Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon

doi:10.1038/srep21623

. 2016 Feb 12:6:21623.

doi: 10.1038/srep21623.

Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon

Lihong Chen¹, Jiapeng Han², Xiaomin Deng³, Shenglong Tan⁴, Lili Li¹, Lun Li¹, Junfei Zhou¹, Hai Peng¹, Guangxiao Yang², Guangyuan He², Weixiong Zhang^{1

5}

Affiliations

¹ The Institute for Systems Biology, Jianghan University, Wuhan 430056, China.
² The Genetic Engineering International Cooperation Base of Chinese Ministry of Science and Technology, Chinese National Center of Plant Gene Research (Wuhan) HUST Part, College of Life Science and Technology, Huazhong University of Science &Technology (HUST), Wuhan 430074, China.
³ Ministry of Agriculture Key Laboratory of Biology and Genetic Resources of Rubber Tree/State Key Laboratory Breeding Base of Cultivation and Physiology for Tropical Crops, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou 571737, China.
⁴ School of Information Engineering, Hubei University of Economics, Wuhan 430205, China.
⁵ Department of Computer Science and Engineering and Department of Genetics, Washington University, St. Louis, MO 36130, USA.

PMID: 26869021
PMCID: PMC4751504
DOI: 10.1038/srep21623

Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon

Lihong Chen et al. Sci Rep. 2016.

. 2016 Feb 12:6:21623.

doi: 10.1038/srep21623.

Authors

Lihong Chen¹, Jiapeng Han², Xiaomin Deng³, Shenglong Tan⁴, Lili Li¹, Lun Li¹, Junfei Zhou¹, Hai Peng¹, Guangxiao Yang², Guangyuan He², Weixiong Zhang^{1

5}

Affiliations

¹ The Institute for Systems Biology, Jianghan University, Wuhan 430056, China.
² The Genetic Engineering International Cooperation Base of Chinese Ministry of Science and Technology, Chinese National Center of Plant Gene Research (Wuhan) HUST Part, College of Life Science and Technology, Huazhong University of Science &Technology (HUST), Wuhan 430074, China.
³ Ministry of Agriculture Key Laboratory of Biology and Genetic Resources of Rubber Tree/State Key Laboratory Breeding Base of Cultivation and Physiology for Tropical Crops, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou 571737, China.
⁴ School of Information Engineering, Hubei University of Economics, Wuhan 430205, China.
⁵ Department of Computer Science and Engineering and Department of Genetics, Washington University, St. Louis, MO 36130, USA.

PMID: 26869021
PMCID: PMC4751504
DOI: 10.1038/srep21623

Abstract

APETALA2/ethylene-responsive element binding protein (AP2/EREBP) transcription factors constitute one of the largest and most conserved gene families in plant, and play essential roles in growth, development and stress response. Except a few members, the AP2/EREBP family has not been characterized in Brachypodium distachyon, a model plant of Poaceae. We performed a genome-wide study of this family in B. distachyon by phylogenetic analyses, transactivation assays and transcript profiling. A total of 149 AP2/EREBP genes were identified and divided into four subfamilies, i.e., ERF (ethylene responsive factor), DREB (dehydration responsive element binding gene), RAV (related to ABI3/VP) and AP2. Tandem duplication was a major force in expanding B. distachyon AP2/EREBP (BdAP2/EREBP) family. Despite a significant expansion, genomic organizations of BdAP2/EREBPs were monotonous as the majority of them, except those of AP2 subfamily, had no intron. An analysis of transcription activities of several closely related and duplicated BdDREB genes showed their functional divergence and redundancy in evolution. The expression of BdAP2/EREBPs in different tissues and the expression of DREB/ERF subfamilies in B. distachyon, wheat and rice under abiotic stresses were investigated by next-generation sequencing and microarray profiling. Our results are valuable for further function analysis of stress tolerant AP2/EREBP genes in B. distachyon.

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Figures

**Figure 1**
(A) Phylogeny of the *B. distachyon* AP2/EREBP (APETALA2/ethylene-responsive element binding protein) family. (B) Domain structures of the AP2/EREBP genes.

