Genome-wide identification, phylogeny and expression analysis of GRAS gene family in tomato
© Huang et al. 2015
Received: 9 March 2015
Accepted: 11 August 2015
Published: 25 August 2015
GRAS transcription factors usually act as integrators of multiple growth regulatory and environmental signals, including axillary shoot meristem formation, root radial pattering, phytohormones, light signaling, and abiotic/biotic stress. However, little is known about this gene family in tomato (Solanum lycopersicum), the most important model plant for crop species with fleshy fruits.
In this study, 53 GRAS genes were identified and renamed based on tomato whole-genome sequence and their respective chromosome distribution except 19 members were kept as their already existed name. Multiple sequence alignment showed typical GRAS domain in these proteins. Phylogenetic analysis of GRAS proteins from tomato, Arabidopsis, Populus, P.mume, and Rice revealed that SlGRAS proteins could be divided into at least 13 subfamilies. SlGRAS24 and SlGRAS40 were identified as target genes of miR171 using5’-RACE (Rapid amplification of cDNA ends). qRT-PCR analysis revealed tissue-/organ- and development stage-specific expression patterns of SlGRAS genes. Moreover, their expression patterns in response to different hormone and abiotic stress treatments were also investigated.
This study provides the first comprehensive analysis of GRAS gene family in the tomato genome. The data will undoubtedly be useful for better understanding the potential functions of GRAS genes, and their possible roles in mediating hormone cross-talk and abiotic stress in tomato as well as in some other relative species.
Transcription factors (TFs) are important part of the functional genomics. Since the first transcription factor was found in maize , a large number of TFs have been proven to participate in various physiological processes and regulatory networks in higher plants. GRAS proteins are named after GAI, RGA and SCR [2–4], the first three functionally identified members in this family. Typically, proteins of this family exhibit considerable sequence homology to each other in their C-terminus, within which motifs including LHR I, VHIID, LHR II, PFYRE and SAW can be recognized in turn [5–7]. In contrast, N-terminus of GRAS family varies in length and sequence, which seems like the major contributor to the functional specificity of each gene [6, 8].
By far, GRAS gene family has been genome-wide explored in several plant species, including Populus, Arabidopsis, rice, Chinese cabbage, Prunus mume, and pine [9–12]. However, only small number of GRAS proteins were functionally characterized, including some members identified in Zea mays, Petunia hybrida, Medicago truncatula, Lilium longiflorum [13–16]. These genes play crucial roles in diverse fundamental processes of plant growth and development. For instance, the most widely known sub-branch of GRAS proteins, which share the amino acid sequence DELLA in their N-terminal region and thus are referred as DELLA proteins, function as repressors of gibberellin signaling . The SCR and SHR, which belong to two different sub-branches of GRAS family, are both involved in radial organization of the root through forming a SCR/SHR complex . Two independent studies demonstrated that endodermis-expressed SCL3 acted as an integrator downstream of the GA/DELLA and SCR/SHR pathways, mediating the GA-promoted cell elongation during root development [18, 19]. Another sub-branch, which contains 4 highly homologous in Arabidopsis, PAT1, SCL5, SCL13, and SCL21, are involved in light signaling pathways. Interestingly, PAT1, SCL5, SCL21 are positive regulators of phytochrome-A signal transduction while SCL13 is mainly participated in phytochrome-B signal transduction [20–22]. Two GRAS proteins, NSP1 and NSP2 can form a DNA binding complex which is essential for nodulation signaling in legumes . MOC1, mainly expressed in the axillary buds, has a pivotal role in controlling rice tillering . Ls and LAS, the homologous gene of MOC1 in tomato and Arabidopsis, also act in the axillary meristem initiation of tomato [25, 26]. In addition, LiSCL is a transcriptional activator of some meiosis-associated genes, participates in the microsporogenesis of the lily anther . HAM mediates signals from differentiating cells for controlling shoot meristem maintenance in the Petunia . And three Arabidopsis orthologs of Petunia HAM, SCL6/SCL6-IV, SCL22/SCL6-III and SCL27/SCL6-II, also known as targets of post-transcriptional degradation by miRNA170/171, have been demonstrated to play an important role in the proliferation of meristematic cells, polar organization and chlorophyll synthesis [27–29].
