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. 2017 Apr 3:8:376.
doi: 10.3389/fpls.2017.00376. eCollection 2017.

Insights into the Structure, Function, and Ion-Mediated Signaling Pathways Transduced by Plant Integrin-Linked Kinases

Sorina C Popescu  1 , Elizabeth K Brauer  2 , Gizem Dimlioglu  1 , George V Popescu  3
Affiliations

Insights into the Structure, Function, and Ion-Mediated Signaling Pathways Transduced by Plant Integrin-Linked Kinases

Sorina C Popescu et al. Front Plant Sci. .

Abstract

Kinases facilitate detection of extracellular signals and set in motion cellular responses for plant adaptation and survival. Some of the energy utilized for kinase signal processing is produced through the activity of ion transporters. Additionally, the synergy between cellular ions and signal transduction influences plant response to pathogens, and their growth and development. In plants, the signaling elements that connect cell wall and membrane sensors with ion homeostasis and transport-mediated processes are largely unknown. Current research indicates that plant Integrin-Linked Kinases (ILKs), a subfamily Raf-like MAP2K Kinases, may have evolved to fulfill this role. In this review, we explore new findings on plant ILKs placing a particular focus on the connection between ILKs proteins unique structural features and ILKs functions. The ankyrin repeat motifs and the kinase domains of ILKs in Arabidopsis and land plants lineage, respectively, are analyzed and discussed as potential determinants of ILKs' metal ion cofactor specificity and their enzymatic and interaction activities. Further, ILKs regulation through gene expression, subcellular localization, and ions and ion transporters is reviewed in the context of recent studies. Finally, using evidence from literature and interactomics databanks, we infer ILKs-dependent cellular pathways and highlight their potential in transmitting multiple types of signals originating at the interface between the cell wall and plasma membrane.

Keywords: calcium; integrin-linked kinases; manganese; plant abiotic response; plant immune response; potassium; transporters.

