The arbuscular mycorrhizal symbiosis attenuates symptom severity and reduces virus concentration in tomato infected by Tomato yellow leaf curl Sardinia virus (TYLCSV)

Mycorrhiza

Volumn 24, Issue 3, 2014, Pages 179-186

  Maffei, Giulia ^a,b   Miozzi, Laura ^b   Fiorilli, Valentina ^a,b   Novero, Mara ^a   Lanfranco, Luisa ^a,b   Accotto, Gian Paolo ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

AM symbiosis; Funneliformis mosseae; Geminivirus; Tomato; Tomato yellow leaf curl Sardinia virus; Viral infection

Indexed keywords

ARBUSCULAR MYCORRHIZA; COLONIZATION; DISEASE; DISEASE SEVERITY; DNA; PLANT; SYMBIOSIS; VIRAL DISEASE; VIRUS;

ARTICLE; BEGOMOVIRUS; GLOMEROMYCOTA; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT DISEASE; SYMBIOSIS; TOMATO; VIROLOGY;

BEGOMOVIRUS; GLOMEROMYCOTA; LYCOPERSICON ESCULENTUM; MYCORRHIZAE; PLANT DISEASES; SYMBIOSIS;

EID: 84896386527     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-013-0527-6     Document Type: Article

References (65)

