Modulation of stress granule dynamics by phosphorylation and ubiquitination in plants

Siou-Luan He; Xiling Wang; Sung-Il Kim; Liang Kong; Ailing Liu; Lei Wang; Ying Wang; Libo Shan; Ping He; Jyan-Chyun Jang

doi:10.1016/j.isci.2024.111162

Modulation of stress granule dynamics by phosphorylation and ubiquitination in plants

iScience. 2024 Oct 23;27(11):111162. doi: 10.1016/j.isci.2024.111162. eCollection 2024 Nov 15.

Authors

Siou-Luan He¹, Xiling Wang², Sung-Il Kim³, Liang Kong³, Ailing Liu^{1

4}, Lei Wang², Ying Wang⁵, Libo Shan³, Ping He³, Jyan-Chyun Jang¹

Affiliations

¹ Department of Horticulture and Crop Science, Center for Applied Plant Sciences, and Center for RNA Biology, The Ohio State University, Columbus, OH 43210, USA.
² Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, and University of Chinese Academy of Sciences, Beijing 10093, China.
³ Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109-1085, USA.
⁴ College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha 410128, Hunan, China.
⁵ Plant Pathology Department and Plant Molecular Cellular Biology Program, University of Florida, Gainesville, FL 32611, USA.

Abstract

The Arabidopsis tandem CCCH zinc finger 1 (TZF1) is an RNA-binding protein that plays a pivotal role in plant growth and stress response. In this report, we show that TZF1 contains two intrinsically disordered regions necessary for its localization to stress granules (SGs). TZF1 recruits mitogen-activated protein kinase (MAPK) signaling components and an E3 ubiquitin ligase KEEP-ON-GOING (KEG) to SGs. TZF1 is phosphorylated by MPKs and ubiquitinated by KEG. Using a high throughput Arabidopsis protoplasts transient expression system, mutant studies reveal that the phosphorylation of specific residues plays differential roles in enhancing or reducing TZF1 SG assembly and protein-protein interaction with mitogen-activated kinase kinase 5 in SGs. Ubiquitination appears to play a positive role in TZF1 SG assembly, because mutations cause a reduction of typical SGs, while enhancing the assembly of large SGs encompassing the nucleus. Together, our results demonstrate that plant SG assembly is distinctively regulated by phosphorylation and ubiquitination.

Keywords: Molecular biology; Plant Biology; Plant physiology.