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Article

Genome-Wide Identification and Analysis of U-Box E3 Ubiquitin-Protein Ligase Gene Family in Banana

by
Huigang Hu
,
Chen Dong
,
Dequan Sun
,
Yulin Hu
and
Jianghui Xie
*
Key Laboratory of Tropical Fruit Biology, Ministry of Agriculture, South Subtropical Crop Research Institute, Chinese Academy of Tropical Agricultural Science, Zhanjiang 524091, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2018, 19(12), 3874; https://doi.org/10.3390/ijms19123874
Submission received: 18 October 2018 / Revised: 29 November 2018 / Accepted: 1 December 2018 / Published: 4 December 2018
(This article belongs to the Section Molecular Genetics and Genomics)
Browse Figures
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Abstract

:
The U-box gene family is a family of genes which encode U-box domain-containing proteins. However, little is known about U-box genes in banana (Musa acuminata). In this study, 91 U-box genes were identified in banana based on its genome sequence. The banana U-box genes were distributed across all 12 chromosomes at different densities. Phylogenetic analysis of U-box genes from banana, Arabidopsis, and rice suggested that they can be clustered into seven subgroups (I–VII), and most U-box genes had a closer relationship between banana and rice relative to Arabidopsis. Typical U-box domains were found in all identified MaU-box genes through the analysis of conserved motifs. Four conserved domains were found in major banana U-box proteins. The MaU-box gene family had the highest expression in the roots at the initial fruit developmental stage. The MaU-box genes exhibited stronger response to drought than to salt and low temperatures. To the best of our knowledge, this report is the first to perform genome-wide identification and analysis of the U-box gene family in banana, and the results should provide valuable information for better understanding of the function of U-box in banana.

1. Introduction

The ubiquitin/26S proteasome (UPS) pathway degrades ubiquitinated substrate proteins and is extensively involved in various cellular processes [1]. The diverse aspects of plant growth and development and the degradation of short-lived regulatory proteins can be regulated by the UPS [2,3,4]. E1 Ub-activating enzyme, E2 Ub-conjugating enzyme, and E3 Ub ligase are necessary for ubiquitin activation and transfer [5]. First, E1 activates the ubiquitin molecule in an ATP-dependent manner, and then E2 facilitates the attachment of ubiquitin molecule to the target protein in the presence of E3 [6]. E3 ligase plays an important role in protein ubiquitination because E3 can identify target proteins for modification [7]. A single protein or a protein complex joins the ubiquitin reaction, which could be conferred by E3 ligase [8,9]. Ubiquitin E3 ligases facilitate the covalent attachment of ubiquitin to target proteins in eukaryotes [10]. HECT, RING finger, and U-box domain proteins are three types of single-protein E3 ligases [11]. U-box proteins are found in yeast, plants, and animals [12,13,14,15]. The U-box domain is composed of approximately 75 amino acids (aa) [16,17]. Many U-box proteins had function of E3 ligases [18,19]. The genome of Arabidopsis thaliana has more than 60 U-box genes, which have many functions in plants [16]. A previous study has identified the functions of U-box E3 ligases in parsley, tomato, tobacco, and rice [20]. OsU-box gene 51 negatively regulates cell death signaling according to cell death assay [17]. The U-box E3 ligase NtACRE276 of tobacco may play a role in Cf9/Avr9-elicited defense [21]. On the basis of protein domains, eight groups of Plant U-box (PUB) genes are present in the 125 PUB genes of soybean [22]. The flowering condition could be changed in GmPUB8-overexpressing Arabidopsis, which flowered earlier under middle- and short-day conditions but later under long-day conditions [22]. Inactivation of the Arabidopsis PUB13 also results in spontaneous cell death, enhanced levels of the defence hormone SA, and early flowering [23]. In grapevine, the PUB gene significantly regulates the accumulation of resistance proteins under both biotic and abiotic stresses [20].
Banana (Musa spp.) is one of the world’s most important fruits [24,25]. The sequencing of the whole genome of banana (Musa acuminata) provides a good platform for the development of banana molecular biology [26]. Until now, the U-box gene family of banana is rarely studied. U-box genes may play important roles in the growth and development of banana, so investigating the E3 gene family in banana is necessary. In this study, the whole genome of the banana U-box gene was determined and analyzed. The conserved domain structure, subgroup classification, evolutionary relationship, intron and exon structure, gene expansion, chromosome mapping, and expression profile analysis were studied, providing a theoretical basis for the analysis of U-box gene functions.

