PHABULOSA Controls the Quiescent Center-Independent Root Meristem Activities in

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Plant roots are programmed to grow continuously into the soil, searching for nutrients and water. The iterative process of cell division, elongation, and differentiation contributes to root growth. The quiescent center (QC) is known to maintain the root meristem, and thus ensure root growth. In this study, we report a novel aspect of root growth regulation controlled independently of the QC by PHABULOSA (PHB). In shr mutant plants, PHB, which in the meristem is actively restricted to the central region of the stele by SHORTROOT (SHR) via miR165/6, suppresses root meristem activity leading to root growth arrest. A high concentration of PHB in the stele does this by modulating B-ARR activity through a QC-independent pathway. Accordingly, we observed a significant recovery of root meristem activity and growth in the shr phb double mutant, while the QC remained absent. However, the presence of QC may be required to sustain continuous root growth. On the basis of our results, we propose that SHR maintains root growth via two separate pathways: by modulating PHB levels in the root stele, and by maintaining the QC identity.

Vyšlo v časopise: PHABULOSA Controls the Quiescent Center-Independent Root Meristem Activities in. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1004973
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004973

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Zdroje

1. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, et al. (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119 : 71–84. 8275865

2. 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. 9384380

3. Bennett T, Scheres B (2010) Root development-two meristems for the price of one? Curr Top in Dev Biol 91 : 67–102. doi: 10.1016/S0070-2153(10)91003-X 20705179

4. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, et al. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119 : 109–120. 15454085

5. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, et al. (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86 : 423–433. 8756724

6. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, et al. (2000) The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling. Cell 101 : 555–567. 10850497

7. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, et al. (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316 : 421–425. 17446396

8. Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, et al. (2006) A molecular framework for plant regeneration. Science 311 : 385–388. 16424342

9. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, et al. (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446 : 811–814. 17429400

10. Sena G, Wang X, Liu HY, Hofhuis H, Birnbaum KD (2009) Organ regeneration does not require a functional stem cell niche in plants. Nature 457 : 1150–1153. doi: 10.1038/nature07597 19182776

11. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, et al. (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16 : 1365–1377. 15155880

12. Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, et al. (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20 : 2102–2116. doi: 10.1105/tpc.108.059584 18723577

13. Tian Q, Uhlir NJ, Reed JW (2002) Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14 : 301–319. 11884676

14. Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, et al. (2008) A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem. Science 322 : 1380–1384. doi: 10.1126/science.1164147 19039136

15. Moubayidin L, Di Mambro R, Sozzani R, Pacifici E, Salvi E, et al. (2013) Spatial coordination between stem cell activity and cell differentiation in the root meristem. Dev Cell 26 : 405–415. doi: 10.1016/j.devcel.2013.06.025 23987513

16. Byrne ME (2006) Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes. PLoS Genet 2: e89. 16846251

17. Zhou J, Sebastian J, Lee JY (2011) Signaling and gene regulatory programs in plant vascular stem cells. Genesis 49 : 885–904. doi: 10.1002/dvg.20795 21898765

18. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, et al. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17 : 61–76. 15598805

19. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, et al. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13 : 1768–1774. 14561401

20. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J 23 : 3356–3364. 15282547

21. Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, et al. (2009) Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr Biol 19 : 1485–1490. doi: 10.1016/j.cub.2009.06.070 19646874

22. Smith ZR, Long JA (2010) Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464 : 423–426. doi: 10.1038/nature08843 20190735

23. Iwata Y, Takahashi M, Fedoroff NV, Hamdan SM (2013) Dissecting the interactions of SERRATE with RNA and DICER-LIKE 1 in Arabidopsis microRNA precursor processing. Nucleic Acids Res 41 : 9129–9140. doi: 10.1093/nar/gkt667 23921632

24. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, et al. (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465 : 316–321. doi: 10.1038/nature08977 20410882

25. Perilli S, Sabatini S (2010) Analysis of root meristem size development. Methods in Mol Biol 655 : 177–187. doi: 10.1007/978-1-60761-765-5_12 20734261

