Genome-wide identification and expression analysis of the ClTCP transcription factors in Citrullus lanatus
© Shi et al. 2016
Received: 27 September 2015
Accepted: 22 March 2016
Published: 12 April 2016
The plant-specific TCP transcription factor family, which is involved in the regulation of cell growth and proliferation, performs diverse functions in multiple aspects of plant growth and development. However, no comprehensive analysis of the TCP family in watermelon (Citrullus lanatus) has been undertaken previously.
A total of 27 watermelon TCP encoding genes distributed on nine chromosomes were identified. Phylogenetic analysis clustered the genes into 11 distinct subgroups. Furthermore, phylogenetic and structural analyses distinguished two homology classes within the ClTCP family, designated Class I and Class II. The Class II genes were differentiated into two subclasses, the CIN subclass and the CYC/TB1 subclass. The expression patterns of all members were determined by semi-quantitative PCR. The functions of two ClTCP genes, ClTCP14a and ClTCP15, in regulating plant height were confirmed by ectopic expression in Arabidopsis wild-type and ortholog mutants.
This study represents the first genome-wide analysis of the watermelon TCP gene family, which provides valuable information for understanding the classification and functions of the TCP genes in watermelon.
The TCP gene family, a small group of transcription factors (TF) exclusive to higher plants, was first described in 1999 . The family plays important roles in regulating diverse physiological and biological processes, including phytohormone biosynthesis and signal transduction, leaf morphogenesis and senescence, branching, flower development, pollen development and the circadian clock [2–15]. TCP proteins are characterized by a 59-amino-acid non-canonical basic-Helix-Loop-Helix (bHLH) motif that is responsible for DNA binding, nuclear targeting and pair-wise protein–protein interaction [1, 16]. This domain was first identified from four proteins with critical roles in the evolution and developmental control of plant morphology: TEOSINTE BRANCHED 1 (TB1) of maize (Zea mays), CYCLOIDEA (CYC) of snapdragon (Antirrhinum majus) and the PROLIFERATING CELL FACTORS 1 and 2 (PCF1 and PCF2) of rice (Oryza sativa) [16–18]. Thus the name of the TCP TF family is derived from the acronym for these proteins. TCP genes can be divided into two subfamilies based on the homology of the TCP domains: class I (or TCP-P) and class II (or TCP-C) . TCP class I, also known as the PCF subfamily, contains rice OsPCF1 and OsPCF2, whereas TCP class II is further subdivided into the CIN and CYC/TB1 subclades . The most obvious difference between the two classes is a four-amino-acid deletion in the basic region of the TCP domain of class I compared with that of class II proteins. Moreover, the DNA binding sequence for the two classes differs slightly but partly overlaps (GGNCCCAC for class I and GTGGNCCC for class II) [20, 21].
Accumulating evidence confirms that class I TCP proteins mainly play a role in cell growth and proliferation [13, 20], whereas the CIN proteins may be involved in lateral organ development and the CYC/TB1 clade is mainly involved in the development of axillary meristems giving rise to either flowers or lateral shoots [5, 7, 9, 22–27]. Generally, the two classes of TCP genes are considered to act antagonistically on specific biological processes. Class I genes are usually assumed to promote plant growth, mainly based on the finding that OsPCF1/OsPCF2 and AtTCP20 act as transcriptional activators of PCNA and CYCB1;1 genes [7, 20, 28]. In practice, most class I single mutants do not show conspicuous phenotypic variation, which might be because of functional redundancies. For example, increasing evidence demonstrates that AtTCP14 and AtTCP15 function redundantly to regulate biological processes and influence plant structure. The two genes also mediate responses of leaves and flowers to cytokinin and promotion of seed germination by gibberellin (GA) [29–31]. More recently, AtTCP14 and AtTCP15 were shown to repress endoreduplication by directly regulating the expression of cell-cycle genes to influence cell and organ growth . Notable plant morphological changes are observed in the tcp14 tcp15 double mutant, such as shortened internode length as well as varied leaf and sepal morphology, whereas single mutants show mild phenotypic defects [29, 33]. Moreover, AtTCP9 and AtTCP19 play a positive role in a redundant manner with AtTCP20 in the control of leaf senescence, as tcp9 tcp20 and tcp19 tcp20 double mutants exhibit earlier onset of senescence in comparison with the wild type, whereas none of the single mutants exhibit accelerated senescence [13, 15].
