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Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods



Phi Bang Cao, Ha Duc Chu, Sahar Azar, Viet Hong La, Thi Thanh Huyen Tran, Xuan Duong Vu, Thi Man Le, Linh Hung Le and Thao Duc Le
 
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ABSTRACT

Background and Objective: In plants, the aldehyde dehydrogenases (ALDHs) have been regarded as the key enzymes involving in numerous growth and developmental processes. This study aimed to identify and analyze ALDH gene family in genome of Eucalyptus grandis, an important woody tree. Materials and Methods: The ALDH family members in the E. grandis genome were identified by a basic local alignment search tool (BLASTP) against the E. grandis proteome database using known Arabidopsis and Vitis ALDHs as queries. Sequences were analyzed by various bioinformatics tools. Results: In this study, a total of 32 members of EgrALDH gene superfamily were identified in E. grandis and their characteristics, including chromosomal distribution, subcellular localization, protein features, gene structure and phylogenetic tree were subsequently analyzed. It has been predicted that the segmental and tandem duplication events (20 out of 21 duplicated pairs) might be the major mechanism of the expansion of EgrALDH genes. The EgrALDH genes have differentially expressed in young leaves, mature leaves, shoot tips, phloem, immature xylem and xylem. Conclusion: Results from this work showed the characteristics, evolutionary and expression analysis of ALDH gene superfamily of this important woody plant. This study provided a comprehensive understanding of the EgrALDH gene superfamily in E. grandis as well as proposed a list of candidate genes for further functional characterization.

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Phi Bang Cao, Ha Duc Chu, Sahar Azar, Viet Hong La, Thi Thanh Huyen Tran, Xuan Duong Vu, Thi Man Le, Linh Hung Le and Thao Duc Le, 2021. Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods. Asian Journal of Plant Sciences, 20: 210-219.

DOI: 10.3923/ajps.2021.210.219

URL: https://scialert.net/abstract/?doi=ajps.2021.210.219
 
Received: September 23, 2020; Accepted: December 05, 2020; Published: March 15, 2021


Copyright: © 2021. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

INTRODUCTION

Being sessile, plants cannot escape when exposed to adverse environmental stresses, such as drought, high salinity and low temperatures. Under these stress conditions, high accumulation of the reactive oxygen species (ROS) can lead to oxidative stress and cell damage1. Seriously, oxidative stress is coupled to the oxidative degradation of lipid membranes, which could generate a number of aldehydes2. These excessive accumulations of aldehydes caused by the oxidative stress was reported to interfere with metabolites and become toxic3. To cope with cellular damage of aldehydes, aldehyde dehydrogenases (ALDH) have been fully reported as late responsive protective proteins that play an important role in the metabolism of endogenous and exogenous aldehydes and thereby mitigate oxidative stress in plants4,5. The expression of the ALDH genes in plants in response to various environmental stresses, including high salinity, dehydration, heat, water logging, oxidative stress or heavy metals has proved their important role in environmental adaptation5,6. Moreover, the ectopic overexpression of ALDH genes has shown to enhance the plant tolerance to both biotic and abiotic stresses7.

Systematically, ALDHs were found throughout all taxa, in both prokaryotes and eukaryotes and have been classified into 24 distinct families based on protein sequence identities6,8. It is demonstrated that 13 ALDH families (out of 24) have been well-characterized in plants9. Among them, six groups are noted to be specific to plants, whereas seven families have mammalian orthologues10,11. The ALDH gene families from several plant species have been studied, including Arabidopsis thaliana12, algae (Chlamydomonas reinhardtii and Ostreococcus tauri)13, moss (Physcomitrella patens)13, rice (Oryza sativa)14, maize (Zea mays)15, soybean (Glycine max)16, grape (Vitis vinifera)17, apple (Malus domestica)18, Gossypium spp.19, poplar (Populus trichocarpa)20, tomato (Solanum lycopersicum)21 and Brassica rapa22. However, no information of the ALDH gene family has been reported in the Eucalyptus grandis, one of the most widely planted hardwoods crops in the world23,24, even the assembled E. grandis genome was recently released25.

The current study systematically identified 32 ALDH genes from E. grandis belonging to ten different families. More specifically, phylogeny, structures, localizations, exon-intron structure, duplications and expression patterns were comprehensively analyzed. This study along with the comparative analysis of ALDH members between the eudicot model plant A. thaliana, the monocot species O. sativa and the four woody plants (Eucalyptus, Populus, Malus and Vitis) could be extremely useful in future evolutionary studies on the E. grandis ALDH family.

