Abstract
Ethylene plays an essential role in response to hypoxic stress in plants. In most plant species, 1-aminocyclopropane-1-carboxylate synthase (ACS) is the key enzyme that regulates the production of ethylene. We examined the expression of ACS genes in Arabidopsis during hypoxia. Our data showed that the expression of 4 of the 12 Arabidopsis ACS genes, ACS2, ACS6, ACS7, and ACS9, is induced during hypoxia with three distinct patterns. The hypoxic induction of ACS9 is inhibited by aminooxy acetic acid, an inhibitor of ethylene biosynthesis. In addition, the hypoxic induction of ACS9 is also reduced in etr1-1 and ein2-1, two ethylene insensitive mutants in ethylene-signaling pathways, whereas the addition of 1-aminocyclopropane-1-carboxylic acid, a direct precursor of ethylene, does not induce ACS9 under normoxic conditions. These results indicate that ethylene is needed, but not sufficient, for the induction of ACS9 during hypoxia. This pattern of regulation is similar to that of ADH that encodes alcohol dehydrogenase, which we have reported previously. In contrast, the increased ethylene production during hypoxia has an inhibitory effect on ACS2 induction in roots, whereas ethylene has no effect on the hypoxic induction of ACS6 and ACS7. Based on these results, we propose that two signaling pathways are triggered during hypoxia. One pathway leads to the activation of ACS2, ACS6, and ACS7, whereas the other pathway leads to the activation of ADH and ACS9.
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Abbreviations
- ACC:
-
1-aminocyclopropane-1-carboxylic acid
- ACS:
-
ACC synthase
- ADH:
-
alcohol dehydrogenase
- AOA:
-
aminooxy acetic acid
- RT:
-
reverse transcriptase
References
F.B. Abeles P.W. Morgan M.E. Saltveit (1992) In Ethylene Plant Biology EditionNumber2 Academic Press New York 264–285
D.O. Adams S.F. Yang (1979) ArticleTitleEthylene biosynthesis: identification of 1-aminocyclopropane 1-carboxylic acid as an intermediate in the conversion of methionine to ethylene Proc. Natl. Acad. Sci. USA 76 170–174
J.M. Alonso T. Hirayama G. Roman S. Nourizadeh J.R. Ecker (1999) ArticleTitleEIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis Science 284 2148–2152
Alonso, J.M. and Ecker, J.R. 2001. The ethylene pathway: a paradigm for plant hormone signaling and interaction. Sci. STKE (70) RE1.
J.M. Arteca R.N. Arteca (1999) ArticleTitleA multi-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase (ACS6) in mature Arabidopsis leaves Plant Mol. Biol 39 209–219
J. Bailey-Serres R.K. Dawe (1996) ArticleTitleBoth 5’ and 3’ sequences of maize adh1 mRNA are required for enhanced translation under low-oxygen conditions Plant Physiol 112 685–695
C.S. Barry M.I. Llop-Tous D. Grierson (2000) ArticleTitleThe regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato Plant Physiol 123 979–986
A. Baxter-Burrell Z. Yang P.S. Springer J. Bailey-Serres (2002) ArticleTitleRopGAP4-dependent Rop GTPASE rheostat control of Arabidopsis oxygen deprivation tolerance Science 296 2026–2028
K.J. Bradford S.F. Yang (1980) ArticleTitleXylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in water logged tomato plants Plant Physiol 65 322–326
M. Buttner K.B. Singh (1997) ArticleTitleArabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein Proc. Natl. Acad. Sci. USA 94 5961–5966
H.S. Chae F. Faure J.J. Kieber (2003) ArticleTitleThe eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein Plant Cell 15 545–559
W.P. Chang L. Hunag M. Shen C. Webster A. Burlingame J.K.M. Roberts (2000) ArticleTitlePatterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low oxygen environment, and identification of proteins by mass spectrometry1 Plant Physiol 122 295–318
C. Chang S.F. Kwok A.B. Bleecker E. Meyerowitz (1993) ArticleTitleArabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators Science 262 539–544
