Auxin and the Maintenance of Root Stem Cell Niches in Plants

doi:10.11983/CBB17130

Abstract

Abstract: The coordination between the maintenance of stem-cell niches and differentiation of their progeny sets the developmental basis of higher multiple-cellular organisms to ensure coherent organ growth. The plant hormone auxin plays important roles in the morphological establishment of shoot and root apical meristem mediated by the maintenance of shoot and root stem-cell niches. Here we review multiple signaling modules discovered in recent years, including the PLETHORA pathway, SCARECROW-SHORT ROOT pathway and environmental factors, for their mechanisms in maintaining root stem cell niches. Auxin participates in these mechanisms by regulating local synthesis, polar transport and signal transduction. By these means, auxin concentration gradient can be maintained accurately in stem-cell niches around the root apical quiescent center, for balancing the proliferation and differentiation of stem-cell niches.

Key words: root apical meristem, stem cell niche, auxin, proliferation and differentiation

Qianqian Zhang, Tong Zheng, Qian Yu, Lei Ge. Auxin and the Maintenance of Root Stem Cell Niches in Plants[J]. Chinese Bulletin of Botany, 2018, 53(1): 126-138.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB17130

https://www.chinbullbotany.com/EN/Y2018/V53/I1/126

Figures/Tables 2

Figure 1 The root apical and the stem cell niche structure of Arabidopsis thalianaRadial pattern of cell layers in root apical meristem (RAM) from central to outsides: stele (STELE), endodermis (EN), cortex (CO), epidermis (EP), lateral root cap (LRC), quiescent center (QC), columella (Col), columella stem cell (CSC), cortex/endodermal initial/daughter cell (CEI/CEID), epidermis/later root cap (EP/LRC), EP/LRC initiation cell and stele initiation cells. Thick white line surrounds root stem cells, QC (green), CSC (light blue), CEI/CEID (light purple), EP/LRC initiation cell (rose red) and stele initiation cell (dark green).

Figure 2 The regulation network for maintenance of the root stem cell nicheThe two major pathways for root stem cell niche maintenance: PLT pathway and SHR-SCR pathway. PLTs protein gradient (density of red triangles) and auxin concentration gradient (density of purple circles) maintain the activity of stem cell niche; BIRDs proteins are involved in repressing the transfer of SHR from endodermis to cortex cells, and work with SCR protein to define the boundary between endodermis and cortex. WOX5 not only maintains the stability of QC, but also repress the activity of CDF4 in CSC cells to maintain the acti- vity of stem cells. CLE40 restricts the expression of WOX5 in QC through binding to ACR4.And the expression of ARF10 and ARF16 has the same effect on WOX5. QC cells are co- lored in orange, cortex cells are colored in light yellow, and endodermis cells are colored in light red; black arrow represents promoted function; ⊥ represents inhibited function; red dotted arrow represents protein movement between cells.

