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 Background The growth-regulating factor-interacting factor (GIF) gene family plays a vital role in regulating plant growth and development, particularly in controlling leaf, seed, and root meristem homeostasis. However, the regulatory mechanism of heteromorphic leaves by GIF genes in Populu...

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Main Authors: Yuqi Yang, Jianhao Sun, Chen Qiu, Peipei Jiao, Houling Wang, Zhihua Wu, Zhijun Li
Format: Article
Language:English
Published: BMC 2024-03-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10221-5
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author Yuqi Yang
Jianhao Sun
Chen Qiu
Peipei Jiao
Houling Wang
Zhihua Wu
Zhijun Li
author_facet Yuqi Yang
Jianhao Sun
Chen Qiu
Peipei Jiao
Houling Wang
Zhihua Wu
Zhijun Li
author_sort Yuqi Yang
collection DOAJ
description Abstract Background The growth-regulating factor-interacting factor (GIF) gene family plays a vital role in regulating plant growth and development, particularly in controlling leaf, seed, and root meristem homeostasis. However, the regulatory mechanism of heteromorphic leaves by GIF genes in Populus euphratica as an important adaptative trait of heteromorphic leaves in response to desert environment remains unknown. Results This study aimed to identify and characterize the GIF genes in P. euphratica and other five Salicaceae species to investigate their role in regulating heteromorphic leaf development. A total of 27 GIF genes were identified and characterized across six Salicaceae species (P. euphratica, Populus pruinose, Populus deltoides, Populus trichocarpa, Salix sinopurpurea, and Salix suchowensis) at the genome-wide level. Comparative genomic analysis among these species suggested that the expansion of GIFs may be derived from the specific Salicaceae whole-genome duplication event after their divergence from Arabidopsis thaliana. Furthermore, the expression data of PeGIFs in heteromorphic leaves, combined with functional information on GIF genes in Arabidopsis, indicated the role of PeGIFs in regulating the leaf development of P. euphratica, especially PeGIFs containing several cis-acting elements associated with plant growth and development. By heterologous expression of the PeGIF3 gene in wild-type plants (Col-0) and atgif1 mutant of A. thaliana, a significant difference in leaf expansion along the medial-lateral axis, and an increased number of leaf cells, were observed between the overexpressed plants and the wild type. Conclusion PeGIF3 enhances leaf cell proliferation, thereby resulting in the expansion of the central-lateral region of the leaf. The findings not only provide global insights into the evolutionary features of Salicaceae GIFs but also reveal the regulatory mechanism of PeGIF3 in heteromorphic leaves of P. euphratica.
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spelling doaj.art-ae25055aabb046128d6038cc5acc178e2024-03-31T11:11:22ZengBMCBMC Genomics1471-21642024-03-0125111210.1186/s12864-024-10221-5Comparative 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 leavesYuqi Yang0Jianhao Sun1Chen Qiu2Peipei Jiao3Houling Wang4Zhihua Wu5Zhijun Li6Key Laboratory of Biological Resource Protection and Utilization of Tarim Basin, Xinjiang Production and Construction GroupKey Laboratory of Biological Resource Protection and Utilization of Tarim Basin, Xinjiang Production and Construction GroupKey Laboratory of Biological Resource Protection and Utilization of Tarim Basin, Xinjiang Production and Construction GroupKey Laboratory of Biological Resource Protection and Utilization of Tarim Basin, Xinjiang Production and Construction GroupCollege of Biological Sciences and Technology, Beijing Forestry UniversityCollege of Life Sciences, Zhejiang Normal UniversityKey Laboratory of Biological Resource Protection and Utilization of Tarim Basin, Xinjiang Production and Construction GroupAbstract Background The growth-regulating factor-interacting factor (GIF) gene family plays a vital role in regulating plant growth and development, particularly in controlling leaf, seed, and root meristem homeostasis. However, the regulatory mechanism of heteromorphic leaves by GIF genes in Populus euphratica as an important adaptative trait of heteromorphic leaves in response to desert environment remains unknown. Results This study aimed to identify and characterize the GIF genes in P. euphratica and other five Salicaceae species to investigate their role in regulating heteromorphic leaf development. A total of 27 GIF genes were identified and characterized across six Salicaceae species (P. euphratica, Populus pruinose, Populus deltoides, Populus trichocarpa, Salix sinopurpurea, and Salix suchowensis) at the genome-wide level. Comparative genomic analysis among these species suggested that the expansion of GIFs may be derived from the specific Salicaceae whole-genome duplication event after their divergence from Arabidopsis thaliana. Furthermore, the expression data of PeGIFs in heteromorphic leaves, combined with functional information on GIF genes in Arabidopsis, indicated the role of PeGIFs in regulating the leaf development of P. euphratica, especially PeGIFs containing several cis-acting elements associated with plant growth and development. By heterologous expression of the PeGIF3 gene in wild-type plants (Col-0) and atgif1 mutant of A. thaliana, a significant difference in leaf expansion along the medial-lateral axis, and an increased number of leaf cells, were observed between the overexpressed plants and the wild type. Conclusion PeGIF3 enhances leaf cell proliferation, thereby resulting in the expansion of the central-lateral region of the leaf. The findings not only provide global insights into the evolutionary features of Salicaceae GIFs but also reveal the regulatory mechanism of PeGIF3 in heteromorphic leaves of P. euphratica.https://doi.org/10.1186/s12864-024-10221-5SalicaceaePopulus EuphraticaGIF genesHeteromorphic leavesRegulatory function
spellingShingle Yuqi Yang
Jianhao Sun
Chen Qiu
Peipei Jiao
Houling Wang
Zhihua Wu
Zhijun Li
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
BMC Genomics
Salicaceae
Populus Euphratica
GIF genes
Heteromorphic leaves
Regulatory function
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic Salicaceae
Populus Euphratica
GIF genes
Heteromorphic leaves
Regulatory function
url https://doi.org/10.1186/s12864-024-10221-5
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