Nuclear Localization of G3BP6 Is Essential for the Flowering Transition in

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2023 Dec 23

PMID 38136569

Authors

Yuzhu Wang

Zhiyong Li

Xiaoju Liang

Yeling Zhou

Jiansheng Liang

Affiliations

Soon will be listed here.

Abstract

The Ras GTPase-activating protein SH3 domain-binding protein (G3BP) belongs to the highly conserved family of RNA-binding proteins, which has been well-investigated in humans and animals. However, limited study of plant G3BP has been reported, and the precise biological function of the G3BP family has not been elucidated yet. In this study, the G3BP family, comprising seven members, was comparatively analyzed. Transcriptome analysis showed that most genes are ubiquitously expressed in various tissues/organs. Transient expression analysis revealed that all G3BPs were presented in the cytoplasm, among which G3BP6 was additionally found in the nucleus. Further study revealed a conserved NLS motif required for the nuclear localization of G3BP6. Additionally, phenotypic analysis revealed that loss-of-function presented late-flowering phenotypes. RNA-sequencing analysis and qRT-PCR assays demonstrated that the expressions of abundant floral genes were significantly altered in plants. We also discovered that overexpression of G3BP6 in the nucleus, rather than in the cytoplasm, propelled bolting. Furthermore, we revealed that the scaffold protein Receptor for Activated C Kinase 1 (RACK1) interacted with and modulated the nuclear localization of G3BP6. Altogether, this study sheds new light on G3BP6 and its specific role in regulating the flowering transition in .

References

Chen J, Ullah H, Temple B, Liang J, Guo J, Alonso J . RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. J Exp Bot. 2006; 57(11):2697-708. DOI: 10.1093/jxb/erl035. View

Briggs S, Bryant S, Jove R, Sanderson S, Smithgall T . The Ras GTPase-activating protein (GAP) is an SH3 domain-binding protein and substrate for the Src-related tyrosine kinase, Hck. J Biol Chem. 1995; 270(24):14718-24. DOI: 10.1074/jbc.270.24.14718. View

Lee H, Yoo S, Lee J, Kim W, Yoo S, Fitzgerald H . Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res. 2010; 38(9):3081-93. PMC: 2875011. DOI: 10.1093/nar/gkp1240. View

Wu G, Poethig R . Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development. 2006; 133(18):3539-47. PMC: 1610107. DOI: 10.1242/dev.02521. View

Prigent M, Barlat I, Langen H, Dargemont C . IkappaBalpha and IkappaBalpha /NF-kappa B complexes are retained in the cytoplasm through interaction with a novel partner, RasGAP SH3-binding protein 2. J Biol Chem. 2000; 275(46):36441-9. DOI: 10.1074/jbc.M004751200. View

Li Z, Fu Y, Wang Y, Liang J . Scaffold protein RACK1 regulates BR signaling by modulating the nuclear localization of BZR1. New Phytol. 2023; 239(5):1804-1818. DOI: 10.1111/nph.19049. View

Onomoto K, Yoneyama M, Fung G, Kato H, Fujita T . Antiviral innate immunity and stress granule responses. Trends Immunol. 2014; 35(9):420-8. PMC: 7185371. DOI: 10.1016/j.it.2014.07.006. View

Serivichyaswat P, Ryu H, Kim W, Kim S, Chung K, Kim J . Expression of the floral repressor miRNA156 is positively regulated by the AGAMOUS-like proteins AGL15 and AGL18. Mol Cells. 2015; 38(3):259-66. PMC: 4363726. DOI: 10.14348/molcells.2015.2311. View

Wu G, Park M, Conway S, Wang J, Weigel D, Poethig R . The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell. 2009; 138(4):750-9. PMC: 2732587. DOI: 10.1016/j.cell.2009.06.031. View

10.

Fernandez D, Wang C, Zheng Y, Adamczyk B, Singhal R, Hall P . The MADS-Domain Factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, Are Necessary to Block Floral Gene Expression during the Vegetative Phase. Plant Physiol. 2014; 165(4):1591-1603. PMC: 4119041. DOI: 10.1104/pp.114.242990. View

11.

French J, Stirling R, Walsh M, Kennedy H . The expression of Ras-GTPase activating protein SH3 domain-binding proteins, G3BPs, in human breast cancers. Histochem J. 2003; 34(5):223-31. DOI: 10.1023/a:1021737413055. View

12.

Abulfaraj A, Mariappan K, Bigeard J, Manickam P, Blilou I, Guo X . The homolog of human G3BP1 is a key regulator of stomatal and apoplastic immunity. Life Sci Alliance. 2018; 1(2):e201800046. PMC: 6238584. DOI: 10.26508/lsa.201800046. View

13.

Urano D, Czarnecki O, Wang X, Jones A, Chen J . Arabidopsis receptor of activated C kinase1 phosphorylation by WITH NO LYSINE8 KINASE. Plant Physiol. 2014; 167(2):507-16. PMC: 4326752. DOI: 10.1104/pp.114.247460. View

14.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

15.

Alam U, Kennedy D . Rasputin a decade on and more promiscuous than ever? A review of G3BPs. Biochim Biophys Acta Mol Cell Res. 2019; 1866(3):360-370. PMC: 7114234. DOI: 10.1016/j.bbamcr.2018.09.001. View

16.

Xu M, Hu T, Smith M, Poethig R . Epigenetic Regulation of Vegetative Phase Change in Arabidopsis. Plant Cell. 2015; 28(1):28-41. PMC: 4746683. DOI: 10.1105/tpc.15.00854. View

17.

Reuper H, Gotte B, Williams L, Tan T, McInerney G, Panas M . G3BP Ortholog Rescues Mammalian Stress Granule Phenotype across Kingdoms. Int J Mol Sci. 2021; 22(12). PMC: 8230867. DOI: 10.3390/ijms22126287. View

18.

Reuper H, Krenz B . Comparison of two Turnip mosaic virus P1 proteins in their ability to co-localize with the Arabidopsis thaliana G3BP-2 protein. Virus Genes. 2021; 57(2):233-237. PMC: 7985126. DOI: 10.1007/s11262-021-01829-w. View

19.

Jaeger K, Wigge P . FT protein acts as a long-range signal in Arabidopsis. Curr Biol. 2007; 17(12):1050-4. DOI: 10.1016/j.cub.2007.05.008. View

20.

Jung J, Lee H, Ryu J, Park C . SPL3/4/5 Integrate Developmental Aging and Photoperiodic Signals into the FT-FD Module in Arabidopsis Flowering. Mol Plant. 2016; 9(12):1647-1659. DOI: 10.1016/j.molp.2016.10.014. View