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Вавиловский журнал генетики и селекции

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Стволовые клетки растений: единство и многообразие

https://doi.org/10.18699/VJ16.172

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Аннотация

Стволовые клетки – недифференцированные клетки многоклеточных организмов, способные делиться, самообновляться и дифференцироваться. Несмотря на существующие различия свойств, у всех многоклеточных организмов можно выделить общие принципы существования стволовых клеток. У растений стволовые клетки находятся в меристемах – структурах, обеспечивающих непрерывный рост растения и предоставляющих материал для образования различных специализированных тканей. Выделяют разнообразные типы меристем: апикальные – побега и корня, латеральные (прокамбий, камбий, перицикл), а также так называемые нерегулярные, развивающиеся при определенных условиях (каллус, меристемы симбиотических клубеньков, спонтанные и патоген-индуцированные опухоли и т. д.). Для каждой из меристем выявлены специфические механизмы регуляции, для которых характерно взаимодействие фитогормонов и основных групп транскрипционных факторов. Активность меристем обусловлена двумя противоположных процессами: пролиферацией и самообновлением стволовых клеток в центральной части меристемы и дифференцировкой специализированных клеток на периферии. Системы WOX-CLAVATA – консервативный для разных меристем регуляторный компонент, который обеспечивает размер и постоянство состава меристемы, а также баланс пролиферации и дифференцировки стволовых клеток. В обзоре рассмотрены сходство и различие принципов организа- ции ниш стволовых клеток у растений и животных, а также в разнообразных меристемах высших растений; особое внимание уделено роли систем WOX-CLAVATA в поддержании меристем и их взаимодействию с другими меристемными регуляторами.

Об авторах

И. Е. Додуева
Санкт-Петербургский государственный университет
Россия
кафедра генетики и биотехнологии, Санкт-Петербург


В. Е. Творогова
Санкт-Петербургский государственный университет
Россия
кафедра генетики и биотехнологии, Санкт-Петербург


М. Азарахш
Санкт-Петербургский государственный университет
Россия
кафедра генетики и биотехнологии, Санкт-Петербург


М. А. Лебедева
Санкт-Петербургский государственный университет
Россия
кафедра генетики и биотехнологии, Санкт-Петербург


Л. А. Лутова
Saint Petersburg State University
Россия
кафедра генетики и биотехнологии, Санкт-Петербург


Список литературы

1. Бузовкина И.С., Лутова Л.А. Генетическая коллекция инбредных линий редиса: история и перспективы. Генетика. 2007;4: 1411-1423.

2. Виноградова А.П., Лебедева М.А., Лутова Л.А. Меристематические характеристики опухолей, индуцированных Agrobacterium tumefaciens у гороха. Генетика. 2015;51(1):54-62.

3. Додуева И.Е., Ганчева М.С., Осипова М.А., Творогова В.Е., Лутова Л.А. Латеральные меристемы высших растений: фитогормональный и генетический контроль. Физиология растений. 2014; 61(5):611-631.

4. Иванов В.Б. Проблема стволовых клеток у растений. Онтогенез. 2003;34(4):243-261.

5. Иванов В.Б. Стволовые клетки в корне и проблема стволовых клеток у растений. Онтогенез. 2007;38(6):406-419.

6. Лутова Л.А., Долгих Е.А., Додуева И.Е., Осипова М.А., Ильина Е.Л. Изучение системного контроля деления и дифференцировки клеток растений на примере опухолевого роста у редиса. Генетика. 2008;44(8):1075-1083.

7. Осипова М.А., Долгих Е.А., Лутова Л.А. Особенности экспрессии меристем-специфичного гена WOX5 при органогенезе клубеньков бобовых растений. Онтогенез. 2011;42(4):264-275.

8. Agusti J., Lichtenberger R., Schwarz M., Nehlin L., Greb T. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet. 2011;7(2):e1001312. DOI 10.1371/journal.pgen.1001312.

9. Ahuja M.R. Genetic tumors in Nicotiana and other plants. Quart. Rev. Biol. 1998;73:439-459.

10. Anzola J.M., Sieberer T., Ortbauer M., Butt H., Korbei B., Weinhofer I., Müllner A.E., Luschnig C. Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc. Natl Acad. Sci. USA. 2010; 107(22):10308-10313. DOI 10.1073/pnas.0913918107.