By contrast, many phenotypic observations on mutants suggest that the class II TCP proteins usually have preventative roles in cell growth and proliferation. CIN-type genes limit cell proliferation at the margins of the developing leaf primordium. In snapdragon, Arabidopsis and tomato cin-type mutants, leaf cells exhibit the ability to continue to divide for a longer period compared with the wild type, thus generating larger leaves of altered shape and/or with a crinkled surface [2, 21, 25, 34, 35]. In addition, many TB1-type TCP genes act as axillary bud-specific regulators, such as TB1 of maize [18, 22], AtBRC1 and AtBRC2 of Arabidopsis [4, 36], PsBRC1 of pea (Pisum sativum)  and OsFC1/OsTB1 of rice [38, 39]. Defects in these genes result in excessive shoot branching, which are indicative of a negative function of these TCP genes on bud activity [4, 36–39]. In some instances, class II TCP genes may also play positive roles in plant growth and development. AtTCP1, a CYC/TB1 subclade member, is implicated in the control of floral symmetry . Over-expression of a dominant-negative form of TCP1, TCP1-SRDX, results in a dwarfed phenotype as well as defects in the longitudinal elongation of cotyledonary petioles, rosette leaves and inflorescence stems in Arabidopsis [9, 40].
To date, only a small number of TCP TFs have been identified and functionally characterized in model plants such as Arabidopsis and rice. Watermelon (Citrullus lanatus L.), an important cucurbit crop, is widely cultivated throughout the world. However, little information is available on the watermelon TCP family. In this study, a global analysis of the TCP gene family in watermelon was carried out for the first time. Twenty-seven ClTCP genes were identified in the watermelon genome and a systematic analysis, including determination of chromosomal location, phylogenetic relationships, gene duplication, conserved motifs and expression pattern was performed. Plant height is an important agronomic trait of watermelon. Normally, watermelon genotypes of reduced plant height are more suitable for intensive culture and early maturation in a greenhouse. ClTCP genes involved in the regulation of plant height in watermelon were identified in this research.
Results and discussion
Identification of TCP genes in Citrullus lanatus
TCP gene family in Citrullus lanatus
Phylogenetic analysis and conserved motifs
Expression profiles of TCP genes in Citrullus lanatus
In contrast, most Class I genes, which usually promote plant growth and cell proliferation, showed more widespread and less tissue-specific expression patterns, such as in leaf, flower, and at an early stage of fruit development (Fig. 4). This finding implied that these genes may play diverse regulatory roles at multiple development stages. In Arabidopsis, several important functions of Class I TCP TFs have been discovered even though few phenotypic variations are observed in the single mutants. For example: AtTCP8 is proposed to be involved in mitochondrial biogenesis . AtTCP14 and AtTCP15 are reported to modulate cell proliferation during seed, leaf, floral and internode development [31, 33, 47]. AtTCP15 may also be important for endoreduplication . AtTCP16 plays a role in early pollen development . AtTCP20, which acts upstream of AtTCP9, controls leaf development via the jasmonate signaling pathway [13, 15, 28]. All of these AtTCP genes have at least one counterpart in watermelon, implying that Class I TCP in watermelon may perform similar functions. Taken together, the above-mentioned findings from model plants highlight that the TCP family performs diverse functions in multiple biological processes. ClTCP genes are likely to share conserved functions with Arabidopsis homologs, as they show not only high sequence similarity but also similar expression patterns.
Role of ClTCP14a and ClTCP15 in plant height
Plant height is an important agronomic trait in watermelon, which dramatically affects planting density and fruiting position in the field. TCP TFs, as well known cell proliferation regulators, are undoubtedly important participants in internode and plant elongation. The present results revealed that ClTCP14a and ClTCP15 redundantly regulated internode length and plant height via a GA-related pathway in transgenic Arabidopsis (Figs. 5, 6 and 7). In Arabidopsis, AtTCP14 and AtTCP15 are reported to regulate internode development by promoting cell proliferation, based mainly on the phenotypes observed in double-mutant and TCP14:SRDX lines . The present results provide direct evidence for this genotype–phenotype correlation. Moreover, AtTCP14 and AtTCP15 are expressed in internodes of young inflorescence stems, young flower pedicels, cotyledons and leaf primordia . These results are generally consistent with the present expression analysis of ClTCP genes in watermelon (Fig. 4). Moreover, it was reported recently that AtTCP14 and AtTCP15 mediate GA-dependent activation of the cell cycle during seed germination . Thus, we hypothesize that ClTCP14a and ClTCP15 may also act downstream of GA and promote cell proliferation during internode formation in a similar manner. Interestingly, our findings suggest that ClTCP14a and ClTCP15 might also affect GA biosynthesis and signaling (Fig. 6), which might result from a feedback regulatory mechanism.
