Abstract
Auxin regulates gene expression through direct physical interaction with TIR1/AFB receptor proteins during different processes of growth and development in plants. Here we report the contribution of auxin signaling pathway to the adaptative response against abiotic stress in Arabidopsis. Phenotypic characterization of tir1/afb auxin receptor mutants indicates a differential participation of each member under abiotic stress. In particular, tir1 afb2 and tir1 afb3 mutants resulted more tolerant to oxidative stress. In addition, tir1 afb2 showed increased tolerance against salinity measured as chlorophyll content, germination rate and root elongation compared with wild-type plants. Furthermore, tir1 afb2 displayed a reduced accumulation of hydrogen peroxide and superoxide anion, as well as enhanced antioxidant enzymes activities under stress. A higher level of ascorbic acid was detected in tir1 afb2 compared with wild-type plants. Thus, adaptation to salinity in Arabidopsis may be mediated in part by an auxin/redox interaction.
Similar content being viewed by others
Abbreviations
- ROS:
-
Reactive oxygen species
- MV:
-
Methyl viologen
- H2O2 :
-
Hydrogen peroxide
- O2 − :
-
Superoxide anion
- AA:
-
Ascorbate
- DHA:
-
Dihydroascorbate
- CAT:
-
Catalase
- APX:
-
Ascorbate peroxidase
References
Achard P, Renou J, Berthomé R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18:656–660
Amako K, Chen GX, Asade K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35:497–504
Arce DP, Godoy AV, Tsuda K, Yamazaki K, Valle EM, Iglesias MJ, Di Mauro MF, Casalongué CA (2010) The analysis of an Arabidopsis triple knock-down mutant reveals functions for MBF1 genes under oxidative stress conditions. J Plant Phys 167:194–200
Bartoli CG, Yu J, Gómez F, Fernández L, McIntosh L, Foyer CH (2006) Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J Exp Bot 57:1621–1631
Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391
Bellincampi D, Dipierro N, Salvi G, Cervone F, De LG (2000) Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol 122:1379–1385
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677
Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119
Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743
Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285
Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 4:373–385
Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856
Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439
Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C et al (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300
Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545
Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641
Potters G, Pasternak TP, Guisez Y, Jansen MA (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Env 32:158–169
Rao MV, Palijyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136
Savaldi-Goldstein S, Baiga TG, Pojer F, Dabi T, Butterfield C, Parry G, Santner A, Dharmasiri N, Tao Y, Estelle M et al (2008) New auxin analogs with growth-promoting effects in intact plants reveal a chemical strategy to improve hormone delivery. Proc Natl Acad Sci USA 105:15190–15195
Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66:361–378
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Tossi V, Cassia R, Lamattina L (2009) Apocynin-induced nitric oxide production confers antioxidant protection in maize leaves. J Plant Phys 166:1336–1341
Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EA (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253
Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 22:377–383
Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317
Acknowledgments
We thank Dr. Mark Estelle for the mutants and helpful discussions concerning on the mechanism of auxin perception and Gustavo Gergoff for his critical reading of the manuscript. This work was supported by grants from CONICET, Universidad Nacional de Mar del Plata and ANPCyT. C.C, M.C.T. and C.G.B. are researchers from CONICET. M.J.I and S.D are postgraduate fellows from the same Institution.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Iglesias, M.J., Terrile, M.C., Bartoli, C.G. et al. Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis . Plant Mol Biol 74, 215–222 (2010). https://doi.org/10.1007/s11103-010-9667-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-010-9667-7