11. Ariel F., Brault-Hernandez M., Laffont C., Huault E., Brault M., Plet J., Moison M., Blanchet S., Ichanté J.L., Chabaud M., Carrere S., Crespi M., Chan R.L., Frugier F. Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell Online. 2012;24(9):3838-3852. DOI 10.1105/tpc.112.103267.

12. Atta R., Laurens L., Boucheron-Dubuisson E., Guivarc’h A., Carnero E., Giraudat-Pautot V., Rech P., Chriqui D. Pluripotency of Arabidopsis xylem pericycle underlies shootregeneration from root and hypocotyl explants grown in vitro. Plant J. 2009;57(4):626-644. DOI 10.1111/j.1365-313X.2008.03715.x.

13. Azarakhsh M., Kirienko A.N., Zhukov V.A., Lebedeva M.A., Dolgikh E.A., Lutova L.A. KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. J. Exp. Bot. 2015; 66(22):7181-7195. DOI 10.1093/jxb/erv414.

14. Beeckman T., Burssens S., Inzé D. The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 2001;52:403-411.

15. Belles-Boix E., Hamant O., Witiak S.M., Morin H., Traas J., Pautot V. KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell. 2006;18(8):1900-1907.

16. Berckmans B., Vassileva V., Schmid S.P., Maes S., Parizot B., Naramoto S., Magyar Z., Alvim Kamei C.L., Koncz C., Bögre L., Persiau G., De Jaeger G., Friml J., Simon R., Beeckman T., De Veylder L. Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell. 2011;23(10):3671-3683. DOI 10.1105/tpc.111.088377.

17. Betsuyaku S., Takahashi F., Kinoshita A., Miwa H., Shinozaki K., Fukuda H., Sawa S. Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol. 2011;52:14-29. DOI 10.1093/pcp/pcq157.

18. Bishopp A., Help H., El-Showk S., Weijers D., Scheres B., Friml J., Benková E., Mähönen A.P., Helariutta Y. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 2011a;21:917-926. DOI 10.1016/j.cub.2011.04.017.

19. Bishopp A., Lehesranta S., Vatén A., Help H., El-Showk S., Scheres B., Helariutta K., Mähönen A.P., Sakakibara H., Helariutta Y. Phloemtransported cytokinin regulates polarauxintransport and maintains vascular pattern in the root meristem. Curr. Biol. 2011b;21(11): 927-932.

20. Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005;433:39-44.

21. Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L., Hattori J., Liu C.-M., van Lammeren A.A.M., Miki B.L.A., Custers J.B., van Lookeren Campagne M.M. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell. 2002;14:1737-1749.

22. Breuninger H., Rikirsch E., Hermann M., Ueda M., Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell. 2008;14:867-876. DOI 10.1016/j.devcel.2008.03.008.

23. Busch W., Miotk A., Ariel F.D., Zhao Z., Forner J., Daum G., Suzaki T., Schuster C., Schultheiss S.J., Leibfried A., Haubeiss S., Ha N., Chan R.L., Lohmann J.U. Transcriptional control of a plant stem cell niche. Dev. Cell. 2010;18(5):849-61.

24. Carlsbecker A., Lee J.Y., Roberts C.J., Dettmer J., Lehesranta S., Zhou J., Lindgren O., Moreno-Risueno M.A., Vaten A., Thitamadee S. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature. 2010;465:316-321. DOI 10.1038/nature08977.

25. Chalupowicz L., Barash I., Panijel M., Sessa G., Manulis-Sasson S. Regulatory interactions between quorum-sensing, auxin, cytokinin, and the Hrp regulon in relation to gall formation and epiphytic fitness of Pantoea agglomerans pv. gypsophilae. Mol. Plant Microbe Interaction. 2009;22:849-856. DOI 10.1094/MPMI-22-7-0849.

26. Chang L., Ramireddy E., Schmülling T. Cytokinin as a positional cue regulating lateral root spacing in Arabidopsis. J. Exp. Bot. 2015; 66(15):4759-4768. DOI 10.1093/jxb/erv252.