26. Ingouff M, Jullien PE, Berger F (2006) The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18 : 3491–3501. 17172356

27. Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17 : 354–358. 12569126

28. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, et al. (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449 : 1053–1057. 17960244

29. Nawy T, Lee J-Y, Colinas J, Wang JY, Thongrod SC, et al. (2005) Transcriptional Profile of the Arabidopsis Root Quiescent Center. Plant Cell 17 : 1908–1925. 15937229

30. Lee J-Y, Colinas J, Wang JY, Mace D, Ohler U, et al. (2006) Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci USA 103 : 6055–6060. 16581911

31. Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, et al. (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14 : 2938–2943. 11114883

32. Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA, et al. (2005) Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nature Methods 2 : 615–619. 16170893

33. Heyer LJ, Kruglyak S, Yooseph S (1999) Exploring Expression Data: Identification and Analysis of Coexpressed Genes. Genome Res 9 : 1106–1115. 10568750

34. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, et al. (2003) A Gene Expression Map of the Arabidopsis Root. Science 302 : 1956–1960. 14671301

35. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, et al. (2006) Whole-Genome Analysis of the SHORT-ROOT Developmental Pathway in Arabidopsis. PLoS Biol 4: e143. 16640459

36. Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J, et al. (2007) A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns. Science 318 : 801–806. 17975066

37. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25 : 288–289. doi: 10.1093/bioinformatics/btn615 19033274

38. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95 : 14863–14868. 9843981

39. Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14 : 557–562. doi: 10.1016/j.tplants.2009.06.010 19734082

40. Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, et al. (2011) Short-Root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol 155 : 384–398. doi: 10.1104/pp.110.165126 21030506

41. Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, et al. (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: A factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci USA 101 : 8039–8044. 15146070

42. Jones B, Gunnerås SA, Petersson SV, Tarkowski P, Graham N, et al. (2010) Cytokinin Regulation of Auxin Synthesis in Arabidopsis Involves a Homeostatic Feedback Loop Regulated via Auxin and Cytokinin Signal Transduction. Plant Cell 22 : 2956–2969. doi: 10.1105/tpc.110.074856 20823193

43. Marhavy P, Bielach A, Abas L, Abuzeineh A, Duclercq J, et al. (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21 : 796–804. doi: 10.1016/j.devcel.2011.08.014 21962902

44. Cui H, Hao Y, Kovtun M, Stolc V, Deng XW, et al. (2011) Genome-wide direct target analysis reveals a role for SHORT-ROOT in root vascular patterning through cytokinin homeostasis. Plant Physiol 157 : 1221–1231. doi: 10.1104/pp.111.183178 21951467

45. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, et al. (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103 : 16598–16603. 17062755

46. Rashotte AM, Carson SD, To JP, Kieber JJ (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132 : 1998–2011. 12913156

47. Muller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453 : 1094–1097. doi: 10.1038/nature06943 18463635

48. Zhang W, To JP, Cheng CY, Eric Schaller G, Kieber JJ (2011) Type-A response regulators are required for proper root apical meristem function through post-transcriptional regulation of PIN auxin efflux carriers. Plant J 68 : 1–10. doi: 10.1111/j.1365-313X.2011.04668.x 21645147

49. Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, et al. (2006) Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development. Science 311 : 94–98. 16400151

50. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11 : 1251–1260. 11525739

51. Miyashima S, Koi S, Hashimoto T, Nakajima K (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138 : 2303–2313. doi: 10.1242/dev.060491 21558378

52. Hsu YC, Li L, Fuchs E (2014) Transit-amplifying cells orchestrate stem cell activity and tissue regeneration. Cell 157 : 935–949. doi: 10.1016/j.cell.2014.02.057 24813615

53. Kalaitzidis D, Scadden DT (2014) Tic-TACs: refreshing hair growth. Cell 157 : 769–770. doi: 10.1016/j.cell.2014.04.014 24813602

