- Email: [email protected]
Patellin protein family functions in plant development and stress response
Journal of Plant Physiology 234–235 (2019) 94–97
Contents lists available at ScienceDirect
Journal of Plant Physiology journal homepage: www.elsevier.com/locate/jplph
Review article
Patellin protein family functions in plant development and stress response a,⁎
a
a
a
b
Huapeng Zhou , Hongqin Duan , Yunhong Liu , Xia Sun , Jinfeng Zhao , Honghui Lin a b
a,⁎
T
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610064, China National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Patellin Sec14 protein PITP Membrane trafficking Plant development and stress tolerance Arabidopsis
The plant patellin (PATL) proteins are yeast Sec14 protein (Sec14p)-like phosphatidylinositol transfer proteins (PITPs), which are widely distributed across the plant kingdom. The model plant Arabidopsis has six PATL members (designated as PATL1-PATL6). Accumulated evidence has indicated the involvement of Arabidopsis PATLs in various biological processes. This mini-review briefly summarizes our current knowledge on individual PATLs regarding their roles in plant development and stress tolerance regulation. The elucidation of PATLs’ biological function in plants will provide new insights on plant membrane trafficking and its regulatory roles in either plant growth or environmental stress response signaling networks.
1. Sec14p-like phosphatidylinositol transfer proteins in plants Phosphatidylinositols (PtdIns) presented in eukaryotic membranes can both serve as scaffold lipids and precursors of other lipids or soluble second messengers, implying an essential role of PtdIns as important signaling molecules in plant stress responses and developmental adaptation (Huang et al., 2016). For instance, phosphoinositides have been reported to play a regulatory role in the activity of ion channels (Hilgemann et al., 2001). PtdIns transfer proteins (PITPs) are able to transfer PtdIns or phosphatidylcholine (PtdCho) between membranes to stimulate a variety of signaling pathways including Ca2+-triggered exocytosis as well as vesicle budding at the trans-Golgi network (TGN) (Aikten et al., 1990; Hay and Martin, 1993; Simon et al., 1998). Importantly, PITPs are likely implicated in regulating PtdIns kinase activities, possibly through a mechanism of “presentation”, which helps PtdIns 4-OH kinases to overcome their inability to effectively engage membrane-embedded PtdIns substrates (Schaaf et al., 2008; Bankaitis et al., 2010). Thus, PITPs are essential for phosphoinositide metabolism and signal transduction. Yeast Sec14 protein (Sec14p) is the founding member of PITP family, and it was identified using the temperaturesensitive sec14-1ts mutant in yeast (Novick et al., 1980). Sec14p is required for membrane trafficking trough the TGN compartments (Bankaitis et al., 1990), and plays an essential role in yeast vitality (Cleves et al., 1991; Fang et al., 1996). In plants, a large number of Sec14p-like proteins have been characterized based on the sequence of yeast Sec14p, and the Sec14 domain of members of this protein superfamily is largely conserved and displays PtdIns and/or PtdCho transfer activities (Vincent et al., 2005; Huang et al., 2016).
⁎
Consistently, some of these plant Sec14 domain-containing proteins can complement the yeast sec14-1ts mutant in terms of lipid binding and transferring activities (De Campos and Schaaf, 2017). Specifically, about 32 Arabidopsis thaliana (Arabidopsis) Sec14p-like proteins in total are characterized (Fig. 1; Bankaitis et al., 2010; Huang et al., 2016; Tejos et al., 2018). In contrast to yeast Sec14p, the majority of these Arabidopsis Sec14p-like proteins exist in a multi-domain form: the Nterminal Sec14 domain is followed by an Nlj16-like “nodulin” (e.g., AtSfh1) or a GOLD (Golgi dynamics) domain (Bankaitis et al., 2010; Huang et al., 2016). It should be noticed that there also exist numerous free-standing Sec14p-like proteins. Phylogenetically, one cluster of Arabidopsis Sec14p-like proteins is then designated as PITPs, and it has greatly expanded in number and diversified in function (Huang et al., 2016; Tejos et al., 2018). Recently, several excellent reviews concerning Sec14p-like proteins and PITPs in plants have been published (Huang et al., 2016; De Campos and Schaaf, 2017), and we refer the interested readers to them for more information. 2. The patellin protein family in plants Arabidopsis patellin proteins (PATL, derived from a Latin word “patella” which means small plate) are typical Sec14-GOLD proteins and belong to the PITP family (Fig. 2; Peterman et al., 2004; Tejos et al., 2018). Considering the fact that PATLs firstly appear in gymnosperm, they might have been added to the plant repertoire rather late during evolution (Huang et al., 2016). Structurally, the PATL protein family is characterized by two conserved domains universally observed in other membrane trafficking-related proteins: a Sec14p-like lipid-binding
Corresponding authors at: College of Life Sciences, Sichuan University, Chengdu 610064, China. E-mail addresses: [email protected] (H. Zhou), [email protected] (H. Lin).
https://doi.org/10.1016/j.jplph.2019.01.012 Received 1 November 2018; Received in revised form 21 January 2019; Accepted 22 January 2019 Available online 24 January 2019 0176-1617/ © 2019 Elsevier GmbH. All rights reserved.
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
trafficking processes for cell plate biogenesis. Thus, PATL family members are putative regulators of membrane trafficking in plants. Phylogenetic analysis has identified 44 PATL sequences (PATL1like) in the plant kingdom, ranging from angiosperm species to gymnosperm species (Peterman et al., 2006). It has also been demonstrated that plant PATL-like proteins can be classified into four distinct clades, and specific residues in the GOLD domain are unique to each clade, implying a subgroup-specific and functional amino acid substitution for PATL (Peterman et al., 2006). This diversification might represent a particular biological function of each PATL subfamily in Arabidopsis. The C-terminus of GOLD domain in PATLs is Lys-rich, and possesses a conserved motif that is similar to the PtdIns(4,5)P2-binding motif in many other membrane trafficking-related proteins (Peterman et al., 2004). Arabidopsis PATL proteins also contain a variable domain in their N-terminus differing in both length and amino acid composition (Peterman et al., 2004, 2006). Importantly, there exists a PXXP motif which might play a role in cytoskeletal dynamics as well as membrane trafficking in the variable domain. A coiled-coil motif for protein-protein interaction is also observed in PATL proteins (Fig. 2; Peterman et al., 2004). The Arabidopsis PATLs are associated with the membrane system. The strong location to the cell plate during cytokinesis is probably common to all PATL protein family members in Arabidopsis (Peterman et al., 2004; Tejos et al., 2018). For instance, Arabidopsis PATL1 is a peripheral membrane protein, although it also partly locates in the cytoplasmic pool. It is found to be distributed across the cell plate but not concentrated at the site of new trafficking vesicle additions. However, it is distributed in the region where the plate is to undergo maturation (Peterman et al., 2004). The subcellular location pattern of Arabidopsis PATL2 is similar to that of PATL1. PATL2 is concentrated at the cell plate during cytokinesis and temporarily retained at the division plane even after the maturation of cell plates (Suzuki et al., 2016; Tejos et al., 2018). Arabidopsis PATLs are expressed in distinct but partly overlapping patterns. They are ubiquitously expressed in diverse organs and at all stages of embryogenesis. For example, PATL1 is expressed in the whole root apical meristem (RAM) and in stele cells in the distal zone of the RAM (Tejos et al., 2018). PATL2 partially resembles PATL1 in the expression pattern, however, it is also observed in pericycle cells in the root elongation zone and might be involved in LRP and vascular development (Tejos et al., 2018). PATL3 is more prominent in external cell layers, while PATL4 is ubiquitously expressed in the whole RAM. Interestingly, both PATL3 and PATL4 are expressed in the basal meristem of the root tip and the lateral root primordia (LRP) (Tejos et al., 2018). The distinct but partly overlapping expression patterns might represent complementary and diversified functions of PATLs in Arabidopsis.
