Evolutionary Adaptations of Plant AGC Kinases: From Light Signaling to Cell Polarity Regulation

Abstract

Signaling and trafficking over membranes involves a plethora of transmembrane proteins that control the flow of compounds or relay specific signaling events. Next to external cues, internal stimuli can modify the activity or abundance of these proteins at the plasma membrane (PM). One such regulatory mechanism is protein phosphorylation by membrane-associated kinases, several of which are AGC kinases. The AGC kinase family is one of seven kinase families that are conserved in all eukaryotic genomes. In plants evolutionary adaptations introduced specific structural changes within the AGC kinases that most likely allow modulation of kinase activity by external stimuli (e.g., light). Starting from the well-defined structural basis common to all AGC kinases we review the current knowledge on the structure-function relationship in plant AGC kinases. Nine of the 39 Arabidopsis AGC kinases have now been shown to be involved in the regulation of auxin transport. In particular, AGC kinase-mediated phosphorylation of the auxin transporters ABCB1 and ABCB19 has been shown to regulate their activity, while auxin transporters of the PIN family are located to different positions at the PM depending on their phosphorylation status, which is a result of counteracting AGC kinase and PP6 phosphatase activities. We therefore focus on regulation of AGC kinase activity in this context. Identified structural adaptations of the involved AGC kinases may provide new insight into AGC kinase functionality and demonstrate their position as central hubs in the cellular network controlling plant development and growth.

Receptor-like cytoplasmic kinase MARIS functions downstream of Cr RLK1L-dependent signaling during tip growth

“…Whether CrRLK1Ls, NADPH oxidases, OXI1/ AGC2 kinases, and MRI/Pti1-like proteins are all part of a linear pathway or, more likely, belong to different pathways that orchestrate complex cross-talk to sustain cell growth remains to be addressed. In this regard, the presence of a module composed of OXI/AGC2 kinases and MRI/Pti1-like RLCKs acting downstream of the CrRLK1Ls and NADPH oxidases could potentially allow the integration of inputs generated by biotic or abiotic stresses with the CW integrity pathway (36,37). Interestingly, in all the different genetic backgrounds tested, MRI R240C is more efficient than the WT form in activating downstream responses.…”

“…Because OXI1 also is involved in root-hair growth and can phosphorylate different members of the RLCK-VIII subfamily, OXI1 is likely to activate MRI during root-hair growth. In PTs, however, OXI1 expression levels are very low, and it seems more likely that either another member of this family, the AGC2 kinases (group VIII), or a combination of them fulfills this role (Table S5) (35)(36)(37). Whether CrRLK1Ls, NADPH oxidases, OXI1/ AGC2 kinases, and MRI/Pti1-like proteins are all part of a linear pathway or, more likely, belong to different pathways that orchestrate complex cross-talk to sustain cell growth remains to be addressed.…”

Inactivation of Plasma Membrane–Localized CDPK-RELATED KINASE5 Decelerates PIN2 Exocytosis and Root Gravitropic Response inArabidopsis

“…In addition to a potential role facilitating outer lateral targeting of some membrane transporters, CRK5 could also play a role in recycling proteins from the outer lateral membranes and thereby contribute to their targeting to the BFA-sensitive membrane recycling pathway. As polar localization of PIN proteins appears to be mediated though nonpolar secretion followed by their internalization and recycling-dependent polarization (Dhonukshe et al, 2008), current models propose that sequential phosphorylation of hydrophilic T-loops of PINs by AGCs and possibly other protein kinases (Zhang et al, 2010) directs their stabilization in basal membranes and subsequent apical transcytosis (Rademacher and Offringa, 2012;Löfke et al, 2013). As most evidence supporting these models is derived from the analysis of polar localization of PIN1 and PIN2 in vertically grown and gravistimulated roots, in this work, we examined in detail how inactivation of CRK5 affects the root gravitropic response.…”

“…Emerging data indicate that cortical actin accumulation regulates clathrin-dependent endocytosis Nagawa et al, 2012), whereas enhanced inositol triphosphate and Ca 2+ levels decelerate exocytosis of PIN1 and PIN2 similarly to mutations of inositol polyphosphate 1-phosphatase and phosphatidylinositol monophosphate 5-kinase genes (Zhang et al, 2011;Mei et al, 2012). Furthermore, signaling through the 3-phosphoinositidedependent kinase1 and interactions with Ca 2+ binding or calmodulinlike proteins appear to regulate the activity of AGC kinases that phosphorylate central hydrophilic loops of PINs, as well as ABCB/ PGPs (Benjamins et al, 2003;Zegzouti et al, 2006;Henrichs et al, 2012;Rademacher and Offringa, 2012).…”

Signals fly when kinases meet Rho-of-plants (ROP) small G-proteins

“…The AKT-mediated inhibition of Rac1 is exerted through the decreased GTP-binding ability of the phosphorylated G-protein [78]. AKT belongs to the large AGC kinase family that is also present in plants [79]. AGC kinases are implicated in many plant development and defence pathways also involving ROP GTPases, such as root hair and pollen tube growth, auxin transport, etc.…”