Genome-Wide Analysis of the MADS-Box Transcription Factor Family in Solanum lycopersicum

Abstract

MADS-box family genes encode transcription factors that are involved in multiple developmental processes in plants, especially in floral organ specification, fruit development, and ripening. However, a comprehensive analysis of tomato MADS-box family genes, which is an important model plant to study flower fruit development and ripening, remains obscure. To gain insight into the MADS-box genes in tomato, 131 tomato MADS-box genes were identified. These genes could be divided into five groups (Mα, Mβ, Mγ, Mδ, and MIKC) and were found to be located on all 12 chromosomes. We further analyzed the phylogenetic relationships among Arabidopsis and tomato, as well as the protein motif structure and exon-intron organization, to better understand the tomato MADS-box gene family. Additionally, owing to the role of MADS-box genes in floral organ identification and fruit development, the constitutive expression patterns of MADS-box genes at different stages in tomato development were identified. We analyzed 15 tomato MADS-box genes involved in floral organ identification and five tomato MADS-box genes related to fruit development by qRT-PCR. Collectively, our study provides a comprehensive and systematic analysis of the tomato MADS-box genes and would be valuable for the further functional characterization of some important members of the MADS-box gene family.

Keywords: MADS-box; floral organ; fruit development; genome-wide analysis; tomato.

Figure 1

Gene structure analysis of MADS-box genes in tomato. The Gene Structure Display Server (GSDS) database was used to perform the exon–intron structure analyses. Lengths of exons and introns of each MADS-box gene were displayed proportionally. The blue boxes represent upstream/downstream, the yellow boxes represent exons, and the black lines represent introns.

Figure 2

Conserved motif analyses of MADS-box genes in tomato. All the conserved motifs were identified by the Multiple EM for Motif Elicitation (MEME) database using the complete amino acid sequences of tomato MADS-box genes. Ten conserved different motifs were indicated by different colors. The details of motifs refer to the Supplementary Figure S2.

Figure 3

Chromosomal locations of tomato MADS-box genes. A total of 12 chromosomes of tomato were labeled with their names, chromosomes 1 to 12, which are indicated at the top of each bar. The position of tomato MADS-box genes on the chromosome was based on the Sol Genomics Network (SGN) and National Center for Biotechnology Information (NCBI) database and the Tomato-EXPEN 2000 was used to draw the physical map of the tomato MADS-box genes.

Figure 4

Heat map representation of tomato MADS-box genes in various tissues. The tissues included the whole root (Rt), young leaf (YL), mature leaves (ML), young flower buds (YFB), and fully open flowers (F), which were at the immature green (IMG), mature green (MG), break (B), and mature (MF) stages of fruit development and ripening. The bar at the bottom of the heat map represents relative gene expression values.

Figure 5

Expression profiles of floral organ identity genes in the four-whorl floral organs of the wild-type (WT) tomato plant for qPCR analysis. Se, sepal; Pe, petal; St, stamen; Ca, carpel. (A)–(O) Expression profiles of SlMADS-MC, SlMBP21, TAP3, SlMBP2, SlMBP1, TM6, TAG1, TAGL1, SlMBP3, SlMBP22, TAGL2, TM5, SlMBP6, SlMADS1 and SlMBP21.Each value represents the mean ± SE of three technical replicates of a single biological sample. The SlCAC gene of tomato was used as the internal standard.

Figure 6

Relative expression of tomato MADS-box genes in difference stages of fruit development and ripening by qPCR analysis. Expression patterns of SlMBP3 (A), MADS-RIN (B), TAGL1 (C), TM4 (D), and SlMBP7(E) in different organs, including mature green (MG), break (B), four days after break (B+4), and seven days after break (B+7). Each value represents the mean ± SE of three technical replicates of a single biological sample. The SlCAC gene of tomato was used as the internal standard.