Ca2+ pulsation in BY-2 cells and evidence for control of mechanosensory Ca2+-selective channels by the plasmalemmal reticulum
Barbara G. Pickard A B and Masaaki Fujiki AA Gladys Levis Allen Laboratory of Plant Sensory Physiology, Biology Department, Washington University, St Louis, Missouri 63130-4899, USA.
B Corresponding author. Email: pickard@wustl.edu
Functional Plant Biology 32(10) 863-879 https://doi.org/10.1071/FP05045
Submitted: 4 March 2005 Accepted: 15 June 2005 Published: 5 October 2005
Abstract
A previously unknown cytoskeletal structure, now named the plasmalemmal reticulum (Gens et al. 2000, Protoplasma 212, 115–134), was found in cultured BY-2 tobacco cells during a search for a force-focusing mechanism that might enhance signal transduction by the cells’ mechanosensory Ca2+-selective cation channels (MCaCs). This polyhedral structure, which links cell wall, plasma membrane, and internal cytoplasm, prominently contains arabinogalactan protein (AGP). To check for reticulum-promoted Ca2+ elevation, the AGP-binding reagent (β-d-glucosyl)3 Yariv phenylglycoside has been applied to BY-2 cells expressing a free cameleon Ca2+ reporter. Ca2+ elevation was substantial and prolonged. Moreover it occurred in the nucleus as well as the cytoplasm. Cells treated with non-binding mannosyl Yariv reagent could not be discriminated from untreated controls or those treated with carrier solution alone. Supply of the MCaC inhibiter Gd3+ just before treatment with Yariv reagent prevented Ca2+ rise. These data strongly support the hypothesis that the plasmalemmal reticulum controls MCaC activity. The massive inward spread of Ca2+ suggested that entry of the ion through the channels initiated a wave of release from the ER, and YCX in the ER showed Ca2+ levels consistent with this premise. Cytosolic and nuclear Ca2+ often pulsed in control cells in near synchrony and at rates ranging from zero to five cycles per ∼20-min recording. (Pulsation was over-ridden by the applied amounts of glucosyl Yariv compound.) Suggestively but very crudely, oscillation rate was assessed as possibly correlating with stage of cell cycle. Because cell Ca2+ was lowered and pulsation was eliminated by Gd3+, MCaCs appear to participate in these endogenous fluctuations. The extent to which pulsing plays regulatory roles in relatively undifferentiated types of cells should be evaluated.
Keywords: arabinogalactan protein, BY-2 cells, cameleon, mechanosensory calcium channels, ultradian rhythms.
Acknowledgments
We are grateful for initial funding to BGP from NASA and NSF (Joint Program in Plant Biology grant IBN 941601) and later funding from the USDA (CREES NRI Plant Response to the Environment Program grant 98–35100–7003), and also to Glenn L Allen, Jr. and Gladys Levis Allen for remarkable and critically timed private funding. The relevant early phase of development of a special microscope system with its associated software was funded by NIH RR011380 (P.I. Jerome R Cox). It enabled critical participation of Frederick U Rosenberger, Keith W Doolittle, and Chrysanthe Preza. Joanne Markham (funded by NIH GM 55708 to José-Angel Conchello) provided additional help with algorithms. Following termination of the NIH grant, further development of the microscope system and software was taken over by Karl Kilborn and others of Intelligent Imaging Innovations, Inc. and funded by the Washington University Biology Department courtesy of Ralph S Quatrano.
We thank Eugene A Nothnagel for his gift of Yariv reagents, Jeffrey W Harper and colleagues for cameleons YC2, YC2.1, and YC3.1, and Gero Miesenböck for ratiometric pHlourin. Thanks also to Marcia J Kieliszewski for encouraging us to examine her GFP-LeAGP-1-transformed BY-2 cells, and to R Howard Berg for imaging them with a two-photon microscope. Unstinting technical help from Jasmine Fazzari and Michael Stewart was much appreciated.
Allen GJ,
Kwak JM,
Chu SP,
Llopis J,
Tsien RY,
Harper JF, Schroeder JI
(1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. The Plant Journal 19, 735–747.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Allen GJ,
Chu SP,
Schumacher K,
Shimazaki CT, Vafeados D , et al.
