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Molecular characterization of a new type of receptor-like kinase (wlrk) gene family in wheat

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Abstract

In plants, several types of receptor-like kinases (RLK) have been isolated and characterized based on the sequence of their extracellular domains. Some of these RLKs have been demonstrated to be involved in plant development or in the reaction to environmental signals. Here, we describe a RLK gene family in wheat (wlrk, wheat leaf rust kinase) with a new type of extracellular domain. A member of this new gene family has previously been shown to cosegregate with the leaf rust resistance gene Lr10. The diversity of the wlrk gene family was studied by cloning the extracellular domain of different members of the family. Sequence comparisons demonstrated that the extracellular domain consists of three very conserved regions interrupted by three variable regions. Linkage analysis indicated that the wlrk genes are specifically located on chromosome group 1 in wheat and on the corresponding chromosomes of other members of the Triticeae family. The wlrk genes are constitutively expressed in the aerial parts of the plant whereas no expression was detected in roots. Protein immunoblots demonstrated that the WLRK protein coded by the Lrk10 gene is an intrinsic plasma membrane protein. This is consistent with the hypothesis that WLRK proteins are receptor protein kinases localized to the cell surface. In addition, we present preliminary evidence that other disease resistance loci in wheat contain genes which are related to wlrk.

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References

  1. Bordier C: Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256: 1604–1607 (1981).

    PubMed  Google Scholar 

  2. Becraft PW, Stinard PS, McCarty DR: CRINKLY4: A TNFRlike receptor kinase involved in maize epidermal differentiation. Science 273: 1406–1409 (1996).

    PubMed  Google Scholar 

  3. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 2: 248–254 (1976).

    Google Scholar 

  4. Braun DM, Walker JC: Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem Sci 21: 70–73 (1996).

    PubMed  Google Scholar 

  5. Briggle LW: Near-isogenic lines of wheat with genes for resistance to Erysiphe graminis f. sp. tritici. Crop Sci 9: 70–72 (1969).

    Google Scholar 

  6. Clark SE, Williams RW, Meyerowitz EM: The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585 (1997).

    PubMed  Google Scholar 

  7. Delorme V, Giranton JL, Hatzfeld Y, Friry A, Heizman P, Ariza JM, Dumas C, Gaude T, Cock JM: Characterization of the S locus genes, SLG and SRK, of the Brassica S3 haplotype: identification of a membrane localized protein encoded by the S locus receptor kinase gene. Plant J 7: 429–440 (1995).

    PubMed  Google Scholar 

  8. Dickinson R: Simply a social disease? Nature 367: 517–518 (1994).

    Article  PubMed  Google Scholar 

  9. Dwyer KG, Kandasamy MK, Mahosky DI, Acciai J, Kudish BI, Miller JE, Nasrallah ME, Nasrallah JB: A superfamily of S locus-related sequences in Arabidopsis: diverse structures and expression patterns. Plant Cell 6: 1829–1843 (1994).

    PubMed  Google Scholar 

  10. Feuillet C, Schachermayr G, Keller B: Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus in wheat. Plant J 11: 45–52 (1997).

    PubMed  Google Scholar 

  11. Gallego F, Feuillet C, Messmer M, Penger A, Graner A, Yano M, Sasaki T, Keller B, Comparative mapping of the two wheat leaf rust resistance loci Lr1 and Lr10 in barley and rice. Genome, in press.

  12. Graner A, Jahoor A, Schondelmaier J, Siedler H, Pillen K, Fischbeck G, Wenzel G, Hermann RG: Construction of an RFLP map of barley. Theor Appl Genet 83: 250–256 (1991).

    Article  Google Scholar 

  13. Hartl L, Weiss H, Zeller FJ, Jahoor A: Use of RFLP markers for the identification of alleles of the Pm3 locus conferring powdery mildew resistance in wheat (Triticum aestivum). Theor Appl Genet 86: 959–963 (1993).

    Google Scholar 

  14. He Z-H, Fujiki M, Kohorn B: A cell wall associated, receptorlike protein kinase. J Biol Chem 271: 19789–19793 (1996).

    PubMed  Google Scholar 

  15. Herve C, Dabos P, Galaud JP, Rouge P, Lescure B: Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domain. J Mol Biol 258: 778–788 (1996).

    PubMed  Google Scholar 

  16. Hong SW, Jon JH, Kwak JM, Nam HG: Identification of a receptor-like kinase gene rapidly induced by abscisic acid, dehydratation, high salt and cold treatments in Arabidopsis thaliana. Plant Physiol 113: 1203–1212 (1997).

    PubMed  Google Scholar 

  17. Hunter T, Lindberg RA: Receptor protein-tyrosine kinases. In: Woodgett JR (ed) Protein Kinases, pp. 177–211. IRL Press (1994).

  18. Kjellbom P, Larsson C: Preparation and polypeptide composition of chlorophyll-free plasma membranes from leaves of light-grown spinach and barley. Physiol Plant 62: 501–509 (1984).

    Google Scholar 

  19. Kjellbom P, Larsson C, Rochester CP, Andersson B: Integral and peripheral proteins of the spinach leaf plasma membrane. Plant Physiol Biochem 27: 169–174 (1989).

    Google Scholar 

  20. Kohorn BD, Lane S, Smith TA: An Arabidopsis serine/ threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. Proc Natl Acad Sci USA 89: 10989–10992 (1992).

