Abstract
Roots of many species respond to gravity (gravitropism) and grow downward only if illuminated. This light-regulated root gravitropism is phytochrome-dependent, mediated by calcium, and inhibited by KN-93, a specific inhibitor of calcium/calmodulin-dependent protein kinase II (CaMK II). A cDNA encoding MCK1, a maize homolog of mammalian CaMK, has been isolated from roots of maize (Zea mays L.). The MCK1 gene is expressed in root tips, the site of perception for both light and gravity. Using the [35S]CaM gel-overlay assay we showed that calmodulin-binding activity of the MCK1 is abolished by 50 μM KN-93, but binding is not affected by 5 μM KN-93, paralleling physiological findings that light-regulated root gravitropism is inhibited by 50 μM KN-93, but not by 5 μM KN-93. KN-93 inhibits light-regulated gravitropism by interrupting transduction of the light signal, not light perception, suggesting that MCK1 may play a role in transducing light. This is the first report suggesting a physiological function for a CaMK homolog in light signal transduction.
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Abbreviations
- CaM:
-
calmodulin
- CaMK (II):
-
Ca2+/calmodulin-dependent protein kinase (II)
- CBP:
-
CaM-binding protein
- CDPK:
-
Ca2+-dependent protein kinase
- MCK1:
-
maize homolog of mamalian CaMK
References
Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357–364
Braam J (1992) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: Induction by calcium and heat shock. Proc Natl Acad Sci USA 89: 3213–3216
Brand JJ, Becker DW (1984) Evidence for direct roles of calcium in photosynthesis. J Bioenerg Biomembr 16: 239–249
Bush DS (1993) Regulation of cytosolic calcium in plants. Plant Physiol 103: 7–13
Davis TN (1992) What's new with calcium? Cell 71: 557–564
Feldman LJ (1985) Root Gravitropism. Physiol Plant 65: 341–344
Feldman LJ, Briggs WR (1986) Light-regulated gravitropism in seedling roots of maize: a role for temperature and phytochrome. Plant Physiol 83: 241–243
Friedmann M, Poovaiah BW (1991) Calcium and protein phosphorylation in the transduction of gravity signal in corn roots. Plant Cell Physiol 32: 299–302
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998–9002
Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52
Harper JF, Sussman MR, Schaller GE, Putnam-Evans C, Charbonneau H, Harmon AC (1991) A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252: 951–954
Hidaka H, Ishikawa T. (1992) Molecular pharmacology of calmodulin pathways in the cell functions. Cell Calcium 13:465–472
Jena PK, Reddy ASN, Poovaiah BW (1989) Molecular cloning and sequencing of a cDNA for plant calmodulin: Signal-induced changes in the expression of calmodulin. Proc Natl Acad Sci USA 86: 3644–3648
Johnson EM, Pao LI, Feldman LJ (1991) Regulation of phytochrome message abundance in root caps of maize; spatial, environmental, and genetic specificity. Plant Physiol 95: 544–550
Kapiloff MS, Mathis JM, Nelson CA, Lin CR, Rosenfeld MG (1991) Calcium/calmodulin-dependent protein kinase mediates a pathway for transcriptional regulation. Proc Natl Acad Sci USA 88: 3710–3716
Lee JS, Mulkey TJ, Evans ML (1983) Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 220: 1375–1376
Levine HIII, Sahyoun NE (1987) Characterization of a soluble 30 000-molecular-weight catalytic fragment of neuronal calmodulin-dependent protein kinase II. Eur J Biochem 168: 481–486
Lin X, Feng X-H, Watson JC (1991) Differential accumulation of transcripts encoding protein kinase homologs in greening pea seedlings. Proc Natl Acad Sci USA 88: 6951–6955
Lin CR, Kapiloff MS, Durgerian S, Tatemoto K, Russo AF, Hanson P, Schulman H, Rosenfeld MG (1987) Molecular cloning of a brain-specific calcium/calmodulin-dependent protein kinase. Proc Natl Acad Sci USA 84: 5962–5966
Lisman J, Goldring M (1988) Evaluation of a model of long term memory based on the properties of the Ca2+/calmodulin-dependent protein kinase. J Physiol 83: 187–197
Lu Y-T, Feldman LJ (1993) Light-regulated gravitropism in maize roots may require a Ca2+/calmodulin-dependent protein kinase II. ASGSB Bull Publ Am Soc Gravit Space Biol 7: 94
Lu Y-T, Feldman LJ, Hidaka H (1993) Inhibitory effects of KN-93, an inhibitor of Ca2+/calmodulin-dependent protein kinase II, on light-regulated root gravitropism in maize. Plant Physiol Biochem 31: 857–862