2. Results

2.1. Identification and Chromosomal Localization of U-Box Gene Family Members

In this study, 91 PUB genes are found in banana genome (Table 1). The MaU-box protein contains a 60–70 aa U-box conserved domain. The length of MaU-box was from 660 (MaU-box69) to 6279 bp (MaU-box57), and the average length was 1789 bp. The predicted protein product range was 219–2092 aa, with an average length of 595 aa. The relative molecular weight (MW) ranged from 23.38 kD to 223.93 kD, with an average of 64.85. The isoelectric point (PI) was in the range of 4.96 (MaU-box78) to 9.57 (MaU-box13). Subcellular localization analysis indicated that 93% of the MaU-box proteins were located in the nucleus and that only six were located in the cytoplasm (Table 1). These findings suggested that the vast majority of MaU-box function in the nucleus.
A MaU-box chromosomal localization map was plotted (Figure 1). Ninety genes from 91 MaU-box genes were located on chromosomes. Chromosome 3, where the largest number of MaU-box genes was found, contained 11 MaU-box genes. It is followed by chromosomes 4, 5, and 11, which contained 10 MaU-box genes. Nine MaU-box genes were located in chromosomes 7, 9, and 10; 7 MaU-box genes were found in chromosome 8; 6 MaU-box genes were observed in chromosome 1; 5 MaU-box genes were localized in chromosome 2; and only 4 MaU-box genes were detected in chromosome 11.

2.2. Gene Structure and Phylogenetic Analysis of U-Box Gene Family Members

By comparing the full-length cDNA sequence with the corresponding genomic DNA sequence, the exon–intron structure of each MaU-box was determined. The number of exons in MaU-box genes ranged from 1 to 18 (Figure 2).
To study the evolutionary relationship of banana U-box proteins, a neighbor-joining (NJ) tree was constructed with U-box proteins from banana, rice, and Arabidopsis (Figure 3). The aa sequences of the U-box of 91 proteins from banana, 61 from Arabidopsis, and 77 from rice were used. Phylogenetic analysis showed that all identified U-box proteins from banana together with Arabidopsis and rice were clearly divided into seven subgroups. Subgroups I, II, III, IV, V, VI, and VII contain 8, 2, 10, 8, 26, 32, and 5 gene family members, respectively. In general, the U-box from banana had a closer relationship with rice compared with Arabidopsis. Interestingly, these MaU-box genes with similar genetic structures are clustered together. For example, MaU-box51/65/84/91 of subgroup I each contain 11 exons, MaU-box66/87 of subgroup II each contain 18 exons, and MaU-box4/19/20/39/45/54 of subgroup III each contain 1 exon.

2.3. Analysis of MaU-Box Gene Family Conserved Motifs

To investigate the structural diversity and predict the function of MaU-box proteins, 20 conserved motifs in banana U-box were identified using the MEME motif search tool and annotated using SMART tools (Figure 4 and Figure 5). Among the 91 U-box genes, 45 (50%) contained U-box conservative motifs without ARM motifs, 22 (24%) contained ARM conservative motifs without U-box motifs, while 24 (26%) contained both U-box conserved motifs and ARM conserved motifs (Figure 6). Motifs 1 and 2 are U-box conservative motifs; motifs 5, 8, 10, 13, 16, and 18 are ARM conservative motifs; motifs 9 and 14 are Pkinase-Tyr motifs; and motif 6 is an STYKc motif. Motifs 3, 4, 7, 11, 12, 15, 17, 19, and 20 are unknown. The features of 20 motifs are shown in Figure 5.

2.4. Expression Profile of MaU-Box Genes in Different Organs

Figure 7 shows that among the 91 MaU-box genes, 88 were at least expressed in one tissue, occupying 97% of all gene numbers. Moreover, among the 88 genes, 76 were expressed in all tissues. The Mau-box gene family was differentially expressed in various tissues. This gene family had the highest expression in the roots, where 48 genes exhibited the highest expression. By contrast, the lowest expression was observed in the male flowers, where 17 genes (MaU-box8/9/13/16/17/19/21/28/30/32/35/37/38/46/50/56/89) exhibited the lowest expression.

