Open Access

Insight into the AP2/ERF transcription factor superfamily in sesame and expression profiling of DREB subfamily under drought stress

  • Komivi Dossa1, 2, 3,
  • Xin Wei1,
  • Donghua Li1,
  • Daniel Fonceka2, 4,
  • Yanxin Zhang1,
  • Linhai Wang1,
  • Jingyin Yu1,
  • Liao Boshou1,
  • Diaga Diouf3,
  • Ndiaga Cissé2 and
  • Xiurong Zhang1Email author
BMC Plant BiologyBMC series – open, inclusive and trusted201616:171

https://doi.org/10.1186/s12870-016-0859-4

Received: 29 April 2016

Accepted: 21 July 2016

Published: 30 July 2016

Abstract

Background

Sesame is an important oilseed crop mainly grown in inclement areas with high temperatures and frequent drought. Thus, drought constitutes one of the major constraints of its production. The AP2/ERF is a large family of transcription factors known to play significant roles in various plant processes including biotic and abiotic stress responses. Despite their importance, little is known about sesame AP2/ERF genes. This constitutes a limitation for drought-tolerance candidate genes discovery and breeding for tolerance to water deficit.

Results

One hundred thirty-two AP2/ERF genes were identified in the sesame genome. Based on the number of domains, conserved motifs, genes structure and phylogenetic analysis including 5 relatives species, they were classified into 24 AP2, 41 DREB, 61 ERF, 4 RAV and 2 Soloist. The number of sesame AP2/ERF genes was relatively few compared to that of other relatives, probably due to gene loss in ERF and DREB subfamilies during evolutionary process. In general, the AP2/ERF genes were expressed differently in different tissues but exhibited the highest expression levels in the root. Mostly all DREB genes were responsive to drought stress. Regulation by drought is not specific to one DREB group but depends on the genes and the group A6 and A1 appeared to be more actively expressed to cope with drought.

Conclusions

This study provides insights into the classification, evolution and basic functional analysis of AP2/ERF genes in sesame which revealed their putative involvement in multiple tissue-/developmental stages. Out of 20 genes which were significantly up- /down-regulated under drought stress, the gene AP2si16 may be considered as potential candidate gene for further functional validation as well for utilization in sesame improvement programs for drought stress tolerance.

Keywords

Sesamum indicum AP2/ERF Transcription factors Gene expression Drought stress

Background

Sesame (Sesamum indicum L., 2n = 2x = 26) is an oil crop that contributes to the daily oil and protein requirements of almost half of the world’s population [1]. It is a high nutritive value crop thanks to its oil quality and quantity ranging from 40 to 62.7 % [2]. It was reported that sesame contain much compounds that benefit to human health, including antioxidant, antiaging, antihypertensive, anticancer, cholesterol lowering and antimutagenic properties [35]. The global demand for vegetable oils is growing and estimated to reach 240 million tons by 2050 [6]. Sesame is therefore a productive plant which may greatly contribute to meet this demand. However to reach this objective, it is important to alleviate the different constraints that impair the crop productivity. Water deficit or drought considered to be one of the greatest abiotic factors that limit global food production [7] is significantly affecting 64 % of the global land area [8]. Drought is one of the major constraints of sesame production especially because it is mainly grown in arid and semi-arid regions where the occurrence of drought is frequent [9]. The crop is highly sensitive to drought during its vegetative stage and its yield is adversely affected by water scarcity [1012]. In addition, the negative effect of drought stress on the sesame oil quality has been reported [1315].

Osmotic stresses including drought induce a cascade of molecular responses in plants. Many stress-responsive genes are expressed differentially to adapt to unfavorable environmental conditions. Induction of stress-related genes occurs mainly at the transcriptional level. The modification of the temporal and spatial expression patterns of the specific stress-related genes is an important part of the plant stress response [16]. Transcription factors (TFs) act as regulatory proteins by regulating in a synchronized manner a set of targeted genes under their control and consequently enhance the stress tolerance of the plant. Among these transcription factors, the AP2/ERF superfamily constitutes one of the biggest gene families, which contains a typical AP2 DNA-binding domain and is widely present in plants [17]. The AP2/ERF superfamily is involved in response to drought, to high-salt content, to temperature change, to disease resistance, in flowering control pathway and has been analyzed by a combination of genetic and molecular approaches [18].

According to the classification of Sakuma et al. (2002) [19] and later on adopted by several authors [2023], AP2/ERF superfamily includes five subfamilies: (1) AP2 (APETALA2), (2) DREB (dehydration-responsive-element-binding), (3) RAV (related to ABI3/VP), (4) ERF (ethylene-responsive-element-binding-factor), and (5) other proteins (Soloist), based on the number of AP2/ERF domains and the presence of other DNA binding domains. While the AP2 family contains two repeated AP2/ERF domains, the ERF and DREB subfamilies contain a single AP2/ERF domain [24]. The RAV family contains a single AP2/ERF domain and a specific B3 motif [25]. The extensive genomic studies of the AP2/ERF superfamily in Arabidopsis [19, 26], poplar [20], soybean [27], rice [28], grape [20, 23], cucumber [29], hevea [30], castor bean [31], Chinese cabbage [32], foxtail millet [33], Salix arbutifolia [22] and Eucalyptus grandis [23] have provided a better understanding of these TFs. This gene family is highly conserved in plant species although number of gene, functional groups, and gene function could differ according to the species, as a result of independent and different evolution processes. There are many evidences of implication of AP2/ERF genes especially DREBs in drought stress responses in crops [34]. In Arabidopsis, DREB2A and DREB2B are reported to be induced by dehydration [19, 3537]. The soybean GmDREB2 protein has also been reported to promote the expression of downstream genes to enhance drought tolerance in transgenic Arabidopsis [38].

