The RALF1–FERONIA Complex Phosphorylates eIF4E1 to Promote Protein Synthesis and Polar Root Hair Growth

Abstract

The molecular links between extracellular signals and the regulation of localized protein synthesis in plant cells are poorly understood. Here, we show that in Arabidopsis thaliana, the extracellular peptide RALF1 and its receptor, the FERONIA receptor kinase, promote root hair (RH) tip growth by modulating protein synthesis. We found that RALF1 promotes FERONIA-mediated phosphorylation of eIF4E1, a eukaryotic translation initiation factor that plays a crucial role in the control of mRNA translation rate. Phosphorylated eIF4E1 increases mRNA affinity and modulates mRNA translation and, thus, protein synthesis. The mRNAs targeted by the RALF1-FERONIA-eIF4E1 module include ROP2 and RSL4, which are important regulators of RH cell polarity and growth. RALF1 and FERONIA are expressed in a polar manner in RHs, which facilitate eIF4E1 polar localization and thus may control local ROP2 translation. Moreover, we demonstrated that high-level accumulation of RSL4 exerts negative-feedback regulation of RALF1 expression by directly binding the RALF1 gene promoter, determining the final RH size. Our study reveals that the link between RALF1-FERONIA signaling and protein synthesis constitutes a novel component regulating cell expansion in these polar growing cells.

FERONIA cytoplasmic domain: node of varied signal outputs

“…Exactly how the dose-dependency phenotypes are mediated by FER-K565R-GFP needs further research. Recently, Zhu et al 2020 noticed that FER-K565R/fer-4 is still able to partially phosphorylate one of the FER kinase substrates (eukaryotic initiation factor 4E 1; elF4E1) to promote root hair growth in response to RALF1 peptides (Zhu et al 2020). This indicates that FER's ability to phosphorylate its substrate can be partially masked by FER-K565R ''kinase-dead'' mutants via an as-yet unknown mechanism.…”

“…Chen et al 2016 found that only the fulllength FER kinase domain interacted with ABA Insensitive 2 (ABI2), but that each of the two halves showed no interaction when assessed using the yeast two-hybrid system; FER-K565R also reduced the interaction with ABI2 in vitro, suggesting FER kinase activity may be important for the FER-ABI2 interaction (Chen et al 2016) FER can also directly interact with and phosphorylate ErbB3-binding protein 1 (EBP1), and the FER cytoplasmic domain (FER-CD) and FER-CD K565R all physically associate with EBP1 in GST pull-down assays, suggesting that FER kinase activity may not be necessary for the FER-EBP1 interaction but that it may be necessary for RALF1-induced phosphorylation of EBP1 . Zhu et al 2020 found the interaction of FER and its substrate eIF4E1 is regulated by their reciprocal phosphorylation (Zhu et al 2020). Together, these results indicated that FER kinase activity may not be necessary for control of PT reception, but it may be necessary for the RALF1 response in root growth.…”

“…1). Taking the root as a model, there is accumulating evidence which shows that RALF1 works together with FER to inhibit primary root growth (Haruta et al 2014) but promotes root hair growth (Zhu 2020), supporting the ideal that FER has cell-type-and/or growth environment-dependent function. FER proteins also have varied roles in stress responses; as an example, FER mediates the regulation of cold, heat, and salt response (Chen et al 2016;Zhao et al 2018), and participates in crosstalk with absicisic acid (ABA) (Chen et al 2016;Yu et al 2012), brassinosteroid (BR) (Deslauriers and Larsen 2010; Hofte 2015), ethylene (ET) (Deslauriers and Larsen 2010), and jasmonic acid (JA) (Guo et al 2018) signaling ( Fig.…”

“…Currently, 14 of the 17 CrRLK1Ls in Arabidopsis thaliana and 5 of the 17 CrRLK1Ls in Oryza sativa have been investigated using genetic techniques (Table 1). Shih et al 2014;Li et al 2015;Kessler et al 2010;Haruta et al 2014;Hansen et al 2018;Ngo et al 2014;Huck et al 2003;Escobar-Restrepo et al 2007;Stegmann et al 2017;Keinath et al 2010;Deslauriers and Larsen 2010;Yang et al 2015;Huang et al 2013;Chen et al 2016;Mao et al 2015;Duan et al 2010;Yu 2014;Feng et al 2018;Yu and Assmann 2018;Xu 2019;Zhu et al 2020;Zhao et al 2018;Kessler et al 2015;Haruta et al 2018;Chakravorty et al 2018;Du 2016;Hansen et al 2019;Dunser et al 2019;Dong et al 2019;Yu et al 2018;Yin et al 2018 have recently been identified as one of the ligands of CrRLK1L family (Haruta et al 2014;Gonneau et al 2018;Ge et al 2017;Stegmann et al 2017). RALFs belongs to a group of cysteine-rich small peptides found in various plant species, and participate in pathogen response, plant growth regulation, and PT generation and growth (Haruta et al 2014;Gonneau et al 2018;Ge et al 2017;Stegmann et al 2017;…”

“…As an example, FER inhibits seed integument cells (Yu et al 2014), primary root (Haruta et al 2014, and PT growth Huck et al 2003;Escobar-Restrepo et al 2007) in Arabidopsis (Fig. 1); however, FER promotes leaf cells Duan et al 2010) and root hair cell growth (Duan et al 2010;Zhu et al 2020) (Fig. 1).…”