(2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289, 2338–2342.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Allen GJ,
Chu SP,
Harrington CL,
Schumacher K,
Hoffman T,
Tang YY,
Grill E, Schroeder JI
(2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411, 1053–1057.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Anderson CM,
Wagner TA,
Perret M,
He Z-H,
He D, Kohorn BD
(2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Molecular Biology 47, 197–206.
| Crossref |
PubMed |
Arif I, Newman IA
(1993) Proton efflux from oat coleoptile cells and exchange with wall calcium after IAA or fusicoccin treatment. Planta 189, 377–383.
Bayer KU,
De Koninck P, Schulman H
(2002) Alternative splicing modulates the frequency-dependent response of CaMKII to Ca2+ oscillations. EMBO Journal 21, 3590–3597.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bunney TD,
Shaw PJ,
Watkins PAC,
Taylor JP,
Beven AF,
Wells B,
Calder GM, Drobak BL
(2000) ATP-dependent regulation of nuclear Ca2+ levels in plant cells. FEBS Letters 476, 145–149.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bush DS
(1995) Calcium regulation in plant-cells and its role in signaling. Annual Review of Plant Physiology and Plant Molecular Biology 46, 95–122.
| Crossref | GoogleScholarGoogle Scholar |
Collings DA,
Carter CN,
Rink JC,
Scott AC,
Wyatt SE, Allen NS
(2000) Plant nuclei can contain extensive grooves and invaginations. The Plant Cell 12, 2425–2439.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Corey D
(2003) Sensory transduction in the ear. Journal of Cell Science 116, 1–3.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cosgrove DJ, Hedrich R
(1991) Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard-cells of Vicia-faba L. Planta 186, 143–153.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
De Koninck P, Schulman H
(1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227–230.
| Crossref |
PubMed |
Demaurex N, Frieden M
(2003) Measurements of the free luminal ER Ca2+ concentration with targeted ‘cameleon’ fluorescent proteins. Cell Calcium 34, 109–119.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ding JP, Pickard BG
(1993a) Mechanosensory calcium-selective cation channels in epidermal cells. The Plant Journal 3, 83–110.
| Crossref | GoogleScholarGoogle Scholar |
Ding JP, Pickard BG
(1993b) Modulation of mechanosensitive calcium channels by temperature. The Plant Journal 3, 713–720.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ding JP,
Badot P-M, Pickard BG
(1993) Aluminum and hydrogen ions inhibit a mechanosensory calcium-selective cation channel. Australian Journal of Plant Physiology 20, 771–778.
| PubMed |
Dutta R, Robinson KR
(2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiology 135, 1398–1406.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edwards, KL ,
and
Pickard, BG (1987). Detection and transduction of physical stimuli in plants. In ‘The cell surface and signal transduction’. pp. 45–66. (Springer: Berlin)
Ehrhardt DW,
Wais R, Long SR
(1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673–681.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Falke L,
Edwards KL,
Pickard BG, Misler S
(1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Letters 237, 141–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Feijo JA,
Sainhas J,
Holdaway-Clarke T,
Cordeiro MS,
Kunkel JG, Hepler PK
(2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. BioEssays 23, 86–94.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Felle H
(1988) Auxin content causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles. Planta 174, 495–499.
| Crossref | GoogleScholarGoogle Scholar |
Gens JS,
Reuzeau C,
Doolittle KW,
McNally JG, Pickard BG
(1996) Covisualization by computational optical sectioning microscopy of an array of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194, 215–230.
| Crossref |
PubMed |
Gens JS,
Fujiki M, Pickard BG
(2000) Arabinogalactan protein and wall associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212, 115–134.
| Crossref |
PubMed |
Gordon, JE (1978).
Guharay F, Sachs F
(1984) Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. Journal of Physiology 352, 685–701.
| PubMed |
Gunning, BES ,
and
Steer, MW (1996).
