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Genetic Mechanisms Regulating Root Cap Cell Renewal in Arabidopsis thaliana L.

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Abstract

Synchronization of spatially separated processes of cells’ division and loss is crucial in renewal and maintenance of organ and tissue structure; however, genetic mechanisms of its regulation are poorly understood. In plants, root cap located at the root tip is quickly renewed protecting the stem cell niche against mechanical injury and performing some other important functions. In spite of continuous supply and differentiation of daughter cells from division of initials (stem cells), the root cap size does not increase because of regular sloughing of differentiated cells at its apex. In order to strictly maintain a permanent size of the root cap, it is important to synchronize divisions of stem cells with removal of the outer cell layer. In Arabidopsis thaliana, which is a model species in plant genetics, root cap structure is plain and well-ordered, and old cells are sloughed as a whole layer; that is why this species is a convenient object for investigation of the mechanisms responsible for root cap renewal. It this review, we will consider maintenance of root cap structure and size in A. thaliana and discuss the data concerning genetic control over this process and promising research avenues in this area.

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REFERENCES

  1. Ganesh, A., Shukla, V., Mohapatra, A., George, A, p., Bhukya, D.P.N., Das, K.K., Kola, V.S.R., Suresh, A., and Ramireddy, E., Root cap to soil interface: A driving force toward plant adaptation and development, Plant Cell Physiol., 2022, vol. 638, p. 1038. https://doi.org/10.1093/pcp/pcac078

    Article  CAS  Google Scholar 

  2. Arnaud, C., Bonnot, C., Desnos, T., and Nussaume, L., The root cap at the forefront, C. R. Biol., 2010, vol. 333, p. 335. https://doi.org/10.1016/j.crvi.2010.01.011

    Article  CAS  PubMed  Google Scholar 

  3. Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K., and Scheres, B., Cellular organisation of the Arabidopsis thaliana root, Development, 1993, vol. 119, p. 71. https://doi.org/10.1242/dev.119.1.71

    Article  CAS  PubMed  Google Scholar 

  4. Fendrych, M., Hautegem, T.V., Durme, M.V. Olvera-Carrillo, Y., Huysmans, M., Karimi, M., Lippens, S., Guérin, C.J., Krebs, M., Schumacher, K., and Nowack, M.K., Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis, Curr. Biol., 2014, vol. 24, p. 931. https://doi.org/10.1016/J.CUB.2014.03.025

    Article  CAS  PubMed  Google Scholar 

  5. Bennett, T., van den Toorn, A., Willemsen, V., and Scheres, B., Precise control of plant stem cell activity through parallel regulatory inputs, Development, 2014, vol. 141, p. 4055. https://doi.org/10.1242/DEV.110148

    Article  CAS  PubMed  Google Scholar 

  6. Sack, F.D. and Kiss, J.Z., Root cap structure in wild type and in a starchless mutant of Arabidopsis, Am. J. Bot., 1989, vol. 76, p. 454. https://doi.org/10.1002/j.1537-2197.1989.tb11334.x

    Article  CAS  PubMed  Google Scholar 

  7. Iijima, M., Morita, S., and Barlow, P.W., Structure and function of the root cap, Plant Prod. Sci., 2008, vol. 11, p. 17. https://doi.org/10.1626/pps.11.17

    Article  Google Scholar 

  8. Maeda, K., Kunieda, T., Tamura, K., Hatano, K., Hara-Nishimura, I., and Shimada, T., Identification of periplasmic root-cap mucilage in develo** columella cells of Arabidopsis thaliana, Plant Cell Physiol., 2019, vol. 60, p. 1296. https://doi.org/10.1093/pcp/pcz047

    Article  CAS  PubMed  Google Scholar 

  9. Wenzel, C.L. and Rost, T.L., Cell division patterns of the protoderm and root cap in the “closed” root apical meristem of Arabidopsis thaliana, Protoplasma, 2001, vol. 218, p. 203. https://doi.org/10.1007/BF01306609

    Article  CAS  PubMed  Google Scholar 

  10. Campilho, A., Garcia, B., Toorn, H.V., Wijk, H.V., Campilho, A., and Scheres, B., Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem, Plant J., 2006, vol. 48, p. 619. https://doi.org/10.1111/j.1365-313X.2006.02892.x

