1-Aminocyclopropane-1-Carboxylic Acid Oxidase (ACO): The Enzyme That Makes the Plant Hormone Ethylene

Abstract

The volatile plant hormone ethylene regulates many plant developmental processes and stress responses. It is therefore crucial that plants can precisely control their ethylene production levels in space and time. The ethylene biosynthesis pathway consists of two dedicated steps. In a first reaction, S-adenosyl-L-methionine (SAM) is converted into 1-aminocyclopropane-1-carboxylic acid (ACC) by ACC-synthase (ACS). In a second reaction, ACC is converted into ethylene by ACC-oxidase (ACO). Initially, it was postulated that ACS is the rate-limiting enzyme of this pathway, directing many studies to unravel the regulation of ACS protein activity, and stability. However, an increasing amount of evidence has been gathered over the years, which shows that ACO is the rate-limiting step in ethylene production during certain dedicated processes. This implies that also the ACO protein family is subjected to a stringent regulation. In this review, we give an overview about the state-of-the-art regarding ACO evolution, functionality and regulation, with an emphasis on the transcriptional, post-transcriptional, and post-translational control. We also highlight the importance of ACO being a prime target for genetic engineering and precision breeding, in order to control plant ethylene production levels.

Keywords: 1-aminocyclopropane-1-carboxylate oxidase; ethylene biosynthesis; phylogeny; physiology; transcriptional and post-translation regulation.

FIGURE 1

Structural representation of the ethylene biosynthesis pathway. Methionine is converted into SAM by SAM synthetase (SAMS) requiring ATP. Next, SAM is converted into methylthioadenosine (MTA) and 1-aminocyclopropane-1-carboxylic acid (ACC) by ACC-synthase (ACS). MTA is recycled back to methionine by the Yang-cycle (several reactions depicted by the dotted line). In the final step, ACC-oxidase (ACO) catalyzes the release of ethylene from ACC using molecular oxygen.

FIGURE 2

Maximal likelihood phylogenetic tree for ACO protein sequences of Arabidopsis thaliana (AT), Tomato (Solanum lycopersicum; Solyc), Apple (Malus domestica; MDP), Rice (Oryza sativa; Os), and Maize (Zea mays; Zm) retrieved from Phytozome (v12.1). Protein sequences were aligned in Geneious (v10.2.2) using the MUSCLE alignment plugin. The phylogenetic tree was build using RAxML (v8.2.11) for best-scoring maximum likelihood tree with rapid bootstrapping (1000 bootstrap replicates). Bootstrap values for the main branches are depicted on the tree. Type I ACO is shown in blue, Type II ACO is shown in red, and Type III ACO is shown in green.

FIGURE 3

ACO protein sequence alignment of Arabidopsis thaliana, Solanum lycopersicum, and Malus domestica. Protein sequences were aligned in Geneious (v10.2.2) using the MUSCLE alignment plugin. Important residues are marked according to the legend shown. Type I ACO is shown in blue, Type II ACO is shown in red, and Type III ACO is shown in green.

FIGURE 4

Tissue-specific and developmental expression profiles of the five Arabidopsis ACOs. Data is adapted from the eFP browser. The color scale depicts a Log2 fold expression range (Waese et al., 2017). (A) Expression in the vegetative rosette and the root, (B) the different leaves, (C) the different flowering organs, (D) mature pollen, (E) the different stages of embryogenesis, (F) the dry and imbibed seed, and (G) a 1-day-old seedling (Nakabayashi et al., 2005; Schmid et al., 2005; Klepikova et al., 2016).

FIGURE 5

Tissue-specific and developmental expression profiles of the seven tomato ACOs during fruit development and ripening. Data is adapted from the Tomato Expression Atlas (TEA). The color scale depicts the reads per million mapped reads (RPM). Days post anthesis (DPA).