Comprehensive Analysis Suggests Overlap** Expression of Rice ONAC Transcription Factors in Abiotic and Biotic Stress Responses
Abstract
:1. Introduction
2. Results
2.1. Inducibility and Overlap** Expression of ONAC Genes in Response to Abiotic Stresses
2.2. Inducibility and Overlap** Expression of ONAC Genes in Response to Biotic Stress
2.3. Overlap** Expression of Different Groups of ONAC Genes in Response to Abiotic and Biotic Stresses
2.4. Evaluation Relationships of ONAC Genes with Overlap** Expression Patterns
3. Discussion
4. Methods
4.1. Plant Growth and Treatments
4.2. Mining and Analysis of Microarray-Based Expression Profiling Data
4.3. qPCR Analysis
4.4. Phylogenetic Analysis
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Nakashima, K.; Yamaguchi-Shinozaki, K.; Shinozaki, K. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front. Plant Sci. 2014, 5, 170. [Google Scholar] [CrossRef]
- Golldack, D.; Li, C.; Mohan, H.; Probst, N. Tolerance to drought and salt stress in plants: Unraveling the signaling networks. Front. Plant Sci. 2014, 5, 151. [Google Scholar] [CrossRef]
- Hines, P.J.; Zahn, L.M. What’s bugging plants? Plant-microbe interactions. Introduction. Science 2009, 324, 741. [Google Scholar] [CrossRef]
- Boller, T.; He, S.Y. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 2009, 324, 742–744. [Google Scholar] [CrossRef] [PubMed]
- Atkinson, N.J.; Urwin, P.E. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 2012, 63, 3523–3543. [Google Scholar] [CrossRef] [PubMed]
- Golldack, D.; Lüking, I.; Yang, O. Plant tolerance to drought and salinity: Stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep. 2011, 30, 1383–1391. [Google Scholar] [CrossRef] [PubMed]
- Gutterson, N.; Reuber, T.L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr. Opin. Plant Biol. 2004, 7, 465–471. [Google Scholar] [CrossRef] [PubMed]
- Eulgem, T.; Somssich, I.E. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 2007, 10, 366–371. [Google Scholar] [CrossRef] [PubMed]
- Singh, K.; Foley, R.C.; Oñate-Sánchez, L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002, 5, 430–436. [Google Scholar] [CrossRef] [PubMed]
- Aida, M.; Ishida, T.; Fukaki, H.; Fujisawa, H.; Tasaka, M. Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 1997, 9, 841–857. [Google Scholar] [CrossRef] [PubMed]
- Ernst, H.A.; Olsen, A.N.; Larsen, S.; Lo Leggio, L. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep. 2004, 5, 297–303. [Google Scholar] [CrossRef] [PubMed]
- Duval, M.; Hsieh, T.F.; Kim, S.Y.; Thomas, T.L. Molecular characterization of AtNAM: A member of the Arabidopsis NAC domain superfamily. Plant Mol. Biol. 2002, 50, 237–248. [Google Scholar]
- Ooka, H.; Satoh, K.; Doi, K.; Nagata, T.; Otomo, Y.; Murakami, K.; Matsubara, K.; Osato, N.; Kawai, J.; Carninci, P.; et al. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 2003, 10, 239–247. [Google Scholar]
- Fang, Y.; You, J.; **e, K.; **e, W.; **ong, L. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol. Genet. Genomics 2008, 280, 547–563. [Google Scholar] [CrossRef]
- Nuruzzaman, M.; Manimekalai, R.; Sharoni, A.M.; Satoh, K.; Kondoh, H.; Ooka, H.; Kikuchi, S. Genome-wide analysis of NAC transcription factor family in rice. Gene 2010, 465, 30–44. [Google Scholar] [CrossRef] [PubMed]
- Rushton, P.J.; Bokowiec, M.T.; Han, S.; Zhang, H.; Brannock, J.F.; Chen, X.; Laudeman, T.W.; Timko, M.P. Tobacco transcription factors: Novel insights into transcriptional regulation in the Solanaceae. Plant Physiol. 2008, 147, 280–295. [Google Scholar] [CrossRef] [PubMed]
