Calpain-Mediated Positional Information Directs Cell Wall Orientation to Sustain Plant Stem Cell Activity, Growth and Development

Plant and Cell Physiology

Volumn 56, Issue 9, 2014, Pages 1855-1866

  Liang, Zhe ^a,d   Brown, Roy C ^b   Fletcher, Jennifer C ^c   Opsahl Sorteberg, Hilde Gunn ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Calpain; Cell cycle; Cell wall positioning; Embryo development; Microtubule organization; Stem cell and meristem regulation

Indexed keywords

ARABIDOPSIS PROTEIN; CALPAIN; DEK1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CELL DIVISION; CELL PROLIFERATION; CELL WALL; CYTOLOGY; EMBRYOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; MICROTUBULE; PHENOTYPE; PLANT CELL; PLANT DEVELOPMENT; PLANT SEED; PROMOTER REGION; STEM CELL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALPAIN; CELL DIVISION; CELL PROLIFERATION; CELL WALL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MERISTEM; MICROTUBULES; PHENOTYPE; PLANT CELLS; PLANT DEVELOPMENT; PROMOTER REGIONS, GENETIC; SEEDS; STEM CELLS;

EID: 84941254482     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv110     Document Type: Article

References (69)

1. Abe, M., Katsumata, H., Komeda, Y. and Takahashi, T. (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130: 635-643.
2. Aoyama, T. and Chua, N.H. (1997) A glucocorticoid-mediated transcrip-tional induction system in transgenic plants. Plant J. 11: 605-612.
3. Bano, D., Dinsdale, D., Cabrera-Socorro, A., Maida, S., Lambacher, N., McColl, B., et al. (2010) Alteration of the nuclear pore complex in Ca(2+)-mediated cell death. Cell Death Differ. 17: 119-133.
4. Becraft, P.W. and Yi, G. (2011) Regulation of aleurone development in cereal grains. J. Exp. Bot. 62: 1669-1675.
5. Bemis, S.M. and Torii, K.U. (2007) Autonomy of cell proliferation and developmental programs during Arabidopsis aboveground organ morphogenesis. Dev. Biol. 304: 367-381.
6. Bergounioux, J., Elisee, R., Prunier, A.L., Donnadieu, F., Sperandio, B., Sansonetti, P., et al. (2012) Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe 11: 240-252.
7. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. and Simon, R. (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617-619.
8. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. and Laux, T. (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14: 867-876.
9. Brown, R.C. and Lemmon, B.E. (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215: 35-49.
10. Brown, R.C., Lemmon, B.E. and Olsen, O.A. (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6: 1241-1252.
11. Burke, B. and Stewart, C.L. (2013) The nuclear lamins: flexibility in function. Nat. Rev. Mol. Cell Biol. 14: 13-24.
12. Byrne, M.E., Barley, R., Curtis, M., Arroyo, J.M., Dunham, M., Hudson, A., et al. (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967-971.
13. Byrne, M.E., Simorowski, J. and Martienssen, R.A. (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957-1965.
14. Chakraborti, S., Alam, M.N., Paik, D., Shaikh, S. and Chakraborti, T. (2012) Implications of calpains in health and diseases. Indian J. Biochem. Biol. 49: 316-328.
15. Chan, J., Calder, G., Fox, S. and Lloyd, C. (2005) Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17: 1737-1748.
16. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
17. Conacci-Sorrell, M. and Eisenman, R.N. (2011) Post-translational control of Myc function during differentiation. Cell Cycle 10: 604-610.
18. Concha, C., Monardes, A., Even, Y., Morin, V., Puchi, M., Imschenetzky, M., et al. (2005) Inhibition of cysteine protease activity disturbs DNA replication and prevents mitosis in the early mitotic cell cycles of sea urchin embryos. J. Cell Physiol. 204: 693-703.
19. Croall, D.E. and Ersfeld, K. (2007) The calpains: modular designs and functional diversity. Genome Biol. 8: 218.
20. Crowell, E.F., Timpano, H., Desprez, T., Franssen-Verheijen, T., Emons, A.M., Hofte, H., et al. (2011) Differential regulation of cellulose orientation at the inner and outer face of epidermal cells in the Arabidopsis hypocotyl. Plant Cell 23: 2592-2605.
