Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum

Autophagy

Volumn 8, Issue 3, 2012, Pages 326-337

  Josefsen, Lone ^a   Droce, Aida ^b   Sondergaard, Teis Esben ^b   Sørensen, Jens Laurids ^b   Bormann, Jörg ^c   Schäfer, Wilhelm ^c   Giese, Henriette ^b   Olsson, Stefan ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Aerial hyphae; Filamentous fungi; Lipid droplets; Lipophagy; Plant infection; Storage lipids

Indexed keywords

AUTOPHAGY PROTEIN 8; CARBON; FAT DROPLET; FUNGAL PROTEIN; NITROGEN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; BARLEY; CONIDIUM; CONTROLLED STUDY; ENERGY CONSUMPTION; FUNGAL STRAIN; FUNGAL STRUCTURES; FUNGUS GROWTH; FUSARIUM GRAMINEARUM; GENE DELETION; GENE INSERTION; LIPID STORAGE; LIPOPHAGOCYTOSIS; MAGNAPORTHE GRISEA; MYCELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT AVAILABILITY; PLANT COMMUNITY; PLANT DISEASE; PODOSPORA ANSERINA; PROTEIN CLEAVAGE; WHEAT;

FUNGI; GIBBERELLA ZEAE; HORDEUM; PODOSPORA ANSERINA; TRITICUM AESTIVUM;

EID: 84859113060     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.18705     Document Type: Article

References (45)

