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  • Research article
  • Open Access

Genome-wide analysis of family-1 UDP glycosyltransferases (UGT) and identification of UGT genes for FHB resistance in wheat (Triticum aestivum L.)

Contributed equally
BMC Plant BiologyBMC series – open, inclusive and trusted201818:67

https://doi.org/10.1186/s12870-018-1286-5

  • Received: 27 November 2017
  • Accepted: 10 April 2018
  • Published:

Abstract

Background

Fusarium head blight (FHB), a devastating disease in wheat worldwide, results in yield loses and mycotoxin, such as deoxynivalenol (DON), accumulation in infected grains. DON also facilitates the pathogen colonization and spread of FHB symptoms during disease development. UDP-glycosyltransferase enzymes (UGTs) are known to contribute to detoxification and enhance FHB resistance by glycosylating DON into DON-3-glucoside (D3G) in wheat. However, a comprehensive investigation of wheat (Triticum aestivum) UGT genes is still lacking.

Results

In this study, we carried out a genome-wide analysis of family-1 UDP glycosyltransferases in wheat based on the PSPG conserved box that resulted in the identification of 179 putative UGT genes. The identified genes were clustered into 16 major phylogenetic groups with a lack of phylogenetic group K. The UGT genes were invariably distributed among all the chromosomes of the 3 genomes. At least 10 intron insertion events were found in the UGT sequences, where intron 4 was observed as the most conserved intron. The expression analysis of the wheat UGT genes using both online microarray data and quantitative real-time PCR verification suggested the distinct role of UGT genes in different tissues and developmental stages. The expression of many UGT genes was up-regulated after Fusarium graminearum inoculation, and six of the genes were further verified by RT-qPCR.

Conclusion

We identified 179 UGT genes from wheat using the available sequenced wheat genome. This study provides useful insight into the phylogenetic structure, distribution, and expression patterns of family-1 UDP glycosyltransferases in wheat. The results also offer a foundation for future work aimed at elucidating the molecular mechanisms underlying the resistance to FHB and DON accumulation.

Keywords

  • UDP-glycosyltransferase
  • Fusarium head blight
  • Wheat
  • Expression pattern
  • Phylogeny
  • Deoxynivalenol

Background

Fusarium head blight (FHB) or scab, primarily caused by Fusarium graminearum, is one of the most devastating diseases in wheat and barley worldwide [1]. FHB infection not only results in heavy yield loss but also deteriorates grain quality due to the production of trichothecene mycotoxins such as deoxynivalenol (DON), nivalenol (NIV) and their acetylated forms 3 (or 15)-acetyl-4-deoxynivalenol, 4-acetylnivalenol or fusarenone X (FX), of which DON is one of the most important members [2]. The accumulation of DON and other toxins in the infected grains is making wheat unfit for human and livestock consumption posing a risk to world food security [3]. DON along with other trichothecenes also act as fungal virulence factors, facilitating the colonization and spread of scab symptoms within wheat spikes [2]. When the TRI5 gene was disrupted, the DON-nonproducing mutants of F. graminearum lacked the ability to spread in wheat spikes [4]. The resistance to DON accumulation is different in FHB infected wheat varieties, highlighting the involvement of a host resistance system during the course of DON production [1]. DON-3-glucoside (D3G), a non-toxic masked form of DON, has been observed in wheat grains in addition to DON and is stored in plant cell vacuoles [5]. Using their enzymatic defense system, plants convert DON into D3G as previously described for the first time in Arabidopsis [6]. The resistance to FHB infection and D3G accumulation in wheat grains is correlated with the ability of a higher conversion of DON into D3G [7]. DON conversion into D3G, a natural detoxification process in plants called glycosylation, along with other mechanisms of detoxification such as acetylation and de-epoxidation, reduce mycotoxin accumulation and are potential resistance factors against FHB [2, 5, 8].

Glycosylation is a widespread cellular modification reaction in all living organisms, attaching a carbohydrate to the hydroxyl or other functional group of a molecule in a biosynthetic pathway [9]. Glycosylation is a form of co-translational and post-translational modification altering the chemical property, sub-cellular location and activity of a variety of bio-molecules [10]. Glycosylation modifications are catalyzed by glycosyltransferase enzymes (GTs), which are highly divergent, polyphyletic and belong to a multigene family [11]. Glycosylation, in addition to other reactions, paves the way to the production of a huge variety of secondary metabolites in plants. GTs from different species can be classified into 94 families based on their amino acid sequence similarities, catalytic mechanisms as well as the presence of conserved sequence motifs according to the most recent update of CAZy (http://www.cazy.org/GlycosylTransferases.html). Among them, family-1 GTs are the most common glycosyltransferases in the plant kingdom generally catalyzing the process of glycosylation by transferring sugar moieties from activated donor molecules to acceptor molecules [5, 12, 13]. Family-1 GTs use uridine 5′-diphosphate sugars as the donor molecule; hence, they are also named uridine-diphosphate glycosyltransferases (UGTs) [14]. These enzymes act upon a huge variety of highly diverse and complex substrates in the plant kingdom such as flavonoids, terpenes, auxin, cytokinin, salicylic acid and many others to regulate plant growth, development, disease resistance and interaction with the environment [15]. The sequences at N-terminal region of these enzymes are highly diverse and are considered to be responsible for recognition of a variety of substrates. The C-terminal region on the other hand contains a conserved motif called Plant Secondary Product Glycosyltransferase (PSPG). The PSPG box is a unique, well conserved region of 44 amino acids found in all UGTs across all studied plant taxa [14, 16].

UDP-glycosyltransferases have been identified in various plant species, including Linum usitatissimum, Arabidopsis thaliana, Malus domestica, Vitis vinifera, Populus trichocarpa, Glycine max, Mimulus guttatus, Oryza sativa, Sorghum bicolor, Brachypodium distachyon, Zea mays, Gossypium raimondii, Gossypium arboreum, Gossypium hirsutum and most recently in Prunus persica, Brassica rapa, and Brassica oleracea with approximately more than 100 UGTs in all the higher plants investigated [15, 1722]. UGTs have been shown to display broad as well as selective substrate specificity in plants recognizing a wide range of acceptor molecules [23, 24]. The UGTs not only glycosylate acceptor molecules, such as anthocyanidins, flavonols, flavonoids, saponins, sterols terpenoids, phenylpropanoids and plant hormones, but also detoxify and deactivate xenobiotics and play a pivotal role in plant-pathogen interactions [9, 21].

Functioning of UGTs has been described in many plants such as Arabidopsis, kiwifruit and strawberry [2528]. Besides their various other attributes, UGT genes have also been demonstrated to contribute to FHB resistance in crops possibly through DON glycosylation [5]. Four highly DON inducible candidate GTs were identified in barley and one of them HvUGT13248 gene, the first monocot DON-glucosyltransferase, extended DON resistance in yeast and has since been expressed in Arabidopsis and wheat providing resistance against DON and other mycotoxins [2933]. Similarly, two DON detoxification genes conjugating DON to D3G have been identified in Brachypodium distachyon [19]. Recently the HvUGT-10 W1 gene isolated from an FHB resistant barley variety (10 W1) also conferred FHB tolerance [34]. In wheat only a few candidate UGT genes such as TaUGTB2, TaUGT1, TaUGT2, TaUGT3, TaUGT4, and TaUGT12887 have been identified and the later 4 genes have been shown to be closely related to FHB resistance; however, a large scale systematic investigation of UGTs in the wheat genome is still lacking [3539].

In this study we identified 179 UGT genes from wheat using the available sequenced wheat genome. The genetic relationships of these UGTs were determined using sequence alignment and phylogenetic tree analysis. The differential expression of genes in various wheat tissues as well as wheat spikes treated with F. graminearum vs control expressions patterns were analyzed using NCBI and universal microarray data and further confirmed through RT-qPCR analysis of the selected genes. This study will hopefully provide a baseline to conduct future functional characterization analysis of wheat UGT genes in order to understand the molecular mechanisms behind substrate specificity in general and especially the resistance to FHB and DON accumulation in crops.