Fig. 1. Phylogenetic tree of Sec14p-like proteins in Arabidopsis. Phylogenetic analysis was performed using the web-based tool freely available at http://www.phylogeny.fr, and the nucleotide sequences of the Sec14 lipidbinding domain of these 32 Arabidopsis Sec14p-like proteins were analyzed. Red box indicates the PATL subfamily in Arabidopsis.
3. PATLs bind phospholipids and function in diverse signaling pathways in plants
Fig. 2. Schematic diagram of the Arabidopsis PATLs protein motifs. A Sec14p-like domain is found in tandem with a GOLD domain, whereas a variable domain if in the N-terminus of each Arabidopsis PATL. Black line box, variable N-terminal domain; green line box, Sec14p-like domain; purple line box, Golgi dynamics domain (GOLD); filled gray box, coiled-coil region; vertical lines, PXXP motif.
Given the fact that a Sec14 phospholipid-binding domain and a Lysrich motif are presented in PATLs, they probably possess the ability to interact with phospholipids (Peterman et al., 2004, 2006). In a test for the ability of PATL1 to bind to unilamellar membrane vesicles composed of PtdIns, PtdCho, or phosphatidylethanolamine (PtdEth), the majority of PATL1 binds vesicles made of PtdIns (Peterman et al., 2004). In contrast, it has a low affinity to PtdIns(4)P and PtdIns(3,5)P2, and no binding to PtdIns(3,4)P2 (Peterman et al., 2004). In comparison to PATL1, however, Arabidopsis PATL2 binds to all the seven phosphorylated forms of PtdIns. Its binding affinity to monophosphorylated PtdIns is at the highest level, while for PtdIns(3,4,5)P3 is at the lowest level (Suzuki et al., 2016). PATL3 has been found to bind PtdIns(4,5)P2 and PtdIns(4)P. However, there exists no interaction between PATL3 and two other negatively charged phospholipids, PtdIns(3)P and phosphatidic acid (PA) (Wu et al., 2017). Since many of these PtdIns phosphorylated derivatives have been implicated in various cellular
domain and a GOLD following the N-terminal variable domain (Fig. 1; Peterman et al., 2004). The GOLD domain is widely found in a group of proteins related to Golgi function, membrane homeostasis, as well as vesicle trafficking (Anantharaman and Aravind, 2002; Peterman et al., 2004). The cell-plate localization of PATL1, the defining member of the PATL protein family, suggests a regulatory role during cytokinesis in plant cells, although the underlying mechanism remains to be elucidated (Peterman et al., 2004). It is speculated that Arabidopsis PATL1 more likely participates in clathrin-dependent endocytosis that aids cell plate remodeling and completion, rather than in the early membrane
95
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
Arabidopsis except for PATL5 could interact with EXO70A1 (Wu et al., 2017). It is possible that EXO70A1 plays a pivotal role in PATLs localization to diverse membrane systems in an exocyst-independent manner. Interestingly, two members of Arabidopsis PATL family, PATL3 and PATL6, interact with Alfalfa mosaic virus (AMV) movement protein (MP), suggesting a possible role of PATLs in viral movement regulation (Peiro et al., 2014). In fact, MPs encoded by plant viruses including AMV could interact with plant host proteins to alter viral movement (Bol, 2003; Boevink and Oparka, 2005; Taliansky et al., 2008; Hong and Ju, 2017). A well-established mechanism is related to plasmadesmata (PD) channels (Kumar et al., 2015; Hong and Ju, 2017). Subcellular localization analysis revealed that either Arabidopsis PATL3 or PATL6 could diminish viral movement by interfering with AMV MP targeting to PD. Consistently, transient overexpression of both proteins resulted in attenuated virus infection, whereas viral RNA accumulation was elevated in PATL3 and PATL6 knockout mutant. Unpredictably, PATL3 and PATL6 themselves cannot target to PD without AMV infection, indicating a virus-induced localization pattern of these PATLs (Peiro et al., 2014). Therefore, PATL3 and 6 might function as a defensive barrier of AMV virus in plants.
