• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of plantsigLink to Publisher's site
Plant Signal Behav. Mar 2011; 6(3): 452–454.
Published online Mar 1, 2011. doi:  10.4161/psb.6.3.14676
PMCID: PMC3142437

Auxin and salicylic acid signalings counteract during the adaptive response to stress

Abstract

In a previous publication, we performed a phenotypic characterization of Arabidopsis auxin receptor mutants grown under oxidative and salt stresses. In particular, the double mutant for TIR1 and AFB2 receptors, tir1 afb2 displayed increased tolerance against salinity measured as germination rate, root elongation and chlorophyll content. Here, it is reported that salicylic acid (SA)-treated tir1 afb2 mutant shows enhanced transcript level of a pathogenesis related gene, PR1. In addition, SA-mediated repression of auxin signaling was also demonstrated. All these findings allow us to suggest that down-regulation of auxin signaling may be a common mechanism within the plant adaptative response against both biotic and abiotic stresses.

Key words: Arabidopsis thaliana, auxin signaling, salicylic acid, stress

The survival of plants to adverse conditions involves the accurate perception and transduction of environmental signals to switch on defense and adaptative responses. In general, the spread of information about environmental changes is through plant hormones, which integrate these stimuli into developmental programs. Interestingly, auxin widely recognized as a key growth regulator is nowadays emerging as a new player in the defense response against biotic and abiotic stresses.1,2 Auxin perception is due to members of a small family of F-box proteins, TIR1 and its paralogs AFB1-3.35 Auxin binding to SCFTIR1-AFBs results in the targeted degradation of Aux/IAA transcriptional repressors via SCF E3-ubiquitin ligase proteasome pathway.6 Thereafter, Aux/IAA degradation promotes activation of Auxin Response Factors (ARFs) and the consequent expression of auxin-responsive genes.7

Previously, we demonstrated the participation of TIR1/AFB auxin receptors in the plant defense response against oxidative and salt stresses by a genetic approach. We found that the double mutant, tir1 afb2, shows tolerance to salt stresses judged by increased germination rate, root elongation and chlorophyll content. Furthermore, GST1, APX1 and Zat12 were upregulated in tir1 afb2 under salinity, suggesting an auxin-mediated negative regulation of the plant defense response against abiotic stress. Hence, in this addendum we explored the expression of the pathogenesis related (PR) marker, PR1, as a salicylic acid (SA)-induced gene in tir1 afb2 mutant plants to get insights on the general role that auxin signaling may play in stressed plants. SA is a key mediator of basal resistance responses against biotrophic pathogens. Thus, ten-day-old Arabidopsis thaliana plants grown on ATS agar medium were transferred to liquid ATS medium containing 1 mM SA for 17 h and incubated in the growth chamber.

Figure 1 shows that PR-1 was induced 3.5-folds in SA-treated tir1 afb2 compared with SA-treated wild-type plants, indicating that auxin signaling might interfere with SA-regulated PR-1 induction. Coincidently, PR-1 is also significantly induced in Arabidopsis mutant plants with reduced IAA levels.1 Thus, auxin and SA signaling pathways seem to be mutually antagonistic because a negative effect of SA on auxin signaling has been previously reported in reference 8. Multiple auxin-related genes, including TIR1 are downregulated in response to SA. Therefore, we explored TIR1 level in TIR1 translational GUS fusion seedlings, pTIR1:cTIR1-GUS after SA treatment. In this line, GUS enzyme is fused to the C-terminal region of TIR1 receptor protein under the control of its natural promoter.9 Six-day-old pTIR1:cTIR1-GUS transgenic seedlings were transferred into liquid ATS medium supplemented or not with 1 mM SA for 5 h and incubated under light and mild shaking. GUS activity was evidenced by the incubation with the substrate X-Gluc at 37°C in the dark.

Figure 1
PR1 expression is upregulated in SA-treated tir1 afb2 mutant. Ten-day-old tir1 afb2 and WT seedlings grown in ATS medium were transferred to 1 mM SA treatment for 17 h under 120 µmol photons m−2 s−1 with 16 h photoperiod at 23°C. ...

Figure 2 shows a strong reduction of GUS activity in SA-treated seedlings, indicating a SA-mediated downregulation of TIR1. These data suggest that SA might inhibit auxin signaling by a translational repression of TIR1/AFB auxin receptors during stress. In the same direction, Wang et al.10 demonstrated that the inhibitory effect on auxin response constitutes part of the SA-mediated disease resistance mechanism in Arabidopsis.

Figure 2
SA triggers repression of TIR1 receptor. Six-d-old pTIR1:cTIR1-GUS transgenic seedlings grown in ATS agar medium were transferred into liquid ATS medium supplemented with 1 mM SA and incubated with mild shaking for 6 h in the growth chamber. After treatment, ...