2.5. Expression Profile of MaU-Box Genes in Fruit Developmental Period

Figure 8 illustrates that 62 MaU-box genes were at least expressed during one developmental phase, 59 of which were expressed in all developmental phases. The MaU-box gene family was also differentially expressed at various developmental phases of banana. The gene family had the highest expression at the beginning of banana’s development phase (day 25), during which 29 genes (MaU-box3/4/8/9/10/13/17/18/19/20/22/25/27/28/34/38/39/41/43/48/49/50/51/52/56/59/61/63/70) had the highest expression. High MaU-box gene expression was also observed during banana fructescence (day 88), which was second only to the expression on day 25. During the maturity phase of fructescence, 21 genes (MaU-box5/7/12/13/16/21/33/42/47/55/57/65/66/67/69/71/81/84/86/87/88) had the highest expression. Four genes had significant linear expression at the developmental phase. Among them, three genes (MaU-box8/27/61) were gradually downregulated, whereas one gene (MaU-box71) was gradually upregulated with increasing development time.

2.6. Differential Expression of MaU-Box Genes under Abiotic Stresses

Figure 9 shows that 60 MaU-box genes responded to drought, salt, and low-temperature stressors. Among these stressors, the MaU-box gene family showed the strongest response to drought. A total of 55 MaU-box genes exhibited the highest expression under this stressor, during which 45 genes were upregulated by more than tenfold. The MaU-box gene family showed the highest expression at 24 h, during which 54 genes exhibited the highest expression. Salt stress also resulted in the high regulation of the MaU-box gene family, and this stressor led to the highest expression of four genes (MaU-box63/65/71/78) and the upregulation of two genes (MaU-box63/65) by more than tenfold (p < 0.05).

3. Discussion

The characteristics and functions of the U-box gene family has been studied in several plants [27,28]. In the present study, systematic phylogenetic analyses were conducted to obtain a detailed classification and nomenclature of the banana U-box. We found 91 PUB (Plant U-box) genes in banana genome. Similarly, 61 U-box proteins of Arabidopsis [12] and 77 U-box-containing proteins of rice had been identified and analyzed [17]. In total, 125 soybean PUB (GmPUB) genes, which encode proteins containing the U-box domain, have been identified [22]. The distribution of U-box proteins among species of different kingdoms is uneven [17]. Our data showed that the banana U-box genes were distributed across all 11 chromosomes at different densities. Phylogenetic analysis of the U-box from banana, Arabidopsis, and rice suggested that the U-box could be clustered into seven subgroups (I–VII). A similar study in soybean found that 125 GmPUB proteins were classified into six groups by phylogenetic analysis [22]. In this study, most banana U-box proteins show closer phylogenetic distance to their putative banana homologs than to their corresponding putative rice and Arabidopsis orthologs. Moreover, the U-box from banana had a closer relationship with rice compared with Arabidopsis. Interestingly, banana proteins MaU-box56, MaU-box78, MaU-box83 and MaU-box84 showed a closer phylogenetic relationship to the rice proteins than to their banana paralogs, suggesting that these banana proteins and their corresponding rice orthologs have evolved from a common ancestor before the speciation of the two species [17]. In the present study, conserved motif analysis showed that all identified MaU-box had typical U-box domains. Generally, a protein–protein interaction domain in E3 ubiquitin ligases interacts with their substrates for ubiquitination [29], and a complete U-box domain was found in all PUB proteins [30,31,32]. The proteins that contained conserved motifs had low sequence similarity, suggesting that mutations were accumulated during evolution [22]. The U-box in banana are found in combination with a variation of domains including armadillo (ARM) repeats, WD40 repeats, the tetratricopeptide (TPR) domain. The ARM repeats have been shown mostly to mediate the interaction with substrates, indicating that interaction renders substrates available for ubiquitination [23]. So the U-box proteins without ARM repeats in banana might have different interactions of E3 ubiquitin ligases with their substrates compared with the U-box proteins containing ARM repeats. The MaU-box gene family was differentially expressed in various tissues of banana. Similarly, several AtPUB-ARM genes were widely expressed in different tissues [33]. The MaU-box gene family had the highest expression in the roots. In a previous study, 12 MaE2 genes had the highest expression levels in roots [24]. These results suggested that MaU-box genes might be involved in the formation of the root system. PUB proteins play important roles in regulating plant growth and development [34]. In the present study, the 29 MaU-box genes (MaU-box3/4/8/9/10/13/17/18/19/20/22/25/27/28/34/38/39/41/43/48/49/50/51/52/56/59/61/63/70) had the highest expression at the beginning of banana’s developmental stage (day 25), which could be explained by the fact that the highly expressed genes usually play important roles in plant development [35], suggesting ubiquitination activation through the first stages of fruit development. Of note, the expression of eight MaE2 genes [23] and three MaU-box genes decreased gradually with prolonged developmental time. In strawberry fruit, all the genes decreased gradually after the flowering stage [36]. These data indicated that some genes (e.g., the MaU-box gene) might play important roles for the growth and development of fruits. Studies have shown that the U-box protein is involved in the response to various environmental stresses [9,20,37]. The U-box protein gene quickly responded to both biotic stress and abiotic stress and significantly influenced the accumulation of resistance related proteins in grapevine [20]. Silencing tomato U-box E3 ligase ACRE74 lead to break down of Cf9-especified resistance against Cladosporium fulvum leaf mold [20]. The U-box genes of rice might be involved in the defense against diseases [17]. A previous study observed differential expression patterns in nine soybean genes under drought stress [22]. In the present study, the MaU-box genes exhibited stronger response to drought than to salt and low temperature. Under drought stress, 45 MaU-box genes were upregulated by more than tenfold. OsPUB57 showed a stronger expression only in the resistant plants carrying the Pi9-resistant gene [17]. Consistent with this study, in our study, the MaPUB84 and MaPUB91 genes which showed closer phylogenetic distance to OsPUB57 had high expressions under stress. These results indicated that PUB genes might have key functions in responding to drought stress in plant.