Lu Y-T, Harrington HM (1994) Isolation of tobacco cDNA clones encoding calmodulin-binding proteins and characterization of a known calmodulin-binding domain. Plant Physiol Biochem 32: 413–422
Lu Y-T, Dharmasiri MAN, Harrington HM (1995) Characterization of a cDNA encoding a novel heat-shock protein that binds to calmodulin. Plant Physiol 108: 1197–1202
Lukas TJ, Burgess WH, Prendergast FG, Lau W, Watterson DM (1986) Calmodulin binding domains: Characterization of a phosphorylation and calmodulin binding site from myosin light chain kinase. Biochemistry 25: 1458–1464
Lukas TJ, Haiech J, Lau W, Craig TA, Zimmer WE (1988) Calmodulin and calmodulin-regulated protein kinases as transducers of intracellular calcium signals. Cold Spring Harbor Symposia on Quantitative Biology LIII: 185–193
Marmé D, (1989) The role of calcium and calmodulin in signal transduction. In: Second messengers in plant growth and development. Alan R. Liss, Inc., pp 57–80
Neuhaus G, Bowler C, Kern R, Chua N-H (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73: 937–952
O'Neil KT, De Grado WF (1990) How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biol Sci 15: 59–64
Pausch MH, Kaim D, Kunisawa R, Admon A, Thorner J (1991) Multiple Ca2+/calmodulin-dependent protein kinase genes in a unicellular eukaryote. EMBO J 10: 1511–1522
Perdue DO, LaFavre AK, Leopold AC (1988) Calcium in the regulation of gravitropism by light. Plant Physiol 86: 1276–1280
Planas-Silva MD, Means AR (1992) Expression of a constitutive form of calcium/calmodulin dependent protein kinase II leads to arrest of the cell cycle in G2. EMBO J 11: 507–517
Poovaiah BW, Reddy ASN (1993) Calcium and signal transduction in plants. Crit Rev Plant Sci 12: 185–211
Roe JL, Rivin CJ, Sessions RA, Feldmann KA, Zambryski PC (1993) The tousled gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development. Cell 75: 939–950
Roberts DM, Harmon AC (1992) Calcium-modulated proteins: Targets of intracellular calcium signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375–414
Schulman H, Hanson PI, Meyer T (1992) Decoding calcium signals by multifunctional CaM kinase. Cell Calcium 13: 401–411
Serlin BS, Roux SJ (1984) Modulation of chloroplast movement in the green alga Mougeotia by the Ca2+ ionophore A23187 and by calmodulin antagonists. Proc Natl Acad Sci USA 81: 6368–6372
Shacklock PS, Read ND, Trewavas AJ (1992) Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358: 753–755
Stinemetz CL, Evans ML (1986) The effect of calmodulin antagonists and asymmetric redistribution of Ca2+ and IAA following gravistimulation. Proc Am Soc Grav Space Biol, 2nd Annual Symposium of the NASA Space Biology Program. Charlottesville, p. 9
Stinemetz CL, Kuzmanoff KM, Evans ML, Jarrett HW (1987) Correlation between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol 84: 1337–1342
Stinemetz CL, Hasenstein KH, Young LM, Evans ML (1992) Effect of calmodulin antagonists on the growth and graviresponsiveness of primary roots of maize. Plant Growth Regul 11: 419–427
Suen KL, Choi JH (1991) Isolation and sequence analysis of a cDNA for a carrot calcium-dependent protein kinase: homology to calcium/calmodulin-dependent protein kinases and calmodulin. Plant Mol Biol 17:581–590
Sumi M, Kizutoshi K, Ishikawa T, Ishii A, Hagiwara M, Nagatsu T Hidaka H (1991) The newly synthesized selective Ca2+/calmodulin-dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12 h cells. Biochem Biophys Res Commun 181: 968–975
Watillon B, Kettmenn R, Boxus P, Burny A (1992) Cloning and characterization of an apple (Malus domestica (L.) Brokh) cDNA encoding a calmodulin-binding protein domain similar to the calmodulin-binding domain of type II mammalian calcium/ calmodulin-dependent protein kinase. Plant Sci 81: 227–235
Watillon B, Kettmenn R, Boxus P, Burny A (1993) A calcium/ calmodulin-binding serine/threonine protein kinase homologous to mammalian type II calcium/calmodulin-dependent protein kinase is expressed in plant cells. Plant Physiol 101: 1381–1384
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This work is supported by the National Aeronautics and Space Administration grant No: NAGW 238.
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Lu, YT., Hidaka, H. & Feldman, L.J. Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta 199, 18–24 (1996). https://doi.org/10.1007/BF00196876
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DOI: https://doi.org/10.1007/BF00196876