Skip to main content
SpringerLink
Log in

Transcriptome-based Discovery of AP2/ERF tRanscription Factors and Expression Profiles Under Herbivore Stress Conditions in Bamboo (Bambusa emeiensis)

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Bambusa emeiensis is one of the most economically important bamboos, yet the yield and quality of this bamboo species continue to be challenged by insect herbivores. APETALA2/ethylene responsive factors (AP2/ERF) comprise a large family of plant transcription factors regulating numerous biological processes and playing critical roles in plant defence responses. In the present study, 47 AP2/ERF genes were identified and classified in the B. emeiensis herbivore-induced transcriptome. Based on AP2 domain numbers, conserved amino-acid residues, motif analyses and phylogenetic trees and BeAP2/ERF proteins were grouped into four subfamilies, namely AP2, ERF, Dehydration-responsive-element-binding (DREB) and Soloist, and these subfamilies consisted of nine, 23, 14 and 1 proteins, respectively. Amino-acid residue sequences of the AP2 domain in B. emeiensis were conserved compared with those in Arabidopsis thaliana. Expression analyses revealed that the treatment (herbivore damage) and control groups exhibited different expression patterns, and majority of BeERF/DREB genes were significantly and differentially expressed in the transcriptome, as verified using quantitative real-time PCR (qPCR). Finally, eight genes were selected for further PCR analyses of tissue-specific expression, of which the four tissues exhibited different expression patterns. Our data indicated that the genes encoding the ERF/DREB subfamily of B. emeiensis play critical roles in its response to herbivores.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Akhtar M, Jaiswal A, Taj G, Jaiswal JP, Qureshi MI, Singh NK (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91:385–395

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun 401:238–44

    Article  CAS  PubMed  Google Scholar 

  • Chia KF (2016) The Arabidopsis transcription factor ERF13 negatively regulates defense against Pseudomonas syringae. Dissertation, UC San Diego

    Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes DEV 17:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couldridge C, Newbury HJ, Ford-Lloyd B, Bale J, Pritchard J (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bull Entomol Res 97:523–32

    Article  CAS  PubMed  Google Scholar 

  • Dinh TT, Girke T, Liu X, Yant L, Schmid M, Chen X (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139:1978–1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du X, Li W, Sheng L, Deng Y, Wang Y, Zhang W, Yu K, Jiang J, Fang W, Guan Z, Chen F, Chen S (2018) Over-expression of chrysanthemum CmDREB6 enhanced tolerance of chrysanthemum to heat stress. BMC Plant Biol 18:178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9:1272–1285

    Article  CAS  PubMed  Google Scholar 

  • Gregg A H, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  Google Scholar 

  • Hu L, Liu S (2011) Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genet Mol Biol 34:624–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang PY, Catino TJ, Zimmerli L (2016) Ethylene response factors in Arabidopsis immunity. J Exp Bot 67:1231–1241

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  CAS  PubMed  Google Scholar 

  • Junya M, Natsumi K, Satoshi K, Fuminori T, Feng Q, Kyoko M, Kazuo S, Kazuko YS (2019) Heat-induced inhibition of phosphorylation of the stress-protective transcription factor DREB2A promotes thermotolerance of Arabidopsis thaliana. J Biol Chem 294:902–917

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhang D, Gao B, Liang Y, Yang H, Wang Y, Wood AJ (2017) Transcriptome-wide identification, classification, and chracterizationa of AP2/ERF family genes in the desert moss Syntrichia caninervis. Front Plant Sci 8:262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HM, Hu SL, Cao Y, Lu XQ, Gang XU, Long ZJ, Ren P (2016) Cloning of WRKY Transcription Factors in Bambusa emeiensis and Stress-induced Expressions. J Bamboo Res 3:1–8

    Google Scholar 

  • Luo C, Liu A, Long W, Liao H, Yang Y (2018). Transcriptome analysis of Cyrtotrachelus buqueti in two cities in China. Gene 647:1–12

