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A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis in Arabidopsis thaliana

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Tsuchisaka, Atsunari, Yu, Guixia, Jin, Hailing, Alonso, Jose M, Ecker, Joseph R, Zhang, Xiaoming, Gao, Shang, Theologis, Athanasios·2009·Genetics

DOI 10.1534/genetics.109.107102PMC PMC2778992

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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.

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Additional file 1 of Phospholipase D activation is required for 1-aminocyclopropane 1-carboxylic acid signaling during sexual reproduction in the marine red alga Neopyropia yezoensis (Rhodophyta)
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Additional file 6 of Early transcriptome changes induced by the Geminivirus C4 oncoprotein: setting the stage for oncogenesis
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Additional file 3 of Early transcriptome changes induced by the Geminivirus C4 oncoprotein: setting the stage for oncogenesis
Deom, C. M., Alabady, M., & Yang, L. (2021) · Figshare · doi:10.6084/m9.figshare.14150825
Additional file 4 of Early transcriptome changes induced by the Geminivirus C4 oncoprotein: setting the stage for oncogenesis
Deom, C. M., Alabady, M., & Yang, L. (2021) · Figshare · doi:10.6084/m9.figshare.14150828
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Authors: Tsuchisaka, A., Yu, G., Jin, H., Alonso, J. M., Ecker, J. R., Zhang, X., Gao, S., & Theologis, A.
Affiliations: Plant Gene Expression Center (US)
University of California, Riverside (US)
Salk Institute for Biological Studies , La Jolla, California 92037
Salk Institute for Biological Studies (US)
Plant Gene Expression Center , Albany, California 94710
ORCID: Yu, Guixia
Jin, Hailing
Ecker, Joseph R
Zhang, Xiaoming
Gao, Shang
Venue: Genetics
Publisher: Oxford University Press (OUP)
Published: 2009-11-01
Volume: 183
Issue: 3
Pages: 979-1003
ISSN: 0016-6731 (ISSN-L)
1943-2631
DOI: 10.1534/genetics.109.107102
PMC: PMC2778992
OpenAlex: W2104743494
Cited by: 309
References: 98
Citations by year: 2026: 13 · 2025: 15 · 2024: 18 · 2023: 23 · 2022: 28 · 2021: 26 · 2020: 21 · 2019: 16 · 2018: 21 · 2017: 20 · 2016: 10 · 2015: 18 · 2014: 17 · 2013: 20 · 2012: 15
FWCI: 17.40
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Postharvest Quality and Shelf Life Management
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords: 1-aminocyclopropane-1-carboxylate synthase, ethylene production, Arabidopsis thaliana, gene family, embryonic lethality, flowering time, FLOWERING LOCUS C, heterodimerization, protein interaction maps, light signaling, disease resistance, gravity response, plant development
MeSH terms: Amino Acids, Cyclic, Epistasis, Genetic, Ethylenes, Genetic Complementation Test, Isoenzymes, Lyases, Mutation, Plant Diseases, S-Adenosylmethionine, Time Factors, Gene Expression Regulation, Enzymologic, Arabidopsis, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Genome, Plant, Reverse Transcriptase Polymerase Chain Reaction, Gene Expression Profiling, Arabidopsis Proteins, Plants, Genetically Modified, Flowers

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A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis in Arabidopsis thaliana

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