Genome-wide identification and expression analysis of the calmodulin-binding transcription activator (CAMTA) gene family in wheat (Triticum aestivum L.)

doi:10.21203/rs.2.22898/v1

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Genome-wide identification and expression analysis of the calmodulin-binding transcription activator (CAMTA) gene family in wheat (Triticum aestivum L.)

https://doi.org/10.21203/rs.2.22898/v1

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Plant calmodulin-binding transcription activator (CAMTA) proteins play important roles in hormone signal transduction, developmental regulation, and environmental stress tolerance. However, in wheat, the CAMTA gene family has not been systematically characterized. In this work, 15 wheat CAMTA genes were identified using a genome-wide search method. Their chromosome location, physicochemical properties, subcellular localization, gene structure, protein domain, and promoter cis-elements were systematically analyzed. Phylogenetic analysis classified the TaCAMTA genes into three groups (groups A, B, and C), numbered 7, 6, and 2, respectively. The results showed that most TaCAMTA genes contained stress-related cis-elements. Finally, to obtain tissue-specific and stress-responsive candidates, the expression profiles of the TaCAMTAs in various tissues and under biotic and abiotic stresses were investigated. Tissue-specific expression analysis showed that all of the TaCAMTA genes were expressed in multiple tissues, suggesting that the wheat CAMTA genes may play important roles in growth and development. Under abiotic stress, TaCAMTA1, 3, and 6 were up-regulated after drought treatment, while the expression levels of TaCAMTA1 and 3 were induced after cold treatment, indicating that they may be involved in drought and cold stress response. This work systematically identified the CAMTA gene family in wheat at the whole-genome-wide level, providing important candidates for further functional analysis in developmental regulation and the stress response in wheat.

Plant Molecular Biology and Genetics

CAMTA

wheat

genome-wide identification

gene expression

Ca²⁺ signals, as one of the most important secondary messengers in plants, are widely involved in many adaptive and developmental processes [1]. In plants, there are three main classes of Ca²⁺ sensors to decode and transmit the Ca²⁺ signals, including calmodulin (together with calmodulin-like proteins) (CaMs/CMLs), calcium-dependent protein kinases (CDPKs), and calcineurin B-like proteins (CBLs) [2]. Most of the calmodulin/calmodulin-like proteins execute their biological functions by binding to calmodulin-binding proteins (CaMBPs), including transcription factors, protein kinases, ion channels, and enzymes, with the exception of CaM7, which can act as a transcription factor to directly regulate the expression of the HY5 gene [3]. To our knowledge, plant CaMs can regulate at least 90 transcription factors, including calmodulin-binding transcription activators (CAMTAs) [4].

CAMTA proteins are characterized by several conserved domains, including a unique DNA-binding domain (CG-1), a transcription factor immunoglobulin-like DNA-binding domain (TIG), ankyrin repeats (ANK), IQ motifs, and a Ca²⁺-dependent calmodulin-binding domain (CaMBD) [5–7]. To date, the CAMTA gene family has been identified in a wide variety of plant species, such as Arabidopsis (Arabidopsis thaliana, six members) [7], tomato (Solanum lycopersicum, seven members) [8], rice (Oryza sativa, seven members) [9], grape (Vitis vinifera, 10 members) [10], maize (Zea mays, nine members) [11], soybean (Glycine max, 15 members) [12], rape (Brassica napus, 18 members) [13], alfalfa (Medicago sativa, seven members) [14], poplar (Populus trichocarpa, seven members) [4], and citrus (Citrus sinensis and Citrus clementina, nine members) [15].

