Fungal and algal gene expression in early developmental stages of lichen-symbiosis

Mycologia

Volumn 103, Issue 2, 2011, Pages 291-306

  Joneson, Suzanne ^a   Armaleo, Daniele ^b   Lutzoni, François ^b  

^a UNIVERSITY OF IDAHO   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Asterochloris sp.; Cladonia grayi; Lichen; Plant fungal interactions; Symbiosis

Indexed keywords

AMINO ACID; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; FUNGUS; GENE EXPRESSION; GLUCOSE; GREEN ALGA; LICHEN; LIPID; METABOLISM; POLYMERASE CHAIN REACTION; PROTEIN; QUANTITATIVE ANALYSIS; SYMBIONT; SYMBIOSIS;

ALGAE; ASTEROCHLORIS; CHLOROPHYTA; CLADONIA GRAYI; FUNGI;

FUNGAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CHEMISTRY; GENE EXPRESSION; GENETICS; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; LICHENS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT; SYMBIOSIS;

AMINO ACID SEQUENCE; ASCOMYCOTA; CHLOROPHYTA; FUNGAL PROTEINS; GENE EXPRESSION; LICHENS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SYMBIOSIS;

EID: 79955947578     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/10-064     Document Type: Article

References (77)

1. Al SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor M. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryotic Microbiol 52:399-451
2. Ahmadjian V. 1959. A contribution toward lichen synthesis. Mycologia 51:56-60
3. Ahmadjian V. 1967. The lichen symbiosis. Waltham, Mass:Blaisdell Publishing. 152 p.
4. Ahmadjian V., Jacobs JB, Russell LA. 1978. Scanning electron microscope study of early lichen synthesis. Science 200: 1062-1064
5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410.
6. Armaleo D. 1991. Experimental microbiology of lichensmycelia fragmentation, a novel growth chamber, and the origins of thallus differentiation. Symbiosis 11:163-177.
7. Armaleo D., May S. 2009. Sizing the fungal and algal genomes of the lichen Cladonia grayi through quantitative PCR. Symbiosis 49:43-51
8. Armaleo D., Miao V. 1999. Symbiosis and DNA methylation in the Cladonia lichen fungus. Symbiosis 26:143-163.
9. Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F. 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: Are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283-287
10. Backor M, Fahselt D. 2003. Cellulose-acetate disks as novel substrate for the resynthesis and culture of lichens. Bryologist 106:439-442
11. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y. 2002. Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108-124, doi:10.1104/pp.010466
12. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795, doi:10.1016/j.jmb.2004. 05.028
13. Berto P, Comménil P, Belingheri L, Dehorter B. 1999. Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in the infection of cauliflower leaves. FEMS Microbiol Lett 180:183-189, doi:10.1111/j.1574-6968.1999.tb08794.x
14. Burke DT, Dawson D, Stearns T. 2000. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. 205 p.
15. Caturla M, Chaparro C, Schroeyers K, Holsters M. 2002. Suppression subtractive hybridization to enrich lowabundance and submergenceenhanced transcripts of adventitious root primordia of Sesbania rostrata. Plant Sci 162:915-921, doi:10.1016/S0168-9452(02)00038-9
16. Cheng J, Randall AZ, Sweredoski MJ, Baldi P. 2005. SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res 33:W72-W76, doi:10.1093/nar/gki396
17. Chu FH, Wang SY, Lee LC, Shaw JF. 2008. Identification and characterization of a lipase gene from Antrodia cinnamomea. Mycol Res 112:1421-1427, doi:10.1016/ j.mycres.2008.06.006
18. Clayden SR. 1998. Thallus initiation and development in the lichen Rhizocarpon lecanorinum. New Phytol 139: 685-695, doi:10.1046/j.1469-8137.1998.00243.x
