TPLATE complex-dependent endocytosis attenuates CLAVATA1 signaling for shoot apical meristem maintenance

. 2023 Sep 06 ; 24 (9) : e54709. [epub] 20230717

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37458257

Grantová podpora
682436 European Research Council - International

Endocytosis regulates the turnover of cell surface localized receptors, which are crucial for plants to rapidly respond to stimuli. The evolutionary ancient TPLATE complex (TPC) plays an essential role in endocytosis in Arabidopsis plants. Knockout or knockdown of single TPC subunits causes male sterility and seedling lethality phenotypes, complicating analysis of the roles of TPC during plant development. Partially functional alleles of TPC subunits however only cause mild developmental deviations. Here, we took advantage of the partially functional TPLATE allele, WDXM2, to investigate a role for TPC-dependent endocytosis in receptor-mediated signaling. We discovered that reduced TPC-dependent endocytosis confers a hypersensitivity to very low doses of CLAVATA3 peptide signaling. This hypersensitivity correlated with the abundance of the CLAVATA3 receptor protein kinase CLAVATA1 at the plasma membrane. Genetic and biochemical analysis as well as live-cell imaging revealed that TPC-dependent regulation of CLAVATA3-dependent internalization of CLAVATA1 from the plasma membrane is required for shoot stem cell homeostasis. Our findings provide evidence that TPC-mediated endocytosis and degradation of CLAVATA1 is a mechanism to dampen CLAVATA3-mediated signaling during plant development.

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Anne P, Amiguet‐Vercher A, Brandt B, Kalmbach L, Geldner N, Hothorn M, Hardtke CS (2018) CLERK is a novel receptor kinase required for sensing of root‐active CLE peptides in Arabidopsis . Development 145: 1–10 PubMed PMC

Arora D, Abel NB, Liu C, Van Damme P, Yperman K, Eeckhout D, Vu LD, Wang J, Tornkvist A, Impens F et al (2020) Establishment of proximity‐dependent biotinylation approaches in different plant model systems. Plant Cell 32: 3388–3407 PubMed PMC

Arora D, Van Damme D (2021) Motif‐based endomembrane trafficking. Plant Physiol 186: 221–238 PubMed PMC

Bashline L, Li S, Zhu X, Gu Y (2015) The TWD40‐2 protein and the AP2 complex cooperate in the clathrin‐mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. Proc Natl Acad Sci USA 112: 12870–12875 PubMed PMC

Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S (2012) Spatio‐temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status‐dependent endosomal sorting. Plant Cell 24: 4205–4219 PubMed PMC

Ben Khaled S, Postma J, Robatzek S (2015) A moving view: subcellular trafficking processes in pattern recognition receptor‐triggered plant immunity. Annu Rev Phytopathol 53: 379–402 PubMed

Bindels DS, Haarbosch L, van Weeren L, Postma M, Wiese KE, Mastop M, Aumonier S, Gotthard G, Royant A, Hink MA et al (2017) mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat Methods 14: 53–56 PubMed

Blumke P, Schlegel J, Gonzalez‐Ferrer C, Becher S, Pinto KG, Monaghan J, Simon R (2021) Receptor‐like cytoplasmic kinase MAZZA mediates developmental processes with CLAVATA1 family receptors in Arabidopsis . J Exp Bot 72: 4853–4870 PubMed

Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617–619 PubMed

Breda AS, Hazak O, Schultz P, Anne P, Graeff M, Simon R, Hardtke CS (2019) A cellular insulator against CLE45 peptide signaling. Curr Biol 29: 2501–2508 PubMed

Brunoud G, Galvan‐Ampudia CS, Vernoux T (2020) Methods to visualize auxin and cytokinin signaling activity in the shoot apical meristem. Methods Mol Biol 2094: 79–89 PubMed

Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis . Development 119: 397–418 PubMed

Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121: 2057–2067

Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis . Cell 89: 575–585 PubMed

Claus LAN, Savatin DV, Russinova E (2018) The crossroads of receptor‐mediated signaling and endocytosis in plants. J Integr Plant Biol 60: 827–840 PubMed

Dejonghe W, Kuenen S, Mylle E, Vasileva M, Keech O, Viotti C, Swerts J, Fendrych M, Ortiz‐Morea FA, Mishev K et al (2016) Mitochondrial uncouplers inhibit clathrin‐mediated endocytosis largely through cytoplasmic acidification. Nat Commun 7: 11710 PubMed PMC

Dejonghe W, Sharma I, Denoo B, De Munck S, Lu Q, Mishev K, Bulut H, Mylle E, De Rycke R, Vasileva M et al (2019) Disruption of endocytosis through chemical inhibition of clathrin heavy chain function. Nat Chem Biol 15: 641–649 PubMed PMC

Deyoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180: 895–904 PubMed PMC

DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1‐related BAM1, BAM2 and BAM3 receptor kinase‐like proteins are required for meristem function in Arabidopsis . Plant J 45: 1–16 PubMed

