Actin filaments modulate hypoosmotic-responsive K+ efflux channels in specialised cells of developing bean seed coats
Wen-Hao Zhang A D , John W. Patrick B and Stephen D. Tyerman CA Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, PR China.
B School of Biological and Chemical Sciences, The University of Newcastle, Newcastle, NSW 2308, Australia.
C School of Agriculture, Food and Wine, The University of Adelaide, PMB#1 Glen Osmond, SA 5064, Australia.
D Corresponding author. Email: whzhang@ibcas.ac.cn
Functional Plant Biology 34(10) 874-884 https://doi.org/10.1071/FP07138
Submitted: 31 May 2007 Accepted: 24 July 2007 Published: 13 September 2007
Abstract
In developing bean (Phaseolus vulgaris L.) seeds, nutrients move in the symplasm from sieve elements to ground-parenchyma cells where they are transported across the plasma membrane into the seed apoplasm. Release of nutrients to the seed apoplasm is related to the osmotic conditions of the apoplasm. A hypoosmotic solution, resulting from enhanced uptake of nutrients by cotyledons, stimulates nutrient release from seed coat to the apoplasm. We investigated hypoosmotic nutrient release by examining the ionic membrane currents that respond to hypoosmotic treatment in protoplasts derived from three important cell types that occur at the seed coat–cotyledonary boundary. A non-selective but predominantly K+ efflux current that displayed a distinct time-dependent inactivation was elicited by membrane depolarisation under hypoosmotic conditions only in ground-parenchyma protoplasts. Hypoosmotic treatment had little effect on whole-cell ionic currents in protoplasts derived from coat chlorenchyma cells and cotyledon dermal cells. The inactivating K+ efflux current was elicited under isosmotic conditions by treatment with cytochalasin D, which disrupts actin filaments. Hypoosmotic treatment and cytochalasin D failed to induce the K+ current in ground-parenchyma protoplasts in the presence of the actin stabiliser, phalloidin. The net efflux of K+ from intact seed coats was enhanced by hypoosmotic treatment and cytochalasin D, and the stimulation of K+ efflux induced by the hypoosmotic treatment and cytochalasin D was abolished by phalloidin. A bursting Cl– channel previously described showed a similar pattern of responses. These results suggest that hypoosmotic-dependent KCl efflux from seed coats is mediated by the inactivating K+ outward current and bursting Cl– channel, and that actin filaments act as components of the transduction process that is a function of cell volume.
Additional keywords: cytoskeleton, hypoosmotic treatment, K+ outward current, patch clamp, Phaseolus vulgaris, seed coat.
Acknowledgements
This study was supported by Australian Research Council grants to S.D. Tyerman and J.W. Patrick, Natural Science Foundation of China (No. 30521002 and No. 30570136) and Chinese Academy of Sciences’ One Hundred Talent Project. We thank Wendy Sullivan for her excellent technical assistance.
Alexandre J, Lassalles JP
(1991) Hydrostatic and osmotic pressure activated channel in plant vacuole. Biophysical Journal 60, 1326–1336.
Berdiev B,
Prat AG,
Cantiello HF,
Ausiello DA,
Fuller C,
Jovov B,
Benos DJ, Ismailov I
(1996) Regulation of epithelial sodium channels by short actin filaments. Journal of Biological Chemistry 271, 17704–17711.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bisson MA,
Beilby MJ, Shepherd VA
(2006) Electrophysiology of turgor regulation in marine siphonous green algae. Journal of Membrane Biology 211, 1–14.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cantiello HF
(1997) Role of actin filament organization in cell volume and ion channel regulation. Journal of Experimental Zoology 279, 425–435.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Coluccio LM, Tilney LG
(1984) Phalloidin enhances actin assembly by preventing monomer dissociation. Journal of Cell Biology 99, 529–535.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ellis EC,
Turgeon R, Spanswick RM
(1992) Quantitative analysis of photosynthate unloading in developing seeds of Phaseolus vulgaris L. II. Pathways and sensitivity to turgor. Plant Physiology 99, 643–651.
| PubMed |
Findlay GP
(2001) Membranes and the electrophysiology of turgor regulation. Australian Journal of Plant Physiology 28, 617–634.
Homann U, Thiel G
(2002) The number of K+ channels in the plasma membrane of guard cell protoplasts changes in parallel with the surface area. Proceedings of the National Academy of Sciences USA 99, 10215–10220.
| Crossref | GoogleScholarGoogle Scholar |
Hwang JU,
Suh S,
Yi H,
Kim J, Lee Y
(1997) Actin filaments modulate both stomatal opening and inward K+-channel activities in guard cells of Vicia faba L. Plant Physiology 115, 335–342.
| PubMed |
Janmey PA
(1998) The cytoskeleton and cell signalling: component localization and mechanical coupling. Physiological Reviews 78, 763–781.
| PubMed |
Liu K, Luan S
(1998) Voltage-dependent K+ channels as targets of osmosensing in guard cells. The Plant Cell 10, 1957–1970.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacRobbie EAC
(2006a) Control of volume and turgor in stomatal guard cells. Journal of Membrane Biology 210, 131–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacRobbie EAC
(2006b) Osmotic effects on vacuolar ion release in guard cells. Proceedings of the National Academy of Sciences USA 103, 1135–1140.
| Crossref | GoogleScholarGoogle Scholar |
Offler CE, Patrick JW
(1984) Cellular structures, plasma membrane surface areas and plasmodesmatal frequencies of seed coats of Phaseolus vulgaris L. in relation to photosynthate transfer. Australian Journal of Plant Physiology 11, 79–100.
