The tip of the iceberg: ROP2 directly interacts with SYP121 to regulate root-hair polarization, elongation, and exocytosis

RICARDI, MARTINIANO M.; ESTEVEZ, JOSÉ M.

MOLECULAR PLANT

OXFORD UNIV PRESS

Año: 2022 vol. 15 p. 1084 - 1086

1674-2052

Root hairs (RHs) grow in a polar manner ascylindrical protrusions from the root epidermis. They significantly expand theroot volume in the rhizosphere to search for water and nutrients, anchor theplant, and promote interactions with several kinds of microorganisms in thesoil. Trichoblasts, the epidermis cell type responsible for RH development,switch from anisotropic cell elongation to tip growth through polarization ofthe growth machinery to a predefined RH initiation domain (RHID) at the plasmamembrane. The first step known in RH initiation is the recruitment of guaninenucleotide exchange factors (GEFs) to the RHID, specifically GEF3 and GEF4 (andto a lesser extent, also GEF12 and GEF14), being that GEF3 is the earliestknown landmark to the RHID and that GEF4 is involved in the downstreamactivation of RH growth during bulging (Denningeret al., 2019) (Figure 1). GEFs areable to interact with plasma membrane-bound receptor-like kinases such asFERONIA (FER) (Duan et al., 2010). Oncelocalized to the RHID, the GEFs recruit the RHO-like GTPase from plants (ROPs)required from the earliest stages of polar growth. ROPs are regulated in timeand space by GEFs by controlling the GTP-/GDP-dependent activation/inactivationcycles that facilitate the release of GDP. On the other hand, GAPs enhance GTPhydrolysis and GDP dissociation inhibitors that recycle ROPs to and from theplasma membrane. ROPs bind plasma membranes through post-translational lipidmodifications and interaction with membrane lipids (Feiguelmanet al., 2018). In addition, all ROPs possess in their carboxy-terminaltail a polybasic region, which interacts with anionic phospholipids likePI(4,5)P2, highly enriched in the plasma membrane (Hirano et al., 2018), and also, vesicle-mediatedROP targeting may occur. In RH, FER-GEFs-ROP2 are able to control RH growth bycontrolling ROS production (Duan et al., 2010).ROP2 is one of the main ROPs responsible for the early polarization in RHs.Together with ROP2, ROP4 and ROP6 are also important for RH polar growth at theinitial stage of tip polarization in the epidermal cells as well as fortip-cell elongation (Denninger et al., 2019).In addition, several proteins such as PIP5K3 (that produces PI(4,5)P2))and root hair defective 2 (RHD2), a NADPH oxidase C (that produces ROS) haveboth been shown to directly interact with ROPs during tip-growth regulation (Wong et al., 2007) and modulate vesicle traffic tothe plasma membrane and cell-wall assembly, respectively.Actively fast polar growing cells like RHs dependon active vesicle trafficking that involves vesicle tethering (via tetheringcomplexes), docking, and fusion (via trans- Soluble N-ethylmaleimide-sensitivefactor attachment protein receptors Q [SNARE] complex andN-ethylmaleimide-sensitive factors) of vesicles with target membranes. SNAREsSYP123 and SYP132 (both SYP121 homologs) coordinately mediated tip-focusedvesicle trafficking for RH elongation by forming complexes withvesicle-membrane-localized R-SNARE VAMP721/722/724 (Ichikawaet al., 2014). Cui et al. (2022) recentlyreported in Molecular Plant that active ROP2 promotes SYP121 accumulationduring RH elongation by a physical interaction and confirms the previouslysuspected relevance of SYP121 in the process (Ichikawaet al., 2014) (Figure 1). Inaddition, ROP2 promotes the interaction between SYP121 and the R-SNARE VAMP722to form a SNARE complex, possibly by counteracting with the SEC1/MUNC18 proteinSEC11, which suppresses SYP121’s function. The authors demonstrate all thisusing classical genetic tools like mutant crosses and over-expressing lines andshowing very solid interaction data. The mild phenotype observed raises somequestions of whether SYP123 or SYP132 might also interact with ROP2. Inaddition, numerous environmental signals such as nutrient availability, changesin temperature, or microbial partners that impact RH development may enhance ortrigger ROP’s activation and modulate SYP-VAMP interactions. In this direction,recently, it was shown that a mutant of FER (fer-8) with reduced ROS levels orplants treated with RALF23 peptide (as ligand of FER) that inactivates theFER-ROP2 related pathway including ROS production were both able to enrichbeneficial Pseudomonas in the complex rhizosphere microbiome (Song et al., 2021). This exemplifies how tightlyinterlinked is the interface between cell surface in the root cells and thesoil environment including the microbiome.Plants have greatly expanded their SNARE proteinfamilies when compared with other species (Sanderfoot2007), and there is an active discussion on their degree of redundancyand specialization. For instance, SYP121 and SYP122 seem to have strongredundancy from a general point of view but are also somehow divergent in theircargo specificity (Waghmare et al., 2018).The same goes for the R-SNAREs VAMP721 and VAMP722, which have a higher degreeof redundancy to the point that both, VAMP721 or VAMP722, can rescue thedouble-mutant phenotype (which is seedling lethality) (Kwonet al., 2008). Future studies with both, VAMP721 and SYP122, with ROP2could enrich this discussion on general versus specialized secretion of thesehighly similar proteins. In addition, since there are at least three ROPsclearly involved in RH initiation and tip-growth process, this opens thequestion if there is any type of specificity in the interaction between ROP2and Could ROP2–SYP121 direct interaction lead to thediscovery of another control point in plant secretion? Is this mechanismspecific for RH polarized growth or could it become true for other types ofelongating cells such as anisotropic growing cells (e.g., roots, hypocotyl,etc.), isotropic (e.g., meristems), hybrid growing cells (e.g., epidermis inleaves and cotyledons), etc.? Could this be revealed as a general mechanism forexocytosis regulation by ROP2 or similar proteins? What about the regulation ofother specialized secretion events like the response to pathogens orpollen-tube growth? Will the RH tips become the tip of the iceberg? Only futurediscoveries will tell. One of the major future challenges in understanding cellpolarity in plant cells, and specifically in roots, will be to elucidate howcell elongation, polarization, and exocytosis are coordinated withenvironmental signals in the soil.