GENOME-WIDE IDENTIFICATION AND CHARACTERIZATION OF THE GATA TRANSCRIPTION FACTOR FAMILY SUGGESTS FUNCTIONAL EXPRESSION PATTERN AGAINST VARIOUS ENVIRONMENTAL CONDITIONS IN CASSAVA (Manihot esculenta)

T. V. Tien¹, V. H. La², N. Q. Trung³, P. C. Thuong⁴, B. T. T. Huong³, L. V. Nguyen³, D. H. Gioi³, Q. T. N. Le⁵, H. Thi T. Tran⁶, H. D. Chu^7,* and P. B. Cao^8,*

¹ National Academy of Public Administration, Nguyen Chi Thanh Road, Dong Da District, Hanoi City 122300, Vietnam

² Hanoi Pedagogical University 2, Phuc Yen City, Vinh Phuc Province 280000, Vietnam

³ Vietnam National University of Agriculture, Ngo Xuan Quang Road, Gia Lam District, Hanoi City 122300, Vietnam

⁴Ministry of Science and Technology, Tran Duy Hung Road, Cau Giay District, Hanoi City 122300, Vietnam

⁵ Thuyloi University, Dong Da District, Hanoi City 122300, Vietnam

⁶Hanoi National University of Education, Xuan Thuy Road, Cau Giay District, Hanoi City 122300, Vietnam

⁷ University of Engineering and Technology, Vietnam National University Hanoi, Xuan Thuy Road, Cau Giay District, Hanoi City 122300, Vietnam

⁸ Hung Vuong University, Nguyen Tat Thanh Street, Nong Trang Ward, Viet Tri City, Phu Tho Province 35000, Vietnam

^*Corresponding author: Ha Duc Chu; Email: cd.ha@vnu.edu.vn and Phi Bang Cao; Email: phibang.cao@hvu.edu.vn

ABSTRACT

GATA transcription factors (TFs) play a significant role in regulating many plant physiological processes. The GATA TF family has been identified and characterized in many important crop species. However, no information is available on the GATA TFs in cassava (Manihot esculenta). In this study, 36 MeGATA genes have been comprehensively identified, annotated, and characterized in the cassava genome using various bioinformatics tools. The gene structure and duplication of the MeGATA genes indicated the redundancy and differences in their gene structural organization. The GATA TFs in cassava could divide into three different groups, as in other plant species. Interestingly, the expression levels of the MeGATA genes were significantly changed in various major organs/tissues in the growth and development, especially in response to adverse environmental conditions. Taken together, this study could propose a list of candidate genes for further functional characterization of stress-inducible MeGATA genes in cassava.

Keywords: GATA, transcription factor, identification, gene duplication, cassava, expression, characterization.

INTRODUCTION

Cassava (Manihot esculenta) has been regarded as one of the most important cash crops that are primarily grown in Asia, Africa, and tropical America (Malik et al., 2020). As containing a high starch percentage in storage root, cassava is a primary food source for at least 750 million people (De Souza et al., 2017). This tube crop can also be processed into starch, flour, and alcohol for daily use in food or feed (Malik et al., 2020). However, adverse environmental conditions caused by climate change, such as drought, salt, and heavy metal stress (considered abiotic stress), and cassava brown strike disease (CBSD) (Tomlinson et al., 2018) (considered biotic stresses) are reported as the main factor significantly affecting the growth, development, and productivity of cassava. Thus, understanding the gene regulation related to the defense mechanism in cassava plants plays a crucial role in improving cassava stress tolerance.

