Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells

• Published in: Cell reports (Cambridge) Vol. 42; no. 2; p. 112130
• Main Authors: Ntefidou, Maria, Eklund, D. Magnus, Le Bail, Aude, Schulmeister, Sylwia, Scherbel, Franziska, Brandl, Lisa, Dörfler, Wolfgang, Eichstädt, Chantal, Bannmüller, Anna, Ljung, Karin, Kost, Benedikt
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 28-02-2023; Elsevier
• Subjects: auxin; Cell Biology; cell differentiation; Cellbiologi; CP: Developmental biology; CP: Plants; CRIB domain; initial cells; land plant evolution; nuclear targeting; Physcomitrium patens; RHO/ROP effectors; RHO/ROP GTPases; tip growth; CRIB domain; CP: Plants; cell differentiation; auxin; land plant evolution; nuclear targeting; Physcomitrium patens; CP: Developmental biology; initial cells; tip growth; RHO/ROP GTPases; RHO/ROP effectors
• DOI: 10.1016/j.celrep.2023.112130
• EISSN: 2211-1247

RHO guanosine triphosphatases are important eukaryotic regulators of cell differentiation and behavior. Plant ROP (RHO of plant) family members activate specific, incompletely characterized downstream signaling. The structurally simple land plant Physcomitrium patens is missing homologs of key animal and flowering plant RHO effectors but contains a single CRIB (CDC42/RAC interactive binding)-domain-containing RIC (ROP-interacting CRIB-containing) protein (PpRIC). Protonemal P. patens filaments elongate based on regular division and PpROP-dependent tip growth of apical initial cells, which upon stimulation by the hormone auxin differentiate caulonemal characteristics. PpRIC interacts with active PpROP1, co-localizes with this protein at the plasma membrane at the tip of apical initial cells, and accumulates in the nucleus. Remarkably, PpRIC is not required for tip growth but is targeted to the nucleus to block caulonema differentiation downstream of auxin-controlled gene expression. These observations establish functions of PpRIC in mediating crosstalk between ROP and auxin signaling, which contributes to the maintenance of apical initial cell identity.
[Display omitted]
•The PpROP interactor PpRIC is the only homolog of key RHO effectors in P. patens•PpRIC homologs are structurally conserved in most land plants except flowering plants•PpRIC has nuclear functions, while most flowering plant homologs modulate F-actin•PpRIC specifically blocks auxin- and high-light-induced caulonema differentiation
Ntefidou et al. show that RICs, key CRIB-domain effectors of ROP (RHO of plant) GTPases, are represented by few closely related homologs in most land plants but display massive diversification in flowering plants. Whereas most flowering plant RICs modulate cytoplasmic F-actin, moss PpRIC has nuclear functions in maintaining apical initial cell identity.