Reversible birefringence suggests a role for molecular self-assembly in forisome contractility
Winfried S. Peters A D , Reinhard Schnetter B and Michael Knoblauch CA Indiana/Purdue University, Department of Biology, 2101 East Coliseum Boulevard, Fort Wayne IN 46805-1499, USA.
B Institut fur Allgemeine Botanik, Justus-Liebig-Universität, Senckenbergstr. 17-21, D-35390 Gießen, Germany.
C School of Biological Sciences, Washington State University, Pullman WA 99164-4236, USA.
D Corresponding author. Email: petersw@ipfw.edu
E This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.
Functional Plant Biology 34(4) 302-306 https://doi.org/10.1071/FP06281
Submitted: 2 November 2006 Accepted: 13 December 2006 Published: 19 April 2007
Abstract
Forisomes are contractile protein bodies that control the effective diameter of the sieve elements of the faboid legumes by reversible, Ca2+-driven changes of shape. Forisomes consist of fibrils; we inferred from available electron-microscopical data (which necessarily provide images of fixed, non-functional forisomes) that a reversible assembly of ordered fibrillar arrays might be involved in the contractile mechanism. Here we examined functional forisomes isolated from Vicia faba L. by differential interference contrast microscopy and polarisation microscopy. We found them birefringent in the longitudinally expanded but not in the contracted state, showing ‘parallel extinction’ with the direction of vibration of the slow ray coinciding with their long axis (positive birefringence). These findings met predictions derived from the theory of form birefringence in rodlet composite bodies, and supported the idea of molecular self-assembly as a factor in forisome contractility.
Additional keywords: calcium-dependent contractility, phloem transport, Vicia faba.
Acknowledgements
We thank Rüdiger Borchardt (Institut für Lithosphärenforschung, Justus-Liebig-Universität, Gießen, Germany) for technical support. This work was funded in parts by the Nanobiotechnology program of the BMBF (Federal Ministry of Education and Research, Germany).
Arsanto JP
(1982) Observations on P-protein in dicotyledons. Substructural and developmental features. American Journal of Botany 69, 1200–1212.
| Crossref | GoogleScholarGoogle Scholar |
Arsanto JP
(1986) Ca2+-binding sites and phosphatase activities in sieve element reticulum and P-protein of chick-pea phloem. A cytochemical and x-ray microanalysis survey. Protoplasma 132, 160–171.
| Crossref | GoogleScholarGoogle Scholar |
van Bel AJE, Knoblauch M
(2000) Sieve element and companion cell: The story of the comatose patient and the hyperactive nurse. Australian Journal of Plant Physiology 27, 477–487.
van Bel AJE,
Ehlers K, Knoblauch M
(2002) Sieve elements caught in the act. Trends in Plant Science 7, 126–132.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bendet IJ, Bearden J
(1972) Birefringence of spermatozoa. II. Form birefringence in bull sperm. Journal of Cell Biology 55, 501–510.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fisher DB
(1975) Structure of functional soybean sieve elements. Plant Physiology 56, 555–569.
| PubMed |
Frey-Wyssling A
(1974) Ultrastructure research in biology before the introduction of the electron microscope. Journal of Microscopy 100, 21–34.
| PubMed |
Gould N,
Thorpe MR,
Koroleva O, Minchin PEH
(2005) Phloem hydrostatic pressure relates to solute loading rate: a direct test of the Münch hypothesis. Functional Plant Biology 32, 1019–1026.
| Crossref | GoogleScholarGoogle Scholar |
Inoué S
(1999) Windows to dynamic fine structures, then and now. FASEB Journal 13, S185–S190.
| PubMed |
Jin LW,
Claborn KA,
Kurimoto M,
Geday MA,
Maezawa I,
Sohraby F,
Estrada M,
Kaminsky W, Kahr B
(2003) Imaging linear birefringence and dichroism in cerebral amyloid pathologies. Proceedings of the National Academy of Sciences USA 100, 15294–15298.
| Crossref | GoogleScholarGoogle Scholar |
Katoh K,
Hammar K,
Smith PJS, Oldenbourg R
(1999) Birefringence imaging directly reveals architectural dynamics of filamentous actin in living growth cones. Molecular Biology of the Cell 10, 197–210.
| PubMed |
Knoblauch M, van Bel AJE
(1998) Sieve tubes in action. The Plant Cell 10, 35–50.