The lack of gene resources associated with drought tolerance hinders genetic improvement in sesame [39]. The recent advances on the sesame genome sequence and the identification of its complement of 27,148 have brought sesame genome research into the functional genomics age [40]. This makes possible genome-wide analysis to find out valuable genes linked to important traits such as drought and to support sesame-breeding programs.

Since little is known about the important AP2/ERF superfamily in sesame, here, we described these TFs and analysed the potential role of DREB subfamily in responses to drought stress. This study will pave the way for the comprehensive analysis and the understanding of the biological roles of AP2/ERF genes in sesame towards the improvement of drought stress tolerance.

Results

Identification and chromosomal location of the AP2/ERF gene superfamily

A total of 132 AP2/ERF genes were confirmed in sesame with complete AP2-type DNA-binding domains ranging from 273 to 5837 bp in length (Table 1; Additional file 1). These genes represent about 0.55 % of the total number of genes in sesame. Based on the nature and the number of DNA-binding domains, they were further divided into four major families namely AP2, ERF, DREB and RAV. Twenty genes were predicted to encode proteins containing double-repeated AP2/ERF domains (AP2 family). Four genes were predicted to encode single AP2/ERF domain, together with one B3 domain (RAV family). One hundred and two genes were predicted to encode proteins containing single AP2/ERF domain (ERF family) including 61 genes assigned to the ERF subfamily and 41 genes assigned to the DREB subfamily. Out of the remaining six genes, four genes (AP2si132, AP2si117, AP2si58 and AP2si131) encoded single AP2/ERF domain distinct from those of the members of the ERF family but were more closely related to those of the AP2 family members. Thus these four genes were then assigned to the AP2 family. Finally, the last two genes (AP2si91 and AP2si96) also contained single AP2 domain which showed a low similarity with the AP2 and ERF families. It was found that they have a high similarity with the amino acid sequence of the Arabidopsis gene “At4g13040” classified as “Soloist”. Therefore, these genes were designated as “Soloist”.
Table 1

Classification of the AP2/ERF superfamily in sesame

Classification

Group

Number

AP2 family

Double AP2/ERF domain

20

Single AP2/ERF

4

domain

ERF family

DREB subfamily

41

A1

9

A2

5

A3

1

A4

10

A5

6

A6

10

ERF subfamily

61

B1

5

B2

4

B3

22

B4

6

B5

19

B6

5

RAV family

 

4

Soloist

 

2

 

Total

132

The names of families, subfamilies and groups were previously reported by Sakuma et al. [19]

Cumulatively, the number of AP2/ERF genes in sesame is slightly lower than the five relative species analyzed: Arabidopsis (147) [19], grape (149) [24], U. gibba (152) [41], tomato (167) [42] and potato (246) [43]. As described for these species relatives, ERF and AP2 families were also overrepresented in the sesame genome. Arabidopsis and sesame have three and two “Soloist” genes respectively while the other four species have only one “Soloist” gene in their genomes. The Fig. 1 summarizes the AP2/ERF superfamily members detected in grape, tomato, potato, Arabidopsis, Utricularia gibba and sesame.
Fig. 1

Phylogeny of the six species and repartition of the AP2/ERF families

The localization of the AP2/ERF genes revealed that they are distributed unevenly distributed on the 16 Linkage Groups (LGs). The precise position (in bp) of each AP2/ERF on the sesame LGs is detailed in Additional file 1. Six genes (AP2si127, AP2si128, AP2si129, AP2si130, AP2si131 and AP2si132) were not mapped because they were located on the unanchored scaffolds (Table 2). The largest number of genes (17; 12.88 %) was found on LG1, whereas LG14 and LG16 have only one gene (0.76 %). The two “Soloist” genes were mapped on the same LG9 (Fig. 2). The distribution pattern of these genes on some LGs pointed out some regions with relatively high accumulation of AP2/ERF genes in cluster. This can be observed in the LG1, LG3, LG4, LG8 and LG12. In overall, each LG had a mixture of the different families except LG11 and LG12 which only contained ERF genes.
Table 2

Summary of the AP2/ERF genes identified in the sesame genome

Gene Name

Locus ID

Linkage Group

Family

Group

ORF length (bp)

Gene Name

Locus ID

Linkage Group

Family

Group

ORF length (bp)

AP2si1

SIN_1009471

LG1

ERF

B2

1176

AP2si67

SIN_1018537

LG6

ERF

B3

717

AP2si2

SIN_1009557

LG1

ERF

A4

678

AP2si68

SIN_1018539

LG6

ERF

A4

678

AP2si3

SIN_1009621

LG1

ERF

B5

564

AP2si69

SIN_1020950

LG6

ERF

B5

624

AP2si4

SIN_1010767

LG1

ERF

B5

537

AP2si70

SIN_1023331

LG6

ERF

B5

714

AP2si5

SIN_1010804

LG1

AP2

 

996

AP2si71

SIN_1006144

LG7

RAV

 

1059

AP2si6

SIN_1013634

LG1

RAV

 