19. Comménil P, Belingheri L, Dehorter B. 1998. Antilipase antibodies prevent infection of tomato leaves by Botrytis cinerea. Physiol Mol Plant Pathol 52:1-14, doi:10.1006/ pmpp.1997.0130
20. Deason T, Bold H. 1960. Exploratory studies of Texas soil algae. Vol. 6022. Austin: Univ. Texas Press. 70 p.
21. Deguchi Y, Banba M, Shimoda Y, Chechetka SA, Suzuri R, Okusako Y, Ooki Y, Toyokura K, Suzuki A, Uchiumi T, Higashi S, Abe M, Kouchi H, Izui K, Hata S. 2007. Transcriptome profiling of Lotus japonicus roots during arbuscular mycorrhiza development and comparison with that of nodulation. DNA Research 14:117-133, doi:10.1093/dnares/dsm014
22. Derewenda U, Brzozowski AM, Lawson DM, Derewenda ZS. 1992a. Catalysis at the interface-the anatomy of a conformational change in a triglyceride lipase. Biochemistry 31:1532-1541, doi:10.1021/bi00120a034
23. Derewenda U, Swenson L, Green R, Wei Y, Yamaguchi S, Joerger R, Haas MJ, Derewenda ZS. 1994. Current progress in crystallographic studies of new lipases from filamentous fungi. Protein Eng 7:551-557, doi:10.1093/protein/ 7.4.551
24. Derewenda ZS, Derewenda U, Dodson GG. 1992b. The crystal and molecular structure of the Rhizomucor miehei triacylglyceride lipase at 1.9 angstrom resolution. J Mol Biol 227:818-839, doi:10.1016/0022-2836(92)90225-9
25. Deveau A, Kohler A, Frey-Klett P, Martin F. 2008. The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N. New Phytol 180:379-390, doi:10.1111/j.1469-8137.2008. 02581.x
26. Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. 1996. Suppression subtractive hybridization: A method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025-6030, doi:10.1073/pnas.93.12.6025
27. Domozych DS, Stewart KD, Mattox KR. 1980. The comparative aspects of cell-wall chemistry in the green-algae (Chlorophyta). J Mol Evol 15:1-12, doi:10.1007/BF01732578
28. Duplessis S, Courty PE, Tagu D, Martin F. 2005. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599-611.
29. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797, doi:10.1093/nar/gkh340
30. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016, doi:10.1006/jmbi.2000.3903
31. Fedorova ND, Badger JH, Robson GD, Wortman JR, Nierman WC. 2005. Comparative analysis of programmed cell death pathways in filamentous fungi. BMC Genomics 6:14, doi:10.1186/1471-2164-6-177
32. Galun M. 1988. Recognition in fungus alga interaction in lichens. Phytoparasitica 16:190-190.
33. Glass NL, Kaneko I. 2003. Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryotic Cell 2:1-8, doi:10.1128/EC.2.1.1-8.2003
34. Green TGA, Smith D. 1974. Lichen Physiology XIV. Differences between lichen algae in symbiosis and in isolation. New Phytol 73:753-766, doi:10.1111/j.1469-8137.1974.tb01303.x
35. Guschina IA, Dobson G, Harwood JL. 2003. Lipid metabolism in cultured lichen photobionts with different phosphorus status. Phytochemistry 64:209-217, doi:10.1016/S0031-9422(03)00279-6
36. Herrero S, Amnuaykanjanasin A, Daub ME. 2007. Identification of genes differentially expressed in the phytopathogenic fungus Cercospora nicotianae between cer-cosporin toxin-resistant and -susceptible strains. FEMS Microbiol Lett 275:326-337, doi:10.1111/j.1574-6968. 2007.00903.x
37. Honegger R. 1990. Surface interactions in lichens. In: Wiessner W, Robinson DG, Starr RC, eds. Experimental phycology. Cell walls and surfaces, reproduction, photosynthesis. Berlin: Springer. p 40-54.
38. Honegger R. 1997. Metabolic interactions at the mycobiontsphotobiont interface in lichens. In:, The Mycota V, Part A. 1997. Plant relationships. Vol. V(A). Berlin-Heidelberg: Springer-Verlag. p 209-221.
39. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiya ma J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lü cking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818-822, doi:10.1038/nature05110
40. Johansson T, Le Quéré A, Ahren D, Sö derströ m B, Erlandsson R, Lundeberg J, Uhlen M, Tunlid A. 2004. Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant-Microbe Interact 17:202-215, doi:10.1094/MPMI.2004.17.2.202
41. Joneson S, Lutzoni F. 2009. Compatibility and thigmotropism in the lichen symbiosis: a reappraisal. Symbiosis 47:109-115, doi:10.1007/BF03182294
42. Kasprzewska A. 2003. Plant chitinases-regulation and function. Cell Mol Biol Lett 8:809-824.
43. Kirk P, Ainsworth G, Bisby G. 2008. Dictionary of the Fungi. 10th ed. Wallingford, UK: CABI Publishing. 784 p.
44. Kohno M, Funatsu J, Mikami B, Kugimiya W, Matsuo T, Morita Y. 1996. The crystal structure of lipase II from Rhizopus niveus at 2.2 angstrom resolution. J Biochem 120:505-510.
45. Konig J, Peveling E. 1984. Cell walls of the phycobionts Trebouxia and Pseudotrebouxia-constituents and their localization. Lichenologist 16:129-144, doi:10.1017/S002428298400030X
46. Kroken S, Taylor JW. 2000. Phylogenetic species, reproductive mode and specificity of the green alga Trebouxiaforming lichens with the fungal genus Letharia. Bryologist 103:645-660, doi:10.1639/0007-2745(2000) 103[0645:PSRMAS]2.0.CO;2
47. Le Quéré A, Wright DP, Söderström B, Tunlid A, Johansson T. 2005. Global patterns of gene regulation associated with the development of ectomycorrhiza between birch Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol Plant-Microbe Interact 18: 659-673, doi:10.1094/MPMI-18-0659
48. Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants. Am J Bot 91:1535-1556, doi:10.3732/ ajb.91.10.1535
49. Lines CEM, Ratcliffe RG, Rees TAV, Southon TE. 1989. A C- 13 NMR study of photosynthate transport and metabolism in the lichen Xanthoria calcicola Oxner. New Phytol 111:447-456, doi:10.1111/j.1469-8137.1989.tb00707.x
50. Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buee M, Brokstein P, Canback B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbe J, Lin YC, Legue V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kues U, Lucas S, van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouze P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88-92, doi:10.1038/ nature06556
51. Martin F, Nehls U. 2009. Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12: 508-515, doi:10.1016/j.pbi.2009.05.007
52. Morehouse EA, James TY, Ganley ARD, Vilgalys R, Berger L, Murphy PJ, Longcore JE. 2003. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol Ecol 12:395-403, doi:10.1046/j.1365-294X.2003.01732.x
53. Mumberg D, Muller R, Funk M. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119-122, doi:10.1016/0378-1119(95)00037-7
54. Myllys L, Lohtander K, Tehler A. 2001. Beta-tubulin, ITS and group I intron sequences challenge the species pair concept in Physcia aipolia and P. caesia. Mycologia 93:335-343, doi:10.2307/3761655
55. Nehls U, Gohringer F, Wittulsky S, Dietz S. 2010. Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol 12:292-301, doi:10.1111/ j.1438-8677.2009.00312.x
56. Niederacher D, Entian KD. 1987. Isolation and characterization of the regulatory HEX2 gene necessary for glucose repression in yeast. Mol Gen Genet 206:505-509, doi:10.1007/BF00428892
57. Nowak TS, Woodards AC, Jung YH, Adema CM, Loker ES. 2004. Identification of transcripts generated during the response of resistant Biomphalaria glabrata to Schistosoma mansoni infection using suppression subtractive hybridization. J Parasitol 90:1034-1040, doi:10. 1645/GE-193R1
