Comparative genomic analysis of the Growth Regulating Factors-Interacting Factors (GIFs) in six Salicaceae species and functional analysis of PeGIF3 reveals their regulatory role in Populus heteromorphic leaves

Abstract

Abstract Background The GIF(Growth-Regulating Factors-Interacting Factors) gene family plays a vital role in regulating plant growth and development, particularly in controlling leaf, seed, and root meristem homeostasis. As an important adaptative trait of heteromorphic leaves in response to desert environment, however, the regulatory mechanism of heteromorphic leaves by GIF genes in Populus euphratica remains unknown. Results Our study aimed to identify and characterize the GIF genes in Populus euphratica and other five Salicaceae species to investigate their role in regulating heteromorphic leaf development. We identified and characterized a total of 27 GIF genes across six Salicaceae species (P. euphratica, Populus pruinose, Populus deltoides, Populus trichocarpa, Salix sinopurpurea, and Salix suchowensis) at the genome-wide level. Then, the comparative genomic analysis among these species suggested that the expansion of GIFsmay be derived the specific Salicaceae whole-genome duplication event after their divergence from Arabidopsis. Elements analysis suggested that GIFswere suffering from diverse regulation by hormones and environment clues. Furthermore, the expression data of PeGIFs in heteromorphic leaves, combined with functional information on GIF genes in Arabidopsis thaliana, indicate the role of PeGIFs in regulating leaf development of P. euphratica, especially PeGIFs contain several auxin-related cis-acting elements such as TGA-box. By heterologous expression the PeGIF3 gene in both wild-type plants (Col-0) and gif1mutant of A. thaliana, a significant difference in leaf expansion along the medial-lateral axis, as well as an increased number of leaf cells, along with the increased number of leaf cells was observed between the overexpressed plants and the wild type. Conclusion The results indicated that PeGIF3 enhances leaf cell proliferation by modulating transcriptional processes, thereby resulting in the expansion of the central-lateral region of the leaf. Our findings not only provide global insights into the evolutionary features of Salicaceae GIFs, but also reveal the regulatory mechanism of PeGIF3 in heteromorphic leaves in P. euphratica.