CAMTAs have been shown to be extensively involved in plant growth and developmental regulation, as well as in biotic and abiotic stress tolerance. In Arabidopsis, CAMTA1 and CAMTA2 work in concert with CAMTA3 to directly bind to the promoter of CBF2 to induce expression, leading to increased plant freezing tolerance [16, 17]. While AtCAMTA1 also positively regulates drought responses by regulating a few stress-responsive genes, including RD26, ERD7, RAB18, LTPs, COR78, CBF1, and HSPs [18], AtCAMTA3 can act as a negative regulator of plant immunity to modulate pathogen defense responses by activating the EDS1-mediated salicylic acid (SA) signaling [19]. A recent study showed that TaCAMTA4 may function as a negative regulator of the defense response against P. triticina, since the virus-induced gene silencing (VIGS)-based knockdown of TaCAMTA4 resulted in the enhanced resistance to P. triticina race 165 [20]. This suggested that one CAMTA member usually participates in multiple signaling pathways, while multiple CAMTA members often work together to participate in one signaling pathway.

Here, we obtained 15 TaCAMTA genes from wheat genomes. Their chromosome location, physicochemical properties, subcellular localization, gene structure, protein domain, promoter cis-elements, and expression profiles in multiple tissues as well as in response to stresses were systematically analyzed. Our work has established a foundation for the further analysis of wheat CAMTA genes and provides a basic understanding of their roles in development and stress responses.

Identification of the TaCAMTA gene family in wheat

Using the method described above, a total of 15 TaCAMTA genes were identified in wheat. Since the TaCAMTA genes were clustered into six homoeologous groups, these genes were designated as TaCAMTA1 to TaCAMTA6 according to their homology with rice CAMTA genes, plus a suffix corresponding to the specific wheat genome identifier (A, B, or D) for each gene name (Table 1, Fig. 1). For example, the TaCAMTA1 genes in genomes A, B, and D were named TaCAMTA1-A, TaCAMTA1-B, and TaCAMTA1-D, respectively. The results showed that TaCAMTA1, 2, 3, and 4 contained three homolog genes (TaCAMTA1-A/B/D, 2-A/B/D, 3-A/B/D, and 4-A/B/D), while TaCAMTA5 harbored two (TaCAMTA5-A/D), and TaCAMTA6 possessed one (TaCAMTA6-B). The highest number (eight genes: TaCAMTA3-A/B/D, 4-A/B/D, and 5-A/D) of TaCAMTA genes was found in homoeologous group 2, three TaCAMTA genes (TaCAMTA1-A/B/D) in homoeologous group 3, three TaCAMTA genes (TaCAMTA2-A/B/D) in homoeologous group 4, and one TaCAMTA gene (TaCAMTA6-B) in homoeologous group 5, while no TaCAMTA gene was identified in homoeologous groups 1, 6, and 7. Information relating to the 15 TaCAMTA genes, including gene names, locus IDs, open reading frame (ORF) lengths, chromosome locations, and the deduced polypeptides is provided in Table 1. The predicted TaCAMTA proteins contain 805 (TaCAMTA1-B) to 1067 (TaCAMTA2-B) amino acid residues, with molecular weights ranging from 90.82 kDa (TaCAMTA1-B) to 119.32 kDa (TaCAMTA2-A), and the isoelectric points ranged from 5.14 (TaCAMTA4-B) to 8.96 (TaCAMTA5-A) (Table 1).

The size of the CAMTA gene family in wheat is similar to that of oilseed rape (B. napus) and soybean (G. max) with 18 and 15 members [12, 13], respectively, but is higher than that of A. thaliana with six members, citrus (C. sinensis and C. clementina) with nine members, maize (Z. mays) with nine members, and alfalfa (M. truncatula) with seven members [5, 11, 14, 15]. The higher number of CAMTA genes may be due to gene duplication during chromosome polyploidization, since oilseed rape and soybean are tetraploid, whereas wheat is allohexaploid (AABBDD).

The subcellular locations were predicted with Plant-mPLoc. According to the results, all 15 wheat CAMTA proteins were located in the nucleus, which corroborates recent studies where the CAMTA proteins have typically been located in the nucleus [4, 21], confirming that their main function is to regulate the expression of other genes as transcription factors.

Table 1 Information of the 15 CAMTA gene members in wheat.

