Accumulation and Transport of 1-Aminocyclopropane-1-Carboxylic Acid (ACC) in Plants: Current Status, Considerations for Future Research and Agronomic Applications

Abstract

1-aminocyclopropane-1-carboxylic acid (ACC) is a non-protein amino acid acting as the direct precursor of ethylene, a plant hormone regulating a wide variety of vegetative and developmental processes. ACC is the central molecule of ethylene biosynthesis. The rate of ACC formation differs in response to developmental, hormonal and environmental cues. ACC can be conjugated to three derivatives, metabolized in planta or by rhizobacteria using ACC deaminase, and is transported throughout the plant over short and long distances, remotely leading to ethylene responses. This review highlights some recent advances related to ACC. These include the regulation of ACC synthesis, conjugation and deamination, evidence for a role of ACC as an ethylene-independent signal, short and long range ACC transport, and the identification of a first ACC transporter. Although unraveling the complex mechanism of ACC transport is in its infancy, new questions emerge together with the identification of a first transporter. In the light of the future quest for additional ACC transporters, this review presents perspectives of the novel findings and includes considerations for future research toward applications in agronomy.

Keywords: 1-aminocyclopropane-1-carboxylic acid; ACC; agriculture; conjugation; deaminase; ethylene; signal; transport.

FIGURE 1

Structural overview of ethylene biosynthesis. The amino acid methionine is converted to S-adenosyl-L-methionine (SAM) by SAM-synthetase (SAMS), a reaction that requires ATP. SAM is then converted to ACC by ACC synthase (ACS), in a reaction that cleaves off a 5′methylthioadenosine (MTA). MTA is recycled back to methionine through a series of intermediate steps, known as the Yang cycle or Methionine Salvage Pathway. In the presence of oxygen, ACC is converted to ethylene by ACC oxidase (ACO). The ovals represent sets of endogenous and exogenous cues stimulating ethylene production. IAA, indol-3-acetic acid (Auxin); CK, cytokinin; BR, brassinosteroid; JA, jasmonic acid; ABA, abscisic acid.

FIGURE 2

Developmental regulation of ACS genes at the transcriptional level. Cartoon representation of the expression of ACS genes during the transition from system 1 to system 2 ethylene biosynthesis in tomato fruit ripening. System 1 ethylene biosynthesis is regulated by the expression of LE-ACS1A and LE-ACS6 in green fruit, followed by a transition period in which LE-ACS1A expression increases and LE-ACS4 expression is induced. The elevated ethylene production results in a negative feedback on the system 1 pathway, reducing LE-ACS1A and LE-ACS6 expression. System 2 ethylene biosynthesis is regulated by the expression of LE-ACS2 and LE-ACS4. Relative levels of gene expression are presented by the size of the arrows; genes negatively regulated by ethylene are presented in orange; genes positively regulated by ethylene are presented in blue.

FIGURE 3

Model for the post-translational regulation of the Arabidopsis ACSs. Type I ACS proteins contain one CDPK and three MAPK phosphorylation sites. They are phosphorylated by MPK3/6 in response to external stress signals and by CDPKs, leading to stabilization and hence, enhanced ethylene production. Dephosphorylation is controlled by PP2A and PP2C. Type II ACS proteins contain one CDPK phosphorylation site and are assumed to also be more stable in their phosphorylated state. These proteins are ubiquitinated by ETO1 and EOL1/2 ubiquitin ligases. Cytokinin (or brassinosteroid) treatment has been suggested to block the ETO or EOL1/2 mediated targeting of type II ACSs. The type III ACS7 protein is potentially phosphorylated by CDPKs at its catalytic site, and is ubiquitinated by the E3 ligase XBAT32. P, phosphate group; S, serine residue.

FIGURE 4

Structural overview of ACC conjugation and deamination. From ACC, three known conjugates can be formed. 1-malonyl-ACC (MACC) is formed by ACC-N-malonyl transferase (AMT), a reaction that requires malonyl-CoA. Jasmonyl-ACC (JA-ACC) is formed by jasmonic acid resistance 1 (JAR1). γ-glutamyl-ACC (GACC) is formed by γ-glutamyl-transpeptidase (GGT), a reaction that requires glutathione (GSH). The deamination of ACC by ACC deaminase yields α-ketobutyrate and ammonium.

FIGURE 5

Dose-dependent response of Arabidopsis thaliana seedlings to exogenously applied ACC suggesting possible involvement of ARE2/LHT1 in ACC transport. Wild type and are2 mutants were grown in the darkness for 4 days on Murashige and Skoog (MS) medium containing various ACC concentrations (0, 0.5, 1, 10, and 20 μM ACC). Scale bar = 5 mm. (A) Representative phenotypes for the wild type (WT) and are2 mutant. (B,C) Hypocotyl lengths and root lengths of seedlings grown as in (A). Figure reproduced from Shin et al. (2015).

FIGURE 6

Gene expression of ethylene biosynthesis genes and genes of the LHT family of amino acid transporters. Cell type-specific relative expression patterns are presented for the root, the hypocotyl, and the leaf. The root stages indicate the developmental stages as described by (Birnbaum et al., 2003) for 6 days old seedlings. Stage I: where the root tip reached its full diameter (about 0.15 mm from the root tip); stage II: where cells begin longitudinal expansion (about 0.30 mm from the root tip); stage III: where root hairs are fully elongated (0.45 to 2 mm from the root tip). For each gene, the cell type-specific expression levels presented were computed relative to the maximal absolute expression, which can be found behind each gene name.

FIGURE 7

Gene expression of ethylene biosynthesis genes and genes of the LHT family of amino acid transporters. Relative expression patterns are presented for given tissues in different developmental stages. For each gene, the relative expression levels presented were computed relative to the maximal absolute expression, which can be found behind each gene name.