27. Chen S.-K., Kurdyukov S., Kereszt A., Wang X.-D., Gresshoff P.M., Rose R.J. The association of homeobox gene expression with stem cell formation and morph genesis in cultured Medicago truncatula. Planta. 2009;230:827-840. DOI 10.1007/s00425-009-0988-1.

28. Chen S., Lang P., Chronis D., Zhang S., De Jong W.S., Mitchum M.G., Wang X. In planta processing and glycosylation of a nematode CLAVATA3/ENDOSPERM SURROUNDING REGION-like effector and its interaction with a host CLAVATA2-like receptor to promote parasitism. Plant Physiol. 2015;167(1):262-272. DOI 10.1104/pp.114.251637.

29. Chuck C., Lincoln C., Hake S. KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell. 1996; 8:1277-1289.

30. Chung K.R., Tzeng D.D. Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustillago esculenta. J. Biol. Sci. 2004;4:744-750. DOI 10.3923/jbs.2004.744.750.

31. Crespi M., Frugier F. De novo organ formation from differentiated cells: root nodule organogenesis. Sci. Signal. 2008;1(49). DOI 10.1126/scisignal.149re11.

32. Cruz-Ramírez A., Díaz-Triviño S., Wachsman G., Du Y., ArteágaVázquez M., Zhang H., Benjamins R., Blilou I., Neef A.B., Chandler V., Scheres B. A SCARECROW-RETINOBLASTOMA protein network controls protective quiescence in the Arabidopsis тroot stem cell organizer. PLoS Biol. 2013;11(11):e1001724. DOI 10.1371/journal.pbio.1001724. DOI 10.1371/journal.pbio.1001724.

33. Cui H., Hao Y., Kovtun M., Stolc V., Deng X.W., Sakakibara H., Kojima M. Genome-wide direct target analysis reveals a role for SHORTROOT in root vascular patterning through cytokinin homeostasis. Plant Physiol. 2011;157:1221-1231. DOI 10.1104/pp.111.183178.

34. De Almeida Engler J., Gheysen G. Nematode-induced endoreduplication in plant host cells: why and how? Mol. Plant Microbe Interact. 2013;6:17-24. DOI 10.1094/MPMI-05-12-0128-CR.

35. De Buck S., De Wilde C., Van Montagu M., Depicker A. Determination of the T-DNA transfer and the T-DNA integration frequencies upon cocultivation of Arabidopsis thaliana root explants. Mol. Plant Microbe Interact. 2000;13:658-665.

36. De Lillo E., Monfreda R. Salivary secretions’ of eriophyoids (Acari: Eriophyoidea): first results of an experimental model. Exp. Appl. Acarol. 2004;34(3-4):291-306.

37. De Rybel B., Vassileva V., Parizot B., Demeulenaere M., Grunewald W., Audenaert D., Van Campenhout J., Overvoorde P., Jansen L., Vanneste S., Möller B., Wilson M., Holman T., Van Isterdael G., Brunoud G., Vuylsteke M., Vernoux T., De Veylder L., Inzé D., Weijers D., Bennett M.J., Beeckman T. A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 2010;20:1697-1706. DOI 10.1016/j. cub.2010.09.007.

38. De Smet I., Vanneste S., Inzé D., Beeckman T. Lateral root initiation or the birth of a new meristem. Plant Mol. Biol. 2006;60:871-887.

39. Devos S., Laukens K., Deckers P., Van Der Straeten D., Beeckman T., Inzé D., Van Onckelen H., Witters E., Prinsen E. A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Mol. Plant Microbe Interact. 2006;19:1431-1443.

40. Dodueva I.E., Frolova N.V., Lutova L.A. Plant tumorigenesis: different ways for shifting systemic control of plant cell division and differentiation. Transgen. Plant J. 2007;1:3-24.

41. Dolzblasz A., Nardmann J., Clerici E., Causier B., van der Graaff E., Chen J., Davies B., Werr W., Laux T. Mol. Plant. 2016; pii: S1674-2052(16)30029-6. DOI 10.1016/j.molp.2016.04.007.

