Biologia Plantarum

, Volume 51, Issue 2, pp 257–267 | Cite as

Expression pattern of the AHP gene family from Arabidopsis thaliana and organ specific alternative splicing in the AHP5 gene

Original Papers

Abstract

Histidine-containing phosphotransmitters (AHPs) transfer a phosphoryl group from membrane receptors to effectors in the nucleus. Five AHP genes have been identified in Arabidopsis. Real-time reverse transcription polymerase chain reaction (RT-PCR) was employed to quantify contents of individual transcripts in Arabidopsis leaves, roots, stems, flowers and siliques. High organ specificity of gene expression was found in AHP1, AHP2, AHP4 while expression of AHP3 and AHP5 appears more ubiquitous. We detected two AHP5 specific PCR products (AHP5 and AHP5L). Out of the five AHP5 introns, the second one was retained unspliced in the longer product (AHP5L) while AHP5 corresponded to a completely spliced AHP5 mRNA. The ratio between alternately and completely spliced AHP5 mRNAs was highest in flowers and lowest in siliques and stems. No evidence for alternative splicing in the remaining AHP transcripts was found. Two open reading frames were identified in AHP5L. The conserved part of the phosphotransfer domain remains unaffected in the longer one as the translation initiation at an intron ATG would result in a polypeptide coded by exons 3 to 6 and a short extension encoded by the intron part of the alternative open reading frame. However, the isoelectric point would shift by about 3 units towards neutral.

Additional key words

Arabidopsis two component systems gene expression analysis real time RT-PCR signal transduction 