| Crossref | GoogleScholarGoogle Scholar |
Knoblauch M, Peters WS
(2004a) Biomimetic actuators: where technology and cell biology merge. Cellular and Molecular Life Sciences 61, 2497–2509.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Knoblauch M, Peters WS
(2004b) Forisomes, a novel type of Ca2+-dependent protein motor. Cell Motility and the Cytoskeleton 58, 137–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Knoblauch M,
Peters WS,
Ehlers K, van Bel AJE
(2001) Reversible calcium-regulated stopcocks in legume sieve tubes. The Plant Cell 13, 1221–1230.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Knoblauch M,
Noll GA,
Müller T,
Prüfer D,
Schneider-Hüther I,
Scharner D,
van Bel AJE, Peters WS
(2003) ATP-independent contractile proteins from plants. Nature Materials 2, 600–603.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Laflèche D
(1966) Ultrastucture et cytochimie des inclusions flagellées des cellules criblées de Phaseolus vulgaris. Journal de Microscopie 5, 493–510.
Lang A, Minchin PEH
(1986) Phylogenetic distribution and mechanism of translocation inhibition by chilling. Journal of Experimental Botany 37, 389–398.
| Crossref |
Lawton DM
(1978a) Ultrastructural comparison of the tailed and tailless P-protein crystals respectively of runner bean (Phaseolus multiflorus) and garden pea (Pisum sativum) with tilting stage electron microscopy. Protoplasma 97, 1–11.
| Crossref | GoogleScholarGoogle Scholar |
Lawton DM
(1978b) P-protein crystals do not disperse in uninjured sieve elements of roots in runner bean (Phaseolus multiflorus) fixed with glutaraldehyde. Annals of Botany 42, 353–361.
Liu L,
Oldenbourg R,
Trimarchi JR, Keefe DL
(2000) A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes. Nature Biotechnology 18, 223–225.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mavroidis C, Dubey A
(2003) From pulses to motors. Nature Materials 2, 573–574.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moriyama Y,
Okamoto H, Asai H
(1999) Rubber-like elasticity and volume changes in the isolated spasmoneme of giant Zoothamnium sp. under Ca2+-induced contraction. Biophysical Journal 76, 993–1000.
| PubMed |
Oldenbourg R
(1996) A new view on polarization microscopy. Nature 381, 811–812.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palevitz BA, Newcomb EH
(1971) The ultrastructure and development of tubular and crystalline P-protein in the sieve elements of certain papilionaceous legumes. Protoplasma 72, 399–425.
| Crossref | GoogleScholarGoogle Scholar |
Pantic-Tanner Z, Eden D
(1999) Calculation of protein form birefringence using the finite element method. Biophysical Journal 76, 2943–2950.
| PubMed |
Peters WS,
van Bel AJE, Knoblauch M
(2006) The geometry of the forisome/sieve element/sieve plate complex in the phloem of Vicia faba L. leaflets. Journal of Experimental Botany 57, 3091–3098.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pickard WF, Minchin PE
(1990) The transient inhibition of phloem translocation in Phaseolus vulgaris by abrupt temperature drops, vibration, and electric shock. Journal of Experimental Botany 41, 1361–1369.
| Crossref |
Pickard WF, Minchin PE
(1992) The nature of the short-term inhibition of stem translocation produced by abrupt stimuli. Australian Journal of Plant Physiology 19, 471–480.
Pickard WF,
Knoblauch M,
Peters WS, Shen AQ
(2006) Prospective energy densities in the forisome, a new smart material. Materials Science and Engineering C 26, 104–112.
| Crossref | GoogleScholarGoogle Scholar |
Schmidt WJ
(1940) Die Doppelbrechung des Stieles von Carchesium, insbesondere die optisch negative Schwankung seines Myonemes bei der Kontraktion. Protoplasma 35, 1–14.
Sjolund RD
(1997) The phloem sieve element: a river runs through it. The Plant Cell 9, 1137–1146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smela E
(2003) Conjugated polymer actuators for biomedical applications. Advanced Materials 15, 481–494.
| Crossref | GoogleScholarGoogle Scholar |
Wergin WP, Newcomb EH
(1970) Formation and dispersal of crystalline P-protein in sieve elements of soybean (Glycine max L.). Protoplasma 71, 365–388.
| Crossref | GoogleScholarGoogle Scholar |
Wiener O
(1912) Theorie des Mischkörpers für das Feld der stationären Strömung. Abhandlungen der Mathematisch-Physikalischen Klasse der Sächsischen Akademie der Wissenschaften 32, 507–604.