    Article  CAS  PubMed  Google Scholar 

  11. Kumpf, R.P. and Nowack, M.K., The root cap: A short story of life and death, J. Exp. Bot., 2015, vol. 66, p. 5651. https://doi.org/10.1093/JXB/ERV295

    Article  CAS  PubMed  Google Scholar 

  12. Dubreuil, C., **, X., Grönlund, A., and Fischer, U., A Local auxin gradient regulates root cap self-renewal and size homeostasis, Curr. Biol., 2018, vol. 28, p. 2581. https://doi.org/10.1016/J.CUB.2018.05.090

    Article  CAS  PubMed  Google Scholar 

  13. Wein, A., Le Gac, A.L., and Laux, T., Stem cell ageing of the root apical meristem of Arabidopsis thaliana, Mech. Ageing Dev., 2020, vol. 190, p. 111313. https://doi.org/10.1016/j.mad.2020.111313

    Article  CAS  PubMed  Google Scholar 

  14. Shi, C.-L., von Wangenheim, D., Herrmann, U., Wildhagen, M., Kulik, I., Kopf, A., Ishida, T., Olsson, V., Anker, M.K., Albert, M., Butenko, M.A., Felix, G., Sawa, S., Claassen, M., Friml, J., and Aalen, R.B., The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling, Nat. Plants, 2018, vol. 4, p. 596. https://doi.org/10.1038/s41477-018-0212-z

    Article  CAS  PubMed  Google Scholar 

  15. Goh, T., Sakamoto, K., Wang, P., Kozono, S., Ueno, K., Miyashima, S., Toyokura, K., Fukaki, H., Kang, B.-H., and Nakajima, K., Autophagy promotes organelle clearance and organized cell separation of living root cap cells in Arabidopsis thaliana, Development, 2022, vol. 149 https://doi.org/10.1242/dev.200593

  16. Xuan, W., Band, L. R., Kumpf, R.P., Van Damme, D., Parizot, B., De Rop, G., Opdenacker, D., Möller, B. K., Skorzinski, N., Njo, M.F., De Rybel, B., Audenaert, D., Nowack, M.K., Vanneste, S., and Beeckman, T., Cyclic programmed cell death stimulates hormone signaling and root development in Arabidopsis, Science, 2016, vol. 351, p. 384. https://doi.org/10.1126/science.aad2776

    Article  CAS  PubMed  Google Scholar 

  17. Bennett, T., van den Toorn, A., Sanchez-Perez, G.F., Campilho, A., Willemsen, V., Snel, B., and Scheres, B., SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis, The Plant Cell, 2010, vol. 22, p. 640. https://doi.org/10.1105/tpc.109.072272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Willemsen, V., Bauch, M., Bennett, T., Campilho, A., Wolkenfelt, H., Xu, J., Haseloff, J. and Scheres, B., The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells, Dev. Cell, 2008, vol. 15, p. 913. https://doi.org/10.1016/j.devcel.2008.09.019

    Article  CAS  PubMed  Google Scholar 

  19. Hawes, M.C., Brigham, L.A., Wen, F., Woo, H.H., and Zhu, Y., Function of root border cells in plant health: Pioneers in the rhizosphere, Annu. Rev. Phytopathol., 1998, vol. 36, p. 311. https://doi.org/10.1146/annurev.phyto.36.1.311

    Article  CAS  PubMed  Google Scholar 

  20. Hawes, M.C., Gunawardena, U., Miyasaka, S., and Zhao, X., The role of root border cells in plant defense, Trends Plant Sci., 2000, vol. 5, p. 128. https://doi.org/10.1016/s1360-1385(00)01556-9

    Article  CAS  PubMed  Google Scholar 

  21. Vicré, M., Santaella, C., Blanchet, S., Gateau, A., and Driouich, A., Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with Rhizobacteria, Plant Physiol., 2005, vol. 138, p. 998. https://doi.org/10.1104/pp.104.051813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Hawes, M. C. Bengough, G., Cassab, G., and Ponce, G., Root caps and Rhizosphere, J. Plant Growth Regul., 2003, vol. 21, p. 352. https://doi.org/10.1007/s00344-002-0035-y

    Article  CAS  Google Scholar 

  23. Driouich, A., Durand, C., and Vicré-Gibouin, M., Formation and separation of root border cells, Trends Plant Sci., 2007, vol. 12 P. 14.

