Genome-wide characterization and evolutionary analysis of the AP2/ERF gene family in lettuce (Lactuca sativa)

Authors: Park, Sunchung - Sun; SHI, AINONG - University Of Arkansas; Meinhardt, Lyndel; Mou, Beiquan

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/5/2023
Publication Date: 12/11/2024
Citation: Park, S., Shi, A., Meinhardt, L.W., Mou, B. 2024. Genome-wide characterization and evolutionary analysis of the AP2/ERF gene family in lettuce (Lactuca sativa). Scientific Reports. 13:21990. https://doi.org/10.1038/s41598-023-49245-4.
DOI: https://doi.org/10.1038/s41598-023-49245-4

Interpretive Summary: Lettuce is one of the most consumed vegetables worldwide. However, due to its herbaceous nature, this crop is vulnerable to environmental stresses like drought, heat, and salinity. The AP2/ERF gene family, a group of transcription factors, is recognized as key factors in stress tolerance in plants. However, our understanding of this gene family in lettuce remains limited, hindering efforts to improve the resilience of lettuce against various stresses. In this study, we identified 224 members of the AP2/ERF family in lettuce through a genome-wide search. An investigation into its duplication patterns and gene expression revealed that some genes undergone duplication, contributing to the expansion of the AP2/ERF gene family. The resulting copies of genes acquired novel functions that help the plant survive harsh conditions. Additionally, an exploration of orthologous relationships uncovered that a substantial number of genes are specific to the lettuce-lineage. These genes might be potential candidates for enhancing stress tolerance of lettuce through genetic improvements. This study deepens our understanding of the AP2/ERF transcription factors in lettuce. The Insights gained can be applied to genetically improve lettuce, enabling it to better weather adverse conditions, especially in the face of climate change. By knowing the family's functionality and evolutionary history, scientists and farmers can develop new ways to develop lettuce varieties that are more resilient to environmental stresses, ensuring the sustainability and security of this crop for the future.

Technical Abstract: The APETALA2/ETHYLENE RESPONSIVE FACTOR (AP2/ERF) gene family plays vital roles in plants, serving as a key regulator in responses to abiotic stresses. Despite its significance, a comprehensive understanding of this family in lettuce remains incomplete. In this study, we performed a genome-wide search for the AP2/ERF family in lettuce and identified a total of 224 members. The duplication patterns provided evidence that both tandem and segmental duplications contributed to the expansion of this family. Ka/Ks ratio analysis demonstrated that, following duplication events, the genes have been subjected to purifying selection pressure, leading to selective constraints on their protein sequence. This selective pressure provides a dosage benefit against stresses in plants. Additionally, a transcriptome analysis indicated that some duplicated genes gained novel functions, emphasizing the contribution of both dosage effect and functional divergence to the family functionalities. Furthermore, an orthologous relationship study showed that 60% of genes descended from a common ancestor of Rosid and Asterid lineages, 28% from the Asterid ancestor, and 12% evolved in the lettuce lineage, suggesting lineage-specific roles in adaptive evolution. These results provide valuable insights into the evolutionary mechanisms of the AP2/ERF gene family in lettuce, with implications for enhancing abiotic stress tolerance, ultimately contributing to the genetic improvement of lettuce crop production.