Next Article in Journal
The Effect of Low-Growing Rootstocks on the Adaptability and Productivity of Sour Cherry Varieties (Prunus cerasus L.) in Arid Conditions
Next Article in Special Issue
Metabolome and Transcriptome Analyses Unravels Molecular Mechanisms of Leaf Color Variation by Anthocyanidin Biosynthesis in Acer triflorum
Previous Article in Journal
Changes of Fruit Abscission and Carbohydrates, Hormones, Related Gene Expression in the Fruit and Pedicel of Macadamia under Starvation Stress
Previous Article in Special Issue
An Integrative Volatile Terpenoid Profiling and Transcriptomics Analysis in Hoya cagayanensis, Hoya lacunosa and Hoya coriacea (Apocynaceae, Marsdenieae)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 8
Issue 5
10.3390/horticulturae8050399
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Genome-Wide Identification and Expression Analysis of RR-Type MYB-Related Transcription Factors in Tomato (Solanum lycopersicum L.)

by
Jiaying Sun
and
Changkui Guo
*
Collaborative Innovation Center for Efficient and Green Production of Agriculture in Mountainous Areas of Zhejiang Province, College of Horticulture Science, Zhejiang Agriculture and Forestry University, Hangzhou 311300, China
*
Author to whom correspondence should be addressed.
Horticulturae 2022, 8(5), 399; https://doi.org/10.3390/horticulturae8050399
Submission received: 18 March 2022 / Revised: 28 April 2022 / Accepted: 28 April 2022 / Published: 2 May 2022
(This article belongs to the Special Issue Genomics and Bioinformatics Applications in Horticulture)
Browse Figures
Versions Notes

Abstract

:
Evidence have indicated that RR-type MYB-related transcription factors (TFs) are functionally diverse in regulating floral development, fruit development, leaf senescence, ABA response, and drought and salt responses. Several RR-type MYB-related TFs in Arabidopsis, Antirrhinum and rice are identified and characterized. However, the complete RR-type MYB-related family in tomato has not been studied to date. Here, a genome-wide identification of tomato RR-type MYB-related TFs (SlMYBR) was performed by bioinformatics analysis, and their expression patterns were analyzed. A total of thirteen SlMYBR genes, which were mainly distributed in the head or tail of the chromosome, were identified from tomato and were divided into three groups. Group II was all MYBR genes from eudicots without genes from monocots. For Group I and Group III, the phylogenetic tree was in accord with the evolutionary relationship of these species. SlMYBR proteins were unstable proteins and located in the nucleus. The promoters of SlMYBR contained multiple important cis-acting elements related to abiotic stress or hormone responses. SlMYBR genes had various temporal and spatial expression patterns. Experiments of spraying exogenous hormone demonstrated that the expression of most genes containing hormone response elements was changed, indicating that the expression patterns were associated with the amount of cis-acting elements. The comprehensive investigation of tomato SlMYBR genes in the present study helps to clearly understand the evolution of RR-type MYB-related TFs and provides a useful reference for the further functional study of SlMYBR genes in tomato.

1. Introduction

In long-term evolution, plants have evolved a variety of mechanisms and complex signal networks to quickly perceive the external unpredictable environment [1]. Of them, the fast changed gene expression against harsh conditions is critical for resisting various biological and abiotic stresses. Therefore, how to rapidly mediate the gene expression under stresses is an important scientific issue. Transcription factors (TFs) are DNA binding proteins that can specifically and directly bind to cis-acting elements of genes to activate or inhibit gene transcription [2]. When plants are subjected to abiotic stresses, the activated transcription factors directly induce or repress the expression of responsive genes to respond to stresses for their survival [3].
The MYB (v-myb avian myeloblastosis viral oncogene homolog) TF family, as one of the largest and most diverse TF families, are widely distributed in higher plants [4]. The MYB gene (v-MYB) is firstly identified from the avian myeloblastosis virus (AMV) [5]. Thereafter, three v-MYB-related genes are found in many vertebrates, and are involved in the regulation of cell proliferation, differentiation and apoptosis [6]; the first plant MYB gene, C1, is isolated from maize (Zea mays), which functions in the biosynthesis of anthocyanin and flavonoids, and trichome differentiation [7]. The widely recognized classification standard of MYB protein is based on the existence of one to four repeats in its sequence with about 52 amino acid residues for each repeat [8]. Each repeat is formed by three α-helices with a helix-turn-helix (HTH) structure containing three regularly spaced tryptophan residues. And the third helix has a recognition helix for binding directly to the major groove of DNA [9,10,11,12]. According to the number of repeats, the MYB family is divided into four groups: 4R-MYB, R1R2R3-MYB, R2R3-MYB and MYB-related [4,13,14,15].
The R2R3-MYB group genes have been extensively studied; whereas the MYB-related genes have attracted little attention. Of the MYB-related genes, there is an RR-type MYB-related subfamily containing two separated MYB repeats with a highly conserved SHAQKY amino acid signature motif in the second MYB domain. This conserved motif was not similar to the sequence of the third helix in the common HTH structure. More specifically, these two MYB domain repeats were not connected in series, but separated by 39 amino acids. Some studies have demonstrated that RR-type MYB-related TFs are functionally diverse in regulating floral development, fruit development, leaf senescence, ABA response, drought and salt responses [16,17,18,19,20,21,22].
DIVARICATA (DIV) encodes RR-type MYB-related TF [20]. In Antirrhinum, the AmDIV is only expressed in the ventral portion of the corolla, and is reported in the control of dorsoventral asymmetry during flower zogomorphy by promoting the growth of ventral petals and their adjacent areas [16,17]. Further study shows that RADIALIS (RAD) prevents DIV and DRIF (DIV-and-RAD-INTERACTING FACTOR) heterodimer complexes to control ventral floral identity [18,19,20]. AtDIV2 negatively modulates salt tolerance and sensitivity to exogenous ABA in seed germination by attenuating the ABA signaling genes in Arabidopsis [21]. Another RR-type MYB-like TF, AtMYBL (or called MYBS1), also functions in response to salt stress and ABA, and promotes leaf senescence [22]. Moreover, both MYBS1 and MYBS2 bind to a sugar response element, the TA-box (TATCCA), and control sugar- and ABA-regulated seed germination and seedling development by the regulation of glucose-responsive gene and ABA signaling gene expression in opposite ways [23]. In rice, MID1 (MYB Important for Drought Response1), encoding a putative RR-type MYB-like TF, is mainly expressed in root and leaf vascular tissues, and can improve anther development and rice yield under drought by directly binding to the promoters of drought-related genes and anther developmental gene [1]. The precise expression regulation of genes is greatly important for balancing the relationships between stresses and plant growth [24,25]. For example, reactive oxygen species (ROS), induced by abiotic stresses, can control flower development, and also can kill the plants when they are overproduced, suggesting that the homeostasis of ROS is critical for plant development [1]. There is evidence that RR-type MYB-related TFs are of significance in this balance, for their expressions are related with environmental changes or exhibit phase-specific and tissue-specific behavior [16,21,22,26].
Tomato (Solanum lycopersicum L.) is an important horticultural crop all over the world, with total global tomato production, 1.87 × 108 tons, in 2020 (https://www.fao.org/faostat/en/#data/QCL, accessed on 27 January 2022). Tomato is considered as a common model plant in horticultural study. Since 1999, the first tomato (Lycopersicon esculentum) RR-type MYB, LeMYBI, has been cloned and characterized [27]. As reported, some RR-type MYBs function in fruit development in tomato [26,28]. However, genome-wide identification and expression analysis of RR-type MYB-related TFs in tomato have no detailed report. In the present study, thirteen RR-type MYB-related TFs were identified by bioinformatics methods; comprehensive analyses in terms of gene structure and conserved motifs, cis-acting elements, phylogenetic analysis, and expression analysis of the RR-type MYB-related genes under hormone-treatment conditions were performed. This study helps to understand clearly the evolution of RR-type MYB-related TFs, and provides fundamental clues for future cloning and functional studies of this subfamily.

