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PMID: 19752216 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana.

Genetics ·Vol. 183 ·No. 3 ·2009-11-00 ·Pages 979-1003

Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A

Abstract

Ethylene (C(2)H(4)) is a unique plant-signaling molecule that regulates numerous developmental processes. The key enzyme in the two-step biosynthetic pathway of ethylene is 1-aminocyclopropane-1-carboxylate synthase (ACS), which catalyzes the conversion of S-adenosylmethionine (AdoMet) to ACC, the precursor of ethylene. To understand the function of this important enzyme, we analyzed the entire family of nine ACS isoforms (ACS1, ACS2, ACS4-9, and ACS11) encoded in the Arabidopsis genome. Our analysis reveals that members of this protein family share an essential function, because individual ACS genes are not essential for Arabidopsis viability, whereas elimination of the entire gene family results in embryonic lethality. Phenotypic characterization of single and multiple mutants unmasks unique but overlapping functions of the various ACS members in plant developmental events, including multiple growth characteristics, flowering time, response to gravity, disease resistance, and ethylene production. Ethylene acts as a repressor of flowering by regulating the transcription of the FLOWERING LOCUS C. Each single and high order mutant has a characteristic molecular phenotype with unique and overlapping gene expression patterns. The expression of several genes involved in light perception and signaling is altered in the high order mutants. These results, together with the in planta ACS interaction map, suggest that ethylene-mediated processes are orchestrated by a combinatorial interplay among ACS isoforms that determines the relative ratio of homo- and heterodimers (active or inactive) in a spatial and temporal manner. These subunit isoforms comprise a combinatorial code that is a central regulator of ethylene production during plant development. The lethality of the null ACS mutant contrasts with the viability of null mutations in key components of the ethylene signaling apparatus, strongly supporting the view that ACC, the precursor of ethylene, is a primary regulator of plant growth and development.

