Skip to main content
Log in

Developmentally regulated organ-, tissue-, and cell-specific expression of calmodulin genes in common wheat

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Recently, we reported on the characterization of the calmodulin (CaM) gene family in wheat [44]. We classified wheat CaM genes into four subfamilies (SFs) designated SF-1 to SF-4, each representing a series of homoeoallelic loci on the homoeologous chromosomes of the three genomes of common wheat. Here we studied the expression of these wheat CaM genes in the course of wheat development. Northern blot analysis using SF-specific probes revealed differences in SF expression levels in different organs and stages of development. Subsequently, cell-specific expression of CaM SFs was investigated by in situ RNA hybridization. In developing seeds, all CaM SFs showed highest expression in the embryo and less in the aleurone and in the starchy endosperm. In primary roots, all four CaM SFs were expressed in the root cap, meristematic regions and in differentiating cells. During development of the roots, expression gradually decreased. The wheat glutenin gene, which was used as a control throughout our experiments, was found to be expressed in the starchy endosperm but not in the aleurone, embryos or vegetative tissues. In stems, at advanced stages of growth, differences in cell-specific expression of CaM SFs were found. For example, SF-2 was highly expressed in differentiating phloem fibers. Thus, CaM genes in common wheat exhibit a developmentally regulated organ-, tissue-, cell- and SF-specific expression patterns.

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.

Similar content being viewed by others

References

  1. Aloni R: Differentiation of vascular tissues. Annu Rev Plant Physiol 38: 179–204 (1987).

    Google Scholar 

  2. Allan E, Trewavas AJ: Quantitative changes in calmodulin and NAD kinase during early cell development in root apex of Pisum sativum. Planta 165: 493–501 (1985).

    Google Scholar 

  3. Baum G, Chen Y, Arazi T, Takatsuji H, Fromm H: A plant glutamate decarboxylase containing a CaMbinding domain: cloning, sequence and functional analysis. J Biol Chem 268: 19610–19617 (1993).

    Google Scholar 

  4. Baum G, LevYadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H: Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J 15: 2988–2996 (1996).

    Google Scholar 

  5. Becker D, Brettschneider R, Lorz H: Fertile transgenic wheat from microprojectile bombardment of scutellar tissue. Plant J 5: 299–307 (1994).

    Google Scholar 

  6. Botella JR, Arteca RN: Differential expression of two calmodulin genes in response to physical and chemical stimuli. Plant Mol Biol 24: 757–766 (1994).

    Google Scholar 

  7. Braam J, Davis RW: Rain, wind, and touchinduced expression of calmodulinrelated genes in Arabidopsis. Cell 60: 357–364 (1990).

    Google Scholar 

  8. Bush DS: Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46: 95–122 (1995).

    Google Scholar 

  9. Cocucci M, Negrini N: Changes in the levels of calmodulin and of a calmodulin inhibitor in the early phases of radish (Raphanus sativusL.) seed germination. Plant Physiol 88: 910–914 (1988).

    Google Scholar 

  10. Corneliussen B, Holm M, Walterson Y, Onions J, Hallberg B, Thornell A, Grundstrom T: Calcium/calmodulin inhibition of basichelixloophelix transcription factor domains. Nature 368: 760–764 (1994).

    Google Scholar 

  11. Cox KH, Goldberg RB: Analysis of plant gene expression. In Shaw CH(ed) Plant Molecular Biology: A Practical Approach, pp. 1–34. IRL Press, Oxford, UK (1988).

    Google Scholar 

  12. Dauwalder M, Roux SJ, Hardison L: Distribution of calmodulin in pea seedlings: immunocytochemical localization in plumules and root apices. Planta 168: 461–470 (1986).

    Google Scholar 

  13. Erlander MG, Tobin AJ: The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem Res 16: 215–226 (1991).

    Google Scholar 

  14. Feinberg AP, Vogelstein B: Atechnique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    Google Scholar 

  15. Fukuda H: Xylogenesis initiation, progression, and cell death. Annu Rev Plant Physiol Plant Mol Biol 47: 299–325 (1996).

    Google Scholar 

  16. Fulton C, Lai EY, Remillard SP: A flagellar calmodulin gene of Naegleria, coexpressed during differentiation with flagellar tubulin genes, shares DNA, RNA, and encoded protein sequence elements. J Biol Chem 270: 5839–5848 (1995).

    Google Scholar 

  17. Gale MD, Youssefian S: Dwarfism gene in wheat. In: Russel GE (ed) Progress in Plant Breeding, pp. 1–35. Butterworth, London (1985).

  18. Galili G, Feldman M: Mapping of glutenin and gliadin genes located on chromosome 1B of common wheat. Mol Gen Genet 193: 293–298 (1984).

    Google Scholar 

  19. Galili S, Galili G, Feldman M: Chromosomal location of genes for rubisco small subunit and rubiscobinding protein in common wheat. Theor Appl Genet 81: 98–104 (1991).

    Google Scholar 

  20. Galili S, Galili G, Avivi Y, Feldman M: Identification and chromosomal location of four subfamilies of the rubisco small subunit genes in common wheat. Theor Appl Genet 83: 385–391 (1992).

    Google Scholar 

  21. Gawienowski MC, Szymanski D, Perera IY, Zielinski RE: Calmodulin isoforms in Arabidopsis encoded by multiple divergent mRNAs. Plant Mol Biol 22: 215–225 (1993).

    Google Scholar 

  22. James P, Vorherr T, Carafoli E: Calmodulinbinding domains: just twofaced or multifaceted? Trend Biochem Sci 20: 38–42 (1995).