21. Delcerro, M., Cogen, J. and Cerro, C.D. (1980) Stevenels blue, an excellent stain for optical microscopical study of plastic embedded tissues. Microsc. Acta 83: 117-121.
22. Demko, V., Perroud, P.F., Johansen, W., Delwiche, C.F., Cooper, E.D., Remme, P., et al. (2014) Genetic analysis of DEFECTIVE KERNEL1 loop function in three-dimensional body patterning in Physcomitrella patens. Plant Physiol. 166: 903-919.
23. Dhonukshe, P., Weits, D.A., Cruz-Ramirez, A., Deinum, E.E., Tindemans, S.H., Kakar, K., et al. (2013) A PLETHORA-auxin transcription module controls cell division plane rotation through MAP65 and CLASP. Cell 155: 1189-1189.
24. Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., et al. (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108: 661-673.
25. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., et al. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
26. Futai, E., Sorimachi, H., Jeong, S., Kitamoto, K., Ishiura, S. and Suzuki, K. (1999) Aspergillus oryzae palB(ory) encodes a calpain-like protease: homology to Emericella nidulans PalB and conservation of functional regions. J. Biosci. Bioeng. 88: 438-440.
27. Galletti, R., Johnson, K.L., Scofield, S., San-Bento, R., Watt, A.M., Murray, J.A., et al. (2015) DEFECTIVE KERNEL 1 promotes and maintains plant epidermal differentiation. Development 142: 1978-1983.
28. Gonzalez-Garcia, M.P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-Garcia, S., Russinova, E., et al. (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138: 849-859.
29. Haecker, A., Gross-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H., Herrmann, M., et al. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657-668.
30. Jackson, D. (1991) In Situ Hybridization in Plants. Oxford University Press, Oxford.
31. Javelle, M., Vernoud, V., Rogowsky, P.M. and Ingram, G.C. (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol. 189: 17-39.
32. Johnson, K.L., Degnan, K.A., Walker, J.R. and Ingram, G.C. (2005) AtDEK1 is essential for specification of embryonic epidermal cell fate. Plant J. 44: 114-127.
33. Johnson, K.L., Faulkner, C., Jeffree, C.E. and Ingram, G.C. (2008) The Phytocalpain Defective Kernel 1 is a novel Arabidopsis growth regulator whose activity is regulated by proteolytic processing. Plant Cell 20: 2619-2630.
34. Knauer, S., Holt, A.L., Rubio-Somoza, I., Tucker, E.J., Hinze, A., Pisch, M., et al. (2013) A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev. Cell 24: 125-132.
35. Lenhard, M., Jurgens, G. and Laux, T. (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129: 3195-3206.
36. Liang, Z., Demko, V., Wilson, R.C., Johnson, K.A., Ahmad, R., Perroud, P.F., et al. (2013) The catalytic domain CysPc of the DEK1 calpain is functionally conserved in land plants. Plant J. 75: 742-754.
37. Lid, S.E., Gruis, D., Jung, R., Lorentzen, J.A., Ananiev, E., Chamberlin, M., et al. (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc. Natl. Acad. Sci. USA 99: 5460-5465.
38. Lid, S.E., Olsen, L., Nestestog, R., Aukerman, M., Brown, R.C., Lemmon, B., et al. (2005) Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally. Planta 221: 339-351.
39. Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K. (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
40. Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., Jurgens, G. and Laux, T. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
41. Muller, S., Wright, A.J. and Smith, L.G. (2009) Division plane control in plants: new players in the band. Trends Cell Biol. 19: 180-188.
42. Murray, J.A.H., Jones, A., Godin, C. and Traas, J. (2012) Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell 24: 3907-3919.
43. Nodine, M.D. and Bartel, D.P. (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482: 94-97.
44. Oda, Y. and Fukuda, H. (2012) Initiation of cell wall pattern by a rho-and microtubule-driven symmetry breaking. Science 337: 1333-1336.
45. Olsen, L.T., Divon, H.H., Al, R., Fosnes, K., Lid, S.E. and Opsahl-Sorteberg, H.G. (2008) The defective seed5 (des5) mutant: effects on barley seed development and HvDek1, HvCr4, and HvSal1 gene regulation. J. Exp. Bot. 59: 3753-3765.