Methods

Identification of UGT genes in wheat

The 44-amino acid conserved sequence of the PSPG motif was used as a query to search against the wheat genome database (TGACv1) at the Ensemble Plants (http://plants.ensembl.org/Triticum_aestivum/) by HMMER profile to identify members of the UGT protein family in wheat [9, 40]. The identified protein sequences of each UGT were further verified through the PFAM (http://pfam.xfam.org/) and the SMART (http://smart.embl-heidelberg.de/) databases to confirm the presence of the UDP-glycosyltransferase domain. The information (including amino acid length, transcript count and location) was also obtained from Ensemble Plants. The molecular weight (MW) and isoelectric point (PI) of each UGT protein were calculated using the online ExPASy program (http://web.expasy.org/compute_pi/) [41]. The subcellular localization of each UGT protein was predicted using the online CELLO v2.5 system (http://cello.life.nctu.edu.tw/cello.html) [42].

Sequence alignment and phylogenetic analysis

Multiple sequence alignments of the wheat UGT protein sequences were performed by MUSCLE (http://www.ebi.ac.uk/Tools/msa/muscle/). The phylogenetic tree was constructed using MEGA 7.0 software (http://www.megasoftware.net/) based on the full-length UGT protein sequences through a neighbor-joining algorithm using a 1000 bootstrap value [43].

Chromosomal locations

The genetic location of each UGT on the chromosomes was retrieved from the final TGACv1 map [40]. The genetic map of each UGT on the chromosome was modified from the primary map drawn by the MapInspect tool (http://mapinspect.software.informer.com/).

Intron mapping

The wheat UGT intron map was constructed by determining the intron positions, splice sites and phases. The intron phases were determined as described previously: the introns positioned between two triplet codons were defined as phase 0, introns positioned after the first base in the codon were defined as phase 1, and the introns positioned after the second base in the codon were defined as phase 2 [20].

Expression profile analysis

A genome-wide expression analysis of the wheat UGT genes in various organs and developmental stages was performed using high-throughput RNA sequence data from 5 organs (root, stem, leaf, spike and grain), each with 3 developmental stages (https://urgi.versailles.inra.fr/files/RNASeqWheat/) [44]. To analyze the expression profiles of the wheat UGT genes after F. graminearum inoculation, the Affymetrix wheat array data with wheat spikelets from the susceptible spring wheat cultivar Roblin inoculated with either water or F. graminearum strains that do or do not produce DON were downloaded (https://www.ncbi.nlm.nih.gov/geo/) for further analysis (accession number GSE54554). The expression profiles of these UGT genes were generated by using MeV 4.7 software (https://sourceforge.net/projects/mev-tm4/files/mev-tm4/).

Plant materials and treatment

The wheat cultivar used in this study was Annong 8455, which is highly susceptible to FHB in China. The wheat plants were grown in a green house at 22 °C for 14-h light and 12 °C for 10-h dark at the Jiangsu Academy of Agricultural Sciences, China.

The early anthesis stage spikelets were chosen for further F. graminearum or water (CK) inoculation as described previously [45]. Approximately 10 μl of fungal suspension (1 × 106 conidia per mL) of F. graminearum or water was injected into the central spikelet of a spike during early anthesis. The inoculated spikes were covered with a plastic bag for 3 days.

RNA isolation and RT-qPCR analysis

To validate the expression pattern of the six selected genes, the total RNA was isolated from the root, stem, leaf, pre-emergence spikelet, pre-anthesis spikelet, and grains of 7, 14 and 21 days after flowering (DAF) using the Promega SV total RNA isolation system (Promega, United States), according to the manufacturer’s instructions. The RNA of the spikelets treated with water or F. graminearum after 2 and 4 days was also extracted in the same way. The first-strand cDNAs were synthesized from the total RNA by using the PrimeScript 1st strand cDNA Synthesis Kit (Takara Bio, Dalian, China), according to the manufacturer’s manual. Real-time PCR was performed with a Roche thermal cycler 96 using SYBR Green to detect gene expression. The wheat tubulin gene was used as an endogenous control. The gene specific primers used for RT-qPCR are listed in the Additional file 1: Table S1. The PCR conditions were as follows: 95 °C for 30 s, 95 °C for 5 s, 60 °C for 20 s and 72 °C for 10 s for 45 cycles. Data from the individual runs were collated using the 2−ΔΔCT method [46]. All the reactions were performed using at least three replicates.

Results

Identification of UGT genes in wheat

A nearly complete and accurate sequence assembly of the allohexaploid wheat reference accession, Chinese Spring (CS42), was released recently, enabling a more in-depth analysis of UGT genes in this key global crop [40]. The conserved UGT domain of 44 amino acids called the PSPG box was used in this study to identify the presence of UGT genes in the wheat genome [9]. A total of 179 putative UGT genes having an average length of 471 amino acids were identified and used for further analysis (Table 1). Most of the genes were in the range of 400 to 500 amino acids, while only a few genes were above 500 and below 300 amino acids in size and 1 to 3 transcripts were counted for these genes (Additional file 2: Figure S1). The theoretical isoelectric point (pI) and molecular weight (Mw) ranged from 4.77 to 10.32 (average pI = 5.79) and from 26.9 kDa to 76.5 kDa (average Mw = 50.9 kDa), respectively (Table 1). The theoretical cellular localization showed 22, 19, 5, 2 and 0.6% of the genes were localized only into the chloroplast, cytoplasm, plasma membrane, mitochondria and nucleus, respectively, while the rest of the genes were localized into any of these compartments (Table 1).
Table 1

The list of the putative wheat UGT genes identified in this study

No.

Gene stable ID

Amino acid length

Transcript count

PI

MW (kDa)