Di Rubbo S, Irani NG, Kim SY, Xu ZY, Gadeyne A, Dejonghe W, Vanhoutte I, Persiau G, Eeckhout D, Simon S et al (2013) The clathrin adaptor complex AP‐2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis . Plant Cell 25: 2986–2997 PubMed PMC

Dievart A, Dalal M, Tax FE, Lacey AD, Huttly A, Li J, Clark SE (2003) CLAVATA1 dominant‐negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15: 1198–1211 PubMed PMC

Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–1914 PubMed

Gadeyne A, Sanchez‐Rodriguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G et al (2014) The TPLATE adaptor complex drives clathrin‐mediated endocytosis in plants. Cell 156: 691–704 PubMed

Gou X, Li J (2020) Paired receptor and coreceptor kinases perceive extracellular signals to control plant development. Plant Physiol 182: 1667–1681 PubMed PMC

Graeff M, Rana S, Marhava P, Moret B, Hardtke CS (2020) Local and systemic effects of brassinosteroid perception in developing phloem. Curr Biol 30: 1626–1638 PubMed

Grefen C, Blatt MR (2012) A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). Biotechniques 53: 311–314 PubMed

Hazak O, Hardtke CS (2016) CLAVATA 1‐type receptors in plant development. J Exp Bot 67: 4827–4833 PubMed

Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez‐Villalon A, Hothorn M, Hardtke CS (2017) Perception of root‐active CLE peptides requires CORYNE function in the phloem vasculature. EMBO Rep 18: 1367–1381 PubMed PMC

Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PloS One 5: e9788 PubMed PMC

Hirst J, Schlacht A, Norcott JP, Traynor D, Bloomfield G, Antrobus R, Kay RR, Dacks JB, Robinson MS (2014) Characterization of TSET, an ancient and widespread membrane trafficking complex. Elife 3: e02866 PubMed PMC

Hobe M, Muller R, Grunewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis . Dev Genes Evol 213: 371–381 PubMed

Hohmann U, Lau K, Hothorn M (2017) The structural basis of ligand perception and signal activation by receptor kinases. Annu Rev Plant Biol 68: 109–137 PubMed

Hu C, Zhu Y, Cui Y, Cheng K, Liang W, Wei Z, Zhu M, Yin H, Zeng L, Xiao Y et al (2018) A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat Plants 4: 205–211 PubMed

Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider‐Pizon J, Hnilikova J, Sisa M, Buyst D, Vilarrasa‐Blasi J, Szatmari AM et al (2012) Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat Chem Biol 8: 583–589 PubMed

Ishida T, Tabata R, Yamada M, Aida M, Mitsumasu K, Fujiwara M, Yamaguchi K, Shigenobu S, Higuchi M, Tsuji H et al (2014) Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis . EMBO Rep 15: 1202–1209 PubMed PMC

Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca‐CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842–845 PubMed

Johnson A, Dahhan DA, Gnyliukh N, Kaufmann WA, Zheden V, Costanzo T, Mahou P, Hrtyan M, Wang J, Aguilera‐Servin J et al (2021) The TPLATE complex mediates membrane bending during plant clathrin‐mediated endocytosis. Proc Natl Acad Sci USA 118: e2113046118 PubMed PMC

Karimi M, Depicker A, Hilson P (2007) Recombinational cloning with plant gateway vectors. Plant Physiol 145: 1144–1154 PubMed PMC

Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi‐Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor‐like kinase that transmits the CLV3 signal in Arabidopsis . Development 137: 3911–3920 PubMed

Kitagawa M, Jackson D (2019) Control of meristem size. Annu Rev Plant Biol 70: 269–291 PubMed

Lammens T, Boudolf V, Kheibarshekan L, Zalmas LP, Gaamouche T, Maes S, Vanstraelen M, Kondorosi E, La Thangue NB, Govaerts W et al (2008) Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc Natl Acad Sci USA 105: 14721–14726 PubMed PMC

Liu D, Kumar R, Claus LAN, Johnson AJ, Siao W, Vanhoutte I, Wang P, Bender KW, Yperman K, Martins S et al (2020) Endocytosis of BRASSINOSTEROID INSENSITIVE1 is partly driven by a canonical Tyr‐based motif. Plant Cell 32: 3598–3612 PubMed PMC

Mbengue M, Bourdais G, Gervasi F, Beck M, Zhou J, Spallek T, Bartels S, Boller T, Ueda T, Kuhn H et al (2016) Clathrin‐dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases. Proc Natl Acad Sci USA 113: 11034–11039 PubMed PMC

Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58: 167–176 PubMed

Mishev K, Lu Q, Denoo B, Peurois F, Dejonghe W, Hullaert J, De Rycke R, Boeren S, Bretou M, De Munck S et al (2018) Nonselective chemical inhibition of Sec7 domain‐containing ARF GTPase exchange factors. Plant Cell 30: 2573–2593 PubMed PMC

Nimchuk ZL (2017) CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two‐step transcriptional compensation loop. PLoS Genet 13: e1006681 PubMed PMC

Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM (2011) Plant stem cell signaling involves ligand‐dependent trafficking of the CLAVATA1 receptor kinase. Curr Biol 21: 345–352 PubMed PMC

Nimchuk ZL, Zhou Y, Tarr PT, Peterson BA, Meyerowitz EM (2015) Plant stem cell maintenance by transcriptional cross‐regulation of related receptor kinases. Development 142: 1043–1049 PubMed PMC

Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294 PubMed

Olsson V, Joos L, Zhu S, Gevaert K, Butenko MA, De Smet I (2019) Look closely, the beautiful may Be small: precursor‐derived peptides in plants. Annu Rev Plant Biol 70: 153–186 PubMed

Ortiz‐Morea FA, Savatin DV, Dejonghe W, Kumar R, Luo Y, Adamowski M, Van den Begin J, Dressano K, Pereira de Oliveira G, Zhao X et al (2016) Danger‐associated peptide signaling in Arabidopsis requires clathrin. Proc Natl Acad Sci USA 113: 11028–11033 PubMed PMC

Paez Valencia J, Goodman K, Otegui MS (2016) Endocytosis and endosomal trafficking in plants. Annu Rev Plant Biol 67: 309–335 PubMed

Poncini L, Wyrsch I, Denervaud Tendon V, Vorley T, Boller T, Geldner N, Metraux JP, Lehmann S (2017) In roots of Arabidopsis thaliana, the damage‐associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PloS One 12: e0185808 PubMed PMC

Roberts I, Smith S, Stes E, De Rybel B, Staes A, van de Cotte B, Njo MF, Dedeyne L, Demol H, Lavenus J et al (2016) CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis . J Exp Bot 67: 4889–4899 PubMed PMC

Schlegel J, Denay G, Wink R, Pinto KG, Stahl Y, Schmid J, Blumke P, Simon RG (2021) Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways. Elife 10: e70934 PubMed PMC

Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644 PubMed

Shinohara H, Matsubayashi Y (2015) Reevaluation of the CLV3‐receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand‐binding point of view. Plant J 82: 328–336 PubMed

Somssich M, Ma Q, Weidtkamp‐Peters S, Stahl Y, Felekyan S, Bleckmann A, Seidel CA, Simon R (2015) Real‐time dynamics of peptide ligand‐dependent receptor complex formation in planta. Sci Signal 8: ra76 PubMed

Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19: 909–914 PubMed

Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp‐Peters S, Pinto KG, Kirschner GK, Schmid JB, Wink RH, Hulsewede A et al (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23: 362–371 PubMed

Su YH, Zhao XY, Liu YB, Zhang CL, O'Neill SD, Zhang XS (2009) Auxin‐induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis . Plant J 59: 448–460 PubMed PMC

Van Damme D, Coutuer S, De Rycke R, Bouget FY, Inze D, Geelen D (2006) Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18: 3502–3518 PubMed PMC

Van Leene J, Eeckhout D, Cannoot B, De Winne N, Persiau G, Van De Slijke E, Vercruysse L, Dedecker M, Verkest A, Vandepoele K et al (2015) An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes. Nat Protoc 10: 169–187 PubMed

Wang P, Pleskot R, Zang J, Winkler J, Wang J, Yperman K, Zhang T, Wang K, Gong J, Guan Y et al (2019) Plant AtEH/Pan1 proteins drive autophagosome formation at ER‐PM contact sites with actin and endocytic machinery. Nat Commun 10: 5132 PubMed PMC

Wang J, Mylle E, Johnson A, Besbrugge N, De Jaeger G, Friml J, Pleskot R, Van Damme D (2020) High temporal resolution reveals simultaneous plasma membrane recruitment of TPLATE complex subunits. Plant Physiol 183: 986–997 PubMed PMC

Wang J, Yperman K, Grones P, Jiang Q, Dragwidge J, Mylle E, Mor E, Nolf J, Eeckhout D, De Jaeger G et al (2021) Conditional destabilization of the TPLATE complex impairs endocytic internalization. Proc Natl Acad Sci USA 118: e2023456118 PubMed PMC

Yamaguchi YL, Ishida T, Sawa S (2016) CLE peptides and their signaling pathways in plant development. J Exp Bot 67: 4813–4826 PubMed

Yperman K, Papageorgiou AC, Merceron R, De Munck S, Bloch Y, Eeckhout D, Jiang Q, Tack P, Grigoryan R, Evangelidis T et al (2021a) Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding. Nat Commun 12: 3050 PubMed PMC

Yperman K, Wang J, Eeckhout D, Winkler J, Vu LD, Vandorpe M, Grones P, Mylle E, Kraus M, Merceron R et al (2021b) Molecular architecture of the endocytic TPLATE complex. Sci Adv 7: eabe7999 PubMed PMC

Zhang Y, Persson S, Hirst J, Robinson MS, Van Damme D, Sanchez‐Rodriguez C (2015) Change your TPLATE, change your fate: plant CME and beyond. Trends Plant Sci 20: 41–48 PubMed

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