Sieve element occlusion (SEO) genes encode structural phloem proteins involved in wound sealing of the phloem

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 28, 2012, Pages

  Ernst, Antonia M ^a   Jekat, Stephan B ^a   Zielonka, Sascia ^a   Müller, Boje ^a   Neumann, Ulla ^b   Rüping, Boris ^c   Twyman, Richard M ^d   Krzyzanek, Vladislav ^c,e   Prüfer, Dirk ^a,c   Noll, Gundula A ^c  

^a FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF WARWICK   (United Kingdom)

^e INSTITUTE OF SCIENTIFIC INSTRUMENTS   (Czech Republic)

Author keywords

Exudation; Phloem protein 1; Photoassimilate transport; Wound response

Indexed keywords

GLYCINE DEHYDROGENASE (DECARBOXYLATING); GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ARTICLE; BLEEDING; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; PHLOEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA INTERFERENCE; SIEVE ELEMENT OCCLUSION GENE; SIEVE TUBE; SQUASH; TOBACCO; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WOUND HEALING; WOUND SEALING;

AMINO ACID SEQUENCE; CUCURBITA; EVOLUTION, MOLECULAR; FABACEAE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; LIGHT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; PHLOEM; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; TOBACCO;

CUCURBITA MAXIMA; FABACEAE; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM;

EID: 84863904778     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1202999109     Document Type: Article

References (69)

1. Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10:35-50. (Pubitemid 28309813)
2. Will T, van Bel AJE (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57:729-737.
3. Cronshaw J (1981) Phloem structure and function. Annu Rev Plant Physiol 32:465-484.
4. Sjölund RD (1997) The phloem sieve element: A river runs through it. Plant Cell 9: 1137-1146.
5. Cronshaw J, Esau K (1967) Tubular and fibrillar components of mature and differentiating sieve elements. J Cell Biol 34:801-815.
6. Esau K, Cronshaw J (1967) Tubular components in cells of healthy and tobacco mosaic virus-infected Nicotiana. Virology 33:26-35.
7. Cronshaw J, Esau K (1968) P protein in the phloem of Cucurbita. I. The development of P-protein bodies. J Cell Biol 38:25-39.
8. Cronshaw J, Esau K (1968) P protein in the phloem of Cucurbita. II. The P protein of mature sieve elements. J Cell Biol 38:292-303.
9. Steer MW, Newcomb EH (1969) Development and dispersal of P-protein in the phloem of Coleus blumei Benth. J Cell Sci 4:155-169.
10. Wooding FBP (1969) P Protein and microtubular systems in Nicotiana callus phloem. Planta 85:284-298.
11. Evert RF, Eschrich W, Eichhorn SE (1973) P-protein distribution in mature sieve elements of Cucurbita maxima. Planta 109:193-210.
12. Sabnis DD, Hart JW (1973) P-protein in sieve elements. I. Ultrastructure after treatment with vinblastine and colchicine. Planta 109:127-133.
13. Behnke H-D, Schulz A (1980) Fine structure, pattern of division, and course of wound phloem in Coleus blumei. Planta 150:357-365.
14. Wu J-L, Hao B-Z (1990) Ultrastructure of P-protein in Hevea brasiliensis during sievetube development and after wounding. Protoplasma 153:186-192.
15. Read SM, Northcote DH (1983) Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin). Eur J Biochem 134:561-569.
16. Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61: 3697-3708.
17. Anderson R, Cronshaw J (1970) Sieve-plate pores in Tobacco and Bean. Planta 91: 173-180.
18. Beyenbach J, Weber C, Kleinig H (1974) Sieve-tube proteins from Cucurbita maxima. Planta 119:113-124.
19. Clark AM, 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. (Pubitemid 27312764)
20. Golecki B, Schulz A, Thompson GA (1999) Translocation of structural P proteins in the phloem. Plant Cell 11:127-140.
21. Lin M-K, Lee Y-J, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8:343-356.
22. Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O (2010) Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. Proc Natl Acad Sci USA 107:13532-13537.
23. Noll GA (2005) Molekularbiologische Charakterisierung der Forisome. Dissertation (Justus-Liebig Universität, Gießen Germany).
24. Noll GA, et al. (2007) Spatial and temporal regulation of the forisome gene for1 in the phloem during plant development. Plant Mol Biol 65:285-294. (Pubitemid 47414560)
25. Noll GA, et al. (2011) Characteristics of artificial forisomes from plants and yeast. Bioeng Bugs 2:111-114.
26. Pélissier HC, Peters WS, Collier R, van Bel AJE, Knoblauch M (2008) GFP tagging of sieve element occlusion (SEO) proteins results in green fluorescent forisomes. Plant Cell Physiol 49:1699-1710.
27. Müller B, et al. (2010) Recombinant artificial forisomes provide ample quantities of smart biomaterials for use in technical devices. Appl Microbiol Biotechnol 88:689-698.
28. Rüping B, 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.
29. Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13:1221-1230. (Pubitemid 32480653)
30. Knoblauch M, et al. (2003) ATP-independent contractile proteins from plants. Nat Mater 2:600-603.
31. Noll GA, et al. (2009) The promoters of forisome genes MtSEO2 and MtSEO3 direct gene expression to immature sieve elements in Medicago truncatula and Nicotiana tabacum. Plant Mol Biol Rep 27:526-533.
32. Bucsenez M, 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 (Stuttg), 10.1111/j.1438-8677.2011.00556.x.
33. Sabnis DD, Sabnis HM (1995) The Cambial Derivatives, ed Iqbal M (Borntraeger, Berlin), pp 271-292.
34. Noll GA, et al. (2011) Native and artificial forisomes: Functions and applications. Appl Microbiol Biotechnol 89:1675-1682.
35. Ernst AM, et al. (2011) The sieve element occlusion gene family in dicotyledonous plants. Plant Signal Behav 6:151-153.
36. Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40(1):119-138.
37. Evert RF (1977) Phloem structure and histochemistry. Annu Rev Plant Physiol 28(1): 199-222.
38. Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309-322.
39. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949-956. (Pubitemid 36339384)
40. King RW, Zeevaart JAD (1974) Enhancement of Phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96-103.
41. Costello LR, Bassham JA, Calvin M (1982) Enhancement of phloem exudation from Fraxinus uhdei Wenz. (Evergreen Ash) using ethylenediaminetetraacetic acid. Plant Physiol 69:77-82.
42. Evert RF, Derr WF (1964) Callose substance in sieve elements. Am J Bot 51:552-559. 43. van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125-149.
43. Mullendore DL, Windt CW, Van As H, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579-593.
44. Batailler B, et al. (2012) Soluble and filamentous proteins in Arabidopsis sieve elements. Plant Cell Environ 35:1258-1273.
45. Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309-2317.
46. 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.
47. 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.
48. Hartig T (1854) Ueber die Querscheidewaende zwischen den einzelnen Gliedern der Siebröhren in Cucurbita pepo. Botanische Zeitung 12:51-54.
49. Froelich DR, et al. (2011) Phloem ultrastructure and pressure flow: Sieve-Element- Occlusion-Related agglomerations do not affect translocation. Plant Cell 23: 4428-4445.
50. Kleinig H, Thönes J, Dörr I, Kollmann R (1975) Filament formation in vitro of a sieve tube protein from Cucurbita maxima and Cucurbita pepo. Planta 127:163-170.
51. Eschrich W, Evert RF, HeyserW (1971) Proteins of the sieve-tube exudate of Cucurbita maxima. Planta 100:208-221.
52. Nuske J, Eschrich W (1976) Synthesis of P-protein in mature phloem of Cucurbita maxima. Planta 132:109-118.
53. Walker TS, Thaine R (1971) Proteins and fine structural components in exudate from sieve tubes in Cucurbita pepo stems. Ann Bot (Lond) 35:773-790.
54. 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 86:1089-1094.
55. Schwan S, Fritzsche M, Cismak A, Heilmann A, Spohn U (2007) In vitro investigation of the geometric contraction behavior of chemo-mechanical P-protein aggregates (forisomes). Biophys Chem 125:444-452. (Pubitemid 46123777)
56. Knoblauch M, Peters WS (2004) Forisomes, a novel type of Ca(2+)-dependent contractile protein motor. Cell Motil Cytoskeleton 58:137-142. (Pubitemid 38849952)
57. Wergin WP, Newcomb EH (1970) Formation and dispersal of crystalline P-Protein in sieve elements of soybean (Glycine max L.). Protoplasma 71:365-388.
58. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410.
59. Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol Genet Genomics 283:233-241.
60. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179-180. (Pubitemid 13081082)
61. Horsch RB, et al. (1986) Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs. Proc Natl Acad Sci USA 83:2571-2575. (Pubitemid 16026924)
62. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473-497.
63. Jefferson RA (1987) Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol Biol Rep 5:387-405.
64. Felts K, et al. (2000) Recombinant Renilla reniformis GFP displays low toxicity. Strategies 13(3):85-87.
65. Collier R, Fuchs B, Walter N, Kevin Lutke W, Taylor CG (2005) Ex vitro composite plants: An inexpensive, rapid method for root biology. Plant J 43:449-457. (Pubitemid 41577011)
66. Thompson MV, Wolniak SM (2008) A plasma membrane-anchored fluorescent protein fusion illuminates sieve element plasma membranes in Arabidopsis and tobacco. Plant Physiol 146:1599-1610. (Pubitemid 352844061)
67. Hawes C, Satiat-Jeunemaitre B (2001) Plant cell biology: a practical approach, eds Hawes C, Satiat-Jeunemaitre B (Oxford Univ Press, Oxford, UK), pp 235-266.
68. Moran DT, Rowley JC (1987) Correlative Microscopy in Biology: Instrumentation and Methods, ed Hayat MA (Academic, New York), pp 1-22.
69. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.