Subcellular location

Location

1

TRIAE_CS42_1AL_TGACv1_000152_AA0004850

569

2

5.6

62.3

Chloroplast Cytoplasmic

TGACv1_000152_1AL: 34,636–36,800

2

TRIAE_CS42_1AL_TGACv1_000696_AA0017290

479

1

5.7

52.2

Cytoplasmic

TGACv1_000696_1AL: 81,630–83,635

3

TRIAE_CS42_1AL_TGACv1_001147_AA0025960

456

1

5.3

49.3

Chloroplast Cytoplasmic PlasmaMembrane

TGACv1_001147_1AL: 8789–10,755

4

TRIAE_CS42_1AL_TGACv1_001208_AA0027000

474

1

6

50.6

Mitochondrial PlasmaMembrane

TGACv1_001208_1AL: 53,142–54,992

5

TRIAE_CS42_1AL_TGACv1_001652_AA0033630

324

1

6.2

35

PlasmaMembrane

TGACv1_001652_1AL: 54,716–56,210

6

TRIAE_CS42_1AS_TGACv1_020318_AA0076580

505

3

5.3

55.2

Cytoplasmic Mitochondrial

TGACv1_020318_1AS: 8106–11,995

7

TRIAE_CS42_1BL_TGACv1_031128_AA0108300

464

1

5.4

49.6

PlasmaMembrane

TGACv1_031128_1BL: 73,386–75,090

8

TRIAE_CS42_1BL_TGACv1_032253_AA0127550

504

1

6

54.1

Chloroplast Cytoplasmic

TGACv1_032253_1BL: 30,766–32,648

9

TRIAE_CS42_1BL_TGACv1_032609_AA0132000

451

1

6

48.4

PlasmaMembrane

TGACv1_032609_1BL: 18,947–20,825

10

TRIAE_CS42_1BL_TGACv1_034076_AA0143330

423

1

5.9

45.3

Cytoplasmic Mitochondrial

TGACv1_034076_1BL: 13,111–14,941

11

TRIAE_CS42_1BS_TGACv1_049891_AA0163670

536

1

5.5

58

Cytoplasmic Chloroplast

TGACv1_049891_1BS: 3226–6480

12

TRIAE_CS42_1BS_TGACv1_050208_AA0169040

542

1

5.6

56.7

Chloroplast PlasmaMembrane

TGACv1_050208_1BS: 22,661–24,740

13

TRIAE_CS42_1DL_TGACv1_061249_AA0190020

486

1

6

52.4

Cytoplasmic PlasmaMembrane

TGACv1_061249_1DL: 118,022–119,855

14

TRIAE_CS42_1DL_TGACv1_061472_AA0196220

473

1

5.6

50.6

Cytoplasmic

TGACv1_061472_1DL: 36,915–38,810

15

TRIAE_CS42_1DL_TGACv1_061688_AA0201770

386

1

6

42.6

Cytoplasmic

TGACv1_061688_1DL: 38,929–45,276

16

TRIAE_CS42_1DL_TGACv1_062127_AA0209080

497

1

5.2

53

Chloroplast Cytoplasmic

TGACv1_062127_1DL: 35,096–37,034

17

TRIAE_CS42_2AL_TGACv1_092977_AA0268460

496

2

5.9

53.3

Chloroplast PlasmaMembrane

TGACv1_092977_2AL: 132,556–134,743

18

TRIAE_CS42_2AL_TGACv1_094039_AA0291500

363

1

6.7

37.6

Chloroplast PlasmaMembrane

TGACv1_094039_2AL: 11,847–13,415

19

TRIAE_CS42_2AL_TGACv1_094526_AA0299210

444

1

5.5

47.4

PlasmaMembrane Chloroplast Cytoplasmic

TGACv1_094526_2AL: 10,962–12,595

20

TRIAE_CS42_2AL_TGACv1_094669_AA0301250

493

1

5.7

53.5

Chloroplast PlasmaMembrane Cytoplasmic

TGACv1_094669_2AL: 43,325–45,075

21

TRIAE_CS42_2AL_TGACv1_095609_AA0312870

479

1

5.4

51.7

Cytoplasmic

TGACv1_095609_2AL: 23,136–25,080

22

TRIAE_CS42_2AS_TGACv1_112708_AA0343800

465

1

9

51

Mitochondrial Chloroplast

TGACv1_112708_2AS: 5716–7407

23

TRIAE_CS42_2AS_TGACv1_113114_AA0351430

314

1

5

35.1

Cytoplasmic

TGACv1_113114_2AS: 82,126–83,619

24

TRIAE_CS42_2AS_TGACv1_113164_AA0352370

474

1

5.5

51.6

Chloroplast

TGACv1_113164_2AS: 56,381–58,985

25

TRIAE_CS42_2AS_TGACv1_113792_AA0360520

471

1

5.8

51.1

Chloroplast

TGACv1_113792_2AS: 1565–3515

26

TRIAE_CS42_2AS_TGACv1_113792_AA0360550

470

1

5.4

50.6

Cytoplasmic Chloroplast

TGACv1_113792_2AS: 12,613–15,275

27

TRIAE_CS42_2BL_TGACv1_132343_AA0436900

489

1

5.7

53.4

Chloroplast

TGACv1_132343_2BL: 30,155–32,015

28

TRIAE_CS42_2BL_TGACv1_133391_AA0442380

485

1

5.4

51.3

Chloroplast PlasmaMembrane Cytoplasmic

TGACv1_133391_2BL: 9937–11,795

29

TRIAE_CS42_2BS_TGACv1_146052_AA0454210

480

2

5.4

54.9

Cytoplasmic Chloroplast

TGACv1_146052_2BS: 172,038–174,105

30

TRIAE_CS42_2BS_TGACv1_146052_AA0454220

234

1

5.2

26

Chloroplast Cytoplasmic

TGACv1_146052_2BS: 175,207–176,915

31

TRIAE_CS42_2BS_TGACv1_146119_AA0455760

477

1

5.9

51.6

Chloroplast PlasmaMembrane

TGACv1_146119_2BS: 73,276–75,131

32

TRIAE_CS42_2BS_TGACv1_146212_AA0458920

477

1

5.9

51.8

Chloroplast

TGACv1_146212_2BS: 40,106–41,900

33

TRIAE_CS42_2BS_TGACv1_146276_AA0461240

458

1

6.2

49.8

Chloroplast

TGACv1_146276_2BS: 43,496–45,300

34

TRIAE_CS42_2BS_TGACv1_146286_AA0461540

466

1

8.4

51.1

Chloroplast Mitochondrial

TGACv1_146286_2BS: 86,006–87,750

35

TRIAE_CS42_2BS_TGACv1_146500_AA0466680

498

1

5.2

52.4

Chloroplast

TGACv1_146500_2BS: 99,495–101,475

36

TRIAE_CS42_2BS_TGACv1_146843_AA0473870

505

1

6.4

53.9

Chloroplast PlasmaMembrane

TGACv1_146843_2BS: 70,557–72,425

37

TRIAE_CS42_2BS_TGACv1_147441_AA0483230

477

1

6.1

50.8

Cytoplasmic

TGACv1_147441_2BS: 41,416–43,450

38

TRIAE_CS42_2BS_TGACv1_147641_AA0485890

519

1

5.6

56.9

Chloroplast

TGACv1_147641_2BS: 19,336–29,770

39

TRIAE_CS42_2DL_TGACv1_158399_AA0517610

492

1

5.4

54

Cytoplasmic

TGACv1_158399_2DL: 87,645–89,545

40

TRIAE_CS42_2DL_TGACv1_159414_AA0537930

482

1

5.4

51.9

PlasmaMembrane Cytoplasmic

TGACv1_159414_2DL: 9459–11,225

41

TRIAE_CS42_2DL_TGACv1_159743_AA0542200

469

1

5.5

51.3

Cytoplasmic

TGACv1_159743_2DL: 29,369–31,464

42

TRIAE_CS42_2DL_TGACv1_160147_AA0547510

499

1

5.9

53.3

PlasmaMembrane Chloroplast

TGACv1_160147_2DL: 11,782–13,675

43

TRIAE_CS42_2DL_TGACv1_160383_AA0549920

485

2

5.5

53.7

Cytoplasmic Mitochondrial Chloroplast

TGACv1_160383_2DL: 17,866–19,990

44

TRIAE_CS42_2DL_TGACv1_160484_AA0550940

476

1

6.4

51.5

PlasmaMembrane

TGACv1_160484_2DL: 22,697–24,835

45

TRIAE_CS42_2DS_TGACv1_177189_AA0568300

505

1

5

53.5

Chloroplast

TGACv1_177189_2DS: 168,676–170,825

46

TRIAE_CS42_2DS_TGACv1_177304_AA0572860

462

1

5.2

49.6

PlasmaMembrane Cytoplasmic

TGACv1_177304_2DS: 18,887–22,885