42. Dubrovsky J.G., Doerner P.W., Colón-Carmona A., Rost T.L. Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol. 2000;124:1648-1657.

43. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 2003;13:1768-1774.

44. Etchells J.P., Provost C.M., Mishra L., Turner S.R. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organization. Development. 2013;140:2224-2234. DOI 10.1242/dev.091314.

45. Etchells J.P., Provost C.M., Turner S.R. Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Gen. 2012;8(11):e1002997.

46. Etchells J.P., Turner S.R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development. 2010;137:767-774. DOI 10.1242/dev.044941.

47. Feldman L.J. The de novo Origin of the Quiescent Center Regenerating Root Apices in Zea mays. Planta. 1976;128(3):207-212. DOI 10.1007/BF00393230.

48. Fiers M., Hause G., Boutilier K., Casamitjana-Martinez E., Weijers D., Offringa R., van der Geest L., van Lookeren Campagne M., Liu C.M. Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene. 2004;327(1): 37-49.

49. Fisher K., Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 2007;17:1061-1066.

50. Frank M., Guiv’Arch A., Krupkova E., Lorenz-Meyer I., Chriqui D., Schmulling T. TUMOROUS SHOOT DEVELOPMENT (TSD) genes are required for co-ordinated plant shoot development. Plant J. 2002;29:73-85.

51. Gagne J.M., Clark S.E. The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell. 2010;22:729-743. DOI 10.1105/tpc.109.068734.

52. Gallois J.-L., Nora F.R., Mizukami Y., Sablowski R. WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Gen. Dev. 2004;18:375-380.

53. Gambino G., Minuto M., Boccacci P., Perrone I., Vallania R., Gribaudo I. Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J. Exp. Bot. 2011;62:1089-1101. DOI 10.1093/jxb/erq349.

54. Garfinkel D.J., Simpson R.B., Ream L.W., White F.F., Gordon M.P., Nester E.W. Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell. 1981;27(1 Pt 2): 143-153.

55. Giron D., Glevarec G. Cytokinin-induced phenotypes in plant-insect interactions: learning from the bacterial world. J. Chem. Ecol. 2014;40(7):826-835. DOI 10.1007/s10886-014-0466-5.

56. Glass N.L., Kosuge T. Role of indoleacetic acid-lysine synthetase in regulation of indoleacetic acid pool size and virulence of Pseudomonas syringae subsp. savastanoi. J. Bacteriol. 1988;170(5): 2367-2373.

57. Gonzalez-Rizzo S., Crespi M., Frugier F. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell Online. 2006;18(10):2680-2693.

58. Gonzali S., Novi G., Loreti E., Paolicchi F., Poggi A., Alpi A., Perata P. A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana. Plant J. 2005;44:633-645.

59. Gursanscky N.R., Jouannet V., Grünwald K., Sanchez P., LaaberSchwarz M., Greb T. MOL1 is required for cambium homeostasis in Arabidopsis. Plant J. 2016;17. DOI 10.1111/tpj.13169.

60. Haecker A., Gross-Hardt R., Geiges B., Sarkar A., Breuninger H., Herrmann M., Laux T. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004;131(3):657-668.

61. Heidstra R., Sabatini S. Plant and animal stem cells: similary et different. Nat. Rev. Mol. Cell Biol. 2014;15(5):301-312. DOI 10.1038/nrm3790.

62. Hinsch J., Vrabka J., Oeser B., Novák O., Galuszka P., Tudzynski P. De novo biosynthesis of cytokinins in the biotrophic fungus Clavicepspurpurea. Environ. Microbiol. 2015;17(8):2935-2951. DOI 10.1111/1462-2920.12838.

63. Hirakawa Y., Kondo Y., Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell. 2010;22:2618-2629. DOI 10.1105/tpc.110.076083.

64. Hirakawa Y., Shinohara H., Kondo Y., Inoue A., Nakanomyo I., Ogawa M., Sakagami Y. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl Acad. Sci. USA. 2008;105:15208-15213. DOI 10.1073/pnas.0808444105.

