cAMP activates hyperpolarization-activated Ca2+ channels in the pollen of Pyrus pyrifolia
Tóm tắt
Many signal-transduction processes in plant cells have been suggested to be triggered by signal-induced opening of calcium ion (Ca2+) channels in the plasma membrane. Cyclic nucleotides have been proposed to lead to an increase in cytosolic free Ca2+ in pollen. However, direct recordings of cyclic-nucleotide-induced Ca2+ currents in pollen have not yet been obtained. Here, we report that cyclic AMP (cAMP) activated a hyperpolarization-activated Ca2+ channel in the Pyrus pyrifolia pollen tube using the patch-clamp technique, which resulted in a significant increase in pollen tube protoplast cytosolic-Ca2+ concentration. Outside-out single channel configuration identified that cAMP directly increased the Ca2+ channel open-probability without affecting channel conductance. cAMP-induced currents were composed of both Ca2+ and K+. However, cGMP failed to mimic the cAMP effect. Higher cytosolic free-Ca2+ concentration significantly decreased the cAMP-induced currents. These results provide direct evidence for cAMP activation of hyperpolarization-activated Ca2+ channels in the plasma membrane of pollen tubes, which, in turn, modulate cellular responses in regulation of pollen tube growth.
Tài liệu tham khảo
Assmann S (1995) Cyclic AMP as a second messenger in higher plants. Plant Physiol 108:885–889
Berridge M (1998) Neuronal calcium signaling review. Neuron 21:13–26
Biel M (2009) Cyclic nucleotide-regulated cation channels. J Biol Chem 284:9017–9021
Bolwell G (1995) Cyclic AMP, the reluctant messenger in plants. Trends Biochem Sci 20:492–495
Bossen M, Kendrick R, Vredenberg W (2006) The involvement of a G-protein in phytochrome-regulated, Ca2+-dependent swelling of etiolated wheat protoplasts. Physiol Plant 80:55–62
Curvetto N, Darjania L, Delmastro S (1994) Effect to two cAMP analogues on stomatal opening in Vicia faba. Plant Physiol Biochem 32:365–372
Durner J, Wendehenne D, Klessig D (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333
Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406
Franklin-Tong VE (1999) Signaling and the modulation of pollen tube growth. Plant Cell 11:727–738
Hamilton DWA, Hills A, K hler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972
Hepler P, Wayne R (1985) Calcium and plant development. Annu Rev Physiol 36:397–439
Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A, Takayama S (2009) Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 150:1322–1334
Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett 581:2237–2246
Komatsu S, Hirano H (1993) Protein kinase activity and protein phosphorylation in rice (Oryza sativa L.) leaf. Plant Sci 94:127–137
Kurosaki F (1997) Role of inward K+ channel located at carrot plasma membrane in signal cross-talking of cAMP with Ca2+ cascade. FEBS Lett 408:115–119
Kurosaki F, Nishi A (1993) Stimulation of calcium influx and calcium cascade by cyclic AMP in cultured carrot cells. Archives Biochem Biophys 302:144–151
Kurosaki F, Kaburaki H, Nishi A (1994) Involvement of plasma membrane-located calmodulin in the response decay of cyclic nucleotide-gated cation channel of cultured carrot cells. FEBS Lett 340:193–196
Lemtiri-Chlieh F, Berkowitz GA (2004) Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J Biol Chem 279:35306–35312
Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci USA 103:18008–18013
Li W, Luan S, Schreiber SL, Assmann SM (1994) Cyclic AMP stimulates K+ channel activity in mesophyll cells of Vicia faba L. Plant Physiol 106:957–961
Ma W, Qi Z, Smigel A, Walker RK, Verma R, Berkowitz GA (2009) Ca2+, cAMP, and transduction of non-self perception during plant immune responses. Proc Natl Acad Sci USA 106:20995–21000
Maathuis FJM, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625
Malho R (2000) Signalling pathways in pollen tube growth and reorientation. Ann Bot 85:59–68
Malho R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173–1184
Martinez-Ballesta M, Cabanero F, Olmos E, Periago P, Maurel C, Carvajal M (2008) Two different effects of calcium on aquaporins in salinity-stressed pepper plants. Planta 228:15–25
Messerli M, Creton R, Jaffe L, Robinson K (2000) Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84–98
Moutinho A, Hussey PJ, Trewavas AJ, Malhó R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci USA 98:10481–10486
Newton R, Smith C (2004) Cyclic nucleotides. Phytochemistry 65:2423–2437
Penson S, Schuurink R, Fath A, Gubler F, Jacobsen J, Jones R (1996) cGMP is required for gibberellic acid-induced gene expression in barley aleurone. Plant Cell 8:2325–2333
Qu HY, Shang ZL, Zhang SL, Liu LM, Wu JY (2007) Identification of hyperpolarization-activated calcium channels in apical pollen tubes of Pyrus pyrifolia. New Phytol 174:524–536
Shang Z, Ma L, Zhang H, He R, Wang X, Cui S, Sun D (2005) Ca2+ influx into lily pollen grains through a hyperpolarization-activated Ca2+-permeable channel which can be regulated by extracellular CaM. Plant Cell Physiol 46:598–608
Spalding E, Goldsmith M (1993) Activation of K+ channels in the plasma membrane of Arabidopsis by ATP produced photosynthetically. Plant Cell 5:477–484
Tezuka T, Hiratsuka S, Takahashi SY (1993) Promotion of the growth of self-incompatible pollen tubes in lily by cAMP. Plant Cell Physiol 34:955–958
Tezuka T, Akita I, Yoshino N, Suzuki Y (2007) Regulation of self-incompatibility by acetylcholine and cAMP in Lilium longiflorum. J Plant Physiol 164:878–885
Thuleau P, Ward J, Ranjeva R, Schroeder J (1994) Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell. EMBO J 13:2970–2975
Tsuruhara A, Tezuka T (2001) Relationship between the self-incompatibility and cAMP level in Lilium longiflorum. Plant Cell Physiol 42:1234–1238
Volotovski ID, Sokolovsky SG, Molchan OV, Knight MR (1998) Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol 117:1023–1030
Wang YF, Fan LM, Zhang WZ, Zhang W, Wu WH (2004) Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol 136:3892–3904
Witters E, Quanten L, Bloemen J, Valcke R, Van Onckelen H (2004) Product identification and adenylyl cyclase activity in chloroplasts of Nicotiana tabacum. Rapid Commun Mass Spectrom 18:499–504
Wu W, Assmann S (1995) Is ATP required for K+ channel activation in Vicia guard cells? Plant Physiol 107:101–109
Wu Y, Xu X, Li S, Liu T, Ma L, Shang Z (2007) Heterotrimeric G-protein participation in Arabidopsis pollen germination through modulation of a plasma membrane hyperpolarization-activated Ca2+-permeable channel. New Phytol 176:550–559
Wu J, Shang Z, Wu J, Jiang X, Moschou P, Sun W, Roubelakis Angelakis K, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053
Zhou J, Olcese R, Qin N, Noceti F, Birnbaumer L, Stefani E (1997) Feedback inhibition of Ca2+ channels by Ca2+ depends on a short sequence of the C terminus that does not include the Ca2+-binding function of a motif with similarity to Ca2+-binding domains. Proc Natl Acad Sci USA 94:2301–2305
Zimmermann S, Nürnberger T, Frachisse J, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94:2751–2755
