The Cytoskeleton in Plant Immunity: Dynamics, Regulation, and Function

Abstract

The plant cytoskeleton, consisting of actin filaments and microtubules, is a highly dynamic filamentous framework involved in plant growth, development, and stress responses. Recently, research has demonstrated that the plant cytoskeleton undergoes rapid remodeling upon sensing pathogen attacks, coordinating the formation of microdomain immune complexes, the dynamic and turnover of pattern-recognizing receptors (PRRs), the movement and aggregation of organelles, and the transportation of defense compounds, thus serving as an important platform for responding to pathogen infections. Meanwhile, pathogens produce effectors targeting the cytoskeleton to achieve pathogenicity. Recent findings have uncovered several cytoskeleton-associated proteins mediating cytoskeletal remodeling and defense signaling. Furthermore, the reorganization of the actin cytoskeleton is revealed to further feedback-regulate reactive oxygen species (ROS) production and trigger salicylic acid (SA) signaling, suggesting an extremely complex role of the cytoskeleton in plant immunity. Here, we describe recent advances in understanding the host cytoskeleton dynamics upon sensing pathogens and summarize the effectors that target the cytoskeleton. We highlight advances in the regulation of cytoskeletal remodeling associated with the defense response and assess the important function of the rearrangement of the cytoskeleton in the immune response. Finally, we propose suggestions for future research in this area.

Multilevel analysis between Physcomitrium patens and Mortierellaceae endophytes explores potential long‐standing interaction among land plants and fungi

“…Of the upregulated genes, we identified enrichment in three ontologies: cytoskeletal reorganization, cell wall biogenesis and the synthesis of various polysaccharide pathways (Data S4). Complementing what was observed with microscopy, cytoskeletal rearrangement in P. patens may be occurring to harbor the L. elongata hyphae within plant cells but the cytoskeleton also plays dynamic roles in plant growth, development, and immune response (Wang et al., 2022). Additionally, we identified enrichment in cell wall biosynthesis (Data S4).…”

Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underliesArabidopsisresponse to viral infection

“…The precise role of CPK3 in viral immunity remains to be determined. CPK3 phosphorylates actin depolymerization factors to modulate the actin cytoskeleton 21,47 , a key player in host-pathogen interaction 48 . In particular, potexviruses induce the remodeling of the actin cytoskeleton to organize the key steps of their cycle, whether it is replication, intra-cellular movement or cell-to-cell propagation 49,50 .…”

Microtubule Regulation in Plants: From Morphological Development to Stress Adaptation

“…Upon pathogen attack, the plant cytoskeleton undergoes rapid remodeling to coordinate the movement of intracellular organelles and the formation of immune microdomain complexes as well as the transportation of defense compounds and the turnover of recognizing receptors [ 191 ]. Although actin remodeling is thought to play an essential role during plant innate immunity, recent studies have highlighted that immunity-related protein secretion and cell wall-based defense depend on MT-based transport [ 192 ].…”

“…Pathogens produce effectors targeting the cytoskeleton to achieve pathogenicity [ 191 ]. By interacting with MAPs, pathogens can control the MT network in the host cells [ 195 , 198 , 199 ].…”