Gunter TE,
Yule DI,
Gunter KK,
Eliseev RA, Salter JD
(2004) Calcium and mitochondria. FEBS Letters 567, 96–102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hamill OP, Martinac B
(2001) Molecular basis of mechanotransduction in living cells. Physiological Reviews 81, 685–740.
| PubMed |
Harper JF
(2001) Dissecting calcium oscillators in plant cells. Trends in Plant Science 6, 395–397.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harper JF,
Breton G, Harmon A
(2004) Decoding Ca2+ signals through plant protein kinases. Annual Review of Plant Biology 55, 263–288.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Haseloff J,
Siemering KR,
Prasher DC, Hodge S
(1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly Proceedings of the National Academy of Science USA 94, 2122–2127.
| Crossref |
Hayakawa K,
Tatsumi H, Sokabe M
(2002) Mechanical stress in the actin cytoskeleton activates SA channels in the vicinity of focal adhesions in endothelial cells. Molecular Biology of the Cell 13, 1916.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Holdaway-Clarke TL, Hepler PK
(2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytologist 159, 539–563.
| Crossref | GoogleScholarGoogle Scholar |
Holdaway-Clarke TL,
Walker NA,
Hepler PK, Overall RL
(2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210, 329–335.
| PubMed |
Holdaway-Clarke TL,
Weddle NM,
Kim S,
Robi A,
Parris C,
Kunkel JG, Hepler PK
(2003) Effect of extracellular Ca2+, pH and borate on growth oscillations in Lilium formosanum pollen tubes. Journal of Experimental Botany 54, 65–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Itano N,
Okamoto S-I,
Zhang D,
Lipton SA, Ruoslahti E
(2003) Cell spreading controls endoplasmic and nuclear calcium: a physical gene regulation pathway from the cell surface to the nucleus. Proceedings of the National Academy of Sciences USA 100, 5181–5186.
| Crossref | GoogleScholarGoogle Scholar |
Johnson KL,
Jones BJ,
Bacic A, Schultz CJ
(2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiology 133, 1911–1925.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kazama H,
Dan H,
Imaseki H, Wasteneys GO
(2004) Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiology 134, 1614–1623.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Köhler RH,
Zipfel WR,
Webb WW, Hanson MR
(1997) The green fluorescent protein as a marker to visualize plant mitochondria in vivo. The Plant Journal 11, 613–621.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lang I,
Barton DA, Overall RL
(2004) Membrane-wall attachments in plasmolysed plant cells. Protoplasma 224, 231–243.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lanini L,
Bachs O, Carafoli E
(1992) The calcium pump of the liver nuclear membrane is identical to that of the endoplasmic reticulum. Journal of Biological Chemistry 267, 11548–11552.
| PubMed |
Lichtscheidl IK, Url WG
(1990) Organization and dynamics of cortical endoplasmic reticulum in inner epidermal cells of onion bulb scales. Protoplasma 157, 203–215.
| Crossref | GoogleScholarGoogle Scholar |
Miesenböck G,
De Angelis DA, Rothman JE
(1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192–195.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miyawaki A,
Llopis J,
Heim R,
McCaffery JM,
Adams JA,
Ikura M, Tsien RY
(1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882–887.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miyawaki A,
Griesbeck O,
Heim R, Tsien RY
(1999) Dynamic and quantitative Ca2+ measurements using improved cameleons. Proceedings of the National Academy of Sciences USA 96, 2135–2140.
| Crossref | GoogleScholarGoogle Scholar |
Nagai T,
Yamada S,
Tominaga T,
Ichikawa M, Miyawaki A
(2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences USA 101, 10554–10559.
| Crossref | GoogleScholarGoogle Scholar |
Ng CKY, McAinsh MR
(2003) Encoding specificity in plant calcium signaling: hot-spotting the ups and downs and waves. Annals of Botany 92, 477–485.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nothnagel EA
(1997) Proteoglycans and related components in plant cells. International Reviews of Cytology 174, 195–291.
Oldroyd GED,
Engstrom EM, Long SR
(2001) Ethylene inhibits the nod factor signal transduction pathway of Medicago truncatula. The Plant Cell 13, 1835–1849.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palmer AE,
Jin C,
Reed JC, Tsien RY
(2004) Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proceedings of the National Academy of Sciences USA 101, 17404–17409.
| Crossref | GoogleScholarGoogle Scholar |
Pauly N,
Knight MR,
Thuleau P,
Van der Luit AH,
Moreau M,
Trewavas AJ,
Ranjeva R, Mazars C
(2000) Cell signalling — control of free calcium in plant cell nuclei. Nature 405, 754–755.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pauly N,
Knight MR,
Thuleau P,
Graziana A,
Muto S,
Ranjeva R, Mazars C
(2001) The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells. Cell Calcium 30, 413–421.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pickard BG
(1994) Contemplating the plasmalemmal control center model. Protoplasma 182, 1–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pickard, BG ,
and
Ding, JP (1992). Gravity sensing by higher plants. In ‘Advances in comparative and environmental physiology. Vol. 10. Comparative aspects of mechanoreceptor systems’. pp. 81–110. (Springer: Berlin)
Pickard BG, Ding JP
(1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control center? Australian Journal of Plant Physiology 20, 439–459.
