1-Aminocyclopropane-1-carboxylic acid oxidase determines the fate of ethylene biosynthesis in a tissue-specific way

In seed plants, ethylene is produced from 1-aminocyclopropane-1-carboxylic acid (ACC) by the enzyme ACC oxidase (ACO). Despite the critical role of ACO in ethylene biosynthesis, the ACO gene family has not been fully characterized in Arabidopsis (Arabidopsis thaliana). This study investigated the 5 ACO genes in Arabidopsis, revealing distinct tissue-specific and developmental expression patterns. Each ACO enzyme exhibited a unique enzymatic capacity for ethylene production, facilitating isoform-specific regulation of ethylene biosynthesis. At the subcellular level, ACO localized predominantly in the cytosol, where ethylene biosynthesis likely occurs, but, unexpectedly, also in the nucleus. Through reverse genetics, including single and higher-order aco mutants, we observed a high degree of gene redundancy, sustaining ethylene biosynthesis. Disruption of all 5 ACO genes resulted in plants unable to produce ethylene but did not adversely affect seedling, vegetative, or reproductive development. However, some development processes associated with high rates of ethylene production, such as germination and petal abscission, were impaired in the aco quintuple mutant, while others, such as leaf senescence, were not. This suggests that modulation of ethylene emission rates by ACOs is key in determining specific developmental processes. Furthermore, the aco quintuple mutant showed impaired responses to abiotic (eg nutrient deficiency and metal toxicity) and biotic stress (eg Botrytis cinerea), akin to ethylene-insensitive plants. This highlights the pivotal role of ethylene in modulating stress responses. In conclusion, the ACO gene family plays a vital role in fine-tuning ethylene biosynthesis in a spatial-temporal way, thereby modulating plant development and stress resilience.