Effects on plant growth and root-knot nematode infection of an endophytic GFP transformant of the nematophagous fungus Pochonia chlamydosporia

Symbiosis

Volumn 57, Issue 1, 2012, Pages 33-42

  Escudero, N ^a   Lopez Llorca, L V ^a  

^a UNIVERSITY OF ALICANTE   (Spain)

Author keywords

Biological control; Fungal egg parasites; Plant growth promotion; Root endophytes; Root knot nematodes; Tomato

Indexed keywords

BIOCONTROL AGENT; BIOLOGICAL CONTROL; ENDOPHYTE; FRUIT; FUNGUS; GROWTH RATE; INOCULATION; JUVENILE; NEMATODE; PLANT DEFENSE; ROOT COLONIZATION; ROOT SYSTEM; VIRULENCE;

FUNGI; HORDEUM; LYCOPERSICON ESCULENTUM; MELOIDOGYNE; MELOIDOGYNE JAVANICA; POCHONIA CHLAMYDOSPORIA;

EID: 84865513147     PISSN: 03345114     EISSN: 18787665     Source Type: Journal    
DOI: 10.1007/s13199-012-0173-3     Document Type: Article

References (53)

1. P Abad J Gouzy JM Aury P Castagnone-Sereno EGJ Danchin E Deleury L Perfus-Barbeoch V Anthouard F Artiguenave VC Blok 2008 Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita Nat biotechnol 26 8 909 915 18660804 10.1038/nbt.1482 1:CAS:528:DC%2BD1cXps1Wmtrc%3D
2. SD Atkins B Peteira IM Clark BR Kerry PR Hirsch 2009 Use of real-time quantitative PCR to investigate root and gall colonisation by co-inoculated isolates of the nematophagous fungus Pochonia chlamydosporia Ann Appl Biol 155 1 143 152 10.1111/j.1744-7348.2009.00333.x 1:CAS:528:DC%2BD1MXhtVeisb%2FO
3. DJ Bailey GL Biran BR Kerry CA Gilligan 2008 Pathozone dynamics of Meloidogyne incognita in the rhizosphere of tomato plants in the presence and absence of the nematophagous fungus, Pochonia chlamydosporia Plant Pathol 57 2 354 362 10.1111/j.1365-3059.2007.01776.x
4. L Barelli IE Padilla-Guerrero MJ Bidochka 2011 Differential expression of insect and plant specific adhesin genes, Mad1 and Mad2, in Metarhizium robertsii Fungal Biol 115 11 1174 1185 22036295 10.1016/j.funbio.2011.08.003 1:CAS:528:DC%2BC3MXhsVSkt7nF
5. Bird AF, Bird J (1991) The structure of nematodes. The egg. Academic, San Diego, pp 7-43
6. JJ Bordallo LV Lopez-Llorca HB Jansson J Salinas L Persmark L Asensio 2002 Colonization of plant roots by egg-parasitic and nematode-trapping fungi New Phytol 154 2 491 499 10.1046/j.1469-8137.2002.00399.x
7. JM Bourne BR Kerry 1999 Effect of the host plant on the efficacy of Verticillium chlamydosporium as a biological control agent of root-knot nematodes at different nematode densities and fungal application rates Soil Biol and Biochem 31 75 84 10.1016/S0038-0717(98)00107-2 1:CAS:528:DyaK1cXotVSqur0%3D
8. JM Bourne BR Kerry FAAM De Leig 1996 The importance of the host plant on the interaction between root-knot nematodes Meloidogyne spp. and the nematophagous fungus, Verticillium chlamydosporium goddard Biocontrol Sci Tech 6 4 539 548 10.1080/09583159631172
9. DW Byrd Jr T Kirkpatrick KR Barker 1983 An improved technique for clearing and staining plant tissues for detection of nematodes J Nematol 15 1 142
10. A Ciancio A Loffredo F Paradies C Turturo MF Sialer 2005 Detection of Meloidogyne incognita and Pochonia chlamydosporia by fluorogenic molecular probes EPPO Bull 35 1 157 164 10.1111/j.1365-2338.2005.00794.x