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

66. Huang G.Z., Dong R.H., Allen R., Davis E.L., Baum T.J., Hussey R.S. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant Microbe Interact. 2006;19:463-470.

67. Ikeuchi M., Sugimoto K., Iwase A. Plantcallus: mechanisms of induction and repression. Plant Cell. 2013;25(9):3159-3173. DOI 10.1105/tpc.113.116053.

68. Ilegems M., Douet V., Meylan-Bettex M., Uyttewaal M., Brand L., Bowman J.L., Stieger P.A. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development. 2010;137(6):975-984. DOI 10.1242/dev.047662.

69. Intrieri M.C., Buiatti M. The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol. Phylogen. Evol. 2001;20:100-110.

70. Ito Y., Nakanomyo I., Motose H., Iwamoto K., Sawa S., Dohmae N., Fukuda H. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science. 2006;313:842-845.

71. Jasinski S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., Phillips A., Hedden P., Tsiantis M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 2005;15:1560-1565.

72. Ji J., Shimizu R., Sinha N., Scanlon M.J. Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signal Behav. 2010b;5(7):916-920. DOI 10.1104/pp.109.149641.

73. Ji J., Strable J., Shimizu R., Koenig D., Sinha N., Scanlon M.J. WOX4 promotes procambial development. Plant Physiol. 2010a;152(3): 1346-1356. DOI 10.1104/pp.109.149641.

74. Jiang F., Feng Z., Liu H., Zhu J. Involvement of plant stem cells or stem cell-like cells in dedifferentiation. Front. Plant Sci. 2015;6:1028. DOI 10.3389/fpls.2015.01028.

75. Klimaszewska K., Overton C., Stewart D., Rutledge R.G. Initiation of somatic embryos and regeneration of plants from primordial shoots of 10-year-old somatic white spruce and expression profiles of 11 genes followed during the tissue culture process. Planta. 2011;233:635-647. DOI 10.1007/s00425-010-1325-4.

76. Kondo T., Sawa S., Kinoshita A., Mizuno S., Kakimoto T., Fukuda H., Sakagami Y. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science. 2006;313:845-848.

77. Kosan C., Godmann M. Genetic and epigenetic mechanisms that maintain hematopoietic stem cell function. Stem Cells Int. 2016;2016: 5178965. DOI 10.1155/2016/5178965.

78. Kosugi S., Ohashi Y. Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol. 2003;132(4):2012-2022.

79. Krupková E., Schmülling T. Developmental consequences of the tumorous shoot development1 mutation, a novel allele of the cellulose-synthesizing KORRIGAN1 gene. Plant Mol. Biol. 2009;71(6): 641-655. DOI 10.1007/s11103-009-9546-2.

80. Kurdyukov S., Song Y., Sheahan M.B., Rose R.J. Transcriptional regulation of early embryo development in the model legume Medicago truncatula. Plant Cell Rep. 2014;33:349-362. DOI 10.1007/s00299-013-1535-x.

81. Lebedeva (Osipova) M.A., Tvorogova V.E., Vinogradova A.P., Gancheva M.S., Azarakhsh M., Ilina E.L., Demchenko K.N., Dodueva I.E., Lutova L.A. Initiation of spontaneous tumors in radish (Raphanus sativus): cellular, molecular and physiological events. J. Plant Physiol. 2015;173:97-104. DOI 10.1016/j.jplph.2014.07.030.

82. Lee J.H., Kim D.M., Lim Y.P., Pai H.S. The shooty callus induced by suppression of tobacco CHRK1 receptor-like kinase is a phenocopy of the tobacco genetic tumor. Plant Cell Rep. 2004;23(6):397-403.

83. Leibfried A., To J.P., Busch W., Stehling S., Kehle A., Demar M., Kieber J.J., Lohmann J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature. 2005;438:1172-1175.

84. Lenhard M., Laux T. Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development. 2003;130:3163-3173.

85. Lin H., Niu L., McHale N.A., Ohme-Takagi M., Mysore K.S., Tadege M. Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proc. Natl Acad. Sci. USA. 2013;110(1):366-371.

86. Liu J., Sheng L., Xu Y., Li J., Yang Z., Huang H., Xu L. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell. 2014;26:1081-1093. DOI 10.1105/tpc.114.122887.