4. Materials and Methods

4.1. Plant Materials and Treatment

The test material “Brazil” banana was obtained from the banana plantation of the National Banana Industry Technical System of Zhanjiang Comprehensive Test Station, South Subtropical Crops Institute, Chinese Academy of Tropical Agricultural Sciences (Zhanjiang, Guangdong, China). Different organs (roots, stems, leaves, female flowers, male flowers) were collected to study the temporal and spatial expression patterns of bananas. The fruits were collected at different developmental stages (25, 45, 65, and 85 days after florescence) to study fruit development. A healthy and consistent banana seedling with four leaves was selected for stress experiments. The banana seedlings were treated with 20% PEG 6000 (drought stress treatment) and 200 mM NaCl (salt stress treatment) and harvested at different time points (1, 6, and 24 h) after treatment [23]. The experiments were performed in triplicate. All samples were frozen in liquid nitrogen and stored at −80 °C for the purpose of extracting RNA for expression analysis.

4.2. Genome Identification of Banana U-Box Gene Family Members

To identify the potential members of the banana U-box protein family, publish the Arabidopsis thaliana and rice U-box protein sequences as seed sequences, and used BLASTP method search the banana genome database (Banana Genome Hub, available online: http://banana-genome.cirad.fr/content/download-dh-pahang) and Phytozome (available online: http://www.phytozome.net/) database. All candidate U-box genes were further verified by using SMART conserved domain search tools (available online: http://smart.embl-heidelberg.de/), eliminating repeat sequences, and deleting genes without the U-box domain. The MW and PI prediction of all U-box proteins was performed using the ProtParam tool (available online: http: //web.expasy.org/orgparam/). Information on the MaU-box gene, including chromosomal location, DNA sequence, CDS sequence, and aa length, was obtained from phyome12 (available online: https://phytozome.jgi.doe.gov/pz/portal.html#!info?alias=Org_Gmax). The MW and theoretical PI of the candidate MaU-box protein were obtained using the ExPASy Online Tool (available online: http://expasy.org/tools/). The subcellular localization of banana U-box protein was predicted by using the online software, Plant-mPLoc (available online: http://www.csbio.sjtu.edu.cn/bioinf/plant-multi/#). Finally, chromosome mapping was performed using the MapInspect tool according to the position of the U-box on the chromosome. For convenience, the MaU-box genes were numbered MaU-box1–MaU-box91 according to the order of chromosome 1 to 11. The structure of each gene was visualized using the Gene Structure Display Server (available online: http://gsds.cbi.pku.edu.cn/).