It is now well-established that stress tolerance is regulated by some specific genes, such as genes encoding functional and regulatory proteins, particularly transcription factors (TFs), enzymes, chaperones, and metabolites that enable plants to withstand adverse environmental conditions (Agarwal and Jha, 2010; Lindemose et al., 2013; Reddy et al., 2013). Particularly, TFs have been described to regulate gene expression by specifically interacting with cis- regulatory elements from the promoter of the targeted genes. Among them, GATA TFs, a group of type IV zinc-finger proteins (Behringer and Schwechheimer, 2015), which specifically bind to the DNA sequence -(A/T)GATA(A/G)- and act as regulators of gene expression (Schwechheimer et al., 2022). This TF has been implicated in the regulation of the development of major organs, including leaves, roots, and flowers (Schwechheimer et al., 2022). Up till now, the GATA TFs have been reported in various higher plant species, including Arabidopsis thaliana (Teakle et al., 2002), rice (Oryza sativa) (Reyes et al., 2004), soybean (Glycine max) (Zhang et al., 2015), apple (Malusdomestica) (Chen et al., 2017), grape (Vitis vinifera) (Zhang et al., 2018), chickpea (Cicer arietinum) (Niu et al., 2020) and potato (Solanum tuberosum) (Yu et al., 2022). However, the information on the GATA TFs in cassava is still lacking, even though the assembly of this important crop has been released recently (Bredeson et al., 2016).

The purpose of this present study was to comprehensively analyze the GATA TFs in cassava by computational approaches. Firstly, all putative members of the GATA TFs were identified and annotated from the recent assembly of cassava. The major characteristics of the GATA TFs were then analyzed by using various web-based tools. Finally, expression patterns of genes encoding GATA TFs in major organs under various conditions were explored by re-analyzing the previous transcriptome databases.

MATERIALS AND METHODS

Identification and annotation of the GATA TFs: To seek the GATA TFs from the assembly of cassava (Bredeson et al., 2016) and the PlantTFDB platform (Jin et al., 2016) was used to screen all potential members of the GATA TFs. The presence of the conserved domain of GATA TFs (Schwechheimer et al., 2022) was confirmed by screening against the Pfam database (Mistry et al., 2021). All potential members of the GATA TFs were then BlastP-ed against the assembly of cassava (Bredeson et al., 2016) from NCBI and Phytozome (Goodstein et al., 2012) to annotate their identifiers, such as GeneID, ProteinID, and LocusID and seek their sequences, including coding DNA sequence (CDSs), genomic DNA sequence (gDNA) and full-length protein sequence, and chromosomal locations for further analyses.

Prediction of the duplication events of genes encoding the GATA TFs: To analyze the gene duplication, a comprehensive comparison between genes encoding the GATA TFs was carried out as previously described (La et al., 2022; Niu et al., 2020). Particularly, the CDSs of all identified genes encoding GATA TFs were aligned by using ClustalX (Larkin et al., 2007). The identity matrix between these genes was then generated by BioEDIT (Hall, 1999). A duplicated pair was defined with the standard of more than 70% identity (La et al., 2022). The rate of non-synonymous substitutions per non-synonymous site (Ka) and synonymous substitutions per synonymous site (Ks) of each pair were measured by using the DnaSP (Rozas et al., 2017).

Analysis of features of the GATA TFs: To calculate the characteristics of the GATA TFs, the full-length protein sequence of each member was used to apply in the Expasy Protparam (Gasteiger et al., 2005) as following the previous study (Niu et al., 2020). Particularly, several properties of each protein molecule, including protein size (amino acid residues), molecular mass (kilo Dalton, kDa), iso-electric point (pI), instability index (II), aliphatic index (AI), and grand average of hydropathy (GRAVY) were explored (Gasteiger et al., 2005).

Investigation of the subcellular localization of the GATA TFs: To predict the subcellular localization of the GATA TFs, full-length protein sequences of all proteins were used to apply the YLoc tool (Briesemeister et al., 2010) as previously described (La et al., 2022). Particularly, the signal peptide from the full-length protein sequence was mapped into 10 locations in the cell of the plant model, including the nucleus, cytoplasm, mitochondrion, plasma membrane, extracellular space, endoplasmic reticulum, peroxisome, Golgi apparatus, vacuole and chloroplast (Briesemeister et al., 2010).

Construction of the phylogenetic tree of the GATA TFs: To investigate the relationship of members of the GATA TFs, a phylogenetic tree was constructed by using the Molecular Evolutionary Genetics Analysis (MEGA) software (Kumar et al., 2016) as previously reported (Chu et al., 2018; Niu et al., 2020). Particularly, all full-length protein sequences were subjected to the software to generate a Neighbor-Joining tree with 1,000 bootstrap repeats. Other default parameters, such as the model, inter-site ratio, and gap deletion data processing were designed as P-distance, uniform ratio, and partial deletion, respectively (Kumar et al., 2016).