Gene	Locus ID	Chr. location^a	ORF length (bp)	Length (AA)	MW (kDa)	pI	Subcellular localization
TaCAMTA1-A	TraesCS3A02G433300	3A(−):674751244-674757428	3420	821	92.48	7.5232	Nucleus
TaCAMTA1-B	TraesCS3B02G469100	3B(−):715886740-715893072	3253	805	90.82	7.1271	Nucleus
TaCAMTA1-D	TraesCS3D02G426700	3D(−):539903862-539910357	3499	818	92.51	7.2482	Nucleus
TaCAMTA2-A	TraesCS4A02G407100	4A(−):679981642-679990156	3806	1066	119.32	5.8827	Nucleus
TaCAMTA2-B	TraesCS4B02G306300	4B(−):595277477-595286089	3764	1067	119.19	5.9095	Nucleus
TaCAMTA2-D	TraesCS4D02G304500	4D(−):472932312-472941309	3988	1066	119.16	5.8827	Nucleus
TaCAMTA3-A	TraesCS2A02G163000	2A(+):115413507-115422090	3443	1026	113.84	5.7467	Nucleus
TaCAMTA3-B	TraesCS2B02G188800	2B(+):164418775-164427330	3780	1027	114.11	5.8397	Nucleus
TaCAMTA3-D	TraesCS2D02G169900	2D(+):113911362-113919591	3783	1026	113.90	5.7476	Nucleus
TaCAMTA4-A	TraesCS2A02G283800	2A(+):475870112-475878163	3530	1027	114.42	5.2722	Nucleus
TaCAMTA4-B	TraesCS2B02G300800	2B(+):423658566-423666571	3407	1028	114.50	5.1358	Nucleus
TaCAMTA4-D	TraesCS2D02G282800	2D(+):355676387-355685067	3899	1030	114.91	5.182	Nucleus
TaCAMTA5-A	TraesCS2A02G229400	2A(−):258345594-258361280	3075	907	101.83	8.9645	Nucleus
TaCAMTA5-D	TraesCS2D02G237300	2D(−):239973233-239987968	2841	907	101.94	8.8824	Nucleus
TaCAMTA6-B	TraesCS5B02G521100	5B(−):683109213-683139863	3240	891	99.46	7.0588	Nucleus

ID: identity; Chr: chromosome; ORF: open reading frame; AA: amino acids; pI: isoelectric point; MW: molecular weight.

a Chromosomal location: “+” and “−” indicate the forward and reverse strand, respectively.

Phylogenetic analysis of the TaCAMTAs

To investigate the phylogenetic relationships of the CAMTA gene families, a phylogenetic tree of CAMTAs from five species, including wheat, Triticum urartu, Aegilops tauschii, A. thaliana, and rice, was constructed using the neighbor-joining (NJ) algorithm. The CAMTA gene families were highly conserved during the evolution of these species (Fig. 1). All of the 36 proteins from the five species were distinctly clustered into three groups (groups A, B, and C). Seven wheat CAMTAs (TaCAMTA2-A/-B/-D, 3-A/B/D, and 6-B), one T. urartu CAMTA (TuCAMTA3), two Ae. tauschii CAMTAs (AetCAMTA2, and 3), three rice CAMTAs (OsCAMTA2, 3, and 6), and three Arabidopsis CAMTAs (AtCAMTA1, 2, and 3) were clustered into group A. In addition, six wheat CAMTAs (TaCAMTA1-A/-B/-D, and TaCAMTA4-A/-B/-D), two T. urartu CAMTAs (TuCAMTA1, and 4), two Ae. tauschii CAMTAs (AetCAMTA1 and 4), two rice CAMTAs (OsCAMTA1, and 4), and one Arabidopsis CAMTA (AtCAMTA4) grouped into group B, while two wheat CAMTAs (TaCAMTA5-A/-D), one T. urartu CAMTA (TuCAMTA5), one Ae. tauschii CAMTA (AetCAMTA5), one rice CAMTA (OsCAMTA5), and two Arabidopsis CAMTAs (AtCAMTA5 and 6) clustered into group C.