Tomato (Solanum lycopersicum) is an important crop because of its great nutritive and commercial value, and also a good model plant for fleshy fruit development. With the release of the whole genome sequence of tomato , it is very convenient to comprehensive analysis an entire gene family now. To date, transcription factor families like ERF, WRKY, SBP-box, IAA, ARF, and TCP have already been identified in tomato [31–36]. Here, considering the important role of GRAS proteins in plant growth regulation and the lack of information about this gene family in the crop, we describe on the first characterization of the entire GRAS gene family of transcription factors in tomato. The present work identified 53 putative SlGRAS genes, together with analyzing their gene classification, chromosome distribution, phylogenetic comparison and exon-intron organization. In addition, the expression profile analysis of SlGRAS genes by real time qPCR in different stages of vegetative and reproductive development were performed, and their transcript abundance in response to different hormones and abiotic stress treatments were also investigated. This study provides details of GRAS gene family and facilitates the further functional characterization of GRAS genes in tomato.
Identification and multiple sequence analysis of SlGRAS genes
Phylogenetic analysis and classification of GRAS members from Arabidopsis and tomato
In addition, to further explore the orthologous relationships of GRAS genes between tomato and other Solanaceae crops, 50 and 30 GRAS genes from potato (Solanum tuberosum) and pepper (Capsicum annuum), respectively, were selected to construct another phylogenetic tree (Additional file 4). We found that almost every member of SlGRAS genes (except for SlGRAS17) has its homologous gene(s) in either or both of potato and pepper genome, suggesting that the evolutional conservation and closer homology relationship among GRAS genes in closely related species.
Expression analysis of SlGRAS genes in different tissues and organs
Expression analysis of SlGRAS genes in response to hormone treatments
Expression analysis of SlGRAS genes in response to abiotic treatments
To date, several attempts have been made to group members of GRAS family into subfamilies that reflect their evolutionary relationships [6–12]. These dendrograms were in substantial agreement though some fine-tunings. The bioinformatic analysis of GRAS proteins showing higher similarity within the same species indicates that gene duplications have occurred after the split among these lineages. Compared to Arabidopsis, larger number of GRAS proteins arisen in tomato suggests more gene duplications events or higher frequency of the retaining copies after duplication in tomato. Taken the tandem duplication events as example, 2/34, 10/45, 15/53, 17/60, 40/106 GRAS genes were identified as tandem duplicated genes in Arabidopsis , P.mume , tomato (Fig. 2), rice , and Populus , respectively, further validating that the duplication events are the most common mechanism contributing to the rapid expansion of GRAS gene family members in different species. Meanwhile, the exon-intron organization analysis showed that 77.4 % of SlGRAS genes were intronless in tomato (Fig. 1), with proportions 82.2 %, 67.6 %, 55 % and 54.7 % in P.mume, Arabidopsis, rice and Populus, respectively [9–12]. The high percentage of intronless genes in GRAS gene family in plant implies the close evolutionary relationship of GRAS proteins. Apart from GRAS gene family, intronless genes are also enriched in some other large gene families, such as F-box transcription factor gene family , DEAD box RNA helicases , and small auxin-up RNAs (SAUR) gene family . Generally, intronless genes are archetypical in the prokaryotic genomes, and there are three explanations for the formation of the intronless genes in eukaryotic genomes: horizontal gene transfer from ancient prokaryotes, duplication of existing intronless genes, and retroposition of intron-containing genes . Zhang et al.  recently reported the origin of plant GRAS genes from prokaryotic genomes of bacteria by horizontal gene transfer. That might be the reason of the abundant intronless genes in the GRAS gene family, which is likely to be its prokaryotic origin followed by extensive duplication events in the evolutionary history.