    Google Scholar 

  23. Jena PK, Reddy ASN, Poovaiah BW: Molecular cloning and sequencing of a cDNA for plant calmodulin: signalinduced changes in the expression of calmodulin. Proc Natl Acad Sci USA 86: 3644–3648 (1989).

    Google Scholar 

  24. Kobayashi H, Fukuda H: Involvement of calmodulin and calmodulinbinding proteins in the differentiation of tracheary elements in Zinnia cells. Planta 194: 388–394 (1994).

    Google Scholar 

  25. Lee SH, Kim JC, Lee MS, Heo WD, Seo HS, Yoon HW, Hong JC, Lee SY, Bahk JD, Hwang I, Cho MJ: Identification of a novel divergent calmodulin isoform from soybean which has differential ability to activate calmodulindependent enzymes. J Biol Chem 270: 21806–21812 (1995).

    Google Scholar 

  26. Lersten NR: Morphology and anatomy of the wheat plant. In: Heyne EG (ed) Wheat and Wheat Improvement, pp. 33–75. American Society of Agronomy Inc, USA (1987).

    Google Scholar 

  27. LevYadun S, Beharav A, Abbo S: Evidence for polygenic control of fibre differentiation in spring wheat and its relationship with the gibberellininsensitivity locus Rht1. Aust J Plant Physiol 23: 185–189 (1996).

    Google Scholar 

  28. Ling V, Assmann SM: Cellular distribution of calmodulin and calmodulinbinding proteins in Vicia faba L. Plant Physiol 100: 970–978 (1992).

    Google Scholar 

  29. Longemann J, Shell J, Willmitzer L: Improved method for the isolation of RNAfrom plant tissues. Anal Biochem 163: 16–20 (1987).

    Google Scholar 

  30. Lu YT, Hidaka H, Feldman LJ: Characterization of a calcium/calmodulindependent protein kinase homolog from maize roots showing lightregulated gravitropism. Planta 199: 18–24 (1996).

    Google Scholar 

  31. Maras B, Sweeney G, Barra D, Bossa F, John RA: The amino acid sequence of glutamate decarboxylase from Escherichia coli. Evolutionary relationship between mammalian and bacterial enzymes. Eur J Biochem 204: 93–98 (1992).

    Google Scholar 

  32. Masson PH: Root gravitropism. BioEssays 17: 119–127 (1995).

    Google Scholar 

  33. Means AR: Molecular mechanisms of action of calmodulin. Rec Prog Horm Res 44: 223–286 (1988).

    Google Scholar 

  34. Okamoto H, Tanaka Y, Sakai S: Molecular cloning of the cDNA for an auxinregulated calmodulin gene. Plant Cell Physiol 36: 1531–1539 (1995).

    Google Scholar 

  35. Penson SP, Schuurink RC, Fath A, Gubler F, Jacobsen JV, Jones RL: cGMP is required for gibberellic acidinduced gene expression in barley aleurone. Plant Cell 8: 2325–2333 (1996).

    Google Scholar 

  36. Poovaiah BW, Reddy ASN: Calcium and signal transduction in plants. CRC Crit Rev Plant Sci 6: 569–573 (1993).

    Google Scholar 

  37. Reddy ASN, Safadi F, Narasimhulu SB, Golovkin M, Hu X: A novel plant calmodulinbinding protein with a kinesin heavy chain motor domain. J Biol Chem 271: 7052–7060 (1996).

    Google Scholar 

  38. Roberts DM, Harmon AC: Calciummodulated proteins: targets of intracellular calcium signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375–414 (1992).

    Google Scholar 

  39. Schuurink RC, Chan PV, Jones RL: Modulation of calmodulin mRNAand protein levels in barley aleurone. Plant Physiol 111: 371–380 (1996).

    Google Scholar 

  40. Sistrunk ML, Antosiewicz DM, Purugganan MM, Braam J: Arabidopsis TCH3 encodes a novel Ca2+binding protein and shows environmentally induced and tissuespecific regulation. Plant Cell 8: 1553–1565 (1994).

    Google Scholar 

  41. Song H, Golovkin M, Reddy ASN, Endow S: In vitro motility of AtKCBP, a calmodulinbinding kinesin protein ofArabidopsis. Proc Natl Acad Sci USA. 94: 322–327 (1997).

    Google Scholar 

  42. Sugiyama T, Rafalski A, Peterson D, Soll D A: wheat HMW glutenin subunit gene reveals a highly repeated structure. Nucl Acids Res 13: 8729–8737 (1985).

    Google Scholar 

  43. Takezawa D, Liu ZH, An G, Poovaiah BW: Calmodulin gene family in potato: developmental and touchinduced expression of the messengerRNA encoding a novel isoform. Plant Mol Biol 27: 693–703 (1995).

    Google Scholar 

  44. Yang T, Segal G, Abbo S, Feldman M, Fromm H: Characterization of the calmodulin gene family in wheat: Structure, chromosomal location, and evolutionary aspects. Mol Gen Genet 252: 684–694 (1996).

    Google Scholar 

  45. Zodoks JC, Chang TT, Konzak CF: A decimal code for the growth stages of cereals. Weed Res 14: 415–421 (1974).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, T., Lev-Yadun, S., Feldman, M. et al. Developmentally regulated organ-, tissue-, and cell-specific expression of calmodulin genes in common wheat. Plant Mol Biol 37, 109–120 (1998). https://doi.org/10.1023/A:1005902905512

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005902905512

Navigation