2. Materials and Methods

2.1. Data Search and Phylogenetic Analysis

To identify the RR-type MYB-related TFs (SlMYBR) in tomato, the Arabidopsis RR-type MYB domain was used as the query to search the tomato genome databases. Nine RR-type MYB-related TFs of Arabidopsis thaliana [18] were used as queries to BLAST with S. lycopersicum, S. tuberosum, Amborella trichopoda, Brachypodium distachyon, Z. mays, Oryza sativa, Vitis vinifera, Cucumis sativus, Malus domestica and Citrus clementina genomes (E-value < e−50) in NCBI (https://www.ncbi.nlm.nih.gov/, accessed on 20 October 2021). The phylogenetic tree of the searched RR-type MYB-related TFs was constructed by neighbor-joining method. The online software EvolView [29] (https://evolgenius.info//evolview-v2/, accessed on 17 March 2022) is used to beautify the phylogenetic tree.

2.2. Collinearity Analysis

To analyze the evolutionary process of SlMYBR genes, tomato and S. lycopersicum, the closest related diploid to tomato and A. thaliana, the model plants were selected for the comparison of gene structures between them to explore the clues to the evolutionary gene events caused by polyploidization. The whole genome FASTA and GFF3 files of A. thaliana (TAIR10), S. lycopersicum (SL3.0) and S. tuberosum (SolTub_3.0) were downloaded from the Ensembl Plants (http://plants.ensembl.org/index.html, accessed on 29 September 2021) website. The analysis software TBtools (https://github.com/CJ-Chen/TBtools/releases, accessed on 30 September 2021) [30] was used to analyze the collinearity among species.

2.3. Analysis of the Physical and Chemical Properties

Gene and protein sequences of RR-type MYB-related TFs were downloaded from Phytozome [31] (https://phytozome-next.jgi.doe.gov/, accessed on 11 September 2021). The online tool ExPASy (http://web.expasy.org/protparam/, accessed on 11 September 2021) was used to predict the physicochemical properties of RR-type MYB-related TFs, including isoelectric points (pI), molecular weight (Mw) and instability index. The online website Cell-PLoc 2.0 [32] (http://www.csbio.sjtu.edu.cn/bioinf/Cell-PLoc-2/, accessed on 11 September 2021) was used to predict subcellular localization.

2.4. Analysis of Gene Structure and Conserved Motifs

A traditional phylogenetic tree was constructed using the selected RR-type MYB-related TFs. The tomato genome database in NCBI website was downloaded. RR-type MYB-related sequences of tomato were aligned and the conserved domains were investigated by using the sequence analysis software Clustal X2. The gene structure and conserved motifs of tomato RR-type MYB-related TFs were analyzed by online website MEME [33,34] (http://meme-suite.org/tools/meme, accessed on 26 August 2021) and TBtools [30].

2.5. Cis-Acting Elements of Gene Promoter

The 2000-bp upstream sequences of thirteen RR-type MYB-related TF genes in tomato were obtained. Their cis-acting elements were predicted by the online website PlantCARE [35] (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 23 September 2021).

2.6. Expression Pattern Analysis

The transcriptome data of root (SRR363116), stem (SRR363117), leaf (SRR363118), flower (SRR363119), fruit mature green (SRR363120), fruit breaker (SRR363121), fruit ripe (SRR363122) in tomato were obtained from NCBI database. These published transcriptomic data [36] were downloaded for expression analysis. All RNA-Seq data were qualitatively controlled by FastQC to obtain cleaned reads. The gene expression was further calculated and analyzed by Kallisto software. The expression level (TPM value) of RR-type MYB-related TF genes was obtained. TPM value was transformed into Log2(TPM + 1) by TBtools. And the heat map of SlMYBRs expression was constructed.

2.7. Plant Materials and Growth Condition

Tomato ‘Micro-Tom’ seeds were immersed in 55 °C water for 30 min to kill pathogens, then sown to the sterilized soil media (one soil with one vermiculite) supplied with the 4-g fertilizer per plate, and transferred to the greenhouse (at 22 °C under long day condition with 10-h light and 14-h dark cycles, 120 μmol·m−2·s−1 LED light intensity, and about 60% humidity). One seed was sown in one pot, which was covered by a transparent plastic film for two days. The transferred day was recorded as the first day.

2.8. Exogenous Hormone Treatment

For the hormone-treatment assay, 25-day-old tomato plants were divided into three groups; they were evenly sprayed with 0.1 mM gibberellic acid (GA), 0.5 mM salicylic acid (SA) and 0.1 mM abscisic acid (ABA), respectively; thereafter, they were covered with a black plastic bag and transferred to greenhouse. Leaf samples were harvested at 0 h, 1 h, 3 h, 6 h, 12 h and 24 h after hormone-treatment, respectively. All experimental samples were frozen by liquid nitrogen and then stored at −80 °C before use. This experiment was done more than three times.