signaling networks (Munnik et al., 1998; Anderson et al., 1999), it is possible that PATL1 functions in plant development and stress responses at least in part through binding to such specific phosphoinositides. An increasing number of studies have characterized Arabidopsis PATLs as putative regulators implicated in diverse signaling pathways (Deng et al., 2007; Hsu et al., 2009; Kiba et al., 2012; Peiro et al., 2014; Zhou et al., 2018). For instance, Arabidopsis PATL protein family members have been reported to function as possible candidates of regulators in auxin signaling and PIN distribution (Tejos et al., 2018). PATLs are auxin-regulated target genes, and the Arabidopsis patl2 patl4 patl5 patl6 (patl2456−/−) quadruple mutant displayed obvious defects in auxin-induced PIN1 lateralization response. PATLs are also redundantly required for auxin-mediated root meristem size and gravitropic growth regulation (Tejos et al., 2018). In addition, the ectopic structures in PATLs loss-of-function mutant plants clearly suggest that PATLs play a crucial but redundant role in embryo patterning and organogenesis. Thus, PATLs might participate in the auxin feedback on PIN polarized localization in plants (Tejos et al., 2018). In Arabidopsis, several PATL1-interacting proteins have been identified, including Salt-Overly-Sensitive1 (SOS1), the major component of SOS pathway (Zhou et al., 2018), and calmodulin4 (CaM4), a multifunctional Ca2+ sensor (Chu et al., 2018), as well as associated molecule with the SH3 domain of STAM3 (AMSH3), a deubiquitinating enzyme (Isono et al., 2010). Thus, these interactors link PATL1 to diverse signaling networks. We recently found that PATL1 is implicated in ion homeostasis regulation in plants partly through SOS1 since PATL1 interacts with SOS1 in planta. Data showed that the PM Na+/H+ antiport activity was much lower in patl1 than in wide-type plant, and the membrane trafficking process might be disturbed due to PATL1 overexpression. It also participates in cellular redox homeostasis during salt stress, and artificial elimination of ROS using antioxidants partly rescues the salt-sensitive phenotype in patl1 mutant (Zhou et al., 2018). There also exists a direct interaction between PATL1 and CaM4. Loss-offunction mutants of PATL1 and CaM4 exhibit a freezing-tolerant phenotype. It is believed CaM4 negatively regulates freezing tolerance in a CBF-independent manner by interacting with PATL1 in Arabidopsis (Chu et al., 2018). In addition, PATL1 might also participate in vesicle trafficking mediated by AMSH3, possibly by directly binding and recruiting AMSH3 to the plasma membrane (PM) (Isono et al., 2010). Since AMSH3 is likely to be a regulator of autophagy in plants, PATL1 might also play a role in regulating autophagy (Katsiarimpa et al., 2013). Importantly, PATL1 can be ubiquitinated, suggesting a possible role of ubiquitination in its function (Igawa et al., 2009; Saracco et al., 2009). Arabidopsis PATL2 can be phosphorylated by mitogen-activated protein (MAP) kinse4 (MPK4), and the Ser-536 of PATL2 is the major site of phosphorylation. However, this phosphorylation has no effect on the subcellular location of PATL2. In contrast, its binding activity to phosphoinositides is significantly altered due to MPK4-mediated phosphorylation, suggesting a role of the MPK4-PATL2 cascade during cytokinesis in plants (Suzuki et al., 2016). In a functional phosphoproteomic profiling in membrane-related proteins, PATL2 is shown to be phosphorylated upon salt treatment, although this phosphorylation might not be mediated by MPK4 (Hsu et al., 2009; Suzuki et al., 2016). Thus, PATL2 probably also functions as a possible regulator of plant salt tolerance in plants. Recently, it has been reported that EXO70A1 interacts with the GOLD domain of PATL3 in Arabidopsis (Wu et al., 2017). EXO70A1 is a member of the exocyst complex which tethers trafficking vesicles at the target membrane before fusion, and has been implicated in plant cytokinesis (Fendrych et al., 2010; Wu and Guo, 2015). The localization of PATL3 to PM and cell plate is not achieved via the endocytic or secretory pathways. However, this process requires EXO70A1. Both PATL3 and EXO70A1 bind phosphoinositide, which might help attract target proteins to the membrane. In fact, all the other PATLs in
4. Concluding remarks and perspectives Up to now, the biological functions of PATL protein family members have not been well characterized. PATLs belong to Sec14p-like protein family, and function as PITPs in plants. All the PATLs possess the binding activity to phosphoinositides, although their affinity varies significantly. In addition, PATL1 might be associated with a number of interacting proteins such as SOS1, CaM4, MPK4, and AMSH3, and importantly, they might also undergo post-translational modifications (PTMs) such as ubiquitination and phosphorylation. These together imply an individually fine-tuned function of each PATL family member. In fact, PATLs are implicated in cytokinesis and their location to the cell plate and PM during cytokinesis might be assisted by specific PthIns, which could attract these PATLs and other target proteins to the membrane. It is believed that the PATL-interacting proteins probably link PATLs to diverse signaling pathways, therefore leading to integration of PATLs into distinct regulatory networks in plants. Multiple strategies should be adopted to elucidate the detailed biological functions of PATLs in plants. Thus, the identification of the possible interacting proteins or targets of specific PATL is required. Methods combined with proteomic investigation and Arabidopsis mutant screening might be used for PATLs-interacting protein determination. On the other hand, detailed subcellular localization assays should also be performed to investigate the biological functions of PATLs in membrane trafficking. Another promising direction is to determine the functional link between the PITP activity of PATLs and their roles in membrane trafficking. One important question that needs to be resolved is how PATLs are regulated. Thus, determination of possible PTMs on PATLs should be carried out. PATLs can be phosphorylated and modified with ubiquitination. Additional PTMs on PATLs might also exist and their effects on PATLs should be carefully investigated in the future. Given that membrane trafficking is involved in various aspects of signaling networks in plants and PALTs are putative membrane-trafficking proteins, it is of paramount importance to determine the regulatory roles of these Sec14p-like PITPs in plant development and stress response pathways. Although several lines of evidence have revealed that particular PATLs are linked to the plant auxin signaling network as well as salt tolerance and plant immunity against specific viruses, it is also interesting to determine whether PATLs participate in any other developmental programs and stress response signaling networks. As aforementioned, PATL1 might also play a role in regulating autophagy since AMSH3 is likely to be a regulator in autophagy in plants. Finally, the following questions are at the top list for careful 96
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
consideration based on what we know about PATLs in plants: (i) what role(s) do PATLs play in membrane trafficking-related processes (e.g. cell plate formation during cytokinesis)? (ii) what is the functional link between the PITP activity of PATLs and their regulatory roles in membrane trafficking? (iii) do there exist additional PATLs-interacting proteins that modulate their biological function and link them to diverse signaling networks? (iv) what other kind of PTMs will happen to PATLs during plant development and stress responses? And last but not the least, (v) what is the evolutionary relationship between various PATLs in the plant kingdom?
