Advertisement

Plant Molecular Biology

, Volume 61, Issue 4–5, pp 757–768 | Cite as

The auxin-induced K+ channel gene Zmk1 in maize functions in coleoptile growth and is required for embryo development

  • Katrin Philippar
  • Kai Büchsenschütz
  • David Edwards
  • Julia Löffler
  • Hartwig Lüthen
  • Erhard Kranz
  • Keith J. Edwards
  • Rainer Hedrich
Article

Abstract

The transcript level and in turn protein density of the K+-uptake channel ZMK1 in maize (Zea mays) coleoptiles is controlled by the phytohormone auxin. ZMK1 is involved in auxin-regulated coleoptile elongation as well as gravi- and phototropism. To provide unequivocal evidence for the role of ZMK1 in these elementary processes we screened for maize plants containing a Mutator-tagged Zmk1 gene. In a site-selected approach, we were able to identify three independent alleles of Mutator-transposon insertions in Zmk1. zmk1-m1::Mu1 plants were characterised by a Mu1 transposon inside intron 1 of ZMK1. When we analysed the Zmk1-transcript abundance in growing coleoptiles of these homozygous mutants, however, we found the K+-channel allele overexpressed. In consequence, elevated levels of K+-channel transcripts resulted in a growth phenotype as expected from more efficient K+-uptake, representing a central factor for turgor formation. Following Zmk1 expression during maize embryogenesis, we found this K+-channel gene constitutively expressed throughout embryo development and upregulated in late stages. In line with a vital role in embryogenesis, the mutations of exon 2 and intron 2 of Zmk1-zmk1-m2::Mu8 and zmk1-m3::MuA2-caused a lethal, defective-kernel phenotype. Thus, these results demonstrate the central role of the auxin-regulated K+-channel gene Zmk1 in coleoptile growth and embryo development.

