First published online October 1, 2004; 10.1104/pp.104.049999
Plant Physiology 136:2982-3000 (2004)
© 2004 American Society of Plant Biologists
Unique and Overlapping Expression Patterns among the Arabidopsis 1-Amino-Cyclopropane-1-Carboxylate Synthase Gene Family Members1,[w]
Atsunari Tsuchisaka and
Athanasios Theologis*
Plant Gene Expression Center, Albany, California 94710
1-Aminocyclopropane-1-carboxylate synthase (ACS) catalyzes the rate-limiting step in the ethylene biosynthetic pathway in plants. The Arabidopsis genome encodes nine ACS polypeptides that form eight functional (ACS2, ACS4-9, and ACS11) homodimers and one nonfunctional (ACS1) homodimer. Transgenic Arabidopsis lines were constructed expressing the  -glucuronidase (GUS) and green fluorescence protein (GFP) reporter genes from the promoter of each of the gene family members to determine their patterns of expression during plant development. All genes, except ACS9, are expressed in 5-d-old etiolated or light-grown seedlings yielding distinct patterns of GUS staining. ACS9 expression is detected later in development. Unique and overlapping expression patterns were detected for all the family members in various organs of adult plants. ACS11 is uniquely expressed in the trichomes of sepals and ACS1 in the replum. Overlapping expression was observed in hypocotyl, roots, various parts of the flower (sepals, pedicle, style, etc.) and in the stigmatic and abscission zones of the silique. Exogenous indole-3-acetic acid (IAA) enhances the constitutive expression of ACS2, 4, 5, 6, 7, 8, and 11 in the root. Wounding of hypocotyl tissue inhibits the constitutive expression of ACS1 and ACS5 and induces the expression of ACS2, 4, 6, 7, 8, and 11. Inducers of ethylene production such as cold, heat, anaerobiosis, and Li+ ions enhance or suppress the expression of various members of the gene family in the root of light-grown seedlings. Examination of GUS expression in transverse sections of cotyledons reveals that all ACS genes, except ACS9, are expressed in the epidermis cell layer, guard cells, and vascular tissue. Similar analysis with root tip tissue treated with IAA reveals unique and overlapping expression patterns in the various cell types of the lateral root cap, cell division, and cell expansion zones. IAA inducibility is gene-specific and cell type-dependent across the root tip zone. This limited comparative exploration of ACS gene family expression reveals constitutive spatial and temporal expression patterns of all gene family members throughout the growth period examined. The unique and overlapping gene activity pattern detected reveals a combinatorial code of spatio-temporal coexpression among the various gene family members during plant development. This raises the prospect that functional ACS heterodimers may be formed in planta.
1 This work was supported by the National Science Foundation (grant nos. MCB–9982895, IBN–0211421) and by the U.S. Department of Agriculture-Agricultural Research Service (CRIS no. 5335–21430–005–00D to A.T.).
[w] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.049999.
* Corresponding author; e-mail theo{at}nature.berkeley.edu; fax 510–559–5678.
Received July 15, 2004;
returned for revision August 31, 2004;
accepted September 9, 2004.
This article has been cited by other articles:
|
|
|
|
 
A. Tsuchisaka, G. Yu, H. Jin, J. M. Alonso, J. R. Ecker, X. Zhang, S. Gao, and A. Theologis
A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis in Arabidopsis thaliana
Genetics,
November 1, 2009;
183(3):
979 - 1003.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Sun, Q.-Y. Tian, J. Chen, and W.-H. Zhang
Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin
J. Exp. Bot.,
October 25, 2009;
(2009)
erp306v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Lin, C.-W. Ho, and D. Grierson
AtTRP1 encodes a novel TPR protein that interacts with the ethylene receptor ERS1 and modulates development in Arabidopsis
J. Exp. Bot.,
September 1, 2009;
60(13):
3697 - 3714.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Lin, S. Zhong, and D. Grierson
Recent advances in ethylene research
J. Exp. Bot.,
August 1, 2009;
60(12):
3311 - 3336.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Zhang, H. Zhang, R. Quan, X.-C. Wang, and R. Huang
Transcriptional Regulation of the Ethylene Response Factor LeERF2 in the Expression of Ethylene Biosynthesis Genes Controls Ethylene Production in Tomato and Tobacco
Plant Physiology,
May 1, 2009;
150(1):
365 - 377.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-Y. Jung, R. Shin, and D. P. Schachtman
Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis
PLANT CELL,
February 1, 2009;
21(2):
607 - 621.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Salman-Minkov, A. Levi, S. Wolf, and T. Trebitsh
ACC Synthase Genes are Polymorphic in Watermelon (Citrullus spp.) and Differentially Expressed in Flowers and in Response to Auxin and Gibberellin
Plant Cell Physiol.,
May 1, 2008;
49(5):
740 - 750.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. A. Paponov, M. Paponov, W. Teale, M. Menges, S. Chakrabortee, J. A.H. Murray, and K. Palme
Comprehensive Transcriptome Analysis of Auxin Responses in Arabidopsis
Mol Plant,
March 1, 2008;
1(2):
321 - 337.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Dugardeyn, F. Vandenbussche, and D. Van Der Straeten
To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis?