4.3. MaU-Box Protein Conserved Motif and Phylogenetic Analysis

The protein conserved motif of the MaU-box gene family was analyzed using MEME Suite 4.11.4 (available online: http://meme.nbcr.net/meme/) software. The maximum number of protein motifs was 20, and the length of the motifs was 6 to 200 aa.
To understand the evolutionary relationship of the U-box gene, we used the Clustal X version 1.83 software (lllkirch, France) with default parameters to compare the sequences of Arabidopsis thaliana, rice, and banana U-box gene family members. The phylogenetic tree was constructed by comparing the results with MEGA6.0 software (state college, PA, USA). The parameters of the software were set as follows: NJ method as the adjacency method and Poisson correction, paired delete, and bootstrap (1000 repetitions).

4.4. Gene Expression Analysis

The MaActin fragment of the banana was selected as the internal reference, and the primers were designed according to the registered sequence. All the MaU-box genes secific primers were designed according to the coding sequences by Primer5 software (PREMIER Biosoft International, Palo Alto, CA, USA) and checked using Blast in NCBI (available online: https://www.ncbi.nlm.nih.gov/). The relative expression level of the U-box gene was calculated using Equation 2−ΔΔCt.

5. Conclusions

Ninety-one U-box genes of the banana genome were classified into seven subgroups. Typical U-box domains were found in all identified MaU-box. The MaU-box gene family had the highest expression in the roots, and the strongest expression was found at the first developmental stage. The MaU-box genes exhibited stronger response to drought than to salt and low temperature. The results of this study provide information on the evolution and functions of the MaU-box genes.

Author Contributions

Data curation, H.H.; Formal analysis, D.S., Y.H.; Investigation, C.D.; Project administration, J.X.; Software, C.D.; Writing–original draft, H.H.; Writing–review & editing, J.X.

Funding

This research was funded by Modern Agro-industry Technology Research System (Project No.CARS-31-16).

Conflicts of Interest

The authors declare no conflict of interest.

