Calcium-energized motor protein forisome controls damage in phloem: potential applications as biomimetic “smart” material

References

• Alosi MC, Melroy DL, Park RB. (1988). The regulation of gelation of phloem exudate from Cucurbita fruit by dilution, glutathione, and glutathione reductase. Plant Physiol, 86, 1089–94
   PubMed Web of Science ®Google Scholar
• Atkinson HJ, Babbitt PC. (2009). An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations. PLoS Comput Biol, 5, e1000541
   PubMed Web of Science ®Google Scholar
• Barnes A, Bale J, Constantinidou C, et al. (2004). Determining protein identity from sieve element sap in Ricinus communis L. by quadrupole time of flight (Q-TOF) mass spectrometry. J Expt Bot, 55, 1473–81
   PubMed Web of Science ®Google Scholar
• Bearda NA, Laverb DR, Dulhuntya AF. (2004). Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog Biophys Mol Biol, 85, 33–69
   PubMedGoogle Scholar
• Behnke HD, Sjolund RD. (1990). Sieve elements: comparative structure, induction and development. Berlin, Germany: Springer
   Google Scholar
• Behnke HD. (1991a). Nondispersive protein bodies in sieve elements: a survey and review of their origin, distribution and taxonomic significance. IAWA Bull, 12, 143–75
   Google Scholar
• Behnke HD. (1991b). Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. ALISO, 3, 167–82
   Google Scholar
• Beyenbach J, Weber C, Kleinig H. (1974). Sieve-tube proteins from Cucurbita maxima. Planta, 119, 113–24
   Google Scholar
• Bostwick DE, Dannenhoffer JM, Skaggs MI, et al. (1992). Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell, 4, 1539–48
   Google Scholar
• Bucsenez M, Rüping B, Behrens S, et al. (2012). Multiple cis-regulatory elements are involved in the complex regulation of the sieve element-specific MtSEO-F1 promoter from Medicago truncatula. Plant Biol, 14, 714--24
   PubMedGoogle Scholar
• Buttafoco L, Kolman NG, Engbers-Buijtenhuijs P, et al. (2006). Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials, 27, 724–34
   PubMed Web of Science ®Google Scholar
• Carolan JC, Fitzroy CI, Ashton PD, et al. (2009). The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics, 9, 2457–67
   PubMed Web of Science ®Google Scholar
• Chakraborty I, Tang WC, Bame DP, Tang TK. (2000). MEMS Micro valve for space applications. Sens Actuators A: Physical, 88, 188–93
   Google Scholar
• Clark AM, Jacobsen KR, Bostwick DE, et al. (1997). Molecular characterization of a phloem-specific gene encoding the filament protein, Phloem Protein 1 (PP1), from Cucurbita maxima. Plant J, 12, 49–61
   PubMedGoogle Scholar
• Cronshaw J, Esau K. (1967). Tubular and fibrillar components of mature and differentiating sieve elements. J Cell Biol, 34, 801–15
   PubMed Web of Science ®Google Scholar
• Ehlers K, Knoblauch M, van Bel AJE. (2000). Ultrastructural features of well-preserved and injured sieve elements: minute clamps keep the phloem transport conduits free for mass flow. Protoplasma, 214, 80–92
   Google Scholar
• Eleftheriou E. (1990). Monocotyledons. In: Behnke HD, Sjolund RD, eds. Sieve elements. Comparative structure, induction and development. Berlin, Germany: Springer, 139–59
   Google Scholar
• Engleman EM, Esau K. (1964). The problem of callose deposition in phloem. Science, 144, 562
   Google Scholar
• Ernst AM, Jekat SB, Zielonka S, et al. (2012). Sieve element occlusion (SEO) genes encode structural phloem proteins involved in wound sealing of the phloem. Proc Natl Acad Sci USA, 109, 980–9
