The maize root stem cell niche: A partnership between two sister cell populations

Planta

Volumn 231, Issue 2, 2010, Pages 411-424

  Jiang, Keni ^a   Zhu, Tong ^b   Diao, Zhaoyan ^a   Huang, Haiyan ^c   Feldman, Lewis J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SYNGENTA BIOTECHNOLOGY INC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Quiescent center; Root; Stem cell; Stem cell niche; Zea mays

Indexed keywords

ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; INDOLEACETIC ACID DERIVATIVE; MESSENGER RNA;

ARTICLE; CLUSTER ANALYSIS; CONFOCAL MICROSCOPY; CYTOLOGY; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MAIZE; MERISTEM; METABOLISM; OXIDATION REDUCTION REACTION; PLANT GENE; PLANT ROOT; STEM CELL NICHE;

ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CLUSTER ANALYSIS; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INDOLEACETIC ACIDS; MERISTEM; MICROSCOPY, CONFOCAL; OXIDATION-REDUCTION; PLANT ROOTS; RNA, MESSENGER; STEM CELL NICHE; TRANSCRIPTION, GENETIC; ZEA MAYS;

ARABIDOPSIS; ZEA MAYS;

EID: 77949775420     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-009-1059-3     Document Type: Article

References (66)

1. Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129: 3965-3974.
2. Baharvand H, Hajheidari M, Ashtiani SK, Salekdeh GH (2006) Proteomic signature of human embryonic stem cells. Proteomics 6: 3544-3549.
3. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102: 11928-11933.
4. Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7: 732-736.
5. Birnbaum K, Shasha DE, Wang JY, Jung J, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302: 1956-1960.
6. Blau HM, Brazelton TR, Weimann JM (2001) The evolving concept of a stem cell: entity or function? Cell 105: 829-841.
7. Bloch D, Lavy M, Efrat Y, Efroni I, Bracha-Drori K, Abu-Abied M, Sadot E, Yalovsky S (2005) Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol Biol Cell 16: 1913-1927.
8. Cai J, Weiss ML, Rao MS (2004) In search of "stemness". Exp Hematol 32: 585-598.
9. Cai L, Huang H, Blackshaw S, Liu JS, Cepko C, Wong WH (2004) Clustering analysis of SAGE data using a Poisson approach. Genome Biol 5: R51.
10. Campilho A, Garcia B, Toorn HVD, Wijk HV, Campilho A, Scheres B (2006) Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem. Plant J 48: 619-627.
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
12. Clowes FAL (1961) Apical meristems. Blackwell, Oxford.
13. Cockcroft S, Carvou N (2007) Biochemical and biological functions of class I phosphatidylinositol transfer proteins. Biochim Biophys Acta 1771: 677-691.
14. De Veylder L, Beemster GTS, Beeckman T, Inzé D (2001) CKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progression. Plant J 25: 617-626.
15. Essers MAG, De Vries-Smits LMM, Barker N, Polderman PE, Burgering BMT (2005) Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184.
16. Feldman LJ (1975) Cytokinins and quiescent center activity in roots of Zea. In: Torrey JG, Clarkson D (eds) The development and function of roots. Academic Press, London, pp 55-72.
17. Feldman LJ, Torrey JG (1976) The isolation and culture in vitro of the quiescent center of Zea mays. Am J Bot 63: 345-355.
18. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
19. Galinha C, Hofhuis H, Luiten M, Wilmsen V, Bilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449: 1053-1057.
20. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lang BM, Moughamer T, Xia Y, Budworth P, Zong J, Miguel T et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100.
21. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17: 1405-1411.
22. Houlard M, Berlivet S, Probst AV, Quivy JP, Hery P, Almouzni G, Gerard M (2006) CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet 2: 1686-1696.
23. Ioio RD, 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.
24. Iyer-Pascuzzi AS, Benfey PN (2008) Transcriptional networks in root cell fate specification. Biochim Biophys Acta 1789: 315-325.
25. Jiang K, Meng YL, Feldman LJ (2003) Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130: 1429-1438.
26. Jiang K, Zhang S, Lee S, Tsai G, Kim K, Huang H, Chilcott C, Zhu T, Feldman LJ (2006) Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol Biol 60: 343-363.
27. Kaya H, Shibahara K-i, Taoka K-i, Iwabuchi M, Bruce Stillman B, Takashi Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104: 131-142.
28. Kim K, Zhang S, Jiang K, Cai L, Lee IB, Feldman LJ, Huang H (2007) Measuring similarities between gene expression profiles through data transformations. BMC Bioinform 8: 29-43.
29. Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J 44: 960-971.
