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FYVE and PHOX domain protein families in P. patens. Schematic diagram of the domain structures of the known plant FYVE and PHOX domain-containing plant proteins. The nomenclature for the different proteins is shown in the right
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Main conclusion: Genome-wide identification, together with gene expression patterns and promoter region analysis of FYVE and PHOX proteins in Physcomitrella patens, emphasized their importance in regulating mainly developmental processes in P. patens.
Abstract
Phosphatidylinositol 3-phosphate (PtdIns3P) is a signaling phospholipid, which regulate...
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... S8, S9), and therefore, we selected the longer of the sequence variants for further analyses. PpFYVE and PpPHOX genes are dispersed throughout the P. patens genome, being located on different chromosomes ( Fig. 1) and the protein members of each subfamily have a conserved modular structure compared to their orthologs from other plant species (Fig. ...
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... synthesize PtdIns(3,5)P 2 from PtdIns3P. Both PpFABs cluster together and share 81% similarity. They harbor three conserved domains: the N-terminal FYVE domain necessary for binding to PtdIns3P-containing membranes, a Cpn60_TCP1 (HSP chaperonin_T complex1) homology domain and a C-terminal kinase domain, in accordance with the description of FABs (Fig. 2). FAB proteins in plants have additional members lacking a FYVE domain. The single FAB protein present in C. reinhardtii lacks a FYVE domain, whereas P. patens and A. thaliana have one (Pp3c17_4720) and two members AtFAB1C (At1g71010) and AtFAB1D (At1g34260), respectively. The class II FYVE is represented by a single protein in P. ...
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... GST-PH AtPRAF4 (Jensen et al. 2001). All FYVE domains of PRAF proteins analyzed exhibit two important substitutions in the basic (R/K) 1 (R/K) HHCR 6 motif, where His4 and Arg6, components of the binding pocket that determines the specificity for binding of PtdIns3P ( Gaullier et al. 2000) are substituted by asparagine and tyrosine (Suppl. Fig. S2). The RCC1 motif is present in several proteins in P. patens, and in other organisms it was reported as a versatile domain which may perform different functions, including guanine nucleotide exchange on small GTP-binding proteins, enzyme inhibition, or interaction with proteins and lipids ( Hadjebi et al. 2008). A guanine nucleotide ...
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... domain consists of ∼ 280 amino acids and is found in eukaryotic proteins involved in vesicle trafficking, yet the function of this domain is unknown. The WxxD, RRHHCR and RVC motifs are less conserved in PpALFYs, any of the four proteins conserved the WxxD motif, and PpALFY 1-2 are the two members with a conserved RRHHCR and RVC motifs (Suppl. Fig. ...
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... phylogenetic analysis of PHOX proteins from the Chlorophytes, Charophytes, Bryophytes, Lycophytes and Angiosperms analyzed, grouped these proteins into five different groups named Class I-V (Figs. 2, 4). Members from P. patens clustered with the subfamilies previously described for A. thaliana with the exception of class V, which are PLDζs (van Leeuwen et al. ...
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... respectively (Fig. 3), whereas other members such as Ostrococcus lucimarinus and Ostreococcus tauri do not encode any FYVE proteins ( Banerjee et al. 2010). Class I (FABs), are highly conserved proteins from yeast to mammals and plants, and members from this class conserved all the canonical ligandbinding site consensus sequence of RRHHCR (Suppl. Fig. S2). Although C. reinhardtii lack FAB proteins with a FYVE domain, it harbors the capacity to synthetize PtdIns(3,5)P 2 ( Meijer et al. 1999), and in similar fashion, in vitro activity assays using heterologous recombinant AtFAB1C-GST, which lacks a FYVE domain shown its ability to synthetize PtdIns(3,5)P 2 from PtdIns3P ( Bak et al. ...
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... class II of FYVE proteins is present in all species analyzed. The first arginine in the consensus sequence R 1 RHHCR has a substitution for glycine or serine (Suppl. Fig. S2), but in A. thaliana it maintains the ability to bind PtdIns3P, together with the SYLF domain exhibited by these proteins ( Sutipatanasomboon et al. 2017). AtFYVE2, the A. thaliana ortholog of PpFYVE2 acts as an autophagy regulator and repressor of cell death, it binds to the ECL Page 15 of 20 62 component of ESCRT-I late endosomes ...