47

TRIAE_CS42_2DS_TGACv1_177710_AA0582890

508

2

5.4

55.8

Chloroplast

TGACv1_177710_2DS: 37,388–39,565

48

TRIAE_CS42_2DS_TGACv1_177916_AA0587150

493

1

5.7

53.3

Chloroplast

TGACv1_177916_2DS: 19,783–21,976

49

TRIAE_CS42_2DS_TGACv1_178033_AA0589680

467

1

6.4

50.9

Chloroplast

TGACv1_178033_2DS: 37,145–39,412

50

TRIAE_CS42_2DS_TGACv1_178118_AA0591100

372

1

8.5

40

PlasmaMembrane

TGACv1_178118_2DS: 56,233–58,495

51

TRIAE_CS42_2DS_TGACv1_178131_AA0591440

497

1

5.7

53

Chloroplast PlasmaMembrane Cytoplasmic

TGACv1_178131_2DS: 31,516–33,382

52

TRIAE_CS42_2DS_TGACv1_178315_AA0594020

476

1

6

51.3

Chloroplast

TGACv1_178315_2DS: 49,188–50,874

53

TRIAE_CS42_2DS_TGACv1_178795_AA0601130

469

1

6.3

50

Cytoplasmic

TGACv1_178795_2DS: 43,800–45,517

54

TRIAE_CS42_3AL_TGACv1_194443_AA0633160

500

2

5.6

54.5

Cytoplasmic

TGACv1_194443_3AL: 22,846–28,150

55

TRIAE_CS42_3AL_TGACv1_194677_AA0637610

475

1

5.5

51.5

Cytoplasmic Chloroplast

TGACv1_194677_3AL: 53,009–55,235

56

TRIAE_CS42_3AL_TGACv1_194875_AA0641170

466

1

5.7

50.6

Cytoplasmic Chloroplast

TGACv1_194875_3AL: 63,326–65,525

57

TRIAE_CS42_3AS_TGACv1_210937_AA0681620

414

1

5.3

44.4

Chloroplast Cytoplasmic

TGACv1_210937_3AS: 119,816–121,716

58

TRIAE_CS42_3AS_TGACv1_211248_AA0687180

551

1

5

59.3

Cytoplasmic Chloroplast

TGACv1_211248_3AS: 47,048–49,241

59

TRIAE_CS42_3AS_TGACv1_211655_AA0692640

472

1

5.3

50.6

Cytoplasmic

TGACv1_211655_3AS: 41,556–44,305

60

TRIAE_CS42_3AS_TGACv1_211823_AA0694680

511

1

5.5

56.9

Cytoplasmic

TGACv1_211823_3AS: 30,616–32,748

61

TRIAE_CS42_3AS_TGACv1_211823_AA0694700

492

1

5.4

54.7

Cytoplasmic

TGACv1_211823_3AS: 44,976–46,896

62

TRIAE_CS42_3B_TGACv1_220919_AA0723700

472

1

6.1

51.3

Chloroplast

TGACv1_220919_3B: 29,856–31,633

63

TRIAE_CS42_3B_TGACv1_220919_AA0723750

469

1

5.5

50.8

Chloroplast PlasmaMembrane

TGACv1_220919_3B: 149,148–150,855

64

TRIAE_CS42_3B_TGACv1_221277_AA0735990

473

1

5.1

51

Cytoplasmic Chloroplast

TGACv1_221277_3B: 36,097–37,935

65

TRIAE_CS42_3B_TGACv1_221877_AA0752320

496

1

5.4

54.8

Cytoplasmic

TGACv1_221877_3B: 70,264–73,165

66

TRIAE_CS42_3B_TGACv1_221924_AA0753300

468

1

5.4

50.8

Cytoplasmic Chloroplast

TGACv1_221924_3B: 38,292–39,921

67

TRIAE_CS42_3B_TGACv1_222356_AA0762980

464

1

5.3

50.9

PlasmaMembrane Chloroplast Cytoplasmic

TGACv1_222356_3B: 55,147–57,245

68

TRIAE_CS42_3B_TGACv1_223815_AA0787850

461

1

5.2

50

Chloroplast Cytoplasmic

TGACv1_223815_3B: 24,267–25,985

69

TRIAE_CS42_3B_TGACv1_224677_AA0799850

457

2

5.4

49.9

Chloroplast Cytoplasmic Mitochondrial

TGACv1_224677_3B: 12,637–14,485

70

TRIAE_CS42_3B_TGACv1_228792_AA0827590

403

1

5.2

44.8

Cytoplasmic

TGACv1_228792_3B: 13,838–16,085

71

TRIAE_CS42_3DL_TGACv1_249782_AA0856200

465

1

6

50.8

Cytoplasmic

TGACv1_249782_3DL: 45,815–54,365

72

TRIAE_CS42_3DL_TGACv1_249823_AA0856930

481

1

5.4

52.8

Cytoplasmic

TGACv1_249823_3DL: 53,186–55,160

73

TRIAE_CS42_3DL_TGACv1_251186_AA0878520

489

1

6.1

53.1

Chloroplast Mitochondrial

TGACv1_251186_3DL: 6166–8082

74

TRIAE_CS42_3DL_TGACv1_251733_AA0884380

472

1

5.8

51.1

Chloroplast

TGACv1_251733_3DL: 18,147–19,817

75

TRIAE_CS42_3DS_TGACv1_271859_AA0909590

560

1

5.4

51.4

Chloroplast Cytoplasmic Mitochondrial

TGACv1_271859_3DS: 46,873–53,915

76

TRIAE_CS42_3DS_TGACv1_272095_AA0914550

443

1

5.5

48.2

Chloroplast Cytoplasmic

TGACv1_272095_3DS: 18,456–20,253

77

TRIAE_CS42_3DS_TGACv1_272144_AA0915540

380

2

5.8

42.2

Cytoplasmic

TGACv1_272144_3DS: 15,466–17,879

78

TRIAE_CS42_3DS_TGACv1_272561_AA0922330

498

1

5.7

53.7

Cytoplasmic Mitochondrial Chloroplast

TGACv1_272561_3DS: 42,311–44,165

79

TRIAE_CS42_3DS_TGACv1_274000_AA0934260

484

1

5.3

51.8

Cytoplasmic

TGACv1_274000_3DS: 16,535–18,425

80

TRIAE_CS42_4AL_TGACv1_288576_AA0952450

503

2

5.4

56.2

Chloroplast Mitochondrial Cytoplasmic

TGACv1_288576_4AL: 121,655–123,785

81

TRIAE_CS42_4AL_TGACv1_291270_AA0993350

455

1

5.8

47

Chloroplast

TGACv1_291270_4AL: 21,446–23,100

82

TRIAE_CS42_4AL_TGACv1_291728_AA0996300

507

1

4.9

54.4

Chloroplast Cytoplasmic

TGACv1_291728_4AL: 4996–7190

83

TRIAE_CS42_4AL_TGACv1_292113_AA0997730

498

1

8.7

54.5

Mitochondrial

TGACv1_292113_4AL: 17,011–18,815

84

TRIAE_CS42_4AL_TGACv1_292676_AA0999440

506

1

5

54.5

Chloroplast Cytoplasmic

TGACv1_292676_4AL: 10,676–12,740

85

TRIAE_CS42_4AL_TGACv1_293019_AA1000030

452

1

6.6

49.7

Mitochondrial Cytoplasmic

TGACv1_293019_4AL: 8872–10,875

86

TRIAE_CS42_4BL_TGACv1_320707_AA1046800

359

1

5.5

39.7

PlasmaMembrane Cytoplasmic

TGACv1_320707_4BL: 6020–7485

87

TRIAE_CS42_4BS_TGACv1_327950_AA1079620

576

1

8.4

62.3

PlasmaMembrane Mitochondrial

TGACv1_327950_4BS: 204,456–207,103

88

TRIAE_CS42_4BS_TGACv1_329322_AA1100160

455

1

6.1

47.2

Chloroplast

TGACv1_329322_4BS: 51,826–53,691

89

TRIAE_CS42_4BS_TGACv1_329455_AA1101520

461

1

6.5

49.8

Chloroplast Cytoplasmic

TGACv1_329455_4BS: 26,226–28,193

90

TRIAE_CS42_4BS_TGACv1_329471_AA1101760

567

1

7.2

61.6

PlasmaMembrane

TGACv1_329471_4BS: 21,537–26,265

91

TRIAE_CS42_4BS_TGACv1_332581_AA1110480

461

1

5.8

49.5

Chloroplast Cytoplasmic PlasmaMembrane

TGACv1_332581_4BS: 1227–3355

92

TRIAE_CS42_4DL_TGACv1_343563_AA1136610

474

1

5.4

51.3

Chloroplast

TGACv1_343563_4DL: 21,876–23,872

93

TRIAE_CS42_4DL_TGACv1_344211_AA1144960

482

1

5.6

52.4

Chloroplast