11. C Gayoso OM Ilárduya F Pomar F Merino de Caceres 2007 Assessment of real-time PCR as a method for determining the presence of Verticillium dahliae in different Solanaceae cultivars Eur J Plant Pathol 118 3 199 209 10.1007/s10658-007-9134-8 1:CAS:528:DC%2BD2sXntFGqurY%3D
12. V Hellwig A Mayer-Bartschmid H Müller G Greif G Kleymann W Zitzmann HV Tichy M Stadler 2003 Pochonins A-F, New Antiviral and Antiparasitic Resorcylic Acid Lactones from Pochonia chlamydosporia var. catenulata J Nat Prod 66 829 837 12828470 10.1021/np020556v 1:CAS:528:DC%2BD3sXkt1CksLs%3D
13. L Hidalgo-Díaz JM Bourne BK Kerry MG Rodríguez 2000 Nematophagous Verticillium spp. in soils infested with Meloidogyne spp. in Cuba: Isolation and screening Int J Pest Manage 46 4 277 284 10.1080/ 09670870050206046
14. N Hierro B Esteve-Zarzoso A González A Mas JM Guillamón 2006 Real-time quantitative PCR (QPCR) and reverse transcription-QPCR for detection and enumeration of total yeasts in wine Appl Environ Microl 72 11 7148 7145 10.1128/AEM.00388-06 1:CAS:528:DC%2BD28Xht1Gksr%2FK
15. PW Inglis FJL Aragao H Frazao BP Magalhaes MC Valadares-Inglis 2000 Biolistic co-transformation of Metarhizium anisopliae var. acridum strain CG423 with green fluorescent protein and resistance to glufosinate ammonium FEMS Microbiol Lett 191 249 254 11024271 10.1111/j.1574-6968.2000.tb09347.x 1:CAS:528:DC%2BD3cXmvFyqsr0%3D
16. Kerry B, Hidalgo-Diaz L (2004). Application of Pochonia chlamydosporia in the integrated control of root-knot nematodes on organically grown vegetable crops in Cuba. Bulletin OILB/SROP 27:123-126
17. Kerry BR, Bourne JM (2002). A manual for Research on Verticillium chlamdosporium, as Potential Biological Control Agent for Root-Knot Nematodes. Ed WPRS/SROP
18. BR Kerry DH Crump 1977 Observations on fungal parasites of females and eggs of the cereal cyst-nematode, Heterodera avenae, and other cyst nematodes Nematologica 23 193 201 10.1163/187529277X00543
19. B Khambay JM Bourne S Cameron B Kerry M Zaki 2000 A nematicidal metabolite from Verticillium chlamydosporium Pest Manag Sci 56 1098 1099 10.1002/1526-4998(200012)56:12<1098::AID-PS244>3.0.CO;2-H 1:CAS:528:DC%2BD3cXoslajurY%3D
20. TJ Kurtti NO Keyhani 2008 Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae Microbiology 154 6 1700 1709 18524924 10.1099/mic.0.2008/016667-0 1:CAS:528:DC%2BD1cXnslyrsrw%3D
21. S Lee SH Kim C Breuil 2002 The use of the green fluorescent protein as a biomarker for sapstain fungi Forest Pathol 32 3 153 161 10.1046/j.1439-0329. 2002.00277.x 1:CAS:528:DC%2BD3sXksVWrsrk%3D
22. LV Lopez-Llorca B Boag 1993 Biological properties of a red pigment produced by the nematophagous fungus Verticillium suchlasporium Nematol medit 21 143 149
23. LV Lopez-Llorca D Claugher 1990 Appressoria of the nematophagous fungus Verticillium suchlasporium Micron Microscoc Acta 21 3 125 130 10.1016/0739-6260(90)90014-7
24. LV Lopez-Llorca JM Duncan 1986 New media for the estimation of fungal infection in eggs of the cereal cyst nematode Nematologica 32 486 490 10.1163/187529286X00354
