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Receptor-like protein kinase-mediated signaling in controlling root meristem homeostasis

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Abstract

Generation of the root greatly benefits higher plants living on land. Continuous root growth and development are achieved by the root apical meristem, which acts as a reservoir of stem cells. The stem cells, on the one hand, constantly renew themselves through cell division. On the other hand, they differentiate into functional cells to form diverse tissues of the root. The balance between the maintenance and consumption of the root apical meristem is governed by cell-to-cell communications. Receptor-like protein kinases (RLKs), a group of signaling molecules localized on the cell surface, have been implicated in sensing multiple endogenous and environmental signals for plant development and stress adaptation. Over the past two decades, various RLKs and their ligands have been revealed to participate in regulating root meristem homeostasis. In this review, we focus on the recent studies about RLK-mediated signaling in regulating the maintenance and consumption of the root apical meristem.

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References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    CAS  PubMed  Google Scholar 

  • Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104:18333–18338

    CAS  PubMed  PubMed Central  Google Scholar 

  • An Z, Liu Y, Ou Y, Li J, Zhang B, Sun D, Sun Y, Tang W (2018) Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance. Proc Natl Acad Sci USA 115:1123–1128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anne P, Hardtke CS (2018) Phloem function and development-biophysics meets genetics. Curr Opin Plant Biol 43:22–28

    CAS  PubMed  Google Scholar 

  • 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:dev162354

    PubMed  PubMed Central  Google Scholar 

  • Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN, Sawa S, Fukuda H, von Wiren N, Takahashi H (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029–2034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berckmans B, Kirschner G, Gerlitz N, Stadler R, Simon R (2020) CLE40 signaling regulates root stem cell fate. Plant Physiol 182:1776–1792

    CAS  PubMed  Google Scholar 

  • Betsuyaku S, Sawa S, Yamada M (2011) The function of the CLE peptides in plant development and plant–microbe interactions. Arabidopsis Book 9:e0149

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Breda AS, Hazak O, Hardtke CS (2017) Phosphosite charge rather than shootward localization determines OCTOPUS activity in root protophloem. Proc Natl Acad Sci USA 114:5721–5730

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Casamitjana-Martinez E, Hofhuis HF, Xu J, Liu C-M, Heidstra R, Scheres B (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol 13:1435–1441

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cock JM, McCormick S (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol 126:939–942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Hu C, Zhu Y, Cheng K, Li X, Wei Z, Xue L, Lin F, Shi H, Yi J et al (2018) CIK receptor kinases determine cell fate specification during early anther development in Arabidopsis. Plant Cell 30:2383–2401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czyzewicz N, Shi CL, Vu LD, Van De Cotte B, Hodgman C, Butenko MA, De Smet I (2015) Modulation of Arabidopsis and monocot root architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 peptide. J Exp Bot 66:5229–5243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS (2013) Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc Natl Acad Sci USA 110:7074–7079

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM (2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2 dependent pathway. Plant Cell 17:2542–2553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer U, Kucukoglu M, Helariutta Y, Bhalerao RP (2019) The dynamics of cambial stem cell activity. Annu Rev Plant Biol 70:293–319

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Gujas B, Kastanaki E, Sturchler A, Cruz TMD, Ruiz-Sola MA, Dreos R, Eicke S, Truernit E, Rodriguez-Villalon A (2020) A reservoir of pluripotent phloem cells safeguards the linear developmental trajectory of protophloem sieve elements. Curr Biol 30:755–766

    CAS  PubMed  Google Scholar 

  • Gutierrez-Alanis D, Yong-Villalobos L, Jimenez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, Mora-Macias J, Sanchez-Rodriguez F, Cruz-Ramirez A, Herrera-Estrella L (2017) Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev Cell 41:555–570

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hobe M, Müller 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 213:371–438

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Je BI, Gruel J, Lee YK, Bommert P, Arevalo ED, Eveland AL, Wu Q, Goldshmidt A, Meeley R, Bartlett M et al (2016) Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits. Nat Genet 48:785–791

    CAS  PubMed  Google Scholar 

  • Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, Meyerowitz EM, Feldman LJ et al (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154:1721–1736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang YH, Hardtke CS (2016) Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling. EMBO Rep 17:1145–1154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang YH, Breda A, Hardtke CS (2017) Brassinosteroid signaling directs formative cell divisions and protophloem differentiation in Arabidopsis root meristems. Development 144:272–280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106:15067–15072

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kutschmar A, Rzewuski G, Stuhrwohldt N, Beemster GT, Inze D, Sauter M (2009) PSK-α promotes root growth in Arabidopsis. New Phytol 181:820–831

    CAS  PubMed  Google Scholar 

  • Lenhard M (2003) Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development 130:3163–3173

    CAS  PubMed  Google Scholar 

  • Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938

    CAS  PubMed  Google Scholar 

  • Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222

    CAS  PubMed  Google Scholar 

  • Li S, Yamada M, Han X, Ohler U, Benfey PN (2016) High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation. Dev Cell 39:508–522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Cai Z, Wang X, Li M, Cui Y, Cui N, Yang F, Zhu M, Zhao J, Du W et al (2019) SERK receptor-like kinases control division patterns of vascular precursors and ground tissue stem cells during embryo development in Arabidopsis. Mol Plant 12:984–1002

    CAS  PubMed  Google Scholar 

  • Lin G, Zhang L, Han Z, Yang X, Liu W, Li E, Chang J, Qi Y, Shpak ED, Chai J (2017) A receptor-like protein acts as a specificity switch for the regulation of stomatal development. Genes Dev 31:927–938

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Xu G, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21:1017–1033

    CAS  PubMed  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93:7623–7627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472

    CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067

    CAS  PubMed  Google Scholar 

  • Meng X, Chen X, Mang H, Liu C, Yu X, Gao X, Torii KU, He P, Shan L (2015) Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr Biol 25:2361–2372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Zhou J, Tang J, Li B, de Oliveira MV, Chai J, He P, Shan L (2016) Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–1338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol 49:1752–1757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946

    PubMed  PubMed Central  Google Scholar 

  • Oehlenschlæger CB, Gersby LBA, Ahsan N, Pedersen JT, Kristensen A, Solakova TV, Thelen JJ, Fuglsang AT (2017) Activation of the LRR receptor-like kinase PSY1R requires transphosphorylation of residues in the activation loop. Front Plant Sci 8:2005

    PubMed  PubMed Central  Google Scholar 

  • Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y (2017) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat Plants 3:17029

    CAS  PubMed  Google Scholar 

  • Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC–MS-based structure analysis. Plant J 55:152–160

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ota R, Ohkubo Y, Yamashita Y, Ogawa-Ohnishi M, Matsubayashi Y (2020) Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis. Nat Commun 11:641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ou Y, Lu X, Zi Q, Xun Q, Zhang J, Wu Y, Shi H, Wei Z, Zhao B, Zhang X et al (2016) RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res 26:686–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15:17–23

    CAS  PubMed  Google Scholar 

  • Racolta A, Nodine MD, Davies K, Lee C, Rowe S, Velazco Y, Wellington R, Tax FE (2018) A common pathway of root growth control and response to CLE peptides through two receptor kinases in Arabidopsis. Genetics 208:687–704

    CAS  PubMed  Google Scholar 

  • Ren SC, Song XF, Chen WQ, Lu R, Lucas WJ, Liu CM (2019) CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex. J Integr Plant Biol 61:1043–1061

    CAS  PubMed  Google Scholar 

  • Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P, Depuydt S, Hardtke CS (2014) Molecular genetic framework for protophloem formation. Proc Natl Acad Sci USA 111:11551–11556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shimizu N, Ishida T, Yamada M, Shigenobu S, Tabata R, Kinoshita A, Yamaguchi K, Hasebe M, Mitsumasu K, Sawa S (2015) BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol 208:1104–1113

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y (2016) Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. Proc Natl Acad Sci USA 113:3897–3902

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293

    CAS  PubMed  Google Scholar 

  • Song W, Liu L, Wang J, Wu Z, Zhang H, Tang J, Lin G, Wang Y, Wen X, Li W et al (2016) Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res 26:674–685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sozzani R, Iyer-Pascuzzi A (2014) Postembryonic control of root meristem growth and development. Curr Opin Plant Biol 17:7–12

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y (2014) Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–346

    CAS  PubMed  Google Scholar 

  • Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–238

    CAS  PubMed  Google Scholar 

  • Tamaki T, Betsuyaku S, Fujiwara M, Fukao Y, Fukuda H, Sawa S (2013) SUPPRESSOR OF LLP1 1-mediated C-terminal processing is critical for CLE19 peptide activity. Plant J 76:970–981

    CAS  PubMed  Google Scholar 

  • Truernit E, Bauby H, Belcram K, Barthelemy J, Palauqui JC (2012) OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306–1315

    CAS  PubMed  Google Scholar 

  • van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287–289

    PubMed  Google Scholar 

  • Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118–1122

    CAS  PubMed  Google Scholar 

  • Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015) Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–268

    CAS  PubMed  Google Scholar 

  • Wang P, Hsu CC, Du Y, Zhu P, Zhao C, Fu X, Zhang C, Paez JS, Macho AP, Tao WA et al (2020) Mapping proteome-wide targets of protein kinases in plant stress responses. Proc Natl Acad Sci USA 117:3270–3280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Liberatore KL, MacAlister CA, Huang Z, Chu YH, Jiang K, Brooks C, Ogawa-Ohnishi M, Xiong G, Pauly M et al (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47:784–792

    CAS  PubMed  Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada M, Han X, Benfey PN (2020) RGF1 controls root meristem size through ROS signalling. Nature 577:85–88

    CAS  PubMed  Google Scholar 

  • Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi YL, Ishida T, Yoshimura M, Imamura Y, Shimaoka C, Sawa S (2017) A collection of mutants for CLE-peptide-encoding genes in Arabidopsis generated by CRISPR/Cas9-mediated gene targeting. Plant Cell Physiol 58:1848–1856

    CAS  PubMed  Google Scholar 

  • Yue K, Sandal P, Williams EL, Murphy E, Stes E, Nikonorova N, Ramakrishna P, Czyzewicz N, Montero-Morales L, Kumpf R et al (2016) PP2A-3 interacts with ACR4 and regulates formative cell division in the Arabidopsis root. Proc Natl Acad Sci USA 113:1447–1452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang TQ, Xu ZG, Shang GD, Wang JW (2019) A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol Plant 12:648–660

    CAS  PubMed  Google Scholar 

  • Zhou W, Wei L, Xu J, Zhai Q, Jiang H, Chen R, Chen Q, Sun J, Chu J, Zhu L et al (2010) Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22:3692–3709

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by National Natural Science Foundation of China (31770312 and 31970339), and Fundamental Research Funds for the Central Universities (lzujbky-2019-ct04 and lzujbky-2020-kb05).

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  1. Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, 730000, China

    Yafen Zhu, Chong Hu & Xiaoping Gou

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  1. Yafen Zhu
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Zhu, Y., Hu, C. & Gou, X. Receptor-like protein kinase-mediated signaling in controlling root meristem homeostasis. aBIOTECH 1, 157–168 (2020). https://doi.org/10.1007/s42994-020-00024-z

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