In this study, 27 TCP genes were identified in the watermelon genome, which were distributed on nine chromosomes with different densities. These TCP genes were classifiable into two classes based on the similarity in TCP domain. Expression analysis showed that members of each class/clade show a similar expression pattern. Moreover, many ClTCP genes showed a similar expression pattern to that of their Arabidopsis homologs, which suggests that the TCP family shows conserved functions in the two species. In addition, the function of two ClTCP genes, ClTCP14a and ClTCP15, in the regulation of internode elongation was confirmed. Ultimately, these findings will lead to potential applications for the improvement of watermelon cultivars via genetic engineering.
Plant materials and growth conditions
Watermelon (Citrullus lanatus L. cv. IVSM9, an inbred line developed by the Laboratory of Germplasm Innovation and Molecular Breeding, Zhejiang University) was used as the main plant material. Plants were grown under a photoperiod of 16 h at 27 °C (day) and 8 h at 24 °C (night) in a phytotron with a photosynthetic photon flux density of 600 μmol m−2 s−1 and relative humidity of 70–80 %.
Arabidopsis thaliana ecotype Columbia-0 (Col-0) was used as the wild type. All Arabidopsis materials, including tcp14-4, tcp15-3, tcp14-4 tcp15-3 and their background were obtained from the University of Leeds, UK, and were genotyped by PCR as described by Kieffer et al. . Plants were grown in Sanyo growth chambers (Sanyo, http://www.sanyobiomedical. co.uk) at 20 °C under long-day conditions with a photoperiod of 16 h/8 h (day/night), photosynthetic photon flux density of 200 μmol m−2 s−1 and 60 % relative humidity.
Information on the chromosomal locations of all AtTCP genes was obtained from The Arabidopsis Information Resource (TAIR; http://www.arabidopsis.org), and that for all ClTCP genes was obtained through BLASTN searches against the Cucurbit Genomics Database (http://www.icugi.org). All TCP genomic data were visualized in a circos map using CIRCOS software (http://circos.ca).
Sequence alignment and phylogenetic analysis
The sequences of 24 TCP family members in the genome of Arabidopsis were retrieved from TAIR (http://www.arabidopsis.org) or PlantTFDB (http://planttfdb.cbi.pku.edu.cn/). Twenty-seven ClTCP genes were identified from a BLAST analysis of the Cucurbit Genomics Database (http://www.icugi.org). A multiple sequence alignments of the amino acid sequences of the TCP proteins of Citrullus lanatus and Arabidopsis was generated with ClustalX 2.0 software with the default settings as described by Thompson et al. . An unrooted phylogenetic tree based on the sequence alignments was constructed using MEGA 5.0 software (http://www.megasoftware.net/)  and the neighbor-joining method with the following parameters: pairwise alignment, 1000 bootstrap replicates, Poisson correction model, uniform substitution rates and complete deletion. In addition, a separate phylogenetic tree was constructed for all of the TCP protein sequences from Citrullus lanatus for further analysis.
Identification of conserved motifs
AtTCP and ClTCP protein sequences were submitted to online searches with the Pfam (http://pfam.xfam.org) and SMART (http://smart.embl-heidelberg.de) tools to identify conserved TCP domains. The R domain was obtained from PlantTFDB (http://planttfdb.cbi.pku.edu.cn/). The method of identifying miR319-targeting TCP genes was described previously . To visualize protein domain structures, IBS 1.0 software (http://www.mybiosoftware.com/ibs-illustrator-of-biological-sequences.html) was used.