2.9. RNA Isolation and qRT-PCR Analysis

The tomato leaves under different treatments were harvested and were ground to powder in liquid nitrogen. Total RNAs were isolated using RNAiso Plus reagent (9108Q, Takara) and then treated with gDNA Eraser (RR047A, Takara Bio Inc., Dalian, China) to remove genomic DNA according to the manufacturer’s protocol. cDNA synthesis and qRT-PCR for mRNA were performed as previously reported [25,37]. Reverse transcription was done as follows: 42 °C for 2 min to remove gDNA, 37 °C for 15 min to reverse transcription reaction, and following 85 °C for 5 s to inactivate the reverse transcriptase. qRT-PCR was performed in 20 μL TB Green® PCR mixtures (RR420A, Takara Bio Inc., Dalian, China) including 10 μL TB Green Premix Ex Taq (Tli RNaseH Plus, Takara Bio Inc., Dalian, China) (2×), 0.4 μL ROX Reference Dye (50×), 1 μL primer mix, 1 μL template, and 7.6 μL ddH2O. qRT-PCR reaction were as follows: 45 cycles of 95 °C for 10 s, 60 °C for 15 s, and 72 °C for 25 s; and the following dissociation stage. The reactions were performed on an ABI StepOnePlus Real-Time PCR System (Applied Biosystems, Bedford, MA, USA). According to SlMYBR mRNA sequences, specific quantitative primers (Table S1) were designed using Beacon Designer 7 software. The S. lycopersicum SlACT gene was selected as the internal control. All experiments had triple biological replicates.

2.10. Statistical Analysis

Statistically significant differences were done using IBM SPSS Statistics software 22.0 by Student’s t-test. The data are present as means of three biological replicates ± SD (standard deviation).

3. Results

3.1. Identification and Characteristics of RR-Type MYB-Related TFs in Tomato

To identify the RR-type MYB-related genes in tomato, the Arabidopsis RR-type MYB domain was used as a query to search the tomato genome database and BLASTP program. Thirteen SlMYBR genes were identified and used for further analysis. We named these SlMYBRs as SlMYBR1 to SlMYBR13 in the light of their chromosomal locations (Table 1). The detailed information about the SlMYBRs was inferred by ExPASy server. The length of the SlMYBR proteins varied from 91 amino acids (aa) (SlMYBR13) to 619 aa (SlMYBR12). The length of most SlMYBR proteins ranged from 200 aa to 300 aa. The Mw of the proteins ranged from 10,469.70 Da to 65,667.07 Da. The range of theoretical isoelectric point (pI) was 4.88 to 9.14, including eight acidic proteins and five basic proteins. The theoretical instability index of these thirteen SlMYBR proteins was more than 40, which implied that they were unstable proteins. The subcellular localization results indicated that all SlMYBR proteins localized in the nucleus (Table 1).
The chromosome distribution information of SlMYBR genes demonstrated that thirteen SlMYBR genes are located to the eight chromosomes (3rd, 4th, 5th, 6th, 9th, 10th, 11th and 12th) of tomato and are distributed at the head or tail of these chromosomes, which was also the place with high gene density (Table 1; Figure 1). On the 4th, 6th, 10th and 12th chromosomes, only one SlMYBR gene were found, respectively. The 3rd, 5th and 11th chromosomes contain two SlMYBR genes, respectively. Three SlMYBR genes were searched on the 9th chromosome containing the highest density of SlMYBR genes (Table 1; Figure 1). The distribution of SlMYBR genes did not completely meet with the MYBR classification (Figure 2). A gene pair, SlMYBR7 and SlMYBR8, with a close proximity localization (about 13-kb separation) on the ninth chromosome belong to Group II; whereas SlMYBR11 and SlMYBR12 (Group II) are distributed on the head or tail of the 11th chromosome separated by more than 53 Mb (Table 1; Figure 2). Moreover, the duplication genes of SlMYBR7 and SlMYBR8, which are clustered on the ninth chromosome, were identified as tandem duplicates, suggesting that the tandem duplication probably contributes to the expansion of the tomato SlMYBR genes.

3.2. Phylogenetic and Synteny Analysis of RR-Type MYB-Related TFs

A total of 97 RR-type MYB-related homologs from 10 representative species, including basal angiosperm (A. trichopoda), eudicots (S. lycopersicum, S. tuberosum, C. sativus, V. vinifera, M. domestica, and C. clementina) and monocots (B. distachyon, Z. mays, and O. sativa), were selected for phylogenetic analysis of RR-type MYB-related TFs. The phylogenetic tree of RR-type MYB-related TFs was constructed using the neighbor-joining method (Figure 2). The phylogenetic results showed that MYBR genes from these different species were classified into three groups (I to III). As expected, SlMYBRs displayed a relatively closer relationship with the MYBR proteins from S. tuberosum. Group I and II contained five SlMYBR genes, respectively, and Group III had three SlMYBR genes. For the Group I and III, MYBR genes from eudicots and monocots were included, showing that the phylogenetic tree was in accord with the evolutionary relationship of these species. While in Group II, MYBR genes were all from eudicots, suggesting that they were eudicot-specific genes or this branch was lost in monocots resulting from gene loss events in the other evolutionary clade when eudicots and monocots are separated. Among the Group II eudicot-specfic MYBR genes, five belong to tomato (SlMYBR5: Solyc05g055240; SlMYBR7: Solyc09g007570; SlMYBR8: Solyc09g007580; SlMYBR11: Solyc11g006720; and SlMYBR12:Solyc11g071500). SlMYBR7 and SlMYBR8 were considered as tandem duplication genes for the expansion of the tomato SlMYBR genes, indicating that it is a clue to evolutionary gene event. SlMYBR5 (or called SlDIVlike5/SlMYBI) is expressed throughout the developing fruit, suggesting the biological significance of eudicot-specfic MYBR genes in fruit development of eudicots.
To further analyze the evolutionary process of SlMYBR genes, a comparative analysis of genome synteny blocks between A. thaliana, S. lycopersicum and S. tuberosum was performed using TBtools. A total of 15 syntenic gene pairs between A. thaliana and S. lycopersicum were found, and a total of 19 syntenic gene pairs between S. lycopersicum and S. tuberosum were searched (Figure 3, Table S2). Moreover, we found only one tandem duplication (SlMYBR7/SlMYBR8) event (Table 1, Figure 3) in the SlMYBR subfamily.