References 63

[1]	于倩倩, 孔祥培, 丁兆军 (2015). 中国科学家在生长素信号转导领域取得突破性研究进展. 植物学报 50, 535-537.
[2]	于燕杰, 张大兵, 袁政 (2016). WOX蛋白家族调控干细胞发育分子机制的研究进展. 植物学报 51, 565-574.
[3]	Adamowski M, Friml J (2015). PIN-dependent auxin trans- port: action, regulation, and evolution.Plant Cell 27, 20-32.
[4]	Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004). ThePLETHORA genes mediate patterning of the Arabi- dopsis root stem cell niche. Cell 119, 109-120.
[5]	Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.Nature 433, 39-44.
[6]	Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang LM, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002). Ectopic expression of BABY BOOM triggers a con- version from vegetative to embryonic growth.Plant Cell 14, 1737-1749.
[7]	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.
[8]	Chen QG, Dai XH, De-Paoli H, Cheng YF, Takebayashi Y, Kasahara H, Kamiya Y, Zhao YD (2014a). Auxin over- production in shoots cannot rescue auxin deficiencies in Arabidopsis roots.Plant Cell Physiol 55, 1072-1079.
[9]	Chen X, Grandont L, Li HJ, Hauschild R, Paque S, Abuzeineh A, Rakusová H, Benkova E, Perrot-Rech- enmann C, Friml J (2014b). Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules.Nature 516, 90-93.
[10]	Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R, Zamioudis C, Miskolczi P, Nieuwland J, Benjamins R, Dhonukshe P, Caballero-Pérez J, Horv- ath B, Long YC, Mähönen AP, Zhang HT, Xu J, Murray JAH, Benfey PN, Bako L, Marée AFM, Scheres B (2012). A bistable circuit involving SCARECROW-RET- INOBLASTOMA integrates cues to inform asymmetric stem cell division.Cell 150, 1002-1015.
[11]	Cruz-Ramírez A, Díaz-Triviño S, Wachsman G, Du Y, Arteága-Vázquez M, Zhang H, Benjamins R, Blilou I, Neef AB, Chandler V, Scheres B (2013). A SCARE- CROW-RETINOBLASTOMA protein network controls pro- tective quiescence in the Arabidopsis root stem cell organizer.PLoS Biol 11, e1001724.
[12]	Cui HC, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007). An evolutionarily conserved mechanism delimiting SHR movement deﬁnes a single layer of endodermis in plants. Science 316, 421-425.
[13]	De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jürgens G, Ingram GC, Inzé D, Benfey PN, Beeckman T (2008). Receptor-like kinase ACR4 restricts formative cell divisions in the Ara- bidopsis root.Science 322, 594-597.
[14]	Dello Ioio R, Linhares FS, Scacchi E, Casamitjana- Martinez E, Heidstra R, Costantino P, Sabatini S (2007). Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation.Curr Biol 17, 678-682.
[15]	Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Tani- guchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008). A genetic framework for the control of cell division and differentiation in the root meristem.Science 322, 1380-1384.
[16]	Dharmasiri N, Dharmasiri S, Estelle M (2005a). The F-box protein TIR1 is an auxin receptor.Nature 435, 441-445.
[17]	Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b). Plant development is regulated by a family of auxin receptor F box proteins.Dev Cell 9, 109-119.
[18]	Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996). TheSCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423-433.
[19]	Ding ZJ, Friml J (2010). Auxin regulates distal stem cell differentiation in Arabidopsis roots.Proc Natl Acad Sci USA 107, 12046-12051.
[20]	Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993). Cellular organisation of theArabidopsis thaliana root. Development 119, 71-84.
[21]	Forzani C, Aichinger E, Sornay E, Willemsen V, Laux T, Dewitte W, Murray JAH (2014). WOX5 suppressesCYC- LIN D activity to establish quiescence at the center of the root stem cell niche. Curr Biol 24, 1939-1944.
[22]	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 de- velopment.Nature 449, 1053-1057.
[23]	Gao YB, Zhang Y, Zhang D, Dai XH, Estelle M, Zhao YD (2015). Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development.Proc Natl Acad Sci USA 112, 2275-2280.
[24]	Gutierrez C (2005). Coupling cell proliferation and develop- ment in plants.Nat Cell Biol 7, 535-541.
[25]	Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000). TheSHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555-567.
[26]	Heyman J, Cools T, Vandenbussche F, Heyndrickx KS, Van Leene J, Vercauteren I, Vanderauwera S, Van- depoele K, De Jaeger G, Van Der Straeten D, De Veylder L (2013). ERF115 controls root quiescent center cell division and stem cell replenishment.Science 342, 860-863.
[27]	Hong JH, Savina M, Du J, Devendran A, Ramakanth KK, Tian X, Sim WS, Mironova VV, Xu J (2017). A sacrifice- for-survival mechanism protects root stem cell niche from chilling stress.Cell 170, 102-113.
[28]	Hwang I, Sheen J, Müller B (2012). Cytokinin signaling networks.Annu Rev Plant Biol 63, 353-380.
[29]	Korasick DA, Westfall CS, Lee SG, Nanao MH, Dumas R, Hagen G, Guilfoyle TJ, Jez JM, Strader LC (2014). Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression.Proc Natl Acad Sci USA 111, 5427-5432.
[30]	Laux T, Würschum T, Breuninger H (2004). Genetic regula- tion of embryonic pattern formation.Plant Cell 16(Suppl), S190-S202.
[31]	Long YC, Smet W, Cruz-Ramírez A, Castelijns B, de Jonge W, Mähönen AP, Bouchet BP, Perez GS, Akh- manova A, Scheres B, Blilou I (2015). Arabidopsis BIRD zinc finger proteins jointly stabilize tissue boundaries by confining the cell fate regulator SHORT-ROOT and con- tributing to fate specification.Plant Cell 27, 1185-1199.
[32]	Mähönen AP, Tusscher KT, Siligato R, Smetana O, Díaz-Triviño S, Salojärvi J, Wachsman G, Prasad K, Heidstra R, Scheres B (2014). PLETHORA gradient formation mechanism separates auxin responses.Nature 515, 125-129.
[33]	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.
[34]	Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998). Role ofWUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815.