TGACv1_344211_4DL: 9685–11,555

94

TRIAE_CS42_5AL_TGACv1_374728_AA1207660

491

1

6

53.4

Cytoplasmic

TGACv1_374728_5AL: 108,276–110,700

95

TRIAE_CS42_5AL_TGACv1_375188_AA1217460

429

1

5.9

46.3

Cytoplasmic Chloroplast PlasmaMembrane

TGACv1_375188_5AL: 37,326–38,987

96

TRIAE_CS42_5AL_TGACv1_375684_AA1225590

475

2

5.8

51.2

Cytoplasmic Chloroplast

TGACv1_375684_5AL: 54,671–56,869

97

TRIAE_CS42_5AL_TGACv1_375893_AA1228550

461

1

6.1

49.4

Mitochondrial

TGACv1_375893_5AL: 47,896–49,580

98

TRIAE_CS42_5AL_TGACv1_375929_AA1229020

476

1

5.6

51.7

PlasmaMembrane

TGACv1_375929_5AL: 57,318–59,915

99

TRIAE_CS42_5AL_TGACv1_376019_AA1230850

491

1

5.8

52.5

Cytoplasmic Mitochondrial

TGACv1_376019_5AL: 40,796–42,980

100

TRIAE_CS42_5AL_TGACv1_377811_AA1249610

472

1

5.8

51.9

Chloroplast

TGACv1_377811_5AL: 10,736–13,180

101

TRIAE_CS42_5BL_TGACv1_404184_AA1288910

490

1

5

53.3

Chloroplast

TGACv1_404184_5BL: 196,689–198,409

102

TRIAE_CS42_5BL_TGACv1_404184_AA1288920

490

1

5.5

53.3

Chloroplast

TGACv1_404184_5BL: 293,989–296,149

103

TRIAE_CS42_5BL_TGACv1_404233_AA1291500

506

1

5.3

54.9

Cytoplasmic

TGACv1_404233_5BL: 154,317–156,325

104

TRIAE_CS42_5BL_TGACv1_404244_AA1291960

470

1

5.6

50.6

Cytoplasmic

TGACv1_404244_5BL: 82,335–84,305

105

TRIAE_CS42_5BL_TGACv1_404293_AA1294180

497

1

5.7

53.7

Cytoplasmic Chloroplast

TGACv1_404293_5BL: 93,246–95,160

106

TRIAE_CS42_5BL_TGACv1_404294_AA1294310

477

1

5.9

50.3

Chloroplast

TGACv1_404294_5BL: 185,737–187,835

107

TRIAE_CS42_5BL_TGACv1_404418_AA1299240

471

1

5.6

50.8

Chloroplast Cytoplasmic

TGACv1_404418_5BL: 207,022–208,895

108

TRIAE_CS42_5BL_TGACv1_405759_AA1334850

464

1

5.8

50.4

Mitochondrial PlasmaMembrane

TGACv1_405759_5BL: 73,581–75,127

109

TRIAE_CS42_5BL_TGACv1_406257_AA1343160

473

1

6.1

51.2

Mitochondrial

TGACv1_406257_5BL: 33,956–36,228

110

TRIAE_CS42_5BL_TGACv1_406579_AA1347330

491

3

5.4

53.3

Chloroplast Cytoplasmic

TGACv1_406579_5BL: 19,551–21,635

111

TRIAE_CS42_5BL_TGACv1_406904_AA1351330

457

1

6.1

49.4

Chloroplast

TGACv1_406904_5BL: 33,027–34,745

112

TRIAE_CS42_5BL_TGACv1_408090_AA1361610

374

1

5.3

40.7

Cytoplasmic

TGACv1_408090_5BL: 6001–9585

113

TRIAE_CS42_5BS_TGACv1_424806_AA1391870

444

1

6.2

48.3

PlasmaMembrane Chloroplast

TGACv1_424806_5BS: 5556–7050

114

TRIAE_CS42_5DL_TGACv1_433291_AA1408500

490

1

5.1

52.4

PlasmaMembrane Chloroplast

TGACv1_433291_5DL: 25,092–26,905

115

TRIAE_CS42_5DL_TGACv1_434244_AA1432540

456

1

4.8

50.3

Chloroplast Cytoplasmic

TGACv1_434244_5DL: 7506–11,405

116

TRIAE_CS42_5DL_TGACv1_435855_AA1455600

491

3

5.4

53.5

Chloroplast Cytoplasmic

TGACv1_435855_5DL: 4016–6117

117

TRIAE_CS42_5DL_TGACv1_436083_AA1457870

455

2

5.6

50

Cytoplasmic

TGACv1_436083_5DL:20522–22,605

118

TRIAE_CS42_5DS_TGACv1_456986_AA1480690

506

3

5.1

54.6

Chloroplast

TGACv1_456986_5DS: 56,363–58,465

119

TRIAE_CS42_5DS_TGACv1_457896_AA1490570

454

1

6.5

49.3

PlasmaMembrane Chloroplast

TGACv1_457896_5DS: 16,778–18,475

120

TRIAE_CS42_6AL_TGACv1_471580_AA1511220

492

1

5.8

53.3

Chloroplast Cytoplasmic

TGACv1_471580_6AL: 48,286–50,301

121

TRIAE_CS42_6AL_TGACv1_472815_AA1526300

492

1

5.2

53.7

Cytoplasmic

TGACv1_472815_6AL: 30,598–36,845

122

TRIAE_CS42_6AL_TGACv1_473165_AA1529140

486

2

5.6

53.1

Chloroplast

TGACv1_473165_6AL: 22,571–24,615

123

TRIAE_CS42_6AS_TGACv1_486256_AA1558890

515

1

5.9

56.4

Chloroplast

TGACv1_486256_6AS: 20,827–22,845

124

TRIAE_CS42_6AS_TGACv1_486559_AA1562640

480

1

5.4

52.6

Chloroplast

TGACv1_486559_6AS: 45,174–47,285

125

TRIAE_CS42_6BL_TGACv1_499376_AA1580390

485

1

5.3

53.3

Chloroplast Cytoplasmic

TGACv1_499376_6BL: 125,626–127,400

126

TRIAE_CS42_6BL_TGACv1_499650_AA1588270

377

1

5.9

40.6

Chloroplast

TGACv1_499650_6BL: 164,606–166,056

127

TRIAE_CS42_6BL_TGACv1_499908_AA1594400

483

1

5.1

53.3

Cytoplasmic

TGACv1_499908_6BL: 62,922–65,065

128

TRIAE_CS42_6BL_TGACv1_500434_AA1604570

464

1

6.2

50.1

Cytoplasmic

TGACv1_500434_6BL:47486–50,072

129

TRIAE_CS42_6BL_TGACv1_500839_AA1610500

490

1

4.9

53.2

Cytoplasmic

TGACv1_500839_6BL: 69,656–71,577

130

TRIAE_CS42_6BL_TGACv1_502282_AA1624090

484

1

5.3

53.2

Cytoplasmic

TGACv1_502282_6BL: 7757–9575

131

TRIAE_CS42_6BS_TGACv1_513285_AA1637340

496

1

5.3

52.3

Chloroplast

TGACv1_513285_6BS: 53,840–59,465

132

TRIAE_CS42_6BS_TGACv1_513359_AA1638830

478

1

5

51.8

Chloroplast Cytoplasmic

TGACv1_513359_6BS: 87,396–89,178

133

TRIAE_CS42_6BS_TGACv1_513952_AA1652850

462

1

6.1

49.1

Mitochondrial Chloroplast

TGACv1_513952_6BS: 89,206–91,232

134

TRIAE_CS42_6BS_TGACv1_514318_AA1658270

493

1

4.8

52.3

Cytoplasmic Chloroplast

TGACv1_514318_6BS: 26,417–28,435

135

TRIAE_CS42_6DL_TGACv1_526838_AA1693090

511

1

10.3

57.2

Nuclear

TGACv1_526838_6DL: 83,730–85,630

136

TRIAE_CS42_6DL_TGACv1_526838_AA1693100

527

1

5.5

57.5

Cytoplasmic

TGACv1_526838_6DL: 91,545–93,815

137

TRIAE_CS42_6DL_TGACv1_527354_AA1702670

479

1

5.8

51.7

Chloroplast PlasmaMembrane Cytoplasmic

TGACv1_527354_6DL: 31,226–34,990

138

TRIAE_CS42_6DL_TGACv1_528544_AA1714910

459

1

5.8

49.6

Cytoplasmic

TGACv1_528544_6DL: 22,658–24,474

139

TRIAE_CS42_6DL_TGACv1_528747_AA1715930

388

1

5.2

43.7

Cytoplasmic

TGACv1_528747_6DL: 19,746–21,729

140

TRIAE_CS42_6DL_TGACv1_529217_AA1717790

537

2

6.7

59

Mitochondrial

TGACv1_529217_6DL: 7806–10,055