3.3. Gene Structure and Conserved Motifs Analysis of RR-Type SlMYBR Genes

To better understand the genetic diversity of the SlMYBR genes, the intron and exon of SlMYBR genes were analyzed by aligning between the mRNA and corresponding genomic sequence. The SlMYBR TFs were divided into three groups based on their structure. Eleven SlMYBR genes contain two exons, except that the SlMYBR7 in group I has four exons and the SlMYBR13 in group III contains only one exon (Figure 4).
Ten conserved motifs of RR-type SlMYBR TFs were analyzed by MEME software (Figure 4). Eleven SlMYBRs contained continuous Motif 4 and Motif 2, whereas SlMYBR7 and SlMYBR8 contained only Motif 2. Two members (SlMYBR2 and SlMYBR3) in group II showed similar gene structure and protein conservation motif. Twelve members contained Motif 1, which was composed of about 50 amino acids, except SlMYB13 (Figure 5). According to the results of multiple sequence alignment (Figure 6), there were two MYB-like binding domains at the N-terminal and C-terminal of RR-type SlMYBR proteins, respectively. Motif 4 and Motif 2 together with five to six additional amino acids between them constituted the first MYB domain. Motif 4 was highly similar to I-box-like protein [18]. Motif 1 constituted the second MYB domain, and there was indeed a highly conserved SHAQKY amino acid signature motif at the third helix. Motif 1 was highly similar to CCA1-like protein [38]. Therefore, we believed that it was the reason why SlMYB7, SlMYBR8 and SlMYBR13 were classified as RR-type SlMYBR TFs even if they both had only one MYB-like domain. Only SlMYB7 and SlMYB8 in group I contained Motif 8. Two genes, SlMYBR5 and SlMYBR11, in group II, contained Motif 6. Members in group III except SlMYBR13 contained Motif 9. The differential distribution of these conserved motifs might be caused by the process of evolution. It might also be the reason behind their functional diversity.

3.4. Cis-Acting Elements of SlMYBR Promoters

Cis-acting element is a sequence that exists in the side sequence of gene and can affect gene expression. RR-type MYB-related TFs were widely involved in hormone, abiotic stress and other signal transduction pathways. We used the online software PlantCARE to predict the cis-acting elements of the 2000-bp sequence upstream of the start codon of SlMYBR genes (usually regarded as the promoter region of gene) to find out which hormones and abiotic stresses affect their expressions.
The predicted data indicated that the promoter regions of SlMYBRs contained lots of cis-acting elements, including light responsive elements (G-Box, I-Box, GT1-motif and AT1-motif), drought-induced element (MYB binding site, MBS), abscisic acid response element (ABRE), gibberellin response element (P-box), salicylic acid response (TCA-element), methyl jasmonate response elements (CGTCA-motif and TGACG-motif), ethylene response element (ERE), the low-temperature response element (LTR), defense and stress responsive site (TC-rich repeats) and the common cis-acting element CAAT-box. Of thirteen SlMYBR genes, SlMYBR9 as the least one had 19 cis-acting elements, whereas SlMYB11 as the most one had 44 cis-acting elements (Figure 7, Table S3). All SlMYBR genes contained light responsive cis-acting element and enhancer cis-acting element CAAT-box, suggesting that SlMYBRs might respond to light. Among them, nine out of thirteen had ABRE and ERE elements; six out of thirteen contained CGTCA-motif, TGACG-motif and MBS elements; five out of thirteen contained P-box and LTR element; four genes contained TCA-element and TC-rich repeats (Figure 7, Table S3), indicating that SlMYBRs possibly functioned in response to hormones and abiotic stresses.

3.5. Expression Profiles Analysis of SlMYBR Genes

To study spatiotemporal expression patterns of SlMYBR genes, transcriptomic data of different tissues were analyzed (Figure 8). SlMYBR2, SlMYBR5 and SlMYBR11 genes were detected in all tested tissues. SlMYBR2 was highly expressed in leaf and fruit ripe stages; SlMYBR5 was mainly expressed in fruit mature green and fruit breaker stages; SlMYBR11 was mainly expressed in the ripe fruit stage. The expression of SlMYBR4 and SlMYBR6 were higher in the fruit mature green stage. These results indicated that SlMYBR2, SlMYBR4, SlMYBR6, SlMYBR5 and SlMYBR11 genes might mainly function in fruit development in tomato. SlMYBR1 and SlMYBR11 had a high expression level in roots, implying that they both might play roles in root development. The expression of SlMYBR10 was distinguished in stems, suggesting that it might be important for the cell differentiation and division. SlMYBR9 was detected in vegetative tissues, including roots, stems and leaves, with low levels in reproductive tissues, showing that it possibly functioned in the regulation of vegetative development. In Group II, SlMYBR7 and SlMYBR8, as tandem-duplication genes, were both expressed with low level in all tested tissues; the expression of SlMYBR12 also exhibited low levels in all tested tissues, whereas the expression of SlMYBR5 and SlMYBR11 was higher than others in Group II. This result indicated that SlMYBR5 and SlMYBR11 were main functional genes in Group II, and anther three genes might have redundant or complementary functions to fit the plant development and environmental changes.

3.6. Expression Pattern of SlMYBRs under Different Hormones Treatment

As mentioned above (Figure 7), the promoters of SlMYBR genes contained a variety of cis-elements in response to hormones, including GA, SA and ABA. To test if these cis-elements were associated with their expression under hormone-treatment, the tomato seedlings were dealt with GA, SA and ABA hormones, and the expression of SlMYBRs was examined by real-time PCR.
SlMYBR1, SlMYBR3, SlMYBR7, SlMYBR8 and SlMYBR9, respectively, had only one gibberellin response element (Figure 7, Table S3). The results (Figure 9A) showed that there were very significant changes after GA treatment for 1 h and 3 h. The expression of SlMYBR1 and SlMYBR3 reached the maximum at 1 h and 6 h after GA-treatment, and then was decreased remarkably. The expression of SlMYBR9 was decreased gently. At 24 h the expression of SlMYBR1, SlMYBR3 and SlMYBR9 was down-regulated by 0.21, 0.13 and 0.16 times, respectively, under GA-treatment. And both SlMYBR1 and SlMYBR9 were in group III. The expression of SlMYBR7 was decreased after the maximum at 12 h.
SlMYBR1, SlMYBR2, SlMYBR5 and SlMYBR6 all contained salicylic acid response element, and only SlMYBR6 contained two salicylic acid response elements (Figure 7, Table S3). SA-treatment results (Figure 9B) showed that the expression of SlMYBR1 was increased slightly at 1 h and decreased significantly at 3 h. After fluctuation, the final expression of SlMYBR1 was down-regulated, which was almost the same as that at 3 h. The expression of SlMYBR2 was decreased significantly at 1 h. The expression of SlMYBR5 was increased remarkably at 1 h. The expression of SlMYB6 was not changed significantly at 1 h and 3 h, but it was increased significantly at 6 h.
Under ABA treatment, we measured the gene expression at 0 h and 24 h (Figure 9C). Among the nine genes containing abscisic acid response element (Figure 7, Table S3), the expression of SlMYBR4, and SlMYBR11 were up-regulated by six and 10 times, respectively. The expression of the other six genes (SlMYBR1, SlMYBR2, SlMYBR3, SlMYBR6, SlMYBR7, and SlMYBR10) was down-regulated. It could be noted that the expression of genes (SlMYBR1, SlMYBR6, SlMYBR10) with only one response element was decreased more than that of genes (SlMYBR2, SlMYBR3, SlMYBR7) with multiple response elements. Furthermore, these genes with only one response element were in group III, whereas genes with multiple response elements were in group I.