    Article  CAS  PubMed  Google Scholar 

  24. Ding, Z. and Friml, J., Auxin regulates distal stem cell differentiation in Arabidopsis roots, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, p. 12046. https://doi.org/10.1073/pnas.1000672107

    Article  PubMed  PubMed Central  Google Scholar 

  25. Hong, J. H., Chu, H., Zhang, C., Ghosh, D., Gong, X., and Xu, L., A quantitative analysis of stem cell homeostasis in the Arabidopsis columella root cap, Front. Plant Sci., 2015, vol. 6, p. 206. https://doi.org/10.3389/fpls.2015.00206

    Article  PubMed  PubMed Central  Google Scholar 

  26. Zazímalová, E., Krecek, P., Skůpa, P., Hoyerová, K., and Petrásek, J., Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins, Cell. Mol. Life Sci., 2007, vol. 64, p. 1621. https://doi.org/10.1007/s00018-007-6566-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Křeček, P., Skůpa, P., Libus, J., Naramoto, S., Tejos, R., Friml, J., and Zažímalová, E., The PIN-FORMED (PIN) protein family of auxin transporters, Genome Biol., 2009, vol. 10, p. 249. https://doi.org/10.1186/gb-2009-10-12-249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Grieneisen, V.A., Xu, J., Marée, A.F., Hogeweg, P., and Scheres, B., Auxin transport is sufficient to generate a maximum and gradient guiding root growth, Nature, 2007, vol. 449, p. 1008. https://doi.org/10.1038/nature06215

    Article  CAS  PubMed  Google Scholar 

  29. Mironova, V.V., Omelyanchuk, N.A., Yosiphon, G., Fadeev, S.I., Kolchanov, N.A., Mjolsness, E., and Likhoshvai, V.A., A plausible mechanism for auxin patterning along the develo** root, BMC Syst. Biol., 2010, vol. 4, p. 98. https://doi.org/10.1186/1752-0509-4-98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K., and Bennett, M., Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex, Genes Dev., 2001, vol.15, p. 2648. https://doi.org/10.1101/gad.210501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Band, L.R., Wells, D.M., Fozard, J.A., Ghetiu, T., French, A.P., Pound, M.P., Wilson, M.H., Yu, L., Li, W., Hijazi, H.I., Oh, J., Pearce, S.P., Perez-Amador, M.A., Yun, J., Kramer, E., et al., Systems analysis of auxin transport in the Arabidopsis root apex, Plant Cell, 2014, vol. 26, p. 862. https://doi.org/10.1105/tpc.113.119495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tian, H., Niu, T., Yu, Q., Quan, T., and Ding, Z., Auxin gradient is crucial for the maintenance of root distal stem cell identity in Arabidopsis, Plant Signal. Behav., 2013, vol. 8, p. e26429. https://doi.org/10.4161/psb.26429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Martin-Arevalillo, R. and Vernoux, T., Decoding the auxin matrix: Auxin biology through the eye of the computer, Annu. Rev. Plant Biol., 2023, vol. 74, p. 387. https://doi.org/10.1146/annurev-arplant-102720-033523

    Article  CAS  PubMed  Google Scholar 

  34. Zhang, Q., Gong, M., Xu, X., Li, H., and Deng, W., Roles of auxin in the growth, development, and stress tolerance of horticultural plants, Cells, 2022, vol. 11, p. 2761. https://doi.org/10.3390/cells11172761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Caumon, H. and Vernoux, T., A matter of time: Auxin signaling dynamics and the regulation of auxin responses during plant development, J. Exp. Bot., 2023, vol. 74, p. 3887. https://doi.org/10.1093/jxb/erad132

    Article  CAS  PubMed  Google Scholar 

  36. Tian, H., Wabnik, K., Niu, T., Li, H., Yu, Q., Pollmann, S., Vanneste, S., Govaerts, W., Rolcík, J., Geisler, M., Friml, J., and Ding, Z., WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis, Mol. Plant, 2014, vol. 7, p. 277. https://doi.org/10.1093/mp/sst118

    Article  CAS  PubMed  Google Scholar 

  37. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y. S., Amasino, R., and Scheres, B., The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche, Cell, 2004, vol. 119, p. 109. https://doi.org/10.1016/j.cell.2004.09.018

    Article  CAS  PubMed  Google Scholar 

  38. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., and Scheres, B., The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots, Nature, 2005, vol. 433, p. 39. https://doi.org/10.1038/nature03184