H.-J. Chung R.J. Ferl (1999) ArticleTitleArabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment1 Plant Physiol 121 429–436
P. Chomczynski N. Sacchi (1987) ArticleTitleSingle-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem 162 156–160
T.R. Conley H.-P. Peng M.-C. Shih (1999) ArticleTitleMutations affecting induction of glycolytic and fermentative genes during germination and environmental stresses in Arabidopsis Plant Physiol 119 599–607
R. Dolferus M. Jacobs W. Peacock E. Dennis (1994) ArticleTitleDifferential interactions of promoter elements in stress responses of the Arabidopsis Adh gene Plant Physiol 105 1075–1087
M.C. Drew (1997) ArticleTitleOxygen deficiency and root metabolism: Injury and acclimation under hypoxia and anoxia Annu. Rev. Plant Physiol. Plant Mol. Biol 48 223–250
M.C. Drew C.J. He P.W. Morgan (2000) ArticleTitleProgrammed cell death and aerenchyma formation in roots Trends Plant Sci 5 123–127
M.C. Drew M.B. Jackson S. Giffard (1979) ArticleTitleEthylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) may be adaptive response to flooding in Zea mays L Planta 153 217–224
P.J. English G.W. Lycett J.A. Roberts M.B. Jackson (1995) Plant Physiol 109 1435–1440
S.L. Fennoy J. Bailey-Serres (1995) ArticleTitlePost-transcriptional regulation of gene expression in oxygen-deprived roots of maize Plant J 7 287–295
R. Ferl B. Laughner (1989) ArticleTitleIn vivo detection of the regulatory factor binding sites of Arabidopsis thaliana Adh Plant Mol. Biol 12 357–366
A.H. Gunawardena D.M. Pearce M.K. Jackson C.R. Hawes D.E. Evans (2001) ArticleTitleCharacterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.) Planta 212 205–214
C.-J. He M.C. Drew P.W. Morgan (1994) ArticleTitleInduction of enzyme associated with lysigenous aerenchyma formation in roots of Zea mays during hypoxia or nitrogen-starvation Plant Physiol 105 861–865
C-J He P.W. Morgan M.C. Drew (1996) ArticleTitleTransduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia Plant Physiol 112 463–472
F.U. Hoeren R. Dolferus Y. Wu W.J. Peacock E.S. Dennis (1998) ArticleTitleEvidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) low oxygen Genetics 149 479–490
R.A. Kennedy M. Rumpho T.C. Fox (1992) ArticleTitleAnaerobic metabolism in plants Plant Physiol 100 1–6
J. Kyozuka M. Olive W. Peacock E. K. Dennis Shimamoto (1994) ArticleTitlePromoter elements required for developmental expression of the maize Adh1 gene in transgenic rice Plant Cell 6 799–810
X. Liang S. Abel J.A. Keller N.F. Shen A. Theologis (1992) ArticleTitleThe 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 89 11046–11050
X. Liang Y. Oono N.F. Shen C. Kohler K. Li P.A. Scolnik A. Theologis (1995) ArticleTitleCharacterization of two members (ACS1 and ACS3) of the 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana Gene 167 17–24
J.M. Lelièvre A. Latché B. Jones M. Bouzayen J.C. Pech (1998) ArticleTitleEthylene and fruit ripening Physiol. Plant 101 727–739
A. Nakatsuka S. Murachi H. Okunishi S. Shiomi R. Nakano Y. Kubo A. Inaba (1998) ArticleTitleDifferential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening Plant Physiol 118 1295–1305
D.C. Olson J.H. Oetiker S.F. Yang (1995) ArticleTitleAnalysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants J. Biol. Chem 270 14056–14061
H.-P. Peng C.-S. Chan M.-C. Shih S.F. Yang (2001) ArticleTitleSignaling events in the hypoxic induction of ADH in Arabidopsis Plant Physiol 126 742–749
J.K. Roberts J. Callis O. Jardetzky V. Walbot M. Freeling (1984b) ArticleTitleCytoplasmic acidosis as a determinant of flooding intolerance in plants Proc. Natl. Acad. Sci. USA 81 6029–6033
J.K. Roberts J. Callis D. Wemmer V. Walbot O. Jardetzky (1984a) ArticleTitleMechanisms of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia Proc. Natl. Acad. Sci. USA 81 3379–3383