MATERIALS AND METHODS

Study area: Study was conducted during October, 2018-2019. The in silico analyses were carried out at Hung Vuong University (Phu Tho, Vietnam), Agricultural Genetics Institute (Ha Noi, Vietnam), Lebanese University (Baabda, Lebanon), Hanoi Pedagogical University 2, (Vinh Phuc, Vietnam) and Hanoi National University of Education (Ha Noi, Vietnam).

Identification of ALDH in Eucalyptus grandis genome: A basic local alignment search tool (BlastP) was performed against the E. grandis proteome database (BioProject: PRJNA49047)25 available in the Phytozome26 using previously identified Arabidopsis12 and V. vinifera ALDH proteins17 as queries. All output putative EgrALDH were verified using the Pfam server27 to validate the presence of the ALDH family domain (PF00171). Then, the selected genes were used for a second TBLASTN round on the Eucalyptus genome25 in the phytozome, this additional step permitted to identify the paralog that had been excluded by their dissimilarity to the Arabidopsis and Vitis orthologs or not annotated. The identified Eucalyptus ALDH proteins were annotated using the criteria established by the ALDH Gene Nomenclature Committee10.

Sequence analysis and Subcellular localization: The predicted protein sequences were analyzed to obtain the number of amino acids (aa-s), molecular weight (kDa) and theoretical isoelectric point (pI) by using ExPASY Protparam28. Subcellular localization prediction was performed based on the identification of signal peptide sequences by Yloc29,30 and ProtComp from Soft berry server (www.softberry.com/berry. phtml).

Exon-intron structure analysis and chromosomal localization: The chromosomal distribution, coding DNA sequence (CDS) and genome DNA region (gDNA) of putative EgrALDH genes were retrieved from the Eucalyptus genome database25. Graphical presentation of gene localization was performed using MapChart V2.131 based on their chromosomal position and the relative distance between these genes on the same chromosome. Exon-intron organization were generated by submitting the CDSs and their corresponding gDNAs to the GSDS V2.0 (Gene Structure Display Server)32.

Phylogenetic and gene evolution analysis: The deduced full-length amino acid sequences of ALDH members from E. grandis, A. thaliana12, V. vinifera17, P. trichocarpa20, M. domestica18 and O. sativa14 were aligned by MAFFT program33. The phylogenetic tree was constructed by MEGA7 software34 with the bootstrap test replicated 1000 times and a JTT model. The ALDH gene duplication was defined according to the previous report35.

Expression analysis of the ALDH genes: The previous transcriptome data36 available in the Phytozome server26 was used to explore the expression profiles of the ALDH genes in various organs/tissues. Briefly, six tissues/organs, including immature xylem (outer glutinous 1-2 mm layer comprising developing xylem cell layers), xylem, phloem (1-2 mm layer from the inner surface of the bark), shoot tips (soft green termini of young crown tip branches containing apical meristems, shoots and a small section of soft green stem below the shoot primordia and the first one or two unfolded leaves), young leaves (three to four soft, rapidly expanding leaves) and mature leaves (older, fully expanded leaves) were separately collected from 5 year old E. grandis trees in a clonal field trial for an Illumina sequencer36. The data was re-analyzed and illustrated by the R script.

RESULTS AND DISCUSSION

Genome-wide identification of ALDH gene families in the E. grandis genome: To identify the EgrALDH gene family in E. grandis, a comprehensive search of the conserved ALDH domain (PF00171) against the assembly of E. grandis has been conducted. Briefly, the members of EgrALDH gene family in E. grandis genome were identified by a series of Blast searches using ALDH proteins of A. thaliana as query sequences. The second round of TBLASTN has performed against E. grandis genome using Eucalyptus proteins to detect all paralogs. Based on their protein sequence identities and phylogenetic relationships with Arabidopsis ALDHs, a total of 32 full-length EgrALDH proteins were identified in E. grandis. The general information of the EgrALDH families was fully described in Table 1.