   Google Scholar
• Esau K. (1969). The phloem. Encyclopedia of plant anatomy, Vol. 5. Berlin, Germany: Bornträger
   Google Scholar
• Evert RF. (1982). Sieve-tube structure in relation to function. BioScience, 32, 789–95
   Web of Science ®Google Scholar
• Evert RF. (1990). Dicotyledons. In: Behnke HD, Sjolund RD, eds. Sieve elements. Comparative structure, induction and development. Berlin, Germany: Springer, 103–37
   Google Scholar
• Evert RF, Eschrich W, Eichhorn SE. (1973). P-protein distribution in mature sieve elements of Cucurbita maxima. Planta, 109, 193–210
   Google Scholar
• Fisher DB. (1975). Structure of functional soybean sieve elements. Plant Physiol, 56, 555–69
   PubMed Web of Science ®Google Scholar
• Fontanellaz ME. (2006). Cloning and molecular characterization of vff1 gene encoding forisomes of Vicia faba [dissertation]. Germany: RWTH
   Google Scholar
• Furch AC, Hafke JB, Schulz A, van Bel AJ. (2007). Ca2+ mediated remote control of reversible sieve tube occlusion in Vicia faba. J Exp Bot, 58, 2827–38
   PubMed Web of Science ®Google Scholar
• Furch ACU, Zimmermann MR, Will T, et al. (2010). Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot, 61, 3697–708
   PubMedGoogle Scholar
• Gaupels F, Furch AC, Will T, et al. (2008). Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals. New Phytol, 178, 634–46
   PubMed Web of Science ®Google Scholar
• Giavalisco P, Kapitza K, Kolasa A, et al. (2006). Towards the proteome of Brassica napus phloem sap. Proteomics, 6, 896–909
   PubMed Web of Science ®Google Scholar
• Glowacki J, Mizuno S. (2007). Collagen scaffolds for tissue engineering. Biopolymers, 89, 338–44
   Web of Science ®Google Scholar
• Golecki B, Schulz A, Thompson GA. (1999). Translocation of structural P proteins in the phloem. Plant Cell, 11, 127–40
   PubMed Web of Science ®Google Scholar
• Groscurth S, Müller B, Schwan S, et al. (2012). Artificial forisomes are ideal models of forisome assembly and activity that allow the development of technical devices. Biomacromolecules, 13, 3076–86
   Google Scholar
• Hartig T. (1854). Ueber die Querscheidewaende zwischen den einzelnen Gliedern derSiebröhren in Cucurbita pepo. Botanische Zeitung, 12, 51–4
   Google Scholar
• Hayashi H, Fukuda A, Suzui N, Fujimaki S. (2000). Proteins in the sieve tube-companion cell complexes: their detection, localization and possible functions. Aust J Plant Physiol, 27, 489–96
   Google Scholar
• Ishiwatari Y, Honda C, Kawashima I, et al. (1995). Thioredoxin h is one of the major proteins in rice phloem sap. Planta, 195, 456–63
   PubMedGoogle Scholar
• Jaeger M, Uhlig K, Clausen-Schaumann H, Duschl C. (2008). The structure and functionality of contractile forisome protein aggregates. Biomaterials, 29, 247–56
   Google Scholar
• Jekat SB, Ernst AM, Zielonka S, et al. (2012). Interactions among tobacco sieve element occlusion (SEO) proteins. Plant Signal Behav, 7, 1724–6
   PubMed Web of Science ®Google Scholar
• Kempers R, Ammerlaan A, van Bel AJE. (1998). Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically phloem-loading species. Plant Physiol, 116, 271–8
   Web of Science ®Google Scholar
• Kempers R, van Bel AJE. (1997). Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a size exclusion limit of at least 10 kDa. Planta, 201, 195–201
   Google Scholar
• Knoblauch M, Peters WS. (2004a). Forisomes, a novel type of Ca2+ dependent contractile protein motor. Cell Motil Cytoskeleton, 58, 137–42
