Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis

Plant Cell

Volumn 23, Issue 9, 2011, Pages 3260-3275

  Pillitteri, Lynn Jo ^a,b   Peterson, Kylee M ^a   Horst, Robin J ^a   Torii, Keiko U ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WESTERN WASHINGTON UNIVERSITY   (United States)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80055034922     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.088583     Document Type: Article

References (76)

1. Abrash, E.B., and Bergmann, D.C. (2009). Asymmetric cell divisions: A view from plant development. Dev. Cell 16: 783-796.
2. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
3. Bergmann, D.C., Lukowitz, W., and Somerville, C.R. (2004). Stomatal development and pattern controlled by a MAPKK kinase. Science 304: 1494-1497.
4. Bergmann, D.C., and Sack, F.D. (2007). Stomatal development. Annu. Rev. Plant Biol. 58: 163-181.
5. Borner, G.H., Sherrier, D.J., Stevens, T.J., Arkin, I.T., and Dupree, P. (2002). Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A genomic analysis. Plant Physiol. 129: 486-499.
6. Boudolf, V., et al. (2009). CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol. 150: 1482-1493.
7. Burkhard, P., Stetefeld, J., and Strelkov, S.V. (2001). Coiled coils: A highly versatile protein folding motif. Trends Cell Biol. 11: 82-88.
8. Chung, H.S., and Howe, G.A. (2009). A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21: 131-145.
9. Clark, S.E., Running, M.P., and Meyerowitz, E.M. (1993). CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119: 397-418.
10. Day, R.C., McNoe, L., and Macknight, R.C. (2007). Evaluation of global RNA amplification and its use for high-throughput transcript analysis of laser-microdissected endosperm. Int. J. Plant Genomics 2007: 61028.
11. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.N. (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.
12. Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J., and Benfey, P.N. (2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320: 942-945.
13. Dong, J., MacAlister, C.A., and Bergmann, D.C. (2009). BASL controls asymmetric cell division in Arabidopsis. Cell 137: 1320-1330.
14. Edgar, R., Domrachev, M., and Lash, A.E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
15. Engler, Jde. A., et al. (2009). Systematic analysis of cell-cycle gene expression during Arabidopsis development. Plant J. 59: 645-660.
16. Fichelson, P., Moch, C., Ivanovitch, K., Martin, C., Sidor, C.M., Lepesant, J.A., Bellaiche, Y., and Huynh, J.R. (2009). Live-imaging of single stem cells within their niche reveals that a U3snoRNP component segregates asymmetrically and is required for self-renewal in Drosophila. Nat. Cell Biol. 11: 685-693.
17. Fisher, K., and Turner, S. (2007). PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17: 1061-1066.
18. Geisler, M., Nadeau, J., and Sack, F.D. (2000). Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12: 2075-2086.
19. Hara, K., Kajita, R., Torii, K.U., Bergmann, D.C., and Kakimoto, T. (2007). The secretory peptide gene EPF1 enforces the stomatal onecell- spacing rule. Genes Dev. 21: 1720-1725.
20. Hara, K., Yokoo, T., Kajita, R., Onishi, T., Yahata, S., Peterson, K.M., Torii, K.U., and Kakimoto, T. (2009). Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol. 50: 1019-1031.
21. Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kreps, J.A., and Kay, S.A. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
22. Hord, C.L., Sun, Y.J., Pillitteri, L.J., Torii, K.U., Wang, H., Zhang, S., and Ma, H. (2008). Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol. Plant 1: 645-658.
23. Hunt, L., and Gray, J.E. (2009). The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19: 864-869.
24. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., and Kakimoto, T. (2001). Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063.
25. Iyer-Pascuzzi, A.S., and Benfey, P.N. (2010). Fluorescence-activated cell sorting in plant developmental biology. Methods Mol. Biol. 655: 313-319.