Abbreviations

AHP

histidine-containing phosphotransmitters

RT-PCR

reverse transcription polymerase chain reaction

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References

  1. An, Y.Q., McDowell, J.M., Huang, S., McKinney, E.C., Chambliss, S., Meagher R.B.: Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues.-Plant J. 10: 107–121, 1996.PubMedCrossRefGoogle Scholar
  2. Brandstatter, I.B., Kieber, J.J.: Two genes with similarity to q-bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis.-Plant Cell 10: 1009–1019, 1998.PubMedCrossRefGoogle Scholar
  3. D’Agostino, I.B., Deruere, J., Kieber, J.J.: Characterization of the response of the Arabidopsis response regulator gene family to cytokinin.-Plant Physiol. 124: 1706–1717, 2000.PubMedCrossRefGoogle Scholar
  4. Grefen, C., Harter, K.: Plant two-component systems: principles, functions, complexity and cross talk.-Planta 219: 733–742, 2004.PubMedCrossRefGoogle Scholar
  5. Haas, B.J., Volfovsky, N., Town, C.D., Troukhan, M., Alexandrov, N., Feldmann, K.A., Flavell, K.B., White, O., Salzberg, S.L.: Full-length messenger RNA sequences greatly improve genome annotation.-Genome Biol. 3: (http://genomebiology.com/2002/3/6/research/0029), 2002.
  6. Hass, C., Lohrmann, J., Albrecht, V., Sweere, U., Hummel, F., Yoo, S.D., Hwang, I., Zhu, T., Schafer, E., Kudla, J., Harter, K.: The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis.-EMBO J. 23: 3290–3302, 2004.PubMedCrossRefGoogle Scholar
  7. Hejátko, J., Pernisová, M., Eneva, T., Palme, K., Brzobohatý, B.: The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis.-Mol. Genet. Genomics 269: 443–453, 2003.PubMedCrossRefGoogle Scholar
  8. Higuchi, M., Pischke, M.S., Mahonen, A.P., Miyawaki, K., Hashimoto, Y., Seki., M., Kobayashi, M., Shinozaki, K., Kato, T., Tabata, S., Helariutta, Y., Sussman, M.R., Kakimoto, T.: In planta functions of the Arabidopsis cytokinin receptor family.-Proc. nat. Acad. Sci. USA 101: 8821–8826, 2004.PubMedCrossRefGoogle Scholar
  9. Horák, J., Brzobohatý, B., Lexa, M.: Molecular and physiological characterization of an insertion mutant in the ARR21 putative response regulator gene from Arabidopsis thaliana.-Plant Biol. 5: 245–254, 2003.CrossRefGoogle Scholar
  10. Hosoda, K., Imamura, A., Katoh, E., Hatta, T., Tachiki, M., Yamada, H., Mizuno, T., Yamazaki, T.: Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators.-Plant Cell 14: 2015–2029, 2002.PubMedCrossRefGoogle Scholar
  11. Hutchison, C.E., Kieber, J.J.: Cytokinin signalling in Arabidopsis.-Plant Cell 14: 47–59. 2002.CrossRefGoogle Scholar
  12. Hwang, I., Chen, H.C., Sheen, J.: Two-component signal transduction pathways in Arabidopsis.-Plant Physiol. 129: 500–515, 2002.PubMedCrossRefGoogle Scholar
  13. Hwang, I., Sheen, J.: Two-component circuitry in Arabidopsis cytokinin signal transduction.-Nature 413: 383–389, 2001.PubMedCrossRefGoogle Scholar
  14. Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Tanaguchi, M., Kiba, T., Ueguchi, C., Sugiyama, T., Mizuno, T.: Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction.-Plant Cell Physiol. 40: 733–742, 1999.PubMedGoogle Scholar
  15. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., Kakimoto, T.: Identification of CRE1 as a cytokinin receptor from Arabidopsis.-Nature 409: 1060–1063, 2001.PubMedCrossRefGoogle Scholar
  16. Ishikawa, T., Yoshimura, K., Tamoi, M., Takeda, T., Shigeoka, S.: Alternative mRNA splicing of 3′-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplasts.-Biochem. J. 328: 795–800, 1997.PubMedGoogle Scholar
  17. Kazan, K.: Altrenative splicing and proteome diversity in plants: the tip of the iceberg has just emerged.-Trends Plant Sci. 8: 468–471, 2003.PubMedCrossRefGoogle Scholar
  18. Lohrmann, J., Bucholz, G., Keitel, C., Sweere, U., Kircher, S., Bäurle, I., Kudla, J., Schäfer, E., Harter, K.: Differential expression and nuclear localization of response regulator-like proteins from Arabidopsis thalina.-Plant Biol. 1: 495–505, 1999.Google Scholar
  19. Lohrmann, J., Sweere, U., Zabaleta, E., Bäurle, I., Keitel, C., Kozma-Bognar, L., Brennicke, A., Schäfer, E., Kudla, J., Harter, K.: The response regulator ARR2: pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis.-Mol. Genet. Genomics 265: 2–13, 2001.PubMedCrossRefGoogle Scholar
  20. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., Dean, C.: FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains.-Cell 89: 737–745, 1997.PubMedCrossRefGoogle Scholar
  21. Macknight, R., Duroux, M., Laurie, R., Dijkwel, P., Simpson, G., Dean, C.: Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA.-Plant Cell 14: 877–888, 2002.PubMedCrossRefGoogle Scholar
