Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways

Journal of Experimental Botany

Volumn 58, Issue 7, 2007, Pages 1591-1601

  Hofmann, Julia ^a   Wieczorek, Krzysztof ^a   Blöchl, Andreas ^b   Grundler, Florian M W ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

AtSUC2; AtSUC4; Heterodera schachtii; Nematode; Plasmodesmata; Sucrose transporter

Indexed keywords

BIOASSAY; GENES; PATHOGENS; PLANTS (BOTANY); SUGAR (SUCROSE); TISSUE;

HETERODERA SCHACHTII; PLASMODESMATA; SUCROSE TRANSPORTER;

BIODIVERSITY;

HETERODERA SCHACHTII;

ARABIDOPSIS PROTEIN; BETA GLUCURONIDASE; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; SUCROSE; SUCROSE TRANSPORT PROTEIN, PLANT; SUT4 PROTEIN, ARABIDOPSIS; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANIMAL; ARABIDOPSIS; ARTICLE; CYTOLOGY; DRUG ANTAGONISM; FEMALE; GENE SILENCING; GENETICS; GIANT CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEMATODE; PARASITOLOGY; PHLOEM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FEMALE; GENE SILENCING; GIANT CELLS; GLUCURONIDASE; GREEN FLUORESCENT PROTEINS; MEMBRANE TRANSPORT PROTEINS; NEMATODA; PHLOEM; PLANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUCROSE;

EID: 34547480956     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erl285     Document Type: Article

References (56)

