Polyploidization leads to salt stress resilience via ethylene signaling in citrus plants

Polyploidization is a common occurrence in the evolutionary history of flowering plants, significantly contributing to their adaptability and diversity. However, the molecular mechanisms behind these adaptive advantages are not well understood. Through comprehensive phenotyping of diploid and tetraploid clones from Citrus and Poncirus genera, we discovered that genome doubling significantly enhances salt stress resilience. Epigenetic and transcriptomic analyses revealed that increased ethylene production in the roots of tetraploid plants was associated with hypomethylation and enhanced chromatin accessibility of the ACO1 gene. This increased ethylene production activates the transcription of reactive oxygen species scavenging genes and stress-related hormone biosynthesis genes. Consequently, tetraploid plants exhibited superior root functionality under salt stress, maintaining improved cytosolic K⁺/Na⁺ homeostasis. To genetically validate the link between salt stress resilience and ACO1 expression, we generated overexpression and knockout lines, confirming the central role of ACO1 expression regulation following genome doubling in salt stress resilience. Our work elucidates the molecular mechanisms underlying the role of genome doubling in stress resilience. We also highlight the importance of chromatin dynamics in fine-tuning ethylene gene expression and activating salt stress resilience pathways, offering valuable insights into plant adaptation and crop genome evolution.