Plant protein disorder: spatial regulation, broad specificity, switch of signaling and physiological status

Abstract

Intrinsically disordered proteins (IDPs) are a group of functional proteins without defined 3D structures. Some structured proteins contain ordered domains and functional intrinsically disordered regions (IDRs). Rather than having a single fixed structure, IDPs/IDRs may adopt various conformations depending on different situations (Kim and Han, 2018; Uversky, 2019). Because of the structural flexibility, IDPs/IDRs are not restricted to lock-key modules but rather interact with different partners under different circumstances. Thus, IDPs/IDRs have versatile roles and multiple functions in numerous biological processes (Tompa et al., 2015; Uversky, 2019). IDRs of transcription factors are proposed to provide functional versatility in molecular recognition via their binding plasticity, which facilitates transcriptional regulation of structural domains (Sun et al., 2012). IDPs/IDRs are key factors triggering liquid–liquid phase separation/transition (LLPS/LLPT), which forms membrane-less compartments apart from liquid fluid in a cell, also known as biomolecular condensates, thus allowing the spatiotemporal organization of biochemical reactions by concentrating macromolecules locally (Cuevas-Velazquez and Dinneny, 2018; Kim et al., 2021). In plants, IDRs of transcription factors and signal transduction proteins often form flexible interaction networks or receive various signals, such as plant-specific NAC (for NO APICAL MERISTEM, ATAF, CUP-SHAPED COTYLEDON) transcription factors involved in seed germination and seedling establishment and GRAS (for GIBBERELLIC ACID INSENSITIVE, REPRESSOR of GAI, and the SCARECROW) proteins functioning in gibberellic acid signaling, whereas specific classes of IDPs are involved in flowering and abiotic stress responses (Sun et al., 2013; Covarrubias et al., 2017). Typical examples of plant IDRs/IDPs are shown in Figure 1A. Readers are invited to visit the previous review papers regarding specific topics such as plant IDPs (Sun et al., 2013; Covarrubias et al., 2017), LLPS in plants (Cuevas-Velazquez and Dinneny, 2018; Kim et al., 2021), and dehydrins in stress responses (Cuevas-Velazquez et al., 2014; Graether and Boddington, 2014; Kosová et al., 2014; Yu et al., 2018). Instead of summarizing the versatile functions of IDPs/IDRs in detail as in the aforementioned review papers, this article highlights the recent breakthroughs in plant IDP/IDR research to provide the whole-picture view; proposes conceptual principles of their action modes on spatial regulation, broad specificity, and signaling/physiological switch; and calls for more research in this emerging field.