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• W2052001330 abstract "Plant growth is adaptively modulated in response to environmental change. The phytohormone gibberellin (GA) promotes growth by stimulating destruction of the nuclear growth-repressing DELLA proteins [1Richards D.E. King K.E. Ait-ali T. Harberd N.P. How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling.Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 67-88Crossref PubMed Scopus (396) Google Scholar, 2Peng J. Carol P. Richards D.E. King K.E. Cowling R.J. Murphy G.P. Harberd N.P. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses.Genes Dev. 1997; 11: 3194-3205Crossref PubMed Scopus (810) Google Scholar, 3Peng J. Richards D.E. Hartley N.M. Murphy G.P. Devos K.M. Flintham J.E. Beales J. Fish L.J. Worland A.J. Pelica F. et al.“Green Revolution” genes encode mutant gibberellin response modulators.Nature. 1999; 400: 256-261Crossref PubMed Scopus (1344) Google Scholar, 4Harberd N.P. Relieving DELLA restraint.Science. 2003; 299: 1853-1854Crossref PubMed Scopus (74) Google Scholar, 5Sasaki A. Itoh H. Gomi K. Ueguchi-Tanaka M. Ishiyama K. Kobayashi M. Jeong D.H. An G. Kitano H. Ashikari M. et al.Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant.Science. 2003; 299: 1896-1898Crossref PubMed Scopus (470) Google Scholar, 6Ueguchi-Tanaka M. Ashikari M. Nakajima M. Itoh H. Katoh E. Kobayashi M. Chow T.-y. Hsing Y.C. Kitano H. Yamaguchi I. et al.GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin.Nature. 2005; 437: 693-698Crossref PubMed Scopus (824) Google Scholar, 7Cheng H. Qin L. Lee S. Fu X. Richards D.E. Cao D. Luo D. Harberd N.P. Peng J. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function.Development. 2004; 131: 1055-1064Crossref PubMed Scopus (381) Google Scholar], thus providing a mechanism for environmentally responsive growth regulation [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar, 9Achard P. Baghour M. Chapple A. Hedden P. Van Der Straeten D. Genschik P. Moritz T. Harberd N.P. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.Proc. Natl. Acad. Sci. USA. 2007; 104: 6484-6489Crossref PubMed Scopus (224) Google Scholar]. Furthermore, DELLAs promote survival of adverse environments [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]. However, the relationship between these survival and growth-regulatory mechanisms was previously unknown. Here, we show that both mechanisms are dependent upon control of the accumulation of reactive oxygen species (ROS). ROS are small molecules generated during development and in response to stress that play diverse roles as eukaryotic intracellular second messengers [10Finkel T. Oxygen radicals and signalling.Curr. Opin. Cell Biol. 1998; 10: 248-253Crossref PubMed Scopus (978) Google Scholar]. We show that Arabidopsis DELLAs cause ROS levels to remain low after either biotic or abiotic stress, thus delaying cell death and promoting tolerance. In essence, stress-induced DELLA accumulation elevates the expression of genes encoding ROS-detoxification enzymes, thus reducing ROS levels. In accord with recent demonstrations that ROS control root cell expansion [11Gapper C. Dolan L. Control of plant development by reactive oxygen species.Plant Physiol. 2006; 141: 341-345Crossref PubMed Scopus (366) Google Scholar, 12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar], we also show that DELLAs regulate root-hair growth via a ROS-dependent mechanism. We therefore propose that environmental variability regulates DELLA activity [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar] and that DELLAs in turn couple the downstream regulation of plant growth and stress tolerance through modulation of ROS levels. Plant growth is adaptively modulated in response to environmental change. The phytohormone gibberellin (GA) promotes growth by stimulating destruction of the nuclear growth-repressing DELLA proteins [1Richards D.E. King K.E. Ait-ali T. Harberd N.P. How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling.Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 67-88Crossref PubMed Scopus (396) Google Scholar, 2Peng J. Carol P. Richards D.E. King K.E. Cowling R.J. Murphy G.P. Harberd N.P. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses.Genes Dev. 1997; 11: 3194-3205Crossref PubMed Scopus (810) Google Scholar, 3Peng J. Richards D.E. Hartley N.M. Murphy G.P. Devos K.M. Flintham J.E. Beales J. Fish L.J. Worland A.J. Pelica F. et al.“Green Revolution” genes encode mutant gibberellin response modulators.Nature. 1999; 400: 256-261Crossref PubMed Scopus (1344) Google Scholar, 4Harberd N.P. Relieving DELLA restraint.Science. 2003; 299: 1853-1854Crossref PubMed Scopus (74) Google Scholar, 5Sasaki A. Itoh H. Gomi K. Ueguchi-Tanaka M. Ishiyama K. Kobayashi M. Jeong D.H. An G. Kitano H. Ashikari M. et al.Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant.Science. 2003; 299: 1896-1898Crossref PubMed Scopus (470) Google Scholar, 6Ueguchi-Tanaka M. Ashikari M. Nakajima M. Itoh H. Katoh E. Kobayashi M. Chow T.-y. Hsing Y.C. Kitano H. Yamaguchi I. et al.GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin.Nature. 2005; 437: 693-698Crossref PubMed Scopus (824) Google Scholar, 7Cheng H. Qin L. Lee S. Fu X. Richards D.E. Cao D. Luo D. Harberd N.P. Peng J. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function.Development. 2004; 131: 1055-1064Crossref PubMed Scopus (381) Google Scholar], thus providing a mechanism for environmentally responsive growth regulation [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar, 9Achard P. Baghour M. Chapple A. Hedden P. Van Der Straeten D. Genschik P. Moritz T. Harberd N.P. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.Proc. Natl. Acad. Sci. USA. 2007; 104: 6484-6489Crossref PubMed Scopus (224) Google Scholar]. Furthermore, DELLAs promote survival of adverse environments [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]. However, the relationship between these survival and growth-regulatory mechanisms was previously unknown. Here, we show that both mechanisms are dependent upon control of the accumulation of reactive oxygen species (ROS). ROS are small molecules generated during development and in response to stress that play diverse roles as eukaryotic intracellular second messengers [10Finkel T. Oxygen radicals and signalling.Curr. Opin. Cell Biol. 1998; 10: 248-253Crossref PubMed Scopus (978) Google Scholar]. We show that Arabidopsis DELLAs cause ROS levels to remain low after either biotic or abiotic stress, thus delaying cell death and promoting tolerance. In essence, stress-induced DELLA accumulation elevates the expression of genes encoding ROS-detoxification enzymes, thus reducing ROS levels. In accord with recent demonstrations that ROS control root cell expansion [11Gapper C. Dolan L. Control of plant development by reactive oxygen species.Plant Physiol. 2006; 141: 341-345Crossref PubMed Scopus (366) Google Scholar, 12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar], we also show that DELLAs regulate root-hair growth via a ROS-dependent mechanism. We therefore propose that environmental variability regulates DELLA activity [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar] and that DELLAs in turn couple the downstream regulation of plant growth and stress tolerance through modulation of ROS levels. In adverse environmental conditions, DELLAs accumulate and both restrain growth and promote plant survival [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]. It was previously unclear whether the unknown mechanisms underlying these two phenomena are distinct or coupled. We therefore first compared the relative contributions of individual DELLAs to the control of plant growth and to the survival of adversity. We measured growth (plant height), developmental rate (timing of floral transition), and stress tolerance (relative survival of salt-stressed plants) of Arabidopsis mutants lacking various single, double, triple, or quadruple combinations of DELLAs (GAI, RGA, RGL1, RGL2) in the gibberellin (GA)-deficient ga1-3 background [7Cheng H. Qin L. Lee S. Fu X. Richards D.E. Cao D. Luo D. Harberd N.P. Peng J. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function.Development. 