1065

AP2si72

SIN_1008777

LG7

ERF

A2

1080

AP2si7

SIN_1013660

LG1

ERF

B5

1074

AP2si73

SIN_1009173

LG7

ERF

B5

1119

AP2si8

SIN_1013661

LG1

ERF

B5

678

AP2si74

SIN_1009317

LG7

AP2

 

1971

AP2si9

SIN_1013877

LG1

ERF

B3

546

AP2si75

SIN_1009337

LG7

ERF

A2

600

AP2si10

SIN_1013878

LG1

ERF

B3

576

AP2si76

SIN_1011553

LG7

ERF

A2

639

AP2si11

SIN_1013899

LG1

ERF

A4

861

AP2si77

SIN_1006545

LG8

ERF

B6

1038

AP2si12

SIN_1014016

LG1

ERF

B6

819

AP2si78

SIN_1006598

LG8

AP2

 

621

AP2si13

SIN_1017801

LG1

ERF

A1

564

AP2si79

SIN_1011988

LG8

ERF

B3

474

AP2si14

SIN_1017805

LG1

ERF

A1

669

AP2si80

SIN_1011989

LG8

ERF

B3

501

AP2si15

SIN_1017959

LG1

ERF

B5

990

AP2si81

SIN_1011991

LG8

ERF

B3

441

AP2si16

SIN_1017978

LG1

ERF

A6

894

AP2si82

SIN_1014868

LG8

ERF

B4

837

AP2si17

SIN_1021559

LG1

ERF

A4

732

AP2si83

SIN_1019697

LG8

ERF

A6

1104

AP2si18

SIN_1005434

LG2

ERF

A5

450

AP2si84

SIN_1026397

LG8

ERF

A6

804

AP2si19

SIN_1013217

LG2

ERF

A5

729

AP2si85

SIN_1026398

LG8

ERF

B5

783

AP2si20

SIN_1013368

LG2

ERF

B4

1254

AP2si86

SIN_1026408

LG8

ERF

B4

768

AP2si21

SIN_1017047

LG2

AP2

A6

1146

AP2si87

SIN_1026470

LG8

RAV

 

1050

AP2si22

SIN_1017255

LG2

ERF

A4

525

AP2si88

SIN_1026594

LG8

ERF

B5

1257

AP2si23

SIN_1018060

LG2

ERF

B5

1173

AP2si89

SIN_1005162

LG9

ERF

A6

969

AP2si24

SIN_1018312

LG2

RAV

 

1125

AP2si90

SIN_1010530

LG9

ERF

A1

645

AP2si25

SIN_1018336

LG2

ERF

B5

1065

AP2si91

SIN_1010676

LG9

Soloist

 

684

AP2si26

SIN_1018337

LG2

ERF

B5

636

AP2si92

SIN_1010728

LG9

ERF

B6

837

AP2si27

SIN_1021103

LG2

AP2

 

1191

AP2si93

SIN_1014969

LG9

ERF

B4

1134

AP2si28

SIN_1023829

LG2

AP2

 

1473

AP2si94

SIN_1024041

LG9

ERF

A1

660

AP2si29

SIN_1023944

LG2

AP2

 

1062

AP2si95

SIN_1024170

LG9

AP2

 

1404

AP2si30

SIN_1010313

LG3

ERF

A4

648

AP2si96

SIN_1024299

LG9

Soloist

 

669

AP2si31

SIN_1010442

LG3

AP2

 

1680

AP2si97

SIN_1024507

LG9

AP2

 

1377

AP2si32

SIN_1011351

LG3

AP2

 

1674

AP2si98

SIN_1001618

LG10

ERF

B3

393

AP2si33

SIN_1011410

LG3

ERF

A5

468

AP2si99

SIN_1001619

LG10

ERF

B3

405

AP2si34

SIN_1015264

LG3

AP2

 

1779

AP2si100

SIN_1001620

LG10

ERF

B3

711

AP2si35

SIN_1015746

LG3

ERF

A6

993

AP2si101

SIN_1010169

LG10

ERF

B5

1029

AP2si36

SIN_1017548

LG3

ERF

B2

1182

AP2si102

SIN_1017733

LG10

AP2

 

1026

AP2si37

SIN_1021800

LG3

ERF

B3

642

AP2si103

SIN_1019010

LG10

ERF

A6

1218

AP2si38

SIN_1021880

LG3

ERF

B5

570

AP2si104

SIN_1026203

LG10

ERF

B2

810

AP2si39

SIN_1021925

LG3

ERF

A6

873

AP2si105

SIN_1005694

LG11

ERF

B5

948

AP2si40

SIN_1021932

LG3

ERF

B5

516

AP2si106

SIN_1008520

LG11

ERF

A4

759

AP2si41

SIN_1022039

LG3

ERF

B4

792

AP2si107

SIN_1012983

LG11

ERF

A1

567

AP2si42

SIN_1001671

LG4

ERF

B3

579

AP2si108

SIN_1024656

LG11

ERF

A5

675

AP2si43

SIN_1001908

LG4

AP2

 

2094

AP2si109

SIN_1024820

LG11

ERF

A4

732

AP2si44

SIN_1006214

LG4

ERF

A2

867

AP2si110

SIN_1005299

LG12

ERF

B1

451

AP2si45

SIN_1007132

LG4

AP2

 

