Association mapping of loci controlling genetic and environmental interaction of soybean flowering time under various photo-thermal conditions

Abstract

Background: Soybean (Glycine max (L.) Merr.) is a short day plant. Its flowering and maturity time are controlled by genetic and environmental factors, as well the interaction between the two factors. Previous studies have shown that both genetic and environmental factors, mainly photoperiod and temperature, control flowering time of soybean. Additionally, these studies have reported gene × gene and gene × environment interactions on flowering time. However, the effects of quantitative trait loci (QTL) in response to photoperiod and temperature have not been well evaluated. The objectives of the current study were to identify the effects of loci associated with flowering time under different photo-thermal conditions and to understand the effects of interaction between loci and environment on soybean flowering.

Methods: Different photoperiod and temperature combinations were obtained by adjusting sowing dates (spring sowing and summer sowing) or day-length (12 h, 16 h). Association mapping was performed on 91 soybean cultivars from different maturity groups (MG000-VIII) using 172 SSR markers and 5107 SNPs from the Illumina SoySNP6K iSelectBeadChip. The effects of the interaction between QTL and environments on flowering time were also analysed using the QTXNetwork.

Results: Large-effect loci were detected on Gm 11, Gm 16 and Gm 20 as in previous reports. Most loci associated with flowering time are sensitive to photo-thermal conditions. Number of loci associated with flowering time was more under the long day (LD) than under the short day (SD) condition. The variation of flowering time among the soybean cultivars mostly resulted from the epistasis × environment and additive × environment interactions. Among the three candidate loci, i.e. Gm04_4497001 (near GmCOL3a), Gm16_30766209 (near GmFT2a and GmFT2b) and Gm19_47514601 (E3 or GmPhyA3), the Gm04_4497001 may be the key locus interacting with other loci for controlling soybean flowering time.

Conclusion: The effects of loci associated with the flowering time of soybean were dependent upon the photo-thermal conditions. This study facilitates the understanding of the genetic mechanism of soybean flowering and molecular breeding for the improvement of soybean adaptability to specific and/or broad regions.

Keywords: Flowering time; Gene by environment interaction; Genetic architecture; Photo-thermal condition; Soybean (Glycine max).

Fig. 1

Population structure of 91 soybean cultivars using 5107 SNP markers. a Estimation of the number of sub-populations. The left figure was a plot of ln (probability of data) vs. K ranging from 1 to 10 and the right figure was a plot of subpopulation number vs. delta K values. b Population structure of 91 soybean cultivars based on SNP markers. The x-axis indicates the cultivars, and the y-axis indicates the Q value from STRUCTURE 2.3.1. The red color represents one sub-group, the green color represents another. c PCA of 91 soybean cultivars with the top two principal components. d Neighbor-joining tree of the 91 soybean cultivars

Fig. 2

The estimated average linkage disequilibrium decay of soybean genome. The dashed line in red indicates the position where r ² is 0.2

Fig. 3

Manhattan plot and linkage disequilibrium block in different environments. Linkage disequilibrium blocks associated with flowering time near Gm11_10847172, Gm11_33034954, Gm16_30766209, Gm20_3880320 and Gm20_43146832. Significance threshold is denoted by the orange line. The up panel was the Manhattan plots of negative log10-transformed P values vs. SNPs. The down panel was haplotype block based on pairwise linkage disequilibriumr²values. LD, 16 h; LT, low temperature (spring sowing); HT, high temperature (summer sowing); SP, Spring sowing season with natural day-length in 2010 pot experiment; SU, Summer sowing season with natural day-length in 2010 pot experiment; 14SP, Spring sowing in 2014 field experiment; 14SU, Summer sowing season in 2014 field experiment; 15SP, Spring sowing season in 2015 field experiment; 15SU, Summer sowing season in 2015 field experiment

Fig. 4

Phenotypic variation between cultivars carrying different alleles of the SNPs significantly associated with flowering time in various environments. The box plot shows the significant difference of days to flowering of the cultivars carrying two alleles of the SNPs. The significant SNPs were Gm11_10847172, Gm11_33034954, Gm16_30766209, Gm20_3880320 and Gm20_43146832. The major allele of significant loci was marked by yellow, and the minor allele was marked by green. Significant differences tested by the student’s t-test are also given (***p < 0.001, **p < 0.01, *p < 0.05). LD, 16 h; LT, low temperature (spring sowing); HT, high temperature (summer sowing); SP, Spring sowing season with natural day-length in 2010 pot experiment; SU, Summer sowing season with natural day-length in 2010 pot experiment; 14SP, Spring sowing in 2014 field experiment; 14SU, Summer sowing season in 2014 field experiment; 15SP, Spring sowing season in 2015 field experiment; 15SU, Summer sowing season in 2015 field experiment

Fig. 5

The plot of network of highly significant loci identified for soybean flowering time. The red dots represent the loci with additive effects; the blue dots represent the loci with both additive and environment-specific effects; red lines between two dots represent epistasis (aa); blue lines between two dots represent both epistasis (aa) and environment-specific epistasis (aae)

Fig. 6

The positions of flowering time-related loci and their corresponding candidate genes. The positions of candidate genes were marked in black, the loci were shown in red,  and the known flowering genes were underlined. The position of the first locus on each chromosome was set as zero, and the left number showed the relative in the genome, 1 = 100 kb