    Article  CAS  PubMed  Google Scholar 

  • Mantyla E, Lang V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148

    Article  PubMed  PubMed Central  Google Scholar 

  • McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizoi J, Ohori T, Moriwaki T, Kidokoro S, Todaka D, Maruyama K, Kusakabe K, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2013) GmDREB2A; 2, a canonical dehydration-responsive element-binding protein2-type transcription factor in soybean, is posttranslationally regulated and mediates dehydration-responsive element-dependent gene expression. Plant Physiol 161:346–361

    Article  CAS  PubMed  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park S, Gilmour SJ, Grumet R, Thomashow MF (2018) CBF-dependent and CBF-independent regulatory pathways contribute to the differences in freezing tolerance and cold-regulated gene expression of two Arabidopsis ecotypes locally adapted to sites in Sweden and Italy. PLoS One 13:e0207723

    Article  PubMed  PubMed Central  Google Scholar 

  • Rashid M, Guangyuan H, Guangxiao Y, Hussain J, Xu Y (2012) AP2/ERF transcription factor in rice: genome-wide canvas and syntenic relationships between monocots and eudicots. EVOL Bioinform Online 8:321–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehrig MN (2010) The role of ERF transcription factors in defenses against specialist and generalist herbivores in Arabidopsis thaliana. Dissertation, University of Missouri-Columbia.

    Book  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-Binding Specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Bioph Res Co 290:998–1009

    Article  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Nat Acad Sci USA 95:11457–14570

    Article  Google Scholar 

  • Wei Y, Chang Y, Zeng H, Liu G, He C, Shi H (2018) RAV transcription factors are essential for disease resistance against cassava bacterial blight via activation of melatonin biosynthesis genes. J Pineal Res 64

  • Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Lv H, Li L, Liu J, Mu S, Li X, Gao J (2015a) Genome-wide analysis of the AP2/ERF transcription factors family and the expression patterns of DREB genes in Moso Bamboo (Phyllostachys edulis). PLOS ONE 10:e0126657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu ZJ, Li XH, Liu ZW, Li H, Wang YX, Zhuang J (2015b) Transcriptome-based discovery of AP2/ERF transcription factors related to temperature stress in tea plant (Camellia sinensis). Funct Integr Genomics 15:741–752

    Article  CAS  PubMed  Google Scholar 

  • Xu ZS, Chen MC, Li LC, Ma YZ (2008) Functions of the ERF transcription factor family in plants. Botany 86:969–977

    Article  CAS  Google Scholar 

  • Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58:585–596

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Xing J, Zhang K, Pang X, Zhao Y, Wang G, Zang J, Huang R, Dong J (2019) Ethylene response factor ERF11 activates BT4 transcription to regulate immunity to Pseudomonas syringae. Plant Physiol 180:1132–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Chengdu Basebiotech Co., Ltd for assistance in original data processing and for related bioinformatics analysis. We also thank other members of the laboratory for suggestions and discussions regarding this work and with respect to revision of the manuscript.

Author information

Author notes

  1. The authors contribute equally to the manuscript.

Authors and Affiliations

  1. Bamboo Diseases and Pests Control and Resources Development Key Laboratory of Sichuan Province, College of Life Science, Leshan Normal University, Leshan, China

    Yuanqiu Li, Chaobing Luo, Ying Chen, Ximeng Xiao, Chun Fu & Yaojun Yang

  2. College of Food and Biological Engineering, Xihua University, Chengdu, China

    Yuanqiu Li, Ying Chen & Ximeng Xiao

Authors
  1. Yuanqiu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chaobing Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ximeng Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chun Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yaojun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yaojun Yang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Luo, C., Chen, Y. et al. Transcriptome-based Discovery of AP2/ERF tRanscription Factors and Expression Profiles Under Herbivore Stress Conditions in Bamboo (Bambusa emeiensis). J. Plant Biol. 62, 297–306 (2019). https://doi.org/10.1007/s12374-019-0059-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-019-0059-5

Keywords

Search

Navigation