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Figures

FIGURE 1
FIGURE 1
Structural features of the Arabidopsis ILKs. (A) Diagrams of the full-length primary protein sequences of the Arabidopsis ILKs containing motifs predicted using the ELM database of eukaryotic linear motifs. (B) Predicted 3D structures of ILKs ankyrin repeats using PHYRE2. Images are colored by rainbow N → C-terminus. (C) Superimposed ILKs’ 3D structures. The structures are colored to represent the succession of secondary structure elements (N-terminal/blue to C-terminal/red). The structural superposition of the PHYRE2 predicted 3D structures and alignments were performed using the ‘Iterative fit’ function of the Swiss-PDB Viewer 4.1.0. (Guex and Peitsch, 1997). (D) The alignment displays the amino acid sequence in each ILK. ‘∗/.’ indicate identical/similar residues. The predicted secondary structure is displayed below the alignment (h: α-helices, s: strands). The ankyrin repeats (ARs) are shown below and highlighted on the secondary structure alignment.
FIGURE 2
FIGURE 2
The evolution of ILKs kinase domains in plants. (A) Phylogenetic tree of Arabidopsis RAF kinases; the ILK clade is shown in red. (B) Alignment of kinase subdomains of the Arabidopsis ILKs showing conservation of residues in the G-loop, catalytic Lys, C-loop and the A-loop. In both B and D, the eukaryotic consensus of each kinase subdomain is shown for comparison. Conserved residues are shaded. (C) Phylogenetic tree of plant ILK1-like kinases; the AtILK is shown in red. ILK1 orthologs were identified in the NCBI database using BLAST; accessions with the highest score from each plant were selected. (D) Alignment of kinase subdomains shown in C. For C and D, full binominal names are as follows: HS (Homo sapiens), DM (Drosophila melanogaster), AT (Arabidopsis thaliana), BN (Brassica napus), BO (B. oleracea var. oleracea), MT (Medicago truncatula), GM (Glycine max), PV (Phaseolus vulgaris), SL (Solanum lycopersicum), ST (S. tuberosum), GR (Gossypium raimondii), OS (Oryza sativa Japonica Group), BD (Brachypodium distachyon), ZM (Zea mays), SI (Setaria indica), PD (Pinus radiata), TB (Taxus baccata), GB (Ginkgo biloba), WM (Welwitschia mirabilis), CM (Cycas micholitzii), LD (Lycopodium deuterodensum), Sse (Selaginella selaginoides), CR (Chlamydomonas reinhardtii), OT (Ostreococcus tauri), VC (Volvox carteri f. nagariensis). The alignments were performed using Clustal Omega; the phylogenetic trees were constructed and visualized using the iTOL Interactive Tree of Life. Protein sequences were obtained from the NCBI (http://www.ncbi.nlm.nih.gov/) or the 1000 Plants (OneKP). Red residues in (B) and (D) are known to be important for catalytic activity in eukaryotic kinases.
FIGURE 3
FIGURE 3
PAMP and DAMP perception is mediated by ILK1 signaling. For flg22 and pep1 treatments, Arabidopsis Col-0 and ilk1-1 seedlings were germinated on MS basal salt mixture supplemented with 2.5 mM MES, 0.9% agar, and 1% sucrose, at 22°C with a long-day (16 h light/8 h dark) photoperiod. For elf18 treatment, seeds were germinated on MS basal salt mixture supplemented with 0.6% agar, 3% sucrose, at 22°C under short-day (8 h light/16 h dark) photoperiod. Five-day (for flg22 and pep1) or seven-day-old (for elf18) seedlings were transferred to liquid MS ±1 μM peptide. The effect of treatment on root growth was analyzed at 10 days post-treatment and visualized in the box plots. Center lines show the medians, box limits indicate the 25th and 75th percentiles, whiskers extend to 5th and 95th percentiles, outliers are represented by dots, and crosses represent sample means. From left to right, n = 183, 197, 69, 64, 61, 46, 319, 331, 106, 105 sample points. ‘∗’ symbols represent statistical significance (p ≤ 0.01).
FIGURE 4
FIGURE 4
ILKs integrate Ca2+- and receptor-mediated signaling in the plant immune response. (A) Nodes represent proteins and edges represent experimentally verified interactions (solid line). The arrangement of nodes is based on the classical a tiered organization of signal transduction cascades; postulated plant integrin-like receptors and plasma membrane receptors are placed in the upper tier, followed by transporters, ILKs, Ca2+-regulated proteins, and phospho-site interacting 14-3-3 proteins. The network was constructed using the information in the Biogrid database and visualized using Cytoscape 3.2.1. (B) Proposed model of ILKs’ roles in signal transduction; the arrows show the known (continuous lines) or postulated (broken lines) direction of signal transduction. Plant or pathogen-derived signals reach the plant cell and activate several signal-processing pathways. (1) Plant Integrin-like receptors sense shifts in the composition and mechanical tension of the cell wall and plasma membrane; ILKs are possible transducers of signals from these receptors, through modulation of transporter activity. (2) Membrane receptor-like kinases (RLKs) bind specific ligands to recruit and activate cytosolic proteins (RLCKs); downstream MAP kinase module transmits the signal to effector proteins located in diverse cellular compartments. (3) Rapid calcium fluxes triggered by stimuli, increase Ca2+ concentration in the cytosol and activate Ca2+ sensors. ILKs bridge ion- and receptor-mediated signaling pathways. ILKs participate in pathways activated by PAMP and DAMP receptors, and their activity may be modulated by Ca2+ sensors (such as calmodulins). Concerted activation of these pathways results in immediate physiological changes, including the depolarization of the PM, turgor pressure, and induction of the transcriptome program. The plant response to pathogen attack encompasses both the activation of the immune system (defense program), as well as appropriate modifications in the plant growth. Continuous lines represent events for which experimental evidence exists, while broken lines depict proposed pathways.
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