  22. Mähönen, A.P., Bonke, M., Kauppinen, L., Riikonen, M., Benfey, P.N., Helariutta Y.: A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis roots.-Gene Dev. 14: 2938–2943, 2000.PubMedCrossRefGoogle Scholar
  23. Mason, M.G., Li, J., Mathews, D.E., Kieber, J.J., Schaller, G.E.: Type-B response regulators display overlapping expression patterns in Arabidopsis.-Plant Physiol. 135: 927–937, 2004.PubMedCrossRefGoogle Scholar
  24. Miyata, S., Urao, T., Yamaguchi-Shinozaki, K., Shinozaki, K. Characterization of genes for two-component phosphorelay mediators with a single HPt domain in Arabidopsis thaliana.-FEBS Lett. 437: 11–14. 1998.PubMedCrossRefGoogle Scholar
  25. Pischke, M.S., Jones, L.G., Otsuga, D., Fernandez, D.E., Drews, G.N., Sussman, M.R.: An Arabidopsis histidine kinase is essential for megagametogenesis.-Proc. nat. Acad. Sci. USA 99: 15800–15805, 2002.Google Scholar
  26. Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J.Z., Ghandehari, D., Sherman, B.K., Yu, G.: Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes.-Science 290: 2105–2110, 2000.PubMedCrossRefGoogle Scholar
  27. Sakai, H., Ayoma, T., Oka, A.: Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators.-Plant J. 24: 703–711, 2000.PubMedCrossRefGoogle Scholar
  28. Sakai, H., Honma, T., Ayoma, T., Sato, S., Kato, T., Tabata, S., Oka, A.: ARR1, a transcription factor for genes immediately responsive for cytokinins.-Science 294: 1519–1521, 2001.PubMedCrossRefGoogle Scholar
  29. Sakai, H., Hua, J., Chen, Q.G., Chang, C., Medrano, L.J., Bleecker, A.B., Meyerowitz, E.M.: ETR2 is an ETR1-like gene involved in ethylene signalling in Arabidopsis.-Proc. nat. Acad. Sci. USA 95: 5812–5817, 1998.PubMedCrossRefGoogle Scholar
  30. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., Yoshimura, K.: Regulation and function of ascorbate peroxidase isoenzymes.-J. exp. Bot. 53: 1305–1319, 2002.PubMedCrossRefGoogle Scholar
  31. Suzuki, T., Ishikawa, K., Yamashino, T., Mizuno, T.: An Arabidopsis histidine-containing phosphotransfer (HPt) factor implicated in phosphorelay signal transduction: overexpression of AHP2 in plants results in hypersensitiveness to cytokinin.-Plant Cell Physiol. 43: 123–129, 2002.PubMedCrossRefGoogle Scholar
  32. Suzuki, T., Sakurai, K., Imamura, A., Nakamura, A., Ueguchi, C., Mizuno, T.: Compilation and characterization of histidine-containing phosphotransmitters implicated in Histo-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana.-Biosci. Biotechnol. Biochem. 64: 2486–2489, 2000.PubMedCrossRefGoogle Scholar
  33. Sweere, U., Eichenberg, K., Lohrmann, J., Mira-Rodado, V., Baurle, I., Kudla, J., Nagy, F., Schafer, E., Harter, K.: Interaction of the response regulator ARR4 with phytochrome B in modulating red light signalling.-Science 294: 1108–1111, 2001.PubMedCrossRefGoogle Scholar
  34. Szyroki, A., Ivashikina, N., Dietrich, P., Roelfsema, M.R., Ache, P., Reintanz, B., Deeken, R., Godde, M., Felle, H., Steinmeyer, R., Palme, K., Hedrich, R.: KAT1 is not essential for stomatal opening.-Proc. nat. Acad. Sci. USA 98: 2917–21, 2001.PubMedCrossRefGoogle Scholar
  35. Tanaka, Y., Suzuki, T., Yamashino, T., Mizuno, T.: Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana.-Biosci. Biotechnol. Biochem. 68: 462–465, 2004.PubMedCrossRefGoogle Scholar
  36. Tsaftaris, A.S., Pasentsis, K., Polidoros, A.N.: Isolation of a differentially spliced C-type flower specific AG-like MADS-box gene from Crocus sativus and characterization of its expression.-Biol. Plant. 49: 499–504, 2005.CrossRefGoogle Scholar
  37. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T., Shinozaki, K.: A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor.-Plant Cell 11: 1743–1754, 1999.PubMedCrossRefGoogle Scholar
  38. Urao, T., Yamaguchi-Shinozaki, K., Shinozaki, K.: Two-component systems in plant signal transduction.-Trends Plant Sci. 5: 7–74, 2000.CrossRefGoogle Scholar
  39. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T., Mizuno, T.: The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane.-Plant Cell Physiol. 42: 1017–1023, 2001.PubMedCrossRefGoogle Scholar
  40. Yang, S.H., Yu, H., Goh, C.J.: Functional characterisation of a cytokinin oxidase gene DSCKX1 in Dendrobium orchid.-Plant mol. Biol. 51: 38–248, 2003.CrossRefGoogle Scholar

Copyright information

© Institute of Experimental Botany, ASCR 2007

Authors and Affiliations

  1. 1.Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.Department of Functional Genomics and Proteomics, Faculty of ScienceMasaryk UniversityBrnoCzech Republic

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