1. Accotto GP, Navas-Castillo J, Noris E, Moriones E, Louro D (2000) Typing of tomato yellow leaf curl viruses in Europe. Eur J Plant Pathol 106: 179-186.
2. Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59: 2029-2041.
3. Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148: 436-454.
4. Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant Microbe Interact 20: 1055-1062.
5. Bekers GJ, Conrath U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10: 425-431.
6. Bonfante P, Anca I-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63: 363-383.
7. Conrath U, Beckers GJM, Flors V, Gracia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ et al (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19: 1062-1071.
8. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11: 1017-1028.
9. Czosnek H (2007) Tomato yellow leaf curl virus disease. Management, molecular biology, breeding for resistance. Springer, Netherlands, ISBN: 978-1-4020-4768-8.
10. D'Amelio R, Massa N, Gamalero E, D'Agostino G, Sampo S, Berta G, Faoro F et al (2007) Preliminary results on the evaluation of the effects of elicitors of plant resistance on chrysanthemum yellows phytoplasma infection. B Insectol 60: 317-318.
11. Daft MJ, Okusanya BO (1973) Effect of Endogone mycorrhiza on plant growth. V. Influence of infection on the multiplication of viruses in tomato, petunia, strawberry. New Phytol 72: 975-983.
12. de la Peña E, Echeverría SR, van der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169: 829-840.
13. Dehne HW (1982) Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72: 1115-1119.
14. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184: 975-987.
15. Fiorilli V, Catoni M, Francia D, Cardinale F, Lanfranco L (2011) The arbuscular mycorrhizal symbiosis reduces disease severity in tomato plants infected by Botrytis cinerea. J Plant Pathol 93: 237-242.
16. Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuehnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16: 413-419.
17. García-Chapa M, Batlle A, Laviña A, Camprubí A, Estaún V, Calvet C (2004) Tolerance increase to pear decline phytoplasma in mycorrhizal OHF-333 pear rootstock. Acta Hort 657: 437-441.
18. Gernns H, Von Alten H, Poehling HM (2001) Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen-is a compensation possible? Mycorrhiza 11: 237-243.
19. Gomez-Ariza J, Balestrini R, Novero M, Bonfante P (2009) Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biol Fert Soils 45: 845-853.
20. Hanssen IM, Lapidot M, Thomma BPHJ (2010) Emerging viral disease of tomato crops. Mol Plant Microbe Interact 23: 539-548.
21. Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68: 101-110.
22. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13: 264-272.
23. Herrera-Medina MJ, Steinkellner S, Vierheilig H, Bote JAO, Garrido JMG (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175: 554-564.
24. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Bureau Technical Communication 22. Farnham Royal, Bucks, UK.
25. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68: 139-146.
26. Ismail Y, Hijri M (2012) Arbuscular mycorrhization with Glomus irregulare induces expression of potato PR homologue genes in response to infection by Fusarium sambucinum. Funct Plant Biol 39: 236-245.
27. Jeske H (2009) Geminiviruses. Curr Top Microbiol Immunol 331: 185-226.
28. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38: 651-664.
29. Khaosaad T, García-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39: 727-734.
30. Kheyr-Pour A, Bendahmane M, Matzeit V, Accotto GP, Crespi S, Gronenborn B (1991) Tomato yellow leaf curl virus from Sardinia is a whitefly-transmitted monopartite geminivirus. Nucleic Acids Res 19: 6763-6769.
31. Kobra N, Jalil K, Youbert G (2009) Effects of three Glomus species as biocontrol agents against verticillium-induced wilt in cotton. J Plant Prot 49(185): 189.
32. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193: 970-984.
33. Lanfranco L, Young JPV (2012) Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr Opin Plant Biol 15: 454-461.
34. Lapidot M, Friedmann M (2002) Breeding for resistance to whitefly-transmitted geminiviruses. Ann Appl Biol 140: 109-127.
35. Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, Zheng CC (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47: 154-163.
36. Lingua G, D'Agostino G, Massa N, Antosiano M, Berta G (2002) Mycorrhiza-induced differential response to a yellows disease in tomato. Mycorrhiza 12: 191-198.
37. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50: 529-544.
38. López-Ráez JA, Verhage A, Fernández I, Garciá JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61: 2589-2601.
39. Lozano-Durán R, Rosas-Díaz T, Usmaroli G, Luna AP, Taconnat L, Deng XW, Bejarano ER (2011) Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23: 1014-1032.
40. Mansoor S, Zafar Y, Briddon RW (2006) Geminivirus disease complexes: the threat is spreading. Trends Plant Sci 11: 209-212.
41. Miozzi L, Catoni M, Fiorilli V, Philip MM, Accotto GP, Lanfranco L (2011) Arbuscular mycorrhizal symbiosis limits foliar transcriptional responses to viral infection and favors long-term virus accumulation. Mol Plant Microbe Interact 24: 1562-1572.
42. Morilla G, Krenz B, Jeske H, Bejarano ER, Wege C (2004) Tete a tete of tomato yellow leaf curl virus and tomato yellow leaf curl Sardinia virus in single nuclei. J Virol 78: 10715-10723.
43. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42: 236-250.
44. Ozgonen H, Erkilic A (2007) Growth enhancement and Phytophthora blight (Phytophthora capsici leonian) control by arbuscular mycorrhizal fungal inoculation in pepper. Crop Prot 26: 1682-1688.
45. Penninckx I, Thomma B, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113.
46. Pozo JM, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10: 393-398.
47. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53: 525-534.
48. Pozo MJ, Jung SC, Lòpez-Ràez J, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Heidelberg, pp 193-207.
49. Rasmussen R (2001) Quantification on the LightCycler instrument. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR: methods and applications. Springer, Heidelberg, pp 21-34.
50. Rosendahl S (1985) Interactions between the vesicular-arbuscular mycorrhizal fungus Glomus fasciculatum and Aphanomyces euteiches root rot of peas. J Plant Physiol 144: 31-40.
51. Salvioli A, Zouari I, Chalot M, Bonfante P (2012) The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biol 12: 1-12.
52. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defence responses in Arabidopsis revealed by microarray analysis. PNAS USA 97: 11655-11660.
53. Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant Microbe Interact 12: 1000-1007.
54. Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant Microbe Interact 13: 238-241.
55. Taylor J, Harrier LA (2003) Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Mol Biol 51: 619-629.
56. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
57. st ESM 217-221. INRA Presse, Paris.
58. Utkhede R (2006) Increased growth and yield of hydroponically grown greenhouse tomato plants inoculated with arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. Radicis-lycopersici. Biocontrol 51: 393-400.
59. van der Heijden MGA, Sanders IR (2002) Mycorrhizal ecology. Springer, Berlin.
60. Varma A, Malathi VG (2003) Emerging geminivirus problems: a serious threat to crop production. Ann Appl Biol 142: 145-164.
61. Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8: 214-217.
62. Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V (2013) Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Sol Biol Biochem 60: 45-54.
63. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82: 1198-1227.
64. Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama KG, Levy AA, Silber A (2007) Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J Exp Bot 58: 2491-2501.
65. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH (2008) βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22: 2564-2577.