1. Pollack JK, Harris SD, Marten MR. Autophagy in filamentous fungi. Fungal Genet Biol 2009; 46:1-8; PMID:19010432; http://dx.doi.org/10.1016/j.fgb.2008. 10.010
2. Klionsky DJ, Emr SD. Cell biology - Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:11099404; http://dx.doi.org/10. 1126/science.290.5497.1717
3. Bursch W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 2001; 8:569-81; PMID:11536007; http://dx.doi.org/10. 1038/sj.cdd.4400852
4. Veses V, Richards A, Gow NAR. Vacuoles and fungal biology. Curr Opin Microbiol 2008; 11:503-10; PMID: 18935977; http://dx.doi.org/10.1016/j.mib.2008. 09.017
5. Farré JC, Krick R, Subramani S, Thumm M. Turnover of organelles by autophagy in yeast. Curr Opin Cell Biol 2009; 21:522-30; PMID:19515549; http://dx.doi. org/10.1016/j.ceb.2009.04.015
6. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JAKW. ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 2007; 3:106-16; PMID:17204848
7. Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 2008; 19:3290-8; PMID:18508918; http://dx.doi. org/10.1091/mbc.E07-12-1292
8. Pinan-Lucarré B, Paoletti M, Dementhon K, Coulary-Salin B, Clave C. Autophagy is induced during cell death by incompatibility and is essential for differentiation in the filamentous fungus Podospora anserina. Mol Microbiol 2003; 47:321-33; PMID:12519185; http://dx.doi.org/10.1046/j.1365-2958.2003. 03208.x
9. Nolting N, Bernhards Y, Poggeler S. SmATG7 is required for viability in the homothallic ascomycete Sordaria macrospora. Fungal Genet Biol 2009; 46:531-42; PMID:19351563; http://dx.doi.org/10.1016/j.fgb. 2009.03.008
10. Asakura M, Ninomiya S, Sugimoto M, Oku M, Yamashita S, Okuno T, et al. Atg26-Mediated Pexophagy Is Required for Host Invasion by the Plant Pathogenic Fungus Colletotrichum orbiculare. Plant Cell 2009; 21:1291-304; PMID:19363139; http://dx.doi. org/10.1105/tpc.108.060996
11. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 2006; 312: 580-3; PMID:16645096; http://dx.doi.org/10.1126/science.1124550
12. Nadal M, Gold SE. The autophagy genes ATG8 and ATG1 affect morphogenesis and pathogenicity in Ustilago maydis. Mol Plant Pathol 2010; 11:463-78; PMID:20618705; http://dx.doi.org/10.1111/j.1364-3703.2010.00620.x
13. Boenisch MJ, Schafer W. Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol 2011; 11:110; PMID:21798058; http://dx.doi.org/10.1186/1471-2229-11-110
14. Ribichich KF, Lopez SE, Vegetti AC. Histopathological spikelet changes produced by Fusarium graminearum in susceptible and resistant wheat cultivars. Plant Dis 2000; 84:794-802; http://dx.doi.org/10.1094/PDIS. 2000.84.7.794
15. Wanjiru WM, Kang ZS, Buchenauer H. Importance of cell wall degrading enzymes produced by Fusarium graminearum during infection of wheat heads. Eur J Plant Pathol 2002; 108:803-10; http://dx.doi.org/10. 1023/A:1020847216155
16. Nguyen LN, Bormann J, Le GTT, Stärkel C, Olsson S, Nosanchuk JD, et al. Autophagy-related lipase FgATG15 of Fusarium graminearum is important for lipid turnover and plant infection. Fungal Genet Biol 2011; 48:217-24; PMID:21094265; http://dx.doi.org/10.1016/j.fgb.2010.11.004
17. Jansen C, von Wettstein D, Schafer W, Kogel KH, Felk A, Maier FJ. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci USA 2005; 102:16892-7; PMID:16263921; http://dx. doi.org/10.1073/pnas.0508467102
18. Martínez-Force E, Benítez T. Effects of varying media, temperature, and growth rates on the intracellular concentrations of yeast amino acids. Biotechnol Prog 1995; 11:386-92; PMID:7654310; http://dx.doi.org/10. 1021/bp00034a004
19. Bai GH, Desjardins AE, Plattner RD. Deoxynivalenol-nonproducing fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 2002; 153:91-8; PMID: 12000132; http://dx.doi.org/10. 1023/A:1014419323550
20. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 2000; 151:263-76; PMID:11038174; http://dx.doi.org/10. 1083/jcb.151.2.263
21. Deng YZ, Ramos-Pamplona M, Naqvi NI. Methods for functional analysis of macroautophagy in filamentous fungi. Methods Enzymol 2008; 451:295-310; PMID: 19185728; http://dx.doi.org/10.1016/S0076-6879(08) 03220-5
22. Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 2007; 6:997-1005; PMID: 17416896; http://dx.doi.org/10.1128/EC.00011-07
23. Pinan-Lucarré B, Baiguerie A, Clave C. Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell 2005; 4:1765-74; PMID:16278443; http://dx.doi.org/10.1128/EC.4.11.1765-1774.2005
