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. 2021 Jun 18;22(12):6556.
doi: 10.3390/ijms22126556.

Genome-Wide Identification of Soybean ABC Transporters Relate to Aluminum Toxicity

Junjun Huang  1 , Xiaoyu Li  1 , Xin Chen  1 , Yaru Guo  1 , Weihong Liang  1 , Huahua Wang  1
Affiliations

Genome-Wide Identification of Soybean ABC Transporters Relate to Aluminum Toxicity

Junjun Huang et al. Int J Mol Sci. .

Abstract

ATP-binding cassette (ABC) transporter proteins are a gene super-family in plants and play vital roles in growth, development, and response to abiotic and biotic stresses. The ABC transporters have been identified in crop plants such as rice and buckwheat, but little is known about them in soybean. Soybean is an important oil crop and is one of the five major crops in the world. In this study, 255 ABC genes that putatively encode ABC transporters were identified from soybean through bioinformatics and then categorized into eight subfamilies, including 7 ABCAs, 52 ABCBs, 48 ABCCs, 5 ABCDs, 1 ABCEs, 10 ABCFs, 111 ABCGs, and 21 ABCIs. Their phylogenetic relationships, gene structure, and gene expression profiles were characterized. Segmental duplication was the main reason for the expansion of the GmABC genes. Ka/Ks analysis suggested that intense purifying selection was accompanied by the evolution of GmABC genes. The genome-wide collinearity of soybean with other species showed that GmABCs were relatively conserved and that collinear ABCs between species may have originated from the same ancestor. Gene expression analysis of GmABCs revealed the distinct expression pattern in different tissues and diverse developmental stages. The candidate genes GmABCB23, GmABCB25, GmABCB48, GmABCB52, GmABCI1, GmABCI5, and GmABCI13 were responsive to Al toxicity. This work on the GmABC gene family provides useful information for future studies on ABC transporters in soybean and potential targets for the cultivation of new germplasm resources of aluminum-tolerant soybean.

Keywords: ABC transporter proteins; aluminum toxicity; expression analysis; genomic survey; molecular evolution; soybean.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Chromosomal distribution of soybean ABC genes. The chromosome number is indicated at the top of each bar. The scale on the left represents the length in megabases (Mb). The tandemly duplicated GmABC genes are shown in black boxes.
Figure 2
Figure 2
Phylogenetic tree of ABC transporter proteins from soybean. The unrooted phylogenetic tree was constructed by MEGA 7.0 using the maximum likelihood (ML) algorithm with 1000 bootstraps. Eight subfamilies are highlighted by different colors.
Figure 3
Figure 3
Gene structures of subfamilies GmABCA—GmABCG in soybean. Orange boxes, blue boxes, and black lines indicate UTRs, exons, and introns, respectively. The exon and intron length are calculated by the scale at the bottom.
Figure 4
Figure 4
Conserved motifs of ABC transporter proteins in soybean. The conserved motifs of the GmABC proteins were elucidated using the MEME tool.
Figure 5
Figure 5
Schematic of the interchromosomal relationships of soybean ABC genes. Gray lines indicate all syntenic blocks in the soybean genome, and the colored lines indicate duplicated ABC gene pairs. The heatmaps represent the gene density.
Figure 6
Figure 6
Collinearity analysis of ABC transporter genes between soybean and four other species (A. thaliana, O. sativa, S. tuberosum, and Z. mays). The gray curved lines represent the collinear blocks in the whole genome of soybean and other plants, the four species. The purple curved lines represent syntenic ABC transporter gene pairs.
Figure 7
Figure 7
Expression patterns of ABC transporter genes in developmental stages and tissues of soybean. The color scale bars on the bellow display the expression levels (median log2 (TPM+1)) of each gene. Red represents high expression levels, whereas yellow represents low expression levels.
Figure 8
Figure 8
Distribution of tissue-independent and tissue-specific genes in soybean. (A) The UpSet plot depicts how many GmABCs are expressed in each tissue (suspensor, cotyledon, hypocotyls, embryo, endosperm, seed coat, seedling, root, shoot, leaves, nodule, flower, pod, seed, and callus). Each color represents a tissue, and its length refers to the number of expressed genes. The black dots indicate the number of genes expressed in each tissue. The only dot (red) represents the number of genes unique to this tissue, and two or more dots connected by a line represent the number of genes expressed in several tissues. The green, blue, golden yellow, and pink lines connecting the dots represent the number of genes expressed in two, three, four, and five tissues, respectively. The dark line represents the number of genes expressed in at least six tissues. (B) The Venn diagram shows the specific expressed GmABCs in different tissues of soybean.
Figure 9
Figure 9
Time-dependent expression of seven GmABC gene expressions. The roots of soybean exposed to a 0.5 mM CaCl2 solution (pH 4.5) containing 50 μM AlCl3 for 0, 3, 6, 12, and 24 h were used for analysis. The expression was determined by qRT-PCR and β-tubulin was used as an internal control. The treatment without AlCl3 (0 μM AlCl3) was used for control. All data shown are means ± SD of three biological replicates. Bars with different lowercase letters indicate significant differences (p < 0.05).
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