, Volume 218, Issue 3, pp 370–378 | Cite as

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

  • Stein Erik Lid
  • Ronald H. Al
  • Trygve Krekling
  • Robert B. Meeley
  • Jerry Ranch
  • Hilde-Gunn Opsahl-Ferstad
  • Odd-Arne OlsenEmail author
Original Article


The maize (Zea mays L.) endosperm consists of an epidermal like layer of isodiametric aleurone cells surrounding a central body of starchy endosperm cells. In disorgal1 (dil1) and disorgal2 (dil2) mutants the control of the mitotic division plane is relaxed or missing, resulting in mature grains with disorganized aleurone layers. In addition to orientation of the division plane, both the shape and size of the aleurone cells are affected, and often more than one layer of aleurone cells is present. Homozygous dil1 and dil2 grains are shrunken due to reduced accumulation of starchy endosperm and premature developmental arrest of the embryo, and mature mutant grains germinate at a very low rate and fail to develop into plants. However, homozygous mutant plants can be obtained through embryo rescue, revealing that both mutants have an irregular leaf epidermis as well as roots with a strongly reduced number of root hairs and aberrant root hair morphology. Our results suggest the presence of common regulatory mechanisms for the control of cell division orientation in the aleurone and plant epidermis.


Aleurone Cell division orientation Endosperm Epidermis Zea 



days after pollination


defective kernel mutant


disorganized aleurone layer mutant




light microscopy


pre-prophase band


scanning electron microscopy


Trait Utility System for Corn



We thank Karin S. Olsen, Peter Sekkelsten, Berit Morken, Audrun Utskarpen and Christer R. Nielsen for technical assistance and mutant screening, and Lizabeth C. Meeley for field support.


  1. Abbe EC, Stein OL (1954) The growth of the shoot apex in maize: embryogeny. Am J Bot 41:285–293Google Scholar
  2. Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua N-H, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of Profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632Google Scholar
  3. Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127:4039–4048PubMedGoogle Scholar
  4. Becraft PW, Stinard PS, McCarthy D (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409PubMedGoogle Scholar
  5. Becraft PW, Brown RC, Lemmon BE, Olsen O-A, Opsahl-Ferstad H-G (2001) Endosperm development. In: Bhojwani SS (ed) Current trends in the embryology of angiosperms. Kluwer, Dordrecht, pp 353–374Google Scholar
  6. Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225PubMedGoogle Scholar
  7. Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnabel PS, Meeley RB, Briggs SP (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7:75–84PubMedGoogle Scholar
  8. Bosnes M, Weidemann F, Olsen O-A (1992) Endosperm differentiation in barley wild-type and sex mutants. Plant J 2:661–674Google Scholar
  9. Brown RC, Lemmon BE, Olsen O-A (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252Google Scholar
  10. Cleary AL, Smith LG (1998) The Tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10:1875–1888CrossRefPubMedGoogle Scholar
  11. Cleary AL, Gunning BES, Wasteneys GO, Hepler PK (1992) Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J Cell Sci 103:977–988Google Scholar
  12. Del Cerro M, Cogen M, Del Cerro C (1980) Stevenel’s blue, an excellent stain for optical microscopical study of plastic embedded tissue. Microsc Acta 83:117–121PubMedGoogle Scholar
  13. Gunning BES (1982) The cytokinetic apparatus: its development and spatial regulation. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 229–292Google Scholar
  14. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedGoogle Scholar
  15. Kalla R, Shimamoto K, Potter R, Nielsen R, Linnestad C, Olsen O-A (1994) The promoter of the barley aleurone specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone specific gene expression in transgenic rice. Plant J 4:849–860CrossRefGoogle Scholar
  16. Kessler S, Sriki S, Sinha N (2002) Xcl1 causes delayed oblique periclinal divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position. Development 129:1859–1869PubMedGoogle Scholar
  17. Kiesselbach TA (1949) The structure and reproduction of corn. Res Bull Univ Neb Coll Agric 161:96Google Scholar
  18. Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley RB, Nichols S, Olsen O-A (2002) The defective kernel1 (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 99:5460–5465CrossRefPubMedGoogle Scholar
  19. Mineyuki Y (1999) The pre-prophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49Google Scholar
  20. Morrison IN, Kuo J, O’Brian TP (1975) Histochemistry and fine structure of developing aleurone cells. Planta 123:105–116Google Scholar
  21. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–498Google Scholar
  22. Nelson OE, Chang MT (1974) Effect of multiple aleurone layers on the protein and amino acid content of maize endosperm. Crop Sci 14:374–376Google Scholar
  23. Olsen O-A (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267CrossRefPubMedGoogle Scholar
  24. Olsen O-A, Brown RC, Lemmon BE (1998) A model for aleurone cell development. Trends Plant Sci 3:168–169CrossRefGoogle Scholar
  25. Pickett-Heaps JD, Northcote HD (1966) Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci 1:109–120PubMedGoogle Scholar
  26. Randolph LF (1936) Developmental morphology of the caryopsis in maize. J Agric Res 53:881–916Google Scholar
  27. Ringli C, Baumberger N, Diet A, Frey B, Keller B (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 129:1464–1472CrossRefPubMedGoogle Scholar
  28. 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 100:6552–6557CrossRefPubMedGoogle Scholar
  29. Smith LG, Hake S, Sylvester AW (1996) The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122:481–489PubMedGoogle Scholar
  30. Smith LG, Gerttula SM, Han S, Levy J (2001) TANGLED1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol 152:231–236CrossRefPubMedGoogle Scholar
  31. Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84:821–824PubMedGoogle Scholar
  32. Staiger CJ, Gibbon BC, Kovar DR, Zonia LE (1997) Profilin and actin depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci 2:275–281CrossRefGoogle Scholar
  33. Walbot V (1994) Overview of key steps in aleurone development. In: Freeling M, Walbot V (eds) The maize handbook. Springer, Berlin Heidelberg New York, pp 78–80Google Scholar
  34. Verma DPS (2001) Cytokinesis and building of the cell plate in plants. Annu Rev Plant Physiol Plant Mol Biol 52:751–784Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Stein Erik Lid
    • 2
  • Ronald H. Al
    • 2
  • Trygve Krekling
    • 2
  • Robert B. Meeley
    • 1
  • Jerry Ranch
    • 1
  • Hilde-Gunn Opsahl-Ferstad
    • 2
  • Odd-Arne Olsen
    • 1
    • 2
    Email author
  1. 1.Pioneer Hi-Bred InternationalJohnstonUSA
  2. 2.Department of Chemistry and BiotechnologyAgricultural University of Norway ÅsNorway

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