Prion-like Proteins in Plants: Key Regulators of Development and Environmental Adaptation via Phase Separation

Abstract

Prion-like domains (PrLDs), a unique type of low-complexity domain (LCD) or intrinsically disordered region (IDR), have been shown to mediate protein liquid-liquid phase separation (LLPS). Recent research has increasingly focused on how prion-like proteins (PrLPs) regulate plant growth, development, and stress responses. This review provides a comprehensive overview of plant PrLPs. We analyze the structural features of PrLPs and the mechanisms by which PrLPs undergo LLPS. Through gene ontology (GO) analysis, we highlight the diverse molecular functions of PrLPs and explore how PrLPs influence plant development and stress responses via phase separation. Finally, we address unresolved questions about PrLP regulatory mechanisms, offering prospects for future research.

Keywords: liquid–liquid phase separation; plant development; prion–like domains; prion–like proteins; stress responses.

Figure 1

Gene Ontology (GO) analysis of prion–like protein (PrLP) genes across 10 plant species (Brachypodium distachyon, Hordeum vulgare, Oryza sativa, Sorghum bicolor, Triticum aestivum, Arabidopsis thaliana, Glycine max, Helianthus annuus, Prunus persica, and Solanum lycopersicum). Bubble size represents the number of genes, while color variation represents different p–values.

Figure 2

Prion−like proteins (PrLPs) regulate plant meristem maintenance and light signaling. (A) STM, BELLs, and MED8 form condensates to maintain the SAM. (B) PLTs form NBs with WOX5 and RNA to control the destiny of the CSC and sustain the RAM. (C) PYCO1 forms pyrenoids to bind rubisco, enhancing the efficiency of CO₂ fixation in photosynthesis. (D) The SWAP/SFPS/RRC1 complex interacts with photobodies to regulate alternative splicing of pre–mRNAs. Diamonds indicate PrLPs; ellipses represent other proteins; dashed circles indicate droplet–like condensates; solid–line circles represent gel–like condensates. BELL: BEL1−like; CSC: columella stem cell; NB: nuclear body; Pfr: physiological active far−red form; phyB: phytochrome B; PLT: PLETHORA; Pr: physiological inactive red form; PYCO1: pyrenoid component 1; RAM: root apical meristem; RRC1: REDUCED RED−LIGHT RESPONSES IN CRY1CRY2 BACKGROUND1; SAM: shoot apical meristem; SFPS: SPLICING FACTOR FOR PHYTOCHROME SIGNALING; snRNP: small nuclear ribonucleoproteins; STM: SHOOT MERISTEMLESS; SWAP1: SUPPRESSOR OF WHITE APRICOT/SURP RNA−BINDING DOMAIN CONTAINING PROTEIN1; WOX5: WUSCHEL−RELATED HOMEOBOX 5.

Figure 3

Prion–like proteins (PrLPs) regulate plant reproductive growth. (A) PrLPs regulate flowering and fruit development. (B) SPRI2/SRS7 condensates facilitate the development of interspecific reproductive barriers. (C) YTH07 and EHD6 bind to m⁶A–modified mRNA and form condensates to initiate flowering in rice. (D) TMF and TFAM1/2/3/11 form condensates to modulate the development of inflorescences in tomatoes. Diamonds indicate PrLPs; ellipses represent other proteins; dashed circles indicate droplet–like condensates; solid–line circles represent gel–like condensates. AN: ANANTHA; DCP5: DECAPPING 5; EHD6: EARLY HEADING DATE 6; FCA: FLOWERING CONTROL LOCUS A; FLC: FLOWERING LOCUS C; FLD: FLOWERING LOCUS D; FLM: FLOWERING LOCUS M; FRI: FRIGIDA; FRL: FRIGIDA like; FT: FLOWERING LOCUS T; H3K4me1: monomethylated H3K4; H3K27me3: trimethylated H3K27; H3K36me3: trimethylated H3K36; HRLP: hnRNP R–LIKE PROTEIN; LD: LUMINIDEPENDENS; m⁶A: N⁶–methyladenosine; OsCOL4: CONSTANS–like 4; RNA Pol II: RNA polymerase II; SDG26: SET DOMAIN GROUP 26; SPRI2: STIGMATIC PRIVACY 2; SR45: SERINE/ARGININE–RICH 45; SSF: SISTER OF FCA; TFAM: TMF family member; TMF: TERMINATING FLOWER.

Figure 4

PrLPs regulate plant adaptation to stresses. (A) PrLPs coordinate the plant’s response to abiotic stress. (a,b). PrLPs modulate plant responses to hyperosmotic stress. (b–d). PrLPs modulate plant responses to salt stress. (e,f). PrLPs govern plant responses to heat stress. (B) PrLPs exhibit responses to biotic stressors. (a,b). SGs or PB for immune responses. (c). D–bodies involved in pri–miRNA processing. (d). SGs assemble in response to allelopathic effects. Diamonds indicate PrLPs; ellipses represent other proteins; dashed circles indicate droplet–like condensates. AGO1: ARGONAUTE1; BELL: BEL1–like; CARP9: CONSTITUTIVE ALTERATIONS IN THE SMALL RNA PATHWAYS9; D–body: dicing body; DCL1: Dicer–like1; DCP: DECAPPING; ECT: EVOLUTIONARILY CONSERVED C–TERMINAL REGION; ELF3: EARLY FLOWERING 3; ELF4: EARLY FLOWERING 4; HYL1: Hyponastic Leaves1; m6A: N6–methyladenosine; PA: phenolic acid; PB: processing body; pri–miRNA: primary microRNA; RBP: RNA–binding protein; RBP47B: RNA–binding protein 47B; RH: RNA helicase; RNAi: RNA interference; RNP: ribonucleoprotein; RP: ribosome protein; SA: salicylic acid; SE: SERRATE; SEU: SEUSS; SG: stress granule; SGS3: SUPPRESSOR OF GENE SILENCING 3; STM: SHOOT MERISTEMLESS; TuMV: Turnip mosaic virus; UBP1b: OLIGOURIDYLATE BINDING PROTEIN 1b; VCS: VARICOSE; XRN: 5′–to–3′ exonuclease exoribonuclease.