Function of the NAC transcription factor family genes in the regulation of biotic stresses responses in plants

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Review Paper 01/02/2017
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Function of the NAC transcription factor family genes in the regulation of biotic stresses responses in plants

A.M. Sharoni, M. Nuruzzaman, M.M. Rahman, A.K.M.R. Islam, M.M. Hossain, M.F. Alam, MA Rahman, A. Imtiaj, S. Kikuchi
J. Bio. Env. Sci.10( 2), 141-153, February 2017.
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NAC transcription factor is one of the largest families of transcriptional regulators in plants, and members of the NAC gene family have been suggested to play important roles in the regulation of the transcriptional reprogramming associated with plant stress responses. A phylogenetic analysis of NAC genes, with a focus on rice and Arabidopsis, was performed. Herein, we present an overview of the regulation of the stress responsive NAC SNAC/(IX) group of genes that are implicated in the resistance to different stresses. SNAC factors have important roles for the control of biotic stress tolerance and overexpression can improve stress tolerance via biotechnological approaches. We also review the recent progress in elucidating the roles of NAC transcription factor in plant biotic stress. Modification of the expression pattern of transcription factor genes and/or changes in their activity contribute to the elaboration of various signaling pathways and regulatory networks. Though, a single NAC gene often responds to several stress factors, and their protein products may participate in the regulation of several seemingly disparate processes as negative or positive regulators. Additionally, the NAC proteins function via auto-regulation or cross-regulation is extensively found among NAC genes. These observations assist in the understanding of the complex mechanisms of signaling and transcriptional reprogramming controlled by NAC proteins.


Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9, 841–857.

Bhattacharjee S. 2005. Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr. Sci. 89, 1113–1121.

Biruma M, Martin T, Fridborg I, Okori P, Dixelius C. 2012. Two loci in sorghum with NB-LRR encoding genes confer resistance to Colletotrichum sublineolum. Theor. Appl. Genet. 124, 1005–1015.

Buchanan-Wollaston, VEarl S,  Harrison  E,   Page T, Pink D.   2003. The molecular analysis of leaf senescence–a genomics approach. Plant Biotechnol J.  1, 3–22.

Chakravarthy S, Vela0squez AC, Martin GB.  2010. Identification of Nicotiana benthamiana genes involved in pathogen-associated molecular pattern-triggered immunity. Mol. Plant Microbe Interact. 23, 715–726.

Chen Q, Wang Q, Xiong L, Lou Z. 2011. A structural view of the conserved domain of rice stress-responsive NAC1. Protein Cell 2, 55–63.

Collinge M, Boller T. 2001. Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol. Biol. 46, 521–529.

de Zélicourt  A,  Diet A,   Gruber V, Frugier F.  2012. Dual involvement of a Medicago truncatula NAC transcription factor in root abiotic stress response and symbiotic nodule senescence. Plant J.  70, 220-30.

Delessert C, Kazan K,  Dolferus R. 2005. The transcriptionfactor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J. 43, 745–757.

Distelfeld APearce SP, Avni R,  Dubcovsky J. 2012. Divergent functions of orthologous NAC transcription factors in wheat and rice. Plant Mol. Biol. 78, 515–24.

Ernst HA, AN, Olsen S, Larsen, Lo-Leggio L. 2004. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors, EMBO Rep. 5, 297–303.

Eulgem T, Somssich IE. 2007. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366–371.

Fujita M, Fujita Y, Noutoshi  Y, Shinozaki K. 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436–42.

Gepstein SSabehi G, Dor C, Bassani M. 2003. Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629–42.

Guo HS, Xie Q, Fei JF. Chua NH. 2005. Micro RNA directs mRNA cleavage of the transcription factor NAC1 to down-regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17, 1376–86.

Guo Y, Gan S. 2006. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601–12.

Guo Y, Cai Z, Gan S. 2004. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 27, 521–549.

Gutterson N, Reuber TL. 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr. Opin. Plant Biol. 7, 465–471.

He XJ, Mu RL, Cao WH, Chen SY. 2005. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J. 44, 903–916.

Hu R,  Qi G, Kong Y, Kong D, Gao Q, Zhou G. 2010. Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol. 10, 145.

Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L. 2006. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. U.S.A. 103, 12987–12992.

Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L. 2008. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 67, 169–181.

Jensen M,  Kjaersgaard K, O’Shea C, Skriver K.  2010. The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signaling. Biochem. J. 426, 183–196.

Jensen MK, Rung JH, Lyngkjaer MF, Collinge DB. 2007. The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol. Biol. 65, 137–150.

Jensen MK, Hagedorn PH,  Rung JH,  Lyngkjaer MF, Collinge DB. 2008. Transcriptional regulationbyanNAC (NAMATAF1,2-CUC2) transcription factor attenuates ABA signaling for efficient basal defence towards Blumeria graminis f sp hordei in Arabidopsis. Plant J. 56, 867–880.

Kaneda T, Taga Y, Isogai  A, Che FS. 2009. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J. 28, 926–936.

Kim JH, Woo HR, Hwang D, Nam HG. 2009. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053–1057.

Kim SG, Kim SY, Park CM. 2007a. A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226, 647–654.

Kim SY, Kim SG, Yoon HK, Park CM. 2007b. Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res. 35, 203–213.

Le D, Nishiyama T, Watanabe RT, Tran  LS. 2011. Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res. 18, 263–76.

Lee S, Seo PJ, Lee HJ, Park CM. 2012. A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. 70, 831–44.

Li W, Zhong S, Li G, Li Q,  He Z. 2011. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence. Cell Res. 21, 835–848.