141

TRIAE_CS42_6DS_TGACv1_542680_AA1727420

511

1

7.3

55.4

Mitochondrial

TGACv1_542680_6DS: 110,916–113,054

142

TRIAE_CS42_6DS_TGACv1_542696_AA1728130

480

1

5.5

52.3

Chloroplast Cytoplasmic

TGACv1_542696_6DS: 29,236–31,123

143

TRIAE_CS42_6DS_TGACv1_543630_AA1742350

484

2

5.3

53

Chloroplast Cytoplasmic

TGACv1_543630_6DS: 21,813–23,926

144

TRIAE_CS42_6DS_TGACv1_543780_AA1744110

496

1

4.8

52.8

Cytoplasmic Chloroplast

TGACv1_543780_6DS: 23,657–25,745

145

TRIAE_CS42_7AL_TGACv1_556001_AA1752070

731

2

8.8

76.5

PlasmaMembrane Mitochondrial

TGACv1_556001_7AL: 5064–14,615

146

TRIAE_CS42_7AL_TGACv1_556001_AA1752080

460

2

5.5

50.7

Chloroplast

TGACv1_556001_7AL: 63,295–65,765

147

TRIAE_CS42_7AL_TGACv1_556054_AA1753810

488

1

5.7

53.3

Cytoplasmic Chloroplast

IWGSC_CSS_7AL_4383366: 4–1333

148

TRIAE_CS42_7AL_TGACv1_556712_AA1769470

419

1

6

45

Chloroplast PlasmaMembrane Cytoplasmic

TGACv1_556712_7AL: 76,829–78,415

149

TRIAE_CS42_7AL_TGACv1_558513_AA1793890

449

1

5.5

49.3

PlasmaMembrane

TGACv1_558513_7AL: 9716–12,339

150

TRIAE_CS42_7AL_TGACv1_559924_AA1801280

467

2

6.1

49.9

Chloroplast PlasmaMembrane

TGACv1_559924_7AL: 15,613–17,418

151

TRIAE_CS42_7AS_TGACv1_570575_AA1837870

507

1

5.5

54.7

Cytoplasmic

TGACv1_570575_7AS: 49,636–52,320

152

TRIAE_CS42_7AS_TGACv1_571539_AA1848450

469

1

5.5

49.9

Chloroplast

TGACv1_571539_7AS: 11,854–13,474

153

TRIAE_CS42_7AS_TGACv1_573368_AA1852750

442

1

5.6

47.6

Chloroplast Mitochondrial

TGACv1_573368_7AS: 816–2486

154

TRIAE_CS42_7BL_TGACv1_576822_AA1856120

402

1

6.9

44

Chloroplast

TGACv1_576822_7BL: 170,238–172,395

155

TRIAE_CS42_7BL_TGACv1_576994_AA1862270

463

1

5.4

50.9

Cytoplasmic PlasmaMembrane Mitochondrial

TGACv1_576994_7BL: 67,842–69,505

156

TRIAE_CS42_7BL_TGACv1_577254_AA1870230

252

1

4.9

26.9

Cytoplasmic Chloroplast Extracellular

TGACv1_577254_7BL: 76,415–77,415

157

TRIAE_CS42_7BL_TGACv1_577547_AA1878460

420

1

7.2

45.2

PlasmaMembrane Chloroplast

TGACv1_577547_7BL: 29,086–30,601

158

TRIAE_CS42_7BL_TGACv1_579457_AA1907470

484

1

5.2

52.7

Chloroplast

TGACv1_579457_7BL: 41,356–43,187

159

TRIAE_CS42_7BS_TGACv1_591871_AA1924040

397

1

5.1

29.3

Cytoplasmic Chloroplast

TGACv1_591871_7BS: 76,246–80,992

160

TRIAE_CS42_7BS_TGACv1_592186_AA1932820

529

1

5

56.5

Chloroplast Cytoplasmic

TGACv1_592186_7BS: 90,491–92,505

161

TRIAE_CS42_7BS_TGACv1_592546_AA1940110

482

1

6.1

52

PlasmaMembrane Mitochondrial

TGACv1_592546_7BS: 65,246–67,190

162

TRIAE_CS42_7BS_TGACv1_593204_AA1949410

497

1

5.3

53.4

Chloroplast

TGACv1_593204_7BS: 13,157–15,085

163

TRIAE_CS42_7BS_TGACv1_593321_AA1950440

465

1

5.8

50

PlasmaMembrane

TGACv1_593321_7BS: 38,716–40,476

164

TRIAE_CS42_7BS_TGACv1_593432_AA1951550

470

1

5.8

51.4

Chloroplast

TGACv1_593432_7BS: 27,150–29,205

165

TRIAE_CS42_7DL_TGACv1_603213_AA1978480

481

1

5.5

52.2

Chloroplast

TGACv1_603213_7DL: 60,111–61,985

166

TRIAE_CS42_7DL_TGACv1_603403_AA1982990

421

1

5.4

43.7

Chloroplast PlasmaMembrane

TGACv1_603403_7DL: 64,856–66,500

167

TRIAE_CS42_7DL_TGACv1_603951_AA1991550

458

1

5.3

49.8

Chloroplast PlasmaMembrane

TGACv1_603951_7DL: 21,366–23,048

168

TRIAE_CS42_7DL_TGACv1_603951_AA1991560

453

1

5.3

49.1

Chloroplast PlasmaMembrane

TGACv1_603951_7DL: 27,012–28,816

169

TRIAE_CS42_7DL_TGACv1_604766_AA2001560

438

1

5.6

47

Mitochondrial Chloroplast

TGACv1_604766_7DL: 35,976–38,150

170

TRIAE_CS42_7DS_TGACv1_621774_AA2025670

478

1

5.2

50.8

Chloroplast

TGACv1_621774_7DS: 76,896–78,775

171

TRIAE_CS42_7DS_TGACv1_622710_AA2044230

489

2

5.3

54.5

Cytoplasmic

TGACv1_622710_7DS: 15,926–17,908

172

TRIAE_CS42_7DS_TGACv1_623144_AA2050000

447

1

5.8

48.4

Cytoplasmic Chloroplast

TGACv1_623144_7DS: 33,046–34,980

173

TRIAE_CS42_7DS_TGACv1_624130_AA2059090

488

1

5.9

52.5

Mitochondrial PlasmaMembrane

TGACv1_624130_7DS: 15,066–16,815

174

TRIAE_CS42_7DS_TGACv1_626811_AA2066910

480

1

5.7

50.7

PlasmaMembrane Chloroplast

TGACv1_626811_7DS: 3831–5558

175

TRIAE_CS42_U_TGACv1_642463_AA2118110

489

1

6.2

52.4

Chloroplast

TGACv1_642463_U: 55,580–57,595

176

TRIAE_CS42_U_TGACv1_642555_AA2119560

296

1

5.3

31.8

Chloroplast Cytoplasmic

TGACv1_642555_U: 31,767–32,735

177

TRIAE_CS42_U_TGACv1_642847_AA2124040

479

1

5.9

51.5

Chloroplast PlasmaMembrane

TGACv1_642847_U: 26,547–28,358

178

TRIAE_CS42_U_TGACv1_644603_AA2140590

673

1

7.6

72.7

Chloroplast

TGACv1_644603_U: 19,926–22,260

179

TRIAE_CS42_U_TGACv1_658309_AA2151750

368

1

8.3

40.7

Chloroplast

TGACv1_658309_U: 1–1355

Phylogenetic analysis of UGTs in wheat

The identified UGTs were subjected to phylogenetic analysis to see their grouping pattern and genetic relationships based on the 18 Arabidopsis UGTs sequences (Additional file 3: Table S2) [20, 22]. The wheat UGTs were clustered into 16 major phylogenetic groups, with a lack of Arabidopsis conserved phylogenetic group K (Fig. 1). The 14 UGT groups (A-N) described initially in Arabidopsis are considered as conserved groups, and all these groups except group K were found in this study [47]. The number of UGTs in each group varied, as group E, the largest of the groups, contained 37 UGT members, while group N, the smallest of the groups, had only one member. The three new groups identified in our study were O, P and Q containing 3, 13 and 36 UGT members, respectively.
Fig. 1
Fig. 1