24. Kikuma T, Ohneda M, Arioka M, Kitamoto K. Functional analysis of the ATG8 homologue Aoatg8 and role of autophagy in differentiation and germination in Aspergillus oryzae. Eukaryot Cell 2006; 5:1328-36; PMID:16896216; http://dx.doi.org/10.1128/EC. 00024-06
25. Richie DL, Fuller KK, Fortwendel J, Miley MD, McCarthy JW, Feldmesser M, et al. Unexpected link between metal ion deficiency and autophagy in Aspergillus fumigatus. Eukaryot Cell 2007; 6:2437-47; PMID: 17921348; http://dx.doi.org/10. 1128/EC.00224-07
26. Righelato RC, Trinci APJ, Pirt SJ, Peat A. The influence of maintenance energy and growth rate on the metabolic activity, morphology and conidiation of Penicillium chrysogenum. J Gen Microbiol 1968; 50: 399-412; PMID:5652074
27. Lew RR. How does a hypha grow? The biophysics of pressurized growth in fungi. Nat Rev Microbiol 2011; 9:509-18; PMID:21643041; http://dx.doi.org/10. 1038/nrmicro2591
28. Weber RWS, Wakley GE, Thines E, Talbot NJ. The vacuole as central element of the lytic system and sink for lipid droplets in maturing appressoria of Magnaporthe grisea. Protoplasma 2001; 216:101-12; PMID:11732192; http://dx.doi.org/10.1007/BF02680137
29. Ryan FJ, Beadle GW, Tatum EL. The tube method of measuring the growth rate of Neurospora. Am J Bot 1943; 30:784-99; http://dx.doi.org/10.2307/2437554
30. Singh R, Kaushik S, Wang YJ, Xiang YQ, Novak I, Komatsu M, et al. Autophagy regulates lipid metabolism. Nature 2009; 45811315; PMID:19779424
31. Halloran GM, Lee JW. Plant Nitrogen Distribution in Wheat Cultivars. Aust J Agric Res 1979; 30:779-89; http://dx.doi.org/10.1071/AR9790779
32. Ilgen P, Maier FJ, Schäfer W. Trichothecenes and lipases are host-induced and secreted virulence factors of Fusarium graminearum. Cereal Res Commun 2008; 36:421-8; http://dx.doi.org/10.1556/CRC.36.2008. Suppl.B.35
33. Gardiner DM, Kazan K, Manners JM. Novel genes of Fusarium graminearum that negatively regulate deoxynivalenol production and virulence. Mol Plant Microbe Interact 2009; 22:1588-600; PMID:19888824; http://dx.doi.org/10.1094/ MPMI-22-12-1588
34. Gale LR, Bryant JD, Calvo S, Giese H, Katan T, O'Donnell K, et al. Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics 2005; 171:985-1001; PMID:16079234; http://dx.doi.org/10.1534/genetics.105.044842
35. Langseth W, Bernhoft A, Rundberget T, Kosiak B, Gareis M. Mycotoxin production and cytotoxicity of Fusarium strains isolated from Norwegian cereals. Mycopathologia 1998-1999; 144:103-13; PMID: 10481290; http://dx.doi.org/10. 1023/A:1007016820879
36. Malz S, Grell MN, Thrane C, Maier FJ, Rosager P, Felk A, et al. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet Biol 2005; 42:420-33; PMID:15809006; http://dx.doi.org/10.1016/j.fgb.2005.01.010
37. Frandsen RJN, Andersson JA, Kristensen MB, Giese H. Efficient four fragment cloning for the construction of vectors for targeted gene replacement in filamentous fungi. BMC Mol Biol 2008; 9:70; PMID:18673530; http://dx.doi.org/10.1186/1471-2199-9-70
38. Tobiasen C, Aahman J, Ravnholt KS, Bjerrum MJ, Grell MN, Giese H. Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 2007; 51: 43-58; PMID:17043871; http://dx.doi.org/10. 1007/s00294-006-0103-0
39. Ryan FJ, Beadle GW, Tatum EL. The tube method of measuring the growth rate of Neurospora. Am J Bot 1943; 30:784-99; http://dx.doi.org/10.2307/2437554
40. White B, Woodward D. A simple method for making disposable race tubes. Fungal Genet Newsl 1995; 42:79.
41. Klittich C, Leslie JF. Nitrate Reduction Mutants of Fusarium moniliforme (Gibberella fujikuroi). Genetics 1988; 118:417-23; PMID:17246415
42. Skov J, Lemmens M, Giese H. Role of a Fusarium culmorum ABC transporter (FcABC1) during infection of wheat and barley. Physiol Mol Plant Pathol 2004; 64:245-54; http://dx.doi.org/10.1016/j.pmpp.2004.09. 005
43. Jenczmionka NJ, Maier FJ, Losch AP, Schafer W. Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr Genet 2003; 43:87-95; PMID:12695848
44. Samson RA,Houbraken J, Thrane U, Frisvad JC, Andersen B. Food and indoor fungi. CBS "KNAW" Fungal Biodiversity Centre, Utrecht, The Netherlands, 2010.
45. Smedsgaard J. Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr A 1997; 760:264-70; PMID: 9062989; http://dx.doi.org/10.1016/S0021-9673(96) 00803-5