Abstract
Cell–cell communication plays a crucial role in plant growth and development and relies to a large extent on peptide ligand–receptor kinase signaling mechanisms. The CRINKLY4 (CR4) family of receptor-like kinases is involved in a wide range of developmental processes in plants, including mediating columella stem cell identity and differentiation in the Arabidopsis thaliana root tip. Members of the CR4 family contain a signal peptide, an extracellular part, a single-pass transmembrane helix and an intracellular cytoplasmic protein kinase domain. The main distinguishing features of the family are the presence of seven “crinkly” repeats and a TUMOR NECROSIS FACTOR RECEPTOR (TNFR)-like domain in the extracellular part. Here, we investigated the evolutionary origin of the CR4 family and explored to what extent members of this family are conserved throughout the green lineage. We identified members of the CR4 family in various dicots and monocots, and also in the lycophyte Selaginella moellendorffii and the bryophyte Physcomitrella patens. In addition, we attempted to gain insight in the evolutionary origin of different CR4-specific domains, and we could detect “crinkly” repeat containing proteins already in single celled algae. Finally, we related the presence of likely functional CR4 orthologs to its best described signaling module comprising CLAVATA3/EMBRYO SURROUNDING REGION-RELATED 40 (CLE40), WUSCHEL RELATED HOMEOBOX 5 (WOX5), CLAVATA 1 (CLV1), and ARABIDOPSIS CR4 (ACR4), and established that this module likely is already present in bryophytes and lycophytes.
Highlights
Stem cells are fundamental for post-embryonic plant growth, and the stem cell niche is subject to a tight regulation
Features of the CR4 Family in A. thaliana In A. thaliana, the CR4 family consists of five members distributed over two clades; one that includes ARABIDOPSIS CRINKLY 4 (ACR4)/CRINKLY 4 (CR4) (AT3G59420–Q9LX29), CRINKLY 4 RELATED 1 (CCR1 or CRR1) (AT3G09780– Q9S7D9), and CRINKLY 4 RELATED 2 (CCR2 or CRR2) (AT2G39180–O80963) and one with CRINKLY 4 RELATED 3 (CCR3 or CRR3) (AT3G55950–Q9LY50) and CRINKLY 4 RELATED 4 (CCR4)/CRINKLY 4-RELATED KINASE 1 or CYTOKININ-REGULATED KINASE 1 (CRK1) (AT5G47850– Q9FIJ6) (Figure 1A)
The ARABIDOPSIS CR4 (ACR4) extracellular part is required for protein function, and the “crinkly” repeats include several cysteine residues in C(X∼10)CWG motifs that are likely important for stabilizing disulfide bridges and generating the β-propeller structure of the extracellular part (Gifford et al, 2005) (Figure 2A)
Summary
Stem cells are fundamental for post-embryonic plant growth, and the stem cell niche is subject to a tight regulation (ten Hove et al, 2015). Stem cells are located in the central zone of the shoot apical meristem and around the quiescent center in the root apical meristem. Initiated during early embryogenesis they constantly produce cells during the entire plant life (Scheres, 2007). Despite the obvious involvement of receptor kinases in animals, our understanding of their role in plant growth and development remains very incomplete. Mutations in receptor kinases often lead to obvious and crucial developmental defects as they are, for example, involved in root and shoot apical meristem maintenance (De Smet et al, 2009; Stahl and Simon, 2012; Wierzba and Tax, 2013)
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