Abstract
Plant hormones have a plethora of functions in control of plant development, stress response, and primary metabolism, including nutrient homeostasis. In the plant nutrition, the interplay of hormones with responses to nitrate and phosphate deficiency is well described, but relatively little is known about the interaction between phytohormones and regulation of sulfur metabolism. As for other nutrients, sulfate deficiency results in modulation of root architecture, where hormones are expected to play an important role. Accordingly, sulfate deficiency induces genes involved in metabolism of tryptophane and auxin. Also jasmonate biosynthesis is induced, pointing to the need of increase the defense capabilities of the plants when sulfur is limiting. However, hormones affect also sulfate uptake and assimilation. The pathway is coordinately induced by jasmonate and the key enzyme, adenosine 5′-phosphosulfate reductase, is additionally regulated by ethylene, abscisic acid, nitric oxid, and other phytohormones. Perhaps the most intriguing link between hormones and sulfate assimilation is the fact that the main regulator of the response to sulfate starvation, SULFATE LIMITATION1 (SLIM1) belongs to the family of ethylene related transcription factors. We will review the current knowledge of interplay between phytohormones and control of sulfur metabolism and discuss the main open questions.
Similar content being viewed by others
References
Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci U S A 104:18333–18338
Baek D et al (2010) A stress-inducible sulphotransferase sulphonates salicylic acid and confers pathogen resistance in Arabidopsis. Plant Cell Environ 33:1383–1392
Barlier I et al (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97:14819–14824
Barroso C, Romero LC, Cejudo FJ, Vega JM, Gotor C (1999) Salt-specific regulation of the cytosolic O-acetylserine(thiol)lyase gene from Arabidopsis thaliana is dependent on abscisic acid. Plant Mol Biol 40:729–736
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
Bittner F, Oreb M, Mendel RR (2001) ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. J Biol Chem 276:40381–40384
Blilou I et al (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
Boerjan W et al (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419
Brunold C (1978) Regulation of sulfate assimilation in plants: 7. Cysteine inactivation of adenosine 5’-phosphosulfate sulfotransferase in Lemna minor L. Plant Physiol 61:342–347
Brunold C, Suter M (1984) Regulation of sulfate assimilation by nitrogen nutrition in the duckweed Lemna minor L. Plant Physiol 76:579–583
Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78
Cao MJ et al (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29
Chang KN et al (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife 2:e00675
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144
Chao DY et al (2014) Variation in sulfur and selenium accumulation is controlled by naturally occurring isoforms of the key sulfur assimilation enzyme ADENOSINE 5′-PHOSPHOSULFATE REDUCTASE2 across the Arabidopsis species range. Plant Physiol 166:1593–1608
Collier MD, Fotelli MN, Nahm M, Kopriva S, Rennenberg H, Hanke DE, Gessler A (2003) Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level—interactions between cytokinins and soluble N compounds. Plant Cell Environ 26:1549–1560
Czyzewicz N, Yue K, Beeckman T, De Smet I (2013) Message in a bottle: small signalling peptide outputs during growth and development. J Exp Bot 64:5281–5296
Devoto A, Ellis C, Magusin A, Chang HS, Chilcott C, Zhu T, Turner JG (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513
Ernst L et al (2010) Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. J Exp Bot 61:3395–3405
Estavillo GM et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857
Frerigmann H, Gigolashvili T (2014) MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol Plant 7:814–828
Frerigmann H, Berger B, Gigolashvili T (2014) bHLH05 is an interaction partner of MYB51 and a novel regulator of glucosinolate biosynthesis in Arabidopsis. Plant Physiol 166:349–369
Garcia I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC (2010) Mitochondrial beta-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 22:3268–3279
Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984
Gigolashvili T, Berger B, Mock HP, Muller C, Weisshaar B, Flugge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901
Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013
Grubb CD, Zipp BJ, Ludwig-Muller J, Masuno MN, Molinski TF, Abel S (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893–908
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333
Harada E, Kusano T, Sano H (2000) Differential expression of genes encoding enzymes involved in sulfur assimilation pathways in response to wounding and jasmonate in Arabidopsis thaliana. J Plant Physiol 156:272–276
Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000) β-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1171
Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808
Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663
Jost R et al (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth Res 86:491–508
Kasajima I et al (2007) The BIG gene is involved in regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol Plantarum 129:351–363
Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665
Kim BH, von Arnim AG (2009) FIERY1 regulates light-mediated repression of cell elongation and flowering time via its 3′(2′),5′-bisphosphate nucleotidase activity. Plant J 58:208–219
Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106:15067–15072
Kopriva S, Muheim R, Koprivova A, Trachsel N, Catalano C, Suter M, Brunold C (1999) Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. Plant J 20:37–44
Kopriva S, Suter M, von Ballmoos P, Hesse H, Krahenbuhl U, Rennenberg H, Brunold C (2002) Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol 130:1406–1413
Koprivova A, Kopriva S (2014) Molecular mechanisms of regulation of sulfate assimilation: first steps on a long road. Front Plant Sci 5:589
Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746
Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420
Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167
Koprivova A, Harper AL, Trick M, Bancroft I, Kopriva S (2014) Dissection of the control of anion homeostasis by associative transcriptomics in Brassica napus. Plant Physiol 166:442–450