1338

AP2si111

SIN_1005300

LG12

ERF

B1

753

AP2si46

SIN_1012110

LG4

ERF

A2

1095

AP2si112

SIN_1005329

LG12

ERF

B3

435

AP2si47

SIN_1012139

LG4

ERF

A3

1023

AP2si113

SIN_1005330

LG12

ERF

B3

795

AP2si48

SIN_1016446

LG4

ERF

B5

1197

AP2si114

SIN_1014405

LG12

ERF

B1

708

AP2si49

SIN_1016588

LG4

ERF

A1

507

AP2si115

SIN_1014559

LG12

ERF

A6

1059

AP2si50

SIN_1016589

LG4

ERF

A1

678

AP2si116

SIN_1003959

LG13

ERF

A5

369

AP2si51

SIN_1016611

LG4

ERF

B6

930

AP2si117

SIN_1003961

LG13

ERF

 

585

AP2si52

SIN_1016730

LG4

ERF

B3

690

AP2si118

SIN_1004087

LG13

AP2

 

1515

AP2si53

SIN_1016731

LG4

ERF

B3

963

AP2si119

SIN_1004332

LG13

ERF

A6

1110

AP2si54

SIN_1016732

LG4

ERF

B3

684

AP2si120

SIN_1004964

LG14

ERF

B1

684

AP2si55

SIN_1005501

LG5

AP2

 

1395

AP2si121

SIN_1004866

LG15

AP2

 

1545

AP2si56

SIN_1007557

LG5

ERF

A5

660

AP2si122

SIN_1004869

LG15

ERF

B4

273

AP2si57

SIN_1013461

LG5

ERF

A4

807

AP2si123

SIN_1007981

LG15

AP2

 

1152

AP2si58

SIN_1023649

LG5

AP2

 

789

AP2si124

SIN_1008036

LG15

ERF

B6

1140

AP2si59

SIN_1009676

LG6

ERF

B3

492

AP2si125

SIN_1025656

LG15

AP2

 

1950

AP2si60

SIN_1009677

LG6

ERF

B3

720

AP2si126

SIN_1016948

LG16

ERF

B1

666

AP2si61

SIN_1009815

LG6

AP2

 

1026

AP2si127

SIN_1002608

NA

ERF

B3

525

AP2si62

SIN_1012570

LG6

ERF

B2

756

AP2si128

SIN_1002609

NA

ERF

B3

801

AP2si63

SIN_1015461

LG6

ERF

B5

1071

AP2si129

SIN_1002610

NA

ERF

B3

648

AP2si64

SIN_1015594

LG6

ERF

A4

532

AP2si130

SIN_1002670

NA

ERF

A1

612

AP2si65

SIN_1015595

LG6

ERF

A1

630

AP2si131

SIN_1000334

NA

AP2

 

1182

AP2si66

SIN_1018534

LG6

ERF

B3

765

AP2si132

SIN_1000313

NA

AP2

 

1182

Fig. 2

Mapping of sesame AP2/ERF genes based on their physical positions. Vertical bars represent linkage groups (LG) of the sesame genome. The LG numbers are indicated at the top of each LG. The scale on the left is in megabases

Phylogenetic analysis and mapping of orthologous genes

Two Maximum Likelihood (ML) trees were constructed, the first resulting from the alignments of only AP2/ERF domains of the 132 protein sequences in sesame; the second ML tree resulted from the alignments of 202 full length protein sequences including 132 AP2/ERF in sesame and 70 protein sequences selected from each family of AP2/ERF reported in the 5 relative species (12 in tomato, 13 in U. gibba, 5 in potato, 31 in Arabidopsis and nine in grape). In the first ML tree, all genes of AP2 family were clearly distinguished from those of the ERF family. The RAVs and Soloists appeared to be more close to the AP2 family (Additional file 2). The second ML tree was constructed to precisely dissect the functional groups within each subfamily according to Arabidopsis AP2/ERF genes which have been investigated extensively. The un-rooted tree divided the AP2/ERF genes into 15 major groups (Fig. 3). We found 6 groups (A1-A6 and B1-B6) within DREB and ERF subfamilies, respectively. In contrast to the DREB subfamily groups which clustered together, strangely, the ERF subfamily genes formed two clades intervened by DREB: one gathered B1, B2, B3, and B4 and the other gathered B5 and B6. The number of genes belonging to each group is reported in the Table 1 and more in details in Table 2.
Fig. 3

Maximum likelihood tree of AP2/ERF proteins in sesame, Arabidopsis, Utricularia gibba, grape, potato and tomato. Bootstrap values ≥ 50 % are shown

In addition, we performed a genome-wide comparative analysis to identify the orthologous AP2/ERF transcription factors between sesame, Arabidopsis, grape and tomato (Fig. 4). Largest orthology of AP2/ERF genes in sesame was found with tomato (38) followed by Arabidopsis (24) and least with grape (13). The orthologous gene pairs and localization in each genome are presented in Additional file 3. All the four families were represented in the orthologous gene pairs and distributed throughout all the LGs except the LG16. Out of the 24 gene pairs between sesame and Arabidopsis, 15 of Arabidopsis AP2/ERF genes retained one copy, three genes (AT1G13260, AT1G15360 and AT5G51990) retained two copies and only one gene (AT3G54320) conserved a tripled copy in sesame genome. Inversely, two genes in sesame (AP2si6 and AP2si13) preserved two copies and 22 genes retained one copy in Arabidopsis genome. In summary, 22 AP2/ERF genes in sesame have 15 corresponding genes in Arabidopsis genome. When compared with tomato, it was revealed that nine genes retained two copies while 20 genes retained one copy in the sesame genome. Similar to Arabidopsis, orthologous genes of grape also showed the retention of one, two and three copies patterns of genes in sesame genome. Interestingly, four sesame genes (AP2si27, AP2si29, AP2si61 and AP2si78) belonging to the AP2 family, found their orthologous counterpart in tomato, grape and Arabidopsis at once. In overall, the results of the orthologs analysis and the phylogenetic relationships between sesame and its relatives were consistent with some orthologous genes found to be closely located in the tree.
Fig. 4

