Transcriptome-based mining and expression profiling of Pythium responsive transcription factors in Zingiber sp.
Transcription factors (TFs) fine-tune the host defense transcriptome in response to pathogen invasions. No information is available on Zingiber zerumbet (Zz) TFs involved in defense response against Pythium myriotylum. Here, we provide a global identification, characterization, and temporal expression profiling of Zz TFs following an incompatible interaction with P. myriotylum using a transcriptome sequencing approach. We identified a total of 903 TFs belonging to 96 families based on their conserved domains. Evolutionary analysis clustered the Zz TFs according to their phylogenetic affinity, providing glimpses of their functional diversities. High throughput expression array analysis highlighted a complex interplay between activating and repressing transcription factors in fine-tuning Zz defense response against P. myriotylum. The high differential modulation of TFs involved in cell wall fortification, lignin biosynthesis, and SA/JA hormone crosstalk allows us to envisage that this mechanism plays a central role in restricting P. myriotylum proliferation in Zz. This study lays a solid foundation and provides valuable resources for the investigation of the evolutionary history and biological functions of Zz TF genes involved in defense response.
KeywordsBiotic stress Defense response Ginger Plant-pathogen interaction Transcriptional reprogramming
VSN and LA gratefully acknowledge Kerala State Council for Science, Technology and Environment (KSCSTE), Government of Kerala Post-Doctoral Fellowship (Award No: 001-11/PDF/2016/KSCSTE) and research fellowship (Award No. 010-55/FHSP/2010/CSTE), respectively. SK thanks Science and Engineering Research Board (SERB), Government of India for National Post-Doctoral Fellowship (File No. PDF/2017/002022). KG gratefully acknowledges Council for Scientific and Industrial Research (CSIR), Government of India for research fellowship (F. No. 9/716(0103)/2008- EMR-I). GT acknowledges CSIR, Government of India for a research grant (No. 38(1397)/14EMR-II). We thank the anonymous reviewers for their valuable comments in improving the manuscript.
VSN executed the bioinformatics pipelines, performed data analysis, and drafted the manuscript. SK contributed to the bioinformatics analysis and drafting the manuscript. TEA contributed to the data analysis. KAG performed transcriptome sequencing and assembly. LA performed microarray analysis. AN contributed to data analysis. GT conceived and supervised the study. All authors read, commented on, and approved the final version of the manuscript.
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Conflict of interest
The authors declare that they have no competing interests.
- Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:808–815. https://doi.org/10.1093/nar/gks1094 CrossRefGoogle Scholar
- Froidure S, Canonne J, Daniel X, Jauneau A, Briere C, Roby D, Rivas S (2010) AtsPLA2-α nuclear relocalization by the Arabidopsis transcription factor AtMYB30 leads to repression of the plant defense response. Proc Natl Acad Sci 107:15281–15286. https://doi.org/10.1073/pnas.1009056107 CrossRefPubMedGoogle Scholar
- Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883 CrossRefPubMedPubMedCentralGoogle Scholar
- Hu W, Yang H, Yan Y, Wei Y, Tie W, Ding Z, Zuo J, Peng M, Li K (2016) Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep 6. https://doi.org/10.1038/srep22783
- Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, von Mering C, Bork P (2016) EGGNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293. https://doi.org/10.1093/nar/gkv1248 CrossRefPubMedGoogle Scholar
- Jayaswall K, Mahajan P, Singh G, Parmar R, Seth R, Raina A, Swarnkar MK, Singh AK, Shankar R, Sharma RK (2016) Transcriptome analysis reveals candidate genes involved in blister blight defense in tea (Camellia sinensis (L) Kuntze). Sci Rep 6:1–14. https://doi.org/10.1038/srep30412 CrossRefGoogle Scholar
- Kavitha PG, Thomas G (2007) Evaluation of Zingiberaceae for resistance to ginger soft rot caused by Pythium aphanidermatum (Edson) fitzp. Plant Genet Resour Newslett 152:54–57Google Scholar
- Kim T-W, Wang Z-Y (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704. https://doi.org/10.1146/annurev.arplant.043008.092057 CrossRefPubMedGoogle 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. https://doi.org/10.1104/pp.105.068544 CrossRefPubMedPubMedCentralGoogle Scholar
- Muthamilarasan M, Khandelwal R, Yadav CB, Bonthala VS, Khan Y, Prasad M (2014) Identification and molecular characterization of MYB transcription factor superfamily in C4 model plant foxtail millet (Setaria italica L.). PLoS One 9:e109920. https://doi.org/10.1371/journal.pone.0109920 CrossRefPubMedPubMedCentralGoogle Scholar
- Muthamilarasan M, Bonthala VS, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M (2015) Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci 6:1–15. https://doi.org/10.3389/fpls.2015.00910 CrossRefGoogle Scholar
- Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS, Carvalho CM, Fietto LG, Fontes EPB (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23. https://doi.org/10.1016/j.gene.2009.05.012 CrossRefPubMedGoogle 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 Biophys Res Commun 290:998–1009. https://doi.org/10.1006/bbrc.2001.6299 CrossRefPubMedGoogle Scholar
- Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC, Vingron M, Slusarenko AJ, Hoheisel JD (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277:10555–10561. https://doi.org/10.1074/jbc.M104863200 CrossRefGoogle Scholar
- Song A, Gao T, Li P, Chen S, Guan Z, Wu D, Xin J, Fan Q, Zhao K, Chen F (2016) Transcriptome-wide identification and expression profiling of the DOF transcription factor gene family in Chrysanthemum morifolium. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00199
- Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673 CrossRefPubMedPubMedCentralGoogle Scholar
- White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: PCR Protocols, a Guide to Methods and Applications, pp. 315-322.Google Scholar
- Windram O, Madhou P, McHattie S, Hill C, Hickman R, Cooke E, Jenkins DJ, Penfold CA, Baxter L, Breeze E, Kiddle SJ, Rhodes J, Atwell S, Kliebenstein DJ, Kim YS, Stegle O, Borgwardt K, Zhang C, Tabrett A, Legaie R, Moore J, Finkenstadt B, Wild DL, Mead A, Rand D, Beynon J, Ott S, Buchanan-Wollaston V, Denby KJ (2012) Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530–3557. https://doi.org/10.1105/tpc.112.102046 CrossRefPubMedPubMedCentralGoogle Scholar
- Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA, Zhang P, Banf M, Dai X, Martin GB, Giovannoni JJ, Zhao PX, Rhee SY, Fei Z (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670. https://doi.org/10.1016/j.molp.2016.09.014 CrossRefPubMedGoogle Scholar