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

Prions are often considered as molecular memory devices, generating reproducible memory of a conformational change. Prion-like proteins (PrLPs) have been widely demonstrated to be present in plants, but their role in plant stress and memory remains unexplored. In this work, we report the widespread presence of PrLPs in plants through a comprehensive meta-analysis of 39 genomes representing major taxonomic groups. We find diverse functional roles associated with these proteins in various species and term the full complement of PrLPs in a genome as its prionome. In particular, we found the rice prionome being significantly enriched in transposons/retrotransposons (Ts/RTRs) and identified over 60 rice PrLPs that were differentially regulated in stress and developmental responses. This prompted us to explore whether and to what extent PrLPs may build stress memory. By integrating the available rice interactome, transcriptome, and regulome data sets, we could find links between stress and memory pathways that would not have otherwise been discernible. Regulatory inferences derived from the superimposition of these data sets revealed a complex network and cross talk between PrLPs, transcription factors (TFs), and the genes involved in stress priming. This integrative meta-analysis connects transient and transgenerational memory mechanisms in plants with PrLPs, suggesting that plant memory may rely upon protein-based signals in addition to chromatin-based epigenetic signals. Taken together, our work provides important insights into the anticipated role of prion-like candidates in stress and memory, paving the way for more focused studies for validating the role of the identified PrLPs in memory acclimation.

Automated summary

This study revealed the widespread presence of Prion-like proteins (PrLPs) in plants through a comprehensive meta-analysis of 39 genomes, shedding light on their role in plant stress and memory. The rice prionome was found to be significantly enriched in transposons/retrotransposons and over 60 rice PrLPs were identified to be differentially regulated in stress and developmental responses, suggesting their importance in stress memory. The integrative meta-analysis connected transient and transgenerational memory mechanisms in plants with PrLPs, indicating that plant memory may rely not only on chromatin-based epigenetic signals but also on protein-based signals.