Orthologous relationships of AP2/ERF genes between a sesame and Arabidopsis; b sesame and tomato; c sesame and grape genomes. Green bars represent the chromosomes of each pair of species. “LG” represents the linkage groups of sesame genome and “Chr” represents the chromosomes of the other species genomes

Based on the accumulated evidences indicating that the AP2/ERF proteins are involved in various abiotic stress responses and then could help in marker-aided breeding, we performed SSR search in all of AP2/ERF genes in sesame. The analysis yielded 91 SSR markers distributed throughout the LGs. Twelve genes yielded two SSRs and no SSR marker was found in 47 AP2/ERF genes (Additional file 4). Surprisingly, only two SSR motif types were retrieved including trinucleotide motif (90.91 %) and hexanucleotide motif (8.91 %). These markers developed, would be useful in genotyping and MAS for sesame improvement towards abiotic stresses.

Gene structure and conservative motifs distribution analysis of AP2/ERF genes

To gain insights into the structural diversity of the AP2/ERF genes, we constructed a phylogenetic tree with the full length protein sequences of the four families and displayed the exon/intron organization in the coding sequences by comparing their ORFs with their genomic sequences (Fig. 5). Sesame AP2/ERF genes contained 1 to 10 exons with nearly 70 % of intronless genes. The schematic structures revealed that most of the ERF genes have 1 exon except the genes AP2si1, AP2si3, AP2si4, AP2si20, AP2si36, AP2si38, AP2si40, AP2si41, AP2si60, AP2si62, AP2si69, AP2si86, AP2si93, AP2si111 and AP2si116 which have exactly two exons. The four RAV genes also possess only one exon with similar lengths. Unlike the ERF genes, the coding sequences of the AP2 genes are disrupted by many introns with the number of exons ranging from three (AP2si58) to ten (AP2si121, AP2si118, AP2si97, AP2si95, AP2si55, AP2si31). One exceptional case is the gene AP2si117 which displayed only one exon. Finally, the two “Soloist” genes showed exactly six exons, distributed in similar regions of the genes. Besides the consistency with the phylogenetic analysis, we found that the genes that clustered in the same group displayed similar exon–intron structures, differing only in intron and exon lengths. This can be observed in the first clade of ERF which gathered 5 genes (AP2si3, AP2si4, AP2si38, AP2si40 and AP2si69) displaying 2 exons. However, this is not the case for all close gene pairs. For instance, the gene AP2si117 with only one exon occurred in the same cluster with the genes AP2si45, AP2si55, AP2si95, AP2si97, AP2si131, AP2si132 and AP2si121 which displayed more than eight exons.
Fig. 5

Gene structures of 132 AP2/ERF proteins according to each family. Exons and introns are represented by colored boxes and black lines, respectively

In addition, to investigate the motifs shared by related proteins in the different families, the MEME motif search tool was employed and the motifs found were then subjected to SMART annotation and confirmed in Pfam database. In total, 15 conserved motifs were identified, lengths ranging from 11-50 amino acids (Additional file 5). The motifs 1, 2, 3 and 5 specifying the AP2 domain were identified in all the 132 AP2/ERF proteins while the motif 12 related to B3 domain was found in the four RAV genes (Additional file 6). However, the remaining motifs were unidentified when searched by SMART and Pfam databases. We further analyzed the motifs other than the AP2/ERF conserved domain existing in some ERF/DREB functional groups based on the conserved motifs described by Nakano et al. [26]. The results showed that although small amino-acids vary slightly, sesame ERF/DREB groups are characterized by the same conserved motifs identified by Nakano et al. [26] in Arabidopsis and rice (Additional file 7). This indicated the good conservation of this gene family in plant species. The phylogenetic tree and the motifs dissection results were consistent because most of the closely related members in the phylogenetic tree had common motifs composition and organization (Fig. 6).
Fig. 6

Motifs identified by MEME tools in sesame AP2/ERF protein sequences according to each family. Fifteen motifs were identified and indicated by different colors. Motif location was showed

Tissue-specific expression profiling of AP2/ERF genes and drought stress responses of DREB subfamily genes

Transcriptome data from three tissue samples namely root, leaf and stem were used for identifying genes differentially expressed in these tissues. Heat maps were generated according to the different AP2/ERF subfamilies based on the RPKM values for each gene in all tissue samples (Fig. 7). Apart from AP2si47 gene that was not expressed across the tissues, all AP2/ERF genes displayed very diverse expression. In general, it is observed that gene expression patterns were almost conserved within subfamilies, although expression levels of specific members could be changed from tissue to tissue. The ERF family exhibited the highest expression in all tissues. Similarly, high expressions of two members (AP2si6 and AP2si24) of the RAV family were shown in all tissues while the two remaining members displayed a relatively low expression level. The AP2 family expression levels were lower than most of other AP2/ERF genes. In general, majority of genes displayed a higher expression in the root compared to other tissues. Furthermore, 84.73 % of TFs (111) were expressed in all tissues suggesting a control of a broad set of genes at transcriptional level. The AP2 genes AP2si131, AP2si31 and AP2si27 exhibited stem-specific expression; the ERF gene AP2si115 exhibited root-specific expression while no specific gene was expressed in leaf (Fig. 7). The genes AP2si6 and AP2si24 (RAV family); AP2si36, AP2si54, AP2si127 and AP2si129 (ERF subfamily) were found to be constitutively expressed at a relatively high levels in all the three tissues.
Fig. 7