[Figure 1]

Gene architectures and protein domain structures of the TaCAMTA members

The number of introns in all of the 15 TaCAMTA genes varied from 10 to 13, in which three CAMTA genes (TaCAMTA1-A/D and 6-B) possessed 10 introns, four CAMTA genes (TaCAMTA1-B and 4-A/B/D) possessed 11 introns, six CAMTA genes (TaCAMTA2-A/B/D and 3-A/B/D) possessed 12 introns, and two CAMTA genes (TaCAMTA5-A/D) possessed 13 introns (Fig. 2). Similar genomic structures of the CAMTA genes have been observed in other plant species, suggesting the conservation of CAMTA genes across plant species [8, 11, 12, 21].

[Figure 2]

Ten TaCAMTA proteins (TaCAMTA2-A/B/D, 3-A/B/D, 4-A/B/D, and 6-B) were predicted to contain all of the conserved domains of a typical CAMTA protein, including a CG-1 DNA-binding domain (Pfam03859), a TIG domain involved in non-specific DNA binding (Pfam01833), several ankyrin repeats (Pfam12796), an IQ motif (Pfam00612), and a calmodulin-binding domain (CaMB) (Fig. 3). Additionally, five TaCAMTA proteins (TaCAMTA1-A/B/D and TaCAMTA5-A/D) contained all of the conserved domains except for the TIG domain, which is consistent with previous studies that CAMTAs can be divided into two groups based on whether the TIG domain is present [22].

It has been confirmed that the IQ motif is able to bind with CaM in a Ca²⁺-independent manner, while the CaMB domain interacts with CaM in a Ca²⁺-dependent way [5, 7, 8]. It is interesting to note that all the wheat CAMTAs contain the IQ motif and a CaMB domain, indicating that wheat CAMTAs may interact with CaM in both a Ca²⁺-dependent and Ca²⁺-independent manner.

[Figure 3]

Cis-acting regulatory elements in the promoters of the TaCAMTAs

Several stresses/stimuli response cis-acting elements in the promoter regions (2000 bp upstream of the translation start site ATG) of the 15 TaCAMTA genes were predicted. Seven cis-elements were used in this study: abscisic acid (ABA)-responsive element (ABRE: ACGTG, ACGTSSSC, or MACGYGB) [23], SA-responsive promoter element (SARE: TGACG) [24], environmental signal response element (G-box: CACGTG) [25], WRKY binding site (W-box: TTGAC, or TGACC/T) [26, 27], phosphate starvation-responsive element (P1BS: GNATATNC) [28], sulfur-responsive element (SURE: GAGAC) [29], and the CAMTA binding site (CG-box: A/C/GCGCGG/T/C) [5].

The results showed that there were various known stresses/stimuli-related cis-acting elements that existed in the promoter regions of the 15 TaCAMTA genes. ABRE, SARE, W-box, and CG-box could be found in the promoter of all the 15 TaCAMTA genes, and four TaCAMTAs (TaCAMTA1-D, 3-B, 4-A, and 4-D) contained all seven types of cis-elements in the promoter region, including ABRE, SARE, G-box, W-box, P1BS, SURE, and CG-box. Meanwhile, the remainder of the 11 TaCAMTA genes contained at least five cis-elements in their promoter region (Table 2). It has been reported that more stress-related cis-elements are located in the promoter regions of wheat CAMTA genes than other plant species [13, 14], indicating that wheat CAMTA genes may be more widely involved in the plant response to stress.

Table 2 Numbers of stress-related cis-elements in the promoter regions of the TaCAMTA genes.

	ABRE	SARE	G-box	W-box	P1BS	SURE	CG-box
TaCAMTA1-A	11	1	1	4	1	0	17
TaCAMTA1-B	4	3	0	5	1	1	11
TaCAMTA1-D	7	7	2	3	1	3	10
TaCAMTA2-A	3	3	1	9	0	3	4
TaCAMTA2-B	10	1	1	5	0	3	14
TaCAMTA2-D	6	2	1	9	0	3	8
TaCAMTA3-A	1	2	0	5	0	2	3
TaCAMTA3-B	4	5	1	1	1	4	6
TaCAMTA3-D	2	5	1	2	0	2	5
TaCAMTA4-A	9	2	1	8	1	5	9
TaCAMTA4-B	5	4	2	7	0	3	10
TaCAMTA4-D	8	4	1	6	1	4	10
TaCAMTA5-A	1	1	0	7	0	3	5
TaCAMTA5-D	1	3	1	6	0	1	3
TaCAMTA6-B	1	1	0	11	1	2	2

ABRE, ABA-responsive element; SARE, SA-responsive promoter element; G-box, environmental signal response element; W-box, WRKY binding site; P1BS, phosphate starvation-responsive element; SURE, sulfur-responsive element; CG-box, the CAMTA binding site.