biogenesis. EMBO J . 15, 6447–6459. Fendrych, M., Synek, L., Pecenkova, T., Toupalova, H., Cole, R., Drdova, E., et al., 2010. The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22 (9), 3053–3065. Hay, J., Martin, T., 1993. Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca2+-activated secretion. Nature 366, 572–575. Hilgemann, D.W., Feng, S., Nasuhoglu, C., 2001. The complex and intriguing lives of PIP2 with ion channels and transporters. Science (STKE) re19. Hong, J., Ju, H., 2017. The Plant cellular systems for plant virus movement. Plant Pathol. J. 33 (3), 213–228. Hsu, J., Wang, L., Wang, S., Lin, C., Ho, K., Shi, F., Chang, I., 2009. Functional phosphoproteomic profiling of phosphorylation sites in membrane fractions of saltstressed Arabidopsis thaliana. Proteome Sci. 7 (1), 42. Huang, J., Ghosh, R., Bankaitis, V.A., 2016. Sec14-like phosphatidylinositol transfer proteins and the biological landscape of phosphoinositide signaling in plants. Biochim. Biophys. Acta 1861 (9), 1352–1364. Igawa, T., Fujiwara, M., Takahashi, H., Sawasaki, T., Endo, Y., Seki, M., et al., 2009. Isolation and identification of ubiquitin-related proteins from Arabidopsis seedlings. J. Exp. Bot. 60 (11), 3067–3073. Isono, E., Katsiarimpa, A., Muller, I., Anzenberger, F., Stierhof, Y., Geldner, N., et al., 2010. The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22 (6), 1826–1837. Katsiarimpa, A., Kalinowska, K., Anzenberger, F., Weis, C., Ostertag, M., Tsutsumi, C., et al., 2013. The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25 (6), 2236–2252. Kiba, A., Nakano, M., Vincent-Pope, P., Takahashi, H., Sawasaki, T., Endo, Y., et al., 2012. A novel Sec14 phospholipid transfer protein from Nicotiana benthamiana is upregulated in response to Ralstonia solanacearum infection, pathogen associated molecular patterns and effector molecules and involved in plant immunity. J. Plant Physiol. 169, 1017–1022. Kumar, D., Kumar, R., Hyun, T., Kim, J., 2015. Cell-to-cell movement of viruses via plasmodesmata. J. Plant Res. 128 (1), 37–47. Munnik, T., Irvine, R., Musgrave, A., 1998. Phospholipid signaling in plants. Biochim. Biophys. Acta 1389, 222–272. Novick, P., Field, C., Schekman, R., 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205–215. Peiro, A., Izquierdogarcia, A., Sancheznavarro, J., Pallas, V., Mulet, J., Aparicio, F., 2014. Patellins 3 and 6, two members of the plant patellin family, interact with the movement protein of Alfalfa mosaic virus and interfere with viral movement. Mol. Plant Pathol. 15 (9), 881–891. Peterman, T.K., Ohol, Y.M., Mcreynolds, L., Luna, E., 2004. Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol. 136 (2), 3080–3094. Peterman, T., Sequeira, A., Samia, J., Lunde, E., 2006. Molecular cloning and characterization of patellin1, a novel sec14-related protein, from zucchini (Cucurbita pepo). J. Plant Physiol. 163 (11), 1150–1158. Saracco, S., Hansson, M., Scalf, M., Walker, J., Smith, L.M., Vierstra, R., 2009. Tandem affinity purification and mass spectrometric analysis of ubiquitylated proteins in Arabidopsis. Plant J. 59 (2), 344–358. Schaaf, G., Ortlund, E.A., Tyeryar, K.R., Mousley, C.J., Ile, K.E., Garrett, T.A., Ren, J., Woolls, M.J., Raetz, C.R., Redinbo, M.R., Bankaitis, V.A., 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell 29 (2), 191–206. Simon, J., Morimoto, T., Bankaitis, V., Gottlieb, T., Ivanov, I., Adesnik, M., Sabatini, D., 1998. An essential role for the phosphatidylinositol transfer protein in the scission of coatomer-coated vesicles from the trans-Golgi network. Proc. Natl. Acad. Sci. U. S. A. 95, 11181–11186. Suzuki, T., Matsushima, C., Nishimura, S., Higashiyama, T., Sasabe, M., Machida, Y., 2016. Identification of phosphoinositide-binding protein patellin2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis. Plant Cell Physiol. 57 (8), 1744–1755. Taliansky, M., Torrance, L., Kalinina, N., 2008. Role of plant virus movement proteins. Methods Mol. Biol. 33–54. Tejos, R., Rodriguezfurlan, C., Adamowski, M., Sauer, M., Norambuena, L., Friml, J., 2018. Patellins are regulators of auxin-mediated PIN1 relocation and plant development in Arabidopsis thaliana. J. Cell. Sci. 131 (2), 1–10. Vincent, P., Chua, M., Nogue, F., Fairbrother, A., Mekeel, H., Xu, Y., et al., 2005. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J. Cell Biol. 168, 801–812. Wu, B., Guo, W., 2015. The exocyst at a glance. J. Cell. Sci. 128 (16), 2957–2964. Wu, C., Tan, L., Van Hooren, M., Tan, X., Liu, F., Li, Y., et al., 2017. Arabidopsis EXO70A1 recruits patellin3 to the cell membrane independent of its role as an exocyst subunit. J. Integr. Plant Biol. 59 (12), 851–865. Zhou, H., Wang, C., Tan, T., Cai, J., He, J., Lin, H., 2018. Patellin1 negatively modulates salt tolerance by regulating PM Na+/H+ antiport activity and cellular redox homeostasis in Arabidopsis. Plant Cell Physiol. 59 (8), 1630–1642.
Accession numbers Sequence data from this article can be found in the GenBank/EMBL and JGI databases under the following accession numbers: PATL1, At1g72150; PATL2, At1g22530; PATL3, At1g72160; PATL4, At1g30690; PATL5, At4g09160 and PATL6, At3g51670; SOS1, At2g01980; CaM4, At1g66410; AMSH3, At4g16144; MPK4, At4g01370; and EXO70A1, At5g03540. Author contributions All the authors contributed to discussion. H.Z. wrote the article with assistance of H.D. Y.L., X.S., and J.Z. contributed to the reference collection. H.Z. and H.D. also contributed by illustrating the artwork. H.Z. and H.L. supervised the projects. Acknowledgments We sincerely apologize to those authors not able to cite their works in this review due to space limitation. We thank Dr. Yan Guo from China Agricultural University for reading the manuscript and stimulating discussions. This work was supported by National Natural Science Foundation of China (NSFC) (Grant 31870241 and 31600201 to H.Z). All the authors declare no conflict of interest. References Aikten, J.F., van Heusden, G.P., Temkin, M., Dowhan, W, 1990. The gene encoding the phosphatidylinositol transfer protein is essential for cell growth. J. Biol. Chem. 265 (8), 4711–4717. Anantharaman, V., Aravind, L., 2002. The GOLD domain, a novel protein module involved in Golgi function and secretion. Genome Biol. 3 (5), 1–7. Anderson, R., Boronenkov, I., Doughman, S., Kunz, J., Loijens, J., 1999. Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J. Biol. Chem. 274 (15), 9907–9910. Bankaitis, V.A., Aitken, J.R., Cleves, A.E., Dowhan, W., 1990. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347, 561–562. Bankaitis, V., Mousley, C., Schaaf, G., 2010. The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem. Sci. 35, 150–160. Boevink, P., Oparka, K., 2005. Virus-host interactions during movement processes. Plant Physiol. 138 (4), 1815–1821. Bol, J., 2003. Alfalfa mosaic virus: coat protein-dependent initiation of infection. Mol. Plant Pathol. 4 (1), 1–8. Chu, M., Li, J., Zhang, J., Shen, S., Li, C., Gao, Y., et al., 2018. AtCaM4 interacts with a Sec14-like protein, PATL1, to regulate freezing tolerance in Arabidopsis in a CBFindependent manner. J. Exp. Bot. 69 (21), 5241–5253. Cleves, A.E., Mcgee, T., Bankaitis, V.A., 1991. Phospholipid transfer proteins: a biological debut. Trends Cell Biol. 1, 30–34. De Campos, M.K., Schaaf, G., 2017. The regulation of cell polarity by lipid transfer proteins of the SEC14 family. Curr. Opin. Plant Biol. 40, 158–168. Deng, Z., Zhang, X., Tang, W., Osesprieto, J., Suzuki, N., Gendron, J., et al., 2007. A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell. Proteom. 6 (12), 2058–2071. Fang, M., Kearns, B.G., Gedvilaite, A., Kagiwada, S., Kearns, M., Fung, M.K.Y., Bankaitis, V.A., 1996. Kes1p shares homology with human oxysterol binding protein and participates in a novel regulatory pathway for yeast Golgi-derived transport vesicle
97
Contents lists available at ScienceDirect
Journal of Plant Physiology journal homepage: www.elsevier.com/locate/jplph
Review article
Patellin protein family functions in plant development and stress response a,⁎
a
a
a
b
Huapeng Zhou , Hongqin Duan , Yunhong Liu , Xia Sun , Jinfeng Zhao , Honghui Lin a b
a,⁎
T
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610064, China National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Patellin Sec14 protein PITP Membrane trafficking Plant development and stress tolerance Arabidopsis
The plant patellin (PATL) proteins are yeast Sec14 protein (Sec14p)-like phosphatidylinositol transfer proteins (PITPs), which are widely distributed across the plant kingdom. The model plant Arabidopsis has six PATL members (designated as PATL1-PATL6). Accumulated evidence has indicated the involvement of Arabidopsis PATLs in various biological processes. This mini-review briefly summarizes our current knowledge on individual PATLs regarding their roles in plant development and stress tolerance regulation. The elucidation of PATLs’ biological function in plants will provide new insights on plant membrane trafficking and its regulatory roles in either plant growth or environmental stress response signaling networks.