Liu JL, Wang XJ, Mitchell T, Wang GL. 2010. Recent progress and understanding of the molecular mechanisms of the rice Magnaporthe oryzae interaction. Mol. Plant Pathol. 11, 419–427.

Liu Y, Schiff M, Dinesh-Kumar SP. 2002. Virus-induced gene silencing in tomato. Plant J. 31, 777–786.

Nakashima K, Ito Y, Yamaguchi-Shinozaki K. 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149, 88–95.

Nakashima K, Tran LS, VanNguyen D, Fujita M, Yamaguchi-Shinozaki K. 2007. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51, 617–630.

Nilsson LMüller R,  Nielsen R. 2010. Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol. Plant 139, 129–43.

Nuruzzaman M, Sharoni AM, Satoh K, Kondoh H, Hosaka A, Kikuchi S. 2012a. A genome-wide survey of the NAC transcription factor family in monocots and eudicots. Introduction to Genetics – DNA Methylation, Histone Modification and Gene Regulation. iConcept Press. ISBN:978-14775549-4-4.

Nuruzzaman M,  Manimekalai R,  Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S. 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene  465, 30–44.

Nuruzzaman M, Sharoni AM, Kumar AK,  Leung H, Attia K, Kikuchi S.  2012b. Comprehensive gene expression analysis of the NAC gene family under normal growth conditions, hormone treatment, and drought stress conditions in rice using near-isogenic lines (NILs) generated from crossing Aday Selection (drought tolerant) and IR64. Mol. Genet. Genomics 287, 389–410.

Ochiai K,  Shimizu A, Okumoto Y, Fujiwara T, Matoh T. 2011. Suppression of a NAC-like transcription factor gene improves boron-toxicity tolerance in rice. Plant Physiol. 156, 1457–63.

Ohnishi T,  Sugahara S, Hirano HY, Tsutsumi N. 2005. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst.  80, 135–9.

Olsen AN, Ernst HA, Lo Leggio L, Skriver K. 2005. NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 10:1360–1385.

Ooka, H., Satoh, K., Doi, K., T. Nagata and S. Kikuchi. 2003. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 10, 239–247.

Rushton PJ,  Bokowiec MT., Laudeman TW, Timko MP. 2008. Tobaccotranscription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol. 147, 280–295.

Satoh K, Kondoh H, Omura  T, Kikuchi S. 2011. Relationship between symptoms and gene expression induced by the infection of three strains of rice dwarf virus. PLoS One 3, e18094.

Scofield SR, Nelson RS. 2009. Resources for virus-induced gene silencing in the grasses. Plant Physiol. 149, 152–157.

Scofield SR, Huang L, Brandt AS, Gill BS. 2005. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol. 138, 2165–2173.

Seo PJ,  Kim  MJ, Park CM. 2010 Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J. 61, 661–671.

Sindhu A, Chintamanani S, Johal GS. 2008. A guardian of grasses: specific origin and conservation of a unique disease-resistance gene in the grass lineage. Proc. Natl. Acad. Sci. U.S.A. 105, 1762–1767.

Souer E, Van Houwelingen A, Kloos D, Mol J, Koes R. 1996. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85, 159–170.

Sperotto RA, Ricachenevsky FK, Fett JP. 2009. Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230, 985–1002.

Sun L,  Zhang H,  Li  D, Song F. 2013. Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol. Biol. 81, 41–56.

Takasaki H, Maruyama K, Nakashima K. 2010. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol. Genet. Genomics 284, 173–183.

Tian C, Wan P, Sun S, Li J, Che M. 2004. Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol. Biol. 54, 519–532.

Valent B, Khang CH. 2010. Recent advances in rice blast effector research. Curr. Opin. Plant Biol. 13, 434–441.

Van der Linde K, Kastner C, Doehlemann G. 2011. Systemic virus-induced gene silencing allows functional characterization of maize genes during biotrophic interaction with Ustilago maydis. New Phytol. 189, 471–483.

Van Loon LC, Rep M, Pieterse CM. 2006. Significance of inducible defense-related proteins in infected pants. Annu. Rev. Phytopathol. 44, 135–162.

Wang X,  Basnayake  BM, Song F. 2009a. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol. Plant Microbe Interact. 22, 1227–1238.

Wang X,  Goregaoker  SP, Culver JN. 2009b. Interaction of the Tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J. Virol. 83, 9720–9730.

Wu Y, Deng Z, Lai J, Xie Q. 2009. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res. 19, 1279–1290.

Xia N,  Zhang G, Huanga LL, Kanga ZS. 2010b. TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol. Mol. Plant Pathol. 74, 394–402.

Xia N,  Zhang G, Huang  LL, Kang ZS. 2010a. Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol. Biol. Rep. 37, 3703–3712.

Xie Q, Frugis G, Colgan D, Chua N. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14, 3024–3036.

Xie Q, Sanz-Burgos AP Gutierrez C. 1999. GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Mol. Biol. 39, 647–656.

Yoshii M, Shimizu T, Omura T. 2009. Disruption of a novel gene for a NAC-domain protein in rice confers resistance to rice dwarf virus. Plant J. 57, 615–625.

Yoshii M, Yamazaki M, Rakwal R, Hirochika H. 2010. The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J. 61, 804–15.

Zhou H, Li S,  Zhang J. 2007. Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J. 52, 420–434.

Zhou M, Li D,  Li Z, Hu Q, Yang C, Zhu L, Luo H. 2013. Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 161, 1375–91.

Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. 2004. Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621–2632.