30. Manfield IW, Devlin PF, Jen C-H, Westhead DR, Gilmartin PM (2007) Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family. Plant Physiol 143: 941-958.
31. McElver J, Patton D, Rumbaugh M, Liu C, Yang LJ, Meinke D (2000) The TITAN5 gene of Arabidopsis encodes a protein related to the ADP ribosylation factor family of GTP binding proteins. Plant Cell 12: 1379-1392.
32. Menges M, de Jager SM, Gruissem W, Murray JAH (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41: 546-566.
33. Mikkers H, Frisén J (2005) Deconstructing stemness. EMBO J 24: 2715-2719.
34. Nabatiyan A, Szüts D, Krude T (2006) Induction of CAF-1 expression in response to DNA strand breaks in quiescent human cells. Mol Cell Biol 26: 1839-1849.
35. Naito T, Kiba T, Koizumi N, Yamashino T, Mizuno T (2007) Characterization of a unique GATA family gene that responds to both light and cytokinin in Arabidopsis thaliana. Biosci Biotechnol Biochem 71: 1557-1560.
36. Nakajima K, Benfey PN (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14 Suppl: S265-S276.
37. Nawy T, Lee J-Y, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcription profile of the Arabidopsis root quiescent center. Plant Cell 17: 1908-1925.
38. Nibau C, Wu H-M, Cheung AY (2006) RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants. Trends Plant Sci 11: 309-315.
39. Nijnik A, Woodbine L, Marchetti C, Dawson S, Lambe T, Liu C, Rodrigues NP, Crockford TL, Cabuy E, Vindigni A, Enver T, Bell JI, Slijepcevic P, Goodnow CC, Jeggo PA, Cornall RJ (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447: 686-690.
40. O'Brien KP, Remm M, Sonnhammer ELL (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res 33 (Database Issue): D476-D480.
41. Park Y, Gerson SL (2005) DNA repair defects in stem cell function and aging. Annu Rev Med 56: 495-508.
42. Ramalho-Santos M, Soonsang Y, Matsuzaki Y, Mulligan RC, Melton DA (2002) "Stemness": Transcriptional profiling of embryonic and adult stem cells. Science 298: 597-600.
43. Ridgway P, Almouzni G (2000) CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair. J Cell Sci 113: 2647-2658.
44. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541-1544.
45. Robert JS (2004) Model systems in stem cell biology. BioEssays 26: 1005-1012.
46. Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York.
47. Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143: 1429-1438.
48. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoye T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463-472.
49. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814.
50. Scherer GF, Zahn M, Callis J, Jones AM (2007) A role for phospholipase A in auxin-regulated gene expression. FEBS Lett 581: 4205-4211.
51. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635-644.
52. Sena G, Wang X, Liu H-Y, Hofhuis H, Birnbaum KD (2009) Organ regeneration does not require a functional stem cell niche in plants. Nature 457: 1150-1153.
53. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7: 847-859.
54. Tseng GC, Wong WH (2005) Tight clustering: a resampling-based approach for identifying stable and tight patterns in data. Biometrics 61: 10-16.
55. van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signaling. Nature 378: 62-65.
56. Vernoux T, Benfey P (2005) Signals that regulate stem cell activity during plant development. Curr Opin Genet Dev 15: 388-394.
57. Vernoux T, Wilson RC, Seeley KA, Reichheld J-P, Muroy S, Brown S, Maughan SC, Cobbett CS, van Montagu M, Inzé D et al (2000) The root meristemless1/cadmium sensitive 2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97-110.
58. Wang H, Zhou Y, Fowke LC (2006) The emerging importance of cyclin-dependent kinase inhibitors in the regulation of the plant cell cycle and related processes. Can J Bot 84: 640-650.
59. Wildwater M, Campiho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123: 1337-1349.
60. 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.
61. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525-536.
62. Xu J, Hofhuis H, Heidstra R, Sauer M, J Friml J, Scheres B (2006) A molecular framework for plant regeneration. Science 311: 385-388.
63. Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 16: 2586-2600.
64. Zhu T, Budworth P, Chen W, Provart N, Chang H-S, Guimil S, Su WP, Zou G, Wang X (2003) Transcriptional control of nutrient partitioning during rice grain filling. Plant Biotechnol J 1: 59-70.
65. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719.
66. Zipori D (2004) The nature of stem cells: state rather than entity. Nat Rev Genet 5: 873-878.