Abstract
The ectomycorrhiza formation involves intense gene expression control in both partners that leads to several morphological and physiological changes. The purpose of this chapter was to review the main genes from ectomycorrhizal fungi (EMF) expressed in association with roots or under mycorrhizal stimulus. Researchers looked at different EMF and host interactions, and screened different experimental conditions and techniques. It was possible to group a large number of ectomycorrhizal genes/proteins into different physiological categories according to probable functions within symbiotic associations. In total 389 ESTs/proteins were listed from different fungal genus and species. Ectomycorrhizal genes were grouped in eight physiological categories as follows (1) cell growth and organization, (2) morphogenesis, (3) energy metabolism, (4) protein synthesis and protein interaction, transcriptional and translation regulation, (5) ion transport, amino acid and peptide transport, (6) cell signaling and structural membrane proteins, (7) RNA/DNA processing and (8) cell defense and apoptosis. We observed that related genes change their expression level during formation and maintenance of symbiotic relationships; however, all of them are basally expressed in most symbiotic conditions. There seems to be a tendency for gene expression suppression (down-regulation) during short association periods or even during the preinfection interaction. This tendency can be observed in protein synthesis genes, carbon metabolism genes and membrane proteins like SRAPs and hydrophobins, which are proteins believed to be important agents for ectomycorrhiza formation. However, genes of unknown function can highlight a knowledge gap concerning fungal origin sequences in symbiosis, and alert the urgent need to encourage future studies in molecular ectomycorrhizal associations.
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References
Acioli-Santos B, Sebastiana M, Pessoa F, Sousa L, Figueiredo A, Fortes AM, Balde A, Maia LC, Pais MS (2008) Fungal transcript pattern during the preinfection stage (12 h) of ectomycorrhiza formed between Pisolithus tinctorius and Castanea sativa roots, identified using cDNA microarrays. Curr Microbiol 57:620–625
Aguilera J, Prieto JA (2001) The Saccharomyces cerevisiae aldose reductase is implied in the metabolism of methylglyoxal in response to stress conditions. Curr Genet 39:273–283
Babbitt PC, Hasson MS, Wedekind JE, Palmer DJ, Barrett WC, Reed GH, Rayment I, Ringe D, Kenyon GL, Gerlt JA (1996) The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the r-protons of carboxylic acids. Biochemistry 35:16489–16501
Bellamine A, Mangla AT, Nes WD, Waterman MR (1999) Characterization and catalytic properties of the sterol 14 α-demethylase from Mycobacterium tuberculosis. Biochemistry 96:8937–8942
Bender A, Pringle JR (1991) Use of a screen for synthetic lethal and multicopy suppressed mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol Cell Biol 11:1295–1305
Berg JM, Tymoczko JL, Stryer L (2004) Bioquímica 5ª Ed. Guanabara Koogan S.A., Rio de Janeiro, p p1059
Bydlowiski P, Magnannelli AC, Chamone DAF (1998) Hyper-homocistenemia e doenças vaso-oclusivas. Arquivos Brasileiros de Cardiologia 71:69–76
Campbell JL, Scheckman R (1997) Selective packaging of cargo molecules into endoplasmic reticulum-derived COPII vesicles. Proc Natl Acad Sci 94:837–842
Chan HM, La Thangue NB (2001) P300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci 114:2363–2373
Chapple C (1998) Molecular-genetics analysis of plant cytochrome P450-dependent monoxigenases. Annu Rev Plant Physiol Plant Mol Biol 49:311–343
Chowdhury S, Smith KW, Gustin MC (1992) Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation. J Cell Biol 118:561–571
Condeelis J (1995) Elongation factor 1α, translation and the cytoskeleton. Trends Biochem Sci 20:169–170
Duplessis S, Courty P, Tagu D, Martim F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611
Eades CJ, Gilbert A, Goodman CD, Hintz WE (1998) Identification and analysis of a class 2 alpha-mannosidase from Aspergillus nidulans. Glycobiology 8:17–33
Emanuelsson O, Elofsson A, Von Heijne G, Cristobal S (2003) In silico prediction of the peroxisomal proteome in fungi, plants and animals. J Mol Biol 330:443–456