1. Aldape MJ, Elmer AM, Chao WS, Grimesa HD. 2003. Identification and characterization of a sucrose transporter isolated from the developing cotyledons of soybean. Archives of Biochemistry and Biophysics 409, 243-250.
2. André A, Maucourt M, Moing A, Rolin D, Renaudin J. 2005. Sugar import and phytopathogenicity of Spiroplasma citri: glucose and fructose play distinct roles. Molecular Plant-Microbe Interaction 18, 33-42.
3. Barker L, Kühn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB. 2000. SUT2, a putative sucrose sensor in sieve elements. The Plant Cell 12, 1153-1164.
4. Böckenhoff A. 1995. Untersuchungen zur Physiologie der Nährstoffversorgung des Rübenzystennematoden Heterodera schachtii und der von ihm induzierten Nährzellen in Wurzeln von Arabidopsis thaliana unter Verwendung einer speziell adaptierten in situ Mikroinjektionstechnik. PhD thesis, University of Kiel, Germany.
5. Böckenhoff A, Grundler FMW. 1994. Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology 109, 249-254.
6. Böckenhoff A, Prior DAM, Grundler FMW, Oparka KJ. 1996. Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiology 112, 1421-1427.
7. de Almeida Engler J, Van Pouke K, Karim M, De Groodt R, Gheysen G, Engler G, Gheysen G. 2004. Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. The Plant Journal 38, 12-26.
8. Delrot S, Atanassova R, Maurousset L. 2000. Regulation of sugar, amino acid and peptide plant membrane transporters. Biochimica et Biophysica Acta 1465, 281-306.
9. Dorhout R, Gommers FJ, Kollöffel C. 1993. Phloem transport of carboxyfluorescein through tomato roots infected with Meloidogyne incognita. Physiological and Molecular Plant Pathology 43, 1-10.
10. Erwee MG, Goodwin PB. 1985. Symplast domains in extrastelar tissues of Egeria densa Planch. Planta 163, 9-19.
11. Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C. 2003. Induction of the Hahsp17.7g4 promoter by rootknot nematodes: involvment of heat-shock elements in promoter activity in giant cells. Molecular Plant-Microbe Interaction 16, 1062-1068.
12. Favery B, Chelysheva LA, Lebris M, Jammes F, Marmagne A, de Almeida-Engler J, Lecomte P, Vaury C, Arkowitz RA, Abad P. 2004. Arabidopsis formin AtFH6 is a plasma membrane-associated protein up-regulated in giant cells induced by parasitic nematodes. The Plant Cell 16, 2529-2540.
13. Flemetakis E, Dimou M, Cotzur D, Efrose RC, Aivalakis G, Colebatch G, Udvardi MK, Katinakis P. 2003. A sucrose transporter, LjSUT4, is up-regulated during Lotus japonicus nodule development. Journal of Experimental Botany 54, 1789-1791.
14. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE. 2003. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, at{beta}fruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiology 132, 821-829.
15. + symporter from Plantago major L. supports the model of apoplast phloem loading. The Plant Journal 6, 697-706.
16. Gal TZ, Aussenberg ER, Burdman S, Kapulnik Y, Koltai H. 2006. Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 224, 155-162.
17. García-Rodríguez S, Pozo MJ, Azcón-Aguilar C, Ferrol N. 2005. Expression of a tomato sugar transporter is increased in leaves of mycorrhizal or Phytophthora parasitica-infected plants. Mycorrhiza 15, 489-496.
18. Gisel A, Barella S, Hempel FD, Zambryski PC. 1999. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126, 1879-1889.
19. Golinowski W, Grundler FMW, Sobczak M. 1996. Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194, 103-116.
20. Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR. 2000. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proceedings of the National Academy of Sciences, USA 97, 13979-13984.
21. Grundler FMW, Sobczak M, Golinowski W. 1998. Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. European Journal of Plant Pathology 104, 545-551.
22. Hammes UZ, Schachtman DP, Berg RH, Nielsen E, Koch W, McIntyre LM, Taylor CG. 2005. Nematode-induced changes of transporter gene expression in Arabidopsis roots. Molecular Plant-Microbe Interaction 18, 1247-1257.
23. Haritatos E, Medville R, Turgeon R. 2000. Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211, 105-111.
24. Heinen P. 2001. Charakterisierung des nematodenresponsiven Gens und Promoters pyk20 in Arabidopsis thaliana und Untersuchung des Potentials zur Entwicklung von Nematodenresistenz. PhD thesis, Agrar- und Ernährungswissenschaftlichen Fakultät, Christian-Albrecht Universität, Germany.
25. Hofmann J, Grundler FMW. 2006. Females and males of root-parasitic cyst nematodes induce different symplasmic connections between their syncytial feeding cells and the phloem in Arabidopsis thaliana. Plant Physiology and Biochemistry 44, 430-433.
26. Hoth S, Schneidereit A, Lauterbach C, Scholz-Starke J, Sauer N. 2005. Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiology 138, 383-392.
27. Juergensen K. 2001. Untersuchungen zum Assimilat- und Wassertransfer in der Interaktion zwischen Arabidopsis thaliana and Heterodera schachtii. PhD thesis, Agrar- und Ernä hrungswissenschaftlichen Fakultät, Christian-Albrecht Universität, Germany.
28. Juergensen K, Scholz-Starke J, Sauer N, Hess P, van Bel AJE, Grundler FMW. 2003. The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia. Plant Physiology 131, 1-9.
29. Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC. 2002. Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 129, 1261-1271.
30. Knop C, Stadler R, Sauer N, Lohaus G. 2004. AmSUT1, a sucrose transporter in collection and transport phloem of the putative symplastic phloem loader Alonsoa meridionalis. Plant Physiology 134, 204-214.
31. Koltai H, Bird DM. 2000. High throughput cellular localization of specific plant mRNAs by liquid-phase in situ reverse transcription- polymerase chain reaction of tissue sections. Plant Physiology 123, 1203-1212.
32. Koltai H, Dhandaydham M, Opperman C, Thomas J, Bird D. 2001. Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Molecular Plant-Microbe Interaction 14, 1168-1177.
33. Kühn C. 2003. A comparison of the sucrose transporter systems of different plant species. Plant Biology 5, 215-232.
34. Kühn C, Hajirezaei MR, Fernie AR, Roessner-Turnali U, Czechowski T, Hirner B, Frommer WB. 2003. The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiology 131, 102-113.
35. Lee Y-H, Tegeder M. 2004. Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. The Plant Journal 40, 60-74.
36. -ΔΔCt method. Methods 25, 402-408.
37. Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ. 2004. Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection. Molecular Plant Pathology 5, 409-423.
38. Mølhøj M, Verma R, Reiter W-D. 2004. The biosynthesis of D-galacturonate in plants: functional cloning and characterization of a membrane-anchored UDP-D-glucuronate 4-epimerase from Arabidopsis. Plant Physiology 135, 1221-1230.
39. Niebel A, Almeida-Engler J, Hemerly A, Ferreira P, Inzé D, van Montagu M, Gheysen G. 1996. Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. The Plant Journal 10, 1037-1043.
40. Noiraud N, Delrot S, Lemoine R. 2000. The sucrose transporter of celery: identification and expression during salt stress. Plant Physiology 122, 1447-1455.
41. Patrick JW. 1990. Sieve element unloading: cellular pathway, mechanism and control. Physiologia Plantarum 78, 298-308.
42. Puthoff DP, Nettleton D, Rodermel SR, Baum TJ. 2003. Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analysis of microarray expression profiles. The Plant Journal 33, 911-921.
43. Rinne PL, Van der Schoot C. 1998. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125, 1477-1485.
44. Ruan Y-L, Xu S-M, White R, Furbank RT. 2004. Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiology 136, 4104-4113.
45. Scholz-Starke J. 2002. Die Rolle pflanzlicher Zuckertransportproteine beim Assimilattransfer in das Nährzellensystem von Heterodera schachtii. PhD thesis, University Erlangen-Nuremberg, Germany.
46. Sijmons PC, Grundler FMW, von Mende S, Burrows PR, Wyss U. 1991. Arabidopsis thaliana as a new model host for plant parasitic nematodes. The Plant Journal 1, 245-254.
47. Stadler R, Brandner J, Schulz A, Gahrtz M, Sauer N. 1995. Phloem loading by PmSUC2 sucrose carrier from Plantago major occurs into companion cells. The Plant Cell 7, 1545-1554.
48. Stadler R, Sauer N. 1996. The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Botanica Acta 109, 299-306.
49. + symporter gene directs expression of β-glucuronidase to the phloem: evidence of phloem loading and unloading by SUC2. Planta 196, 564-570.
50. Truernit E, Schmid J, Epple P, Illig J, Sauer N. 1996. The sink-specific and stress-regulated arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. The Plant Cell 8, 2169-2182.
51. Urbanczyk-Wochniak E, Filipecki M, Przybecki Z. 2002. A useful protocol for in situ RT-PCR on plant tissues. Cellular and Molecular Biology Letters 7, 7-18.
52. Weber H, Borisjuk L, Heim U, Buchner P, Wobus U. 1995. Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. The Plant Cell 7, 1835-1846.
53. Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB, Ward JM. 2000. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. The Plant Cell 12, 1345-1355.
54. Wieczorek K, Golecki B, Gerdes L, et al. 2006. Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. The Plant Journal 48, 98-112.
55. Wright K, Oparka K. 1997. Metabolic inhibitors induce symplastic movement of solutes from the transport phloem of Arabidopsis roots. Journal of Experimental Botany 48, 1807-1814.
56. Wyss U, Grundler FMW, Münch A. 1992. The parasitic behaviour of second-stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica 38, 98-111.