Lee BR et al (2012) Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? PLoS One 7:e39425
Li B et al (2014) Promoter-based integration in plant defense regulation. Plant Physiol 166:1803–1820
Lingam S et al (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23:1815–1829
Lisjak M et al (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935
Loudet O et al (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39:896–900
Marsolais F, Boyd J, Paredes Y, Schinas AM, Garcia M, Elzein S, Varin L (2007) Molecular and biochemical characterization of two brassinosteroid sulfotransferases from Arabidopsis, AtST4a (At2g14920) and AtST1 (At2g03760). Planta 225:1233–1244
Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J 38:779–789
Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314
Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251
Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci U S A 93:7623–7627
Mikkelsen MD, Petersen BL, Glawischnig E, Jensen AB, Andreasson E, Halkier BA (2003) Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol 131:298–308
Mikkelsen MD, Naur P, Halkier BA (2004) Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J 37:770–777
Mugford SG et al (2009) Disruption of adenosine-5 ‘-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21:910–927
Nam YJ, Tran LS, Kojima M, Sakakibara H, Nishiyama R, Shin R (2012) Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS One 7:e47797
Neuenschwander U, Suter M, Brunold C (1991) Regulation of sulfate assimilation by light and O-acetyl-l-Serine in Lemna minor L. Plant Physiol 97:253–258
Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650
Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870
Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56:1887–1896
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Noctor G et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484
Nussbaum S, Schmutz D, Brunold C (1988) Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. Plant Physiol 88:1407–1410
Ohkama N, Takei K, Sakakibara H, Hayashi H, Yoneyama T, Fujiwara T (2002) Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol 43:1493–1501
Park S-W et al (2013) Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc Natl Acad Sci USA 110:9559–9564
Passaia G, Queval G, Bai J, Margis-Pinheiro M, Foyer CH (2014) The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. J Exp Bot 65:1403–1413
Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19:1851–1865
Reintanz B et al (2001) Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13:351–367
Robles P et al (2010) The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. Plant Physiol 152:1357–1372
Rodriguez VM, Chetelat A, Majcherczyk P, Farmer EE (2010) Chloroplastic phosphoadenosine phosphosulfate metabolism regulates basal levels of the prohormone jasmonic acid in Arabidopsis leaves. Plant Physiol 152:1335–1345
Ruiz JM, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969
Sakakibara H, Suzuki M, Takei K, Deji A, Taniguchi M, Sugiyama T (1998) A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J 14:337–344
Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448
Sanchez-Fernandez R et al (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci USA 94:2745–2750
Sauter M, Cornell KA, Beszteri S, Rzewuski G (2004) Functional analysis of methylthioribose kinase genes in plants. Plant Physiol 136:4061–4071
Sauter M, Moffatt B, Saechao MC, Hell R, Wirtz M (2013) Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. Biochem J 451:145–154
Schweizer F et al (2013) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–3132
Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076
Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486
Sonderby IE, Burow M, Rowe HC, Kliebenstein DJ, Halkier BA (2010a) A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol 153:348–363
Sonderby IE, Geu-Flores F, Halkier BA (2010b) Biosynthesis of glucosinolates–gene discovery and beyond. Trends Plant Sci 15:283–290
Stamler JS (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78:931–936
Tada Y et al (2008) Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956
Takahashi H et al (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184
Vauclare P et al (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740
Vernoux T et al (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110
Wang Z, Mao JL, Zhao YJ, Li CY, Xiang CB (2015) L-Cysteine inhibits root elongation through auxin/PLETHORA and SCR/SHR pathway in Arabidopsis thaliana. J Integr Plant Biol 57:186–197
Wawrzynska A, Sirko A (2014) To control and to be controlled: understanding the Arabidopsis SLIM1 function in sulfur deficiency through comprehensive investigation of the EIL protein family. Front Plant Sci 5:575
Wawrzynska A, Lewandowska M, Sirko A (2010) Nicotiana tabacum EIL2 directly regulates expression of at least one tobacco gene induced by sulphur starvation. J Exp Bot 61:889–900
Wawrzynska A, Moniuszko G, Sirko A (2015) Links between ethylene and sulfur nutrition-a regulatory interplay or just metabolite association? Front Plant Sci 6:1053
Wilson PB et al (2009) The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J 58:299–317
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718
Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550
Xiong L, Lee B, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15:1971–1984
Yamasaki K et al (2005) Solution structure of the major DNA-binding domain of Arabidopsis thaliana ethylene-insensitive3-like3. J Mol Biol 348:253–264
Yatusevich R et al (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J 62:1–11
Zhang GB, Yi HY, Gong JM (2014) The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–3998
Zhao Q, Wu Y, Gao L, Ma J, Li CY, Xiang CB (2014) Sulfur nutrient availability regulates root elongation by affecting root indole-3-acetic acid levels and the stem cell niche. J Integr Plant Biol 56:1151–1163
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632
Zuchi S, Cesco S, Varanini Z, Pinton R, Astolfi S (2009) Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 230:85–94
Acknowledgments
Research in SK’s lab is supported by Deutsche Forschungsgemeinschaft (EXC 1028).
Author contribution
AK and SK reviewed the literature and wrote the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Koprivova, A., Kopriva, S. Hormonal control of sulfate uptake and assimilation. Plant Mol Biol 91, 617–627 (2016). https://doi.org/10.1007/s11103-016-0438-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-016-0438-y