Phylogenetic analysis of bread wheat UGT family genes. The MUSCLE and MEGA 7 softwares were used for the sequence alignment and construction of the phylogenetic tree using the full length sequences of 179 wheat UGTs and 18 Arabidopsis UGTs

Genome distribution of wheat UGT genes

Based on the current wheat genome annotation information, the genetic mapping of UGT genes on wheat chromosomes was further investigated (Fig. 2). A total of 51, 67, and 61 UGT genes were non-randomly distributed in the A, B and D sub-genomes respectively (Table 1; Fig. 2). The number of UGTs varied from a minimum of 2 UGTs per chromosome to a maximum of 15 UGTs per chromosome among all the sub-genomes. Within the sub-genome A, chromosomes 6 and 2 had the minimum (5) and maximum (10) number of UGTs, respectively, and within sub-genome B, chromosomes 1 and 4 had the minimum (6) UGTs each, and its chromosome 5 had the maximum number (13) of UGTs.
Fig. 2
Fig. 2

Chromosome distribution of 179 wheat UGT genes. The wheat UGTs were distributed among seven chromosomes and each of the 3 sub-genomes A, B and D. The different colored bars represent a chromosome and the name of each chromosome along with its sub-genome is mentioned, on top of each bar

Structure of wheat UGT genes

The exon-intron structure is important to know the possibility of existence of alternative isoforms of a gene product that if so, can contribute to the complexity of cellular constitution and compartmentalization. The UGTs identified in this study were searched for intron existence, intron size and phases of introns (Additional file 4: Table S3). Among the 179 UGT genes identified in this study, 81 UGTs (44.5%) contained introns and among the intron containing UGTs 60, 17 and 4 had 1, 2 and 3 introns, respectively (Additional file 4: Table S3). After mapping the introns to the amino acid sequence alignment, at least 10 intron insertion events numbered I-1 to I-10, as per their position in the protein sequence, were observed (Fig. 3). The intron (I-4) was the most widespread intron found across 38 sequences of wheat UGTs spread across groups A, B, D, E, F, G, H, I, J and Q. The phylogenetic group Q sequences had the highest number (27) of intron insertions, but only 6 different types of introns were found in this group; on the other hand, group A and D shared the highest number (7) of different types of intron insertions (Additional file 4: Table S3). A variable number of intron phases were observed for the UGT protein sequences showing abundance of 0 and 1 phases and scarcity of introns in phase 2. The most abundant phase was 0 (48%), followed by phase 1 (42%) and only 15% were in phase 2 (Additional file 4: Table S3).
Fig. 3
Fig. 3

Distribution of introns among 81 wheat UGT genes. The map represents the intron positions (inverted triangles) and phases (different colors of the inverted triangles) on the amino acid (thick grey lines) residues encoded by the UGT genes. The red, green and blue colors represent the 0, 1 and 2 phases of introns, respectively. The scale on top represents the amino acid count of the UGT genes, and the numbers on the bottom represent the identity of each intron

Expression profiles of wheat UGT genes in various tissues at different developmental stages

To study the expression profiles of UGT genes during the life cycle of the wheat plant, the relative expression of UGT genes in the root, shoot, leaf, spike and grains each at three developmental stages were analyzed as per the Zadoks scale [44]. Using the online high-throughput RNA sequences data, the expression profiles of probes representing 109 wheat UGT genes were found and were further depicted as a heat map (Fig. 4; Additional file 5: Table S4). The specific expression profile at different developmental stages revealed that most of the genes were expressed at a specific time in each tissue. Among all only nine genes showed extensive expression in almost all of the tissues but not in all the developmental stages and two of these genes TRIAE_CS42_1BL_TGACv1_032609_AA0132000 and TRIAE_CS42_4AL_TGACv1_288576_AA0952450 showed the highest expression level in most of the tissues. The expression of most UGT genes varied in each organ at different developmental time course, like in grain, leaf, spike and stem the highest expression occurred at the Z85, Z71, Z39 and Z65 stages, respectively (Fig. 4). It was also noted that the highest number of genes were expressed in roots followed by leaves, stem, grains and spikes. None of the genes, except one in spikes, two in stem and three in roots, showed the highest expression in all three developmental stages of these organs. Over all approximately 57% UGTs were showing relatively high expression in the life cycle of the wheat plant based on this data (Fig. 4).
Fig. 4
Fig. 4

Expression profiles of wheat UGT genes in five different tissues at three different developmental stages. The different colors represent the abundance of the transcripts. The developmental stages are denoted using the Zadoks scale

Expression profiles of wheat UGT genes under Fusarium graminearum treatment

In the present study, expression patterns of the UGT genes in response to F. graminearum strains producing DON or not after 2 and 4 days after inoculation were investigated using the online Affymetrix wheat array data (GSE54554) to study the roles of UGT genes in response to FHB resistance. The expression profile of UGT genes at 2 and 4 days after infection (DAI) compared to the control plants showed a differential expression pattern under infected conditions (Fig. 5; Additional file 6: Table S5). One of the most remarkable observations was that the number of genes showing extensive expression during F. graminearum stress producing DON was almost double that of the number of genes expressed during F. graminearum stress without DON at both 2 DAI and 4 DAI. Among all only 10 genes showed relative higher up-regulation at all circumstances of 2 and 4 DAI except for the control plants, while on the other hand 5 genes were clearly down regulated at all circumstances after F. graminearum inoculation (Fig. 5).
Fig. 5
Fig. 5

Relative expression profiles of wheat UGT genes during Fg-DON and Fg + DON treatment. The wheat spikes were inoculated with the F. graminearum strain that did not produce DON (Fg-DON) as well as with the F. graminearum strain that produced DON (Fg + DON), with water as the control. Relative expression potential of UGT genes is represented by the scale of different colors. The red or green colors represent the higher or lower relative abundance, respectively, of each transcript in each sample

Validation of the expression of UGT genes by RT-qPCR

We employed RT-qPCR to validate the expression profile of the UGT genes in different tissues as well as during F. graminearum inoculation of spikes at different time intervals in wheat. A total of 6 UGT transcript sequences were selected to be used for expression profiling in the root, stem, spike and grains and were further employed for expression profiling of the UGT genes in F. graminearum inoculated spikes. The 6 UGT genes were TRIAE_CS42_4DL_TGACv1_343563_AA1136610, TRIAE_CS42_3B_TGACv1_228792_AA0827590, TRIAE_CS42_1AL_TGACv1_000696_AA0017290, TRIAE_CS42_3DS_TGACv1_274000_AA0934260, TRIAE_CS42_3DL_TGACv1_251733_AA0884380 and TRIAE_CS42_6BL_TGACv1_499376_AA1580390. The leaf tissues relative to the root and stem showed high expression of the 6 selected genes, in addition to a variable expression of the same genes in the leaf tissues (Fig. 6a). The spikelets at three different developmental stages did not show any noticeable expression of the tested genes (Fig. 6a). The transcript accumulation increased in grains with the development of grain maturity and highest expression was noted at the most mature stage (Fig. 6a). When the spikelets were inoculated with F. graminearum at two different time intervals, the results clearly indicated the extensive expression of the selected genes in F. graminearum inoculated spikes compared to the control plants (Fig. 6b-g). The gene TRIAE_CS42_TGACv1_228792_AA0827590 gave the highest relative expression at both time intervals in the F. graminearum inoculated spikes compared to the rest of the genes tested (Fig. 6f).
Fig. 6
Fig. 6

Validation of the expression level of UGTs by qRT-PCR analysis. Expression confirmation assay of the six selected UGT genes were performed in various wheat tissues at different time intervals (a) and under F. graminearum treatment (b-g)

Discussion

The advent of genome sequencing and the availability of global genomic databases have made it possible to examine complex genomes such as wheat in much greater detail. The identification and validation of FHB resistance genes in wheat is one of the major focuses in the current era of molecular investigations, pertaining to high FHB related economic losses and grain contamination due to DON accumulation. Glycosylation is one of the most important modification and detoxification phenomenon of plant secondary metabolites [15, 48]. Glycosylation, mediated by plants’ indigenous UGTs, in addition to various cellular process and maintenance of cellular homeostasis, also plays a potential role in DON detoxification and FHB resistance. UGTs have been identified and analyzed in a few plant species such as Arabidopsis, flax, maize and cotton; however, they have not been identified on a large scale in wheat except in a few individual reports [14, 15, 20, 22].