58. Oliver E, Crittenden PD, Beckett A, Brown DH. 1989. Growth of lichen-forming fungi on membrane filters. Lichenologist 21:387-392, doi:10.1017/S0024282989000666
59. Pahlich S, Zakaryan RP, Gehring H. 2006. Protein arginine methylation: cellular functions and methods of analysis. Biochim Biophysic Acta-Proteins Proteomics 1764: 1890-1903, doi:10.1016/j.bbapap.2006.08.008
60. Peter M, Courty PE, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F. 2003. Analysis of expressed sequence tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus microcarpus. New Phytol 159:117-129, doi:10.1046/j.1469-8137.2003.00796.x
61. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002-2007.
62. Polidori E, Agostini D, Zeppa S, Potenza L, Palma F, Sisti D, Stocchi V. 2002. Identification of differentially expressed cDNA clones in Tilia platyphyllos-Tuber borchii ectomycorrhizae using a differential screening approach. Mol Genet Genomics 266:858-864.
63. Rasmussen R. 2001. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, eds. Rapid cycle real time PCR: methods and applications. Heidelberg, Germany: Springer. p 21-34.
64. Raven J. 1977. The evolution of vascular land plants in relation to supracellular transport processes. Adv Bot Res 5:153-219, doi:10.1016/S0065-2296(08)60361-4
65. Richardson D, Hill DJ, Smith DC. 1968. Lichen physiology XI. Role of alga in determining pattern of carbohydrate movement between lichen symbionts. New Phytol 67: 469-486, doi:10.1111/j.1469-8137.1968.tb05476.x
66. Richardson D, Smith DC. 1968. Lichen physiology X. Isolated algal and fungal symbionts of Xanthoria aureola. New Phytol 67:69-77, doi:10.1111/j.1469-8137.1968.tb05455.x
67. Schoch CL, Sung GH, Lopez-Giraldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh SO, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Budel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O'Donnell K, Sipman H, Rogers JD, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston PR, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Trappe JM, Yahr R, Lutzoni F, Spatafora JW. 2009. The Ascomycota Tree of Life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224-239, doi:10.1093/sysbio/syp020
68. Schwendener S. 1869. Die Flechten als Parasiten der Algen. Verhandlungen der Schweizerischen Naturforschenden Gesellschaft in Basel [translated by Leon Shernoff, 2004, from The Origins of Symbiosis 5:527-550.]
69. Selosse MA, Le Tacon F. 1998. The land flora: a phototrophfungus partnership? Trends Ecol Evol 13:15-20, doi:10.1016/S0169-5347(97)01230-5
70. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, Lehvaslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E. 2002. The bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611-1618, doi:10.1101/gr.361602
71. Stothard P. 2000. The sequence manipulation suite: Java-Script programs for analyzing and formatting protein and DNA sequences. Biotechniques 28:1102-1104.
72. Taylor TN. 1990. Fungal associations in the terrestrial paleoecosystem. Trends Ecol Evol 5:21-25, doi:10. 1016/0169-5347(90)90008-2
73. Trembley ML, Ringli C, Honegger R. 2002. Morphological and molecular analysis of early stages in the resynthesis of the lichen Baeomyces rufus. Mycol Res 106:768-776, doi:10.1017/S0953756202006081
74. Voiblet C, Duplessis S, Encelot N, Martin F. 2001. Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant J 25:181-191, doi:10.1046/j.1365-313x.2001.00953.x
75. Voigt CA, Schäfer W, Salomon S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J 42: 364-375, doi:10.1111/j.1365-313X.2005.02377.x
76. Xie WQ, Rothblum LI. 1991. Rapid, small-scale RNA isolation from tissue-culture cells. Biotechniques 11: 324-327.
77. Zolan ME, Pukkila PJ. 1986. Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6:195-200.