[35]	Mockaitis K, Estelle M (2008). Auxin receptors and plant development: a new signaling paradigm.Annu Rev Cell Dev Biol 24, 55-80.
[36]	Moreno-Risueno MA, Sozzani R, Yardımcı GG, Petricka JJ, Vernoux T, Blilou I, Alonso J, Winter CM, Ohler U, Scheres B, Benfey PN (2015). Transcriptional control of tissue formation throughout root development.Science 350, 426-430.
[37]	Moubayidin L, Di Mambro R, Sozzani R, Pacifici E, Salvi E, Terpstra I, Bao DP, van Dijken A, Dello Ioio R, Perilli S, Ljung K, Benfey PN, Heidstra R, Costantino P, Sabatini S (2013). Spatial coordination between stem cell activity and cell differentiation in the root meristem.Dev Cell 26, 405-415.
[38]	Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010). The rate of cell diffe- rentiation controls the Arabidopsis root meristem growth phase.Curr Biol 20, 1138-1143.
[39]	Nanao MH, Vinos-Poyo T, Brunoud G, Thévenon E, Mazzoleni M, Mast D, Lainé S, Wang SC, Hagen G, Li HB, Guilfoyle TJ, Parcy F, Vernoux T, Dumas R (2014). Structural basis for oligomerization of auxin transcriptional regulators.Nat Commun 5, 3617.
[40]	Ortega-Martínez O, Pernas M, Carol RJ, Dolan L (2007). Ethylene modulates stem cell division in theArabidopsis thaliana root. Science 317, 507-510.
[41]	Paque S, Mouille G, Grandont L, Alabadí D, Gaertner C, Goyallon A, Muller P, Primard-Brisset C, Sormani R, Blázquez MA, Perrot-Rechenmann C (2014). AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in Arabidopsis. Plant Cell 26, 280-295.
[42]	Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009). Complex regulation of the TIR1/AFB family of auxin receptors.Proc Natl Acad Sci USA 106, 22540-22545.
[43]	Pi LM, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D, Hennig L, Groot E, Laux T (2015). Organizer- derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression ofCDF4 expres- sion. Dev Cell 33, 576-588.
[44]	Rademacher EH, Lokerse AS, Schlereth A, Llavata-Peris CI, Bayer M, Kientz M, Freire Rios A, Borst JW, Lukowitz W, Jürgens G, Weijers D (2012). Different auxin response machineries control distinct cell fates in the early plant embryo.Dev Cell 22, 211-222.
[45]	Santuari L, Sanchez-Perez GF, Luijten M, Rutjens B, Terpstra I, Berke L, Gorte M, Prasad K, Bao DP, Timmermans-Hereijgers JLPM, Maeo K, Nakamura K, Shimotohno A, Pencik A, Novak O, Ljung K, van Heesch S, de Bruijn E, Cuppen E, Willemsen V, Mähönen AP, Lukowitz W, Snel B, de Ridder D, Scheres B, Heidstra R (2016). ThePLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots. Plant Cell 28, 2937-2951.
[46]	Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashi- moto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007). Conserved factors regulate signaling inArabi- dopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814.
[47]	Schlereth A, Moller B, Liu WL, Kientz M, Flipse J, Rade- macher EH, Schmid M, Jürgens G, Weijers D (2010). MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor.Nature 464, 913-916.
[48]	Schnittger A, Schöbinger U, Stierhof YD, Hülskamp M (2002). Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes.Curr Biol 12, 415-420.
[49]	Sena G, Wang XN, Liu HY, Hofhuis H, Birnbaum KD (2009). Organ regeneration does not require a functional stem cell niche in plants.Nature 457, 1150-1153.
[50]	Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JAH, Benfey PN (2010). Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth.Nature 466, 128-132.
[51]	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.
[52]	Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Gälweiler L, Palme K, Jürgens G (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF.Science 286, 316-318.
[53]	Tian HY, Wabnik K, Niu TT, Li HB, Yu QQ, Pollmann S, Vanneste S, Govaerts W, Rolčík J, Geisler M, Friml J, Ding ZJ (2014). WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis.Mol Plant 7, 277-289.
[54]	Tromas A, Paque S, Stierlé V, Quettier AL, Muller P, Lechner E, Genschik P, Perrot-Rechenmann C (2013). Auxin-binding protein 1 is a negative regulator of the SCF (TIR1/AFB) pathway.Nat Commun 4, 2496.
[55]	Vilarrasa-Blasi J, González-García MP, Frigola D, Fàbre- gas N, Alexiou KG, López-Bigas N, Rivas S, Jauneau A, Lohmann JU, Benfey PN, Ibañes, Caño-Delgado AI (2014). Regulation of plant stem cell quiescence by a brassinosteroid signaling module.Dev Cell 30, 36-47.
[56]	Wang RH, Estelle M (2014). Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway.Curr Opin Plant Biol 21, 51-58.
[57]	Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B (2007). Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action.Genes Dev 21, 2196-2204.
[58]	Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005). TheRETINOBLA- STOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337-1349.
[59]	Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006). A molecular framework for plant regeneration.Science 311, 385-388.
[60]	Xu TD, Dai N, Chen JS, Nagawa S, Cao M, Li HJ, Zhou ZM, Chen X, De Rycke R, Rakusova H, Wang WY, Jones AM, Friml J, Patterson SE, Bleecker AB, Yang Z (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling.Science 343, 1025-1028.
[61]	Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M (2009). TheTRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol 151, 168-179.
[62]	Zhang HM, Han W, De Smet I, Talboys P, Loya R, Hassan A, Rong HL, Jurgens G, Paul Knox J, Wang MH (2010). ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis pri- mary root meristem.Plant J 64, 764-774.
[63]	Zhou WK, Wei LR, Xu J, Zhai QZ, Jiang HL, Chen R, Chen Q, Sun JQ, Chu JF, Zhu LH, Liu CM, Li CY (2010). Arabidopsis tyrosylprotein sulfotransferase acts in the au- xin/PLETHORA pathway in regulating postembryonic main- tenance of the root stem cell niche.Plant Cell 22, 3692-3709.