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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AHP:
-
histidine-containing phosphotransmitters
- RT-PCR:
-
reverse transcription polymerase chain reaction
References
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.
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.
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.
Grefen, C., Harter, K.: Plant two-component systems: principles, functions, complexity and cross talk.-Planta 219: 733–742, 2004.
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.
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.
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.
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.
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.
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.
Hutchison, C.E., Kieber, J.J.: Cytokinin signalling in Arabidopsis.-Plant Cell 14: 47–59. 2002.
Hwang, I., Chen, H.C., Sheen, J.: Two-component signal transduction pathways in Arabidopsis.-Plant Physiol. 129: 500–515, 2002.
Hwang, I., Sheen, J.: Two-component circuitry in Arabidopsis cytokinin signal transduction.-Nature 413: 383–389, 2001.
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.
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.
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.
Kazan, K.: Altrenative splicing and proteome diversity in plants: the tip of the iceberg has just emerged.-Trends Plant Sci. 8: 468–471, 2003.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sakai, H., Ayoma, T., Oka, A.: Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators.-Plant J. 24: 703–711, 2000.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Urao, T., Yamaguchi-Shinozaki, K., Shinozaki, K.: Two-component systems in plant signal transduction.-Trends Plant Sci. 5: 7–74, 2000.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hradilová, J., Brzobohatý, B. Expression pattern of the AHP gene family from Arabidopsis thaliana and organ specific alternative splicing in the AHP5 gene. Biol Plant 51, 257–267 (2007). https://doi.org/10.1007/s10535-007-0051-7
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10535-007-0051-7