Table 1:Summary of EgrALDH families in Eucalyptus grandis
Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Chr: Chromosome, C: Cytoplasm, ER: Endoreticulum, G: Golgi apparatus, M: Mitochondrion, Px: Peroxisome, PL: Peptide length, SCL: Subcellular localization

Domain analysis using Pfam allowed to validate all of the 32 candidate sequences encoding members of 10 of the 24 ALDH families, including EgrALDH2, 3, 5, 6, 7, 10, 11, 12, 18 and 22 (Table 1), which were also previously confirmed in other plant species10,11,17,19,21,37,38. Interestingly, it found that EgrALDH2 and 3 families formed two largest groups in E. grandis, with 12 and nine members, respectively (Table 1). By contrast, six of the 10 EgrALDH families are represented by only a single gene, including EgrALDH5, 7, 10, 12, 18 and 22, while the remaining two families, EgrALDH6 and 11 are constituted by two and three genes, respectively (Table 1).

This study also showed that E. grandis ALDH superfamily is the second most expanded gene superfamily (32 members), as compared to identified ALDH superfamily in other plant species. More specifically, a total of 39 members have been recorded in M. domestica18, while 30, 29, 26 and 25 ALDH genes have been found in Gossypium spp.19, S. lycopersicum21, P. trichocarpa20 and V. vinifera17, respectively. Additionally, 24 members have been identified in the ALDH gene family of both Z. mays15 and Selaginella moellindorffii10. Previously, 21, 20, 16 ALDH genes were also recorded in P. patens, O. sativa14 and A. thaliana10,11, respectively, while only nine and six ALDH genes were found in C. reinhardtii and O. tauri13, respectively. Interestingly, the study found that only one gene was recorded in ALDH12 and 22 families of all identified plant species, such as cotton19, A. thaliana10,11, P. patens and O. sativa14. Taken together, current findings strongly suggested that the members in the ALDH superfamily in plant species are highly variable and the expansion of these gene families could be explained by their function in detoxifying generated aldehydes9,39.

Characterization and subcellular localization of EgrALDH proteins: Next, various general features of EgrALDH proteins were also analyzed based on the ExPASY Protparam tool28. These encoded EgrALDH proteins ranged from 399-732 aa-s in length, relevant the molecular weight from 44.38-79.26 kDa (Table 1). The pI values of EgrALDH proteins were varied from acidic (5.38) to base (9.06) (Table 1). Among all, EgrALDH18B1 is noted as the largest protein of ALDH family, exhibiting a molecular weight of 79.26 kDa with 732 aa-s (Table 1). In the previous studies, the features of ALDH proteins in plant species have been also characterized and discussed. Specifically, the molecular mass of Gora ALDH in G. raimondii was varied from 479 (GoraALDH3F1) to 1023 aa-s (GoraALDH6B3)19.

The genomic full-length of ALDHs identified in E. grandis varies from 2647-9162 nucleotides. As the divergence of exon-intron structure often plays an important role in the evolution of gene families, the exon-intron structures of all 32 EgrALDH genes were also analyzed (Fig. 1). The results showed that genes in the same family generally displayed similar exon-intron structures with some exceptions that the gain or loss of one or more than one exons happens in particular members in each case. The members of ALDH2 family divided into two groups, five exhibits 11 exons and seven reveal nine exons. The genes of ALDH3 family contain 10 exons except for EgrALDH3F4 which includes only nine exons. Both EgrALDH6B1 and EgrALDH6B2 have 19 exons. In the ALDH11 family, two genes EgrALDH11A2 and EgrALDH11A3 contain nine exons while only eight exons are predicted in EgrALDH11A1. For single gene families, 20 exons are found in EgrALDH5F1 and EgrALDH18B1, 14 in EgrALDH7B4 and EgrALDH22A1, 15 in EgrALDH10A9 and 16 in EgrALDH12A1.

Furthermore, the cellular localization of the EgrALDH proteins was investigated by retrieving their full-length aa sequences against the Yloc29,30 and ProtComp from Softberry server. As a result, all EgrALDH proteins were distributed in various organelles. More specifically, a majority of EgrALDH proteins was localized in the cytoplasm (14), mitochondrion (eight) and peroxisome (eight), while a small amount of EgrALDH proteins was distributed on Golgi apparatus (one) and ER (one). Taken together, the highly variable structure of EgrALDHs in E. grandis may suggest their potentially different functional roles in different biological processes or under different growth conditions.

Chromosomal localization, phylogeny and duplication analysis of E. grandis ALDH gene families: Chromosomal localizations of ALDH members indicate that the 32 E. grandis genes are unequally distributed on eight chromosomes out of the E. grandis eleven chromosomes (Fig. 2). More specifically, chromosome 3 had the largest number of ten EgrALDHs followed by chromosome 2 with seven EgrALDHs. Only one single EgrALDH gene found on each of chromosomes 7 and 11 (Fig. 2). Chromosome 6 and chromosome 10 had every three EgrALDHs, while chromosome 8 and 9 had 2 and 5 EgrALDH genes, respectively (Fig. 2).