4. Discussion

Tomato, an annual herb, is considered as one of the most important vegetables and fruits, and is widely planted in the world [39]. To meet social needs, the improvement of tomato variety in flavor and stress-tolerance is urgently needed [40]. Thus it is of great importance to uncover the significant gene resources in regulating fruit quality and stress-tolerance in tomato. Previous studies have shown that RR-type MYB-related TFs play important roles in fruit development and abiotic-stress responses [1,26,28]. In the present report, we completely investigated the RR-type MYB-related TFs in tomato (SlMYBR) and analyzed their expression patterns in different tissues and under hormone treatment. In total, thirteen SlMYBRs were found, which is more than reported before [28]. And we found some hormone-response SlMYBR genes (SlMYBR1-7, SlMYBR9 and SlMYBR10) and some tissue-specific SlMYBR genes (SlMYBR1, SlMYBR4, SlMYBR5, SlMYBR6, SlMYBR10 and SlMYBR11) which may be useful for the tomato variety breeding.
Herein, based on phylogenetic and gene structure analysis, thirteen SlMYBR genes were divided into three groups. The SlMYBR genes with similar gene structure and functions clustered into a group, suggesting that they possibly underwent common evolutionary origins and had a similar evolution in their functions [41]. We found a particular group, group II, with no MYBR genes, from the monocots. The genes in group II might regulate eudicot-specific traits, or they were preserved to increase the balance of development for eudicots. One gene duplication event (tandem duplication) occurred in the SlMYBR family, and one paralogous gene pair (SlMYBR7 and SlMYBR8 genes) was produced, which is important for evolution and gene expansion and helps to coordinate different developmental processes. Moreover, the structures and motifs of SlMYBR were conserved with a MYB-like DNA binding domain in the N-terminal (I-box-like) and a highly conserved SHAQKY motif in the C-terminal (CCA1-like), indicating that the SlMYBR family might have similar functions.
So far, there is little functional study on the SlMYBR genes in tomato. Generally, the gene functions are closely linked to their expression pattern; and the gene expressions are tightly associated with the cis-elements in promoters. In token SlMYBR1, as an example, it was mainly expressed in the roots, and repressed by GA, SA and ABA, demonstrating that SlMYBR1 possibly functioned in the regulation of root development by response to some hormones. SlMYBR5 had a high expression level in fruit development process, indicating that they might play critical roles in regulating fruit development. SlMYBR5, also known as SlMYBI/SlDIV5, competes with FSM1 (SlRAD) for FSB1 (SlDRIF5) binding to regulate fruit development, which is conserved and present in Solanales [26,28]. In addition, RAD, DIV and DRIF are expressed in snapdragon ovaries and developing fruit, the same as these in tomato [26], suggesting that the RR-type MYB-like TFs have conserved expression patterns and functions.
ABA as a well-known stress-related hormone functions in stress-response and controlling plant development [42]. The expression of AtDIV2 is induced by ABA, and loss-of-function of AtDIV2 leads to an increased salt-stress tolerance by altering the levels of ABA1 and ABI3 genes in Arabidopsis [21]. In the present study, SlMYBR11, as the homologous gene of AtDIV2 in Group II, was also induced by ABA, indicating that SlMYBR11 might function in the stress response. The AtMYBL transcript is also induced by ABA and salt stress in Arabidopsis [22], while its homologous gene SlMYBR2 in tomato was repressed by ABA, suggesting that the group III genes have functional differentiation in the ABA response. Moreover, the expression of AtMYBL is at its maximum level after 6-h under ABA treatment and declined at 12-h ABA-treatment in Arabidopsis [22], whereas we only detected the expression of SlMYBR2 after 24-h under ABA treatment. That is probably why these two results are opposite to each other.
The cis-acting elements as important molecular switches are critical for gene regulation to mediate multiple biological processes, including biotic or abiotic stress responses, hormone responses and developmental processes [43]. The gene promoter contains cis-elements as binding sites of TFs and the basic transcriptional machinery. Therefore, clearly understanding the main cis-acting elements in genes is the primary step in studying their function. Several cis-acting elements of SlMYBR genes were identified in the present study. We dealt tomato seedlings with hormones to detect if the cis-elements are tightly linked with gene expression. For the GA-treatment assay, three out of five genes (SlMYBR1, SlMYBR3 and SlMYBR9) containing GA-responsive elements were down-regulated in expression. Combined with the function of GA in regulation of plant development, the discovery of GA-responsive elements in SlMYBR genes will provide a basis for their functional studies in GA mediated plant growth and development [44]. For SA-treatment assays, three out of four genes (SlMYB1, SlMYB2, and SlMYB6) containing SA-responsive elements had repressed expression. As is well known, SA functions in defense signaling [45]. Therefore, some SlMYBRs might play roles in defense signaling via the SA signaling pathway. After ABA treatment, the expression of ~90% SlMYBR genes with an ABA-responsive element was reduced. Interestingly, the changed expression of genes containing multiple response elements was less than that of genes containing only one response element. Therefore, the cis-elements are of importance for plants against environmental change. Altogether, our results revealed that SlMYBR TFs could be used as a potential gene family to genetically improve the tomato stress-response and fruit development.

