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Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration

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Abstract

Members of basic helix-loop-helix (bHLH) gene family found in all eukaryotes play crucial roles in response to stress. Though, most eukaryotes carry the proteins of this family, biological functions of the most bHLH family members are not deeply evaluated in plants. In this study, we conducted a comprehensive genome-wide analysis of bHLH transcription factors in salt tolerant common bean. We identified 155 bHLH protein-encoding genes (PvbHLH) by using in silico comparative genomics tools. Based on the phylogenetic tree, PvbHLH genes were classified into 8 main groups with 21 subfamilies. Exon–intron analysis indicated that proteins belonging to same main groups exhibited a closely related gene structure. While, the PvbHLH gene family has been mainly expanded through segmental duplications, a total of 11 tandem duplication were detected. Genome-wide expression analysis of bHLH genes showed that 63 PvbHLH genes were differentially expressed in at least one tissue. Three of them displayed higher expression values in both leaf and root tissues. The in silico micro-RNA target transcript analyses revealed that totally 100 PvHLH genes targeted by 86 plant miRNAs. The most abundant transcripts, which were targeted by all 18 plant miRNA, were belonging to PvHLH-22 and PvHLH-44 genes. The expression of 16 PvbHLH genes in the root and leaf tissues of salt-stressed common bean was evaluated using qRT-PCR. Among them, two of PvbHLHs, PvbHLH-54, PvbHLH-148, were found to be up-regulated in both tissues in correlation with RNA-seq measurements. The results of this study could help improve understanding of biological functions of common bean bHLH family under salt stress. Additionally, it may provide basic resources for analyzing bHLH protein function for improving economic, agronomic and ecological benefit in common bean and other species.

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Authors and Affiliations

  1. Department of Agricultural Biotechnology, Faculty of Agriculture, Ondokuz Mayıs University, Samsun, Turkey

    Musa Kavas & Elif Seda Atabay

  2. Department of Genetics and Bioengineering, Faculty of Engineering and Architecture, Kastamonu University, Kastamonu, Turkey

    Mehmet Cengiz Baloğlu

  3. Department of Biology, Faculty of Science, Çankırı Karatekin University, Cankiri, Turkey

    Ummugulsum Tanman Ziplar & Turgay Ünver

  4. Department of Horticulture, Faculty of Agriculture, Çukurova University, Adana, Turkey

    Hayriye Yıldız Daşgan

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  1. Musa Kavas
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  2. Mehmet Cengiz Baloğlu
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  3. Elif Seda Atabay
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  4. Ummugulsum Tanman Ziplar
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  6. Turgay Ünver
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Correspondence to Musa Kavas.

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This study was supported by Research Fund of Ondokuz Mayıs University (PYO.ZRT.1901.13.017).

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Communicated by A. K. Tyagi.

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438_2015_1095_MOESM1_ESM.tif

Sup. Figure 1. Conserved amino acid motifs in the bHLH domains. The overall height of each letter and bar shows the conservation of the sequence at that position (TIFF 1473 kb)

Sup Figure 2. Percentage of bHLH genes on each bean chromosome to show their distribution abundance (JPEG 36 kb)

438_2015_1095_MOESM3_ESM.jpg

Sup Figure 3. Time of duplication and divergence (MYA) of PvbHLH genes. Time of duplication and divergence (MYA) rates were calculated with synonymous substitution rate (Ks) and estimated using tandem and segmental duplicated PvbHLH genes (JPEG 111 kb)

438_2015_1095_MOESM4_ESM.jpg

Sup Figure 4. Exon–intron structures of the PvbHLH genes. The bHLH family members were classified according to Fig. 1 (Phylogenetic tree). The values in parentheses show the number of corresponding clusters of bHLH genes. Yellow boxes represent exons and black lines represent introns (JPEG 2608 kb)

Sup Figure 5. Interaction between PvbHLHs and plant miRNAs (JPEG 878 kb)

Sup Figure 6. Relationship of Maximum Likelihood phylogenetic tree of the PvbHLH domains (PNG 3033 kb)

Table S1. Primer sequences of PvbHLH genes for qRT-PCR expression analysis (XLSX 11 kb)

Table S2. The characteristics of PvbHLH family genes in common bean (XLSX 28 kb)

Table S3. Summary of bHLH transcription family factors of plants (XLSX 9 kb)

Table S4. The Ka/Ks ratios and estimated divergence-time for tandemly-duplicated bHLH proteins (XLSX 10 kb)

Table S5. The Ka/Ks ratios and estimated divergence time for segmentally-duplicated bHLH proteins (XLSX 17 kb)

Table S6. Blast2Go annotation details of bHLH protein sequences (XLSX 20 kb)

Table S7. Expression patterns of the PvbHLH genes obtained from re-analyzing the RNA-Seq data (XLSX 34 kb)

Table S8. MDA and Proline content of salt-stressed and control tissues (XLSX 17 kb)

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Kavas, M., Baloğlu, M.C., Atabay, E.S. et al. Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genomics 291, 129–143 (2016). https://doi.org/10.1007/s00438-015-1095-6

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