MeSH Terms
Amino Acids, Cyclic/metabolism Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Epistasis, Genetic Ethylenes/biosynthesis Flowers/genetics,growth & development,metabolism Gene Expression Profiling Gene Expression Regulation, Developmental Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Genetic Complementation Test Genome, Plant/genetics Isoenzymes/genetics,metabolism Lyases/genetics,metabolism Mutation Plant Diseases/genetics,microbiology Plants, Genetically Modified Reverse Transcriptase Polymerase Chain Reaction S-Adenosylmethionine/metabolism Time Factors
Chemicals
Amino Acids, Cyclic Arabidopsis Proteins Ethylenes Isoenzymes 1-aminocyclopropane-1-carboxylic acid S-Adenosylmethionine ethylene Lyases 1-aminocyclopropanecarboxylate synthase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Tsuchisaka Atsunari
Plant Gene Expression Center, Albany, California 94710, USA. [email protected]
Yu Guixia
Jin Hailing
Alonso Jose M
Ecker Joseph R
Zhang Xiaoming
Gao Shang
Theologis Athanasios
References (81)
81 references, click to expand
  1. The complexity of disease signaling in Arabidopsis.
    Curr Opin Immunol. 2001 Feb;13(1):63-8 PMID: 11154919
  2. Cloning the Arabidopsis GA1 Locus by Genomic Subtraction.
    Plant Cell. 1992 Feb;4(2):119-128 PMID: 12297643
  3. Understanding gibberellic acid signaling--are we there yet?
    Curr Opin Plant Biol. 2008 Feb;11(1):9-15 PMID: 18077204
  4. Light signal transduction in higher plants.
    Annu Rev Genet. 2004;38:87-117 PMID: 15568973
  5. Local auxin production: a small contribution to a big field.
    Bioessays. 2009 Jan;31(1):60-70 PMID: 19154004
  6. Multilevel interactions between ethylene and auxin in Arabidopsis roots.
    Plant Cell. 2007 Jul;19(7):2169-85 PMID: 17630276
  7. Gravity sensing and signaling.
    Curr Opin Plant Biol. 2004 Dec;7(6):712-8 PMID: 15491921
  8. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  9. Highly specific gene silencing by artificial microRNAs in Arabidopsis.
    Plant Cell. 2006 May;18(5):1121-33 PMID: 16531494
  10. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.
    Cell. 1993 Feb 12;72(3):427-41 PMID: 8431946
  11. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.
    Plant Cell. 1999 May;11(5):949-56 PMID: 10330478
  12. Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis.
    Plant Cell. 2008 Nov;20(11):3065-79 PMID: 19017745
  13. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling.
    Nature. 2008 Feb 14;451(7180):789-95 PMID: 18273012
  14. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.
    Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6484-9 PMID: 17389366
  15. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense.
    Plant Physiol. 2008 Jul;147(3):1347-57 PMID: 18467450
  16. Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum.
    Mol Plant Microbe Interact. 2004 Jul;17(7):763-70 PMID: 15242170
  17. Circadian rhythms of ethylene emission in Arabidopsis.
    Plant Physiol. 2004 Nov;136(3):3751-61 PMID: 15516515
  18. Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members.
    Mol Plant. 2008 Mar;1(2):308-20 PMID: 19825542
  19. Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection.
    Plant Cell. 2003 Jan;15(1):93-106 PMID: 12509524
  20. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members.
    Plant Physiol. 2004 Oct;136(2):2982-3000 PMID: 15466221
  21. NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis.
    Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18825-9 PMID: 18000043
  22. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea.
    Plant Physiol. 1999 Dec;121(4):1093-102 PMID: 10594097
  23. A morning-specific phytohormone gene expression program underlying rhythmic plant growth.
    PLoS Biol. 2008 Sep 16;6(9):e225 PMID: 18798691
  24. Molecular interactions between light and hormone signaling to control plant growth.
    Plant Mol Biol. 2009 Mar;69(4):409-17 PMID: 18797998
  25. Regulation of ACS protein stability by cytokinin and brassinosteroid.
    Plant J. 2009 Feb;57(4):606-14 PMID: 18980656
  26. RNA sensors and riboswitches: self-regulating messages.
    Curr Biol. 2003 Apr 1;13(7):R285-91 PMID: 12676109
  27. Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family.
    Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2275-80 PMID: 14983000
  28. The role of local biosynthesis of auxin and cytokinin in plant development.
    Curr Opin Plant Biol. 2008 Feb;11(1):16-22 PMID: 18409210
  29. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein.
    Nature. 2004 Apr 29;428(6986):945-50 PMID: 15118728
  30. Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering.
    Development. 2007 Aug;134(15):2841-50 PMID: 17611230
  31. Integration of plant responses to environmentally activated phytohormonal signals.
    Science. 2006 Jan 6;311(5757):91-4 PMID: 16400150
  32. Alteration of auxin polar transport in the Arabidopsis ifl1 mutants.
    Plant Physiol. 2001 Jun;126(2):549-63 PMID: 11402186
  33. Photoperiodic control of flowering: not only by coincidence.
    Trends Plant Sci. 2006 Nov;11(11):550-8 PMID: 17035069
  34. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization.
    Plant Cell. 2001 Apr;13(4):935-41 PMID: 11283346
  35. Complementation analysis of mutants of 1-aminocyclopropane- 1-carboxylate synthase reveals the enzyme is a dimer with shared active sites.
    J Biol Chem. 1998 May 15;273(20):12509-14 PMID: 9575209
  36. Auxin: a trigger for change in plant development.
    Cell. 2009 Mar 20;136(6):1005-16 PMID: 19303845
  37. A role for brassinosteroids in light-dependent development of Arabidopsis.
    Science. 1996 Apr 19;272(5260):398-401 PMID: 8602526
  38. Integration of spatial and temporal information during floral induction in Arabidopsis.