Parker DR,
Zelazny LW, Kinraide TB
(1987) Improvements to the program GEOCHEM. Soil Science Society of America Journal 51, 488–491.
Patrick JW
(1984) Photosynthate unloading from seed coats of Phaseolus vulgaris L. Control by water relations. Journal of Plant Physiology 115, 297–310.
Patrick JW
(1994) Turgor-dependent unloading of assimilates from coats of developing legume seed. Assessment of the significance of the phenomenon in the whole plant. Physiologia Plantarum 90, 645–654.
| Crossref | GoogleScholarGoogle Scholar |
Patrick JW
(1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology and Plant Molecular Biology 48, 191–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Patrick JW, Offler CE
(2001) Compartmentation of transport and transfer events in developing seeds. Journal of Experimental Botany 52, 551–564.
| Crossref |
PubMed |
Pedersen SF,
Hoffmann EK, Mills JW
(2001) The cytoskeleton and cell volume regulation. Comparative Biochemistry and Physiology 130, 385–399.
| PubMed |
Pei ZM,
Baizabal-Aguirre VM,
Allen GJ, Schroeder JI
(1998) A transient outward-rectifying K+ channel current down-regulated by cytosolic Ca2+ in Arabidopsis thaliana guard cells. Proceedings of the National Academy of Sciences USA 95, 6548–6553.
| Crossref | GoogleScholarGoogle Scholar |
Prat AG,
Xiao YF,
Ausiello DA, Cantiello HF
(1995) cAMP-independent regualtion of CFTR by the actin cytoskeleton. American Journal of Physiology. Cell Physiology 268, C1552–C1561.
Raucher D, Sheeta MP
(2001) Phospholipase C activation by anesthetics decreases membrane- cytoskeleton adhesion. Journal of Cell Science 114, 3759–3766.
| PubMed |
Schubert T, Akopian A
(2004) Actin filaments regulate voltage-gated ion channels in salamander retinal ganglion cells. Neuroscience 125, 583–590.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Steudle E
(1989) Water-flow in plants and its coupling to other processes – an overview. Methods in Enzymology 174, 183–225.
Stoeckel H, Takeda K
(2002) Plasmalemmal voltage-activated K+ currents in protoplasts from tobacco BY-2 cells: possible regulation by actin microfilaments? Protoplasma 220, 79–87.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walker NA,
Patrick JW,
Zhang WH, Fieuw S
(1995) Efflux of photosynthate and acid from developing seed coats of Phaseolus vulgaris L.: a chemiosmotic analysis of pump-driven efflux. Journal of Experimental Botany 45, 597–697.
Walker NA,
Zhang WH,
Harrington G,
Holdaway N, Patrick JW
(2000) Effluxes of solutes from developing seed coats of Phaseolus vulgaris L. and Vicia faba L.: locating the effects of turgor in a coupled chemisosmotic system. Journal of Experimental Botany 51, 1047–1055.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wang X-D,
Harrington G,
Patrick JW,
Offler CE, Fieuw S
(1995) Cellular pathways of photosynthate transport in coats of developing seed of Vicia faba L. and Phaseolus vulgaris L.: principal cellular sites of efflux. Journal of Experimental Botany 46, 49–63.
| Crossref | GoogleScholarGoogle Scholar |
Wang Y-F,
Fan L-M,
Zhang W-Z,
Zhang W, Wu W-H
(2004) Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiology 136, 3892–3904.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wojtaszek P,
Anielska-Mzaur A,
Gabrys H,
Baluska F, Volkmann D
(2005) Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing. Functional Plant Biology 32, 721–736.
| Crossref | GoogleScholarGoogle Scholar |
Wolswinkel P
(1992) Transport of nutrients into developing seeds: a review of physiological mechanisms. Seed Science Research 2, 59–73.
Zhang W,
Fan L-M, Wu WH
(2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiology 143, 1140–1151.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang WH,
Atwell BJ,
Patrick JW, Walker NA
(1996) Turgor-dependent assimilates efflux from coats of developing Phaseolus vulgaris L. seeds: water relations of the cells involved in efflux. Planta 119, 25–33.
Zhang WH,
Walker NA,
Patrick JW, Tyerman SD
(1997) Mechanism of solute efflux from seed coat: whole-cell K+ currents in the plasma membrane of protoplasts derived from Vicia faba L. seed coats. Journal of Experimental Botany 48, 1565–1572.
Zhang WH,
Walker NA,
Tyerman SD, Patrick JW
(2000) Fast activation of a time-dependent outward current in protoplasts derived from coats of developing Phaseolus vulgaris seeds. Planta 211, 894–898.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang WH,
Skerrett M,
Walker NA,
Tyerman SD, Patrick JW
(2002) Non-selective cation channels and currents in protoplasts derived from coats of developing seeds of beans. Plant Physiology 128, 388–399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang WH,
Walker NA,
Tyerman SD, Patrick JW
(2004a) Pulsing Cl– channels linked to hypoosmotically-induced turgor regulation in coat cells of developing bean seeds. Journal of Experimental Botany 55, 993–1001.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang WH,
Walker NA,
Tyerman SD, Patrick JW
(2004b) Ca2+-dependent K current in dermal cells of developing bean cotyledons. Plant, Cell & Environment 27, 251–262.
| Crossref | GoogleScholarGoogle Scholar |