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Ijms 19 03874 g001 550
Figure 1. MaU-box chromosomal localization maps. The size of a chromosome is indicated by its relative length in centimorgan (cM).
Figure 1. MaU-box chromosomal localization maps. The size of a chromosome is indicated by its relative length in centimorgan (cM).
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Figure 2. MaU-box gene structures.
Figure 2. MaU-box gene structures.
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Figure 3. Phylogenetic tree representing relationships among U-box domains of banana, Arabidopsis and rice. The different colors and different numbers (Group I–VI) indicate different MaPUB subgroups. The different shapes indicate different species.
Figure 3. Phylogenetic tree representing relationships among U-box domains of banana, Arabidopsis and rice. The different colors and different numbers (Group I–VI) indicate different MaPUB subgroups. The different shapes indicate different species.
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Figure 4. Distribution of conserved motifs for the banana MaU-box proteins.
Figure 4. Distribution of conserved motifs for the banana MaU-box proteins.
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Figure 5. The conserved domains in the MaU-box proteins.
Figure 5. The conserved domains in the MaU-box proteins.
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Figure 6. The typical protein structures in the MaU-box proteins.
Figure 6. The typical protein structures in the MaU-box proteins.
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Figure 7. Expression profiles of MaU-box genes in male flowers (MF), female flowers (FF), stems (S), roots (R), and leaves (L).
Figure 7. Expression profiles of MaU-box genes in male flowers (MF), female flowers (FF), stems (S), roots (R), and leaves (L).
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Figure 8. Expression profiles of MaU-box genes in banana pulp during the fruit developmental period. d: day.
Figure 8. Expression profiles of MaU-box genes in banana pulp during the fruit developmental period. d: day.
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Figure 9. Expression analysis of MaU-box genes in banana leaves under different abiotic treatments.
Figure 9. Expression analysis of MaU-box genes in banana leaves under different abiotic treatments.
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Table
Table 1. The information of Plant U-box (PUB) gene family in banana.
Table 1. The information of Plant U-box (PUB) gene family in banana.
Gene NameLocus IDChromosome LocationGene DNA (bp)CDS (bp)Protein Length (aa)Molecular Weight (kD)Theoretical pIExonPutative Localization
MaPUB1GSMUA_Achr1T12080_001chr1:9216255..9219037 reverse2783194464772.515.023Nucleus
MaPUB2GSMUA_Achr1T13220_001chr1:10096902..10098167 forward1266119139641.137.662Nucleus
MaPUB3GSMUA_Achr1T13730_001chr1:10477987..10483072 forward5086112837542.25.585Cytoplasm, Nucleus
MaPUB4GSMUA_Achr1T16210_001chr1:12121706..12123412 reverse1707170756860.398.621Cytoplasm
MaPUB5GSMUA_Achr1T22790_001chr1:17158846..17160507 reverse1662136245347.148.763Nucleus
MaPUB6GSMUA_Achr1T24290_001chr1:18636205..18639761 reverse3557183661166.295.486Nucleus
MaPUB7GSMUA_Achr2T08620_001chr2:12553612..12555419 reverse1808130543447.085.682Nucleus
MaPUB8GSMUA_Achr2T09640_001chr2:13094735..13107492 forward12,758254784894.336.836Nucleus
MaPUB9GSMUA_Achr2T11370_001chr2:14269037..14272568 forward3532230176684.565.854Nucleus
MaPUB10GSMUA_Achr2T15530_001chr2:16801361..16803647 reverse2287198366072.399.223Nucleus
MaPUB11GSMUA_Achr2T20690_001chr2:20462606..20463811 forward1206120640142.656.751Nucleus
MaPUB12GSMUA_Achr3T00280_001chr3:253594..258827 forward5234181260365.435.525Nucleus
MaPUB13GSMUA_Achr3T01110_001chr3:844229..845967 forward1739164154655.979.572Nucleus