5. Conclusions

A total of thirteen SlMYBR genes were identified in tomato by genome-wide analysis. These SlMYBRs underwent detailed characterization analysis and were divided into three groups. Group II was all MYBR genes from eudicots without genes from monocots. For Group I and Group III, the phylogenetic tree was in accord with the evolutionary relationship of these species. The spatiotemporal expression patterns of these SlMYBR genes demonstrated that SlMYBR genes may function in fruit development and hormone responses with conserved gene structures and motifs. Taken together, our present study provides the reference for future exploration of the potential functions of the SlMYBR genes in the regulation of growth and development and abiotic-stress responses in tomato.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae8050399/s1, Table S1: Primers used in this study; Table S2: Syntenic gene pairs between A. thaliana, S. lycopersicum and S. tuberosum; Table S3: Cis-acting elements of SlMYBR genes.

Author Contributions

Conceptualization, C.G.; experiments and data analysis, J.S.; writing—original draft preparation, J.S.; writing—review and editing, C.G. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Natural Science Foundation of Zhejiang Province (LY20C020002), National Natural Science Foundation of China (31770352), and funds from Zhejiang Agriculture and Forestry University (2019JQ03).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The whole genome data of tomato is downloaded from the NCBI database (https://www.ncbi.nlm.nih.gov/search/all/?term=txid4081, accessed on 5 July 2021), and the taxonomy ID is 4081. The transcriptome data is obtained from NCBI (https://trace.ncbi.nlm.nih.gov/Traces/study, accessed on 11 October 2021), and the accession numbers is SRP009216.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Guo, C.; Yao, L.; You, C.; Wang, S.; Cui, J.; Ge, X.; Ma, H. MID1 plays an important role in response to drought stress during reproductive development. Plant J. 2016, 88, 280–293. [Google Scholar] [CrossRef] [PubMed]
  2. Ptashne, M. How eukaryotic transcriptional activators work. Nature 1988, 335, 683–689. [Google Scholar] [CrossRef]
  3. Wray, G.A.; Hahn, M.W.; Abouheif, E.; Balhoff, J.P.; Pizer, M.; Rockman, M.V.; Romano, L.A. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 2003, 20, 1377–1419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Dubos, C.; Stracke, R.; Grotewold, E.; Weisshaar, B.; Martin, C.; Lepiniec, L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010, 15, 573–581. [Google Scholar] [CrossRef]
  5. Klempnauer, K.H.; Gonda, T.J.; Bishop, J.M. Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: The architecture of a transduced oncogene. Cell 1982, 31, 453–463. [Google Scholar] [CrossRef]
  6. Weston, K. Myb proteins in life, death and differentiation. Curr. Opin. Genet. Dev. 1998, 8, 76–81. [Google Scholar] [CrossRef]
  7. Paz-Ares, J.; Ghosal, D.; Wienand, U.; Peterson, P.A.; Saedler, H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 1987, 6, 3553–3558. [Google Scholar] [CrossRef]
  8. Baldoni, E.; Genga, A.; Cominelli, E. Plant MYB transcription factors: Their role in drought response mechanisms. Int. J. Mol. Sci. 2015, 16, 15811–15851. [Google Scholar] [CrossRef] [Green Version]
  9. Ambawat, S.; Sharma, P.; Yadav, N.R.; Yadav, R.C. MYB transcription factor genes as regulators for plant responses: An overview. Physiol. Mol. Biol. Plants 2013, 19, 307–321. [Google Scholar] [CrossRef] [Green Version]
  10. Millard, P.S.; Kragelund, B.B.; Burow, M. R2R3 MYB transcription factors—Functions outside the DNA-binding domain. Trends Plant Sci. 2019, 24, 934–946. [Google Scholar] [CrossRef]
  11. Gabrielsen, O.S.; Sentenac, A.; Fromageot, P. Specific DNA binding by c-Myb: Evidence for a double helix-turn-helix-related motif. Science 1991, 253, 1140–1143. [Google Scholar] [CrossRef] [PubMed]
  12. Martin, C.; Paz-Ares, J. MYB transcription factors in plants. Trends Genet. 1997, 13, 67–73. [Google Scholar] [CrossRef]
  13. Li, H.H.; Zhou, Y.W.; Ma, Z.X.; Lu, X.Q.; Li, Y.L.; Chen, H. Genome-wide identification and expression analysis of MYB transcription factors and their responses to abiotic stresses in woodland strawberry (Fragaria vesca). Horticulturae 2021, 7, 97. [Google Scholar] [CrossRef]
  14. Xu, Q.; He, J.; Dong, J.H.; Hou, X.J.; Zhang, X. Genomic survey and expression profiling of the MYB gene family in watermelon. Hortic. Plant J. 2018, 4, 1–15. [Google Scholar] [CrossRef]
  15. Li, Z.; Peng, R.; Tian, Y.; Han, H.; Xu, J.; Yao, Q. Genome-wide identification and analysis of the MYB transcription factor superfamily in Solanum lycopersicum. Plant Cell Physiol. 2016, 57, 1657–1677. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Galego, L.; Almeida, J. Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev. 2002, 16, 880–891. [Google Scholar] [CrossRef] [Green Version]
  17. Howarth, D.G.; Donoghue, M.J. Duplications and expression of DIVARICATA-like genes in dipsacales. Mol. Biol. Evol. 2009, 26, 1245–1258. [Google Scholar] [CrossRef] [Green Version]
  18. Gao, A.; Zhang, J.; Zhang, W. Evolution of RAD- and DIV-like genes in plants. Int. J. Mol. Sci. 2017, 18, 1961. [Google Scholar] [CrossRef] [Green Version]
  19. Raimundo, J.; Sobral, R.; Bailey, P.; Azevedo, H.; Galego, L.; Almeida, J.; Coen, E.; Costa, M.M. A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in Antirrhinum flower asymmetry. Plant J. 2013, 75, 527–538. [Google Scholar] [CrossRef]