2004; 131: 1055-1064Crossref PubMed Scopus (381) Google Scholar] (Figure S1 available online). Strikingly, we observed a strong correlation between the relative growth and developmental effects of DELLAs and the degree of salt-stress tolerance that they confer (ρ = −0.96 and 0.94, respectively), suggesting a common regulatory mechanism (Figure 1A). To reveal the molecular basis of this regulatory mechanism, we performed a transcriptome-profiling analysis with complete Arabidopsis microarray (CATMA) chips [13Crowe M.L. Serizet C. Thareau V. Aubourg S. Rouze P. Hilson P. Beynon J. Weisbeek P. van Hummelen P. Reymond P. et al.CATMA: A complete Arabidopsis GST database.Nucleic Acids Res. 2003; 31: 156-158Crossref PubMed Scopus (127) Google Scholar, 14Hilson P. Allemeersch J. Altmann T. Aubourg S. Avon A. Beynon J. Bhalerao R.P. Bitton F. Caboche M. Cannoot B. et al.Versatile gene-specific sequence tags for Arabidopsis functional genomics: Transcript profiling and reverse genetics applications.Genome Res. 2004; 14: 2176-2189Crossref PubMed Scopus (255) Google Scholar]. Transcript levels of the wild-type (WT), ga1-3, and ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 (also called ga1-3 quadruple-DELLA) were analyzed in response to short exposure (30 and 60 min) of plants to 200 mM NaCl (and controls without salt treatment). Statistical analysis of comparisons (see the Supplemental Data) revealed that 2.2% of the 24,576 Arabidopsis genes represented on the chip displayed DELLA-dependent changes in mRNA levels (either constitutively and/or salt induced; Table S1). In order to identify common set of genes whose expression was affected by various stresses, we compared the expression profile of DELLA-regulated genes with publicly available microarray data (http://urgv.evry.inra.fr/CATdb) in which the effects of salt, mannitol, or the pathogen Erwinia amylovora were surveyed (Figure 1B). Surprisingly, this analysis led to the identification of 126 genes (23.2% of all DELLA-regulated genes) of which a wide range (more than one-third) of genes that respond to oxidative stress. Among those, we found that the genes encoding the antioxidant systems such as the Cu/Zn superoxide dismutases (Cu/Zn-SOD), catalases, peroxidases, or glutathione S-transferases [15Apel K. Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction.Annu. Rev. Plant Biol. 2004; 55: 373-399Crossref PubMed Scopus (7177) Google Scholar] were upregulated in plants that accumulate DELLAs (Table S2). In addition, most of the DELLA-regulated genes identified did not display constitutive changes but rather earlier induction or repression to salt, indicating that DELLAs sensitize plants to stress (Figure 1B). Besides, salt or mannitol treatment enhances accumulation of DELLAs (via reduction in GA levels [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]) (Figure 1C). Thus, our findings suggest that stress-induced DELLA accumulation activates a complex genetic regulation network to control in part the amount of ROS. We next showed that DELLA-dependent regulation of “antioxidant” genes affects cellular ROS levels, by ester-loading 5-(and 6)-carboxy-2′,7′-dichlorodihydrofluorescein diacetate (H2DCFDA), a ROS-sensitive dye with good intracellular retention, into growing roots [16Jiang K. Meng Y.L. Feldman L.J. Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment.Development. 2003; 130: 1429-1438Crossref PubMed Scopus (151) Google Scholar]. In the absence of salt stress, WT (Ler) and ga1-3 quadruple-DELLA mutant roots exhibited higher basal levels of ROS than did ga1-3 roots (Figure 2A, Figure S2). Application of 50 mM NaCl increased ROS levels within WT roots and even more so within ga1-3 quadruple-DELLA roots. In accordance, spy-3 mutant roots (SPINDLY, a negative regulator of GA signaling [17Jacobsen S.E. Olszewski N.E. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction.Plant Cell. 1993; 8: 887-896Google Scholar]) also exhibited higher levels of ROS than did WT (Col) roots in the presence of NaCl (Figure 2B). In contrast, there was no detectable ROS accumulation within salt-treated ga1-3 roots (Figure 2A). Combined treatment of ga1-3 with both GA and NaCl resulted in an increase in ROS levels, similar to that seen with salt-treated WT roots (Figure S2A). Furthermore, a genetic analysis indicates that it is the combined effect of GAI and RGA that predominate in salt-activated ROS accumulation (Figure S2B). A comparable observation was obtained with diaminobenzidine (DAB, a hydrogen peroxide [H2O2]-sensitive dye) or nitroblue tetrazolium (NBT, a superoxide [O2−]-sensitive dye) in salt-treated leaves (Figures S3A and S3B). Thus, in line with the transcriptome data, DELLA activity reduces ROS levels of salt-treated plants. The likely source of the ROS generated in the above experiments (Figure 2A) is an NADPH oxidase [15Apel K. Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction.Annu. Rev. Plant Biol. 2004; 55: 373-399Crossref PubMed Scopus (7177) Google Scholar]. The NADPH-oxidase products of the Arabidopsis AtrbohD and AtrbohF genes are known to produce ROS after pathogen attack or abscisic acid (ABA) treatment [18Torres M.A. Dangl J.L. Jones J.D.G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Proc. Natl. Acad. Sci. USA. 2002; 99: 517-522Crossref PubMed Scopus (1122) Google Scholar, 19Torres M.A. Jones J.D.G. Dangl J.L. Reactive oxygen species signalling in response to pathogens.Plant Physiol. 2006; 141: 373-378Crossref PubMed Scopus (1077) Google Scholar, 20Kwak J.M. Mori I.C. Pei Z.M. Leonhardt N. Torres M.A. Dangl J. Bloom R.E. Bodde S. Jones J.D.G. Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis.EMBO J. 2003; 22: 2623-2633Crossref PubMed Scopus (1173) Google Scholar]. After salt treatment, we found that AtrbohD, but not AtrbohF, is required for ROS production (Figure 2B; Figure S4A). Accordingly, application of diphenylene iodonium (DPI, inhibitor of flavoprotein activity such as NADPH oxidases [19Torres M.A. Jones J.D.G. Dangl J.L. Reactive oxygen species signalling in response to pathogens.Plant Physiol. 2006; 141: 373-378Crossref PubMed Scopus (1077) Google Scholar]) substantially prevented ROS accumulation in WT and ga1-3 quadruple-DELLA mutant roots (Figure 2A). In addition, a loss-of-function AtrbohD mutation (atrbohD) abolished ROS accumulation of spy-3 (in spy-3 atrbohD; Figure 2B). Interestingly, DELLAs do not modulate AtrbohD and AtrbohF transcript levels or NADPH-oxidase activity in fractionated plasma membranes (Figures S4A and S4B). However, O2− generating activity in leaf discs was found to be more than 4-fold and 5-fold higher in WT and ga1-3 quadruple-DELLA mutant plants, respectively, compared with ga1-3 plants (Figure S4C). In contrast, O2− production was found to be very similar upon potassium-cyanide treatment (KCN, inhibitor of Cu/Zn-SOD activity [21Kliebenstein D.J. Monde R.A. Last R.L. Superoxide dismutase in Arabidopsis: An electic enzyme family with disparate regulation and protein localization.Plant Physiol. 1998; 118: 637-650Crossref PubMed Scopus (443) Google Scholar]) or H2O2 (inhibitor of both Cu/Zn-SOD and Fe-SOD activities [21Kliebenstein D.J. Monde R.A. Last R.L. Superoxide dismutase in Arabidopsis: An electic enzyme family with disparate regulation and protein localization.Plant Physiol. 1998; 118: 637-650Crossref PubMed Scopus (443) Google Scholar]), suggesting that DELLAs control ROS accumulation via their effects on SOD activity. Arabidopsis Cu/Zn-SOD are encoded by three genes (CSD1, CSD2, and CSD3) [21Kliebenstein D.J. Monde R.A. Last R.L. Superoxide dismutase in Arabidopsis: An electic enzyme family with disparate regulation and protein localization.Plant Physiol. 1998; 118: 637-650Crossref PubMed Scopus (443) Google Scholar] and, on the basis of our microarray data, CSD1 and CSD2 were downregulated in ga1-3 quadruple-DELLA mutant (Table S2). Indeed, we confirmed that the levels of both transcripts and proteins were respectively reduced in ga1-3 quadruple-DELLA mutant and increased in ga1-3 in comparison to WT plants (Figure S5). In consequence, SOD and catalase activities were enhanced in ga1-3 plants compared to WT plants (Figure S5). Thus, DELLAs restrain stress-induced ROS accumulation by acting on the ROS scavenging system. ROS generation is correlated with plant cell death [15Apel K. Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction.Annu. Rev. Plant Biol. 2004; 55: 373-399Crossref PubMed Scopus (7177) Google Scholar]. We next investigated H2O2-induced cell death in WT, ga1-3, and ga1-3 quadruple-DELLA mutant seedling roots, by using propidium iodide (PI), a nucleic-acid stain that can only penetrate cells with damaged or leaking cell membranes [22Cutler S.R. Somerville C.R. Imaging plant cell death: GFP-Nit1 aggregation marks an early step of wound and herbicide induced cell death.BMC Plant Biol. 2005; 5: 4Crossref PubMed Scopus (30) Google Scholar]. Whereas ga1-3 quadruple-DELLA and WT roots began to exhibit cell death within 30 min and 1 hr of H2O2 treatment, respectively, ga1-3 roots did so only after 2 hr (Figure 2C). It is noteworthy that H2O2 treatment had no effect on RGA stability and thus likely on DELLAs in general (Figure S6). Thus, DELLAs delay H2O2-induced cell death, thereby promoting stress tolerance [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]. Necrotrophic pathogens often promote host cell death through generation of ROS [18Torres M.A. Dangl J.L. Jones J.D.G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Proc. Natl. Acad. Sci. USA. 2002; 99: 517-522Crossref PubMed Scopus (1122) Google Scholar, 19Torres M.A. Jones J.D.G. Dangl J.L. Reactive oxygen species signalling in response to pathogens.Plant Physiol. 2006; 141: 373-378Crossref PubMed Scopus (1077) Google Scholar]. For example, the necrotrophic fungal Botrytis cinerea causes severe diseases in a wide range of plant species, promoting plant cell death through ROS generation [23Mengiste 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: 2551-2565Crossref PubMed Scopus (378) Google Scholar]. We therefore investigated the contribution of DELLAs to pathogen-induced cell death. We found that 2 days after inoculation with Botrytis, ga1-3 quadruple-DELLA mutant leaves displayed substantially higher cell-death rate than did Botrytis-inoculated WT control leaves (Figures 3A and 3D), the magnitude of these damages being proportional to the amount of H2O2 accumulated (Figures 3B and 3C). In contrast, Botrytis-inoculated ga1-3 leaves exhibited no damaged cell (Figures 3A and 3D) and no detectable H2O2 accumulation (Figures 3B and 3C). Finally, as upon NaCl treatment, AtrbohD mutation abolished the accumulation in H2O2 of spy-3 in Botrytis-inoculated spy-3 atrbohD leaves (Figures 3E and 3F). Thus, DELLAs promote survival of adversity by restraining ROS inducing cell death. The results presented in Figure 1A suggest a common regulatory mechanism for DELLA-dependent controls of plant growth and stress tolerance. ROS play diverse roles in plant biology [11Gapper C. Dolan L. Control of plant development by reactive oxygen species.Plant Physiol. 2006; 141: 341-345Crossref PubMed Scopus (366) Google Scholar, 15Apel K. Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction.Annu. Rev. Plant Biol. 2004; 55: 373-399Crossref PubMed Scopus (7177) Google Scholar, 19Torres M.A. Jones J.D.G. Dangl J.L. Reactive oxygen species signalling in response to pathogens.Plant Physiol. 2006; 141: 373-378Crossref PubMed Scopus (1077) Google Scholar]. In addition to their well-known involvement in stress tolerance, ROS function as second messengers in ABA signaling in guard cells [20Kwak J.M. Mori I.C. Pei Z.M. Leonhardt N. Torres M.A. Dangl J. Bloom R.E. Bodde S. Jones J.D.G. Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis.EMBO J. 2003; 22: 2623-2633Crossref PubMed Scopus (1173) Google Scholar] and, like GA, control root cell growth [11Gapper C. Dolan L. Control of plant development by reactive oxygen species.Plant Physiol. 2006; 141: 341-345Crossref PubMed Scopus (366) Google Scholar, 12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar, 24Fu X. Harberd N.P. Auxin promotes Arabidopsis root growth by modulating gibberellin response.Nature. 