MRF Family Genes Are Involved in Translation Control, Especially under Energy-Deficient Conditions, and Their Expression and Functions Are Modulated by the TOR Signaling Pathway

Abstract

Dynamic control of protein translation in response to the environment is essential for the survival of plant cells. Target of rapamycin (TOR) coordinates protein synthesis with cellular energy/nutrient availability through transcriptional modulation and phosphorylation of the translation machinery. However, mechanisms of TOR-mediated translation control are poorly understood in plants. Here, we report that Arabidopsis thaliana MRF (MA3 DOMAIN-CONTAINING TRANSLATION REGULATORY FACTOR) family genes encode translation regulatory factors under TOR control, and their functions are particularly important in energy-deficient conditions. Four MRF family genes (MRF1-MRF4) are transcriptionally induced by dark and starvation (DS). Silencing of multiple MRFs increases susceptibility to DS and treatment with a TOR inhibitor, while MRF1 overexpression decreases susceptibility. MRF proteins interact with eIF4A and cofractionate with ribosomes. MRF silencing decreases translation activity, while MRF1 overexpression increases it, accompanied by altered ribosome patterns, particularly in DS. Furthermore, MRF deficiency in DS causes altered distribution of mRNAs in sucrose gradient fractions and accelerates rRNA degradation. MRF1 is phosphorylated in vivo and phosphorylated by S6 kinases in vitro. MRF expression and MRF1 ribosome association and phosphorylation are modulated by cellular energy status and TOR activity. We discuss possible mechanisms of the function of MRF family proteins under normal and energy-deficient conditions and their functional link with the TOR pathway.

Integration of nutrient, energy, light, and hormone signalling via TOR in plants

“…As the conserved direct targets of TOR protein kinase, S6K1/2 relay signalling by phosphorylating RPS6 (the 40S ribosomal subunit S6) and MRF (MA3 domain-containing translation regulatory factor) in response to light, sugar, and energy status in plants (Ren et al, 2012;Xiong et al, 2013;Dobrenel et al, 2016b;Enganti et al, 2017;Lee et al, 2017;Chen et al, 2018). Comprehensive phenotypic analyses of rps6a and rps6b mutants and genetic complementation support downstream roles of RPS6 in light and nutrient-dependent TOR functions in root, leaf, and flowering regulation (Ren et al, 2012), as well as in the control of rRNA synthesis (Kim et al, 2014;Son et al, 2015) (Fig.…”

TOR signaling in plants: conservation and innovation

“…After activation by TAV, TOR activates S6K1 and thus phosphorylates eIF3h and RISP (re-initiation-supporting protein) to recruit re-initiation factors and polysomes to re-initiate mRNA translation (Schepetilnikov et al, 2011;Thiébeauld et al, 2009). Furthermore, MRF1 (MA3 DOMAIN-CONTAINING TRANSLATION REGULATORY FACTOR 1) was recently reported to be an S6K substrate, which regulates mRNA translation especially in energy deficient conditions (Lee et al, 2017).…”

Translational gene regulation in plants: A green new deal

“…TOR kinase additionally signals to a variety of translation-relevant proteins including MRFs, which are partners of eIF4A helicase, the RP eS6, and the inhibitor of Pol III, MAF1 (Ahn et al, 2019;Bush et al, 2016;D. H. Lee et al, 2017).…”

“…(Based on: Ahn et al, 2019;Y. Dong et al, 2017;Izquierdo et al, 2018;Lageix et al, 2008;Lee et al, 2017;Lokdarshi, Guan, et al, 2020;Nukarinen et al, 2016;A. Rodrigues et al, 2013;M.…”