  20. Madrigal, Y.; Alzate, J.F.; Gonzalez, F.; Pabon-Mora, N. Evolution of RADIALIS and DIVARICATA gene lineages in flowering plants with an expanded sampling in non-core eudicots. Am. J. Bot. 2019, 106, 334–351. [Google Scholar] [CrossRef]
  21. Fang, Q.; Wang, Q.; Mao, H.; Xu, J.; Wang, Y.; Hu, H.; He, S.; Tu, J.; Cheng, C.; Tian, G.; et al. AtDIV2, an R-R-type MYB transcription factor of Arabidopsis, negatively regulates salt stress by modulating ABA signaling. Plant Cell Rep. 2018, 37, 1499–1511. [Google Scholar] [CrossRef] [PubMed]
  22. Zhang, X.; Ju, H.W.; Chung, M.S.; Huang, P.; Ahn, S.J.; Kim, C.S. The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol. 2011, 52, 138–148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Chen, Y.S.; Chao, Y.C.; Tseng, T.W.; Huang, C.K.; Lo, P.C.; Lu, C.A. Two MYB-related transcription factors play opposite roles in sugar signaling in Arabidopsis. Plant Mol. Biol. 2017, 93, 299–311. [Google Scholar] [CrossRef] [PubMed]
  24. Zhao, J.; Shi, M.; Yu, J.; Guo, C. SPL9 mediates freezing tolerance by directly regulating the expression of CBF2 in Arabidopsis thaliana. BMC Plant Biol. 2022, 22, 59. [Google Scholar] [CrossRef] [PubMed]
  25. Guo, C.; Xu, Y.; Shi, M.; Lai, Y.; Wu, X.; Wang, H.; Zhu, Z.; Poethig, R.S.; Wu, G. Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis. Plant Cell 2017, 29, 1293–1304. [Google Scholar] [CrossRef] [Green Version]
  26. Sengupta, A.; Hileman, L.C. A CYC-RAD-DIV-DRIF interaction likely pre-dates the origin of floral monosymmetry in Lamiales. EvoDevo 2022, 13, 3. [Google Scholar] [CrossRef]
  27. Rose, A.; Meier, I.; Wienand, U. The tomato I-box binding factor LeMYBI is a member of a novel class of Myb-like proteins. Plant J. 1999, 20, 641–652. [Google Scholar] [CrossRef] [Green Version]
  28. Machemer, K.; Shaiman, O.; Salts, Y.; Shabtai, S.; Sobolev, I.; Belausov, E.; Grotewold, E.; Barg, R. Interplay of MYB factors in differential cell expansion, and consequences for tomato fruit development. Plant J. 2011, 68, 337–350. [Google Scholar] [CrossRef]
  29. Subramanian, B.; Gao, S.; Lercher, M.J.; Hu, S.; Chen, W.H. Evolview v3: A webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Res. 2019, 47, W270–W275. [Google Scholar] [CrossRef]
  30. Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
  31. Goodstein, D.M.; Shu, S.; Howson, R.; Neupane, R.; Hayes, R.D.; Fazo, J.; Mitros, T.; Dirks, W.; Hellsten, U.; Putnam, N.; et al. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 2012, 40, D1178–D1186. [Google Scholar] [CrossRef] [PubMed]
  32. Chou, K.; Shen, H. Cell-PLoc 2.0: An improved package of web-servers for predicting subcellular localization of proteins in various organisms. Nat. Sci. 2010, 2, 1090–1103. [Google Scholar] [CrossRef] [Green Version]
  33. Nystrom, S.L.; McKay, D.J. Memes: A motif analysis environment in R using tools from the MEME Suite. PLoS Comput. Biol. 2021, 17, e1008991. [Google Scholar] [CrossRef] [PubMed]
  34. Bailey, T.L.; Johnson, J.; Grant, C.E.; Noble, W.S. The MEME Suite. Nucleic Acids Res. 2015, 43, W39–W49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Lescot, M.; Dehais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van de Peer, Y.; Rouze, P.; Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002, 30, 325–327. [Google Scholar] [CrossRef]
  36. Sato, S.; Tabata, S.; Hirakawa, H.; Asamizu, E.; Shirasawa, K.; Isobe, S.; Kaneko, T.; Nakamura, Y.; Shibata, D.; Aoki, K.; et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485, 635–641. [Google Scholar]
  37. Guo, C.; Jiang, Y.; Shi, M.; Wu, X.; Wu, G. ABI5 acts downstream of miR159 to delay vegetative phase change in Arabidopsis. New Phytol. 2021, 231, 339–350. [Google Scholar] [CrossRef]
  38. Chen, Y.; Yang, X.; He, K.; Liu, M.; Li, J.; Gao, Z.; Lin, Z.; Zhang, Y.; Wang, X.; Qiu, X.; et al. The MYB transcription factor superfamily of Arabidopsis: Expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 2006, 60, 107–124. [Google Scholar]
  39. Al-Dairi, M.; Pathare, P.B.; Al-Yahyai, R. Effect of postharvest transport and storage on color and firmness quality of tomato. Horticulturae 2021, 7, 163. [Google Scholar] [CrossRef]
  40. Ayenan, M.A.T.; Danquah, A.; Hanson, P.; Asante, I.K.; Danquah, E.Y. Tomato (Solanum lycopersicum L.) genotypes respond differently to long-term dry and humid heat stress. Horticulturae 2022, 8, 118. [Google Scholar] [CrossRef]
  41. Liu, Y.; Aslam, M.; Yao, L.A.; Zhang, M.; Wang, L.; Chen, H.; Huang, Y.; Qin, Y.; Niu, X. Genomic analysis of SBP gene family in Saccharum spontaneum reveals their association with vegetative and reproductive development. BMC Genom. 2021, 22, 767. [Google Scholar] [CrossRef] [PubMed]
  42. Cao, B.; Bai, J.; Wang, X.; Zhang, Y.; Yu, X.; Hu, S.; He, Y. BnA.JAZ5 attenuates drought tolerance in rapeseed through mediation of ABA-JA crosstalk. Horticulturae 2022, 8, 131. [Google Scholar] [CrossRef]
  43. Aysha, J.; Noman, M.; Wang, F.; Liu, W.; Zhou, Y.; Li, H.; Li, X. Synthetic promoters: Designing the cis regulatory modules for controlled gene expression. Mol. Biotechnol. 2018, 60, 608–620. [Google Scholar] [CrossRef] [PubMed]
  44. Azeez, A.; Sane, A.P.; Tripathi, S.K.; Bhatnagar, D.; Nath, P. The gladiolus GgEXPA1 is a GA-responsive alpha-expansin gene expressed ubiquitously during expansion of all floral tissues and leaves but repressed during organ senescence. Postharvest Biol. Technol. 2010, 58, 48–56. [Google Scholar] [CrossRef]
  45. Gačnik, S.; Veberič, R.; Hudina, M.; Koron, D.; Mikulič-Petkovšek, M. Salicylate treatment affects fruit quality and also alters the composition of metabolites in strawberries. Horticulturae 2021, 7, 400. [Google Scholar] [CrossRef]