26. Jia, G., Liu, X., Owen, H.A., and Zhao, D. (2008). Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc. Natl. Acad. Sci. USA 105: 2220-2225.
27. Jun, J., Fiume, E., Roeder, A.H., Meng, L., Sharma, V.K., Osmont, K.S., Baker, C., Ha, C.M., Meyerowitz, E.M., Feldman, L.J., and Fletcher, J.C. (2010). Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol. 154: 1721-1736.
28. Kanaoka, M.M., Pillitteri, L.J., Fujii, H., Yoshida, Y., Bogenschutz, N.L., Takabayashi, J., Zhu, J.K., and Torii, K.U. (2008). SCREAM/ ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation. Plant Cell 20: 1775-1785.
29. Kerk, N.M., Ceserani, T., Tausta, S.L., Sussex, I.M., and Nelson, T.M. (2003). Laser capture microdissection of cells from plant tissues. Plant Physiol. 132: 27-35.
30. Kiba, T., Yamada, H., and Mizuno, T. (2002). Characterization of the ARR15 and ARR16 response regulators with special reference to the cytokinin signaling pathway mediated by the AHK4 histidine kinase in roots of Arabidopsis thaliana. Plant Cell Physiol. 43: 1059-1066.
31. Kondo, Y., Hirakawa, Y., Kieber, J.J., and Fukuda, H. (2011). CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol. 52: 37-48.
32. Kono, A., Umeda-Hara, C., Adachi, S., Nagata, N., Konomi, M., Nakagawa, T., Uchimiya, H., and Umeda, M. (2007). The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19: 1265-1277.
33. Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J., and Lohmann, J.U. (2005). WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438: 1172-1175.
34. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
35. Lohse, M., et al. (2010). Robin: an intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 153: 642-651.
36. Lupas, A., Van Dyke, M., and Stock, J. (1991). Predicting coiled coils from protein sequences. Science 252: 1162-1164.
37. MacAlister, C.A., Ohashi-Ito, K., and Bergmann, D.C. (2007). Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445: 537-540.
38. Menke, F.L., and Scheres, B. (2009). Plant asymmetric cell division, vive la différence! Cell 137: 1189-1192.
39. Nakamura, R.L., McKendree, W.L., Jr., Hirsch, R.E., Sedbrook, J.C., Gaber, R.F., and Sussman, M.R. (1995). Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol. 109: 371-374.
40. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41.
41. Nakagawa, T., Nakamura, S., Tanaka, K., Kawamukai, M., Suzuki, T., Nakamura, K., Kimura, T., and Ishiguro, S. (2008). Development of R4 gateway binary vectors (R4pGWB) enabling high-throughput promoter swapping for plant research. Biosci. Biotechnol. Biochem. 72: 624-629.
42. Nakazono, M., Qiu, F., Borsuk, L.A., and Schnable, P.S. (2003). Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: Identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15: 583-596.
43. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51: 1126-1136.
44. Obayashi, T., Nishida, K., Kasahara, K., and Kinoshita, K. (2011). ATTED-II updates: Condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol. 52: 213-219.
45. O'Connor, T.R., Dyreson, C., and Wyrick, J.J. (2005). Athena: A resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21: 4411-4413.
46. Ohashi-Ito, K., and Bergmann, D.C. (2006). Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18: 2493-2505.
47. Peterson, K.M., Rychel, A.L., and Torii, K.U. (2010). Out of the mouths of plants: The molecular basis of the evolution and diversity of stomatal development. Plant Cell 22: 296-306.
48. Pillitteri, L.J., Bemis, S.M., Shpak, E.D., and Torii, K.U. (2007b). Haploinsufficiency after successive loss of signaling reveals a role for ERECTA-family genes in Arabidopsis ovule development. Development 134: 3099-3109.
49. Pillitteri, L.J., Bogenschutz, N.L., and Torii, K.U. (2008). The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. Plant Cell Physiol. 49: 934-943.
50. Pillitteri, L.J., Sloan, D.B., Bogenschutz, N.L., and Torii, K.U. (2007a). Termination of asymmetric cell division and differentiation of stomata. Nature 445: 501-505.
