Plant Prionome maps reveal specific roles of prion-like proteins in stress and memory

Abstract

Prions can be considered as molecular memory devices, generating reproducible memory of a conformational change. Prion-like proteins (PrLPs) have been demonstrated to be present in plants, but their role in plant stress and memory remains largely unexplored. In this work, we report the widespread presence of PrLPs in plants through a comprehensive analysis of 39 genomes representing major taxonomic groups. We find diverse functional roles associated with plant prionomes. Investigation of the rice transcriptome further delineated the role of PrLPs in stress and developmental responses, leading us to explore whether and to what extent PrLPs may build stress memory. The rice prionome is significantly enriched for Transposons/Retrotransposons (Ts/RTRs), and we derived transcriptional regulatory inferences from diurnal gene expression revealing a complex regulatory network between PrLPs, transcription factors and genes known to be involved in stress priming, as well as transient and trans-generational plant memory. Overall, our data suggest that plant memory mechanisms may rely upon protein-based signals embedded in PrLPs, in addition to chromatin-based epigenetic signals and provides important insights into the anticipated role of prions in stress and memory.

Exploring cryptic amyloidogenic regions in prion-like proteins from plants

“…Since the original characterization of prion domains in yeast (Chernoff et al, 1995;Serio et al, 1999), PrLDs with similar features have been identified and studied in other organisms such as viruses (Tetz and Tetz, 2018), bacteria (Iglesias et al, 2015;Yuan and Hochschild, 2017;Choi et al, 2022), protozoan (Pallares et al, 2018) or humans (An and Harrison, 2016;Iglesias et al, 2019). Plants have received less attention, with only a few studies focusing on PrLDs' coverage and function (Chakrabortee et al, 2016;Dorone et al, 2021;Garai et al, 2021). To identify the potential presence of CARs in PrLDs (pCARs) from plants, the proteomes of five different model higher plants were first screened with the PLAAC algorithm.…”

“…An opposite tendency is observed for interpCARs, which seem to compensate the sequential amyloidogenic load by reducing the aromatics and increasing b-breakers. (Garai et al, 2021) proteins from plants. The fact that a significant proportion of PrLDs is pCAR-positive makes it challenging to disentangle the contributions of the complete PrLD sequence and pCARs only in a given protein to the detected enrichments.…”

Heterotypic interactions in the dilute phase can drive co-condensation of prion-like low-complexity domains of FET proteins and mammalian SWI/SNF complex

“…Prion-like domains (PLDs) are typically characterized by their low complexity sequence features with an overrepresentation of aromatic (Y/F) and polar amino acids (G/S/Q/N) and depletion of charged residues 6,7 . Proteins with PLDs have been identified in all life forms [8][9][10][11][12] . Prion proteins were initially discovered as proteinaceous infectious agents in bovine spongiform encephalopathy and other neurodegenerative diseases 4, [13][14][15] , but are increasingly recognized with key functional roles in driving phase separation of RNA-binding proteins in the cell, and in the formation of functional amyloids 16,17 .…”

Complex Networks of Prion-Like Proteins Reveal Cross Talk Between Stress and Memory Pathways in Plants

“…CK extends thanks to Ashwani Pareek, Stress Physiology and Molecular Biology Laboratory, School of Life Sciences, JNU, for hosting her during the DST-INSPIRE fellowship. A version of this article is available online as a preprint in bioRxiv ( Garai et al, 2020 ).…”