Thus, despite the differences in defense pathways between biotic and abiotic stresses, downregulation of auxin signaling may be considered a common strategy that plants adopt to deal with a broad spectrum of adverse conditions. It should be noted that SA-mediated repression of auxin response may be just one of the diverse molecular mechanisms that may operate throughout auxin in Arabidopsis plants. For instance, the microRNA miR393 which has emerged as a key regulator of TIR1, AFB2 and AFB3 is induced in Arabidopsis plants in response to flagellin and Pseudomonas syringae as well as under different abiotic stresses, such as cold, dehydration and salinity.11 Furthermore, Navarro et al.12 reported that miR393-mediated repression of auxin receptors constitutes a plant strategy to attenuate infection. In addition, different members of the auxin-responsive GH3 gene family that encode IAA-conjugating enzymes and therefore modulate endogenous auxin pool have been associated to plant defense responses. For example, Arabidopsis mutant, wes 1-D, exhibites enhanced tolerance to drought, freezing temperature, salinity and pathogen infection.1 GH3.5 is reported as a regulator of both, auxin and SA signalings during plant-pathogen interactions.13 The activation of different GH3s resulted in increased tolerance against pathogens and drought in rice.1417 Additionally, auxin availability could be perturbed through an effect on auxin carriers under stress.18 Not surprisingly, auxin transport is inhibited by flavonoids, one of the plant metabolites synthesized in response to environmental signals.19 Grunewald et al.20 revealed that nematodes manipulate expression and subcelullar localization of PINs proteins to facilitate infection in Arabidopsis leaves.

In conclusion, all these findings allowed us to propose a hypothetical model where the adaptative response to biotic and abiotic stress seems to be mediated in part, through the negative regulation of auxin which may include auxin transport, homeostasis and signaling (Fig. 3). Reorganization of plant growth and developmental programs are critical to maximize plant survival under stress. Future research will reveal the intrincated mechanisms and switches that plants adopt to develop such highly dynamic responses.

Figure 3
A hypothetical model shows the participation of TIR1/AFB2-mediated auxin signaling during environmental stress. Endogenous auxin pool may be regulated by GH3 genes which encode auxin-conjugating enzymes. Auxin availability may be also linked to auxin ...

Acknowledgements

This work was supported by grants from the Universtiy of Mar del Plata, ANPCyT, CONICET. M.C.T. and C.C. are members of the research staff of CONICET. M.J.I. is a graduate fellow of the same institution. Authors wish to thank Dr. Mark Estelle for pTIR1:TIR1c-GUS seeds and Dr. Diego Fiol for his critical reading of the manuscript.

References

1. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, et al. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem. 2007;282:10036–10046. [PubMed]
2. Wolters H, Jurgens G. Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet. 2009;10:305–317. [PubMed]
3. Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature. 2005;435:441–445. [PubMed]
4. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell. 2005;9:109–119. [PubMed]
5. Kepinski S, Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 2005;435:446–451. [PubMed]
6. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature. 2001;414:271–276. [PubMed]
7. Hagen G, Guilfoyle T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol. 2002;49:373–385. [PubMed]
8. Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2006;2:123. [PMC free article] [PubMed]
9. Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, et al. Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA. 2009;106:22540–22545. [PMC free article] [PubMed]
10. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol. 2007;17:1784–1790. [PubMed]
11. Sunkar R, Chinnusamy V, Zhu J, Zhu JK. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 2007;12:301–309. [PubMed]
12. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science. 2006;312:436–439. [PubMed]
13. Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, et al. Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol. 2007;145:450–464. [PMC free article] [PubMed]
14. Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, et al. Activation of the indole-3-acetic acid amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell. 2008;20:228–240. [PMC free article] [PubMed]
15. Domingo C, Andres F, Tharreau D, Iglesias DJ, Talon M. Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant Microbe Interact. 2009;22:201–210. [PubMed]
16. Zhang S, Li C, Cao J, Zhang Y, Zhang S, Xia Y, et al. Altered architecture and enhanced drought tolerance in rice via the downregulation of IAA by TLD1/OsGH3.13 activation. Plant Physiol. 2009;151:1889–1901. [PMC free article] [PubMed]
17. Fu J, Liu H, Li Y, Yu H, Li X, Xiao J, et al. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol. 2010;155:589–602. [PMC free article] [PubMed]
18. Shibasaki K, Uemura M, Tsurumi S, Rahman A. Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell. 2009;21:3823–3838. [PMC free article] [PubMed]
19. Peer WA, Murphy AS. Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci. 2007;12:556–563. [PubMed]
20. Grunewald W, Cannoot B, Friml J, Gheysen G. Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog. 2009;5:1000266. [PMC free article] [PubMed]

Articles from Plant Signaling & Behavior are provided here courtesy of Landes Bioscience
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...