Intrinsically disordered proteins (IDPs) are highly abundant in eukaryotic proteomes and important for cellular functions. An IDR (intrinsically disordered region) within an IDP often undergoes disorder-to-order transitions upon binding to various partners, allowing an IDP to recognize and bind different partners at various binding interfaces [8, 51, 52]. By computational and bioinformatics tools, Sun et al.  demonstrated that the GRAS proteins are intrinsically disordered. One of the distinguishing features of GRAS proteins is its variable N-terminal, which is predicted to contain MoRFs (molecular recognition features), short interaction-prone segments that are located within IDRs and are able to recognize their interacting partners by undergoing disorder-to-order transitions upon binding to these specific partners [51, 52]. In tomato, except a few uncanonical GRAS proteins, multiple sequence analysis of tomato GRAS proteins showed that most members in this family possess a highly variable N-terminal domain, indicating the functional versatility of this gene family in tomato. Highly conserved C-terminal domains (GRAS domain) were observed in most SlGRAS proteins. Generally, Leucine-rich regions I (LR I) and II (LR II) flank the VHIID motif to form a LR I-VHIID-LR II pattern present in most GRAS proteins. It has been widely and experimentally confirmed for many GRAS proteins that the LRI-VHIID-LRII pattern or individual motifs within the pattern are used for interactions with protein partners [17, 23, 51–54].
Due to the functional diversity of GRAS genes, many members of this gene family need to be further functionally characterized. The expression patterns of SlGRAS genes here could help us to assess their possible functions. 8 SlGRAS genes were undetectable in any tissues/organs suggests a tendency to degenerate those genes after gene duplication or the lost of their functions during evolution. On the whole, the expression patterns vary greatly among different members even between those orthologous pair genes (SlGRAS1 and SlGRAS32, SlGRAS11 and SlGRAS18, SlGRAS42 and SlGRAS46) (Fig. 6). Previously, expression profiles of GRAS genes in Populus and P.mume also demonstrated rather broad expression patterns across a variety of tissues, not only among subfamilies but members in the same clade [9, 11]. These results suggest that GRAS genes may undergo neo-functionalization or sub-functionalization in many higher plant species. Yet still, some GRAS genes with extremely high sequence identity (SlGRAS1 and SlGRAS14, SlGRAS2 and SlGRAS3, SlGRAS7 and SlGRAS12, SlGRAS9 and SlGRAS10) (Fig. 6) exhibited conserved expression patterns, implying their retention by genetic redundancy and selection for their contributions to the robustness of the genetic network. SlGRAS25,SlGRAS39 and SlGRAS15 with high mRNA levels in roots and stems suggests conserved functions with their homologous gene AtSHR  and AtSCR , which are involved in root and shoot radial patterning in Arabidopsis. The strong ovary-preferential expression of SlGRAS41 during flower-fruit transition suggests its potential role in fruit development by modulating brassinosteroid signaling . The homologs of AtSCL3 (SlGRAS11, SlGRAS18) displayed high mRNA levels in anthesis flowers, indicating that they may exert new functions during pollination/fertilization by modulating GA signaling [18, 19]. Our results have proved that SlGRAS24 and SlGRAS40 can be cleaved by miR171 (Fig. 5), one of the most conserved miRNAs in plants, suggesting that they may have similar functions with their homologous genes characterized in other species such as Arabidopsis . However, the expression patterns of SlGRAS24 and SlGRAS40 in tomato are largely different, which suggests that the complicated and widespread functions of the miR171-GRASs regulatory networks in tomato. Noticeably, according to the Supplementary Table 75 of Tomato Genome Consortium , there are 14 SlGRAS genes (SlGRAS1, SlGRAS2, SlGRAS8, SlGRAS9, SlGRAS12, SlGRAS13, SlGRAS14, SlGRAS17, SlGRAS18, SlGRAS24, SlGRAS32, SlGRAS38, SlGRAS40, SlGRAS48) were differentially expressed from mature green stage fruits to breaker stage fruits. Our results are consistent with the above data, suggesting the pivotal roles of these genes during fruit ripening. Two of them, SlGRAS18 and SlGRAS38, predominantly expressed in breaker and red ripening stage fruits, have been reported as target genes of RIN [56, 57], which is key transcriptional regulator during fruit ripening. Moreover, the spatio-temporal expression patterns revealed that the majority members of SlGRAS identified presented sharply increase or decrease upon pollination/fertilization either or both in stamen and ovary (i.e., SlGRAS8, SlGRAS11, SlGRAS14, SlGRAS16, SlGRAS18, SlGRAS20, SlGRAS24, SlGRAS27, SlGRAS36) (Fig. 7), indicating their potential active roles during ovary and anther development. Considering the relationship between GRAS genes and GA signaling, we speculate that members of this gene family involve in mediating GA responses during flower-to-fruit transition.