**Figure 2. Phylogeny of the *B. distachyon* DREB (dehydration responsive element binding gene) and ERF (ethylene responsive factor) subfamily proteins based on their conserved domain sequences.**
Different subgroups of DREB and ERF subfamily proteins are highlighted in different colors.

**Figure 3. Chromosomal distributions of the *B. distachyon* AP2/EREBP genes. *chrm* is an abbreviation for chromosome.**
Tandem duplicated gene clusters were highlighted in boxes. The dotted lines, connecting the AP2/EREBP genes in different chromosomes, show the chromosomal segment duplication events. The genes in different subfamilies were color coded. AP2/EREBP is shorted for APETALA2/ethylene-responsive element binding protein.

**Figure 4. Transactivation activity assays of 10 *B. distachyon* DREB proteins.**
AH109 yeast cells, transformed with plasmid containing different BdDREB genes individually, were cultivated in nutritional selective medium (A) SD/-Trp, SD/-Trp-His, SD/-Trp-His-Ade or (B) SD/-Trp-His-X-α-gal. The empty vector pGBKT7 was negative control. Photos were taken after incubating at 28 °C for three days. DREB is shorted for dehydration responsive element binding gene.

**Figure 5. Expression profiles of BdAP2/EREBP (APETALA2/ethylene-responsive element binding protein) genes in three tissues of roots, stems and leaves.**
Expression profiles (in log₂ based values) of the BdDREB (A), BdERF (B), BdAP2 (C) and BdRAV (D) genes in three tissues. Bd is shorted for *B. distachyon*. DREB, ERF, AP2 and RAV were shorted for dehydration responsive element binding gene, ethylene responsive factor, APETALA2 and related to ABI3/VP, respectively.

**Figure 6**
Expression profiles (in log₂ based fold change) of BdDREB (A), BdERF (B), BdRAV (C) and BdAP2 (D) genes under four abiotic stress conditions. Bd is shorted for *B. distachyon*. DREB, ERF, AP2 and RAV were shorted for dehydration responsive element binding gene, ethylene responsive factor, APETALA2 and related to ABI3/VP, respectively.

Figure 7. Comparisons of expression profiles of three representative pairs of duplicated AP2/EREBP genes in *B. distachyon* across 20 time points (in hours) after cold, heat, drought and high-salinity stress treatments.
Represented in y-axes are the expressions, in log₂ based fold changes of the corresponding treatments. The correlation (R) between two duplicated genes is measured by the Pearson correlation coefficient of the expressions of the pair of genes. AP2/EREBP is shorted for APETALA2/ethylene-responsive element binding protein.

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References

1. Dubouzet J. G. et al.. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33, 751–763 (2003). - PubMed
1. Gutterson N. & Reuber T. L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7, 465–471 (2004). - PubMed
1. Kume S. et al.. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet Syst 80, 185–197 (2005). - PubMed
1. Yamaguchi-Shinozaki K. & Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57, 781–803 (2006). - PubMed
1. Sakuma Y. et al.. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103, 18822–18827 (2006). - PMC - PubMed

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[1] Dubouzet J. G. et al.. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33, 751–763 (2003). - PubMed

[2] Dubouzet J. G. et al.. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33, 751–763 (2003). - PubMed

[3] Gutterson N. & Reuber T. L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7, 465–471 (2004). - PubMed

[4] Gutterson N. & Reuber T. L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7, 465–471 (2004). - PubMed

[5] Kume S. et al.. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet Syst 80, 185–197 (2005). - PubMed

[6] Kume S. et al.. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet Syst 80, 185–197 (2005). - PubMed

[7] Yamaguchi-Shinozaki K. & Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57, 781–803 (2006). - PubMed

[8] Yamaguchi-Shinozaki K. & Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57, 781–803 (2006). - PubMed

[9] Sakuma Y. et al.. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103, 18822–18827 (2006). - PMC - PubMed

[10] Sakuma Y. et al.. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103, 18822–18827 (2006). - PMC - PubMed

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Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon

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Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon

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