| PubMed |
Pont-Lezica RF,
McNally JG, Pickard BG
(1993) Wall-to-membrane linkers in onion epidermis. Plant, Cell & Environment 16, 111–123.
Qi Z,
Kishigami A,
Nakagawa Y,
Iida H, Sokabe M
(2004) Mechanosensitive anion channel in Arabidopsis thaliana mesophyll cells. Plant & Cell Physiology 45, 1704–1708.
| Crossref |
PubMed |
Robert V,
Gurlini P,
Tosello V,
Nagai T,
Miyawaki A,
Di Lisa F, Pozzan T
(2001) Beat-to-beat oscillations of mitochondrial [Ca2+] in cardiac cells. EMBO Journal 20, 4998–5007.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roy S,
Jauh GY,
Hepler PK, Lord EM
(1998) Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204, 450–458.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roy SJ,
Holdaway-Clarke RL,
Hackett GR,
Kunkel JG,
Lord EM, Hepler PK
(1999) Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. The Plant Journal 19, 379–386.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ryan PR,
Newman IA, Arif I
(1992) Rapid calcium exchange for protons and potassium in cell walls of Chara. Plant, Cell & Environment 15, 675–683.
Sachs F
(1997) Mechanical transduction by ion channels: how forces reach the channel. Society of General Physiologists Series 97 52, 209–218.
Sanders D,
Brownlee C, Harper JF
(1999) Communicating with calcium. The Plant Cell 11, 691–706.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sanders D,
Pelloux J,
Brownlee C, Harper JF
(2002) Calcium at the crossroads of signaling. The Plant Cell 14, S401–S417.
| PubMed |
Serpe MD, Nothnagel EA
(1994) Effects of Yariv phenylglycosides on Rosa cell suspensions: evidence for the involvement of arabinogalactan-proteins in cell proliferation. Planta 193, 542–550.
Shabala SN,
Newman IA, Morris J
(1997) Oscillations in hydrogen and calcium ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiology 113, 111–118.
| PubMed |
Stickens D, Verbelen J-P
(1996) Spatial structure of mitochondria and ER denotes changes in cell physiology of cultured tobacco protoplasts. The Plant Journal 9, 85–92.
| Crossref | GoogleScholarGoogle Scholar |
Sukharev S, Corey DP
(2004) Mechanosensitive channels: multiplicity of families and gating paradigms. Science ,
Sun WX,
Zhao ZD,
Hare MC,
Kieliszewski MJ, Showalter AM
(2004) Tomato LeAGP-1 is a plasma membrane-bound, glycosylphosphatidylinositol-anchored arabinogalactan-protein. Physiologia Plantarum 120, 319–327.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Verica JA, He ZH
(2002) The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiology 129, 455–459.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Watahiki MK,
Trewavas AJ, Parton RM
(2004) Fluctuations in the pollen tube tip-focused calcium gradient are not reflected in nuclear calcium level: a comparative analysis using recombinant yellow cameleon calcium reporter. Sexual Plant Reproduction 17, 125–130.
| Crossref | GoogleScholarGoogle Scholar |
Xiong TC,
Jauneau A,
Ranjeva R, Mazars C
(2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signaling. The Plant Journal 40, 12–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yoneda A,
Akatsuka M,
Kumagai F, Hasezawa S
(2004) Disruption of actin microfilaments causes cortical microtubule disorganization and extra-phragmoplast formation at M / G(1) interface in synchronized tobacco cells. Plant & Cell Physiology 45, 761–769.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhu JK,
Shi J,
Singh U,
Wyatt SE,
Bressan RA,
Hasegawa PM, Carpita NC
(1993) Enrichment of vitronectin-like and fibronectin-like proteins in NaCl-adapted plant-cells and evidence for their involvement in plasma-membrane cell-wall adhesion. The Plant Journal 3, 637–646.
