polymorphisms (SNPs) related to cold tolerance in rice at the germination stage. These were located on chromosome 4, which could explain 11.9%-25.4% of the phenotype. In addition, 24 candidate genes were screened in the 50-kb region upstream and downstream of these three SNPs. Further linkage disequilibrium analysis and haplotype analysis were carried out and highly significant differences were found between different haplotypes of the LOC_Os04g24840 and LOC_Os04g25140 genes for cold tolerance. LOC_Os04g24840 was divided into five haplotypes by the coding region SNP, and Hap_3 was significantly more cold tolerant than Hap_1; LOC_Os04g25140 was divided into 18 haplotypes by the coding region SNP and the amino acid variation (S>L) at 77 bp was different in japonica and indica rice. These results showed that the genes encoding glycosyltransferases (LOC_Os04g24840) and F-box protein (LOC_Os04g25140) might be closely related to cold tolerance in rice.【Conclusion】 A total of three SNP loci were detected in 238 rice germplasm resources, and two candidate genes were screened for their association with cold tolerance during germination in rice.

Key words: Oryza sativa L., seed germinability, cold tolerance, germination rate, GWAS

Fig. 1

Frequency histogram of GR of 5-10 days"

Fig. 2

PCA analysis of rice whole-genome SNP data"

Fig. 3

Histogram of kinship between samples and heat map of kinship A: Histogram of kinship between samples; B: Heat map of relationship between samples"

Fig. 4

Genome-wide association study analysis of LTGR and relative LTGR in 238 rice accessions"

Table 1

Gene annotation of 24 candidate genes"

染色体 Chr. 基因号 Gene ID 基因注释 Annotation
Chr.4 LOC_Os04g24830 含锌指、CCHC型结构域的蛋白质 Zinc finger, CCHC-type domain containing protein
Chr.4 LOC_Os04g24840 糖基转移酶，推测，表达Glycosyltransferase, putative, expressed
Chr.4 LOC_Os04g24850 细胞分裂素-O-葡糖基转移酶2，假定的，表达Cytokinin-O-glucosyltransferase 2, putative, expressed
Chr.4 LOC_Os04g24860 逆转录酶子蛋白，推定，未分类，表达Retrotransposon protein, putative, unclassified, expressed
Chr.4 LOC_Os04g24870 逆转录酶子蛋白，推定，未分类Retrotransposon protein, putative, unclassified
Chr.4 LOC_Os04g24880 逆转录酶子蛋白，推定，未分类，表达Retrotransposon protein, putative, unclassified, expressed
Chr.4 LOC_Os04g24900 表达蛋白Expressed protein
Chr.4 LOC_Os04g24910 表达蛋白Expressed protein
Chr.4 LOC_Os04g24920 转座子蛋白，推定，CACTA，En/Spm亚类，表达
Transposon protein, putative, CACTA, En/Spm sub-class, expressed
Chr.4 LOC_Os04g24930 表达蛋白Expressed protein
Chr.4 LOC_Os04g24940 表达蛋白Expressed protein
Chr.4 LOC_Os04g24950 假定的蛋白质Hypothetical protein
Chr.4 LOC_Os04g24960 转座子蛋白，推定，CACTA，En/Spm亚类，表达
Transposon protein, putative, CACTA, En/Spm sub-class, expressed
Chr.4 LOC_Os04g25100 转座子蛋白，推定，未分类，表达Transposon protein, putative, unclassified, expressed
Chr.4 LOC_Os04g25110 Ulp1蛋白酶家族，含有C端催化域的蛋白，表达式ulp1;
Ulp1 protease family, C-terminal catalytic domain containing protein, expressedulp1
Chr.4 LOC_Os04g25120 表达蛋白Expressed protein
Chr.4 LOC_Os04g25130 逆转录子蛋白，推定，LINE亚类，表达Retrotransposon protein, putative, LINE subclass, expressed
Chr.4 LOC_Os04g25140 OsFBDUF20-含有F-box和DUF结构域的蛋白，已表达;
OsFBDUF20- F-box and DUF domain containing protein, expressed
Chr.4 LOC_Os04g25150 花粉过敏原，推定，表达Pollen allergen, putative, expressed
Chr.4 LOC_Os04g25160 花粉过敏原，推定，表达Pollen allergen, putative, expressed
Chr.4 LOC_Os04g25170 逆转录酶原蛋白，推定，未分类，表达Retrotransposon protein, putative, unclassified, expressed
Chr.4 LOC_Os04g25180 假定的蛋白质Hypothetical protein
Chr.4 LOC_Os04g25190 花粉过敏原，推定，表达Pollen allergen, putative, expressed
Chr.4 LOC_Os04g25210 转座子蛋白，推定，未分类，表达Transposon protein, putative, unclassified, expressed

Fig. 5

Gene prediction in linkage disequilibrium region of association locus The 24 black boxes in the middle part of the figure are the 24 candidate genes in order, the red vertical lines represent the locations of the 3 significant SNPs and the 4 grey arrows indicate LOC_Os04g24830, LOC_Os04g24840, LOC_Os04g24850 and LOC_Os04g25140, respectively"

Fig. 6

Nucleotide diversity in the coding region of LOC_Os04g24840 and LOC_Os04g25140 in 165 cultivated rice Red represents haplotypes common to both japonica and indica, blue represents sense mutations in SNPs in the coding region of the gene; green identifies a nucleotide variation at 235 bp (C>T) leading to an early terminator in the gene; yellow indicates a base difference between japonica and indica rice at 77 bp (C>T)"

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