2003; 421: 740-743Crossref PubMed Scopus (559) Google Scholar]. To determine whether DELLAs restrain growth and promotes survival of adversity via a common mechanism, we evaluated the contribution of ROS to GA-mediated root and root-hair growth. We found that the root growth of ga1-3 seedlings (which accumulate lower basal levels of ROS than the WT, see Figure 2A) was more resistant to the inhibitory effect of DPI than that of the WT (Figure 4A). In consequence, although ga1-3 roots are shorter than those of the WT [24Fu X. Harberd N.P. Auxin promotes Arabidopsis root growth by modulating gibberellin response.Nature. 2003; 421: 740-743Crossref PubMed Scopus (559) Google Scholar], their length was almost identical upon 0.1 μM DPI treatment (Figure 4A). In contrast, the root growth of ga1-3 quadruple-DELLA mutant seedlings was slightly but statistically more sensitive to DPI than that of the WT. For higher concentrations of DPI (more than 1 μM), the cell elongation characteristic of DELLA-deficient mutants was abolished, phenocopying the ga1-3 mutant (Figure S7 and Table S3). Moreover, we found that ga1-3 seedlings exhibited shorter root hairs and ga1-3 quadruple-DELLA longer root hairs than those of WT seedlings (Figure 4B). Finally, the rhd2-1 mutation (ROOT HAIR DEFECTIVE2 [RHD2] gene encodes the NADPH oxidase C [12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar]) suppressed the root-hair growth of spy-3 (in spy-3 rhd2-1; Figure 4B). Thus, ROS contribute at least in part in the GA-mediated root cell growth. Although it was previously clear that DELLAs are repressors of GA responses, the mechanism by which DELLAs mediate these effects was unclear. Whereas previous reports have suggested that GA might modulate ROS levels [25Schopfer P. Plachy C. Frahry G. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid.Plant Physiol. 2001; 125: 1591-1602Crossref PubMed Scopus (419) Google Scholar, 26Fath A. Bethke P.C. Jones R.L. Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic-acid-induced programmed cell death in barley aleurone.Plant Physiol. 2001; 126: 156-166Crossref PubMed Scopus (184) Google Scholar], we here show that two key DELLA-dependent GA responses (stress survival and growth processes) are regulated via a common mechanism. DELLAs modulate ROS levels through the regulation of gene transcripts encoding for ROS detoxification enzymes. DELLAs thus repress ROS accumulation (and as a consequence ROS-induced cell death) and hence enhance tolerance to both biotic and abiotic stresses. DELLA-dependent modulation of ROS accumulation also contributes to the GA-mediated cell elongation that is an important driver of growth. The precise way in which GA-mediated regulation of ROS levels acts as a biological signal in plants remains unclear. Perhaps ROS act as second messengers and modulate Ca2+ content, as in the stomatal guard cell or in the root hair [12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar, 20Kwak J.M. Mori I.C. Pei Z.M. Leonhardt N. Torres M.A. Dangl J. Bloom R.E. Bodde S. Jones J.D.G. Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis.EMBO J. 2003; 22: 2623-2633Crossref PubMed Scopus (1173) Google Scholar, 27McCubbin A.G. Ritchie S.M. Swanson S.J. Gilroy S. The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function.Plant J. 2004; 39: 206-218Crossref PubMed Scopus (51) Google Scholar], or perhaps they allow the cell wall to expand by decreasing the resistance of the wall to the pressure [11Gapper C. Dolan L. Control of plant development by reactive oxygen species.Plant Physiol. 2006; 141: 341-345Crossref PubMed Scopus (366) Google Scholar]. Whatever the mechanism, it is clear that stress-related environmental regulation of GA signaling contributes to fine tuning of ROS levels, thereby regulating cell growth and stress tolerance. Arabidopsis thaliana lines used in this study were derived either from the Landsberg erecta (Ler) (ga1-3, gai, multiple-DELLA mutant lines) [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar] or Columbia (Col) (spy-3, atrbohD, atrbohF, and rhd2-1) [12Foreman J. Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. et al.Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1599) Google Scholar, 17Jacobsen S.E. Olszewski N.E. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction.Plant Cell. 1993; 8: 887-896Google Scholar, 20Kwak J.M. Mori I.C. Pei Z.M. Leonhardt N. Torres M.A. Dangl J. Bloom R.E. Bodde S. Jones J.D.G. Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis.EMBO J. 2003; 22: 2623-2633Crossref PubMed Scopus (1173) Google Scholar] ecotype. atrbohD spy-3, atrbohF spy-3, and rhd2-1 spy-3 double mutants were generated by crossing of corresponding single-mutant line (polymerase chain reaction [PCR]-based screening and sequencing were used for confirmation). The plant height (measured at 6 weeks) and bolting time were determined on a population of 30 plants grown on soil in controlled environment chambers (16 hr photoperiod; 20°C). The salt-survival experiment performed on a population of at least 48 plants for each of the 17 genotypes was as previously described [8Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals.Science. 2006; 331: 91-94Crossref Scopus (966) Google Scholar]. The Rank correlation coefficients were calculated with the CORREL PEARSON function of Excel. For root-length determination, the lengths of 7-day-old roots of at least 30 seedlings (grown vertically on growth medium (GM)-agar plates [9Achard P. Baghour M. Chapple A. Hedden P. Van Der Straeten D. Genschik P. Moritz T. Harberd N.P. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.Proc. Natl. Acad. Sci. USA. 2007; 104: 6484-6489Crossref PubMed Scopus (224) Google Scholar]) were measured 5 days after transfer to DPI (concentration as indicated). The experiment was repeated twice. Root hairs were measured from 7-day-old seedlings grown on half concentrated GM medium. Images of root were captured with a Nikon E800 microscope. Root hairs that were in focus throughout their length were measured with Image J 1.33u (W. Rasband) software. For each line, at least 100 root hairs were measured. Microarray analysis was carried with the CATMA array [13Crowe M.L. Serizet C. Thareau V. Aubourg S. Rouze P. Hilson P. Beynon J. Weisbeek P. van Hummelen P. Reymond P. et al.CATMA: A complete Arabidopsis GST database.Nucleic Acids Res. 2003; 31: 156-158Crossref PubMed Scopus (127) Google Scholar, 14Hilson P. Allemeersch J. Altmann T. Aubourg S. Avon A. Beynon J. Bhalerao R.P. Bitton F. Caboche M. Cannoot B. et al.Versatile gene-specific sequence tags for Arabidopsis functional genomics: Transcript profiling and reverse genetics applications.Genome Res. 2004; 14: 2176-2189Crossref PubMed Scopus (255) Google Scholar], containing 24,576 gene-specific tags from Arabidopsis thaliana. RNA samples from two independent biological replicates were used for each comparison, with dye-swap technical replicates (i.e., four hybridizations per comparison). The labeling, hybridizations, and scanning were performed as previously described [28Lurin C. Andres C. Aubourg S. Bellaoui M. Bitton F. Bruyere C. Caboche M. Debast C. Gualberto J. Hoffmann B. et al.Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis.Plant Cell. 2004; 16: 2089-2103Crossref PubMed Scopus (923) Google Scholar]. Normalization and statistical analysis were based on two dye swaps [28Lurin C. Andres C. Aubourg S. Bellaoui M. Bitton F. Bruyere C. Caboche M. Debast C. Gualberto J. Hoffmann B. et al.Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis.Plant Cell. 2004; 16: 2089-2103Crossref PubMed Scopus (923) Google Scholar]. To determine differentially expressed genes, we performed a paired t test on the log ratios, assuming that the variance of the log ratios was the same for all genes. The raw p values were adjusted by the Bonferroni method, which controls the FWER [29Ge Y. Dudoit S. Speed T.P. Resampling-based multiple testing for microarray data analysis.Test. 2003; 12: 1-77Crossref Scopus (351) Google Scholar]. We considered as being differentially expressed the genes with a FWER at threshold of 5%. The Bonferroni method (with a type I error equal to 5%) keeps a strong control of the false positives in a multiple-comparison context [29Ge Y. Dudoit S. Speed T.P. Resampling-based