The Neighbor-Joining tree was generated using the full-length protein sequences of 32 EgrALDHs, 25 VvALDHs, 26 PtALDHs, 39 MdALDHs, 16 AtALDHs and 21 OsALDHs in E. grandis, V. vinifera, P. trichocarpa, M. domestica, A. thaliana and O. sativa, respectively. Bootstrap values were indicated at each branch.

Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Fig. 1:Exon-intron structure of E. grandis ALDH genes

Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Fig. 2:Chromosomal distribution of ALDH and duplication regions in E. grandis genome

Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Fig. 3:Phylogenetic tree of ALDH proteins in plant species

A phylogenetic tree has been conducted using the all identified full-length ALDH proteins in E. grandis, A. thaliana12, O. sativa 14, P. trichocarpa20, V. vinifera17 and M. domestica18 to study the evolutionary relationships (Fig. 3). The unrooted tree clearly showed the relatedness of E. grandis ALDH proteins with their counterparts in all the five other compared species. Phylogenetic analysis indicates that E. grandis ALDHs exist in 10 families that are clustered in four clades with confidence bootstrap value (>50). The clade 1 comprises two families, ALDH2 and 10 and the clade 2 comprises two families, ALDH5 and 7 (Fig. 3). Next, the clade 3 contains ALDH6 and 12, while four remaining ALDH groups, including ALDH3, 11, 18 and 22 are categorized in the clade 4 (Fig. 3). The topology was similar to that constructed with ALDH genes from the other plant species (Fig. 3). As expected, the homologous genes of different species cluster together in one branch (Fig. 3). Inconsistency with previous results found in rice and in poplar, ALDH18 was the most distantly related family in the phylogeny indicating that these proteins had the greatest degree of sequence divergence with proteins in other ALDH families and did not contain the conserved ALDH active sites.

In E. grandis, families 2, 3, 5, 6, 7, 10, 12, 18 and 22 make up 37.50 (12 out of 32), 28.13 (9 out of 32), 3.13 (1 out of 32), 6.25 (2 out of 32), 3.13 (1 out of 32), 3.13 (1 out of 32), 9.38 (3 out of 32), 3.13 (1 out of 32), 3.13 (1 out of 32) and 3.13% (1 out of 32) of the total number of members of the ALDH superfamily, respectively (Fig. 4).

Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Fig. 4:
Distribution of ALDH genes from S. italica, Z. mays, O. sativa, P. trichocarpa, M. domestica, V. vinifera, A. thaliana and E. grandis

Particularly, the ALDH2 group (12 out of 32, 37.50% of ALDH superfamily) was more prominent in Eucalyptus as compared to the other plant species, such as S. italica (6 out of 20, 30.00% of ALDH superfamily), Z. mays (6 out of 24, 25.00% of ALDH superfamily), O. sativa (5 out of 21, 23.81% of ALDH superfamily)14, P. trichocarpa (4 out of 26, 15.38% of ALDH superfamily)20, M. domestica (13 out of 39, 33.33% of ALDH superfamily)18, V. vinifera (5 out of 25, 20.00% of ALDH superfamily)17 and A. thaliana (3 out of 16, 18.75% of ALDH superfamily)12 (Fig. 4). Similarly, the ALDH3 group in E. grandis (9 out of 32, 28.13% of the ALDH superfamily) constituted a higher proportion of ALDH superfamily than ALDH3 group in other plant species did, such as S. italica (4 out of 20, 20.00% of ALDH superfamily), Z. mays (5 out of 24, 20.83% of ALDH superfamily), O. sativa (5 out of 21, 23.81% of ALDH superfamily)14, P. trichocarpa (6 out of 26, 23.08% of ALDH superfamily)20, M. domestica (7 out of 39, 17.95% of ALDH superfamily)18, V. vinifera (4 out of 25, 16.00% of ALDH superfamily)17 and A. thaliana (3 out of 16, 18.75% of ALDH superfamily)12 (Fig. 4).