1. Sec14p-like phosphatidylinositol transfer proteins in plants Phosphatidylinositols (PtdIns) presented in eukaryotic membranes can both serve as scaffold lipids and precursors of other lipids or soluble second messengers, implying an essential role of PtdIns as important signaling molecules in plant stress responses and developmental adaptation (Huang et al., 2016). For instance, phosphoinositides have been reported to play a regulatory role in the activity of ion channels (Hilgemann et al., 2001). PtdIns transfer proteins (PITPs) are able to transfer PtdIns or phosphatidylcholine (PtdCho) between membranes to stimulate a variety of signaling pathways including Ca2+-triggered exocytosis as well as vesicle budding at the trans-Golgi network (TGN) (Aikten et al., 1990; Hay and Martin, 1993; Simon et al., 1998). Importantly, PITPs are likely implicated in regulating PtdIns kinase activities, possibly through a mechanism of “presentation”, which helps PtdIns 4-OH kinases to overcome their inability to effectively engage membrane-embedded PtdIns substrates (Schaaf et al., 2008; Bankaitis et al., 2010). Thus, PITPs are essential for phosphoinositide metabolism and signal transduction. Yeast Sec14 protein (Sec14p) is the founding member of PITP family, and it was identified using the temperaturesensitive sec14-1ts mutant in yeast (Novick et al., 1980). Sec14p is required for membrane trafficking trough the TGN compartments (Bankaitis et al., 1990), and plays an essential role in yeast vitality (Cleves et al., 1991; Fang et al., 1996). In plants, a large number of Sec14p-like proteins have been characterized based on the sequence of yeast Sec14p, and the Sec14 domain of members of this protein superfamily is largely conserved and displays PtdIns and/or PtdCho transfer activities (Vincent et al., 2005; Huang et al., 2016).
⁎
Consistently, some of these plant Sec14 domain-containing proteins can complement the yeast sec14-1ts mutant in terms of lipid binding and transferring activities (De Campos and Schaaf, 2017). Specifically, about 32 Arabidopsis thaliana (Arabidopsis) Sec14p-like proteins in total are characterized (Fig. 1; Bankaitis et al., 2010; Huang et al., 2016; Tejos et al., 2018). In contrast to yeast Sec14p, the majority of these Arabidopsis Sec14p-like proteins exist in a multi-domain form: the Nterminal Sec14 domain is followed by an Nlj16-like “nodulin” (e.g., AtSfh1) or a GOLD (Golgi dynamics) domain (Bankaitis et al., 2010; Huang et al., 2016). It should be noticed that there also exist numerous free-standing Sec14p-like proteins. Phylogenetically, one cluster of Arabidopsis Sec14p-like proteins is then designated as PITPs, and it has greatly expanded in number and diversified in function (Huang et al., 2016; Tejos et al., 2018). Recently, several excellent reviews concerning Sec14p-like proteins and PITPs in plants have been published (Huang et al., 2016; De Campos and Schaaf, 2017), and we refer the interested readers to them for more information. 2. The patellin protein family in plants Arabidopsis patellin proteins (PATL, derived from a Latin word “patella” which means small plate) are typical Sec14-GOLD proteins and belong to the PITP family (Fig. 2; Peterman et al., 2004; Tejos et al., 2018). Considering the fact that PATLs firstly appear in gymnosperm, they might have been added to the plant repertoire rather late during evolution (Huang et al., 2016). Structurally, the PATL protein family is characterized by two conserved domains universally observed in other membrane trafficking-related proteins: a Sec14p-like lipid-binding
Corresponding authors at: College of Life Sciences, Sichuan University, Chengdu 610064, China. E-mail addresses: [email protected] (H. Zhou), [email protected] (H. Lin).
https://doi.org/10.1016/j.jplph.2019.01.012 Received 1 November 2018; Received in revised form 21 January 2019; Accepted 22 January 2019 Available online 24 January 2019 0176-1617/ © 2019 Elsevier GmbH. All rights reserved.
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
trafficking processes for cell plate biogenesis. Thus, PATL family members are putative regulators of membrane trafficking in plants. Phylogenetic analysis has identified 44 PATL sequences (PATL1like) in the plant kingdom, ranging from angiosperm species to gymnosperm species (Peterman et al., 2006). It has also been demonstrated that plant PATL-like proteins can be classified into four distinct clades, and specific residues in the GOLD domain are unique to each clade, implying a subgroup-specific and functional amino acid substitution for PATL (Peterman et al., 2006). This diversification might represent a particular biological function of each PATL subfamily in Arabidopsis. The C-terminus of GOLD domain in PATLs is Lys-rich, and possesses a conserved motif that is similar to the PtdIns(4,5)P2-binding motif in many other membrane trafficking-related proteins (Peterman et al., 2004). Arabidopsis PATL proteins also contain a variable domain in their N-terminus differing in both length and amino acid composition (Peterman et al., 2004, 2006). Importantly, there exists a PXXP motif which might play a role in cytoskeletal dynamics as well as membrane trafficking in the variable domain. A coiled-coil motif for protein-protein interaction is also observed in PATL proteins (Fig. 2; Peterman et al., 2004). The Arabidopsis PATLs are associated with the membrane system. The strong location to the cell plate during cytokinesis is probably common to all PATL protein family members in Arabidopsis (Peterman et al., 2004; Tejos et al., 2018). For instance, Arabidopsis PATL1 is a peripheral membrane protein, although it also partly locates in the cytoplasmic pool. It is found to be distributed across the cell plate but not concentrated at the site of new trafficking vesicle additions. However, it is distributed in the region where the plate is to undergo maturation (Peterman et al., 2004). The subcellular location pattern of Arabidopsis PATL2 is similar to that of PATL1. PATL2 is concentrated at the cell plate during cytokinesis and temporarily retained at the division plane even after the maturation of cell plates (Suzuki et al., 2016; Tejos et al., 2018). Arabidopsis PATLs are expressed in distinct but partly overlapping patterns. They are ubiquitously expressed in diverse organs and at all stages of embryogenesis. For example, PATL1 is expressed in the whole root apical meristem (RAM) and in stele cells in the distal zone of the RAM (Tejos et al., 2018). PATL2 partially resembles PATL1 in the expression pattern, however, it is also observed in pericycle cells in the root elongation zone and might be involved in LRP and vascular development (Tejos et al., 2018). PATL3 is more prominent in external cell layers, while PATL4 is ubiquitously expressed in the whole RAM. Interestingly, both PATL3 and PATL4 are expressed in the basal meristem of the root tip and the lateral root primordia (LRP) (Tejos et al., 2018). The distinct but partly overlapping expression patterns might represent complementary and diversified functions of PATLs in Arabidopsis.
