Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches

Annals of Botany

Volumn 108, Issue 3, 2011, Pages 459-469

  Cannesan, Marc Antoine ^a   Gangneux, Christophe ^b   Lanoue, Arnaud ^c   Giron, David ^d   Laval, Karine ^b   Hawes, Martha ^e   Driouich, Azeddine ^a   Vicré Gibouin, Maïté ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b Laboratoire BioSol   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d UNIVERSITÉ DE TOURS   (France)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

Aphanomyces euteiches; pathogen; phenolics; pisatin; Pisum sativum; root border cells; root cap; root infection

Indexed keywords

PHENOL DERIVATIVE;

CROP ROTATION; DISEASE CONTROL; FLOW CYTOMETRY; INFECTIOUS DISEASE; INTEGRATED PEST MANAGEMENT; LEGUME; LIQUID CHROMATOGRAPHY; MORPHOLOGY; PHENOLIC COMPOUND; QUANTITATIVE ANALYSIS; ROOT ROT; ROOT SYSTEM; SECONDARY METABOLITE;

APHANOMYCES; ARTICLE; FLOW CYTOMETRY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PEA; PHYSIOLOGY; PLANT DISEASE; PLANT ROOT CAP;

APHANOMYCES; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; PEAS; PHENOLS; PLANT DISEASES; PLANT ROOT CAP;

APHANOMYCES EUTEICHES; PISUM SATIVUM;

EID: 80052006829     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr177     Document Type: Article

References (53)