46. Opsahl-Sorteberg, H.G., Divon, H.H., Nielsen, P.S., Kalla, R., Hammond-Kosack, B., Shimamoto, K., et al. (2004) Identification of a 49-bp fragment of the HvLTP2 promoter directing aleurone cell specific expression. Gene 341: 49-58.
47. Perroud, P.F., Demko, V., Johansen, W., Wilson, R.C., Olsen, O.A. and Quatrano, R.S. (2014) Defective Kernel 1 (DEK1) is required for three-dimensional growth in Physcomitrella patens. New Phytol. 203: 794-804.
48. Robinson, D.O. and Roeder, A.H. (2015) Themes and variations in cell type patterning in the plant epidermis. Curr. Opin. Genet. Dev. 32C: 55-65.
49. Roeder, A.H.K., Cunha, A., Ohno, C.K. and Meyerowitz, E.M. (2012) Cell cycle regulates cell type in the Arabidopsis sepal. Development 139: 4416-4427.
50. Santos, D.M., Xavier, J.M., Morgado, A.L., Sola, S. and Rodrigues, C.M.P. (2012) Distinct regulatory functions of Calpain 1 and 2 during neural stem cell self-renewal and differentiation. PLoS One 7: e33468.
51. Savaldi-Goldstein, S., Peto, C. and Chory, J. (2007) The epidermis both drives and restricts plant shoot growth. Nature 446: 199-202.
52. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jurgens, G. and 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.
53. Sessions, A., Weigel, D. and Yanofsky, M.F. (1999) The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meri-stems and young primordia. Plant J. 20: 259-263.
54. Smith, L.G., Gerttula, S.M., Han, S. and Levy, J. (2001) Tangled1: a micro-tubule binding protein required for the spatial control of cytokinesis in maize. J. Cell Biol. 152: 231-236.
55. Sorimachi, H., Hata, S. and Ono, Y. (2011) Impact of genetic insights into calpain biology. J. Biochem. 150: 23-37.
56. Spinner, L., Gadeyne, A., Belcram, K., Goussot, M., Moison, M., Duroc, Y., et al. (2013) A protein phosphatase 2A complex spatially controls plant cell division. Nat. Commun. 4: 1863.
57. Steeves, T.A. and Sussex, I.M. (1989) Patterns in Plant Development. Cambridge University Press, New York.
58. Takada, S. and Jurgens, G. (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134: 1141-1150.
59. Takada, S., Takada, N. and Yoshida, A. (2013) ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140: 1919-1923.
60. Tian, Q., Olsen, L., Sun, B., Lid, S.E., Brown, R.C., Lemmon, B.E., et al. (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19: 3127-3145.
61. Uyttewaal, M., Burian, A., Alim, K., Landrein, B.T., Borowska-Wykret, D., Dedieu, A., et al. (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149: 439-451.
62. Vollmer, A.H., Youssef, N.N. and DeWald, D.B. (2011) Unique cell wall abnormalities in the putative phosphoinositide phosphatase mutant AtSAC9. Planta 234: 993-1005.
63. Wang, C., Barry, J.K., Min, Z., Tordsen, G., Rao, A.G. and Olsen, O.A. (2003) The calpain domain of the maize DEK1 protein contains the conserved catalytic triad and functions as a cysteine proteinase. J. Biol. Chem. 278: 34467-34474.
64. +-translocating inorganic pyrophosphatase (Vpp1) marks partial aleurone cell fate in cereal endosperm development. Plant Mol. Biol. 56: 325-337.
65. Wurschum, T., Gross-Hardt, R. and Laux, T. (2006) APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18: 295-307.
66. Xu, X.F.M., Zhao, Q., Rodrigo-Peiris, T., Brkljacic, J., He, C.S., Muller, S., et al. (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc. Natl. Acad. Sci. USA 105: 18637-18642.
67. Yadav, R.K., Perales, M., Gruel, J., Girke, T., Jonsson, H. and Reddy, G.V. (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25: 2025-2030.
68. Yi, G., Lauter, A.M., Scott, M.P. and Becraft, P.W. (2011) The thick aleur-one1 mutant defines a negative regulation of maize aleurone cell fate that functions downstream of defective kernel1. Plant Physiol. 156: 1826-1836.
69. Zhao, S., Liang, Z., Demko, V., Wilson, R., Johansen, W., Olsen, O.A., et al. (2012) Massive expansion of the calpain gene family in unicellular eukaryotes. BMC Evol. Biol. 12: 193.