Plant growth and development are regulated by a chemically and structurally diverse group of hormones. Many known growth and development responses to hormones are due to modulation of gene expression, and these responses are among the best characterized to date . In general, hormones control the expression of genes by regulating the abundance of two types of gene regulatory proteins, transcription factors and transcriptional repressors. To our knowledge, the relationship between GRAS proteins and hormones remain scarce, apart from the widely known gibberellin [3, 54], only a few reports mentioned some members involved in auxin and brassinosteroid signal transduction [41, 59, 60]. Among four hormones conducted here, auxin (Indole 3-acetic acid, IAA) is involved in almost all aspects of plant growth and development, from embryogenesis to senescence, from root tip to shoot tip . Gibberellic acid also regulates a diverse array of developmental processes such as seed development and germination, organ elongation and control of flowering time . Ethylene and salicylic acid play important roles in biotic stresses , while ethylene is also the key regulator during fleshy fruit ripening . It has been reported that BnSCL1, a GRAS protein identified in Brassica napus, showed differential dose response to auxin in shoots and roots . The current results demonstrated that the majority of SlGRAS genes detected here displayed distinct changes following different hormone treatments, and some of them even exhibited opposite trends in roots and shoots, suggesting that GRAS transcription factors regulate gene expression by modulating phytohormone signaling through complicated networks (Fig. 8). Additionally, several studies have revealed that GRAS genes play potential regulatory roles in stress responses. PeSCL7, a member of GRAS genes from poplar, was regarded useful for engineering drought- and salt-tolerant trees . Over-expression of a BnLAS gene in Arabidopsis thaliana could increase its drought tolerance . The DELLA protein was proved to be involved in many abiotic stresses such as low temperature, phosphate starvation, and high NO concentration [66–68]. As for the evidence of GRAS proteins in the regulation of plant defence responses in tomato: transcripts corresponding to GRAS genes in resistant tomato plants infected with virulent phytopathogenic bacteria were different [69, 70]. Furthermore, the expression analysis by qRT-PCR showed that several tomato GRAS genes were associated with plant disease resistance and mechanical stress response . Many transcription factor families have been shown to display stress-responsive gene expression with significant overlap in response to various stress treatments, indicating the cross correlation upon signaling pathways involved in various stresses. The induction of SlGRAS genes in response to more than one stress treatments in the present work highlights the wide involvement of GRAS genes in environmental adaptation (Fig. 9). We observed that SlGRAS genes showed larger accumulation under salt, cold, and heat treatments compared to other three treatments, suggesting that the SlGRAS gene family members might play more important roles in response to these three stress conditions. Combined analysis of all qPCR data (Figs. 6, 8, 9 and 10), we found that four highly homologous genes belonging to AtPAT subfamily (SlGRAS2, SlGRAS3, SlGRAS7, SlGRAS34) exhibit similar expression levels when responding to hormone and abiotic treatments, implying that these genes may be also involved in hormone signaling and stress response. Consistently, two genes of this subfamily from rice, CIGR1 and CIGR2, were reported to be gibberellin and stress related . SlGRAS36 was significantly decreased in response to all hormone treatments while obviously increased in its mRNA levels upon four abiotic stresses. Likewise, SlGRAS4 was induced by all hormone treatments, and the strong upregulation of its transcripts under cold stress suggests the great potential for cold stress tolerance. Interestingly, both SlGRAS36 and SlGRAS4 share strong sequence similarity to AtSCL14, a GRAS transcription factor that is essential for the activation of stress-inducible promoters . A homologous gene of AtSCL14 from rice, OsGRAS23, is involved in drought stress response through regulating expression of stress-responsive genes . Thus, we deduce that SlGRAS36 and SlGRAS4 may play important role in eliciting stress responsive genes in tomato. Besides, several SlGRAS genes were dramatically regulated under both hormone and abiotic stress treatments, indicating the coordinate response of these two determinants.