Structural analysis of genes encoding the GATA TFs: To analyze the structure of genes encoding the GATA TFs, the organization of the exon and intron of each gene was explored as previously described (Niu et al., 2020). Briefly, the lengths of gDNA and CDS of each gene were calculated by using the BioEDIT software (Hall, 1999). The gDNA and CDS were then subjected to the Gene Structure Display Server (GSDS) (Hu et al., 2015) to construct the exon/intron structure.

Re-analysis of expression patterns of genes encoding the GATA TFs: To investigate the expression profiles of genes encoding the GATA TFs in cassava, previously reported microarray databases available in the NCBI GEO (Barrett et al., 2013) were used to comprehensively analyze. Briefly, the expression patterns of genes encoding the GATA TFs were explored in 11 major organs/tissues, including leaf blade, leaf mid vein, petiole, stem, lateral bud, shoot apical meristem (SAM), storage root, fibrous root, root apical meristem (RAM), organized embryogenic structure (OES) and friable embryogenic callus (FEC) by retrieving the GSE82279 dataset as previously provided (Wilson et al., 2017). The fragments per kilobase of transcript per million reads mapped (FPKM) value was used to represent the expression profile of each gene (Wilson et al., 2017). Next, three transcriptome atlas, related to biotic stress, particularly CBSD inoculation (GSE56467) as previously reported (Maruthi et al., 2014), and abiotic stress conditions, including polyethylene glycol 6000 treatment (GSE93098) (Ding et al., 2017) and drought stress (GSE98537) (Zhu et al., 2020) were re-analyzed. Finally, the heatmaps of the GATA gene’s expression were then clustered by R script.

RESULTS AND DISCUSSION

Genome-wide survey and expansion of the GATA TFs in cassava: As a result, a total of 36 putative members of the GATA TFs was identified in the cassava assembly (Table 1). These members were then annotated as the MeGATAs, and 36 MeGATAs were renamed from MeGATA1 to 36 based on their positions in the chromosomes (Figure 1). The chromosomal distribution of all 36 members of the GATA TFs in cassava was described in Figure 1.

Table 1. Summary of the MeGATA TFs in cassava.

pI - Isoelectric point, II - Instability index, AI - Aliphatic index, GRAVY - Grand average of hydropathy, SL - Subcellular localization

Previously, the GATA TFs have been screened in several plant species, such as A. thaliana (Teakle et al., 2002), rice (Reyes et al., 2004), soybean (Zhang et al., 2015), chickpea (Niu et al., 2020) and potato (Yu et al., 2022). For example, 29 and 28 members of the GATA TFs have been studied in A. thaliana and rice, respectively (Reyes et al., 2004; Teakle et al., 2002). In soybean, the GATA TFs contained 64 members ( Zhang et al., 2015), while 19 and 35 GATA TFs were identified and characterized in grape (Zhang et al., 2018) and apple (Chen et al., 2017), respectively. Additionally, 25 members of the GATA TFs have been reported in chickpea (Niu et al., 2020). Recently, the GATA TFs, with 49 members have been identified in potato (Yu et al., 2022). This present study screened 36 members of the GATA TFs in cassava, which were assigned as MeGATA01 to MeGATA36 according to the selected order (Table 1, Figure 1), lower than potato (49 members) (Yu et al., 2022) and soybean (64 members) (Zhang et al., 2015), but higher than grape (19 members) (Z. Zhang et al., 2018), chickpea (25 members) (Niu et al., 2020), rice (28 members) (Reyes et al., 2004), A. thaliana (29 members) (Teakle et al., 2002) and apple (35 members) (Chen et al., 2017).