Expression profile analysis of AP2/ERF genes in sesame tissues according to each family. a ERF. b AP2 family c RAV and Soloist families d Venn diagram depicting the distribution of shared expressed AP2/ERF genes among sesame tissues. Transcriptome data were used to measure the expression level of AP2/ERF genes in roots, stem tip and leaves. The color scale for expression values is shown

qRT-PCR was used to analyze the expression profiles of DREB genes under drought stress condition. As shown in Fig. 8, an overall differential expression patterns were observed among the genes. Twenty-three DREB genes were up-regulated under drought stress including 13 genes with more than 2-fold rate increase of expression level (p value <0.01), suggesting that these genes might play some important roles in the regulation of drought stress in sesame. More remarkably, the gene AP2si16 belonging to the DREB6 group, significantly exhibited the highest expression level with more than 16-fold rate increase. The genes AP2si90 (DREB1), AP2si13 (DREB1), AP2si84 (DREB6), AP2Si106 (DREB4), AP2si35 (DREB6), AP2si116 (DREB5), AP2si49 (DREB1) and AP2si39 (DREB6) also displayed strong expression levels (from 3 to 8-fold rate increase). In contrast, the 3-days of drought stress has decreased the transcript abundance of 18 (44 %) DREB genes. Four genes namely AP2si115 (DREB6), AP2si47 (DREB3), AP2si103 (DREB6) and AP2si11 (DREB4) were the most repressed ones with more than 10-fold decrease of expression levels. In overall, DREB groups show acute responses to drought and might related to sesame drought tolerance knowing that the material used in the qRT-PCR is a strong drought tolerant accession.
Fig. 8

DREB genes induction rates in sesame roots during 3 days of drought stress in comparison to control condition. Transcripts abundance was quantified through qRT-PCR and the experimental values were normalized using sesame actin7 as reference gene. The mean values issued from three independent biological replicates were analysed for significance using the statistical t-test (p value <0.01). The histograms represent the relative expression values of induction rates (stress/control). The green bars represent the most up-regulated genes, the pink bars represent the genes moderately up-regulated and the red bars represent the down-regulated genes. * means significant 2-fold rate increase in gene expression (stress/control)

Discussion

In this study, 132 AP2/ERF family genes were identified in the sesame genome. Compared to the five related species, sesame harbors the lowest number of AP2/ERF genes. Sesame was estimated to have diverged from the tomato-potato lineage approximately 125 MYA (million years ago) and from U. gibba approximately 98 MYA [40]. Moreover, genome analysis showed that both U. gibba and sesame had undergone recent duplication events (WGD). The relatively low number of AP2/ERF genes found in sesame genome is surprising, knowing on one hand that, sesame is relatively tolerant to drought and many other abiotic stresses [44] compared to the 5 related species and in the other hand, the role of AP2/ERF genes in response to abiotic stresses in plants. This suggests the possibility of a gene loss event, which often follows WGD, during the evolutionary process of sesame. Similar assumptions were posited in castor bean which also naturally displays a strong tolerance to diverse environmental stresses but contains small AP2/ERF superfamily members [31]. We further compared the members of each subfamily between sesame and U. gibba and found that genes loss might occur mainly in ERF and DREB subfamilies.

According to the classification of [19], the AP2 family members should have had two AP2/ERF domains. However, in this study, it was discordant that 4 genes namely AP2si132, AP2si117, AP2si58 and AP2si131 with only one AP2/ERF domain were classified in the same group as the “real” AP2 family members. Recently, many authors reported similar results regarding the AP2 family members with only one AP2/ERF domain (four genes found in Arabidopsis [26]; five in tomato [42]; seven in hevea [30]; five in Brassica rapa [45]; three in switchgrass [46]. This implies more detailed analysis in the AP2 family is needed for a new classification approach.

Using phylogeny approach may afford insights into genes function and facilitate the identification of orthologous genes assuming that, genes with conserved functions show a tendency to cluster together. This approach has been widely applied for prediction of the functions of AP2/ERF proteins in many plant species such as grape, foxtail millet, Brassica, rice [33]. The proximity of the RAV and Soloist genes to the AP2 family found in this study was recently reported in switchgrass [46]. Moreover, the ML tree based on the AP2/ERF protein sequences of the 6 species displays particular pattern with 2 clades of the ERF subfamily groups failing to cluster together as found by Song et al. [32]; Lata et al. [33]; Rao et al. [22]. Further in-depth in silico analysis is requisite for finding the possible reasons for such observations [33].

Based on the phylogenetic tree, different functions could be assigned to the AP2/ERF groups in sesame. For instance, the group B6 including five sesame ERF genes, clusters together with the Arabidopsis gene RAP2.11 known to be involved in plant response to low-potassium conditions [47]. We speculated that these five genes might have similar functions. The Group A2 included five sesame genes (AP2si44, AP2si46, AP2si72, AP2si75 and AP2si76) and was close to the well-studied gene DREB2A in Arabidopsis involved in responses to water stress and heat stress [34]. Hence, it is possible to hypothesize that these genes might be involved in similar activities. Likewise, individual gene function could also be predicted based on the close relationships between sesame and Arabidopsis through the homolog-based gene function prediction. For example, the gene AP2si55 belonging to the AP2 family might play similar role as its ortholog AT4G36920 from Arabidopsis involved in the floral identity specification as well as development of the ovule and seed coat [48, 49].