multiple testing for microarray data analysis.Test. 2003; 12: 1-77Crossref Scopus (351) Google Scholar]. Microarray studies and statistical analyses are described in more details in the Supplemental Data. Microarray data from this article were deposited at Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/, no. GSE8556) and at CATdb (http://urgv.evry.inra.fr/CATdb/; Project RS06-07_DELLA) according to the “Minimum Information about a Microarray Experiment” standards. For experiments with H2DCFDA, 7-day-old seedlings were treated with 10 μM DPI (and controls) for 30 min at 22°C and then incubated for 30 min at 4°C in 10 μM H2DCFDA plus NaCl and/or DPI (and controls). Seedlings were then washed with 10 mM MES, 0.1 mM KCl, and 0.1 mM CaCl2 (pH 6.0) and left for 60 min at 22°C before experimentation. Dye excitation was at 488 nm; emitted light was detected at 522 nm. DAB staining was performed on fully expanded leaves treated with NaCl or inoculated with pathogens as previously described [18Torres M.A. Dangl J.L. Jones J.D.G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Proc. Natl. Acad. Sci. USA. 2002; 99: 517-522Crossref PubMed Scopus (1122) Google Scholar]. For the visualization of cell death, 7-day-old seedling roots treated with 2 mM H2O2 were stained with 10 μg/ml PI. For each imaging, at least 20 seedlings or leaves (for each genotype) were analyzed. The experiments were repeated three times. Quantification of the staining (H2DCFDA and DAB staining) was performed with Image J 1.33u (W. Rasband) in arbitrary units (mean ± standard error [SE]). The index of staining was calculated for each image as the average of the index of stained pixels measured in three points inside the stained area minus the average of three points outside the stained area. Botrytis cinerea (2 × 105 spores per ml in potato dextrose broth [Duchefa]) was inoculated by placement of 5 μl droplets onto 6-week-old fully expanded leaves (8 hr photoperiod; 20°C) from at least 30 plants per genotype. The experiment was repeated twice. Cell death was quantified by ion leakage from rosette leaves into 4 ml of distilled water for 3 hr, measured with a conductivity meter (Horiba B173). Mean and SE were calculated from ten leaves per genotype. The experiment was repeated twice. We thank J. Peng for the multiple-DELLA mutant lines, Tp. Sun for the pRGA:GFP-RGA line and the antibody to RGA, L. Dolan for rhd2-1, N.E. Olszewski for spy-3, J.I. Schroeder for atrbohD and atrbohF, T. Heitz for the Botrytis cinerea strain, D. Kliebenstein for the antibody to CSD2, and L. Taconnat for transcriptome. We gratefully acknowledge funding from the Centre National de la Recherche Scientifique, the ANR grant JC07_189599, and the European Molecular Biology Organization Grant ALTF-414-2005. We thank L. Navarro, J.D.G. Jones, and L.J. Sweetlove for comments on the manuscript. Download .pdf (1.1 MB) Help with pdf files Document S1. Additional Results, Additional Experimental Procedures, Seven Figures, and One Table Download .xls (.19 MB) Help with xls files Table S1. List of DELLA-Regulated GenesList of the 597 genes displaying significant differential expression between ga1-3 and the WT (ga1-3) or between ga1-3 quadruple-DELLA and the WT (penta) after 30 min and 1 hr salt treatment (200 mM NaCl) or control (without salt treatment). log2 rat and Bonf Pval represent log2 ratios and p values adjusted by the Bonferroni method, respectively (see Experimental Procedures). Download .xls (.05 MB) Help with xls files Table S2. List of DELLA-Dependent Stress-Regulated GenesList of the 126 DELLA-regulated genes (among the 597 genes identified, Table S1) that coregulate with those of WT Arabidopsis plants that have been treated with salt (NaCl), mannitol (Man), or inoculated with the bacteria Erwinia amylovora (Erw). log2 rat represents log2 ratios between ga1-3 and the WT (ga1-3), between ga1-3 quadruple-DELLA and the WT (penta), or between the treated WT and nontreated WT (Erw/Man/NaCl). Oxidative-stress-response genes are outlined in yellow." @default.
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