Abstract
A T-DNA insertion in the Arabidopsis thaliana DEK1 gene, encoding a calpain-like cysteine proteinase with a predicted membrane anchor, causes unorganized embryo development displaying irregular mitotic divisions in the embryo proper and suspensor. Embryo development is arrested at the globular stage, and the embryo proper lacks a defined protoderm. In the endosperm, the aleurone-like peripheral cell layer is partly or completely lacking. The Arabidopsis DEK1 wild-type transcript is expressed evenly throughout the endosperm and the embryo in developing seed as determined using in situ hybridization. The conclusion that the observed phenotype is caused by a T-DNA insertion in the Arabidopsis DEK1 gene is confirmed by complementation with the Arabidopisis DEK1 genomic sequence, as well as analysis of a second T-DNA insertion allele. Over-expression of the Arabidopsis DEK1 gene coding sequence under the control of the 35S promoter causes a number of developmental phenotypes, including a global lack of trichomes, leaves exhibiting improper dorsiventral symmetry and aberrant cell organization in flowers. We interpret the data to suggest a role for DEK1 in providing cells with positional clues for an appropriate developmental context within plant tissues.
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Abbreviations
- DAP:
-
Days after pollination
- dek:
-
Defective kernel
- MPSS:
-
Massively parallel signature sequencing
- PPB:
-
Preprophase band
References
Ahn J-W, Kim M, Lim JH, Kim G-T, Pai H-S (2004) Phytocalpain controls the proliferation and differentiation fates of cells in plant organ development. Plant J 38:969–981
Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127:4039–4048
Becraft PW, Stinard PS, McCarthy D (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409
Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225
Berger F (2003) Endosperm: the crossroad of seed development. Curr Opin Plant Biol 6:42–50
Bowman JL (2000) Axial patterning in leaves and other lateral organs. Curr Opin Genet Dev 10:399–404
Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634
Brown R, Lemmon BE, Nguyen H, Olsen O-A (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42
Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res 13:4777–4788
Galbiati M, Moreno MA, Nadzan G, Zourelidou M, Dellaporta SL (2000) Large-scale T-DNA mutagenesis in Arabidopsis for functional genomic analysis. Funct Integr Genomics 1:25–34
Gardner RC, Howarth AJ, Hahn P, Brown-Luedi M, Shepherd RJ, Messing J (1981) The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acids Res 9:2871–2888
Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organization during ovule integument and sepal margin development. Development 130:4249–4258
Jackson DP (1991) In situ hybridisation in plants. In: Bowles DJ, Gurr SJ, McPherson M (eds) Molecular plant pathology: a practical approach. Oxford University Press, Oxford, pp 163–174
Larkin J, Brown M, Schiefelbein J (2003) How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 54:403–430
Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen O-A (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
Lid SE, Al RH, Krekling T, Meeley RB, Ranch J, Opsahl-Ferstad H-G, Olsen O-A (2004) The maize disorganized aleurone layer 1 and 2 (dil1, dil2) mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378
Lu P, Porat R, Nadeau JA, O’Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8:2155–2168
Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin related KNOLLE gene product. Cell 84:61–71
Marks M (1997) Molecular genetic analysis of trichome development in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 48:137–163
Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49
Murashige T, Skoog T (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497
Nguyen H, Brown RC, Lemmon BE (2002) Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicacaceae). Protoplasma 219:210–220
Olsen O-A (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:S214–S227
Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493
Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156:1349–1362
Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399
Rosso MG, Li Y, Strizhov N, Reis B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259
Sato K, Kawashima S (2001) Calpain function in the modulation of signal transduction molecules. Biol Chem 382:743–751
Schellmann S, Schnittger A, Kirik V, Wada T, Okada A, Beermann K, Thumfahrt J, Jürgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046
Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6:74–78
Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen O-A (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Natl Acad Sci USA 100:6552–6557
Sheridan WF, Neuffer MG (1980) Defective kernel mutants of maize. II. Morphological and embryo culture studies. Genetics 95:945–960
Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983
Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jurgens G, Mayer U (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol 12:153–158
Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116
Waizenegger I, Lukowitz W, Assaad F, Schwarz H, Jurgens G, Mayer U (2000) The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis. Curr Biol 10:1371–1374
Walker AR, Davison PA, Bolognesi-P.A.Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1350
Wang C, Barry JK, Min Z, Tordsen G, Rao AG, 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
Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308
Acknowledgments
We would like to thank Barbro Sæther (Norwegian Arabidopsis Research Centre, University of Oslo, Norway) for help with in situ hybridizations, Elin Ørmen and Trygve Krekling (Agricultural University of Norway) for technical assistance with microscopy techniques, Kjetil Fosnes (Agricultural University of Norway) for technical assistance with construct design and Fred Gruis (Pioneer Hi-Bred) for critical reading of this manuscript. The work of S.E. Lid, L. Olsen, R. Nestestog and H-G. Opsahl-Sorteberg was supported by the Norwegian Research Council.
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Lid, S.E., Olsen, L., Nestestog, R. et al. Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally. Planta 221, 339–351 (2005). https://doi.org/10.1007/s00425-004-1448-6
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DOI: https://doi.org/10.1007/s00425-004-1448-6