J. Exp. Bot.,
January 1, 2008;
59(1):
1 - 16.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Khanna, Y. Shen, C. M. Marion, A. Tsuchisaka, A. Theologis, E. Schafer, and P. H. Quail
The Basic Helix-Loop-Helix Transcription Factor PIF5 Acts on Ethylene Biosynthesis and Phytochrome Signaling by Distinct Mechanisms
PLANT CELL,
December 1, 2007;
19(12):
3915 - 3929.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Trainotti, A. Tadiello, and G. Casadoro
The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches
J. Exp. Bot.,
October 8, 2007;
(2007)
erm178v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. N. Stepanova, J. Yun, A. V. Likhacheva, and J. M. Alonso
Multilevel Interactions between Ethylene and Auxin in Arabidopsis Roots
PLANT CELL,
July 1, 2007;
19(7):
2169 - 2185.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Ruzicka, K. Ljung, S. Vanneste, R. Podhorska, T. Beeckman, J. Friml, and E. Benkova
Ethylene Regulates Root Growth through Effects on Auxin Biosynthesis and Transport-Dependent Auxin Distribution
PLANT CELL,
July 1, 2007;
19(7):
2197 - 2212.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. W. Woodward, S. E. Ratzel, E. E. Woodward, Y. Shamoo, and B. Bartel
Mutation of E1-CONJUGATING ENZYME-RELATED1 Decreases RELATED TO UBIQUITIN Conjugation and Alters Auxin Response and Development
Plant Physiology,
June 1, 2007;
144(2):
976 - 987.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Kraft, R. Kuglitsch, J. Kwiatkowski, M. Frank, and K. Grossmann
Indole-3-acetic acid and auxin herbicides up-regulate 9-cis-epoxycarotenoid dioxygenase gene expression and abscisic acid accumulation in cleavers (Galium aparine): interaction with ethylene
J. Exp. Bot.,
April 1, 2007;
58(6):
1497 - 1503.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. G. Ralph, J.W. Hudgins, S. Jancsik, V. R. Franceschi, and J. Bohlmann
Aminocyclopropane Carboxylic Acid Synthase Is a Regulated Step in Ethylene-Dependent Induced Conifer Defense. Full-Length cDNA Cloning of a Multigene Family, Differential Constitutive, and Wound- and Insect-Induced Expression, and Cellular and Subcellular Localization in Spruce and Douglas Fir
Plant Physiology,
January 1, 2007;
143(1):
410 - 424.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Iwai, A. Miyasaka, S. Seo, and Y. Ohashi
Contribution of Ethylene Biosynthesis for Resistance to Blast Fungus Infection in Young Rice Plants
Plant Physiology,
November 1, 2006;
142(3):
1202 - 1215.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. R. Knopf and T. Trebitsh
The Female-Specific Cs-ACS1G Gene of Cucumber. A Case of Gene Duplication and Recombination between the Non-Sex-Specific 1-Aminocyclopropane-1-Carboxylate Synthase Gene and a Branched-Chain Amino Acid Transaminase Gene
Plant Cell Physiol.,
September 1, 2006;
47(9):
1217 - 1228.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Tanaka, T. Sano, M. Tamaoki, N. Nakajima, N. Kondo, and S. Hasezawa
Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis
J. Exp. Bot.,
July 1, 2006;
57(10):
2259 - 2266.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. van der Graaff, R. Schwacke, A. Schneider, M. Desimone, U.-I. Flugge, and R. Kunze
Transcription Analysis of Arabidopsis Membrane Transporters and Hormone Pathways during Developmental and Induced Leaf Senescence
Plant Physiology,
June 1, 2006;
141(2):
776 - 792.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Gomi, D. Ogawa, S. Katou, H. Kamada, N. Nakajima, H. Saji, T. Soyano, M. Sasabe, Y. Machida, I. Mitsuhara, et al.
A Mitogen-activated Protein Kinase NtMPK4 Activated by SIPKK is Required for Jasmonic Acid Signaling and Involved in Ozone Tolerance via Stomatal Movement in Tobacco
Plant Cell Physiol.,
December 1, 2005;
46(12):
1902 - 1914.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. N. Stepanova, J. M. Hoyt, A. A. Hamilton, and J. M. Alonso
A Link between Ethylene and Auxin Uncovered by the Characterization of Two Root-Specific Ethylene-Insensitive Mutants in Arabidopsis
PLANT CELL,
August 1, 2005;
17(8):
2230 - 2242.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. R. Ecker
Reentry of the Ethylene MPK6 Module
PLANT CELL,
December 1, 2004;
16(12):
3169 - 3173.
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Chang and A. B. Bleecker
Ethylene Biology. More Than a Gas
Plant Physiology,
October 1, 2004;
136(2):
2895 - 2899.
[Full Text]
[PDF]
|
|
|
|
|