G. Roman B. Lubarsky J.J. Kieber M. Rothenberg J.R. Ecker (1995) ArticleTitleGenetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway Genetics 139 1393–1409
M.M. Sachs C.C. Subbaiah I.N. Sabb (1996) ArticleTitleAnaerobic gene expression and flooding tolerance in maize J. Exp. Bot 47 1–15
A. Samach H. Onouchi S.E. Gold G.S. Ditta Z. Schwarz-Sommer M.F. Yanofsky G. Coupland (2000) ArticleTitleDistinct roles of CONSTANS target genes in reproductive development of Arabidopsis Science 288 1613–1616
T.D. Schmittgen B.A. Zakrajsek A.G. Mills V. Gorn M.J. Singer M.W. Reed (2000) ArticleTitleQuantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods Anal. Biochem 285 194–204
J.C. Sedbrook P.J. Kronebusch G.G. Borisy A.J. Trewavas P.H. Masson (1996) ArticleTitleTransgenic aequorin reveals organ-specific cytosolic Ca2+ responses to anoxia in Arabidopsis thaliana seedlings Plant Physiol 111 243–257
L.N. Sellner G.R. Turbett (1998) ArticleTitleComparison of three RT-PCR methods Biotechniques 25 230–234
O.Y. Shiu J.H. Oetiker W.K. Yip S.F. Yang (1998) ArticleTitleThe promoter of LE-ACS7, an early flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of the tomato, is tagged by a Sol3 transposon Proc. Natl. Acad. Sci. USA 95 10334–10339
C.C. Subbaiah D.S. Bush M.M. Sachs (1994a) ArticleTitleElevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells Plant Cell 6 1747–1762
C.C. Subbaiah J. Zhang M.M. Sachs (1994b) ArticleTitleInvolvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings Plant Physiol 105 369–376
D. Straeten ParticleVan Der R.A. Rodrigues-Pousada R. Villarroel S. Hanley H.M. Goodman M. Montagu ParticleVan (1992) ArticleTitleCloning, genetic mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase Proc. Natl. Acad. Sci. USA 89 9969–9973
K.L. Wang H. Li J.R. Ecker (2002a) ArticleTitleEthylene biosynthesis and signaling networks Plant Cell 14 IssueIDSuppl S131–151
Q. Wang R. Sjolund M.-C. Shih (2002b) ArticleTitleInvolvement of calcium in the anoxic signaling pathways of Arabidopsis thaliana J. Plant Physiol. Mol. Biol 28 441–448
K.E. Woeste C. Ye J. Kieber (1999) ArticleTitleTwo Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase Plant Physiol 119 521–529
T. Yamagami A. Tsuchisaka K. Yamada W.F. Haddon L.A. Harden A. Theologis (2003) ArticleTitleBiochemical characterization of the Arabidopsis ACSome J. Biol. Chem 278 49102–49112
Yang, S.F. 1987. The role of ethylene and ethylene synthesis in fruit ripening. Plant Senescence: Its Biochemistry and Physiology. In: W.W. Thomson, E.A. Nothaagel and Huffaker (Eds.), The American Society of Plant Physiologists, pp. 156–166.
S.F. Yang N.E. Hoffman (1984) ArticleTitleEthylene biosynthesis and its regulation in higher plants Annu. Rev. Plant. Physiol 35 155–189
T.I. Zarembinski A. Theologis (1997) ArticleTitleExpression characteristics of OS-ACS1 and OS-ACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase gene family in rice (Oryza sativa L. cv. Habiganj Aman II) during partial submergence Plant Mol. Biol 33 71–77
G.Y. Zhong J.K. Burns (2003) ArticleTitleProfiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis Plant Mol. Biol 53 117–131
Z. Zhou J. Almeida Engler Particlede D. Rouan F. Michiels M. Montagu ParticleVan D. Straeten ParticleVan Der (2002) ArticleTitleTissue localization of a submergence-induced 1-aminocyclopropane-1-carboxylic acid synthase in rice Plant Physiol 129 72–84
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Peng, HP., Lin, TY., Wang, NN. et al. Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58, 15–25 (2005). https://doi.org/10.1007/s11103-005-3573-4
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DOI: https://doi.org/10.1007/s11103-005-3573-4