- Le, D.T.; Nisjiyama, R.; Watanabe, Y.; Mochida, K.; Yamaquchi-Shinozaki, K.; Shinozaki, K.; Tran, L.S. Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res. 2011, 18, 263–276. [Google Scholar] [CrossRef] [PubMed]
- Hu, R.; Qi, G.; Kong, Y.; Kong, D.; Gao, Q.; Zhou, G. Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol. 2010, 10, 145. [Google Scholar] [CrossRef] [PubMed]
- Olsen, A.N.; Ernst, H.A.; Leggio, L.L.; Skriver, K. NAC transcription factors: Structurally distinct, functionally diverse. Trends Plant Sci. 2005, 10, 79–87. [Google Scholar] [CrossRef] [PubMed]
- Zhong, R.; Lee, C.; Ye, Z.H. Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci. 2010, 15, 625–632. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Deyholos, M.K. Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol. 2006, 6, 25. [Google Scholar] [CrossRef] [PubMed]
- Tran, L.S.; Nakashima, K.; Sakuma, Y.; Simpson, S.D.; Fujita, Y.; Maruyama, K.; Fujita, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 2004, 16, 2481–2498. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Deng, Z.; Lai, J.; Zhang, Y.; Yang, C.; Yin, B.; Zhao, Q.; Zhang, L.; Li, Y.; Yang, C.; **e, Q. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res. 2009, 19, 1279–1290. [Google Scholar] [CrossRef] [PubMed]
- Fujita, M.; Fujita, Y.; Maruyama, K.; Seki, M.; Hiratsu, K.; Ohme-Takagi, M.; Tran, L.S.; Yamaguchi-shinozaki, K.; Shinozaki, K. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J. 2004, 39, 863–876. [Google Scholar] [CrossRef] [PubMed]
- Hu, H.; Dai, M.; Yao, J.; **ao, B.; Li, X.; Zhang, Q.; **ong, L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 2006, 103, 12987–12992. [Google Scholar] [CrossRef] [PubMed]
- Hu, H.; You, J.; Fang, Y.; Zhu, X.; Qi, Z.; **ong, L. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 2008, 67, 169–181. [Google Scholar] [CrossRef] [PubMed]
- Ohnishi, T.; Sugahara, S.; Yamada, T.; Kikuchi, K.; Yoshiba, Y.; Hirano, H.Y.; Tsutsumi, N. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet. Syst. 2005, 80, 135–139. [Google Scholar]
- Nakashima, K.; Tran, L.S.; Van Nguyen, D.; Fujita, M.; Maruyama, K.; Todaka, D.; Ito, Y.; Hayashi, N.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 2007, 51, 617–630. [Google Scholar] [CrossRef] [PubMed]
- Takasaki, H.; Maruyama, K.; Kidokoro, S.; Ito, Y.; Fujita, Y.; Shinozaki, K.; Yamaguchi, S.K.; Nakashima, K. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol. Genet. Genomics 2010, 284, 173–183. [Google Scholar] [CrossRef] [PubMed]
- Jeong, J.S.; Kim, Y.S.; Baek, K.H.; Jung, H.; Ha, S.H.; Do Choi, Y.; Kim, M.; Reuzeau, C.; Kim, J.K. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol. 2010, 153, 185–197. [Google Scholar] [CrossRef] [PubMed]
- Zheng, X.; Zhen, B.; Lu, G.; Han, B. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem. Biophys. Res. Commun. 2009, 379, 985–989. [Google Scholar] [CrossRef] [PubMed]
- Peng, H.; Yu, X.; Cheng, H.; Shi, Q.; Zhang, H.; Li, J.; Ma, H. Cloning and characterization of a novel NAC family gene CarNAC1 from chickpea (Cicer arietinum L.). Mol. Biotechnol. 2010, 44, 30–40. [Google Scholar] [CrossRef] [PubMed]
- Peng, H.; Cheng, H.Y.; Chen, C.; Yu, X.W.; Yang, J.N.; Gao, W.R.; Shi, Q.H.; Zhang, H.; Li, J.G.; Ma, H. A NAC transcription factor gene of chickpea (Cicer arietinum L.), CarNAC3, is involved in drought stress response and various developmental processes. J. Plant Physiol. 2009, 166, 1934–1945. [Google Scholar]
- Peng, H.; Cheng, H.Y.; Yu, X.W.; Shi, Q.H.; Zhang, H.; Li, J.G.; Ma, H. Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally and stress-regulated. Plant Physiol. Biochem. 2009, 47, 1037–1045. [Google Scholar]