    Article  CAS  PubMed  Google Scholar 

  39. Cruz-Ramírez, A., Díaz-Triviño, S., Blilou, I., Grieneisen, V.A., Sozzani, R., Zamioudis, C., Miskolczi, P., Nieuwland, J., Benjamins, R., Dhonukshe, P., Caballero-Pérez, J., Horvath, B., Long, Y., Mähönen, A.P., Zhang, H., et al., A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division, Cell, 2012, vol. 150, p. 1002. https://doi.org/10.1016/j.cell.2012.07.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yang, W., Cortijo, S., Korsbo, N., Roszak, P., Schiessl, K., Gurzadyan, A., Wightman, R., Jönsson, H., and Meyerowitz, E., Molecular mechanism of cytokinin-activated cell division in Arabidopsis, Science, 2021, vol. 371, p. 1350. https://doi.org/10.1126/science.abe2305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Svolacchia, N. and Sabatini, S., Cytokinins, Curr. Biol., 2023, vol. 33, p. 10. https://doi.org/10.1016/j.cub.2022.11.022

    Article  CAS  Google Scholar 

  42. Antoniadi, I., Plačková, L., Simonovik, B., Doležal, K., Turnbull, C., Ljung, K., and Novák, O., Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex, Plant Cell, 2015, vol. 27, p. 1955. https://doi.org/10.1105/tpc.15.00176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Stolz, A., Riefler, M., Lomin, S. N., Achazi, K., Romanov, G. A., and Schmülling, T., The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors, Plant J., 2011, vol. 67, p. 157. https://doi.org/10.1111/j.1365-313X.2011.04584.x

    Article  CAS  PubMed  Google Scholar 

  44. Tsilimigka, F., Poulios, S., Mallioura, A., and Vlachonasios, K., ADA2b and GCN5 affect cytokinin signaling by modulating histone acetylation and gene expression during root growth of Arabidopsis thaliana, Plants, 2022, vol. 11, p. 1335. https://doi.org/10.3390/plants11101335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Antoniadi, I., Novák, O., Gelová, Z., Johnson, A., Plíhal, O., Simerský, R., Mik, V., Vain, T., Mateo-Bonmatí, E., Karady, M., Pernisova, M., Plačková, L., Opassathian, K., Hejátko, J., Friml, J., et al., Cell-surface receptors enable perception of extracellular cytokinins, Nat. Commun., 2020, vol. 11, p. 4284. https://doi.org/10.1101/726125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Di Mambro, R., Svolacchia, N., Ioio, R. D., Pierdonati, E., Salvi, E., Pedrazzini, E., Vitale, A., Perilli, S., Sozzani, R., Benfey, P.N., Busch, W., Costantino, P., and Sabatini, S., The lateral root cap acts as an auxin sink that controls meristem size, Curr. Biol., 2019, vol. 29, p. 1199. https://doi.org/10.1016/j.cub.2019.02.022

    Article  CAS  PubMed  Google Scholar 

  47. Wang, Z., Rong, D., Chen, D., **ao, Y., Liu, R., Wu, S., and Yamamuro, C., Salicylic acid promotes quiescent center cell division through ROS accumulation and down-regulation of PLT1, PLT2, and WOX5, J. Integr. Plant Biol., 2021, vol. 63, p. 583. https://doi.org/10.1111/jipb.13020

    Article  CAS  PubMed  Google Scholar 

  48. Pasternak, T., Groot, E.P., Kazantsev, F.V., Teale, W., Omelyanchuk, N., Kovrizhnykh, V., Palme, K., and Mironova, V.V., Salicylic acid affects root meristem patterning via auxin distribution in a concentration-dependent manner, Plant Physiol., 2019, vol. 180, p. 1725. https://doi.org/10.1104/pp.19.00130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ke, M., Ma, Z., Wang, D., Sun, Y., Wen, C., Huang, D., Chen, Z., Yang, L., Tan, S., Li, R., Friml, J., Miao, Y., and Chen, X., Salicylic acid regulates PIN2 auxin transporter hyperclustering and root gravitropic growth via Remorin-dependent lipid nanodomain organisation in Arabidopsis thaliana, New Phytol., 2021, vol. 229, p. 963. https://doi.org/10.1111/nph.16915