25. LV Lopez-Llorca GH Duncan 1987 A study of fungal endoparasitism of the cereal cyst nematode Heterodera avenae by scanning electron microscopy Can J Microbiol 34 613 619 10.1139/m88-101
26. LV Lopez-Llorca WM Robertson 1992 Ultrastructure of infection of cyst nematode eggs by the nematophagous fungus Verticillium Suchlasporium Nematologica 39 4 65 74
27. LV Lopez-Llorca JJ Bordallo J Salinas E Monfort ML Lopez-Serna 2002 Use of Light and scanning electron microscopy to examine colonisation of barley rhizosfere by the nematophagous fungus Verticillium chlamydosporium Micron 33 61 67 11473815 10.1016/S0968-4328(00)00070-6 1:STN:280:DC%2BD3MvislGktA%3D%3D
28. Lopez-Llorca LV, Jansson HB, Maciá-Vicente JG, Salinas J (2006) Nematophagous fungi as root endophytes. In: Microbial root endophytes, Springer-Verlag, pp 191-206
29. LV Lopez-Llorca S Gomez-Vidal E Monfort E Larriba J Casado-Vela F Elortza HB Jansson J Salinas J Martín-Nieto 2010 Expression of serine proteases in egg-parasitic nematophagous fungi during barley root colonization Fungal Genet Biol 47 4 342 351 20097301 10.1016/j.fgb.2010.01.004 1:CAS:528: DC%2BC3cXivFeltrY%3D
30. JG Maciá-Vicente HB Jansson NJ Talbot LV Lopez-Llorca 2009 Real-time PCR quantification and live-cell imaging of endophytic colonization of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia New Phytol 182 1 213 228 19170898 10.1111/j.1469-8137.2008.02743.x
31. JG Maciá-Vicente LC Rosso A Ciancio HB Jansson LV Lopez-Llorca 2009 Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: Effects on plant growth and disease Ann Appl Biol 155 3 391 401 10.1111/j.1744-7348.2009.00352.x
32. RH Manzanilla-López I Esteves SJ Powers BR Kerry 2011 Effects of crop plants on abundance of Pochonia chlamydosporia and other fungal parasites of root-knot and potato cyst nematodes Ann Appl Biol 159 1 118 129 10.1111/j.1744-7348.2011.00479.x
33. MA McClure TH Kruk I Misaghi 1973 A method for obtaining quantities of clean Meloidogyne eggs J Nematol 5 3 230 19319340 1:STN:280: DC%2BD1M3jtFKqtA%3D%3D
34. E Monfort LV Lopez-Llorca HB Jansson J Salinas JO Park K Sivasithamparam 2005 Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot Soil Biol Biochem 37 7 1229 1235 10.1016/j.soilbio.2004.11.019 1:CAS:528:DC%2BD2MXivFyqsL4%3D
35. XM Niu YL Wang YS Chu HX Xue N Li LX Wei MH Mo KQ Zhang 2010 Nematodetoxic aurovertin-type metabolites from a rook-knot nematode parasitic fungus Pochonia chlamydosporia J Agric Food Chem 58 828 834 20000774 10.1021/jf903259n 1:CAS:528:DC%2BD1MXhsFGnt7bJ
36. Nordbring-Hertz B, Jansson HB, Tunlid A (2006) Encyclopedia of life sciences. pp 1-11
37. CM Olivares-Bernabeu LV Lopez-Llorca 2002 Fungal egg-parasites of plant-parasitic nematodes from Spanish soils Rev Iberoam Micol 19 2 104 110
38. L Persmark HB Jansson 1997 Nematophagous fungi in the rhizosphere of agricultural crops FEMS Microbiol Ecol 22 4 303 312 10.1111/j.1574-6941.1997. tb00382.x 1:CAS:528:DyaK2sXjtVShtL4%3D
39. R Segers MT Butt BR Kerry A Beckett JF Peberdy 1996 The role of the proteinase VCP1 produced by the nematophagous Verticillium chlamydosporium in the infection process of nematode eggs Mycol Res 100 421 428 10.1016/S0953-7562(96)80138-9 1:CAS:528:DyaK28XjsFWnt74%3D
