Legume Research

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Legume Research, volume 45 issue 6 (june 2022) : 700-710

Genome-wide Analysis of WRKY Transcription Factors Family in Chickpea (Cicer arietinum L.)

Rajendra Tukaram Shende1,*, Reeva Singh1, Arun Kumar1, Rakesh Singh Sengar1
1Department of Agricultural Biotechnology, Sardar Vallabhbhai Patel University of Agriculture and Technology, Meerut-250 110, Uttar Pradesh, India.
  • Submitted17-02-2020|

  • Accepted29-10-2020|

  • First Online 28-01-2021|

  • doi 10.18805/LR-4352

Cite article:- Shende Tukaram Rajendra, Singh Reeva, Kumar Arun, Sengar Singh Rakesh (2022). Genome-wide Analysis of WRKY Transcription Factors Family in Chickpea (Cicer arietinum L.) . Legume Research. 45(6): 700-710. doi: 10.18805/LR-4352.
Background: Chickpea (Cicer arietinum L.) is used as a protein source across the world. In plants WRKY transcription factors play an important role in regulation of stress resistance. An attempt was made to analyze WRKY genes in chickpea using genomic data.

Methods: In this In Silico investigation during 2018-2019, to analyze the WRKY genes in chickpea using genomic data. iTak database are used to obtain gene data. Bioinformatics tools were used to analyzed the chickpea genomic data.

Result: This study reported 61 Car WRKY genes, located on the seven main chromosomes of chickpea. Great variations were reported in terms of protein length, molecular weight, grand average of hydropathicity (GRAVY) value and theoretical isoelectric points of Car WRKYs. Gene Structure Display Server (GSDS) demonstrated that the Car WRKY 56 gene lack introns. Phylogenetic analysis of Car WRKY proteins divided in three main groups (I, II and III); group II was divided into three subgroups like IIa, IIb and IIc. By this an attempt has made to provide novel information on Car WRKY genes to study abiotic stress mechanism in chickpea.
Chickpea (Cicer arietinum L.), a legume having 2n=2x=16 chromosomes is self-pollinated crop. It is a cool season crop and globally cultivated in dry and semi-dry areas (Acharjee and Sarmah 2013; Sani et al., 2018). It ranks third in the world among pulse crops after dry beans and dry peas. India ranks first in area and production among the chickpea growing countries (Muehlbauer and Sarker 2017). Chickpea seeds are rich in protein (26.4%), carbohydrate (64.6%) and vitamins. It fixes nitrogen symbiotically with root nodule forming bacteria, rhizobium this helps to increase soil fertility by addition of 60 kg ha-1 nitrogen under regular precipitation. (Varshney et al., 2013; Unkovich and Pate, 2000). Complete genome sequence assembly offers good opportunity for genome-wide identification and analysis of WRKY genes. (Thudi et al., 2016; Varshney et al., 2013).
       
Transcription factors (TFs) in promoter region are known to play a role in transcription by interacting with their corresponding cis-regulatory elements. WRKY TFs are known for presence of heptad amino acid sequence-WRKYGQK in DNA binding domain extending up to 70-80 amino acids in length (Ciolkowski et al., 2008; Duan et al., 2007; Yamasaki et al., 2005; 2012). In higher plants WRKY TFs is principal family (Eulgem et al., 2000) reported first time in sweet potato (WRKY TF (SPF1), for gene regulation under abiotic stress (Ishiguro and Nakamura, 1994), are known to play role in in the crosstalk of signaling pathways (Eulgem et al., 2000; Chen et al., 2012; Agarwal et al., 2011). The WRKY genes were found to be responsive during wounding in chickpea by activating defenses through up-regulation of genes coding oxidase, pathogenesis, phenylpropanoid pathway and CYTP450 related to biotic stress (Kumar et al., 2016; Pandey et al., 2017).
       
