Abstract
NAC family genes encode plant-specific transcription factors involved in diverse biological processes. In this study, the Arabidopsis NAC gene ATAF1 was found to be induced by drought, high-salinity, abscisic acid (ABA), methyl jasmonate, mechanical wounding, and Botrytis cinerea infection. Significant induction of ATAF1 was found in an ABA-deficient mutant aba2 subjected to drought or high salinity, revealing an ABA-independent mechanism of expression. Arabidopsis ATAF1-overexpression lines displayed many altered phenotypes, including dwarfism and short primary roots. Furthermore, in vivo experiments indicate that ATAF1 is a bona fide regulator modulating plant responses to many abiotic stresses and necrotrophic-pathogen infection. Overexpression of ATAF1 in Arabidopsis increased plant sensitivity to ABA, salt, and oxidative stresses. Especially, ATAF1 overexpression plants, but not mutant lines, showed remarkably enhanced plant tolerance to drought. Additionally, ATAF1 overexpression enhanced plant susceptibility to the necrotrophic pathogen B. cinerea, but did not alter disease symptoms caused by avirulent or virulent strains of P. syringae pv tomato DC3000. Transgenic plants overexpressing ATAF1 were hypersensitive to oxidative stress, suggesting that reactive oxygen intermediates may be related to ATAF1-mediated signaling in response to both pathogen and abiotic stresses.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Torres MA, Dangl JL . Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 2005; 8:397–403.
Apel K, Hirt H . Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373–399.
Mauch-Mani B, Mauch F . The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 2005; 8:409–414.
Fujita M, Fujita Y, Noutoshi Y, et al. 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.
Seki M, Narusaka M, Ishida J, et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 2002; 31:279–292.
AbuQamar S, Chen X, Dhawan R, et al. Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J 2006; 48:28–44.
Cheong YH, Chang HS, Gupta R, et al. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 2002; 129:661–677.
Davletova S, Schlauch K, Coutu J, Mittler R . The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 2005; 139:847–856.
Schenk PM, Kazan K, Wilson I, et al. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 2000; 97:11655–11660.
Dombrecht B, Xue GP, Sprague SJ, et al. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 2007; 19:2225–2245.
Laurie-Berry N, Joardar V, Street IH, Kunkel BN . The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact 2006; 19:789–800.
Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R . JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 2004; 16:1938–1950.
Mengiste T, Chen X, Salmeron J, Dietrich R . The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 2003; 15:2551–2565.
Hibara K, Takada S, Tasaka M . CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation. Plant J 2003; 36:687–696.
He XJ, Mu RL, Cao WH, et al. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 2005; 44:903–916.
Ishida T, Aida M, Takada S, Tasaka M . Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol 2000; 41:60–67.
Xie Q, Frugis G, Colgan D, Chua NH . Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 2000; 14:3024–3036.
Guo Y, Gan S . AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 2006; 46:601–612.
Collinge M, Boller T . Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 2001; 46:521–529.
Selth LA, Dogra SC, Rasheed MS, et al. A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell 2005; 17:311–325.
Xie Q, Sanz-Burgos AP, Guo H, Garcia JA, Gutierrez 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.
Jensen MK, Rung JH, Gregersen PL, et al. The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol 2007; 65:137–150.
Nakashima K, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K . A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J 1997; 12:851–861.
Simpson SD, Nakashima K, Narusaka Y, et al. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 2003; 33:259–270.
Tran LS, Nakashima K, Sakuma Y, et al. 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.
Zheng X, Chen 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.
Bu Q, Jiang H, Li CB, et al. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 2008; 18:756–767.
Delessert C, Kazan K, Wilson IW, et al. The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 2005; 43:745–757.
Nakashima K, Tran LS, Van ND, et al. 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.
Ohnishi T, Sugahara S, Yamada T, et al. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst 2005; 80:135–139.
Jensen MK, Hagedorn PH, de Torres-Zabala M, et al. Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signaling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 2008; 56:867–880.
