Divergent Roles for Maize PAN1 and PAN2 Receptor-Like Proteins in Cytokinesis and Cell Morphogenesis

Abstract

Pangloss1 (PAN1) and PAN2 are leucine-rich repeat receptor-like proteins that function cooperatively to polarize the divisions of subsidiary mother cells (SMCs) during stomatal development in maize (Zea mays). PANs colocalize in SMCs, and both PAN1 and PAN2 promote polarization of the actin cytoskeleton and nuclei in these cells. Here, we show that PAN1 and PAN2 have additional functions that are unequal or divergent. PAN1, but not PAN2, is localized to cell plates in all classes of dividing cells examined. pan1 mutants exhibited no defects in cell plate formation or in the recruitment or removal of a variety of cell plate components; thus, they did not demonstrate a function for PAN1 in cytokinesis. PAN2, in turn, plays a greater role than PAN1 in directing patterns of postmitotic cell expansion that determine the shapes of mature stomatal subsidiary cells and interstomatal cells. Localization studies indicate that PAN2 impacts subsidiary cell shape indirectly by stimulating localized cortical actin accumulation and polarized growth in interstomatal cells. Localization of PAN1, Rho of Plants2, and PIN1a suggests that PAN2-dependent cell shape changes do not involve any of these proteins, indicating that PAN2 function is linked to actin polymerization by a different mechanism in interstomatal cells compared with SMCs. Together, these results demonstrate that PAN1 and PAN2 are not dedicated to SMC polarization but instead play broader roles in plant development. We speculate that PANs may function in all contexts to regulate polarized membrane trafficking either directly or indirectly via their influence on actin polymerization.Leucine-rich repeat (LRR)-receptor-like kinases (RLKs) regulate many aspects of plant development and physiology. While few ligands have been definitively identified, the general view of the function of these proteins is that interaction of ligand(s) with the LRRcontaining extracellular domains regulates the activity of the intracellular kinase domains, triggering downstream cellular responses. While the kinase domains of many such receptor-like proteins appear to be catalytically inactive (an estimated approximately 20% of all Arabidopsis [Arabidopsis thaliana] RLKs, based on bioinformatics analyses; Castells and Casacuberta, 2007), many such "pseudokinases" nevertheless participate in signal transduction via interaction with active kinases (other LRR-RLKs or cytoplasmic kinases; Llompart et al., 2003;Boudeau et al., 2006;Rajakulendran and Sicheri, 2010).We previously identified a pair of LRR-RLKs in maize (Zea mays), Pangloss1 (PAN1) and PAN2, which function cooperatively to polarize the asymmetric divisions of subsidiary mother cells (SMCs) during stomatal development (Cartwright et al., 2009;Zhang et al., 2012).

Neuronal apoptosis inhibitory protein (NAIP) localizes to the cytokinetic machinery during cell division

“…Interestingly, in fission yeast53 and in the slime mold Dictyostelium discoidea 54, LRR containing proteins have been associated with cytokinesis. Similarly, plant LRR proteins have been linked to cytokinesis as well55565758.…”

Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes

“…Polar localization of this complex is a prerequisite for recruitment of receptor-like kinases (RLKs) PAN2 and PAN1, both polarly localized at the end of SMC proximal to GMC (Cartwright et al 2009;Zhang et al 2012). Afterwards, Rho-GTPases of plants (ROPs) are recruited to the polar SMC site (Humphries et al 2011;Sutimantanapi et al 2014;Facette et al 2015). Besides, phospholipases C and D are necessary for the perception or the transduction of the stimulus emitted by the GMCs (Apostolakos et al 2008), whereas auxin stimulation is accomplished by the catalytic activity of phosphatidylinositol-3-kinase (PI3K; Livanos et al 2015).…”

Auxin as an inducer of asymmetrical division generating the subsidiary cells in stomatal complexes ofZea mays

“…55,56 Considering that PAN1 and ROPs cooperate on positioning SMC nucleus and that in pan1 mutants AF-patches were absent, 54,55 it may be suggested that PAN1 may generally interfere with cortical AF-organization. This protein also accumulates at definite regions of subsidiary cells and intervening cells of stomatal rows of Z. mays, 57,58 where distinct AF accumulations have also been found. 34,58 Thus, the AF-patches at the polar end of Z. mays SMCs, should not be considered as prime polarizing factors, since they are absent from SMCs in other grasses like Triticum turgidum, but they may be related to the local SMC bulging toward the inducing GMC.…”

“…This protein also accumulates at definite regions of subsidiary cells and intervening cells of stomatal rows of Z. mays, 57,58 where distinct AF accumulations have also been found. 34,58 Thus, the AF-patches at the polar end of Z. mays SMCs, should not be considered as prime polarizing factors, since they are absent from SMCs in other grasses like Triticum turgidum, but they may be related to the local SMC bulging toward the inducing GMC. 12,34 Evidence favoring this hypothesis is that in TIBA-and LY294002-treated SMCs, where the polar nucleus migration and the asymmetrical division were inhibited, AF-patches were assembled.…”