   PubMedGoogle Scholar
• Knoblauch M, Peters WS. (2004b). Biomimetic actuators: where technology and cell biology merge. CMLS, 61, 2497–509
   PubMedGoogle Scholar
• Knoblauch M, Peters WS, Ehlers K, van Bel AJE. (2001). Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell, 13, 1221–30
   PubMed Web of Science ®Google Scholar
• Knoblauch M, Stubenrauch M, van Bel AJ, Peters WS. (2012). Forisome performance in artificial sieve tubes. Plant Cell Environ, 35, 1419–27
   Google Scholar
• Knoblauch M, van Bel AJE. (1998). Sieve tubes in action. Plant Cell, 10, 35–50
   Web of Science ®Google Scholar
• Knoblauch M, Noll GA, Müller T, et al. (2003). ATP-independent contractile proteins from plants. Nat Mater, 2, 600–3
   PubMed Web of Science ®Google Scholar
• Kollmann R. (1973). Cytologie des Phloems. In: Ruska H, Sitte P, eds. Grundlagen der cytologie. Jena, Germany: Gustav Fischer, 479–505
   Google Scholar
• Lawton DM. (1978a). Ultrastructural comparison of tailed and tail-less P-protein crystals respectively of runner bean (Phaseolus multiflorus) and garden pea (Pisum sativum) with tilting stage electron micoscopy. Protoplasma, 97, 1–11
   Web of Science ®Google Scholar
• Lawton DM. (1978b). P-protein crystals do not disperse in uninjured sieve elements in roots of runner bean (Phaseolus multiflorus) fixed with glutaraldehyde. Ann Bot, 42, 353–61
   Google Scholar
• Lee DR, Arnold DC, Fensom DS. (1971). Some microscopical observations of functioning sieve tubes of Heracleum using Nomarski optics. J Exp Bot, 22, 25–38
   Google Scholar
• Lin M-K, Lee Y-J, Lough TJ, et al. (2009). Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics, 8, 343–56
   Google Scholar
• MacLennan DH, Reithmeier RAF. (1998). Ion tamers. Nat Struct Biol, 5, 409–11
   PubMedGoogle Scholar
• Martin LM. (1995). Thioredoxin – a fold for all reasons. Structure, 3, 245–50
   PubMed Web of Science ®Google Scholar
• McNairn RB, Currier HB. (1968). Translocation blockage by sieve plate callose. Planta, 82, 369–80
   Google Scholar
• Miki H, Okada Y, Hirokawa N. (2005). Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol, 15, 467–76
   PubMed Web of Science ®Google Scholar
• Miles PW. (1999). Aphid saliva. Biol Rev Camb Philos Soc, 74, 41–85
   Web of Science ®Google Scholar
• Mrazek A. (1910). Über geformte eiweiβhaltige inhaltstoffe bei den leguminosen. Österr Bot Z, 60, 198–201
   Google Scholar
• Müller B, Noll GA, Ernst AM. (2010). Recombinant artificial forisomes provide ample quantities of smart biomaterials for use in technical devices. Appl Microbiol Biotechnol, 88, 689–98
   PubMed Web of Science ®Google Scholar
• Musetti R, Buxa SV, Marco FD, et al. (2013). Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Mol Plant Microbe Interact, 4, 379–86
   Google Scholar
• Murray C, Christeller JT. (1995). Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudate and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biol Chem, 376, 281–7
   PubMedGoogle Scholar
• Noll GA. (2005). Molekularbiologische Charakterisierung der Forisome. Doctoral Thesis (in German; supervisor: A.J.E. van Bel), Justus-Liebig Universität, Gießen, Germany. http://geb.unigiessen.de/geb/volltexte/2007/4805/pdf/NollGundula-2005–12–12.pdf
   Google Scholar
• Noll GA, Fontanellaz ME, Rüping B, et al. (2007). Spatial and temporal regulation of the forisome gene for1 in the phloem during plant development. Plant Mol Biol, 65, 285–94