54. Lander AD, Kimble J, Clevers H, Fuchs E, Montarras D, et al. (2012) What does the concept of the stem cell niche really mean today? BMC Biol 10 : 19. doi: 10.1186/1741-7007-10-19 22405133

55. Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol 15 : 19–33. doi: 10.1038/nrm3721 24326621

56. Buczacki SJ, Zecchini HI, Nicholson AM, Russell R, Vermeulen L, et al. (2013) Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495 : 65–69. doi: 10.1038/nature11965 23446353

57. Rost TL (2011) The organization of roots of dicotyledonous plants and the positions of control points. Ann Bot 107 : 1213–1222. doi: 10.1093/aob/mcq229 21118839

58. Baum SF, Dubrovsky JG, Rost TL (2002) Apical organization and maturation of the cortex and vascular cylinder inArabidopsis thaliana (Brassicaceae) roots. Am J Bot 89 : 908–920. doi: 10.3732/ajb.89.6.908 21665690

59. Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in angiosperms. Ann Bot 101 : 319–340. 17954472

60. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, et al. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95 : 805–815. 9865698

61. Gallagher KL, Benfey PN (2009) Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 57 : 785–797. doi: 10.1111/j.1365-313X.2008.03735.x 19000160

62. Dello Ioio R, Linhares FS, Sabatini S (2008) Emerging role of cytokinin as a regulator of cellular differentiation. Curr Opin Plant Biol 11 : 23–27. 18060829

63. Dello Ioio R, Galinha C, Fletcher AG, Grigg SP, Molnar A, et al. (2012) A PHABULOSA/Cytokinin Feedback Loop Controls Root Growth in Arabidopsis. Curr Biol 22 : 1699–1704. doi: 10.1016/j.cub.2012.07.005 22902752

64. Jander G, Baerson SR, Hudak JA, Gonzalez KA, Gruys KJ, et al. (2003) Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol 131 : 139–146. 12529522

65. Ingram P, Dettmer J, Helariutta Y, Malamy JE (2011) Arabidopsis Lateral Root Development 3 is essential for early phloem development and function, and hence for normal root system development. Plant J 68 : 455–467. doi: 10.1111/j.1365-313X.2011.04700.x 21749503

66. Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, et al. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9 : 1797–1810. 7622040

67. van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378 : 62–65. 7477287

68. Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B (1998) The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125 : 521–531. 9425146

69. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta C(T)) Method. Methods 25 : 402–408. 11846609

70. Hejatko J, Blilou I, Brewer PB, Friml J, Scheres B, et al. (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nature Protoc 1 : 1939–1946.

71. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 : 249–264. 12925520

72. Naouar N, Vandepoele K, Lammens T, Casneuf T, Zeller G, et al. (2009) Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J 57 : 184–194. doi: 10.1111/j.1365-313X.2008.03662.x 18764924

73. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.

74. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, et al. (2006) TM4 microarray software suite. Methods Enzymol 411 : 134–193. 16939790

75. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 : 735–743. 10069079

76. Novák O, Tarkowski P, Tarkowská D, Doležal K, Lenobel R, et al. (2003) Quantitative analysis of cytokinins in plants by liquid chromatography-single-quadrupole mass spectrometry. Anal Chim Acta 480 : 207–218.

77. Bieleski RL (1964) The problem of halting enzyme action when extracting plant tissues. Anal Biochem 9 : 431–442. 14239480

78. Faiss M, Zalubilova J, Strnad M, Schmulling T (1997) Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants. Plant J 12 : 401–415. 9301091

79. Novak O, Hauserova E, Amakorova P, Dolezal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69 : 2214–2224. doi: 10.1016/j.phytochem.2008.04.022 18561963

80. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2 : 1565–1572. 17585298

81. Cho YH, Yoo SD (2010) Expression of epitope-tagged proteins in Arabidopsis leaf mesophyll protoplasts. Methods Mol Biol 657 : 33–42. doi: 10.1007/978-1-60761-783-9_3 20602205