RNA isolation and RT-PCR analysis
Total RNA was isolated from tissues using the RNAprep Pure Plant Kit and treated with DNase I (Tiangen, http://www.tiangen.com). RNA concentration and quality were assessed using a Thermo 2000 Bioanalyzer with a RNA NanoDrop (Thermo Scientific, http://www.thermo.com). Reverse transcription was performed with 1 μg total RNA in a 20-μl volume, using the ReverTra Ace® qPCR RT Master Mix with gDNA Remover kit (Toyobo) and diluted to 200 μl with water. For semi-qPCR and PCR, 1 μL reverse-transcription product was used as the PCR template in a 20-μl volume reaction. Different PCR annealing temperatures were applied to optimize results and the PCR was terminated after 35 cycles. PCR products were separated by 1.5 % agarose gel electrophoresis and visualized under an ultraviolet scanner. For RT-qPCR analysis, a 20-μl qPCR mixture was employed, which contained 2.5 μl first-strand cDNAs, 10 μl 2× FastStart Universal SYBR Green Master (Roche) and 0.25 μM of the forward and reverse primers for each gene. Relative expression levels of each gene were normalized to mRNA levels of yellow-leaf-specific protein 8 (CLYLS8) as a loading control. Three biological replicates were analyzed in each case. CT values were obtained with the Real-Time PCR System StepOne version 2.1 software (Applied Biosystems). Relative fold expression changes were calculated by the comparative CT method: fold change was calculated as 2−∆∆CT. The ∆CT values were calculated as the difference between the CT value and the CT value of CLYLS8. ∆∆CT was the difference between the ∆CT value of TCP genes and the ∆CT value of the reference gene. The gene-specific primers for semi-quantitative PCR and RT-qPCR procedures are listed in Additional file 7: Table S2.
To study the function of ClTCP14a and ClTCP15, two constructs were developed using the CaMV35S promoter. Full-length ClTCP14a cDNA (1197 bp) and ClTCP15 cDNA (1062 bp) were amplified by two-round PCR: the first round with the gene-specific primers ClTCP14a-Fl-F and ClTCP14a-Fl-R, and ClTCP15-Fl-F and ClTCP15-Fl-R, respectively; the second round with the common primers attB1-F and attB2-R. Finally, both sequences were cloned into the Gateway™ vector pMDC83 (Invitrogen) via the BP and LR reactions as described by Curtis and Grossniklaus . The primers used for vector construction are listed in Additional file 8: Table S3.
Transformation of Arabidopsis
The two constructs were transformed into Agrobacterium tumefaciens strain GV3101 (pMP90) . Transformation of both wild-type and tcp14 tcp15 plants was conducted by means of the floral dip method . After transformation, plants were kept in a growth chamber until seed set. Transformant selection was done on germination medium containing 50 μg ml−1 Hygromycin-B (Roche, http://www.roche.com) for 10 days, after which germinated T1 seedlings were transferred to soil and grown until seed set. During selection of T1 plants, a plant line negative for hygromycin resistance was selected and maintained as a negative control. In addition, overexpression analysis of TCP14a or TCP15 in candidate transgenic Arabidopsis was employed to confirm the successful transformation (Additional file 6: Figure S5). Homozygous T3 plants were used in this study. Sixty primary transformants were identified and analyzed in most experiments.
Inflorescence height and internode length of 42-day-old Arabidopsis plants were measured. All measurements were obtained from three independent experiments, and at least 10 replicate seedlings were measured in each experiment.
Samples dissected and prepared for scanning electron microscopic analysis were analyzed as previously described .
Gibberellic acid (150 mg L−1) (Biotech Grade biosharp, http://www.biosharp.cn) and 150 mg L−1 chlormequat chloride (Shanghai BioRc Co., Ltd.) were sprayed onto the leaf surface of watermelon seedlings at the two-true-leaf stage. Water was applied as the control. Three days later, the treatment was repeated. The plant height was measured at the six-true-leaf stage.
Availability of supporting data
The datasets supporting the results of this article are available at http://0-dx.doi.org.brum.beds.ac.uk/10.5061/dryad.9pp6q
This work was supported by the earmarked fund for Modern Agro-Industry Technology Research System of China (CARS-26-17), National Natural Science Foundation of China (31501782), Zhejiang Provincial Natural Science Foundation of China (LQ16C150002), Education Department Research Program of Zhejiang province (Y201329960) and Fundamental Research Funds for the Central Universities (2013QNA6013). We thank Dr. Martin Kieffer for donation of the mutants.
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