   PubMed Web of Science ®Google Scholar
• Noll GA, Müller B, Ernst AM, et al. (2011). Native and artificial forisomes: functions and applications. Appl Microbiol Biotechnol, 89, 1675–82
   Google Scholar
• 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, 399–426
   Google Scholar
• Parthasarathy MV, Pesacreta TC. (1980). Microfilaments in plant vascular cells. Can J Bot, 58, 807–15
   Google Scholar
• Pélissier HC, Peters WS, Collier R, et al. (2008). GFP tagging of sieve element occlusion [SEO] proteins results in green fluorescent forisomes. Plant Cell Physiol, 49, 1699–710
   PubMed Web of Science ®Google Scholar
• Peters WS, Knoblauch M, Warmann SA, et al. (2007a). Tailed forisomes of Canavalia gladiata: a new model to study Ca2+ driven protein contractility. Ann Bot, 100, 101–9
   PubMedGoogle Scholar
• Peters WS, Schnetter R, Knoblauch M. (2007b). Reversible birefringence suggests a role for molecular self-assembly in forisome contractility. FPB, 34, 302–6
   PubMedGoogle Scholar
• Przybyla DE, Chmielewski J. (2010). Higher-order assembly of collagen peptides into nano- and microscale materials. Biochemistry, 49, 4411–19
   PubMed Web of Science ®Google Scholar
• Read SM, Northcote DH. (1983). Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin). Eur J Biochem, 134, 561–9
   PubMedGoogle Scholar
• Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ. (2001). The phloem as a conduit for inter-organ communication. Curr Opin Plant Biol, 4, 202–9
   PubMed Web of Science ®Google Scholar
• Rüping B, Ernst AM, Jekat SB, et al. (2010). Molecular and phylogenetic characterization of the sieve element occlusion gene family in Fabaceae and non-Fabaceae plants. BMC Plant Biol, 10, 219
   PubMed Web of Science ®Google Scholar
• Roy A, Kucukural A, Zhang Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc, 5, 725–38
   PubMed Web of Science ®Google Scholar
• Roy A, Yang J, Zhang Y. (2012). COFACTOR: an accurate comparative algorithm for structure-based protein function annotation. Nucleic Acids Res, 40, W471–7
   PubMed Web of Science ®Google Scholar
• Sabnis DD, Hart JW. (1973). P-protein in sieve elements. I. Ultrastructure after treatment with vinblastine and colchicine. Planta, 109, 127–33
   PubMedGoogle Scholar
• Sabnis DD, Sabnis HM. (1995). Phloem proteins: structure, biochemistry and function. In: Iqbal M, eds. The cambial derivatives, encyclopedia of plant anatomy. Vol. 9, Berlin, Germany: Borntraeger, 271–92
   Google Scholar
• Schobert C, Grosmann P, Gottschalk M, et al. (1995). Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta, 196, 205–10
   Google Scholar
• Schwan S, Fritzsche M, Cismak A, et al. (2007). In vitro investigation of the geometric contraction behavior of chemo-mechanical P-protein aggregates [forisomes]. Biophys Chem, 125, 444–52
   PubMed Web of Science ®Google Scholar
• Shahinpoor M. (2003). Ionic polymer-conductor composites as biomimetic sensors, robotic actuators and artificial muscles – a review. Electrochim Acta, 48, 2343–53
   Web of Science ®Google Scholar
• Shoureshi RA, Shen AQ. (2007). Design of a biomimetic-based monitoring and diagnostic system for civil structures. Int J Nanotechol, 4, 309–24
   Google Scholar
• Sjolund RD. (1997). The phloem sieve element: a river runs through it. Plant Cell, 9, 1137–46
   PubMed Web of Science ®Google Scholar
• Smith LM, Sabnis DD, Johnson RPC. (1987). Immunocytochemical localization of phloem lectin from Cucurbita maxima using peroxidase and colloidal-gold labels. Planta, 170, 461–70