    Google Scholar 

  21. Korzun V, Malyshev S, Kartel N, Westermann T, Weber WE, Börner A: A genetic linkage map of rye (Secale cereale L.). Theor Appl Genet, in press.

  22. Kosambi DD: The estimation of map distances from recombinant values. Ann Eugen 12: 172–175 (1944).

    Google Scholar 

  23. Laemmli UK: Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680–685 (1970).

    PubMed  Google Scholar 

  24. Lander ES, Green P, Abrahamsom J, Barlow A, Daly MJ, Lincoln SE, Newburg L: MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174–181 (1987).

    PubMed  Google Scholar 

  25. Larsson C, Widell S, Kjellbom P: Preparation of high purity plasma membranes. Meth Enzymol 148: 558–568 (1987).

    Google Scholar 

  26. Lee HS, Karunanandaa B, Mc Cubbin A, Gilroy S, Kao TH: PRK1, a receptor-like kinase of Petunia inflata, is essential for postmeiotic development of pollen. Plant J 9: 613–624 (1996).

    Google Scholar 

  27. Li J, Chory J: A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938 (1997).

    PubMed  Google Scholar 

  28. McIntosh RA: Catalogue of gene symbols for wheat. In: Miller TE, Koebner RMD (eds) Proceedings of the Seventh International Wheat Genetic Symposium, vol 2, pp. 1225–1323. Institute of Plant Research, Cambridge, UK (1988).

    Google Scholar 

  29. Mc Intosh RA, Wellings CR, RF Park: Wheat rusts: an atlas of resistance genes. CSIRO Australia/Kluwer Academic Publishers, Dordrecht, Netherlands (1995).

    Google Scholar 

  30. Nasrallah JB, Nishio T, Nasrallah ME: The selfincompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu Rev Plant Physiol Plant Mol Biol 42: 393–422 (1991).

    Article  Google Scholar 

  31. Nasrallah JB, Nasrallah ME: Pollen-stigma signalling in the sporophytic self-incompatibility response. Plant Cell 5: 1325–1335 (1993).

    Article  PubMed  Google Scholar 

  32. Pastuglia M, Roby D, Dumas C, Cock JM: Rapid induction by wounding and bacterial infection of an S gene family receptorlike kinase gene in Brassica oleracea. Plant Cell 9: 49–60 (1997).

    PubMed  Google Scholar 

  33. Schachermayr G, Feuillet C, Keller B: Molecular markers for the detection of the wheat leaf rust resistance gene Lr10 in diverse genetic backgrounds. Mol Breed 3: 65–74 (1997).

    Google Scholar 

  34. Schönfeld M, Ragni A, Fischbeck G, Jahoor A: RFLP mapping of three new loci for resistance genes to powdery mildew (Erysiphe graminis f. sp. hordei) in barley. Theor Appl Genet 93: 48–56 (1996).

    Google Scholar 

  35. Sears ER: Chromosome mapping with the aid of telocentrics. In: MacKey J (ed) Proceedings 2nd International Wheat Genetics Symposium, Lund. (Hereditas (Suppl 2) p. 370–381 (1966).

  36. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald PC: A receptor-like kinase protein encoded by the rice disease resistance gene Xa-21. Science 270: 1804–1806 (1995).

    PubMed  Google Scholar 

  37. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB: Molecular cloning of a putative receptor protein kinase gene encoded at the self incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88: 8816–8820 (1991).

    PubMed  Google Scholar 

  38. Stein JC, Dixit R, Nasrallah ME, Nasrallah JB: SRK, the stigma-specific locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell 8: 429–445 (1996).

    PubMed  Google Scholar 

  39. Stöhr C, Snogerup L, Pennel RI, Kjellbom: An agarose gel electrophoretic method for the separation of arabinogalactan proteins. Plant J 10: 943–948 (1996).

    Google Scholar 

  40. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JDG: Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitial specificity in Cf-4 and Cf-9. Plant Cell 9: 2209–2224 (1997)

    PubMed  Google Scholar 

  41. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y: The Arabidopsis ERECTA gene encodes a putative receptor-like kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746 (1996).

    PubMed  Google Scholar 

  42. Towbin H, Stahelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354 (1979).

    PubMed  Google Scholar 

  43. Walker JC: Structure and function of the receptor-like kinases of higher plants. Plant Mol Biol 26: 1599–1609 (1994).

    PubMed  Google Scholar 

  44. Wang X, Zafian P, Choudhary M, Lawton M: The PRK5 receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc Natl Acad Sci USA 93: 2598–2602 (1996).

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Plant Biology, University of Zürich, Zollikerstr. 107, 8008, Zürich, Switzerland

    Catherine Feuillet & Beat Keller

  2. Department of Plant Biochemistry, Lund University, P.O. Box 117, 22100, Lund, Sweden

    Christophe Reuzeau & Per Kjellbom

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  1. Catherine Feuillet
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  2. Christophe Reuzeau
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  3. Per Kjellbom
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  4. Beat Keller
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Feuillet, C., Reuzeau, C., Kjellbom, P. et al. Molecular characterization of a new type of receptor-like kinase (wlrk) gene family in wheat. Plant Mol Biol 37, 943–953 (1998). https://doi.org/10.1023/A:1006062016593

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