Mare et al., (2004) reported involvement of WRKY genes in abiotic stress tolerance, their played a role for increased drought tolerance in Arabidopsis and rice; e.g. transgenic rice (OsWRKY11 gene) known for improved drought and heat tolerance (Wu et al., 2009; Seki et al., 2002). The WRKY gene has differentially expressed in chickpea plants under drought condition (Ramalingam et al., 2015). By these studies, the role of TFs in signaling pathways has been revealed; however, there is little knowledge of the molecular mechanisms involved in drought tolerance in legume especially in chickpea. Using iTAk-database the WRKY TFs were identified but their properties were not reported. This study was conducted for genome-wide identification and analysis of WRKY genes of chickpea to provide the opportunity for functional validation of WRKY genes during abiotic stress.

Identification of CarWRKY family genes

Different approaches for identification of WRKY TFs in chickpea were used. We used iTAK- database (http://itak.feilab.net/cgi-bin/itak/db_family_gene_list.cgi) for obtaining chickpea WRKY TFs. HMM (Hidden Markov Model) (http://smart.embl-heidelberg.de/) was used to examine resulting protein sequences for presence of WRKY domain (Letunic et al., 2012). The e-value showing hits less than 0.01 were collected. Putative WRKY genes were selected on the basis of non-redundant protein sequences encoding complete WRKY domain and discarded those genes which do not have complete WRKY domain. Gene sequences, protein sequences and chromosomal location of selected chickpea WRKY TFs were obtained from Chickpea Genome Transcriptome Database (http://itak.feilab.net/cgi-bin/itak/index.cgi) and NCBI (https://www.ncbi.nlm.nih.gov).

 
Chromosome localization and gene structure analysis
 
Chromosomal localization of CarWRKY genes was analyzed by using MapInspect software. Complementary DNA sequences with respective genome sequence were aligned to construct the gene structure of CarWRKY through Gene Structure Display Server (GSDS 2.0, http://gsds.cbi.pku.edu.cn/) (Hu et al., 2015).
 
Conserved motif and protein property analysis
 
Multiple Em for Motif Elicitation (MEME) tool (http://meme-suite.org/tools/meme) was used for analysis of conserved domain of CarWRKY proteins and parameters optimized were: any number of repetitions; maximum number of motifs (15), minimum sites (5) and optimum width of each motif (ranged between 6-50 residues). The MAST program of meme tool was used to search detected motifs in protein databases (Ma et al., 2015). ProtParam tool ExPASy was used for calculating Isoelectric Point (pI), grand average of hydropathicity (GRAVY) and theoretical molecular weight (MW).
 
Sequence alignment and phylogenetic analysis
 
To perform multiple sequence alignments WRKY proteins of Cicer aretinum. ClustalW program was used. MEGA 6.0 software was used to the build phylogenetic tree by using neighbor-joining (NJ) method with 1000 replicates of bootstrap test (Kumar et al., 2016). Classification of CarWRKY TFs was carried on the basis of multiple sequence alignment, this was used to assign the corresponding groups and subgroups.
Genome-wide identification of chickpea WRKY gene family
 
The WRKY domain (PF03106) obtained from the Pfam protein family database (http://pfam.sanger.ac.uk/) (Finn et al., 2008) was used for HMM profile. SMART tools were used for testing of each WRKY TFs matching sequence with less than 0.01 e-value, this resulted in to 67 putative genes that could be annotated as WRKY TFs. The six WRKY genes (Ca_01713, Ca_03832, Ca_5782, Ca_06124, Ca_16393 and Ca_21883) were removed due to the lack of WRKY domain. Remaining 61 putative genes were named as per their location on chromosome as CarWRKY01 to CarWRKY61. Five genes were not mapped to any chromosomes were names as CarWRKY57 to CarWRKY61 (Table 1).
 

Table 1: Features of the gene and proteins of putative CarWRKY family in chickpea.


