Genome-wide identification, evolution, and role of SPL gene family in beet (Beta vulgaris L.) under cold stress

Abstract

Background: SPL transcription factors play vital roles in regulating plant growth, development, and abiotic stress responses. Sugar beet (Beta vulgaris L.), one of the world's main sugar-producing crops, is a major source of edible and industrial sugars for humans. Although the SPL gene family has been extensively identified in other species, no reports on the SPL gene family in sugar beet are available.

Results: Eight BvSPL genes were identified at the whole-genome level and were renamed based on their positions on the chromosome. The gene structure, SBP domain sequences, and phylogenetic relationship with Arabidopsis were analyzed for the sugar beet SPL gene family. The eight BvSPL genes were divided into six groups (II, IV, V, VI, VII, and VIII). Of the BvSPL genes, no tandem duplication events were found, but one pair of segmental duplications was present. Multiple cis-regulatory elements related to growth and development were identified in the 2000-bp region upstream of the BvSPL gene start codon (ATG). Using quantitative real-time polymerase chain reaction (qRT-PCR), the expression profiles of the eight BvSPL genes were examined under eight types of abiotic stress and during the maturation stage. BvSPL transcription factors played a vital role in abiotic stress, with BvSPL3 and BvSPL6 being particularly noteworthy.

Conclusion: Eight sugar beet SPL genes were identified at the whole-genome level. Phylogenetic trees, gene structures, gene duplication events, and expression profiles were investigated. The qRT-PCR analysis indicated that BvSPLs play a substantial role in the growth and development of sugar beet, potentially participating in the regulation of root expansion and sugar accumulation.

Keywords: Abiotic stress; Beta vulgaris; Gene expression; Genome-wide analysis; SPL gene family.

Fig. 1

(A) Phylogenetic tree of the relationship between Beta vulgaris and Arabidopsis thaliana SPL proteins. Different block colors represent different subgroups, with green stars representing Arabidopsis thaliana and red triangles representing Beta vulgaris in the legend. (B) Multiple sequence alignment of the SBP domains of different subgroups of Beta vulgaris and Arabidopsis thaliana

Fig. 2

Phylogenetic relationship, gene structure, motif distribution, and cis-acting elements of sugar beet SPL genes. Among them, the number marked on the Node represents the confidence level. (A) Phylogenetic tree of the sugar beet SPL family, each node has 1000 repetitions. (B) Schematic diagram of the gene structure of sugar beet SPL genes, including UTR (untranslated region), CDS (coding sequence), domains (SBP, ANK domains), and introns (Number indicates the phase of the corresponding intron.). Light green represents UTR, yellow represents CDS, pink represents the structural domain SBP, and dark green represents structural domain ANK. (C) Conserved amino acid motifs (motifs 1–10) in BvSPL proteins: the line represents the relative length of the protein. (D) Cis-acting elements in the 2000 bp promoter sequence upstream of the BvSPL genes; different color blocks represent different cis-acting elements

Fig. 3

(A) Distribution of the eight BvSPL genes in beet chromosomes, with gene density on chromosomes (Bin size = 100,000). (B) Chromosome distribution and gene duplication relationship of sugar beet SPL genes. The colored lines represent gene pairs between different chromosomes: the red line represents the BvSPL gene pair; from the inside out, the first and second outer circles are chromosome density (Bin size = 100,000), the third is the chromosome; the chromosome color is consistent with the gene pair line color on the chromosome

Fig. 4

(A) Collinearity analysis of beet with six plants (Arabidopsis thaliana, Solanum lycopersicum, Fagopyrum tataricum, Oryza sativa, Zea mays, and Sorghum bicolor). Red lines represent the species’ beet SPL genes and gene pairs, and gray represents collinear blocks in the beet and the species’ genomes. (B) The phylogenetic tree and motif composition of the SPL proteins of beet and six plants (Arabidopsis thaliana, Solanum lycopersicum, Fagopyrum tataricum, Oryza sativa, Zea mays, and Sorghum bicolor). Different module colors represent different motifs. The numbers on the evolutionary tree represent confidence levels. Red fonts represent BvSPL

Fig. 5

(A) Relative expression levels and gene expression correlations of BvSPL genes in beet seedling roots, stems, and leaves at 0 h, 2 h, and 24 h under eight types of abiotic stress detected using quantitative real-time polymerase chain reaction (qRT-PCR). The lowercase letters above the bars indicate significant treatment differences (α = 0.05, LSD). The expression level of BvSPL gene was normalized to the expression level of BvACTIN, and its relative expression level was displayed at 0 h, 2 and 24 h. (B) Correlation of BvSPL gene expression under eight types of abiotic stress. The expression values of the color gradient mapping from low (blue) to high (red) on the right side of the figure. (C) Predicted protein–protein interaction network of beet BvSPL proteins within the beet. Orange represents BvSPL proteins; blue represents other proteins within the beet; the larger the circle, the more interacting proteins there are

Fig. 6

(A) The expression patterns of eight SPL genes in mature sugar beet roots, stems, and leaves were detected using quantitative real-time polymerase chain reaction (qRT-PCR) technology. The lowercase letters above the bars indicate significant differences between treatments (α = 0.05, LSD). The expression level of BvSPL gene was normalized to the expression level of BvACTIN, and its relative expression level was displayed at 0 h, 2 and 24 h. (B) Correlation analysis of the expression of BvSPL genes in mature beet. The expression values of the color gradient mapping from low (blue) to high (red) on the right side of the figure