MaPUB14GSMUA_Achr3T02030_001chr3:1351349..1352952 reverse1604126041945.718.643Nucleus
MaPUB15GSMUA_Achr3T06000_001chr3:4040242..4042320 reverse2079156051955.217.563Nucleus
MaPUB16GSMUA_Achr3T06160_001chr3:4178177..4180306 reverse2130170456761.789.342Cytoplasm
MaPUB17GSMUA_Achr3T06320_001chr3:4302726..4305879 reverse31542805934103.265.675Nucleus
MaPUB18GSMUA_Achr3T10610_001chr3:7831098..7835605 reverse45082745914101.976.585Nucleus
MaPUB19GSMUA_Achr3T12370_001chr3:9151629..9153329 reverse1701170156659.938.641Cytoplasm
MaPUB20GSMUA_Achr3T14620_001chr3:14736420..14738258 reverse1839167755859.68.581Cytoplasm
MaPUB21GSMUA_Achr3T19660_001chr3:20989179..20992456 forward32782946981107.655.924Nucleus
MaPUB22GSMUA_Achr3T25750_001chr3:25831272..25832624 forward1353129042946.175.382Nucleus
MaPUB23GSMUA_Achr4T00200_001chr4:193350..195464 reverse2115211570475.886.391Nucleus
MaPUB24GSMUA_Achr4T01530_001chr4:1265636..1274901 reverse9266183661167.065.896Cytoplasm, Nucleus
MaPUB25GSMUA_Achr4T03430_001chr4:2727458..2728362 reverse90581026928.368.732Nucleus
MaPUB26GSMUA_Achr4T04900_001chr4:3844084..3846449 forward2366158752859.155.657Nucleus
MaPUB27GSMUA_Achr4T05020_001chr4:3920776..3926784 forward60092853950105.015.915Cytoplasm, Nucleus
MaPUB28GSMUA_Achr4T05030_001chr4:3927558..3929980 reverse2423157552458.485.867Nucleus
MaPUB29GSMUA_Achr4T06990_001chr4:5215355..5216775 forward1421121240341.428.563Nucleus
MaPUB30GSMUA_Achr4T07400_001chr4:5497755..5499122 reverse1368130543447.465.632Nucleus
MaPUB31GSMUA_Achr4T11070_001chr4:7963314..7965615 reverse2302126942243.295.562Nucleus
MaPUB32GSMUA_Achr4T14130_001chr4:10562237..10563578 forward1342104434737.035.722Nucleus
MaPUB33GSMUA_Achr5T01020_001chr5:597533..598908 forward1376120640142.818.422Nucleus
MaPUB34GSMUA_Achr5T05220_001chr5:3854463..3856370 forward1908145848551.156.233Nucleus
MaPUB35GSMUA_Achr5T07140_001chr5:5158762..5162462 forward3701188762869.155.757Nucleus
MaPUB36GSMUA_Achr5T08500_001chr5:6179256..6185540 reverse628531291042114.115.845Nucleus
MaPUB37GSMUA_Achr5T11040_001chr5:7966157..7968849 reverse2693209469776.135.744Nucleus
MaPUB38GSMUA_Achr5T12380_001chr5:8892024..8899046 forward7023240380090.496.3912Nucleus
MaPUB39GSMUA_Achr5T13700_001chr5:9859570..9861021 forward1452136545448.238.751Cytoplasm
MaPUB40GSMUA_Achr5T21060_001chr5:22947743..22958748 reverse11,006241280390.015.489Nucleus
MaPUB41GSMUA_Achr5T21360_001chr5:23436476..23440174 forward3699228075983.626.064Cytoplasm, Nucleus
MaPUB42GSMUA_Achr5T28670_001chr5:28750592..28755063 reverse4472171357062.665.756Nucleus
MaPUB43GSMUA_Achr6T02470_001chr6:1615103..1616422 reverse1320114338040.988.693Nucleus
MaPUB44GSMUA_Achr6T06560_001chr6:4418997..4420524 forward1528112237340.577.672Nucleus
MaPUB45GSMUA_Achr6T10990_001chr6:7323129..7324847 reverse1719171957259.68.221Cytoplasm, Nucleus
MaPUB46GSMUA_Achr6T11310_001chr6:7517739..7519221 reverse1483114338041.256.733Nucleus
MaPUB47GSMUA_Achr6T18140_001chr6:12201719..12203017 reverse1299123040943.265.842Nucleus
MaPUB48GSMUA_Achr6T22980_001chr6:22176387..22181121 reverse4735188462769.888.5710Nucleus
MaPUB49GSMUA_Achr6T25390_001chr6:26469894..26479975 reverse10,08256371878202.195.287Cytoplasm, Nucleus
MaPUB50GSMUA_Achr6T25670_001chr6:26728664..26729950 forward1287128742844.868.661Nucleus
MaPUB51GSMUA_Achr6T28500_001chr6:28868630..28876365 forward7736183361067.968.799Nucleus
MaPUB52GSMUA_Achr6T36530_001chr6:34466958..34471270 reverse4313198366072.486.426Nucleus
MaPUB53GSMUA_Achr7T04450_001chr7:3366660..3370421 forward3762234979888.287.8811Nucleus
MaPUB54GSMUA_Achr7T05890_001chr7:4367855..4369228 forward1374137445748.069.351Cytoplasm
MaPUB55GSMUA_Achr7T09440_001chr7:7719776..7722069 forward2294191763870.348.954Nucleus
MaPUB56GSMUA_Achr7T09650_001chr7:7847312..7851814 reverse4503220873582.738.710Cell membrane, Chloroplast, Cytoplasm, Nucleus
MaPUB57GSMUA_Achr7T17740_001chr7:20510968..20523478 reverse12,51162792092223.935.639Cytoplasm, Nucleus
