Genome-wide association mapping and genomic prediction analyses reveal the genetic architecture of grain yield and agronomic traits under drought and optimum conditions in maize

Abstract

Background: Drought is a major abiotic stress in sub-Saharan Africa, impacting maize growth and development leading to severe yield loss. Drought tolerance is a complex trait regulated by multiple genes, making direct grain yield selection ineffective. To dissect the genetic architecture of grain yield and flowering traits under drought stress, a genome-wide association study (GWAS) was conducted on a panel of 236 maize lines testcrossed and evaluated under managed drought and optimal growing conditions in multiple environments using seven multi-locus GWAS models (mrMLM, FASTmrMLM, FASTmrEMMA, pLARmEB, pKWmEB, ISIS EM-BLASSO, and FARMCPU) from mrMLM and GAPIT R packages. Genomic prediction with RR-BLUP model was applied on BLUEs across locations under optimum and drought conditions.

Results: A total of 172 stable and reliable quantitative trait nucleotides (QTNs) were identified, of which 77 are associated with GY, AD, SD, ASI, PH, EH, EPO and EPP under drought and 95 are linked to GY, AD, SD, ASI, PH, EH, EPO and EPP under optimal conditions. Among these QTNs, 17 QTNs explained over 10% of the phenotypic variation (R² ≥ 10%). Furthermore, 43 candidate genes were discovered and annotated. Two major candidate genes, Zm00001eb041070 closely associated with grain yield near peak QTN, qGY_DS1.1 (S1_216149215) and Zm00001eb364110 closely related to anthesis-silking interval near peak QTN, qASI_DS8.2 (S8_167256316) were identified, encoding AP2-EREBP transcription factor 60 and TCP-transcription factor 20, respectively under drought stress. Haplo-pheno analysis identified superior haplotypes for qGY_DS1.1 (S1_216149215) associated with the higher grain yield under drought stress. Genomic prediction revealed moderate to high prediction accuracies under optimum and drought conditions.

Conclusion: The lines carrying superior haplotypes can be used as potential donors in improving grain yield under drought stress. Integration of genomic selection with GWAS results leads not only to an increase in the prediction accuracy but also to validate the function of the identified candidate genes as well increase in the accumulation of favorable alleles with minor and major effects in elite breeding lines. This study provides valuable insight into the genetic architecture of grain yield and secondary traits under drought stress.

Keywords: Drought; Genome-wide association study; Genomic prediction; Haplotype; Maize; Yield.

Fig. 1

Frequency distributions for GY (grain yield); AD (days to 50% anthesis); SD (days to 50% silking); ASI (Anthesis-Silking interval); EPO (Ear position, Ear–plant height ratio), EPP (Ear per plant, PH = Plant height. and EH (Ear height). in 236 diverse maize lines evaluated under drought and optimum conditions. Underscore DS = Drought and OPT = Optimum conditions

Fig. 2

Pearson’s correlation analysis between the eight traits in 236 diverse maize lines under drought and optimum conditions. The blue color indicates the significant positive correlations, and red color indicates the significant negative correlation among different traits: GY (grain yield); AD (days to 50% anthesis); SD (days to 50% silking); ASI (Anthesis-Silking interval); EPO (Ear position, Ear–plant height ratio), EPP (Ear per plant, PH = Plant height. and EH (Ear height). (A) Under optimum (OPT) condition, (B) Under Drought (DS) condition

Fig. 3

SNP density, Population Structure, and linkage disequilibrium (LD) in 236 diverse maize lines. A The distribution of 215,542 SNPs across the ten maize chromosomes. B Three-dimensional (3D) principal component analysis, displaying four distinct subpopulations (green, red, cadet blue, and blue). C A scree plot shows variance explained by each of the first ten principal components. The Optimal number of PCs retained, k = 4, is indicated in red dot. D Phylogenetic trees, displaying four unique groups based on neighbor-joining method. E A heat map of kinship matrix, showing the degree of genetic relatedness among the diverse maize lines. F Genome-wide average LD decay estimated across and for each of the ten maize chromosomes

Fig. 4

Number of significantly associated QTNs detected by each of the seven GWAS models implemented in this study. A Number of QTNs/SNP detected for grain yield (GY); days to 50% anthesis (AD); days to 50% silking (SD); Anthesis-Silking interval (ASI); plant height (PH), eight height (EH), ear-plant height ratio (EPH) and ear per plant (EPP) under drought condition (B). Number of QTNs/SNP detected for grain yield (GY); days to 50% anthesis (AD); days to 50% silking (SD); Anthesis-Silking interval (ASI); plant height (PH), eight height (EH), ear-plant height ratio (EPH) and ear per plant (EPP) under optimum condition C. Number of QTNs detected by the eight GWAS models under drought condition (D) Number of QTNs detected by the eight GWAS models under Optimum condition (E) Chromosomal Distribution of QTN effects. The circle diameter is proportional to the absolute value of the QTN effect. The colors indicate the direction of the effects: red indicates negative QTN effect, and blue indicates positive QTN effect. F Chromosomal distribution of QTNs based on seven GWAS methods. The x-axis indicates genomic locations by chromosomal order, and the significant QTNs are plotted against genome location. Each row represents one QTN identified by a different method

Fig. 5

Chromosomal distribution of QTNs identified in this study

Fig. 6

Regional Manhattan plot, haplotype block analysis of qGY_DS1.1 (S1_216149215), and haplotype effect for GY under drought (A). Regional Manhattan plot of peak QTN, qGY_DS1.1 (S1_216149215) on chromosome 1. Y-axis on the left indicates –log10 (P-values) of QNT, Y-axis on the right indicates the LOD scores. The dashed line represents LOD score of 3. The pink point indicates peak QTNs simultaneously detected indicates least two models (B). Gene structure of Zm00001ed41070 related to peak qGY_DS1.1 (S1_216149215) on chr1 and haplotype of qGY_DS1.1 (S1_216149215) from 217 maize line (C). LD block of peak QTN, qGY_DS1.1 (S1_216149215) of region of 155 bp nearest to candidate gene, Zm00001ed41070. The thick sky blue and pinks segments represent a strand of a chromosome with QTN/SNP positions. The high intensity of the red blocks indicate the D prime value are close to one indicating the six QTNs/SNP are in very high linkage disequilibrium or QTN/SNPs inherited together. D Boxplot and phenotypic difference between four haplotypes based on BLUP value of GY using Tukey’s HSD test. Haplotypes with the same letters are not significantly different. N is the number of lines grouped in the same haplotype group

Fig. 7

Genomic prediction accuracies for grain yield (GY) and other agronomic traits evaluated under optimum and drought conditions