Gene expression patterns can also provide important clues for gene function prediction [50]. The tissue-specific expression profiling showed that most of the AP2/ERF genes are expressed in all sesame tissues analyzed. However, a higher expression was detected in sesame root and similar results were reported in castor bean [31], Chinese cabbage [32] and foxtail millet [33]. The ERF, RAV and Soloist family members displayed higher expression in sesame tissues than AP2 family members indicating that these families might play a central role in tissues development and sesame plant growth [32].

The variability in expression patterns of sesame DREB genes observed in this study indicated that they might be involved in different regulation pathways for drought stress response. Moreover, we observed that the genes from the same group could be expressed differently in response to drought stress and, therefore, are thought to have different functions. Expression analyses of DREB genes also showed unusual and plausible roles for some group members during drought stress. This is the case of the DREB6 group members which functions are scarcely reported in the literature [51]. Out of the ten members of this group, seven were highly up-regulated, pinpointing their importance in drought stress response in sesame. In the same line, the DREB1 genes are mostly known as cold response genes [52, 53]; however, as reported by some authors [5356] and confirmed in our study (seven genes up-regulated vs three down-expressed), these genes are highly involved in drought stress response pathways in sesame knowing that sesame is not cold areas crop but grown in arid and semi-arid areas. Hence, these functional DREB groups might probably participate in the relative drought tolerance naturally exhibited by sesame. Intriguingly, it is noteworthy that, the DREB2 genes which are well described in many crops as actively involved in drought response pathways [35, 36, 57, 58] do not seem to be highly expressed in our study. This uncommon feature may indicate that this group’s members might be involved principally in the regulation of other stress transduction pathways in sesame. Knowing sesame as a survivor crop mainly grown in marginal areas with the occurrence of high temperatures and frequent drought, we may hypothesize from our results that, sesame has probably oriented and dedicated a large part of its DREB group’s members to regulate its main abiotic stresses especially drought. The strongly up-regulated gene identified in this study (AP2si16) is the ortholog of AT1G64380 in Arabidopsis, described as responsive to the chitin treatment, a main elicitor of the plant defense response against pathogens [59]. This indicates possible new functions of this gene which plays essential role in abiotic stress tolerance in plant and may be an excellent candidate for the engineering of sesame breeding with improved drought stress tolerance.

Conclusions

To the best of our knowledge, no study has been conducted on the AP2/ERF superfamily in sesame to date. Therefore, this is the first comprehensive study on these TFs in sesame aiming to help elucidating the genetic basis for the stress adaptation of sesame especially for drought tolerance. One hundred and thirty two AP2/ERF genes were identified in the sesame genome including all families previously reported in the AP2/ERF superfamily. In addition, the expression patterns described together with the comparison of homologs from other species can provide a basis for identifying the roles of the different members of sesame AP2/ERF genes. Hence, further works should rely on these gene resources to characterize candidate genes to improve tolerance to major abiotic constraints of sesame production.

Methods

Data resources and AP2/ERF superfamily transcription factor identification in sesame

AP2/ERF genes and proteins sequences of Arabidopsis thaliana, Vitis vinifera, Solanum lycopersicum, Solanum tuberosum and Utricularia gibba were downloaded from the Plant Transcription Factor DataBase (http://planttfdb.cbi.pku.edu.cn/) [41]. In addition, the sesame genome and proteome were downloaded from the Sinbase (http://ocri-genomics.org/Sinbase/) [60]. The phylogeny data of the six species were downloaded from NCBI Taxonomy common tree (http://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi).

The Hidden Markov Model (HMM) profile of the AP2/ERF domain (PF00847) was obtained from Pfam v28.0 database (http://pfam.xfam.org/) [61] and searched against the sesame proteome using Unipro UGENE [62]. A total of 132 AP2/ERF proteins were obtained as candidate AP2/ERF genes. To further confirm these candidate genes, their amino acid sequences were explored on the Pfam database (http://pfam.xfam.org/search) and the Simple Modular Architecture Research Tool (SMART) [63] based on the conserved domain, to ensure the presence of AP2/ERF domain in each candidate protein.

Chromosomal location, Gene structure and Motif identification of AP2/ERF genes

The physical positions of the identified AP2/ERF genes in sesame were searched on the Sinbase and mapped onto the 16 Linkage Groups (LGs) of sesame genome using MapChart 2.3 [64]. A structural figure of sesame AP2/ERF genes, including the numbers and locations of the exon and intron, was constructed based on Sinbase information and displayed using the Gene Structure Display Server (GSDS 2.0) web-based bioinformatics tool (http://gsds.cbi.pku.edu.cn/) [65]. The motif identification of sesame AP2/ERF protein sequences was performed using a motif-based sequence analysis tool, MEME Suite version 4.10.2 [66] with the following parameters: the optimum width of amino acid sequences was set from 6 to 50, the maximum number of motifs to 15, the number of repetitions to “any number” and all other parameters set at default. The amino acid sequences of the 15 motifs identified by MEME Suite were searched on Pfam database to find out the AP2/ERF motifs and their sequences logo were generated.