    Article  CAS  PubMed  Google Scholar 

  50. Armengot, L., Marquès-Bueno, M.M., Soria-Garcia, A., Müller, M., Munné-Bosch, S., and Martínez, M.C., Functional interplay between protein kinase CK 2 and salicylic acid sustains PIN transcriptional expression and root development, Plant J., 2014, vol. 78, p. 411. https://doi.org/10.1111/tpj.12481

    Article  CAS  PubMed  Google Scholar 

  51. Gonzalez-García, M.P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-García, S., Russinova, E., and Caño-Delgado, A.I., Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots, Development, 2011, vol. 138, p. 849. https://doi.org/10.1242/dev.057331

    Article  CAS  PubMed  Google Scholar 

  52. Lee, H.S., Kim, Y., Pham, G., Kim, J.W., Song, J.H., Lee, Y., Hwang, Y.-S., Roux, S.J., and Kim, S.H., Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation, J. Exp. Bot., 2015, vol. 66, p. 4835. https://doi.org/10.1093/jxb/erv316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Wei, Z. and Li, J., Brassinosteroids regulate root growth, development, and symbiosis, Mol. Plant, 2016, vol. 9, p. 86. https://doi.org/10.1016/j.molp.2015.12.00

    Article  CAS  PubMed  Google Scholar 

  54. Chen, Q., Sun, J., Zhai, Q., Zhou, W., Qi, L., Xu, L., Wang, B., Chen, R., Jiang, H., Qi, J., Li, X., Palme, K., and Li, C., The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis, Plant Cell, 2011, vol. 23, p. 3335. https://doi.org/10.1105/tpc.111.089870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Christmann, A., Hoffmann, T., Teplova, I., Grill, E., and Muller, A., Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis, Plant Physiol., 2005, vol. 137, p. 209. https://doi.org/10.1104/pp.104.053082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhang, H., Han, W., De Smet, I., Talboys, P., Loya, R., Hassan, A., Rong, H., Jürgens, G., Knox, J.P., and Wang, M.H., ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem, Plant J., 2010, vol. 64, p. 764. https://doi.org/10.1111/j.1365-313X.2010.04367.x

    Article  CAS  PubMed  Google Scholar 

  57. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Sheres, B., Heidstra, R., and Laux, T., Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers, Nature, 2007, vol. 446, p. 811. https://doi.org/10.1038/nature05703

    Article  CAS  PubMed  Google Scholar 

  58. Hardtke, C.S. and Berleth, T., The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development, EMBO J., 1998, vol. 17, p. 1405. https://doi.org/10.1093/emboj/17.5.1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Tsuchisaka, A. and Theologis, A., Unique and overlap** expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members, Plant Physiol., 2004, vol. 136, p. 2982. https://doi.org/10.1104/pp.104.049999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M. J., Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation, Plant Cell, 2007, vol. 19, p. 2186. https://doi.org/10.1105/tpc.107.052100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Li, G., Zhu, C., Gan, L., Ng, D., and **a, K., GA 3 enhances root responsiveness to exogenous IAA by modulating auxin transport and signalling in Arabidopsis, Plant Cell Rep., 2015, vol. 34, p. 483. https://doi.org/10.1007/s00299-014-1728-y

    Article  CAS  PubMed  Google Scholar 

  62. Forzani, C., Aichinger, E., Sornay, E., Willemsen, V., Laux, T., Dewitte, W., and Murray, J.A., WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche, Curr. Biol., 2014, vol. 24, p. 1939. https://doi.org/10.1016/j.cub.2014.07.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Berckmans, B., Kirschner, G., Gerlitz, N., Stadler, R., and Simon, R., CLE40 signaling regulates root stem cell fate, Plant Physiol., 2020 V. 182, p. 1776. https://doi.org/10.1104/pp.19.00914

    Article  CAS  PubMed  Google Scholar 

  64. Pi, L., Aichinger, E., van der Graaff, E., Llavata-Peris, C.I., Weijers, D., Hennig, L., Groot, E., and Laux, T., Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression, Dev. Cell, 2015, vol. 33, p. 576. https://doi.org/10.1016/j.devcel.2015.04.024

    Article  CAS  PubMed  Google Scholar 

  65. Stahl, Y., Wink, R.H., Ingram, G.C., and Simon, R., A signaling module controlling the stem cell niche in Arabidopsis root meristems, Curr. Biol., 2009, vol. 19, p. 909. https://doi.org/10.1016/j.cub.2009.03.060