Although some classical functions of GRAS transcription factors have already been characterized in several plant species, more members of the GRAS family in agricultural crops, especially in those with fleshy fruits, remain to be further studied. In this work, 53 GRAS transcription factors were indentified in tomato. The information generated about the structure of SlGRAS proteins will shed light on their functional analysis. The comparative, phylogenetic, and expression analyses of GRAS members will be useful to comprehensive functional characterization of the GRAS gene family, and to better understanding their possible roles in mediating hormone cross-talk and abiotic stress. After all, the data shown here should be taken into consideration in future studies for genetic improvements of agronomic traits and/or stress tolerance in tomato and probably other Solanaceae plants.
Plant materials and growth conditions
Tomato plants (Solanum lycopersicum cv. Micro-Tom) were grown on soil in greenhouse with suitable conditions: 14/10 h light/dark cycle, 25/20 °C day/night temperature and 60 % relative humidity, and the plant nutrient solution were irrigated once per week. Roots, stems, and leaves were collected on two-month-old plants, flowers (bud, anthesis) and fruit (immature, breaker stage, and red fruit) were harvested at the proper time. Stamens and ovaries were collected 2 days before anthesis (-2 dpa), the first day of anthesis (0 dpa), and 2 days post anthesis (2 dpa), respectively. All tissues were collected from six well-grown plants between 9:00 a.m. and 10:00 a.m. and thoroughly mixed, then frozen in liquid nitrogen immediately, and each tissues/organs were sampled for three independent times.
Identification of tomato GRAS genes
At first, we used “GRAS” as a key word and the S.lycopersicum genome was chosen as initial queries, a total of 54 putative GRAS genes were obtained from the Phytozome database (http://www.phytozome.net). Meanwhile, systematic BLAST homology searches using amino sequence of the 32 AtGRAS proteins obtained from the National Center for Biotechnology Information (NCBI) were performed on all sequences in the International Tomato Annotation Group Release 2.4 tomato proteins (2.40) (BLASTP, E value ≤ 1 × 10-5) and tomato WGS chromosomes (2.50)(TBLASTN, E value ≤ 1 × 10-5) (SGN http://solgenomics.net/tools/blast/). Taken together, 53 potential GRAS genes were identified from the currently available genomic databases. Subsequently, online bioinformatics tools, ExPASy-PROSITE (http://prosite.expasy.org/) and TBLASTN of NCBI (http://blast.st-va.ncbi.nlm.nih.gov/Blast.cgi?PROGRAM=tblastn&PAGE_TYPE=BlastSearch&LINK_LOC=blasthome) were used to further confirm the presence of GRAS domain in resulting sequences.
Bioinformatic analyses of tomato GRAS genes
The 53 putative GRAS genes were renamed according to their chromosomal location except 19 members were kept as their already existed name (SlGRAS1-SlGRAS17, SlDELLA, SlLS). The functional domain distribution and exon-intron structures of the GRAS proteins were obtained from Phytozome (http://www.phytozome.net). The tandemly duplicated genes were defined as an array of two or more SlGRAS genes with Smith-Waterman alignment e values ≤1 × 10-25 in the range of 350-kb distance, as proposed by Lehti-Shiu et al. . We downloaded the GRAS protein sequences of Populus, rice, and P.mume according to two previous publications [11, 12], and at least one gene of each subfamily was selected based on the phylogenetic trees. Then, together with all 32 Arabidopsis AtGRAS proteins and 48 tomato SlGRAS proteins, the multiple sequence alignment were performed using the ClustalX2.0 program using the default settings. A phylogenetic tree based on the alignment was constructed using MEGA6.0 by the NJ (neighbour-joining) method with the bootstrap test replicated 1000 times.