Horticulturae 08 00399 g001 550
Figure 1. Genome density and distribution of SlMYBR genes on tomato chromosomes.
Figure 1. Genome density and distribution of SlMYBR genes on tomato chromosomes.
Horticulturae 08 00399 g001
Horticulturae 08 00399 g002 550
Figure 2. The phylogenetic tree of RR-type MYB-related TFs in A. thaliana (blue circle), S. lycopersicum (red circle), S. tuberosum (violet circle), A. trichopoda (yellow star), B. distachyon (gray triangle), Z. mays (gold triangle), O. sativa (brown triangle), V. vinifera (purple square), C. sativus (green square), M. domestica (coral square), C. clementina (orange square).
Figure 2. The phylogenetic tree of RR-type MYB-related TFs in A. thaliana (blue circle), S. lycopersicum (red circle), S. tuberosum (violet circle), A. trichopoda (yellow star), B. distachyon (gray triangle), Z. mays (gold triangle), O. sativa (brown triangle), V. vinifera (purple square), C. sativus (green square), M. domestica (coral square), C. clementina (orange square).
Horticulturae 08 00399 g002
Horticulturae 08 00399 g003 550
Figure 3. Synteny analysis of A. thaliana, S. lycopersicum and S. tuberosum.
Figure 3. Synteny analysis of A. thaliana, S. lycopersicum and S. tuberosum.
Horticulturae 08 00399 g003
Horticulturae 08 00399 g004 550
Figure 4. Gene structure and conserved motifs of SlMYBR genes.
Figure 4. Gene structure and conserved motifs of SlMYBR genes.
Horticulturae 08 00399 g004
Horticulturae 08 00399 g005 550
Figure 5. Amino acid conserved motifs of SlMYBR proteins.
Figure 5. Amino acid conserved motifs of SlMYBR proteins.
Horticulturae 08 00399 g005
Horticulturae 08 00399 g006 550
Figure 6. Multiple sequence alignment of SlMYBR proteins. ‘*’ indicates positions which have a single, fully conserved residue.
Figure 6. Multiple sequence alignment of SlMYBR proteins. ‘*’ indicates positions which have a single, fully conserved residue.
Horticulturae 08 00399 g006
Horticulturae 08 00399 g007 550
Figure 7. Analysis of cis-acting elements in the promoters of SlMYBR genes.
Figure 7. Analysis of cis-acting elements in the promoters of SlMYBR genes.
Horticulturae 08 00399 g007
Horticulturae 08 00399 g008 550
Figure 8. The expression patterns of SlMYBR genes in different tissues of S. lycopersicum. The left showed the sampled tissues of tomato, and the right showed the expression patterns of SlMYBR genes.
Figure 8. The expression patterns of SlMYBR genes in different tissues of S. lycopersicum. The left showed the sampled tissues of tomato, and the right showed the expression patterns of SlMYBR genes.
Horticulturae 08 00399 g008
Horticulturae 08 00399 g009 550
Figure 9. Expression analysis of SlMYBR genes under different exogenous hormone treatment: (A) GA; (B) SA; (C) ABA. The qRT-PCR data represent the mean of three biological replicates (±SD). Asterisks indicate significant differences from the 0-h sample using a Student’s t-test (** p < 0.01; * p < 0.05).
Figure 9. Expression analysis of SlMYBR genes under different exogenous hormone treatment: (A) GA; (B) SA; (C) ABA. The qRT-PCR data represent the mean of three biological replicates (±SD). Asterisks indicate significant differences from the 0-h sample using a Student’s t-test (** p < 0.01; * p < 0.05).
Horticulturae 08 00399 g009
Table
Table 1. Characteristics of the SlMYBRs in tomato.
Table 1. Characteristics of the SlMYBRs in tomato.
Gene NameGene IDLocationNo. of Amino AcidspIMw (Da)Instability IndexSubcellular Localization
SlMYBR1Solyc03g096350SL2.50ch03:58394818..583962142737.131,417.0849.9Nucleus
SlMYBR2Solyc03g119740SL2.50ch03:68293180..682945542996.5932,825.5259.72Nucleus
SlMYBR3Solyc04g008870SL2.50ch04:2492192..24941872676.9229,774.2846.4Nucleus
SlMYBR4Solyc05g052610SL2.50ch05:62818453..628196342437.0228,526.0749.59Nucleus
SlMYBR5Solyc05g055240SL2.50ch05:64968898..649723701885.4621,500.7740.46Nucleus
SlMYBR6Solyc06g076770SL2.50ch06:47685103..476871903079.1434,693.954.45Nucleus
SlMYBR7Solyc09g007570SL2.50ch09:1163232..11648772564.9828,668.458.34Nucleus
SlMYBR8Solyc09g007580SL2.50ch09:1176695..11779072004.8821,988.4656.06Nucleus
SlMYBR9Solyc09g014250SL2.50ch09:5739856..57419302928.3533,064.8656.42Nucleus
SlMYBR10Solyc10g076820SL2.50ch10:59788934..597903152838.9632,916.8258.57Nucleus
SlMYBR11Solyc11g006720SL2.50ch11:1335551..13372612106.4524,593.6354.75Nucleus
SlMYBR12Solyc11g071500SL2.50ch11:54954825..549581856195.6965,667.0757.76Nucleus
SlMYBR13Solyc12g089170SL2.50ch12:64288495..64288771915.5110,469.754.49Nucleus
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Sun, J.; Guo, C. Genome-Wide Identification and Expression Analysis of RR-Type MYB-Related Transcription Factors in Tomato (Solanum lycopersicum L.). Horticulturae 2022, 8, 399. https://doi.org/10.3390/horticulturae8050399

AMA Style

Sun J, Guo C. Genome-Wide Identification and Expression Analysis of RR-Type MYB-Related Transcription Factors in Tomato (Solanum lycopersicum L.). Horticulturae. 2022; 8(5):399. https://doi.org/10.3390/horticulturae8050399

Chicago/Turabian Style

Sun, Jiaying, and Changkui Guo. 2022. "Genome-Wide Identification and Expression Analysis of RR-Type MYB-Related Transcription Factors in Tomato (Solanum lycopersicum L.)" Horticulturae 8, no. 5: 399. https://doi.org/10.3390/horticulturae8050399

APA Style

Sun, J., & Guo, C. (2022). Genome-Wide Identification and Expression Analysis of RR-Type MYB-Related Transcription Factors in Tomato (Solanum lycopersicum L.). Horticulturae, 8(5), 399. https://doi.org/10.3390/horticulturae8050399

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop