EBP1 nuclear accumulation negatively feeds back on FERONIA-mediated RALF1 signaling

Abstract

FERONIA (FER), a plasma membrane receptor-like kinase, is a central regulator of cell growth that integrates environmental and endogenous signals. A peptide ligand rapid alkalinization factor 1 (RALF1) binds to FER and triggers a series of downstream events, including inhibition of Arabidopsis H+-ATPase 2 activity at the cell surface and regulation of gene expression in the nucleus. We report here that, upon RALF1 binding, FER first promotes ErbB3-binding protein 1 (EBP1) mRNA translation and then interacts with and phosphorylates the EBP1 protein, leading to EBP1 accumulation in the nucleus. There, EBP1 associates with the promoters of previously identified RALF1-regulated genes, such as CML38, and regulates gene transcription in response to RALF1 signaling. EBP1 appears to inhibit the RALF1 peptide response, thus forming a transcription–translation feedback loop (TTFL) similar to that found in circadian rhythm control. The plant RALF1-FER-EBP1 axis is reminiscent of animal epidermal growth factor receptor (EGFR) signaling, in which EGF peptide induces EGFR to interact with and phosphorylate EBP1, promoting EBP1 nuclear accumulation to control cell growth. Thus, we suggest that in response to peptide signals, plant FER and animal EGFR use the conserved key regulator EBP1 to control cell growth in the nucleus.

ErbB-3 BINDING PROTEIN 1 Regulates Translation and Counteracts RETINOBLASTOMA RELATED to Maintain the Root Meristem

“…Fluorescently tagged EBP1 could be detected throughout the cytosol, nucleus, and nucleolus, although the nuclear and nucleolar accumulation were largely masked when EBP1 was tagged at its C terminus. We conclude that EBP1 is likely found in all three compartments as suggested by the N-terminally tagged version, because (1) growth factor signaling promoted nuclear accumulation of EBP1-GFP (Li et al, 2018), (2) others have detected tagged EBP1 proteins in plant nuclei of various cell types (Zhang et al, 2005;Cao et al, 2009;Li et al, 2016;Palm et al, 2019), and (3) native Arabidopsis EBP1 was detected in a purified nucleolar preparation (Pendle et al, 2005).…”

“…In a recent study, EBP1 was identified as an interactor with the FERONIA receptor-like kinase with a major function in regulating cell expansion. FER-ONIA directly phosphorylates EBP1, leading to its nuclear localization to regulate genes responsive to FERONIA signaling (Li et al, 2018).…”

Transcriptomic analysis of Lycium ruthenicum Murr. during fruit ripening provides insight into structural and regulatory genes in the anthocyanin biosynthetic pathway

“…Nine independent cDNA libraries from three different maturation stages (S1, S2, and S3) of the L. ruthenicum fruits were constructed according to the method detailedly described by Li et al [45]. Each library was sequenced in parallel using the Illumina HiSeq XTen sequencing platform at Shanghai Oe Biotech.…”

Cold tolerance in rice plants is partially controlled by root responses

“…FERONIA (FER), a receptor-like kinase, is involved in brassinosteroids and auxin signaling pathways, which have positive roles in cell growth and development. Such activation occurs through the interaction with a Rapid Alkalinization Factor (RALF1) peptide, triggering a series of downstream events related with plant growth and stress response (Li et al 2018).…”