Gene duplication events were considered to play an important role in the amplification of gene families. To investigate the expansion of EgrALDH superfamily in E. grandis genome, gene duplication analysis was performed. A total of 21 duplicated gene pairs were detected (Table 2). Only one Whole Genome Duplication (WGD) was found to be present only in EgrALDH2B1 and EgrALDH2B5 gene whereas 20 remaining duplicated gene pairs belong to Tandem (TD) and Segmental Duplication (SD). These duplication events occurred in three groups, including EgrALDH2, 3 and 6 have been predicted. Both segmental and tandem duplications explain the expansion of genes families in Eucalyptus23. In this study, the ALDH2 and ALDH3 families were expanded due to three duplication types, including WGD, SG and TD. These results are in agreement with the expansion of ALDH superfamily in grape17, poplar20, Chinese cabbage22.

There were probably three alternative outcomes in the evolution of duplicate genes, including non-functionalization, neofunctionalization and sub-functionalization40. To examine the selective pressures on duplicated EgrALDH gene pairs, the Ka/Ks ratio for each pair of duplicated genes was calculated using the coding sequences. In the present study, 14 pairs of duplicated ALDH2 with a Ka/Ks ratio >1 were found, which suggested that they had experienced positive selection. However, there were six pairs of duplicated ALDH3 and one pair of duplicated ALDH11 with a Ka/Ks ratio <1 suggesting that these genes had experienced purifying selection pressure with limited functional divergence after duplications. These results showed that duplication events have played an important role in the evolution of the ALDH gene family in E. grandis. Tian et al.20 reported that Ka/Ks ratios of all 10 PtALDH gene pairs were less than 1, suggesting that poplar ALDH gene pairs have evolved mainly under the influence of purifying selection.

Expression profiles of the EgrALDH genes in various tissues: Data was obtained from the previous transcriptome atlas and illustrated by R script. The expression pattern of a gene <10 FPKM (fragments per kilobase of transcript per million reads mapped) values = below the limit of detection, >20 FPKM values = detected expression, >50 FPKM values = highly expressed gene, >100 FPKM values = exclusively expressed gene.

Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
Fig. 5:
Heatmap of EgrALDH gene expression patterns in various tissues/organs during the growth and development of the E. grandis plants

Table 2:Ka/Ks analysis for the duplicated ALDH gene pairs from Eucalyptus grandis
Image for - Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods
TD: Tandem duplication, SD: Segmental duplication, WGD: Whole genome duplication

To explore the expression patterns of the EgrALDH genes in various organs/tissues, the previous transcriptome was used to re-analyzed36. Briefly, lllumina RNA-sequencing provided transcriptome data from six tissues, including immature xylem, xylem, phloem, shoot tips, young and mature leaves harvested from E. grandis trees in a clonal field trial36. According to Fig. 5, the EgrALDH genes have differentially expressed in the examined tissues. Three genes, including EgrALDH3F4, 2B5 and 11A3, were exclusively expressed in at least one major organ/tissue. More specifically, EgrALDH3F4 was found to strongly induce in the mature leaf, while EgrALDH2B5 and 11A3 were noted to exclusively express in immature xylem and xylem, young and mature leaves, respectively. EgrALDH10A9 gene was found to highly express in shoot tips, phloem and immature xylem, while EgrALDH7B4 was induced in mature leaf. However, the expression of several genes, including EgrALDH2B4, 2C2, 2C3, 2C4, 2C6, 2C7, 3F1, 3F5, 3F6 and 3F7 were under of detection. Taken together, re-analysis of the previous transcriptome atlas indicated diverse functions for the EgrALDH genes in the regulation of growth and development of various tissues/organs of E. grandis plants.

CONCLUSION

In this present study, a total of 32 EgrALDH genes, particularly 12 EgrALDH2s, nine EgrALDH3s, one EgrALDH5, two EgrALDH6s, one EgrALDH7, one EgrALDH10, three EgrALDH11s, one EgrALDH12, one EgrALDH18 and one EgrALDH22 was identified in the E. grandis genome and their general features were provided. Using various in silico analysis, this study provided the first sight into the understanding of the EgrALDH superfamily, including the protein characteristics, exon/intron organization, gene location, phylogenetic tree. This study demonstrated that the duplication events, including segmental and tandem duplication, might play the main roles in the EgrALDH genes. To sum up, this study has provided a solid foundation of the EgrALDH gene superfamily in E. grandis for further functional characterization.

SIGNIFICANCE STATEMENT

This study firstly showed the characteristics, evolutionary and expression analysis of ALDH gene superfamily of E. grandis. Results layed the foundation for future researches of functionality, particularly those involving ALDH members of this important woody species.

ACKNOWLEDGMENT

This study was funded by the fundamental research program of Hung Vuong University.

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