Modified 5’-RACE to identify the slicing sites of SlGRAS24 and SlGRAS40
The 5’-Full RACE kit (TaKaRa, JAPAN) was used for RNA ligase-mediated rapid amplification of cDNA ends (RLM-RACE) assay according to the manufacture’s specification. Briefly, total RNAs were extracted from the seedlings of wild-type tomato, and Poly(A) mRNA was directly ligated to the 5’-RACE adaptor (60 nucleotides). The oligo(dT) primer was used to prime cDNA synthesis with reverse transcriptase. PCR was performed according to Tm of each GSP primers (Additional file 5), which were designed at the predicted 3′ products of complementary site of mature miRNA sequence. Finally, the PCR products were purified, cloned into pEASY-Blunt Cloning vector (Transgene) and were sent to sequencing for each product.
Hormone and abotic stress treatments
For hormone treatment, 12-day-old tomato seedlings were soaked in liquid MS medium with 20 μM ethephon (Eth), 20 μM gibberellin (GA3), 20 μM indole acetic acid (IAA), 20 μM salicylic acid (SA) for 3 h, respectively. Roots and shoots of treated samples were harvested separately. Seedlings soaked in liquid MS medium without any hormone were used as control.
About one-month-old tomato plants were subjected to various abiotic stress treatments. For cold or heat treatment, tomato plants which were grown in green house were transferred to a cold chamber maintained at 4 ± 1 °C or in an incubator at 42 ± 1 °C, respectively. Salt, osmotic and oxidative stress treatments were carried out by spraying leaves with 200 mM NaCl, 100 mM mannitol and 100 mM hydrogen peroxide. Leaves were sampled at 6 h post treatment and untreated plants were used as controls. The drought treatment consisted of withholding water for up to 15 days. Well-watered plants were maintained as controls by watering plants daily.
At each treatment, materials from six separate seedlings/plants were combined to form one sample, and all of the treatment experiments were performed in three independent times. All these samples were frozen in liquid nitrogen immediately and stored at -80 °C until RNA extraction.
RNA isolation and real-time quantitative PCR analysis
Total RNA was extracted using TRIzol reagent (Invitrogen, USA) according to the manufacturers’ instruction. RNA integrity was verified by 1.2 % agar gel electrophoresis and the RNA concentration was measured using NanoDrop 1000 (Thermo, USA). The PrimeScript™ RT reagent Kit with gDNA Eraser (TaKaRA, JAPAN) was used to remove any genomic DNA contamination and the first strand cDNA synthesis following the manufacturers’ protocol. Approximately 2 μg of RNA was used for each 20 μL reaction. Real-time quantitative PCR was conducted using SsoAdvanced™ Universal SYBR Green Supermix (BIO-RAD, USA) on a CFX96 Touch™ Real-Time PCR Detection System (BIO-RAD, USA). Each reaction mixture contained 10 μl SYBR Green Supermix, 1 μl cDNA template, 0.5 μl each primer, and 8 μl sterile distilled H2O. The PCR amplification cycle was as follows: 95 °C for 30 s, 40 cycles at 95 °C for 5 s, and 58 °C for 20 s. Melting curve analysis was performed ranging 60 to 95 °C to verify the specificity of the amplicon for each primer pairs. Relative fold differences were calculated based on the comparative Ct method using the 2-△△Ct method with the SlUBI as an internal reference gene. All the primers for qPCR were designed based on the reference sequence obtained from the tomato WGS chromosomes 2.50 (Additional file 5).
Availability of supporting data
Phylogenetic data (alignments and phylogenetic trees) supporting the results of this article have been deposited in TreeBASE respository and is available under the URL http://purl.org/phylo/treebase/phylows/study/TB2:S18045.
This work was supported by grants from the National High Technology Research and Development Program of China (2012AA101702), National Basic Research Program of China (2013CB127101), the National Natural Science Foundation of China (31071798, 31272166), the Committee of Science and Technology of Chongqing (2011BA1024), the Fundamental Research Funds for the Central Universities (CDJXS10231118).
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