Fig. 1. Phylogenetic tree of Sec14p-like proteins in Arabidopsis. Phylogenetic analysis was performed using the web-based tool freely available at http://www.phylogeny.fr, and the nucleotide sequences of the Sec14 lipidbinding domain of these 32 Arabidopsis Sec14p-like proteins were analyzed. Red box indicates the PATL subfamily in Arabidopsis.
3. PATLs bind phospholipids and function in diverse signaling pathways in plants
Fig. 2. Schematic diagram of the Arabidopsis PATLs protein motifs. A Sec14p-like domain is found in tandem with a GOLD domain, whereas a variable domain if in the N-terminus of each Arabidopsis PATL. Black line box, variable N-terminal domain; green line box, Sec14p-like domain; purple line box, Golgi dynamics domain (GOLD); filled gray box, coiled-coil region; vertical lines, PXXP motif.
Given the fact that a Sec14 phospholipid-binding domain and a Lysrich motif are presented in PATLs, they probably possess the ability to interact with phospholipids (Peterman et al., 2004, 2006). In a test for the ability of PATL1 to bind to unilamellar membrane vesicles composed of PtdIns, PtdCho, or phosphatidylethanolamine (PtdEth), the majority of PATL1 binds vesicles made of PtdIns (Peterman et al., 2004). In contrast, it has a low affinity to PtdIns(4)P and PtdIns(3,5)P2, and no binding to PtdIns(3,4)P2 (Peterman et al., 2004). In comparison to PATL1, however, Arabidopsis PATL2 binds to all the seven phosphorylated forms of PtdIns. Its binding affinity to monophosphorylated PtdIns is at the highest level, while for PtdIns(3,4,5)P3 is at the lowest level (Suzuki et al., 2016). PATL3 has been found to bind PtdIns(4,5)P2 and PtdIns(4)P. However, there exists no interaction between PATL3 and two other negatively charged phospholipids, PtdIns(3)P and phosphatidic acid (PA) (Wu et al., 2017). Since many of these PtdIns phosphorylated derivatives have been implicated in various cellular
domain and a GOLD following the N-terminal variable domain (Fig. 1; Peterman et al., 2004). The GOLD domain is widely found in a group of proteins related to Golgi function, membrane homeostasis, as well as vesicle trafficking (Anantharaman and Aravind, 2002; Peterman et al., 2004). The cell-plate localization of PATL1, the defining member of the PATL protein family, suggests a regulatory role during cytokinesis in plant cells, although the underlying mechanism remains to be elucidated (Peterman et al., 2004). It is speculated that Arabidopsis PATL1 more likely participates in clathrin-dependent endocytosis that aids cell plate remodeling and completion, rather than in the early membrane
95
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
Arabidopsis except for PATL5 could interact with EXO70A1 (Wu et al., 2017). It is possible that EXO70A1 plays a pivotal role in PATLs localization to diverse membrane systems in an exocyst-independent manner. Interestingly, two members of Arabidopsis PATL family, PATL3 and PATL6, interact with Alfalfa mosaic virus (AMV) movement protein (MP), suggesting a possible role of PATLs in viral movement regulation (Peiro et al., 2014). In fact, MPs encoded by plant viruses including AMV could interact with plant host proteins to alter viral movement (Bol, 2003; Boevink and Oparka, 2005; Taliansky et al., 2008; Hong and Ju, 2017). A well-established mechanism is related to plasmadesmata (PD) channels (Kumar et al., 2015; Hong and Ju, 2017). Subcellular localization analysis revealed that either Arabidopsis PATL3 or PATL6 could diminish viral movement by interfering with AMV MP targeting to PD. Consistently, transient overexpression of both proteins resulted in attenuated virus infection, whereas viral RNA accumulation was elevated in PATL3 and PATL6 knockout mutant. Unpredictably, PATL3 and PATL6 themselves cannot target to PD without AMV infection, indicating a virus-induced localization pattern of these PATLs (Peiro et al., 2014). Therefore, PATL3 and 6 might function as a defensive barrier of AMV virus in plants.
signaling networks (Munnik et al., 1998; Anderson et al., 1999), it is possible that PATL1 functions in plant development and stress responses at least in part through binding to such specific phosphoinositides. An increasing number of studies have characterized Arabidopsis PATLs as putative regulators implicated in diverse signaling pathways (Deng et al., 2007; Hsu et al., 2009; Kiba et al., 2012; Peiro et al., 2014; Zhou et al., 2018). For instance, Arabidopsis PATL protein family members have been reported to function as possible candidates of regulators in auxin signaling and PIN distribution (Tejos et al., 2018). PATLs are auxin-regulated target genes, and the Arabidopsis patl2 patl4 patl5 patl6 (patl2456−/−) quadruple mutant displayed obvious defects in auxin-induced PIN1 lateralization response. PATLs are also redundantly required for auxin-mediated root meristem size and gravitropic growth regulation (Tejos et al., 2018). In addition, the ectopic structures in PATLs loss-of-function mutant plants clearly suggest that PATLs play a crucial but redundant role in embryo patterning and organogenesis. Thus, PATLs might participate in the auxin feedback on PIN polarized localization in plants (Tejos et al., 2018). In Arabidopsis, several PATL1-interacting proteins have been identified, including Salt-Overly-Sensitive1 (SOS1), the major component of SOS pathway (Zhou et al., 2018), and calmodulin4 (CaM4), a multifunctional Ca2+ sensor (Chu et al., 2018), as well as associated molecule with the SH3 domain of STAM3 (AMSH3), a deubiquitinating enzyme (Isono et al., 2010). Thus, these interactors link PATL1 to diverse signaling networks. We recently found that PATL1 is implicated in ion homeostasis regulation in plants partly through SOS1 since PATL1 interacts with SOS1 in planta. Data showed that the PM Na+/H+ antiport activity was much lower in patl1 than in wide-type plant, and the membrane trafficking process might be