       
As WRKY transcription family is one of the most important family for regulation of genes in plants, it primarily involved in modulation of stress and not in developmental processes in plants (Rushtom et al., 2000). Thus, based on the publicly available sequence information total 61 CarWRKY genes were identified. Comparatively chickpea has a large number of transcription factors as compared to grapes 59 (WRKYs) (Guo et al., 2014), castor bean (58 WRKYs) (Zou et al., 2016), physic nut (58 WRKYs) (Xiong et al., 2013), peach (58 WRKYs) (Chen et al., 2016), cucumber (57 WRKYs) (Ling et al., 2011), tea (50 WRKY) (Wu et al., 2016), barley (45 WRKYs), (Mangelsen et al., 2008) and hemp (40 WRKYs) (Xin et al., 2016). However, maize (136 WRKYs) (Wei et al., 2012), soybean (131 WRKYs) (Yu et al., 2016), apple (127 WRKYs) (Meng et al., 2016), poplar (104 WRKYs) (He et al., 2012), rice (100 WRKYs) (Ross et al., 2007), kiwi fruit (97 WRKYs), (Jing and Liu, 2018), tomato (81 WRKYs) (Huang et al., 2012), Arabidopsis (72 WRKYs) (Eulgem et al., 2000) reported more number of transcription factors in comparison with chickpea.
       
More number of WRKY transcription factors may be due increased plant genome size during evolution (Meng et al., 2016). The genome size of some plant species can be given as: apple (927 and 724.3 Mb) (Han et al., 2007), soybean (978 Mb) (Song et al., 2016), chickpea (738.09 Mb) (Varshney et al., 2013), kiwifruit (616.1 Mb) (Huang et al., 2013), grape (490 Mb) (Jaillon et al., 2007) and finally cucumber (367 Mb) (Huang et al., 2009). However, some scientists interpreted that there is not any correlation between number of WRKY TFs and the genome size of respective plant (Song et al., 2016). There is variation in WRKY TFs of apple and soybean although their genome size is approximately similar.
 
Physiochemical property analysis
 
ProtParam tool ExPASy revealed longest amino acid CarWRKY33 (724 aa) and CarWRKY41 is the shortest (105 aa) found in chickpea however protein size ranged between 12.63 kDa (CarWRKY41) to 78.62 kDa (CarWRKY33) and theoretical isoelectric point (pI) ranged 4.77 (CarWRKY01) to 9.91 (CarWRKY51). This indicates the physiological traits of WRKY proteins extraordinarily varied for PI and MW, exhibiting a high degree of complexity within the CarWRKY genes. The GRAVY value for all studied genes was below zero and ranged from -1.157 to -487 (Table 1), which suggests that all 61 CarWRKY proteins were hydrophilic. As per Drews et al., (2004) grand average of hydropathicity (GRAVY) value of protein above zero shows hydrophobic characteristics, while the value below zero shows its hydrophilic nature.

Chromosomal localization
 
Sixty-one CarWRKY genes distributed unevenly on among chromosomes. Fifty-six out sixty-one CarWRKY genes were distributed on seven chromosomes (Fig 1). Another five genes (CarWRKY57-CarWRKY61) are not assigned to any chromosome, because they reported on scaffold region. Chromosome 1 located largest number of genes (10 CarWRKY genes) and lowest number of gens were present on chromosome 4 (6 CarWRKY genes). The chromosome number 3 and 6 contain 9 CarWRKY genes while chromosome 7 contain 8 CarWRKY genes. Chromosome 2 and 5 contained equal number of 7 genes. In common bean Wang et al., (2016) reported similar results, they reported 90 PvWRKY genes distributed across all 11 chromosomes and named as PvWRKY1 to PvWRKY90. Chromosome 8 contained largest 18 WRKY genes, followed by chromosome 2 and 9 with 16 and 12 genes respectively.
 

Fig 1: CarWRKY genes distributed on chickpea chromosomes.


 
Gene structure analysis
 
As per Gene Structure Display Server (GSDS 2.0) we determined the structure of all 61 CarWRKY genes i.e. the intron/exon distribution pattern to get information about the evaluations of these genes in chickpea. Most of the introns reported to be located near the 5’ end. The diversity exhibited in terms of number of introns ranged between 1 to 5. Five genes reported presence of one intron, however, two introns were reported in 33 CarWRKY genes, seven genes reported three introns, 4 Introns in 9 genes and 5 introns in 6 genes. Larger introns were reported in 33 genes whereas CarWRKY56 did not contain any intron.
 

