Pathogenic attributes of Sclerotinia sclerotiorum: Switching from a biotrophic to necrotrophic lifestyle

Plant Science

Volumn 233, Issue , 2015, Pages 53-60

  Kabbage, Mehdi ^a   Yarden, Oded ^b   Dickman, Martin B ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Biotrophy; Damage curve; Fungal pathogens; Lifestyle designations; Necrotrophy; Sclerotinia sclerotiorum

Indexed keywords

ASCOMYCETES; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT DISEASE;

ASCOMYCOTA; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASES; PLANTS;

FUNGI; SCLEROTINIA SCLEROTIORUM;

EID: 84964308208     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2014.12.018     Document Type: Review

References (48)

1. Taylor T.N., Remy W., Hass H. Fungi from the lower devonian rhynie chert - Chytridiomycetes. Am. J. Bot. 1992, 79:1233-1241.
2. Bolton M.D., Thomma B.P., Nelson B.D. Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 2006, 7:1-16.
3. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005, 43:205-227.
4. Horbach R., Navarro-Quesada A.R., Knogge W., Deising H.B. When and how to kill a plant cell: infection strategies of plant pathogenic fungi. J. Plant Physiol. 2011, 168:51-62.
5. Lai Z., Mengiste T. Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr. Opin. Plant Biol. 2013, 16:505-512.
6. Prusky D., Alkan N., Mengiste T., Fluhr R. Quiescent and necrotrophic lifestyle choice during postharvest disease development. Annu. Rev. Phytopathol. 2013, 51:155-176.
7. Amselem J., et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011, 7:e1002230.
8. Spanu P.D., et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 2010, 330:1543-1546.
9. Zhao Z., Liu H., Wang C., Xu J.R. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2013, 14:274.
10. Rovenich H., Boshoven J.C., Thomma B.P. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr. Opin. Plant Biol. 2014, 20C:96-103.
11. Giraldo M.C., Valent B. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 2013, 11:800-814.
12. Ciuffetti L.M., Manning V.A., Pandelova I., Betts M.F., Martinez J.P. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol. 2010, 187:911-919.
13. Faris J.D., et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:13544-13549.
14. Guyon K., Balague C., Roby D., Raffaele S. Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 2014, 15:336.
15. Kabbage M., Williams B., Dickman M.B. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog. 2013, 9:e1003287.
16. Cessna S.G., Sears V.E., Dickman M.B., Low P.S. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 2000, 12:2191-2200.
17. Godoy G., Steadman J.R., Dickman M.B., Dam R. Use of mutants to demonstrate the role of oxalic-acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 1990, 37:179-191.
18. Liang X., et al. Oxaloacetate acetylhydrolase gene mutants of Sclerotinia sclerotiorum do not accumulate oxalic acid, but do produce limited lesions on host plants. Mol. Plant Pathol. 2014, 10.1111/mpp.12211.
19. Dutton M.V., Evans C.S. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 1996, 42:881-895.
20. Kim K.S., Min J.Y., Dickman M.B. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant Microbe Interact. 2008, 21:605-612.
21. Williams B., Kabbage M., Kim H.J., Britt R., Dickman M.B. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog. 2011, 7.
22. Liu Y., et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell 2005, 121:567-577.
23. Govrin E.M., Levine A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 2000, 10:751-757.
24. Shabab M., et al. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 2008, 20:1169-1183.
25. van den Burg H.A., Harrison S.J., Joosten M.H., Vervoort J., de Wit P.J. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe Interact. 2006, 19:1420-1430.
26. Mosquera G., Giraldo M.C., Khang C.H., Coughlan S., Valent B. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 2009, 21:1273-1290.
27. Marcel S., Sawers R., Oakeley E., Angliker H., Paszkowski U. Tissue-adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 2010, 22:3177-3187.
28. Vargas W.A., et al. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol. 2012, 158:1342-1358.
29. Torregrosa C., et al. Cytological, genetic, and molecular analysis to characterize compatible and incompatible interactions between Medicago truncatula and Colletotrichum trifolii. Mol. Plant Microbe Interact. 2004, 17:909-920.
30. Bhadauria V., Banniza S., Vandenberg A., Selvaraj G., Wei Y. EST mining identifies proteins putatively secreted by the anthracnose pathogen Colletotrichum truncatum. BMC Genomics 2011, 12:327.
31. O'Connell R.J., et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat. Genet. 2012, 44:1060-1065.
32. Kleemann J., et al. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog. 2012, 8:e1002643.
33. Dickman M.B., Mitra A. Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiol. Mol. Plant Pathol. 1992, 41:255-263.
34. Rollins J.A., Dickman M.B. Increase in endogenous and exogenous cyclic AMP levels inhibits sclerotial development in Sclerotinia sclerotiorum. Appl. Environ. Microbiol. 1998, 64:2539-2544.
35. Rollins J.A., Dickman M.B. pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl. Environ. Microbiol. 2001, 67:75-81.
36. Harel A., Bercovich S., Yarden O. Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol. Plant Microbe Interact. 2006, 19:682-693.
37. Erental A., Harel A., Yarden O. Type 2A phosphoprotein phosphatase is required for asexual development and pathogenesis of Sclerotinia sclerotiorum. Mol. Plant Microbe Interact. 2007, 20:944-954.
38. Erental A., Dickman M.B., Yarden O. Sclerotial development in Sclerotinia sclerotiorum: awakening molecular analysis of a "Dormant" structure. Fungal Biol. Rev. 2008, 22:6-16.
39. Djamei A., et al. Metabolic priming by a secreted fungal effector. Nature 2011, 478:395-398.
40. van der Burgt A., Jashni M.K., Bahkali A.H., de Wit P.J.G.M. Pseudogenization in pathogenic fungi with different host plants and lifestyles might reflect their evolutionary past. Mol. Plant Pathol. 2014, 15:133-144.
41. Tariq V.N., Jeffries P. Ultrastructure of penetration of Phaseolus spp. by Sclerotinia sclerotiorum. Can. J. Bot. 1986, 64:2909-2915.
42. Jamaux I., Gelie B., Lamarque C. Early stages of infection of rapeseed petals and leaves by Sclerotinia sclerotiorum revealed by scanning electron-microscopy. Plant Pathol. 1995, 44:22-30.
43. Garg H., Li H., Sivasithamparam K., Kuo J., Barbetti M.J. The infection processes of Sclerotinia sclerotiorum in cotyledon tissue of a resistant and a susceptible genotype of Brassica napus. Ann. Bot. 2010, 106:897-908.
44. Khang C.H., et al. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 2010, 22:1388-1403.
45. van Kan J.A., Shaw M.W., Grant-Downton R.T. Botrytis species: relentless necrotrophic thugs or endophytes gone rogue?. Mol. Plant Pathol. 2014, 15(9):957-961.
46. Andrew M., Barua R., Short S.M., Kohn L.M. Evidence for a common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs, biotrophs, endophytes, host generalists and specialists. PLoS ONE 2012, 7:e29943.
47. Jarosz D.F., Lancaster A.K., Brown J.C., Lindquist S. An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 2014, 158:1072-1082.
48. Casadevall A., Pirofski L.A. The damage-response framework of microbial pathogenesis. Nat. Rev. Microbiol. 2003, 1:17-24.