Keywords

Auxin Coleoptile growth Embryo development K+ channel Maize Mutator transposons 

Abbreviations

ZMK1

Zea mays K+ channel 1

Mutator

Mu

IAA

indole-3-acetic acid

TEA

tetraethylammonium

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbe, EC, Stein, OL 1954The growth of the shoot apex in maize: embryogenyAm J Bot41285293CrossRefGoogle Scholar
  2. Bandurski, RS 1998Metabolic targets for control of IAA levels in maizeProc 25th Annu Meeting Plant Growth Regul Soc Am26181186Google Scholar
  3. Barkan, A, Martienssen, RA 1991Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1Proc Natl Acad Sci USA8835023506PubMedCrossRefGoogle Scholar
  4. Bennetzen, JL 1996The Mutator transposable element system of maizeCurr Top Microbiol Immunol204195229PubMedGoogle Scholar
  5. Bennetzen, JL, Swanson, J, Taylor, WC, Freeling, M 1984DNA insertion in the first intron of maize Adh1 affects message levels: cloning of progenitor and mutant Adh1 allelesProc Natl Acad Sci USA8141254128PubMedCrossRefGoogle Scholar
  6. Bensen, RJ, Johal, GS, Crane, VC, Tossberg, JT, Schnable, PS, Meeley, RB, Briggs, SP 1995Cloning and characterization of the maize An1 genePlant Cell77584PubMedCrossRefGoogle Scholar
  7. Blauth, SL, Kim, KN, Klucinec, J, Shannon, JC, Thompson, D, Guiltinan, M 2002Identification of mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays LPlant Mol Biol48287297PubMedCrossRefGoogle Scholar
  8. Callis, J, Fromm, M, Walbot, V 1987Introns increase gene expression in cultured maize cellsGenes Dev111831200PubMedGoogle Scholar
  9. Chen, JG, Ullah, H, Young, JC, Sussman, MR, Jones, AM 2001ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesisGenes Dev15902911PubMedCrossRefGoogle Scholar
  10. Claussen, M, Lüthen, H, Blatt, M, Böttger, M 1997Auxin-induced growth and its linkage to potassium channelsPlanta201227234CrossRefGoogle Scholar
  11. Darwin, C 1880The power of movements in plantsJohn MurrayAlbemarle Street, LondonGoogle Scholar
  12. Das, L, Martiensen, R 1995Site-selected transposon mutagenesis at the hcf106 locus in maizePlant Cell7287294PubMedCrossRefGoogle Scholar
  13. Giudice, L, Manna, F, Massardo, DR, Motto, M, Alifano, P, Wolf, K 1990The Mu1 transposable element of maize contains two promoter signals recognized by the Escherichia coli RNA polymeraseMol Gen Genet22276Google Scholar
  14. Dellaporta, S 1994Plant DNA miniprep and microprep: versions 2.1–2.3Freeling, MWalbot, V eds. The maize handbookSpringer-Verlag New York, IncNew York522525Google Scholar
  15. Demarty, M, Morvan, C, Thellier, M 1978Exchange properties of isolated cell walls of Lemna minor LPlant Phys62477481Google Scholar
  16. Edwards, D, Coghill, J, Batley, J, Holdsworth, M, Edwards, KJ 2002aAmplification and detection of transposon insertion flanking sequences using fluorescent MuAFLPBioTechniques3210901097Google Scholar
  17. Edwards, D, Stevenson, D, Forsyth, A, Hegarty, M, Batley, J, Holdsworth, M, Edwards, KJ 2002bIdentification of transposon-tagged maize genes displaying homology to arrayed cDNA clones with the use of mutator insertion displayGenome Lett14855CrossRefGoogle Scholar
  18. Felle, H, Peters, W, Palme, K 1991The electrical response of maize to auxinsBiochim Biophys Acta1064199204PubMedCrossRefGoogle Scholar
  19. Felle, HH, Hanstein, S, Steinmeyer, R, Hedrich, R 2000Dynamics of ionic activities in the apoplast of the sub-stomatal cavity of intact Vicia faba leaves during stomatal closure evoked by ABA and darknessPlant J24297304PubMedCrossRefGoogle Scholar
  20. Fischer-Iglesias, C, Sundberg, B, Neuhaus, G, Jones, AM 2001Auxin distribution and transport during embryonic pattern formation in wheatPlant J26115129PubMedCrossRefGoogle Scholar
  21. Freeling, M, Walbot, V 1994The maize handbookSpringer-Verlag New York, IncNew YorkGoogle Scholar
  22. Frias, I, Caldeira, MT, Perez-Castineira, JR, Navarro-Avino, JP, Culianez-Macia, FA, Kuppinger, O, Stransky, H, Pages, M, Hager, A, Serrano, R 1996A major isoform of the maize plasma membrane H(+)-ATPase: characterization and induction by auxin in coleoptilesPlant Cell815331544PubMedCrossRefGoogle Scholar
  23. Friml, J 2003Auxin transport – shaping the plantCurr Opin Plant Biol6712PubMedCrossRefGoogle Scholar
  24. Friml, J, Palme, K 2002Polar auxin transport – old questions and new concepts?Plant Mol Biol49273284PubMedCrossRefGoogle Scholar
  25. Friml, J, Benkova, E, Mayer, U, Palme, K, Muster, G 2003Automated whole mount localisation techniques for plant seedlingsPlant J34115124PubMedCrossRefGoogle Scholar
  26. Fu, S, Meeley, R, Scanlon, MJ 2002Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesisPlant Cell1431193132PubMedCrossRefGoogle Scholar
  27. Fuchs, I, Philippar, K, Ljung, K, Sandberg, G, Hedrich, R 2003Blue light regulates an auxin-induced K+-channel gene in the maize coleoptileProc Natl Acad Sci USA1001179511800PubMedCrossRefGoogle Scholar
  28. Hager, A, Menzel, H, Krauss, A 1971Versuche und Hypothese zur Primärwirkung des Auxins beim StreckungswachstumPlanta1004775CrossRefGoogle Scholar
  29. Hager, A, Debus, G, Edel, HG, Stransky, H, Serrano, R 1991Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane proton ATPasePlanta185527537CrossRefGoogle Scholar
  30. Iino, M, Long, C, Wang, X 2001Auxin- and abscisic acid-dependent osmoregulation in protoplasts of Phaseolus vulgaris pulviniPlant Cell Phys4212191227CrossRefGoogle Scholar
  31. Kawai, M, Uchimiya, H 2000Coleoptile senescence in rice (Oryza sativa L.)Ann Bot86405414CrossRefGoogle Scholar