Tissue-specific expression patterns of the TaCAMTA genes

To elucidate the possible functions of the TaCAMTA genes in wheat, qRT-PCR assay was performed to investigate the spatial expression patterns of the TaCAMTAs. The results showed that all of the 6 TaCAMTA gene groups were expressed in multiple tissues, and the expression levels were generally higher in seedling than reproductive stage. TaCMATA2, 4, 5, and 6 showed highest expression in leaf during reproductive stage, while the expression of all TaCAMTAs were relatively lower in grain than other tissues (Fig. 4). This suggests that wheat CAMTA genes may play important roles in wheat growth and development.

[Figure 4]

Expression profiles of the TaCAMTA genes during abiotic stress

Previous studies have shown that plant CAMTAs could be involved in diverse environmental stresses. AtCAMTA1 and SlSR1L played a positive function in drought stress in Arabidopsis and tomato [18, 30], while plant CAMTAs also respond to salt and cold stress [11, 16, 31]. However, to date there is no information available on wheat CAMTAs involved in abiotic stresses. In this light, the expression profiles of the TaCAMTAs were analyzed under drought, NaCl, cold and heat stress. It showed that the TaCAMTA1, 3, and 6 were up-regulated after drought treatment, while the expression levels of TaCAMTA1 and 3 were induced after cold treatment (Fig. 5), indicating that they may play an important role in drought and cold stress response. Interestingly, the expression levels of almost all TaCAMTAs were inhibited by NaCl and heat treatment in wheat (Fig. 5), suggesting a different regulation and functions of TaCAMTAs in wheat compared with other plant species.

[Figure 5]

In conclusion, 15 CAMTA genes were identified in wheat in the present study. Analysis of the gene structure and protein domain, physicochemical properties, and the phylogenetic relationships indicated that the CAMTA gene family was highly conserved during plant evolution. Tissue-specific expression analysis suggested that the wheat CAMTA genes may play important roles in growth and development. Under abiotic stress, TaCAMTA1, 3, 6 may be associated with drought tolerance, while TaCAMTA1 and 3 may be involved in cold adaptation. Our findings provide new insight into the CAMTA gene family in wheat as well as a foundation for further studies on the roles of TaCAMTA genes in wheat development and growth as well as the stress response.

Genome-wide identification of the CAMTA gene family

Protein sequences of Triticum aestivum (IWGSC1.1), Triticum urartu (ASM34745v1), and Aegilops tauschii (ASM34733v1) were obtained from the Ensemble plant database (http://plants.ensembl.org) to predict the CAMTA genes [32]. The Hidden Markov Model (HMM) profile of the CG-1 domain (PF03859), the ANK repeat domain (PF00023), and the IQ domain (PF00612) sequences were downloaded from the PFAM database [33] and used to examine all wheat protein sequences using the HMMER search tool [34]. The obtained protein sequences were checked using the National Center for Biotechnology Information (NCBI) - Conserved domain database (CDD) search (https://www.ncbi.nlm.nih.gov/cdd) to identify the conserved protein domain with the default parameters. The redundant sequences containing complete CG-1, ANK repeats, and the IQ domain were further removed by alignment, and the remainder were considered as putative CAMTA genes. Finally, the biochemical parameters of the TaCAMTA proteins were calculated using the Compute pI/MW tool in the ExPASy database (https://web.expasy.org/compute_pi/). Subcellular localization of the TaCAMTA proteins was predicted online by Plant-mPLoc [35].