To explain the expansion of genes encoding GATA TFs in cassava, the gene duplication was predicted based on the similarity of their corresponding CDSs. As expected, among 36 MeGATA genes, a total of 10 duplication events (with 20 duplicated genes) was found by using various tools as previously described (La et al., 2022; Niu et al., 2020). The similarity of the duplicated MeGATA genes was varied from 72.2 (MeGATA11 and 34) to 90.1% (MeGATA03 and 04) (Table 2). All duplicated MeGATA pairs have been produced by segmental duplication events (Table 2, Figure 1). Particularly, two duplicated pairs, MeGATA02 and 06, and MeGATA03 and 04 have occurred from chromosomes 1 and 2, respectively (Table 2, Figure 1), while two (MeGATA07 and 29, MeGATA08 and 31) and two (MeGATA10 and 32, MeGATA11 and 34) were found to localize on chromosomes 3 and 15, and chromosomes 3 and 16, respectively (Table 2, Figure 1). Next, two pairs, namely MeGATA17 and 26, and MeGATA20 and 25 were distributed on chromosomes 7 and 10, respectively (Table 2, Figure 1). Two remaining duplicated pairs, namely MeGATA12 and 28, and MeGATA15 and 36 were mapped on chromosomes 4 and 11, and chromosomes 5 and 18, respectively (Table 2, Figure 1).

Table 2. The information of duplicated events occurred in the MeGATA gene family in cassava

Next, in order to predict the natural pressure acting on the MeGATA genes during evolution, the Ka and Ks values of 10 duplicated pairs were estimated by using DnaSP software (Rozas et al., 2017) according to previous guided (La et al., 2022; Niu et al., 2020). According to Table 2, the Ka/Ks rate of all duplicated MeGATA genes from cassava was found to range from 0.32 (MeGATA03 and 04) to 1.11 (MeGATA02 and 06). It is indicated that the Ka/Ks ratio of a majority of the duplicated pairs (eight out of 10) is less than 1.0, suggesting that the MeGATA genes may undergo strong purifying selection pressure during evolution.

Previously, the duplication events were also predicted in genes encoding GATA TFs from higher plant species. For example, eight duplication events (18 duplicated genes) were found as segmental duplications in CaGATA genes in chickpea (Niu et al., 2020). In soybean, 23 (out of 25) duplicated pairs of GmGATA genes were localized in segmental duplication blocks ( Zhang et al., 2015). Recently, 16 duplicated StGATA genes were detected to be involved in duplicated genomic blocks in potato (Yu et al., 2022). Taken together, these findings strongly hypothesized that segmental duplication events might play a key role in the expansion of genes encoding GATA TFs in cassava, perhaps in higher plant species.

Analysis of protein features and subcellular localization of the GATA TFs in cassava: Table 1 summarized six features (including size, mass, pI, II, AI, and GRAVY) of 36 members of the GATA TFs in cassava. Among them, MeGATA21 was found as the smallest member of the GATA TFs in cassava (with 106 amino acid residues, while the largest member was MeGATA03 (544 amino acid residues) (Table 1). The molecular mass of the GATA TFs in cassava varied from 12.17 (MeGATA21) to 60.49 kDa (MeGATA03) (Table 1). The pI value of MeGATA21 was 11.02 and MeGATA18 was 4.73, which were the largest and smallest pI values in the GATA TFs in cassava, respectively (Table 1). Additionally, the II and AI scores of the GATA TFs in cassava were found to range from 36.11 (MeGATA30) to 69.15 (MeGATA05) and from 39.68 (MeGATA06) to 74.52 (MeGATA01), respectively (Table 1). The GRAVY value of the GATA TFs in cassava was minus, ranging from -0.49 (MeGATA11) to -1.06 (MeGATA07) (Table 1).

Previously, the general characteristics of the GATA TFs were also comprehensively analyzed in other higher plant species. Zhang et al. (2015) revealed that the amino acid residues of the GmGATA proteins in soybean were 80 and the largest was 551, and their masses ranged from 9.1 to 60.8 kDa. The pI values of the GmGATA proteins in soybean varied from 4.63 to 9.66 (Zhang et al., 2015). In grapes, the VvGATA proteins were reported to range from 109 to 386 amino acid residues in size (Zhang et al., 2018). Additionally, the protein sizes of the CaGATA proteins in chickpea were between 133 (14.9 kDa) and 541 amino acid residues (60.2 kDa), and 22 out of 25 CaGATA proteins in chickpea were unstable (II scores were greater than 40) (Niu et al., 2020). The pI scores of the CaGATA proteins in chickpea were varied from 4.27 to 10.27, while the GRAVY scores of all CaGATA proteins in chickpea were less than 0 (Niu et al., 2020). More recently, the length and molecular weight of the StGATA proteins ranged from 118 to 380 amino acid residues and from 13.15 to 60.63 kDa, respectively, while their pI values were found to be great differences (from 4.53 to 10.34) (Yu et al., 2022). Taken together, this study strongly suggested that the GATA TFs in cassava, perhaps in higher plant species exhibited high variation in their general characteristics.