  32. Keller, CP, Volkenburgh, E 1996Osmoregulation by oat coleoptile protoplasts – effect of auxinPlant Phys11010071016Google Scholar
  33. Lid, SE, Meeley, RB, Min, Z, Nichols, S, Olsen, OA 2004Knock-out mutants of two members of the AGL2 subfamily of MADS-box genes expressed during maize kernel developmentPlant Sci167575582CrossRefGoogle Scholar
  34. Lisch, D 2002Mutator transposonsTrends Plant Sci7498504PubMedCrossRefGoogle Scholar
  35. Lohse, G, Hedrich, R 1992Characterization of the plasma membrane proton ATPase from Vicia faba guard cells modulation by extracellular factors and seasonal changesPlanta188206214CrossRefGoogle Scholar
  36. May, BP, Liu, H, Vollbrecht, E, Senior, L, Rabinowicz, PD, Roh, D, Pan, X, Stein, L, Freeling, M, Alexander, D, Martienssen, R 2003Maize-targeted mutagenesis: a knockout resource for maizeProc Natl Acad Sci USA1001154111546PubMedCrossRefGoogle Scholar
  37. McClintock, B 1950The origin and behavior of mutable loci in maizeProc Natl Acad Sci USA36344355PubMedCrossRefGoogle Scholar
  38. Meeley, RB, Briggs, SP 1995Reverse genetics for maizeMaize Genet Newslett696782Google Scholar
  39. Mena, M, Ambrose, BA, Meeley, RB, Briggs, SP, Yanofsky, MF, Schmidt, RJ 1996Diversification of C-function activity in maize flower developmentScience27415371540PubMedCrossRefGoogle Scholar
  40. Neuffer, MG, Sheridan, WF 1980Defective kernel mutants of maize. I. Genetic and lethality studiesGenetics95929944PubMedGoogle Scholar
  41. Olsen, OA 2001Endosperm development: cellularization and cell fate specificationAnnu Rev Plant Physiol Plant Mol Biol52233267PubMedCrossRefGoogle Scholar
  42. Philippar, K, Fuchs, I, Lüthen, H, Hoth, S, Bauer, C, Haga, K, Thiel, G, Ljung, K, Sandberg, G, Böttger, M, Becker, D, Hedrich, R 1999Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropismProc Natl Acad Sci USA961218612191PubMedCrossRefGoogle Scholar
  43. Philippar, K, Becker, D, Ljung, K, Sandberg, G, Edwards, K, Hedrich, R 2000Living with gravityTrends Plant Sci58687PubMedCrossRefGoogle Scholar
  44. Philippar, K, Büchsenschütz, K, Abshagen, M, Fuchs, I, Geiger, D, Lacombe, B, Hedrich, R 2003The K+ channel KZM1 is capable to mediate potassium uptake into the phloem and guard cells of the C4 grass Zea mays J Biol Chem2781697316981PubMedCrossRefGoogle Scholar
  45. Philippar, K, Ivashikina, N, Ache, P, Christian, M, Luthen, H, Palme, K, Hedrich, R 2004Auxin activates KAT1 and KAT2, two K+-channel genes expressed in seedlings of Arabidopsis thaliana Plant J37815827PubMedCrossRefGoogle Scholar
  46. Plesch, G, Ehrhardt, T, Mueller-Roeber, B 2001Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expressionPlant J28455464PubMedCrossRefGoogle Scholar
  47. Rayle, DL, Cleland, R 1970Enhancement of wall loosening and elongation by acid solutionsPlant Phys46250253CrossRefGoogle Scholar
  48. Rober-Kleber, N, Albrechtova, JTP, Fleig, S, Huck, N, Michalke, W, Wagner, E, Speth, V, Neuhaus, G, Fischer-Iglesias, C 2003Plasma membrane H-ATPase is involved in auxin-mediated cell elongation during wheat embryo developmentPlant Phys13113021312CrossRefGoogle Scholar
  49. Robertson, DS 1978Characterization of a mutator system in maizeMutat Res/Fund Mol Mech Mutagen512128CrossRefGoogle Scholar
  50. Sambrook, J, Fritsch, EF, Maniatis, T 1989Molecular cloning: a laboratory manualCold Spring Harbor Laboratory PressCold Spring Harbor, NYGoogle Scholar
  51. Scanlon, MJ, Stinard, PS, James, MG, Myers, AM, Robertson, DS 1994Genetic analysis of 63 mutations affecting maize kernel development isolated from Mutator stocksGenetics136281294PubMedGoogle Scholar
  52. Scanlon, MJ, Henderson, DC, Bernstein, B 2002SEMAPHORE1 functions during the regulation of ancestrally duplicated knox genes and polar auxin transport in maizeDevelopment12926632673PubMedGoogle Scholar
  53. Thiel, G, Weise, R 1999Auxin augments conductance of K+ inward rectifier in maize coleoptile protoplastsPlanta2083845CrossRefGoogle Scholar
  54. Very, AA, Sentenac, H 2002Cation channels in the Arabidopsis plasma membraneTrends Plant Sci7168175PubMedCrossRefGoogle Scholar
  55. Walbot, V 2000Saturation mutagenesis using maize transposonsCurr Opin Plant Biol3103107PubMedCrossRefGoogle Scholar
  56. Weijers, D, Jürgens, G 2005Auxin and embryo axis formation: the ends in sight?Curr Opin Plant Biol83237PubMedCrossRefGoogle Scholar
  57. Went, FW 1926On growth-accelerating substances in the coleoptile of Avena sativa Proc Sect Sci, Koninklijke Akad Wetenschappen Amsterdam301019Google Scholar
  58. Yanagisawa, S, Schmidt, RJ 1999Diversity and similarity among recognition sequences of Dof transcription factorsPlant J17209214PubMedCrossRefGoogle Scholar
  59. Yanagisawa, S, Sheen, J 1998Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expressionPlant Cell107589PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Katrin Philippar
    • 1
    • 5
  • Kai Büchsenschütz
    • 1
  • David Edwards
    • 2
  • Julia Löffler
    • 3
  • Hartwig Lüthen
    • 3
  • Erhard Kranz
    • 3
  • Keith J. Edwards
    • 4
  • Rainer Hedrich
    • 1
  1. 1.Julius-von-Sachs-Institut, Lehrstuhl Molekulare Pflanzenphysiologie und BiophysikUniversität WürzburgWuerzburgGermany
  2. 2.Primary Industries Research Victoria, Department of Primary IndustriesLa Trobe UniversityBundooraAustralia
  3. 3.Biozentrum Klein Flottbek und Botanischer GartenUniversität HamburgHamburgGermany
  4. 4.School of Biological SciencesUniversity of BristolBristolUK
  5. 5.Department für Biologie 1, Botanik IIILudwig-Maximilians-Universität MünchenMunichGermany

Personalised recommendations