Phylogenetic tree construction and sequence analysis

Protein sequences from Arabidopsis and rice were obtained from NCBI (http://www.ncbi.nlm.nih.gov/) and EnsemblPlants (http://plants.ensembl.org/index.html). The amino acid sequences of all CAMTAs were aligned using the ClustalX program with the default parameters, and a phylogenetic tree was constructed in MEGA-X using the neighbor-joining method with 1000 bootstrap replicates [36]. The display of the phylogenetic tree was optimized using the Interactive Tree Of Life (iTOL) v4 [37].

The schematic structures of the TaCAMTA genes were analyzed online using the Gene Structure Display Server 2.0 based on exon/intron data (GSDS 2.0, http://gsds.cbi.pku.edu.cn/) [38]. The domain structures of the TaCAMTA proteins were analyzed in the Pfam database (http://pfam.janelia.org/) and NCBI Conserved Domains Search online tool (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) [39]. The CaMB domain was specifically analyzed using the Calmodulin Target Database (http://calcium.uhnres.utoronto.ca/ctdb/ctdb/).

Prediction of cis-acting elements in the TaCAMTA genes

To investigate the cis-elements in the promoter sequences of the TaCAMTA genes, 2-kb sequences upstream of the initiation codon (ATG) were collected from the Ensemble plant database (http://plants.ensembl.org) and subjected to the PLACE database (https://www.dna.affrc.go.jp/PLACE) [32, 40].

Plant materials and treatments

Jinhe 9123, a drought-insensitive wheat variety cultivated by our lab, was used in this study. For stress treatment experiments, seeds were surface-sterilized in 1% NaClO and repeatedly rinsed with tap water, then seeded in 1/2 Hoagland nutrient solution after immersion and imbibition for 12 h, and hydroponically cultivated in the incubator with a 16/8-h photoperiod at 25 °C. Four ten-day-old homogeneous seedlings groups, each of which included 30 seedlings from three biological replicates, were subjected to different treatments, including 16.1% PEG6000, 200 mM NaCl, cold (4 °C) and heat (40 °C). The shoot tissue was sampled for the experiment. For analyses of tissue-specific expression patterns, root and shoot from ten-day-old seedlings, root, stem, leaf, spike at flowering in reproductive stage, and grain 15 DAA were collected from wheat plants. Collected samples were immediately frozen in liquid nitrogen and stored at −80 °C for RNA extraction.

RNA isolation and gene expression analysis

Total RNA of collected samples was isolated using the EasyPure^® Plant RNA Kit (ER301-01, Transgen, China). For reverse transcription, the first-strand cDNA was synthesized using a PrimeScript^TM RT reagent Kit (RR047A, TaKaRa, Japan). Quantitative real-time PCR (qRT-PCR) for examination of the TaCAMTAs expression patterns were performed using the TB Green^TM Premix Ex Taq^TM II (RR820A, TaKaRa, Japan) with 7500 Real-Time PCR System (Applied Biosystem, USA). Gene specific and internal reference gene TaActin primers were listed in Additional file 1: Table S1. The qRT-PCR program was carried out as follows: predenaturation at 95 °C for 30 s; denaturation at 95 °C for 5 s, annealing at 58 °C for 30 s, extension at 60 °C for 34 s, 45 cycles. 2^−ΔΔCt method was used to analyze the data [41]. All experiments were performed with three technical replicates and three biological replicates, and the data were represented by mean value ± standard error of three biological replicates.

Additional file 1: Table S1. Primer sequences of TaCAMTA and TaActin genes used for qRT-PCR analysis.

The data sets supporting the article are included within the article and its additional files.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Funding

This research was financially supported by the National Natural Science Foundation of China (31600216), the Natural Science Foundation of Hebei Province, China (C2017301066), and the HAAFS Agriculture Science and Technology Innovation Project (2019-4-8-1).

Authors' contributions

ZS designed the study and wrote the manuscript. YF carried out bioinformation analyses. DFS carried out the qRT-PCR analyses. LYW and LMY collected plant materials. ZH and CJF carried out RNA isolation.

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Genome-wide identification and expression analysis of the calmodulin-binding transcription activator (CAMTA) gene family in wheat (Triticum aestivum L.)

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