    Article  CAS  PubMed  Google Scholar 

  66. Zhang, L., Yang, Y., Mu, C., Liu, M., Ishida, T., Sawa, S., Zhu, Y., and Pi, L., Control of root stem cell differentiation and lateral root emergence by CLE16/17 peptides in Arabidopsis, Front. Plant Sci., 2022, vol. 13, p. 869888. https://doi.org/10.3389/fpls.2022.869888

    Article  PubMed  PubMed Central  Google Scholar 

  67. Stahl, Y., Grabowski, S., Bleckmann, A., Kühnemuth, R., Weidtkamp-Peters, S., Pinto, K.G., Kirschner, G.K., Schmid, J.B., Wink, R.H., Hülsewede, A., Felekyan, S., Seidel, C.A., and Simon, R., Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes, Curr. Biol., 2013, vol. 23, p. 362. https://doi.org/10.1016/j.cub.2013.01.045

    Article  CAS  PubMed  Google Scholar 

  68. Yue, K., Sandal, P., Williams, E. L., Murphy, E., Stes, E., Nikonorova, N., Ramakrishna, P., Czyzewicz, N., Montero-Morales, L., Kumpf, R., Lin, Z., van de Cotte, B., Iqbal, M., Van Bel, M., Van De Slijke, E., et al., PP2A-3 interacts with ACR4 and regulates formative cell division in the Arabidopsis root, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, p. 1447. https://doi.org/10.1073/pnas.1525122113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kinoshita, A., ten Hove, C. A., Tabata, R., Yamada, M., Shimizu, N., Ishida, T., Yamaguchi, K., Shigenobu, S., Takebayashi, Y., Iuchi, S, Kobayashi, M., Kurata, T., Wada, T., Seo, M., and Hasebe, M., A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem, Development, 2015, vol. 142, p. 444. https://doi.org/10.1242/dev.113167

    Article  CAS  PubMed  Google Scholar 

  70. Wang, J.W., Wang, L.J., Mao, Y.B., Cai, W.J., Xue, H.W., and Chen, X.Y., Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis, Plant Cell, 2005, vol. 17, p. 2204. https://doi.org/10.1105/TPC.105.033076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ornelas-Ayala, D., Vega-León, R., Petrone-Mendoza, E., Garay-Arroyo, A., García-Ponce, B., Álvarez-Buylla, E.R., and Sanchez, M.D.L.P., ULTRAPETALA1 maintains Arabidopsis root stem cell niche independently of ARABIDOPSIS TRITHORAX1, New Phytol., 2020, vol. 225, p. 1261. https://doi.org/10.1111/nph.16213

    Article  CAS  PubMed  Google Scholar 

  72. Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I., Korthout, H., Chatterjee, J., Mariconti, L., Gruissem, W., and Scheres, B., The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots, Cell, 2005, vol. 123, p. 1337. https://doi.org/10.1016/j.cell.2005.09.042

    Article  CAS  PubMed  Google Scholar 

  73. Kawakatsu, T., Stuart, T., Valdes, M., Breakfield, N., Schmitz, R.J., Nery, J.R., Mark, A.U., Han, X., Benfey, P.N., and Ecker, J.R., Unique cell-type-specific patterns of DNA methylation in the root meristem, Nat. Plants, 2016, vol. 2, p. 16058. https://doi.org/10.1038/nplants.2016.58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kornet, N. and Scheres, B., Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis, Plant Cell, 2009, vol. 21, p. 1070. https://doi.org/10.1105/tpc.108.065300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Ngo, A.H., Kanehara, K., and Nakamura, Y., Non-specific phospholipases C, NPC2 and NPC6, are required for root growth in Arabidopsis, Plant J., 2019, vol. 100, p. 825. https://doi.org/10.1111/tpj.14494

    Article  CAS  PubMed  Google Scholar 

  76. Lin, Y.C., Kobayashi, K., Wada, H., and Nakamura, Y., Phosphatidylglycerophosphate phosphatase is required for root growth in Arabidopsis, Biochim. Biophys. Acta, Mol. Cell Biol. Lipids, 2018, vol. 1863, p. 563. https://doi.org/10.1016/j.bbalip.2018.02.007

    Article  CAS  Google Scholar 

  77. Begum, T., Reuter, R., and Schöffl, F., Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis, Mech. Dev., 2013, vol. 130, p. 54. https://doi.org/10.1016/j.mod.2012.05.008