87. Long J.A., Moan E.I., Medford J.J., Barton M.K. A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis. Nature. 1996;379:66-69.

88. Lotan T., Ohto M., Yee K.M., West M.A.L., Lo R., Kwong R.W., Yamagishi K., Fischer R.L., Goldberg R.B., Harada J.J. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell. 1998;93:1195-1205.

89. Lu S.W., Chen S., Wang J., Yu H., Chronis D., Mitchum M.G., Wang X. Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol. Plant Microbe Interact. 2009;22(9):1128-1142. DOI 10.1094/MPMI-22-9-1128.

90. Mähönen A.P., Bonke M., Kauppinen L., Riikonen M., Benfey P.N., Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Gen. Dev. 2000;14(23): 2938-2943.

91. Mähönen A.P., Higuchi M., Törmäkangas K., Miyawaki K., Pischke M.S., Sussman M.R., Helariutta Y., Kakimoto T. Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr. Biol. 2006;16:1116-1122.

92. Mathesius U., Weinman J.J., Rolfe B.J., Djordjevic M.A. Rhizobia can induce nodules in white clover by “hijacking” mature cortical cells activated during lateral root development. Mol. Plant Microbe Interact. 2000;13:170-182.

93. Matveeva T.V., Frolova N.V., Smets R., Dodueva I.E., Buzovkina I.S., Van Onckelen H., Lutova L.A. Hormonal control of tumor formation in radish. J. Plant Growth Regul. 2004;23:37-43.

94. Mayer K.F., Schoof H., Haecker A., Lenhard M., Jurgens G., Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998;95(6):805-815.

95. Mohrin M., Bourke E., Alexander D., Warr M.R., Barry-Holson K., Le Beau M.M., Morrison C.G., Passegué E. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell. 2010;7(2):174-185. DOI 10.1016/j.stem.2010.06.014.

96. Mortier V., Den Herder G., Whitford R., Van de Velde W., Rombauts S., D’Haeseleer K., Holsters M., Goormachtig S. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 2010;153:222-237. DOI 10.1104/pp.110.153718.

97. Nardmann J., Reisewitz P., Werr W. Discrete shoot and root stem cellpromoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol. Biol. Evol. 2009;26:1745-1755. DOI 10.1093/molbev/msp084.

98. Nardmann J., Werr W. Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytologist. 2013;199: 1081-1092. DOI 10.1111/nph.12343.

99. Ohmori Y., Tanaka W., Kojima M., Sakakibara H., Hirano H.Y. WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell. 2013;25(1):229-241.

100. Oka-Kira E., Kawaguchi M. Long-distance signaling to control root nodule number. Curr. Opinion Plant Biol. 2006;9:496-502.

101. Okamoto S., Ohnishi E., Sato S., Takahashi H., Nakazono M., Tabata S., Kawaguchi M. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 2009;50(1):67-77. DOI 10.1093/pcp/pcn194.

102. Okushima Y., Fukaki H., Onoda M., Theologis A., Tasaka M. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell. 2007;19(1):118-130.

103. Okushima Y., Mitina I., Quach H.L., Theologis A. AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J. 2005;43:29-46.

104. Op den Camp R.H., De Mita S., Lillo A., Cao Q., Limpens E., Bisseling T., Geurts R. A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol. 2011;157(4):2013-2022. DOI 10.1104/pp.111.187526.

105. Osipova M.A., Mortier V., Demchenko K.N., Tsyganov V.E., Tikhonovich I.A., Lutova L.A., Dolgikh E.A., Goormachtig S. WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiol. 2012;158:1329-1341. DOI 10.1104/pp.111.188078.

106. Palovaara J., Hallberg H., Stasolla C., Luit B., Hakman I. Expression of a gymnosperm PIN homologous gene correlates with auxin immunolocalization pattern at cotyledon formation and in demarcation of the procambium during Picea abies somatic embryo development and in seedling tissues. Tree Physiol. 2010;30:479-489. DOI 10.1093/treephys/tpp126.

