Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life

Abstract

Invasive cell growth and migration is usually considered a specifically metazoan phenomenon. However, common features and mechanisms of cytoskeletal rearrangements, membrane trafficking and signalling processes contribute to cellular invasiveness in organisms as diverse as metazoans and plants – two eukaryotic realms genealogically connected only through the last common eukaryotic ancestor (LECA). By comparing current understanding of cell invasiveness in model cell types of both metazoan and plant origin (invadopodia of transformed metazoan cells, neurites, pollen tubes and root hairs), we document that invasive cell behavior in both lineages depends on similar mechanisms. While some superficially analogous processes may have arisen independently by convergent evolution (e.g. secretion of substrate- or tissue-macerating enzymes by both animal and plant cells), at the heart of cell invasion is an evolutionarily conserved machinery of cellular polarization and oriented cell mobilization, involving the actin cytoskeleton and the secretory pathway. Its central components - small GTPases (in particular RHO, but also ARF and Rab), their specialized effectors, actin and associated proteins, the exocyst complex essential for polarized secretion, or components of the phospholipid- and redox- based signalling circuits (inositol-phospholipid kinases/PIP2, NADPH oxidases) are aparently homologous among plants and metazoans, indicating that they were present already in LECA.Reviewer: This article was reviewed by Arcady Mushegian, Valerian Dolja and Purificacion Lopez-Garcia.

Live‐cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p‐derived biosensor

“…In addition to pollen tubes, tip growth can be found also in other evolutionary distinct cell types such as root hairs, neuronal cells or fungal hyphae. All of these cells share conserved modules that are involved in the establishment and maintenance of tip growth, in particular small ROP (Rho Of Plants) and Rab GTPases, actin cytoskeleton, ion gradients, calcium‐dependent protein kinases, reactive oxygen species and vesicle tethering complexes such as the exocyst (Cole & Fowler, ; Žárský & Potocký, ; Vaškovičová et al ., ). Signaling lipids could be also considered as such tip‐growth related conserved regulatory molecules.…”

Analysis of Exocyst Subunit EXO70 Family Reveals Distinct Membrane Polar Domains in Tobacco Pollen Tubes

“…One of the key components regulating cell polarity is the exocyst complex. It is a heterooctameric protein complex (TerBush et al, 1996) that is shared across eukaryotes (Vaškovi cová et al, 2013;Martin-Urdiroz et al, 2016) and that tethers secretory vesicles to the plasma membrane (PM) and regulates their subsequent fusion. In animal and yeast model systems, many molecular interactions involved in exocyst function have already been discovered: EXO70 and SEC3 drive exocyst to the target site by interaction with phosphatidylinositol 4,5-bisphosphate (PIP 2 ) and small GTPases of the Rho family (He et al, 2007;Liu et al, 2007;Wu et al, 2010;Pleskot et al, 2015), both budding yeast (Saccharomyces cerevisiae) Sec15p (France et al, 2006) and Exo70p interact with the cell polarity determinant Bem1p (Liu and Novick, 2014), SEC15 interacts with secretory vesicle-associated Rab GTPases (Wu et al, 2005) and promotes myosin motor release after vesicle fusion with the PM (Donovan and Bretscher, 2015), and budding yeast Sec6p binds SNARE proteins and promotes SNARE complex assembly (Dubuke et al, 2015) and also binds the SNARE interactor Sec1p (Morgera et al, 2012).…”

Formins and membranes: anchoring cortical actin to the cell wall and beyond

“…Detailed discussion of the RHO-controlled, actin nucleation or actin-microtubule co-ordination-based cortical processes in non-plant lineages, including formation of invasive structures such as e.g., metazoan filopodia, would be out of scope of this review, and can be found elsewhere (e.g., Chesarone et al, 2010; Yang and Svitkina, 2011; Vaškovičová et al, 2013). What follows is a summary of biological implications of the formin-membrane interactions discussed in the previous section.…”

“…Formins (FH2 proteins) are a large family of evolutionarily conserved proteins sharing the well-defined FH2 domain (cd smart00498, pfam02181), originally identified in metazoans and fungi and later found to be ubiquitous among eukaryotes (Higgs, 2005; Higgs and Peterson, 2005; Chalkia et al, 2008; Grunt et al, 2008) and thus apparently dating back to the last eukaryotic common ancestor (see Vaškovičová et al, 2013). Land plants have three formin subfamilies, termed Class I, II and III (Deeks et al, 2002; Grunt et al, 2008), with only two of them (Class I and Class II) present in the angiosperms, and the third clade (Class III) found in mosses and lycophytes.…”