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... the root tip ( Briggs et al. 2006). The results from this study, where PpPRAF2 is up-regulated in the juvenile protonemata mainly in caulonemata suggest a role of this protein in these fast tip growing cells. PRAF proteins exhibit another deviation of the RRHH 4 CR 6 canonical motif, where asparagine and tyrosine substitute His4 and Arg6 (Suppl. Fig. S2). Although a recombinant 6XHis-FYVE AtPRAF4 exhibit binding towards PtdIns3P, a double mutant GST-FYVE AtPRAF4-N658H,Y660R has an increased affinity to PtdIns3P, highlighting the importance of this residues for the specific binding ( Gaullier et al. 2000;Jensen et al. 2001). Yet, the role of FYVE domain in these proteins is ...
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... and WD40 domains are conserved through land plant evolution, the FYVE domain of these proteins is absent in the liverwort M. polymorpha and in tracheophytes, suggesting that its function was not further essential. In addition, the FYVE domain of PpALFYs exhibits a low degree of conservation in comparison to the canonical FYVE sequence (Suppl. Fig. ...
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... In addition, the expression of almost all ATG genes analyzed also increased in the 48 h to 72 h time window after the incision, providing initial evidence that supports a link between autophagy and the development of the polar growing protonemata. Furthermore, the expression data for this tissue grown in optimal conditions (Xiao et al., 2011;Agudelo-Romero et al., 2020) indicated that levels of most ATG genes are higher in caulonemata than in chloronemata ( Figure S5B). Considering that caulonemata elongate three times faster than chloronemata, these observations suggest a role for autophagy in apical growth. ...
Physcomitrium patens apical growing protonemal cells have the singularity that they continue to undergo cell divisions as the plant develops. This feature provides a valuable tool to study autophagy in the context of a multicellular apical growing tissue coupled to development. Herein, we showed that the core autophagy machinery is present in the moss P. patens, and characterized the 2D and 3D growth and development of atg5 and atg7 loss-of-function mutants under optimal and nutrient-deprived conditions. Our results showed that 2D growth of the different morphological and functional protonemata apical growing cells, chloronema and caulonema, is differentially modulated by this process. These differences depend on the protonema cell type and position along the protonemal filament, and growth condition. As a global plant response, the absence of autophagy favors the spread of the colony through protonemata growth at the expense of a reduction of the 3D growth, such as the buds and gametophore development, and thus the adult gametophytic and reproductive phases. Altogether this study provides valuable information suggesting that autophagy has roles during apical growth with differential responses within the cell types of the same tissue and contributes to life cycle progression and thus the growth and development of the 2D and 3D tissues of P. patens.
... van Leeuwen et al., 2004;Agudelo-Romero et al., 2020). A BLAST search in 27 plant genomes representing all major evolutionary lineages of land plants (Phytozome 11; www.phytozome.jgi.doe.gov) ...
During evolution, land plants generated unique proteins that participate in endosomal sorting and multivesicular endosome (MVE) biogenesis, many of them with specific phosphoinositide‐binding capabilities. Nonetheless, the function of most plant phosphoinositide‐binding proteins in endosomal trafficking remains elusive.
Here, we analysed several Arabidopsis mutants lacking predicted phosphoinositide‐binding proteins and first identified fyve4‐1 as a mutant with a hypersensitive response to high‐boron conditions and defects in degradative vacuolar sorting of membrane proteins such as the borate exporter BOR1‐GFP.
FYVE4 encodes a plant‐unique, FYVE domain‐containing protein that interacts with SNF7, a core component of ESCRT‐III (Endosomal Sorting Complex Required for Transport III). FYVE4 affects the membrane association of the late‐acting ESCRT components SNF7 and VPS4, and modulates the formation of intraluminal vesicles (ILVs) inside MVEs. The critical function of FYVE4 in the ESCRT pathway was further demonstrated by the strong genetic interactions with SNF7B and LIP5. Although the fyve4‐1, snf7b and lip5 single mutants were viable, the fyve4‐1 snf7b and fyve4‐1 lip5 double mutants were seedling lethal, with strong defects in MVE biogenesis and vacuolar sorting of ubiquitinated membrane proteins.
Taken together, we identified FYVE4 as a novel plant endosomal regulator, which functions in ESCRTing pathway to regulate MVE biogenesis.
... The PI3P-binding pocket is formed by the conserved WxxD, (R/K)(R/K)HHCR, and RVC motifs at the end of the b1-strand, whereby the lipid's head group ends up parallel to the b1 strand. Due to its small size, PPI specificity is mostly indirect, with only PI3P or PI5P fitting inside the FYVE pocket, with PI3P being preferred (Kutateladze and Overduin, 2001;Agudelo-Romero et al., 2020). Membrane localization is further positively influenced by coincidence detection, either via homodimerization, additional lipid-binding motifs, or protein-protein interaction (Lystad and Simonsen, 2016). ...