107. Parizot B., Laplaze L., Ricaud L., Boucheron-Dubuisson E., Bayle V., Bonke M., De Smet I., Poethig S.R., Helariutta Y., Haseloff J., Chriqui D., Beeckman T., Nussaume L. Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol. 2008;146: 140-148.

108. Parizot B., Roberts I., Raes J., Beeckman T., De Smet I. In silico analyses of pericycle cell populations reinforce their relation with associated vasculature in Arabidopsis. Philos. Trans. Royal Soc. B. Biol. Sci. 2012;367:1479-1488. DOI 10.1098/rstb.2011.0227.

109. Pautot V., Dockx J., Hamant O., Kronenberger J., Grandjean O., Jublot D., Traas J. KNAT2: evidence for a link between knotted-like genes and carpel development. Plant Cell. 2001;13(8):1719-1734.

110. Plet J., Wasson A., Ariel F., Le Signor C., Baker D., Mathesius U., Crespi M., Frugier F. MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J. 2011;65(4):622-633. DOI 10.1111/j.1365-313X.2010.04447.x.

111. Reineke G., Heinze B., Schirawski J., Buettner H., Kahmann R., Basse C.W. Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilagomaydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol. Plant Pathol. 2008; 9:339-355.

112. Replogle A., Wang J., Bleckmann A., Hussey R.S., Baum T.J., Sawa S., Davis E.L., Wang X., Simon R., Mitchum M.G. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 2011;65:430-440. DOI 10.1111/j.1365-313X.2010.04433.x.

113. Santiago J., Henzler C., Hothorn M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science. 2013;341:889-892. DOI 10.1126/science.1242468.

114. Sarkar A.K., Luijten M., Miyashima S., Lenhard M., Hashimoto T., Nakajima K., Scheres B., Heidstra R., Laux T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature. 2007;446(7137):811-814.

115. Scheres B., Wolkenfelt H., Willemsen V., Terlouw M., Lawson E., Dean C., Weisbeek P. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development. 1994;120:2475-2487.

116. Schnabel E., Journet E.P., de Carvalho-Niebel F., Duc G., Frugoli J. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol. Biol. 2005;58(6):809-822.

117. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7-25.

118. Schoof H., Lenhard M., Haecker A., Mayer K.F., Jürgens G., Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100:635-644.

119. Schrader J., Nilsson J., Mellerowicz E., Berglund A., Nilsson P., Hertzberg M., Sandberg G. A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell. 2004;16:2278-2292.

120. Searle I.R., Men A.E., Laniya T.S., Buzas D.M., Iturbe-Ormaetxe I., Carroll B.J., Gresshoff P.M. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science. 2003; 299:109-112.

121. Sieberer T., Hauser M.T., Seifert G.J., Luschnig C. PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr. Biol. 2003;13:837-842.

122. Skoog F., Miller C.O. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 1957;11: 118-130.

123. Stahl Y., Wink R.H., Ingram G.C., Simon R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 2009;19:909-914. DOI 10.1016/j.cub.2009.03.060.

124. Su Y.H., Liu Y.B., Bai B., Zhang X.S. Establishment of embryonic shoot-root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front. Plant Sci. 2015; 14(5):792.

125. Su Y.H., Zhao X.Y., Liu Y.B., Zhang C.L., O’Neill S.D., Zhang X.S. Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J. 2009;59(3):448-460. DOI 10.1111/j.1365-313X.2009.03880.x.

126. Suer S., Agusti J., Sanchez P., Schwarz M., Greb T.WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011; 23:3247-3259. DOI 10.1105/tpc.111.087874.

127. Sugimoto K., Jiao Y., Meyerowitz E.M. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell. 2010;18(3):463-471. DOI 10.1016/j.devcel.2010.02.004.

128. Suzaki T., Yano K., Ito M., Umehara Y., Suganuma N., Kawaguchi M. Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development. 2012;139(21):3997-4006. DOI 10.1242/dev.084079.