- Yang, R.; Deng, C.; Ouyang, B.; Ye, Z. Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol. Biol. Rep. 2011, 38, 857–863. [Google Scholar] [CrossRef] [PubMed]
- Han, Q.; Zhang, J.; Li, H.; Luo, Z.; Ziaf, K.; Ouyang, B.; Wang, T.; Ye, Z. Identification and expression pattern of one stress-responsive NAC gene from Solanum lycopersicum. Mol. Biol. Rep. 2011, 39, 1713–1720. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Basnayake, B.M.; Zhang, H.; Li, G.J.; Li, W.; Virk, N.; Menqiste, T.; Song, F. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol. Plant Microbe. Interact. 2009, 22, 1227–1238. [Google Scholar] [CrossRef] [PubMed]
- Delessert, C.; Kazan, K.; Wilsom, L.W.; van der Straetend, D.; Manners, J.; Dennis, E.S.; Dolferus, R. The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J. 2005, 43, 745–757. [Google Scholar] [CrossRef] [PubMed]
- Jensen, M.K.; Rung, J.H.; Gregersen, P.L.; Gjetting, T.; Fuglsang, A.T.; Hansen, M.; Joehnk, N.; Lyngkjaer, M.F.; Collinge, D.B. The HvNAC6 transcription factor: A positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol. Biol. 2007, 65, 137–150. [Google Scholar] [CrossRef] [PubMed]
- Kaneda, T.; Taga, Y.; Takai, R.; Iwano, M.; Matsui, H.; Takayama, S.; Isoga, A.; Che, F.S. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J. 2009, 28, 926–936. [Google Scholar] [CrossRef] [PubMed]
- Yoshii, M.; Shimizu, T.; Yamazaki, M.; Higashi, T.; Miyao, A.; Hirochika, H.; Omura, T. Disruption of a novel gene for a NAC-domain protein in rice confers resistance to rice dwarf virus. Plant J. 2009, 57, 615–625. [Google Scholar] [CrossRef] [PubMed]
- Ren, T.; Qu, F.; Morris, T.J. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 2000, 12, 1917–1926. [Google Scholar] [CrossRef] [PubMed]
- **e, Q.; Sanz-Burgos, A.P.; Guo, H.; García, J.A.; Gutiérrez, C. GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Mol. Biol. 1999, 39, 647–656. [Google Scholar] [CrossRef] [PubMed]
- Selth, L.A.; Dogra, S.C.; Rasheed, M.S.; Healy, H.; Randles, J.W.; Rezaian, M.A. A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell 2005, 17, 311–325. [Google Scholar] [CrossRef] [PubMed]
- Oh, S.K.; Lee, S.; Yu, S.H.; Choi, D. Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 2005, 222, 876–887. [Google Scholar] [CrossRef] [PubMed]
- **a, N.; Zhang, G.; Liu, X.Y.; Deng, L.; Cai, G.L.; Zhang, Y.; Wang, X.J.; Zhao, J.Z.; Huang, L.L.; Kang, Z.S. Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol. Biol. Rep. 2010, 37, 3703–3712. [Google Scholar] [CrossRef] [PubMed]
- Faria, J.A.; Reis, P.A.; Reis, M.T.; Rosado, G.L.; Pinheiro, G.L.; Mendes, G.C.; Fontes, E.P. The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biol. 2011, 11, 129. [Google Scholar] [CrossRef]
- Mahajan, S.; Tuteja, N. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 2005, 444, 139–158. [Google Scholar] [CrossRef] [PubMed]
- Tyagi, A.K.; Kapoor, S.; Khurana, J.P.; Ray, S. Expression data for stress treatment in rice seedlings. 2007. GSE6901. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Kim, T.H. Plant stress surveillance monitored by ABA and disease signaling interactions. Mol. Cells 2012, 33, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Wasilewska, A.; Vlad, F.; Sirichandra, C.; Redko, Y.; Jammes, F.; Valon, C.; Frei dit Frey, N.; Leung, J. An update on abscisic acid signaling in plants and more. Mol. Plant 2008, 1, 198–217. [Google Scholar] [CrossRef] [PubMed]