    Article  CAS  PubMed  Google Scholar 

  78. Cnops, G., Wang, X., Linstead, P., Montagu, M.V., Lijsebttens, M.V., and Dolan, L., Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root, Development, 2000, vol. 127, p. 3385. https://doi.org/10.1242/dev.127.15.3385

    Article  CAS  PubMed  Google Scholar 

  79. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R., and Scheres, B., PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development, Nature, 2007, vol. 449, p. 1053. https://doi.org/10.1038/nature06206

    Article  CAS  PubMed  Google Scholar 

  80. Ercoli, M.F., Ferela, A., Debernardi, J.M., Perrone, A.P., Rodriguez, R.E., and Palatnik, J.F., GIF transcriptional coregulators control root meristem homeostasis, Plant Cell, 2018, vol. 30, p. 347. https://doi.org/10.1105/tpc.17.00856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Olvera-Carrillo, Y., Van Bel, M., Van Hautegem, T., Fendrych, M., Huysmans, M., Simaskova, M., van Durme, M., Buscaill, P., Rivas, S., Coll, N.S., Coppens, F., Maere, S., and Nowack, M.K., A Conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants, Plant Physiol., 2015, vol. 169, p. 2684. https://doi.org/10.1104/pp.15.00769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Huysmans, M., Buono, R.A., Skorzinski, N., Radio, M.C., De Winter, F., Parizot, B., Mertens, J., Karimi, M., Fendrych, M., and Nowack, M.K., NAC transcription factors ANAC087 and ANAC046 control distinct aspects of programmed cell death in the Arabidopsis columella and lateral root cap, Plant Cell, 2018, vol. 30, p. 2197. https://doi.org/10.1105/tpc.18.00293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Shimamura, R., Ohashi, Y., Taniguchi, Y.Y., Kato, M., Tsuge, T., and Aoyama, T., Arabidopsis PLDζ1 and PLDζ2 localize to post-Golgi membrane compartments in a partially overlap** manner, Plant Mol. Biol., 2022, vol. 108, p. 31. https://doi.org/10.1007/s11103-021-01205-0

    Article  CAS  PubMed  Google Scholar 

  84. Møller, S.G. and McPherson, M.J., Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase, Plant J., 1998, vol. 13, p. 781. https://doi.org/10.1046/j.1365-313x.1998.00080.x

    Article  PubMed  Google Scholar 

  85. Feng, Q., Cubría-Radío, M., Vavrdová, T., De Winter, F., Schilling, N., Huysmans, M., Nanda, A.K., Melnyk, C.W., and Nowack, M.K., Repressive ZINC FINGER OF ARABIDOPSIS THALIANA proteins promote programmed cell death in the Arabidopsis columella root cap, Plant Physiol., 2023, vol. 192, p. 1151. https://doi.org/10.1093/plphys/kiad130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Durand, C., Vicré-Gibouin, M., Follet-Gueye, M.L., Duponchel, L., Moreau, M., Lerouge, P., and Driouich, A., The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan, Plant Physiol., 2009, vol. 150, p. 1411. https://doi.org/10.1104/pp.109.136382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Kamiya, M., Higashio, S.-Y., Isomoto, A., Kim, J.-M., Seki, M., Miyashima, S., and Nakajima, K., Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis, Development, 2016, vol. 143, p. 4063. https://doi.org/10.1242/dev.142331

    Article  CAS  PubMed  Google Scholar 

  88. Karve, R., Suárez-Román, F., and Iyer-Pascuzzi, A.S., The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release, Plant Physiol., 2016, vol. 171, p. 2101. https://doi.org/10.1104/pp.16.00453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Feng, Q., Rycke, R. D., Dagdas, Y., and Nowack, M.K., Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap, Curr. Biol., 2022, vol. 32, p. 4548. https://doi.org/10.1016/j.cub.2022.03.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to V.V. Lavrekha for helpful remarks.

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This work was supported by the Russian Science Foundation, project no. 20-14-00140.

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Cherenko, V.A., Omelyanchuk, N.A. & Zemlyanskaya, E.V. Genetic Mechanisms Regulating Root Cap Cell Renewal in Arabidopsis thaliana L.. Russ J Plant Physiol 71, 51 (2024). https://doi.org/10.1134/S1021443724604610

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