Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa)

Abstract

Background: Squamous promoter binding protein-like (SPL) proteins are a class of transcription factors that play essential roles in plant growth and development, signal transduction, and responses to biotic and abiotic stresses. The rapid development of whole genome sequencing has enabled the identification and characterization of SPL gene families in many plant species, but to date this has not been performed in quinoa (Chenopodium quinoa).

Results: This study identified 23 SPL genes in quinoa, which were unevenly distributed on 18 quinoa chromosomes. Quinoa SPL genes were then classified into eight subfamilies based on homology to Arabidopsis thaliana SPL genes. We selected three dicotyledonous and monocotyledonous representative species, each associated with C. quinoa, for comparative sympatric mapping to better understand the evolution of the developmental mechanisms of the CqSPL family. Furthermore, we also used 15 representative genes from eight subfamilies to characterize CqSPLs gene expression in different tissues and at different fruit developmental stages under six different abiotic stress conditions.

Conclusions: This study, the first to identify and characterize SPL genes in quinoa, reported that CqSPL genes, especially CqSPL1, play a critical role in quinoa development and in its response to various abiotic stresses.

Keywords: Abiotic stress; Chenopodium quinoa; Genome-wide analysis; SPL gene family.

Fig. 1

A phylogenetic tree of SPL proteins from Chenopodium quinoa and Arabidopsis thaliana constructed using MEGA 7.0. The tree shows the division of SPL proteins into eight subfamilies. SPL proteins from C. quinoa are labeled in red and SPL proteins from A. thaliana are labelled in black

Fig. 2

Multiple sequence alignment of SBP domains of eight subfamilies of the CqSPL protein family. The Zn-finger (Zn-1, Cys3His; Zn-2, Cys2HisCys) and NLS structures are indicated

Fig. 3

Analysis of conserved motifs and gene structures in the phylogenetic tree of 23 CqSPL genes. A A phylogenetic tree was constructed using the amino acid sequences of the quinoa SPL genes using the NJ method. B Exons and introns are shown as yellow rectangles and gray lines, respectively. The SBP conserved domain and ANK region are clearly marked. 0, 1, and 2 indicate exon phase. C Ten conserved motifs predicted in SPL proteins are shown as differently colored boxes

Fig. 4

The distribution of 23 CqSPL genes on different chromosomes. The leftmost scale represents chromosome length. Green bars indicate chromosomes and to the left of each green bar is the chromosome number

Fig. 5

Analysis of interchromosomal fragment duplication of SPL genes in the quinoa genome. The colored lines represent all synthetic blocks and the red lines specifically indicate the duplicated pairs among the 23 CqSPL genes

Fig. 6

Phylogenetic relationships and motif compositions of SPL proteins of seven different plant species (C. quinoa, A. thaliana, S. lycopersicum, V. vinifera, S. bicolor, O. sativa, and Z. mays). A An unrooted phylogenetic tree was constructed using the neighbor-joining method as implemented by Geneious R11. B Distribution of the conserved motifs in SPL proteins. Ten differently colored boxes represent different motifs and their position in each SPL protein sequence (Table S2)

Fig. 7

Analysis of SPL genes found in Chenopodium quinoa and in six representative plant species (A. thaliana, S. lycopersicum, V. vinifera, S. bicolor, O. sativa, and Z. mays). Gray lines in the background indicate neighboring blocks in the genomes of C. quinoa and other plants; red lines highlight syntenic C. quinoa SPL gene pairs

Fig. 8

Gene expression of 15 CqSPL genes in various tissues and during fruit development. A Expression patterns of 15 CqSPL genes in flower, leaf, root, stem and fruit tissues as determined by qRT-PCR. Error bars represent standard error of three technical replicates. Lowercase letters indicate significant differences among treatment means (α = 0.05, LSD). B Positive numbers indicate positive correlations; negative numbers indicate negative correlations. Red numbers indicate statistically significant correlations (α = 0.05). C Expression patterns of 15 CqSPL genes at different developmental stages of quinoa fruit as determined by qRT-PCR (data shown are: 7 days post anthesis (DPA), 14 DPA, 21 DPA, 28 DPA, and 35 DPA). Error bars represent standard error of three technical replicates. Lowercase letters indicate significant differences among treatment means (α = 0.05, LSD). D Positive numbers indicate positive correlations; negative numbers indicate negative correlations. Red numbers indicate statistically significant correlations (α = 0.05)

Fig. 9

Expression analysis of 15 CqSPL genes in samples from root, stem, and leaf tissue of seedlings subjected to different abiotic stress treatments (i.e., UV radiation, flooding, PEG, NaCl, heat, and cold treatments). A Analysis of the relative expression of 15 CqSPL genes as determined by qRT-PCR. Error bars represent standard error of three technical replicates. Lowercase letters above the bar indicate statistically significant differences among means (α = 0.05, LSD). B Positive numbers indicate positive correlations; negative numbers indicate negative correlations. Red numbers indicate a statistically significant correlation (α = 0.05)