    Science. 2005 Aug 12;309(5737):1056-9 PMID: 16099980
  39. Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms.
    PLoS Genet. 2009 Jan;5(1):e1000328 PMID: 19132085
  40. Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3.
    J Biol Chem. 2007 Jul 6;282(27):19992-20001 PMID: 17493935
  41. Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9789-93 PMID: 1409700
  42. Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family.
    J Biol Chem. 2003 Dec 5;278(49):49102-12 PMID: 12968022
  43. Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function.
    Plant Cell. 2003 Dec;15(12):2816-25 PMID: 14615596
  44. The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana.
    Development. 1995 Sep;121(9):2723-35 PMID: 7555701
  45. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses.
    Cell. 2006 Aug 11;126(3):467-75 PMID: 16901781
  46. The role of ethylene in host-pathogen interactions.
    Annu Rev Phytopathol. 2006;44:393-416 PMID: 16602950
  47. Characterization and sequencing of the active site of 1-aminocyclopropane-1-carboxylate synthase.
    Proc Natl Acad Sci U S A. 1990 Oct;87(20):7930-4 PMID: 2122449
  48. Engineered nanomaterials for biophotonics applications: improving sensing, imaging, and therapeutics.
    Annu Rev Biomed Eng. 2003;5:285-92 PMID: 14527314
  49. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.
    Science. 1993 Oct 22;262(5133):539-44 PMID: 8211181
  50. DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy.
    Curr Biol. 2006 Dec 5;16(23):2366-70 PMID: 17141619
  51. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis.
    Plant Cell. 2007 Jul;19(7):2213-24 PMID: 17630279
  52. Reversible inhibition of tomato fruit senescence by antisense RNA.
    Science. 1991 Oct 18;254(5030):437-9 PMID: 1925603
  53. Auxin promotes Arabidopsis root growth by modulating gibberellin response.
    Nature. 2003 Feb 13;421(6924):740-3 PMID: 12610625
  54. Different Roles for Phytochrome in Etiolated and Green Plants Deduced from Characterization of Arabidopsis thaliana Mutants.
    Plant Cell. 1989 Sep;1(9):867-880 PMID: 12359912
  55. Structure of 1-aminocyclopropane-1-carboxylate synthase, a key enzyme in the biosynthesis of the plant hormone ethylene.
    J Mol Biol. 1999 Dec 3;294(3):745-56 PMID: 10610793
  56. Shedding light on gibberellic acid signalling.
    Curr Opin Plant Biol. 2009 Feb;12(1):57-62 PMID: 18930434
  57. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway.
    Genetics. 1995 Mar;139(3):1393-409 PMID: 7768447
  58. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.
    Cell. 2008 Apr 4;133(1):177-91 PMID: 18394997
  59. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation.
    Plant Cell. 2007 Jul;19(7):2186-96 PMID: 17630275
  60. Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development.
    Cell Mol Life Sci. 2006 Dec;63(23):2738-54 PMID: 17013565
  61. The timing of developmental transitions in plants.
    Cell. 2006 May 19;125(4):655-64 PMID: 16713560
  62. Multiple pathways in the decision to flower: enabling, promoting, and resetting.
    Plant Cell. 2004;16 Suppl:S18-31 PMID: 15037730
  63. Convergence of signaling pathways in the control of differential cell growth in Arabidopsis.
    Dev Cell. 2004 Aug;7(2):193-204 PMID: 15296716
  64. Light-regulated transcriptional networks in higher plants.
    Nat Rev Genet. 2007 Mar;8(3):217-30 PMID: 17304247
  65. Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis.
    Plant J. 2004 Aug;39(4):537-59 PMID: 15272873
  66. DNA methylation is critical for Arabidopsis embryogenesis and seed viability.
    Plant Cell. 2006 Apr;18(4):805-14 PMID: 16531498
  67. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  68. The ethylene signaling pathway: new insights.
    Curr Opin Plant Biol. 2004 Feb;7(1):40-9 PMID: 14732440
  69. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.
    Cell. 2008 Apr 4;133(1):164-76 PMID: 18394996
  70. Ethylene can stimulate Arabidopsis hypocotyl elongation in the light.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2756-61 PMID: 11038610
  71. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation.
    Plant Cell. 2008 Mar;20(3):580-8 PMID: 18375656
  72. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation.
    Mol Cell. 2002 Apr;9(4):789-98 PMID: 11983170
  73. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3.
    Plant Physiol. 2007 May;144(1):367-79 PMID: 17384165
  74. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis.
    Science. 2000 Jun 2;288(5471):1613-6 PMID: 10834834
  75. Integration of floral inductive signals in Arabidopsis.
    Nature. 2000 Apr 20;404(6780):889-92 PMID: 10786797
  76. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi.
    Plant J. 2002 Jan;29(1):23-32 PMID: 12060224
  77. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis.
    Genes Dev. 2006 Apr 1;20(7):898-912 PMID: 16600915
  78. Auxin receptors and plant development: a new signaling paradigm.
    Annu Rev Cell Dev Biol. 2008;24:55-80 PMID: 18631113
  79. Ethylene: a gaseous signal molecule in plants.
    Annu Rev Cell Dev Biol. 2000;16:1-18 PMID: 11031228
  80. Of light and length: regulation of hypocotyl growth in Arabidopsis.
    Bioessays. 2005 Mar;27(3):275-84 PMID: 15714558
  81. The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue.
    Plant Cell. 2000 May;12(5):757-70 PMID: 10810148
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
1943-2631
DOI
10.1534/genetics.109.107102
Email
[email protected]
Published
2009-11-00
Epub
2009-00-14
Pages
979-1003
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC2778992
Subset
IM
External Links
PubMed source DOI: 10.1534/genetics.109.107102 PMC Full Text View journal details
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