disturbed due to PATL1 overexpression. It also participates in cellular redox homeostasis during salt stress, and artificial elimination of ROS using antioxidants partly rescues the salt-sensitive phenotype in patl1 mutant (Zhou et al., 2018). There also exists a direct interaction between PATL1 and CaM4. Loss-offunction mutants of PATL1 and CaM4 exhibit a freezing-tolerant phenotype. It is believed CaM4 negatively regulates freezing tolerance in a CBF-independent manner by interacting with PATL1 in Arabidopsis (Chu et al., 2018). In addition, PATL1 might also participate in vesicle trafficking mediated by AMSH3, possibly by directly binding and recruiting AMSH3 to the plasma membrane (PM) (Isono et al., 2010). Since AMSH3 is likely to be a regulator of autophagy in plants, PATL1 might also play a role in regulating autophagy (Katsiarimpa et al., 2013). Importantly, PATL1 can be ubiquitinated, suggesting a possible role of ubiquitination in its function (Igawa et al., 2009; Saracco et al., 2009). Arabidopsis PATL2 can be phosphorylated by mitogen-activated protein (MAP) kinse4 (MPK4), and the Ser-536 of PATL2 is the major site of phosphorylation. However, this phosphorylation has no effect on the subcellular location of PATL2. In contrast, its binding activity to phosphoinositides is significantly altered due to MPK4-mediated phosphorylation, suggesting a role of the MPK4-PATL2 cascade during cytokinesis in plants (Suzuki et al., 2016). In a functional phosphoproteomic profiling in membrane-related proteins, PATL2 is shown to be phosphorylated upon salt treatment, although this phosphorylation might not be mediated by MPK4 (Hsu et al., 2009; Suzuki et al., 2016). Thus, PATL2 probably also functions as a possible regulator of plant salt tolerance in plants. Recently, it has been reported that EXO70A1 interacts with the GOLD domain of PATL3 in Arabidopsis (Wu et al., 2017). EXO70A1 is a member of the exocyst complex which tethers trafficking vesicles at the target membrane before fusion, and has been implicated in plant cytokinesis (Fendrych et al., 2010; Wu and Guo, 2015). The localization of PATL3 to PM and cell plate is not achieved via the endocytic or secretory pathways. However, this process requires EXO70A1. Both PATL3 and EXO70A1 bind phosphoinositide, which might help attract target proteins to the membrane. In fact, all the other PATLs in
4. Concluding remarks and perspectives Up to now, the biological functions of PATL protein family members have not been well characterized. PATLs belong to Sec14p-like protein family, and function as PITPs in plants. All the PATLs possess the binding activity to phosphoinositides, although their affinity varies significantly. In addition, PATL1 might be associated with a number of interacting proteins such as SOS1, CaM4, MPK4, and AMSH3, and importantly, they might also undergo post-translational modifications (PTMs) such as ubiquitination and phosphorylation. These together imply an individually fine-tuned function of each PATL family member. In fact, PATLs are implicated in cytokinesis and their location to the cell plate and PM during cytokinesis might be assisted by specific PthIns, which could attract these PATLs and other target proteins to the membrane. It is believed that the PATL-interacting proteins probably link PATLs to diverse signaling pathways, therefore leading to integration of PATLs into distinct regulatory networks in plants. Multiple strategies should be adopted to elucidate the detailed biological functions of PATLs in plants. Thus, the identification of the possible interacting proteins or targets of specific PATL is required. Methods combined with proteomic investigation and Arabidopsis mutant screening might be used for PATLs-interacting protein determination. On the other hand, detailed subcellular localization assays should also be performed to investigate the biological functions of PATLs in membrane trafficking. Another promising direction is to determine the functional link between the PITP activity of PATLs and their roles in membrane trafficking. One important question that needs to be resolved is how PATLs are regulated. Thus, determination of possible PTMs on PATLs should be carried out. PATLs can be phosphorylated and modified with ubiquitination. Additional PTMs on PATLs might also exist and their effects on PATLs should be carefully investigated in the future. Given that membrane trafficking is involved in various aspects of signaling networks in plants and PALTs are putative membrane-trafficking proteins, it is of paramount importance to determine the regulatory roles of these Sec14p-like PITPs in plant development and stress response pathways. Although several lines of evidence have revealed that particular PATLs are linked to the plant auxin signaling network as well as salt tolerance and plant immunity against specific viruses, it is also interesting to determine whether PATLs participate in any other developmental programs and stress response signaling networks. As aforementioned, PATL1 might also play a role in regulating autophagy since AMSH3 is likely to be a regulator in autophagy in plants. Finally, the following questions are at the top list for careful 96
Journal of Plant Physiology 234–235 (2019) 94–97
H. Zhou et al.
consideration based on what we know about PATLs in plants: (i) what role(s) do PATLs play in membrane trafficking-related processes (e.g. cell plate formation during cytokinesis)? (ii) what is the functional link between the PITP activity of PATLs and their regulatory roles in membrane trafficking? (iii) do there exist additional PATLs-interacting proteins that modulate their biological function and link them to diverse signaling networks? (iv) what other kind of PTMs will happen to PATLs during plant development and stress responses? And last but not the least, (v) what is the evolutionary relationship between various PATLs in the plant kingdom?