As a part of this study, the subcellular localization of the MeGATA proteins was continued to analyze by using the bioinformatics tool (Briesemeister et al., 2010) as previously reported (La et al., 2022). The prediction of the subcellular localization indicated that most members of the GATA TFs in cassava, specifically 18 and 17 CaGATA proteins were positioned in the cytoplasm and nucleus, respectively, while only MeGATA11 was reported to localize in the Golgi apparatus (Table 1). This finding was also confirmed by a previous study on potato (Yu et al., 2022). Particularly, 28 and 10 (out of 49) members of StGATA proteins were reported to localize in the nucleus and cytoplasm, respectively (Yu et al., 2022).

Classification and structural analysis of the GATA TFs in cassava: The obtained Neighbor-Joining phylogenetic tree showed that the GATA TFs in cassava were clearly divided into three distinct groups, as well-described in Figure 2. Particularly, group 1 comprised three members of the GATA TFs in cassava, namely MeGATA03, 04, and 21, while 10 and 23 members of the GATA TFs in cassava were categorized into groups 2 and 3, respectively (Figure 2).

Previously, a similar phenomenon was also reported for the GATA TFs in other higher plant species. For example, 25 CaGATA proteins in chickpea could be clearly divided into three groups, including group A (17 members), B (five members), and C (three members) (Niu et al., 2020). Moreover, the StGATA proteins in potato were reported to classify into three clades, in which clades 1 and 2 contained three and 13 members, respectively and clade 3 (33 members) contained three subgroups (Yu et al., 2022). The classification into three clades was also observed in other higher plant species, such as A. thaliana (Teakle et al., 2002), rice (Reyes et al., 2004), soybean (Zhang et al., 2015), apple (Chen et al., 2017) and grape (Zhang et al., 2018).

Next, a structural analysis of genes of the GATA TFs was performed as previously reported (Niu et al., 2020). The CDS lengths of the MeGATA genes were varied from 321 (MeGATA21) to 6897 bp (MeGATA03), while the gDNA lengths of the MeGATA genes ranged from 1249 (MeGATA21) to 14641 bp (MeGATA04) (Figure 2). The amounts of exons of the MeGATA genes were reported to be variable, consisting of two to 10 (Figure 2). Particularly, 16 and 10 MeGATA genes contained two and three exons, respectively, while five and three MeGATA genes consisted of seven and 10 exons (Figure 2). Additionally, only MeGATA30 and 03 were reported to harbor four and eight exons (Figure 2). Previously, a large number of genes encoding GATA TFs in other plant species was also indicated to contain two or three exons. Eleven and six (out of 25) CaGATA genes in chickpea consisted of two and three exons, respectively (Niu et al., 2020), while 25 (out of 49) StGATA genes in potato had two and three exons (Yu et al., 2022).

Expression profiles of the MeGATA genes in different tissues during the growth and development: In this study, the FPKM values of the MeGATA genes were re-analyzed and constructed a heatmap of the hierarchical clustering to display the expression patterns of the MeGATA genes (Figure 3).

This study revealed that the expression of four MeGATA genes, including MeGATA08, 09, 19 and 30 was not expressed or low (FPKM values < 10) in any of 11 major organs/tissues, while the remaining MeGATA genes (32 out of 36) were expressed (FPKM values ≥ 10) in at least one major organ/tissue (Figure 3). Among them, MeGATA24 and 13 were noted to be mainly expressed (FPKM values ≥ 100) in lateral bud and stem, respectively, while four MeGATA genes, MeGATA10, 11, 32, and 34 exhibited high transcript abundance in leaf (Figure 3). Interestingly, the expression levels of MeGATA24 gene tend to be high not only in the petiole and SAM but also in the storage root (Figure 3). This re-analysis suggested that these MeGATA genes might play key roles in the tissue development of cassava plants.