MaPUB58GSMUA_Achr7T18640_001chr7:21413794..21415228 forward1435114037941.346.413Cell membrane, Nucleus
MaPUB59GSMUA_Achr7T19940_001chr7:22941467..22943503 reverse2037159052955.78.553Nucleus
MaPUB60GSMUA_Achr7T22130_001chr7:24687902..24690206 reverse2305190263368.336.173Nucleus
MaPUB61GSMUA_Achr7T23310_001chr7:25579820..25581016 forward1197119739843.48.951Nucleus
MaPUB62GSMUA_Achr8T01360_001chr8:1146290..1151389 forward5100173157663.538.578Nucleus
MaPUB63GSMUA_Achr8T04940_001chr8:3264288..3266015 forward1728129943246.785.512Nucleus
MaPUB64GSMUA_Achr8T09590_001chr8:6746141..6747127 forward98798732833.955.911Nucleus
MaPUB65GSMUA_Achr8T11510_001chr8:8320562..8327700 forward7139255285095.416.1211Nucleus
MaPUB66GSMUA_Achr8T12630_001chr8:9406796..9419285 forward12,490157152657.296.3318Nucleus
MaPUB67GSMUA_Achr8T25140_001chr8:29062381..29066399 reverse4019126342044.97.714Nucleus
MaPUB68GSMUA_Achr8T30420_001chr8:32504280..32505566 forward128782227329.048.753Nucleus
MaPUB69GSMUA_Achr9T00690_001chr9:540580..541705 forward112666021923.389.332Cytoplasm, Nucleus
MaPUB70GSMUA_Achr9T01670_001chr9:1306678..1309170 forward2493140146650.568.522Nucleus
MaPUB71GSMUA_Achr9T08750_001chr9:5638998..5640625 forward1628103834536.088.473Nucleus
MaPUB72GSMUA_Achr9T12570_001chr9:8175348..8180293 reverse494690330031.916.012Nucleus
MaPUB73GSMUA_Achr9T14450_001chr9:9395076..9397076 reverse2001139846549.298.955Nucleus
MaPUB74GSMUA_Achr9T14560_001chr9:9502271..9504578 reverse2308175858563.118.673Nucleus
MaPUB75GSMUA_Achr9T15600_001chr9:10315534..10319034 forward3501203167675.016.857Nucleus
MaPUB76GSMUA_Achr9T28820_001chr9:32677125..32679340 reverse2216180059964.899.094Nucleus
MaPUB77GSMUA_Achr9T29420_001chr9:33126026..33130242 reverse4217183661168.186.649Nucleus
MaPUB78GSMUA_Achr10T04850_001chr10:14480133..14481503 forward137173524426.14.962Nucleus
MaPUB79GSMUA_Achr10T09450_001chr10:19291616..19292842 forward1227115538440.378.412Nucleus
MaPUB80GSMUA_Achr10T11310_001chr10:20821803..20823180 forward1378111937239.556.283Nucleus
MaPUB81GSMUA_Achr10T17120_001chr10:24446918..24449504 reverse2587112537440.876.142Nucleus
MaPUB82GSMUA_Achr10T17900_001chr10:24916493..24917809 forward1317113137640.828.253Nucleus
MaPUB83GSMUA_Achr10T22180_001chr10:27439361..27448280 reverse892040411346148.985.4914Nucleus
MaPUB84GSMUA_Achr10T22750_001chr10:27801994..27810019 forward8026263187698.616.1211Cell membrane, Nucleus
MaPUB85GSMUA_Achr10T22780_001chr10:27821009..27830243 forward9235259586496.028.514Nucleus
MaPUB86GSMUA_Achr10T27710_001chr10:30760030..30761828 reverse1799135945250.075.875Nucleus
MaPUB87GSMUA_Achr11T02530_001chr11:1736304..1752382 reverse16,079158152657.226.4118Nucleus
MaPUB88GSMUA_Achr11T06020_001chr11:4516270..4520590 reverse4321204067973.947.633Nucleus
MaPUB89GSMUA_Achr11T09460_001chr11:7338409..7341969 forward3561127842545.728.173Nucleus
MaPUB90GSMUA_Achr11T20980_001chr11:21780963..21789676 reverse8714240079989.465.719Nucleus
MaPUB91GSMUA_AchrUn_randomT07480_001chrUn_random:32367065..32372845 forward5781240380090.956.3711Nucleus

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MDPI and ACS Style

Hu, H.; Dong, C.; Sun, D.; Hu, Y.; Xie, J. Genome-Wide Identification and Analysis of U-Box E3 Ubiquitin-Protein Ligase Gene Family in Banana. Int. J. Mol. Sci. 2018, 19, 3874. https://doi.org/10.3390/ijms19123874

AMA Style

Hu H, Dong C, Sun D, Hu Y, Xie J. Genome-Wide Identification and Analysis of U-Box E3 Ubiquitin-Protein Ligase Gene Family in Banana. International Journal of Molecular Sciences. 2018; 19(12):3874. https://doi.org/10.3390/ijms19123874

Chicago/Turabian Style

Hu, Huigang, Chen Dong, Dequan Sun, Yulin Hu, and Jianghui Xie. 2018. "Genome-Wide Identification and Analysis of U-Box E3 Ubiquitin-Protein Ligase Gene Family in Banana" International Journal of Molecular Sciences 19, no. 12: 3874. https://doi.org/10.3390/ijms19123874

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