Lu PL, Chen NZ, An R, et al. A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 2007; 63:289–305.
Zhang Y, Yang C, Li Y, et al. SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 2007; 19:1912–1929.
Kang JY, Choi HI, Im MY, Kim SY . Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 2002; 14:343–357.
Finkelstein RR, Lynch TJ . The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 2000; 12:599–609.
Hu H, Dai M, Yao J, et al. 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.
Leon-Kloosterziel KM, Gil MA, Ruijs GJ, et al. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 1996; 10:655–661.
Murata Y, Pei ZM, Mori IC, Schroeder J . Abscisic acid activation of plasma membrane Ca(2+) channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 2001; 13:2513–2523.
Glazebrook J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phyto pathol 2005; 43:205–227.
Mittler R . Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002; 7:405–410.
Kazan K, Murray FR, Goulter KC, Llewellyn DJ, Manners JM . Induction of cell death in transgenic plants expressing a fungal glucose oxidase. Mol Plant Microbe Interact 1998; 11:555–562.
Naton B, Hahlbrock K, Schmelzer E . Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells. Plant Physiol 1996; 112:433–444.
Govrin EM, Levine A . The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 2000; 10:751–757.
Fujita M, Fujita Y, Maruyama K, et al. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 2004; 39:863–876.
Zhang X, Garreton V, Chua NH . The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 2005; 19:1532–1543.
Acknowledgements
We would like to thank Dr Nam-Hai Chua (Rockefeller University) for kindly providing the pBA002Myc vector and the Arabidopsis Biological Resource Center (ABRC), Ohio State University for providing T-DNA insertion lines. This work was supported by grants from National Natural Science Foundation of China (No. 30530400/90717006/30670195) to Q Xie and Y Wu, the Chinese Academy of Science (KSCX2-YW-N-010 and CXTD-S2005-2), and the Guangdong Natural Science Foundation, China (No. 5300648) to Z Deng.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Supplementary information, Table S1
Stress-related expression patterns of Arabidopsis NAC genes based on public microarray data. (PDF 11 kb)
Supplementary information, Figure S1
Expression of ATAF1 in Col and aba2, an ABA-deficient mutant under drought and high salinity conditions. (PDF 127 kb)
Supplementary information, Figure S2
Expression of ABA and stress-responsive genes in wild-type, ATAF1-O1, and ataf1-1 plants treated by drought stress. (PDF 178 kb)
Supplementary information, Figure S3
Expression of ABA and stress–responsive genes in wild-type, ATAF1-O1, and ataf1-1 plants induced by 50 μM ABA at different times. (PDF 135 kb)
Supplementary information, Figure S4
Expression of ABA and stress–responsive genes in wild-type, ATAF1-O1, and ataf1-1 plants induced by 150 mM NaCl. (PDF 154 kb)
Supplementary information, Figure S5
Symptom development of plants in response to Bacterial Pathogens. (PDF 112 kb)
Rights and permissions
About this article
Cite this article
Wu, Y., Deng, Z., Lai, J. et al. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19, 1279–1290 (2009). https://doi.org/10.1038/cr.2009.108
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/cr.2009.108
Keywords
This article is cited by
-
Salicylic acid-related ribosomal protein CaSLP improves drought and Pst.DC3000 tolerance in pepper
Molecular Horticulture (2023)
-
A non-invasive method to predict drought survival in Arabidopsis using quantum yield under light conditions
Plant Methods (2023)
-
Overexpression of a rice Tubby–like protein-encoding gene, OsFBT4, confers tolerance to abiotic stresses
Protoplasma (2023)
-
Comparative transcriptome analysis of resistant and susceptible wheat in response to Rhizoctonia cerealis
BMC Plant Biology (2022)
-
Functional analysis of PagNAC045 transcription factor that improves salt and ABA tolerance in transgenic tobacco
BMC Plant Biology (2022)