- Balzergue, S.; Morel, J.; Martin-Magnetite, M.L. Identification of rice genes differentially expressed upon Virulent Infection by Magnaporthe oryzae. 2007. GSE7256. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Marcel, S.; Sawers, R.; Oakeley, E.; Angliker, H.; Paszkowski, U. Temporal gene expression analyisis from rice root (cv. Nipponbare) infected with Magnaporthe oryzae strain Guy11. 2009. GSE18361. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Lin, R.M.; Zhao, W.S.; Meng, X.B.; Wang, M.; Peng, Y.L. Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci. 2007, 172, 120–130. [Google Scholar] [CrossRef]
- DO, N.L. Comparative transcriptional profiling of rice undergoing infection by X. oryzae pv. oryzae or by X. oryzae pv.oryzicola. 2009. GSE16793. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Zhang, X.; Wu, Z.; **e, L.; Lin, Q.; **e, L. Comparative transcriptional profiling of two contrasting rice genotypes in response to rice stripe virus infection. 2008. GSE11025. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Scholes, J.D.; Swarbrick, P.J.; Huang, K.; Slate, J.; Press, M.C. Rice cultivars undergoing a susceptible and resistant interaction with the parasitic Plant STRIGA Hermonthica. 2008. GSE10373. Rice Array Database. Available online: http://www.ricearray.org (accessed on 15 October 2014).
- Kikuchi, K.; Ueguchi-Tanaka, M.; Yoshida, K.T.; Nagato, Y.; Matsusoka, M.; Hirano, H.Y. Molecular analysis of the NAC gene family in rice. Mol. Gen. Genet. 2000, 262, 1047–1051. [Google Scholar] [CrossRef] [PubMed]
- Yokotani, N.; Ichikawa, T.; Kondou, Y.; Matsui, M.; Hirochika, H.; Iwabuchi, M.; Oda, K. Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 2009, 229, 1065–1075. [Google Scholar]
- Seo, P.J.; Kim, M.J.; Park, J.Y.; Kim, S.Y.; Jeon, J.; Lee, Y.H.; Kim, J.; Park, C.M. Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J. 2010, 61, 661–671. [Google Scholar] [CrossRef] [PubMed]
- Cheong, Y.H.; Chang, H.S.; Gupta, R.; Wang, X.; Zhu, T.; Luan, S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002, 129, 661–677. [Google Scholar] [CrossRef] [PubMed]
- Fujita, M.; Fujita, Y.; Noutoshi, Y.; Takahashi, F.; Narusaka, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9, 436–442. [Google Scholar] [CrossRef] [PubMed]
- Rice Oligonucleotide Array Database. Available online: http://www.ricearray.org/ (accessed on 15 October 2014).
- Sun, L.; Zhang, H.; Li, D.; Huang, L.; Hong, Y.; Ding, X.S.; Nelson, R.S.; Zhou, X.; Song, F. Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol. Biol. 2013, 81, 41–56. [Google Scholar] [CrossRef] [PubMed]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Rice Genome Annotation Project. Available online: http://rice.plantbiology.msu.edu/ (accessed on 15 October 2014).
- Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013, 30, 2725–2729. [Google Scholar] [CrossRef]
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Sun, L.; Huang, L.; Hong, Y.; Zhang, H.; Song, F.; Li, D. Comprehensive Analysis Suggests Overlap** Expression of Rice ONAC Transcription Factors in Abiotic and Biotic Stress Responses. Int. J. Mol. Sci. 2015, 16, 4306-4326. https://doi.org/10.3390/ijms16024306
Sun L, Huang L, Hong Y, Zhang H, Song F, Li D. Comprehensive Analysis Suggests Overlap** Expression of Rice ONAC Transcription Factors in Abiotic and Biotic Stress Responses. International Journal of Molecular Sciences. 2015; 16(2):4306-4326. https://doi.org/10.3390/ijms16024306
Chicago/Turabian StyleSun, Lijun, Lei Huang, Yongbo Hong, Huijuan Zhang, Fengming Song, and Dayong Li. 2015. "Comprehensive Analysis Suggests Overlap** Expression of Rice ONAC Transcription Factors in Abiotic and Biotic Stress Responses" International Journal of Molecular Sciences 16, no. 2: 4306-4326. https://doi.org/10.3390/ijms16024306