... Arabidopsis has 15 proteins with a FYVE domain. They all contain the conserved Wxx(D/G), (R/K)(R/K)H(H/N)C(R/Y), and RVC motifs (SupplementalFigure S2;van Leeuwen et al., 2004;Wywial and Singh, 2010;Agudelo-Romero et al., 2020). Lipid binding was analyzed for four of them, including FREE1/FYVE1, a protein that is involved in complex regulation in endosomal trafficking, autophagy, and vacuolar biogenesis as well as ABA signaling and indeed binds PI3P(Barberon et al., 2014;Gao et al., 2014;Kolb et al., 2015;Garcia-Leon et al., 2019;Zhao et al., 2019). ...
Membranes are essential for cells and organelles to function. As membranes are impermeable to most polar and charged molecules, they provide electrochemical energy to transport molecules across and create compartmentalized micro-environments for specific enzymatic and cellular processes. Membranes are also responsible for guided transport of cargoes between organelles and during endo- and exocytosis. In addition, membranes play key roles in cell signaling by hosting receptors and signal transducers, and as substrates and products of lipid second messengers. Anionic lipids and their specific interaction with target proteins play an essential role in these processes, which are facilitated by specific lipid binding domains (LBDs). Protein crystallography, lipid-binding studies, subcellular localization analyses, and computer modelling have greatly advanced our knowledge over the years of how these domains achieve precision binding and what their function is in signaling and membrane trafficking, as well as in plant development and stress acclimation.
... Arabidopsis contains 11 PX proteins (van Leeuwen et al., 2004;Agudelo-Romero et al., 2020;Fig. 4). ...
... The PI3Pbinding pocket is formed by the conserved WxxD, (R/K)(R/K)HHCR and RVC motifs at the end of the β1-strand, whereby the lipid's headgroup ends up parallel to the β1 strand. Due to its small size, PPI specificity is mostly indirect, with only PI3P or PI5P fitting inside the FYVE pocket, with PI3P being preferred (Kutateladze and Overduin, 2001;Agudelo-Romero et al., 2020). Membrane localization is further positively influenced by coincidence detection, either via homodimerization, additional lipid binding motifs, or protein-protein interaction (Lystad and Simonsen, 2016). ...
... They all contain the conserved Wxx(D/G), (R/K)(R/K)H(H/N)C(R/Y), and RVC motifs (Suppl. Fig. S2) (van Leeuwen et al., 2004;Wywial and Singh, 2010;Agudelo-Romero et al., 2020). Lipid binding was analysed for four of them, including FREE1/FYVE1, a protein that is involved in complex regulation in endosomal trafficking, autophagy, and vacuolar biogenesis as well as ABA signalling, and indeed binds PI3P (Barberon et al., 2014;Gao et al., 2014;Kolb et al., 2015;Garcia-Leon et al., 2019;Li et al., 2019;Zhao et al., 2019). ...
Membranes are essential for cells and organelles to function. As membranes are impermeable to most polar and charged molecules, they provide electrochemical energy to transport molecules across and create compartmentalized micro-environments for specific enzymatic and cellular processes. Membranes are also responsible for guided transport of cargoes between organelles and during endo-and exocytosis. In addition, membranes play key roles in cell signaling by hosting receptors and signal transducers, and as substrates and products of lipid second messengers. Anionic lipids and their specific interaction with target proteins play an essential role in these processes, which are facilitated by specific lipid binding domains (LBDs). Protein crystallography, lipid-binding studies, subcellular localization analyses, and computer modelling have greatly advanced our knowledge over the years of how these domains achieve precision binding and what
BEige and Chediak–Higashi domain containing proteins (BDCPs) have been described to function in membrane-dependent processes in eukaryotes. This role was also observed for the BDCP SPIRRIG (SPI) in the model plant Arabidopsis thaliana in the context of cell morphogenesis. Additionally, AtSPI was found to control salt stress resistance by mediating mRNA stability and salt stress-dependent processing body formation. In this work, we utilize an evolutionarily comparative approach to unravel conserved, basal BDCP functions in the liverwort Marchantia polymorpha. Our phenotypic and physiological analyses show that MpSPI is involved in cell morphogenesis and salt resistance regulation, indicating that both functions are evolutionarily conserved between the two species. Co-localization was found with endosomal and P-body markers, suggesting links to membrane-dependent processes and mRNA metabolism. Finally, we present transcriptomics data showing that AtSPI and MpSPI regulate orthologous genes in A. thaliana and M. polymorpha.