   PubMedGoogle Scholar
• Steer MW, Newcomb EH. (1969). Development and dispersal of P-protein in the phloem of Coleus blumei Benth. J Cell Sci, 4, 155–69
   PubMedGoogle Scholar
• Straβburger E. (1891). Über den Bau und die Verrichtungen der Leitungsbahnen in den Pflanzen. Histologische Beitrage 3. Jena: Gustav Fischer
   Google Scholar
• Tuteja N, Sopory SK. (2008). Chemical signaling under abiotic stress environment in plants. Plant Signal Behav, 3, 525–36
   PubMedGoogle Scholar
• Tuteja N, Tuteja R. (1996). DNA helicases: the long unwinding road. Nat Genet, 13, 11–12
   PubMed Web of Science ®Google Scholar
• Tuteja N, Tuteja R. (2006). DNA helicases as molecular motors: an insight. Phys A: Statist Mech App, 372, 70–83
   Web of Science ®Google Scholar
• Tuteja N, Umate P, van Bel AJE. (2010). Forisomes: calcium-powered protein complexes with potential as ‘smart’ biomaterials. Trends Biotechnol, 28, 102–10
   PubMed Web of Science ®Google Scholar
• Tuteja N. (1997). Unraveling DNA helicases from plant cells. Plant Mol Biol, 33, 947–52
   PubMedGoogle Scholar
• Tuteja N. (2009). Integrated calcium signaling in plants. In: Baluska F, Mancuso S, eds. Signaling in plants. Berlin Heidelberg, Germany: Springer-Verlag, 29–49
   Google Scholar
• Uhlig K, Jaeger MS, Lisdat F, Duschl C. (2008). A biohybrid microfluidic valve based on forisome protein complexes. J Microelectrochem Syst, 17, 1322–8
   Google Scholar
• Van Bel AJE, Knoblauch M. (2000). Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Aust J Plant Physiol, 27, 477–87
   Google Scholar
• Van Bel AJE, Knoblauch M, Furch ACU, Hafke, J.B. (2011). (Questions)n on phloembiology. 1. Electropotential waves, Ca2+ fluxes and cellular cascades along the propagation pathway. Plant Sci, 181, 210–18
   PubMedGoogle Scholar
• Van Bel AJE. (1993). The transport phloem. Specifics of its functioning. Progress Botany, 54, 134–50
   Google Scholar
• van der Schoot C, van Bel AJE. (1989). Glass microelectrode measurements of sieve tube membrane potentials in internodes and petioles of tomato (Solanum lycopersicum L.). Protoplasma, 149, 144–54
   Google Scholar
• Walz C, Giavalisco P, Schad M, et al. (2004). Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry, 65, 1795–804
   PubMed Web of Science ®Google Scholar
• Walz C, Juenger M, Schad M, Kehr J. (2002). Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J, 31, 189–97
   PubMed Web of Science ®Google Scholar
• Wang S, Trumble WR, Liao H, et al. (1998). Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat Struct Biol, 5, 476–83
   PubMedGoogle Scholar
• Wergin WP, Newcomb EH. (1970). Formation and dispersal of crystalline P-protein in sieve elements of soybean (Glycine max L.). Protoplasma, 71, 365–88
   Web of Science ®Google Scholar
• Will T, Tjallingii WF, Thönnessen A, van Bel AJE. (2007). Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA, 104, 10536–41
   PubMed Web of Science ®Google Scholar
• Will T, van Bel AJE. (2006). Physical and chemical interactions between aphids and plants. J Exp Bot, 57, 729–37
   PubMed Web of Science ®Google Scholar
• Zhang Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40--8
   PubMed Web of Science ®Google Scholar
• Zimmermann MR, Hafke JB, van Bel AJ, Furch AC. (2013). Interaction of xylem and phloem during exudation and wound occlusion in Cucurbita maxima. Plant Cell Environ, 36, 237–47
   Google Scholar