40. ZA Siddiqi MS Akhtar 2008 Synergistic effects of antagonistic fungi and a plant growth promoting rhizobacterium, an arbuscular mycorrhizal fungus, or composted cow manure on populations of Meloydogyne incognita and growth of tomato Biocontrol Sci Techn 18 3 207 290
41. IA Siddiqui S Ehteshamul-Haque 2000 Effect of Verticillium chlamydosporium and Pseudomonas aeruginosa in the control of Meloidogyne javanica in tomato Nematol Medit 28 193 196
42. IA Siddiqui SS Shaukat 2003 Combination of Pseudomonas aeruginosa and Pochonia chlamydosporia for Control of Root-Infecting Fungi in Tomato J Phytopathology 151 215 222 10.1046/j.1439-0434.2003.00708.x
43. RA Sikora L Pocasangre A Felde B Niere TT Vu AA Dababat 2008 Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes Biol Control 46 15 23 10.1016/j.biocontrol.2008.02.011
44. FJ Sorribas C Ornat M Galeano S Verdejo-Lucas 2003 Evaluation of a Native and Introduced Isolate of Pochonia chlamydosporia against Meloidogyne javanica Biocontrol Sci Techn 13 8 707 714 10.1080/09583150310001606282
45. Stirling GR (2011) Biological control of plant-parasitic nematodes: an ecological perspective, a review of progress and opportunities for further research. Biological Control of Plant-Parasitic Nematodes. pp 1-38
46. JD Tobin PPJ Haydock MC Hare SR Woods DH Crump 2008 Effect of the fungus Pochonia chlamydosporia and fosthiazate on the multiplication rate of potato cyst nematodes (Globodera pallida and G. rostochiensis) in potato crops grown under UK field conditions Biol Control 46 2 194 201 10.1016/j.biocontrol.2008. 03.014
47. EA Tzortzakakis SE Petsas 2003 Investigation of alternatives to methyl bromide for management of Meloidogyne javanica on greenhouse grown tomato Pest Manag Sci 59 1311 1320 14667053 10.1002/ps.764 1:CAS:528:DC%2BD3sXpsV2mu74%3D
48. V Van Damme A Hoedekie N Viaene 2005 Long-term efficacy of Pochonia chlamydosporia for management of Meloidogyne javanica in glasshouse crops Nematology 7 741 745
49. S Verdejo-Lucas FJ Sorribas M Galeno 2003 Evaluating Pochonia chlamydosporia in a double-cropping system of lettuce and tomato in plastic houses infested with Meloidogyne javanica Plant Pathol 52 521 528 10.1046/j.1365-3059.2003.00873.x
50. WML Wesemael N Viaene M Moens 2010 Root-knot nematodes (Meloidogyne spp.) in Europe Nematology 13 1 3 16 10.1163/138855410X526831
51. J Wiedenmann F Oswald GU Nienhaus 2009 Fluorescent proteins for live cell imaging: Opportunities, limitations, and challenges IUBMB Life 61 11 1029 1042 19859977 10.1002/iub.256 1:CAS:528:DC%2BD1MXhsVyrtrzJ
52. L Zhang J Yang Q Niu X Zhao F Ye L Liang KQ Zhang 2008 Investigation on the infection mechanism of the fungus Clonostachys rosea against nematodes using the green fluorescent protein Appl Microbiol Biot 78 6 983 990 10.1007/s00253-008-1392-7 1:CAS:528:DC%2BD1cXkvFagsbc%3D
53. C Zijlstra D Donkers-Venne M Fargette 2000 Identification of Meloidogyne incognita, M. javanica and M. arenaria using sequence characterised amplifed region (SCAR) based PCR assays Nematology 2 8 847 853 10.1163/156854100750112798 1:CAS:528:DC%2BD3MXjsV2qsLg%3D