1. Badreddine I, Lafitte C, Heux L, et al. 2008. Cell wall chitosaccharides are essential components and exposed patterns of the phytopathogenic oomycete Aphanomyces euteiches. Eukaryotic Cell 7: 1980-1993
2. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF. 2000. A kingdomlevel phylogeny of eukaryotes based on combined protein data. Science 290: 972-977.
3. Baluska F, Volkmann D, Barlow PW. 1996. Specialized zones of development in roots: View from the cellular level. Plant Physiology 112: 3-4.
4. Bødker L, Kjøller R, Kristensen K, Rosendahl S. 2002. Interactions between indigenous arbuscular mycorrhizal fungi and Aphanomyces euteiches in field-grown pea. Mycorrrhiza 12: 7-12.
5. Brigham LA, Woo HH, Nicoll SM, Hawes MC. 1995. Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiology 109: 457-463.
6. Brigham LA, Woo HH, Wen F, Hawes MC. 1998. Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals. Plant Physiology 118: 1223-1231.
7. Bruehl GW. 1986. Soilborne plant pathogens. New York, NY: Macmillan Publishing Company.
8. Cruickshank IAM, Perrin DR. 1960. Isolation of a phytoalexin from Pisum sativum L. Nature 187: 799-800.
9. Cunningham JL, Hagedorn DJ. 1962. Attraction of Aphanomyces euteiches zoospores to pea and other plant roots. Phytopathology 52: 616-619.
10. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes M. 2010. Transient exposure of root tips to primary and secondary metabolites: Impact on root growth and production of border cells. Plant and Soil 332: 267-275.
11. Deacon JW, Saxena G. 1998. Germination triggers of zoospore cysts of Aphanomyces euteiches and Phytophthora parasitica. Mycological Research 102: 33-41.
12. Driouich A, Zhang GF, Staehelin LA. 1993. Effect of brefeldin A on the structure of the Golgi apparatus and on the synthesis and secretion of proteins and polysaccharides in sycamore maple (Acer pseudoplatanus) suspension-cultured cells. Plant Physiology 101: 1363-1373.
13. Driouich A, Durand C, Vicré-Gibouin M. 2007. Formation and separation of root border cells. Trends in Plant Science 12: 14-19.
14. Driouich A, Durand C, Cannesan MA, Percoco G, Vicré-Gibouin M. 2010. Border cells versus border-like cells: Are they alike? Journal of Experimental Botany 61: 3827-3831.
15. Durand C, Vicré-Gibouin M, Follet-Gueye ML, et al. 2009. The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiology 150: 1411-1421.
16. Foster RC, Rovira AD, Cock TW. 1983. Ultrastructure of the root-soil interface. St Paul, MN: American Phytopathological Society.
17. Gaulin E, Dramé N, Lafitte C, et al. 2006. Cellulose binding domains of Phytophtora cell wall protein are novel pathogen-associated molecular patterns. The Plant Cell 18: 1766-1777.
18. Gaulin E, Jacquet C, Bottin A, Dumas B. 2007. Root rot disease of legumes caused by Aphanomyces euteiches. Molecular Plant Pathology 8: 539-549.
19. Grau CR, Muehlchen AM, Tofte JE. 1991. Variability in virulence of Aphanomyces euteiches. Plant Disease 75: 1153-1156.
20. Gunawardena U, Hawes MC. 2002. Tissue specific localization of root infection by fungal pathogens: Role of root border cells. Molecular Plant- Microbe Interactions 15: 1128-1136.
21. Gunawardena U, Rodriguez M, Straney D, Romeo JT, Van Etten HD, Hawes MC. 2005. Tissue-specific localization of pea root infection by Nectria haematococca: Mechanisms and consequences. Plant Physiology 137: 1363-1374.
22. Hardham AR. 2007. Cell biology of plant-oomycete interactions. Cellular Microbiology 9: 31-39.
23. Hawes MC, Gunawardena U, Miyasaka S, Zhao X. 2000. The role of root border cells in plant defense. Trends in Plant Science 5: 128-133.
24. Hawes MC, Bengough G, Cassab G, Ponce G. 2003. Root caps and rhizosphere. Journal of Plant Growth Regulation 21: 352-367.
25. Hawes MC, Curlango-RiveraG,Wen F, White GJ, Van Etten HD, Xiong Z. 2011. Extracelluar DNA: The tip of root defenses. Plant Science 180:741-745.
26. Kaimoyo E, Van Etten HD. 2008. Inactivation of pea genes by RNAi supports the involvement of two similar O-methyltransferases in the biosynthesis of (+)-pisatin and of chiral intermediates with a configuration opposite that found in (+)-pisatin. Phytochemistry 69: 76-87.
27. Kjøller R, Rosendahl S. 1998. Enzymatic activity of the mycelium compared with oospore development during infection of pea roots by Aphanomyces euteiches. Phytopathology 88: 992-996.
28. Kraft JM, Boge WL. 1996. Identification of characteristics associated with resistance to root rot disease caused by Aphanomyces euteiches in pea. Plant Disease 80: 1383-1386.
29. Lagopodi AL, Ram AFJ, Lamers GEM, et al. 2002. Novel aspects of tomato root colonization and infection by Fusarium oxysporum f. sp. radicislycopersici revealed by confocal laser scanning microscopic analysis using the green fluorescent protein as a marker. Molecular Plant- Microbe Interactions 15: 172-179.
30. Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse USR. 2010. De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytologist 185: 577-588
31. Madoui MA, Bertrand-Michel J, Gaulin E, Dumas B. 2009. Sterol metabolism in the oomycete Aphanomyces euteiches, a legume root pathogen. New Phytologist 183: 291-300.
32. Medina E. 2009. Neutrophil extracellular traps: A strategic tactic to defeat pathogens with potential consequences for the host. Journal of Innate Immunity 1: 176-180.
33. Olivain C, Alabouvette C. 1999. Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f. sp. lycopersici in comparison with a non-pathogenic strain. New Phytologist 141: 497-510.
34. Papavizas GC, Ayers WA. 1974. Aphanomyces species and their root diseases on pea and sugarbeet: A review. USDA Technical Bulletin No. 1485, 1-159.
35. Pueppke SG, Van Etten HD. 1976. The relation between pisatin and the development of Aphanomyces euteiches in diseased Pisum sativum. Phytopathology 66: 1174-1185.
36. Rovira AD, Campbell R. 1974. Scanning electron microscopy of microorganisms on roots of wheat. Microbial Ecology 1: 15-23.
37. Sauvage H, Moussart A, Bois F, Tivoli B, Barray S, Laval K. 2007. Development of a molecular method to detect and quantify Aphanomyces euteiches in soil. FEMS Microbiology Letters 273: 64-69.
38. Shang H, Grau CR, Peters RD. 2000. Oospore germination of Aphanomyces euteiches in root exudates and on the rhizoplanes of crop plants. Plant Disease 84: 994-999.
39. Staehelin LA, Giddings TH, Kiss JZ, Sack FD. 1990. Macromolecular differentiation of Golgi stacks in root tips of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze substituted samples. Protoplasma 157: 75-91.
40. Sweigard JA, Matthews DE, Van Etten HD. 1986. Synthesis of the phytoalexin pisatin by a methyltransferase from pea. Plant Physiology 80: 277-279.
41. Turlier M, Eparvier A, Alabouvette C. 1994. Early dynamic interactions between Fusarium oxysporum f. sp. lini and the roots of Linum usilatissimum as revealed by transgenic GUS-marked hyphae. Canadian Journal of Botany 72: 1605-1612.
42. Tyler BM. 2002. Molecular basis of recognition between Phytophtora pathogens and their hosts. Annual Review of Phytopathology 40: 137-167.
43. Vandemark G, Kraft JM, Larsen R, Gritsenko M, Boge W. 2000. A PCR based assay by sequence-characterized DNA markers for the identification and detection of Aphanomyces euteiches. Phytopathology 90: 1137-1144.
44. Vicré M, Santaella C, Blanchet S, Gateau A, Driouich A. 2005. Root border-like cells of Arabidopsis: Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiology 138: 998-1009.
45. Wartha F, Beiter K, Normark S, Henriques-Normark B. 2007. Neutrophil extracellular traps: Casting the NET over pathogenesis. Current Opinion in Microbiology 10: 52-56.
46. Weir IE, Maddumage R, Allan AC, Ferguson IB. 2005. Flow cytometric analysis of tracheary element differentiation in Zinnia elegans cells. Cytometry 68: 81-91.
47. Wen F, Van Etten HD, Tsaprailis G, Hawes MC. 2007. Extracellular proteins in pea root tip and border-cell exudates. Plant Physiology 143: 773-783.
48. Wen F, White GJ, Van Etten HD, Xiong Z, Hawes MC. 2009. Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiology 151: 820-829.
49. Wicker E, Hullé M, Rouxel F. 2001. Pathogenic characteristics of isolates of Aphanomyces euteiches recovered from pea in France. Plant Pathology 50: 433-442.
50. Wicker E, Moussart A, Duparque M, Rouxel F. 2003. Further contributions to the development of a differential set of pea cultivars (Pea sativum) to investigate the virulence of isolates of Aphanomyces euteiches. European Journal of Plant Pathology 109: 47-60.
51. Wu Q, Van Etten HD. 2004. Introduction of plant and fungal genes into pea (Pisum sativum L.) hairy roots reduces their ability to produce pisatin and affects their responses to a fungal pathogen. Molecular Plant-Microbe Interactions 17: 798-804.
52. Wuyts N, Maung ZTZ, Swennen R, Waele DD. 2006. Banana rhizodeposition: Characterization of root border cell production and effects on chemotaxis and motility of the parasitic nematode Radopholus similis. Plant and Soil 283: 217-228
53. Yokosava R, Kuninaga S, Sekizaki H. 1986. Aphanomyces euteiches zoospore attractant isolated from pea root: Prunetin. Annals of Phytopathological Society of Japan 52: 809-816