51. Pillitteri, L.J., and Torii, K.U. (2007). Breaking the silence: Three bHLH proteins direct cell-fate decisions during stomatal development. Bioessays 29: 861-870.
52. Ren, B., Liang, Y., Deng, Y., Chen, Q., Zhang, J., Yang, X., and Zuo, J. (2009). Genome-wide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res. 19: 1178-1190.
53. Rowe, M.H., and Bergmann, D.C. (2010). Complex signals for simple cells: The expanding ranks of signals and receptors guiding stomatal development. Curr. Opin. Plant Biol. 13: 548-555.
54. Rychel, A.L., Peterson, K.M., and Torii, K.U. (2010). Plant twitter: Ligands under 140 amino acids enforcing stomatal patterning. J. Plant Res. 123: 275-280.
55. Sachs, T. (1991). Pattern Formation in Plant Tissues. (Cambridge, UK: Cambridge University Press).
56. Saeed, A.I., et al. (2003). TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
57. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and Laux, T. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814.
58. Schachtman, D.P., Schroeder, J.I., Lucas, W.J., Anderson, J.A., and Gaber, R.F. (1992). Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258: 1654-1658.
59. Scheres, B. (2002). Plant patterning: TRY to inhibit your neighbors. Curr. Biol. 12: R804-R806.
60. Schmülling, T., Werner, T., Riefler, M., Krupková, E., and Bartrinay Manns, I. (2003). Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant Res. 116: 241-252.
61. Sena, G., Wang, X., Liu, H.Y., Hofhuis, H., and Birnbaum, K.D. (2009). Organ regeneration does not require a functional stem cell niche in plants. Nature 457: 1150-1153.
62. Sessions, A., Weigel, D., and Yanofsky, M.F. (1999). The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20: 259-263.
63. Shpak, E.D., Berthiaume, C.T., Hill, E.J., and Torii, K.U. (2004). Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131: 1491-1501.
64. Shpak, E.D., Lakeman, M.B., and Torii, K.U. (2003). Dominantnegative receptor uncovers redundancy in the Arabidopsis ERECTA Leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15: 1095-1110.
65. Shpak, E.D., McAbee, J.M., Pillitteri, L.J., and Torii, K.U. (2005). Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309: 290-293.
66. Stolz, A., Riefler, M., Lomin, S.N., Achazi, K., Romanov, G.A., and Schmülling, T. (2011). The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. Plant J. 67: 157-168.
67. ten Hove, C.A., Willemsen, V., de Vries, W.J., van Dijken, A., Scheres, B., and Heidstra, R. (2010). SCHIZORIZA encodes a nuclear factor regulating asymmetry of stem cell divisions in the Arabidopsis root. Curr. Biol. 20: 452-457.
68. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L.A., Rhee, S.Y., and Stitt, M. (2004). MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37: 914-939.
69. Torii, K.U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R.F., and Komeda, Y. (1996). The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735-746.
70. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Bläsing, O.E., Redestig, H., Sreenivasulu, N., Krall, L., Hannah, M.A., Poree, F., Fernie, A.R., and Stitt, M. (2006). PageMan: An interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7: 535.
71. Vanneste, S., et al. (2011). Developmental regulation of CYCA2s contributes to tissue-specific proliferation in Arabidopsis. EMBO J. 30: 3430-3441.
72. Van Leene, J., Boruc, J., De Jaeger, G., Russinova, E., and De Veylder, L. (2011). A kaleidoscopic view of the Arabidopsis core cell cycle interactome. Trends Plant Sci. 16: 141-150.
73. Werner, T., Köllmer, I., Bartrina, I., Holst, K., and Schmülling, T. (2006). New insights into the biology of cytokinin degradation. Plant Biol. 8: 371-381.
74. Yadav, R., Girke, T., Pasala, S., Xie, M., and Reddy, G.V. (2009). Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl. Acad. Sci. USA 106: 4941-4946.
75. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T., and Mizuno, T. (2001). The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42: 1017-1023.
76. Zhao, D.Z., Wang, G.F., Speal, B., and Ma, H. (2002). The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16: 2021-2031.