129. Testone G., Bruno L., Condello E., Chiappetta A., Bruno A., Mele G., Tartarini A., Spanò L., Innocenti A.M., Mariotti D., Bitonti M.B., Giannino D. Peach [Prunuspersica (L.) Batsch] KNOPE1, a class 1 KNOX orthologue to Arabidopsis BREVIPEDICELLUS/KNAT1, is misexpressed during hyperplasia of leaf curl disease. J. Exp. Bot. 2008;59:389-402.

130. Timmers A., Auriac M.-C., Truchet G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development. 1999;126(16):3617-3628.

131. Tooker J.F., Helms A.M. Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J. Chem. Ecol. 2014;40(7):742-753. DOI 10.1007/s10886-014-0457-6.

132. Trotochaud A.E., Hao T., Wu G., Yang Z., Clark S.E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell. 1999;11:393-406.

133. Trumpp A., Essers M., Wilson A. Awakening dormant haematopoietic stem cells. Nat. Rev. Immunol. 2010;10(3):201-209. DOI 10.1038/nri2726.

134. Ueda M., Zhang Z., Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell. 2011;15:264-270. DOI 10.1016/j.devcel.2011.01.009.

135. Ullrich C.I., Aloni R. Vascularization is a general requirement for growth of plant and animal tumours. J. Exp. Bot. 2000;51(353):1951-1960.

136. Van der Graaff E., Laux T., Rensing S.A. The WUS homeobox-containing (WOX) protein family. Gen. Biol. 2009;10(12):248. DOI 10.1186/gb-2009-10-12-248.

137. Vandeputte O., Oden S., Mol A., Vereecke D., Goethals K., El Jaziri M., Prinsen E. Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl. Environ. Microbiol. 2005;71: 1169-1177.

138. Vanstraelen M., Baloban M., Da Ines O., Cultrone A., Lammens T., Boudolf V., Brown S.C., De Veylder L., Mergaert P., Kondorosi E. APC/C-CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl Acad. Sci. USA. 2009;106(28):11806-11811. DOI 10.1073/pnas.0901193106.

139. Veselov D., Langhans M., Hartung W., Aloni R., Feussner I., Götz C., Veselova S., Schlomski S., Dickler C., Bächmann K., Ullrich C.I. Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta. 2003;216(3):512-522.

140. Wang J., Replogle A., Hussey R., Baum T., Wang X., Davis E.L., Mitchum M.G. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 2011;12(2):177-186.

141. Wang X., Mitchum M.G., Gao B., Li C., Diab H., Baum T.J., Hussey R.S., Davis E.L. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 2005;6:187-191.

142. Whitford R., Fernandez A., De Groodt R., Ortega E., Hilson P. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl Acad. Sci. USA. 2008;105:18625-18630.

143. Wilson A., Laurenti E., Oser G., van der Wath R.C., Blanco-Bose W., Jaworski M., Offner S., Dunant C.F., Eshkind L., Bockamp E., Lió P., Macdonald H.R., Trumpp A. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.

144. Yadav R.K., Perales M., Gruel J., Girke T., Jönsson H., Reddy G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Gen. Dev. 2011;25:2025-2030. DOI 10.1101/gad.17258511.

145. Yanai O., Shani E., Dolezal K., Tarkowski P., Sablowski R., Sandberg G., Samach A., Ori N. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 2005;15:1566-1571.

146. Zhang F., Wang Y., Li G., Tang Y., Kramer E.M., Tadege M. STENOFOLIA recruits TOPLESS to repress ASYMMETRIC LEAVES2 at the leaf margin and promote leaf blade outgrowth in Medicago truncatula. Plant Cell. 2014;26(2):650-664. DOI 10.1105/tpc.113.121947.

147. Zheng Q., Zheng Y., Perry S.E. AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and soybean in part by the control of ethylene biosynthesis and response. Plant Physiol. 2013;161:2113-2127. DOI 10.1104/pp.113.216275.

148. Zhou Y., Liu X., Engstrom E.M., Nimchuk Z.L., Pruneda-Paz J.L., Tarr P.T., Yan A., Kay S.A., Meyerowitz E.M. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature. 2015;517(7534):377-380. DOI 10.1038/nature13853.

149. Zimmerman J.L. Somatic Embryogenesis: A model for early development in higher plants. Plant Cell. 1993;5(10):1411-1423.


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