Alignment, phylogenetic analysis and identification of microsatellite markers in sesame AP2/ERF genes

A single alignment of sesame AP2/ERF domain sequences and a multiple alignment analysis of the amino acid sequences of the AP2/ERF genes in sesame, Arabidopsis, grape, tomato, potato and Utricularia gibba were conducted using the Clustal W program built in the MEGA 6.0 software [67] with a gap open penalty of 10 and gap extension penalty of 0.2. Alignments were displayed using BoxShade (http://www.ch.embnet.org/software/BOX_form.html) (Additional file 8) and un-rooted Maximum-Likelihood (ML) trees were constructed in MEGA 6.0 software with a 1000 bootstrap value. Combining the phylogenetic trees with the conserved domain analysis, the AP2/ERF genes in sesame were classified into several subfamilies and groups according to [18]. Furthermore, the web based software Websat (http://wsmartins.net/websat/) [68] was used to identify simple sequence repeats (SSRs) in the predicted 132 AP2/ERF genes in sesame with the following parameters: two to six nucleotide motifs were considered, and the minimum repeat unit was defined as five reiterations for dinucleotides and four reiterations for other repeat units.

Comparative mapping of orthologous AP2/ERF genes in sesame, Arabidopsis, tomato and grape

The amino acid sequences of the predicted AP2/ERF proteins were BLASTp searched against protein sequences of Arabidopsis, tomato and grape in NCBI. Hits with E-value ≥ 1e-40 and at least 75 % homology were considered significant [69]. The comparative orthologous relationships of AP2/ERF genes among the four species were illustrated using Circos program [70].

Tissue-specific expression profiling using RNA-seq and qRT-PCR analysis of AP2/ERF genes under drought stress

To analyze the expression patterns of AP2/ERF genes in sesame, different transcriptome data from root, stem tip, and leaf previously obtained by our group were used. These data were downloaded from SesameFG (http://www.ncgr.ac.cn/SesameFG). The analysis were performed using Cluster3.0 (http://bonsai.hgc.jp/~mdehoon/software/cluster/software.htm), and reads per kilobase per million mapped reads (RPKM) values for each gene in all the tissue samples were log10 transformed. Finally, a heat map was generated by Multi Experiment Viewer (MEV) [71].

Plant materials and stress treatment

A sesame accession highly tolerant to drought “ZZM5396” was obtained from the China National Genebank, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences. Plants were grown in pots containing loam soil mixed with 10 % of added compound fertilizer and were kept in a greenhouse. The experiment was carried out in triplicate at the experimental field of Oil Crops Research Institute, Wuhan (China), with 3 plants kept per pot. The plants were regularly irrigated until early flowering stage and the drought stress was applied by withholding water for 3 days when the plant leaves began wilting. Meanwhile, the control plants were maintained under regular irrigation during all the experiment. The roots of the seedlings were harvested at the third day of stress for both stressed plants and control plants. The samples harvested from three individual plants and pooled were frozen immediately in liquid nitrogen and conserved in -80 °C until further use.

RNA extraction and qRT-PCR analysis

Total RNA was isolated from roots of the 3-day stressed and unstressed sesame seedlings and cDNA library was constructed according to the procedure described by [72].

The DREB subfamily genes are widely reported to be involved in drought stress tolerance in many plants [56, 73]. Hence, this subfamily was retained for gene expression analysis under drought stress in our study. The specific primers for the 41 DREB genes were designed using the Primer Premier 5.0 [74] (Additional file 9). Expression of all sesame DREB subfamily genes was detected by qRT-PCR in triplicate and the sesame actin7 (SIN_1006268) gene was used as an internal control [1]. The 2-ΔΔCt method was applied to calculate the change in expression of each gene [75].

Statistical analysis

To analyze the statistical difference between the expressions of target genes, univariate analysis of variance (ANOVA) with t-test procedure was conducted using R 2.15.2, an open-source software.

Abbreviations

AP2/ERF, APETALA 2/ethylene-responsive element binding factor; DREB, dehydration-responsive element binding protein; HMM, Hidden Markov Model; MAS, marker assisted selection, MEME, multiple em for motif elicitation; ML, maximum likelihood; MYA, million years ago; NCBI, National Center for Biotechnology Information; qRT-PCR, quantitative real time PCR; RAP2, related to AP2; RAV, related to ABI3/VP1; RPKM, reads per kilobase per million mapped reads; TF, transcription factor; WGD, whole-genome duplication; WGT, whole-genome triplication

Declarations

Acknowledgments

We sincerely thank Ms. Pan Liu for laboratory assistance and Ms. Soohyun Kang for the language editing on the manuscript.

Funding

This work was funded by the China Agriculture Research System (CARS-15), Core Research Budget of the Non-profit Governmental Research Institution (1610172014003) and Agricultural Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2013-OCRI).

Availability of data and materials

The data sets supporting the conclusions of this article are included within the article and its additional files. The raw RNA-seq reads are available at SesameFG (http://www.ncgr.ac.cn/SesameFG).

Authors’ contributions

KD and XW carried out the bioinformatics, data analysis and drafted the manuscript. DL helped in the gene expression experiment. YZ and LW provided transcriptome data and contributed in analyzing data and revising the manuscript. DF, JY, DD participated in some figures configuration and revised the manuscript. LB, NC and XZ designed, supervised the experiments and revised the final manuscript. All authors have read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture
(2)
Centre d’Etudes Régional pour l’Amélioration de l’Adaptation à la Sécheresse (CERAAS)
(3)
Laboratoire Campus de Biotechnologies Végétales, Département de Biologie Végétale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop
(4)
CIRAD, UMR AGAP

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