Fig 2: Gene structure of CarWRKY genes.


       
Li et al., (2015) reported similar structural features in rubber plant. They reported introns ranged 1-5 introns in WRKY gene. Some rice species didn’t report any introns in their WRKY genes (Xie et al., 2005; Ross et al., 2007) and supposed that during the evolution there might be intron loss events. Phylogenetic grouping of genes, there diversity in structure between exons and introns is helpful tool for the evolution, diversification and neofunctionalization of gene families (Shiu and Bleecher 2003; Wang et al., 2014).
 
Conserved domain analysis
 
MEME suite tools showed diversity among CarWRKY proteins and predicted motifs in CarWRKY genes family. From the candidate CarWRKY protein, we reported 15 conserved motifs (Fig 3 and 4) each indicating its conserved CarWRKY domain.
 

Fig 3: Schematic representation of amino acid motifs of CarWRKY proteins by using MEME online tools.


 

Fig 4: Sequence logos of chickpea CarWRKY domains.


       
Few WRKY proteins have showed that motifs such as leu-zipper motif, a putative new class of DNA binding protein also exist besides the 60 conserved amino residues (Eulgem et al., 2000; Cormack et al., 2002). The complexity and diversity study of these WRKY motifs shows importance of WRKY genes in growth regulation and stress responses. The WRKY proteins harbor a characteristic WRKY domain of around 60 amino acids with conserved oligopeptide sequence (WRKYGQK) at N-terminal along with Cys2His2/Cys2HisCys zinc finger motif (CX4-7CX22-23HXH/C) at C-terminal (Rushton et al., 2010; Schluttenhofer and Yuan 2015). The conservation of cysteine and histidine in the WRKY domain is responsible for the formation of unique zinc finger-like motif and sequence of WRKY amino acids can directly bind with W box (TTG ACT /C) cis-regulatory element, which are found in upstream regions of target genes (Zhang et al., 2018).
 
Multiple sequence alignment and phylogenetic analysis
 
The ClustalW and Neighbor-Joining (NJ) method criteria was used for construction of unrooted phylogenetic tree with the passion correlation, pairwise detection and bootstrap 1000 replicates parameters. On the basis of classification done by Sakuma et al., (2002) we generated phylogenetic tree, it was classified into three different groups designated as group I, II and III group. Group II was subdivided into three subgroups such as group IIa, IIb and IIc. Group I consisted six genes, group III consisted 15 genes, however, group II reported total 40 genes which was largest among all other groups. Subdivisions of group II consisted 12 genes in subgroup IIa and 14 genes in each sub group IIb and IIc (Fig 5). The phylogenetic tree-based classification of chickpea followed the same trend as in other crop species. The characterization of WRKYs with respect to intron/exon distribution and conserved domains revealed the conservation of gene structure as well as domains among the members of a same group in the phylogenetic tree. These three major groups were subdivided into seven sub classes i.e. I, II, IIa, IIb, IIc and III as reported by Eulgem et al., (2000).
 

Fig 5: Phylogenetic tree of CarWRKY proteins from chickpea.

In this study, we performed a genomic analysis of WRKY transcription factors in chickpea (Cicer arietinum L.). We reported 61 candidate CarWRKY genes from chickpea genome noted as the CarWRKY; subsequently they were analyzed to described their gene and protein features by studying exons/introns, chromosome number etc. while Isoelectric point (pI), protein molecular weight and grand average of hydropathicity (GRAVY) were analyzed to study protein features. On the basis of chromosomal localization all chickpea carWRKY candidate genes were distributed on total seven chromosomes. These genes were classified on the basis of phylogenetic tree into three main and subgroups. Present study on chickpea will helpful for further research on CarWRKY functions in abiotic stress studies.
The authors want to express their sincere gratitude to the Indian Council of Agricultural Research (ICAR) for providing financial support through ICAR-SRF fellowship to corresponding author.

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