Skip to main content
Log in

Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

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

    Article  CAS  PubMed  Google Scholar 

  • Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127:4039–4048

    CAS  PubMed  Google Scholar 

  • Becraft PW, Stinard PS, McCarthy D (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Berger F (2003) Endosperm: the crossroad of seed development. Curr Opin Plant Biol 6:42–50

    Article  Google Scholar 

  • Bowman JL (2000) Axial patterning in leaves and other lateral organs. Curr Opin Genet Dev 10:399–404

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Brown R, Lemmon BE, Nguyen H, Olsen O-A (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42

    Article  Google Scholar 

  • Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin related KNOLLE gene product. Cell 84:61–71

    CAS  PubMed  Google Scholar 

  • Marks M (1997) Molecular genetic analysis of trichome development in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 48:137–163

    Article  Google Scholar 

  • Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49

    Google Scholar 

  • Murashige T, Skoog T (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Nguyen H, Brown RC, Lemmon BE (2002) Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicacaceae). Protoplasma 219:210–220

    Article  Google Scholar 

  • Olsen O-A (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:S214–S227

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Sato K, Kawashima S (2001) Calpain function in the modulation of signal transduction molecules. Biol Chem 382:743–751

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sheridan WF, Neuffer MG (1980) Defective kernel mutants of maize. II. Morphological and embryo culture studies. Genetics 95:945–960

    Google Scholar 

  • Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Odd-Arne Olsen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1448-6

Keywords

Navigation