In the present study we identified 179 putative family-1 UGT genes in wheat based on the Chinese Spring (CS42) reference sequence [40]. The exact number of family-1 UGT genes may be alterable in different wheat cultivars as substantial sequence differences such as nucleotides presence/absence are prevalent among cultivars including wheat. The 179 UGT protein sequences were further subjected to multiple sequence alignment and phylogenetic analysis. The multiple sequence alignment of wheat UGTs clearly showed high sequence divergence, especially at the N-terminus, revealing the diverse roles that UGTs play in the life of plants [15]. In this study, the phylogenetic analysis resulted in 16 different (A-Q) phylogenetic groups with one exception. The conserved group K previously described in other studies was absent in our findings, similarly in another study conserved group C was also not found in Gossypium hirsutum [15]. The loss of a phylogenetic group during evolution suggests either the loss of function or replacement by other factors [15]. In our study group E contained the highest number (37) of UGT genes leading to 21% of the total UGT genes identified in wheat. In Arabidopsis, flax and maize group E had 17, 22 and 35 UGT members, respectively, showing the expansion of group E in different plant species [21, 22]. The new groups O, P and Q were found in this investigation. Group Q, first discovered in maize having only 7 members, while in cotton this group was not found; on contrary, our study showed that group Q was not only found but was the 2nd largest group of UGTs in wheat consisting of 36 members [15, 22].

The UGTs distribution among the chromosomes showed a dispersion of UGTs across all the chromosomes of all the three wheat genomes. A similar pattern of UGTs dispersion was also observed in Arabidopsis and among the three species of cotton [15, 47]. Quantitative trait loci (QTLs) for the resistance to Fusarium head blight have also been found on all wheat chromosomes, and the most stable QTLs related to FHB resistance are supposed to be located on chromosome 3B, 5A and 6B [49], and here we have shown that these chromosomes have as many as 9, 7 and 10 family-1 UGTs, respectively, but the relationship with these QTLs and the exact role of these UGTs in resistance to FHB needs to be further studied. Introns, although do not contribute to protein sequences but their position and phases do affect the protein diversity and overall cellular functioning. Introns relative positions can predict certain clues like how genes and their corresponding proteins evolve and further contribute to the diversification of gene families [22, 50]. A total of 10 different intron insertions were identified in this study, while in other crops such as flax and maize 7 and 9 different introns were found, respectively [20, 22]. Among the 179 identified wheat UGTs, 55% lacked introns which is in accordance with previous reports on Arabidopsis, flax and maize of which 58%, 55% and 60% lack introns, respectively [20, 22, 47]. In our study, intron 5, found across phylogenetic groups A, B, D, E, F, H, I, J and Q, is considered as the most widespread and oldest intron. Similarly, intron 2 in Arabidopsis found in groups F-K, intron 3 and 4 in flax found in groups F-K, and intron 5 in maize found in groups F-J and N are considered the oldest and most widespread introns [20, 22, 47]. Consistent with other findings, we also observed the abundance of phase 0 and 1 introns compared to phase 2 introns [22]. The existence of different UGTs has been shown in various sub-cellular locations such as cytoplasm, vacuoles, endoplasmic reticulum as well as the membrane [5154]. DON accumulates in the cytoplasm, plasma membrane and chloroplasts of plant cells [55], and the UGT protein sequences identified in our study also have divergent sub-cellular localization and might lower DON toxicity if confronted in these organelles.

To better understand the roles of the wheat UGTs during the life cycle of wheat, we performed an expression analysis of online universal microarray data in certain tissues at different developmental stages. The microarray results have revealed probes that specifically match 61% of the identified wheat UGTs, and most of these genes have been expressed at least in a certain tissue during the life cycle of the wheat plant. Similarly, in other crops such as maize and flax it has been shown that 82% and 73% of the corresponding genes showed expression [20, 22]. The genes analyzed in different tissues, as per the microarray results, showed that 13%, 29%, 35%, 9% and 15% of the UGT genes displayed extensive overexpression in grains, leaf, root, spikes and stem, respectively, during all the various stages studied. Using selected UGT gene sequences, RT-qPCR also revealed a differential expression profile in most of the growth stages in certain wheat tissues, suggesting that the UGTs are opting for preferential expression in particular organs during the life cycle of the wheat plant.

FHB is a menace for agriculture crops, especially for wheat growing in the humid regions of the world, and current focus has been placed on understanding the molecular mechanisms behind FHB resistance and the development of germplasms resistant to FHB. It is important to outline the role of the UGTs identified in this study, if any, during the F. graminearum incidence that could further be utilized for the development of resistance against F. graminearum stress. As many other investigators have previously shown the involvement UGTs in host resistance against FHB both in wheat as well as in barley [33, 37]. In our study, the F. graminearum stress responsive genes analyzed using online microarray data revealed some interesting results that were further validated by expression analysis of selected UGT genes using RT-qPCR. The wheat spikes were inoculated with a mutated F. graminearum strain that does not produce DON (Fg-DON) as well as with an F. graminearum strain that produces DON (Fg + DON), with water as the control. An average of 27 and 59% of the UGT genes were up regulated after Fg-DON and Fg + DON inoculation, respectively, compared with the control at 2 DAI. On the other hand, an average of 32 and 69% of the UGT genes displayed up-regulation in the Fg-DON and Fg + DON inoculated plants, respectively, at 4 DAI compared to the control plants. The up-regulation of a high number of UGTs during Fg + DON inoculation is an indication of the wheat indigenous UGTs based DON responsive defense mechanism against FHB. The data also clearly show an extensive up-regulation of a high number of genes on the 4th day after Fg + DON inoculation, showing an increase in response as DON accumulation increases. These results were further confirmed through RT-qPCR amplification of 6 selected UGT genes, where the highest expression was evident at 4 DAI. These genes and validation of the microarray data using a resistant genotype such as Sumai 3 will be the subject of our ongoing research to further dissect the wheat indigenous defense mechanisms and to identify the resistance source underlying F. graminearum infection and DON detoxification.

Conclusions

This study gave a useful insight into the phylogenetic structure, distribution, and expression patterns of family-1 UDP glycosyltransferases of wheat. The results also offer a foundation for future work aimed at elucidating the molecular mechanisms underlying F. graminearum resistance and DON detoxification in one of the world’s most important cereal crops.

Abbreviations

DAI: 

Days after infection

DON: 

Deoxynivalenol

Fg: 

Fusarium graminearum

FHB: 

Fusarium head blight

GT: 

Glycosyltransferase enzymes

PSPG: 

Plant secondary product glycosyltransferase

QTL: 

Quantitative trait loci

UGT: 

UDP glycosyltransferases

Declarations

Funding

This work was partially supported by the National Key Project for the Research and Development of China (2016YFE0112900, 2016YFD0100500), China Agricultural Research System Program (CARS-03), National Natural Science Foundation of China (31561143004), Natural Science Foundation of Jiangsu province, China (BK20170605) and European Union Horizon 2020 Mycokey project (EU678781).

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its Additional files.

Authors’ contributions

HM and YH designed the experiments. YH and DA carried out most of the experiments and analyzed the data. XZ, YZ, LW and PJ assisted in analyzing the data. DA, YH and HM wrote the article. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
Institute of Food Crops, Jiangsu Academy of Agricultural Sciences / Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing, China
(2)
Institute of Biotechnology and Genetic Engineering, The University of Agriculture, Peshawar, Pakistan

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