biogenesis. EMBO J . 15, 6447–6459. Fendrych, M., Synek, L., Pecenkova, T., Toupalova, H., Cole, R., Drdova, E., et al., 2010. The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22 (9), 3053–3065. Hay, J., Martin, T., 1993. Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca2+-activated secretion. Nature 366, 572–575. Hilgemann, D.W., Feng, S., Nasuhoglu, C., 2001. The complex and intriguing lives of PIP2 with ion channels and transporters. Science (STKE) re19. Hong, J., Ju, H., 2017. The Plant cellular systems for plant virus movement. Plant Pathol. J. 33 (3), 213–228. Hsu, J., Wang, L., Wang, S., Lin, C., Ho, K., Shi, F., Chang, I., 2009. Functional phosphoproteomic profiling of phosphorylation sites in membrane fractions of saltstressed Arabidopsis thaliana. Proteome Sci. 7 (1), 42. Huang, J., Ghosh, R., Bankaitis, V.A., 2016. Sec14-like phosphatidylinositol transfer proteins and the biological landscape of phosphoinositide signaling in plants. Biochim. Biophys. Acta 1861 (9), 1352–1364. Igawa, T., Fujiwara, M., Takahashi, H., Sawasaki, T., Endo, Y., Seki, M., et al., 2009. Isolation and identification of ubiquitin-related proteins from Arabidopsis seedlings. J. Exp. Bot. 60 (11), 3067–3073. Isono, E., Katsiarimpa, A., Muller, I., Anzenberger, F., Stierhof, Y., Geldner, N., et al., 2010. The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22 (6), 1826–1837. Katsiarimpa, A., Kalinowska, K., Anzenberger, F., Weis, C., Ostertag, M., Tsutsumi, C., et al., 2013. The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25 (6), 2236–2252. Kiba, A., Nakano, M., Vincent-Pope, P., Takahashi, H., Sawasaki, T., Endo, Y., et al., 2012. A novel Sec14 phospholipid transfer protein from Nicotiana benthamiana is upregulated in response to Ralstonia solanacearum infection, pathogen associated molecular patterns and effector molecules and involved in plant immunity. J. Plant Physiol. 169, 1017–1022. Kumar, D., Kumar, R., Hyun, T., Kim, J., 2015. Cell-to-cell movement of viruses via plasmodesmata. J. Plant Res. 128 (1), 37–47. Munnik, T., Irvine, R., Musgrave, A., 1998. Phospholipid signaling in plants. Biochim. Biophys. Acta 1389, 222–272. Novick, P., Field, C., Schekman, R., 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205–215. Peiro, A., Izquierdogarcia, A., Sancheznavarro, J., Pallas, V., Mulet, J., Aparicio, F., 2014. Patellins 3 and 6, two members of the plant patellin family, interact with the movement protein of Alfalfa mosaic virus and interfere with viral movement. Mol. Plant Pathol. 15 (9), 881–891. Peterman, T.K., Ohol, Y.M., Mcreynolds, L., Luna, E., 2004. Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol. 136 (2), 3080–3094. Peterman, T., Sequeira, A., Samia, J., Lunde, E., 2006. Molecular cloning and characterization of patellin1, a novel sec14-related protein, from zucchini (Cucurbita pepo). J. Plant Physiol. 163 (11), 1150–1158. Saracco, S., Hansson, M., Scalf, M., Walker, J., Smith, L.M., Vierstra, R., 2009. Tandem affinity purification and mass spectrometric analysis of ubiquitylated proteins in Arabidopsis. Plant J. 59 (2), 344–358. Schaaf, G., Ortlund, E.A., Tyeryar, K.R., Mousley, C.J., Ile, K.E., Garrett, T.A., Ren, J., Woolls, M.J., Raetz, C.R., Redinbo, M.R., Bankaitis, V.A., 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell 29 (2), 191–206. Simon, J., Morimoto, T., Bankaitis, V., Gottlieb, T., Ivanov, I., Adesnik, M., Sabatini, D., 1998. An essential role for the phosphatidylinositol transfer protein in the scission of coatomer-coated vesicles from the trans-Golgi network. Proc. Natl. Acad. Sci. U. S. A. 95, 11181–11186. Suzuki, T., Matsushima, C., Nishimura, S., Higashiyama, T., Sasabe, M., Machida, Y., 2016. Identification of phosphoinositide-binding protein patellin2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis. Plant Cell Physiol. 57 (8), 1744–1755. Taliansky, M., Torrance, L., Kalinina, N., 2008. Role of plant virus movement proteins. Methods Mol. Biol. 33–54. Tejos, R., Rodriguezfurlan, C., Adamowski, M., Sauer, M., Norambuena, L., Friml, J., 2018. Patellins are regulators of auxin-mediated PIN1 relocation and plant development in Arabidopsis thaliana. J. Cell. Sci. 131 (2), 1–10. Vincent, P., Chua, M., Nogue, F., Fairbrother, A., Mekeel, H., Xu, Y., et al., 2005. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J. Cell Biol. 168, 801–812. Wu, B., Guo, W., 2015. The exocyst at a glance. J. Cell. Sci. 128 (16), 2957–2964. Wu, C., Tan, L., Van Hooren, M., Tan, X., Liu, F., Li, Y., et al., 2017. Arabidopsis EXO70A1 recruits patellin3 to the cell membrane independent of its role as an exocyst subunit. J. Integr. Plant Biol. 59 (12), 851–865. Zhou, H., Wang, C., Tan, T., Cai, J., He, J., Lin, H., 2018. Patellin1 negatively modulates salt tolerance by regulating PM Na+/H+ antiport activity and cellular redox homeostasis in Arabidopsis. Plant Cell Physiol. 59 (8), 1630–1642.
Accession numbers Sequence data from this article can be found in the GenBank/EMBL and JGI databases under the following accession numbers: PATL1, At1g72150; PATL2, At1g22530; PATL3, At1g72160; PATL4, At1g30690; PATL5, At4g09160 and PATL6, At3g51670; SOS1, At2g01980; CaM4, At1g66410; AMSH3, At4g16144; MPK4, At4g01370; and EXO70A1, At5g03540. Author contributions All the authors contributed to discussion. H.Z. wrote the article with assistance of H.D. Y.L., X.S., and J.Z. contributed to the reference collection. H.Z. and H.D. also contributed by illustrating the artwork. H.Z. and H.L. supervised the projects. Acknowledgments We sincerely apologize to those authors not able to cite their works in this review due to space limitation. We thank Dr. Yan Guo from China Agricultural University for reading the manuscript and stimulating discussions. This work was supported by National Natural Science Foundation of China (NSFC) (Grant 31870241 and 31600201 to H.Z). All the authors declare no conflict of interest. References Aikten, J.F., van Heusden, G.P., Temkin, M., Dowhan, W, 1990. The gene encoding the phosphatidylinositol transfer protein is essential for cell growth. J. Biol. Chem. 265 (8), 4711–4717. Anantharaman, V., Aravind, L., 2002. The GOLD domain, a novel protein module involved in Golgi function and secretion. Genome Biol. 3 (5), 1–7. Anderson, R., Boronenkov, I., Doughman, S., Kunz, J., Loijens, J., 1999. Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J. Biol. Chem. 274 (15), 9907–9910. Bankaitis, V.A., Aitken, J.R., Cleves, A.E., Dowhan, W., 1990. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347, 561–562. Bankaitis, V., Mousley, C., Schaaf, G., 2010. The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem. Sci. 35, 150–160. Boevink, P., Oparka, K., 2005. Virus-host interactions during movement processes. Plant Physiol. 138 (4), 1815–1821. Bol, J., 2003. Alfalfa mosaic virus: coat protein-dependent initiation of infection. Mol. Plant Pathol. 4 (1), 1–8. Chu, M., Li, J., Zhang, J., Shen, S., Li, C., Gao, Y., et al., 2018. AtCaM4 interacts with a Sec14-like protein, PATL1, to regulate freezing tolerance in Arabidopsis in a CBFindependent manner. J. Exp. Bot. 69 (21), 5241–5253. Cleves, A.E., Mcgee, T., Bankaitis, V.A., 1991. Phospholipid transfer proteins: a biological debut. Trends Cell Biol. 1, 30–34. De Campos, M.K., Schaaf, G., 2017. The regulation of cell polarity by lipid transfer proteins of the SEC14 family. Curr. Opin. Plant Biol. 40, 158–168. Deng, Z., Zhang, X., Tang, W., Osesprieto, J., Suzuki, N., Gendron, J., et al., 2007. A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell. Proteom. 6 (12), 2058–2071. Fang, M., Kearns, B.G., Gedvilaite, A., Kagiwada, S., Kearns, M., Fung, M.K.Y., Bankaitis, V.A., 1996. Kes1p shares homology with human oxysterol binding protein and participates in a novel regulatory pathway for yeast Golgi-derived transport vesicle
97