Expression analysis of the MeGATA genes responding to various stress conditions: To assess the transcript levels of the MeGATA genes in major organs/tissues under adverse environmental conditions, the heatmap of the MeGATA gene’s expression was constructed and provided in Figure 4.

Under drought conditions (Zhu et al., 2020), the expression of 13 and nine MeGATA genes was induced and reduced in treated leaf samples (Figure 4). Among them, four genes, namely MeGATA08, 10, 18, and 23 were highly up-regulated, by 240.75-, 324.13-, 60.31-, and 67.74-fold in drought-treated leaf samples, respectively, whereas MeGATA33 was noted to be highly down-regulated (-19.45-fold) in treated leaves (Figure 4). Under PEG 6000 treatment (Ding et al., 2017), the expression of 16 MeGATA genes was significantly changed in at least one major organ/tissue (Figure 4). For example, one and 11 MeGATA genes, including MeGATA36, and MeGATA03, 13, 16, 20, 23, 24, 25, 27, 28, 29, and 33 were obviously up-regulated and down-regulated in these tested tissues under the PEG 6000 treatment (Figure 4). Interestingly, MeGATA03 and 20 were reduced in three tissues, including the bottom leaf, root, and folded leaf or and fully expanded leaf under the PEG 6000 treatment, respectively, while three genes, namely MeGATA24, 25, and 28 were down-regulated in two treated tissues, particularly bottom leaf and folded leaf, root and fully expanded leaf, and bottom leaf and root samples, respectively (Figure 4). These findings suggested that these MeGATA genes might play an important role in the response to drought or osmotic stresses in cassava.

Furthermore, global cassava production has been critically restricted by CBSD (Tomlinson et al., 2018). One transcriptome atlas of cassava leaf samples after artificial inoculation with CBSD was also explored (Maruthi et al., 2014). The results indicated that five MeGATA genes, namely MeGATA10, 20, 25, 27, and 33 were down-regulated in treated leaf samples (Figure 5). This study suggested that these five genes might be related to the response to CBSD infection in cassava.

Previously, the GATA TFs have been reported to participate in the response to adverse environmental conditions in plants. For example, OsGATA16 gene was up-regulated by cold and abscisic treatments but was down-regulated by drought, jasmonic acid, and cytokinin (Zhang et al., 2021). Overexpression of this gene could confer cold tolerance of rice during the seedling period (Zhang et al., 2021). In tomato, overexpression of the SlGATA17, a drought-inducible gene could regulate drought resistance by improving the activity of the phenylpropanoid biosynthesis pathway in transgenic plants (Zhao et al., 2021). Overexpression of BdGATA13, a member belonging to the GATA TFs in model grass Brachpodium distachyon could enhance drought tolerance by resulting in darker green leaves and later flowering in transgenic Arabidopsis plants (Guo et al., 2021). Taken together, the results clearly indicated the function of GATA TFs in plant growth and development processes, especially in the response to adverse environmental stresses.

Conclusions: The present study reported a genome-wide survey and analysis of the MeGATA TF family in cassava, a multi-functional crop in the world. The protein features, gene structures, duplication events, phylogenetic relationship, subcellular localization, and expression profiles of the MeGATA TFs in cassava have been assessed by using bioinformatics tools. These results showed the structural variations in the characteristics of the MeGATA TFs in cassava. By re-analyzing the previous transcriptome databases, the MeGATA genes exhibited differential expression patterns in major organs/tissues in various conditions, more specifically abiotic and biotic stresses. This study could provide a list of potential stress-inducible MeGATA genes for further functional characterization.

Authors Contribution: Conceptualization: H.D.C. and P.B.C., Data collection: T.V.T., V.H.L., N.Q.T., P.C.T., B.T.T.H., L.V.N., D.H.G., Q.T.N.L., H.T.T. T., Guidance of data analysis: P.B.C., D.H.C., T.V.T., V.H.L. Manuscript writing: P.B.C, D.H.C, T.V.T, V.H.L. All authors discussed the results and contributed to the final manuscript.

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