Gupta RS (1995) Phylogenetic analysis of 90kD heat shock family of protein sequences and an examination of the relationship among animals, plants and fungi species. Mol Biol Evol 12:1063–1073
Haerslev T, Jacobson GK, Zedeler K (1995) The prognostic significance of immunohistochemically detectable metallothionein in primary breast carcinomas. Acta Pathol Microbiol Immunol Scand 103:279–285
Hasunuma K, Yabe N, Yoshida Y, Ogura Y, Hamada T (2003) Putative functions of nucleoside diphosphate kinase in plants and fungi. J Bioenerg Biomembr 35:57–65
Hayes JD, Pulford DJ (1995) The glutathione s-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600
He W, Parker R (2000) Functions of Lsm proteins in mRNA degradation and splicing. Curr Opin Cell Biol 12:346–350
Hirata D, Nakano K, Fukui M, Takenaka H, Miyakawa T, Mabuchi I (1998) Genes that cause aberrant cell morphology by overexpression in fission yeast: a role of a small GTP-binding protein Rho2 in cell morphogenesis. J Cell Sci 111:149–159
Hogan DA, Auchtung TA, Hausinger RP (1999) Cloning and characterization of a sulfonate/a-ketoglutarate dioxygenase from Saccharomyces cerevisiae. J Bacteriol 181:5876–5879
Imai K, Kijima T, Noda Y, Sutoh K, Yoda K, Adachi H (2002) A Rho GDP-dissociation inhibitor is involved in cytokinesis of Dictyostelium. Biochem Biophys Res Commun 296:305–312
Jakel S, Albig W, Kutay U, Bischoff FR, Schwamborn K, Doenecke D, Gorlich D (1999) The importin ß/importin 7 heterodimer is a functional nuclear import receptor for histone H1. Eur Mol Biol Organ J 18:2411–2423
Johansson T, Le Quéré A, Ahren D, Söderström B, Erlandsson R, Lundeberg J, Uhlén M, Tunlid A (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microbe Interact 17:202–205
Kawalleck P, Plesh G, Hahlbrock K, Somssich IE (1992) Induction by fungal elicitor of S-adenosyl-l-methionine synthetase and S-adenosyl-l-homocysteine hydrolase mRNAs in cultured cell and leaves of Petroselinum crispum. Proc Natl Acad Sci 89:4713–4717
Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. Fungal Genet Biol 23:18–33
Kim S, Bernreuther D, Thumm M, Podila G (1999a) LB.AUT7, a novel symbisis-regulated gene from an ectomycorrhizal fungus, Laccaria bicolor, is functionally related to vesicular transport and autophagocytosis. J Bacteriol 181:1963–1967
Kim S, Shivanand T, Podila G (1999b) Cloning and identification of symbiosis-regulated genes from the ectomycorrhizal Laccaria bicolor. Mycol Res 103:168–172
Koga M, Tanaka H, Yomogida K, Tsuchida J, Uchida K, Kitamura M, Sakoda S, Matsumiya K, Okuyama A, Nishimune Y (1998) Expression of selenoprotein-p messenger ribonucleic acid in the rat testis. Biol Reprod 58:261–265
Kong FK (1995) Influence of copper, manganese and pH on the growth and several enzyme activities in mycorrhizal fungus Amanita muscaria. Hemosphere 30:199–207
Kuge O, Hara-Kuge S, Orci L, Ravazzola M, Amherdt M, Tanigawa G, Wieland FT, Rothman JE (1993) ζ-COP, a subunit of coatomer, is required for COP-coated vesicle assembly. J Cell Biol 123:1727–1734
Lambeth JD, Seybert DW, Kamin H (1979) Ionic effects on adrenal steroidogenic electron transport. The role of adrenodoxin as an electron shuttle. J Biol Chem 254:7255–7264
Lammers PJ (2004) Symbiotic signalling: new functions for familiar proteins. New Phytol 161:324–326
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. Mol Plant Microbe Interact 18:659–673
Lei J, Lapayerie F, Malajczuk N, Dexheimer J (1990) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius (Pers.) Coker & Couch on toots of Eucalyptus urophylla S. T. Blake in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhizal formation. New Phytol 116:115–122
Macheroux P, Schmid J, Amrhein N, Schaller A (1999) A unique reaction in a common pathway: mechanism and function of chorismate synthase in the shikimate pathway. Planta 207:325–334
Madeo F, Herker E, Maldener C, Wissing S, LäChelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Manzow S, Brancolini C, Marks F, Richter KH (1996) Expression of growth arrest-specific (Gas) genes in murine keratinocytes: Gas2 is specifically regulated. Exp Cell Res 224:200–203
Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, Difazio S, Duplessis S, Tachet LF, Lucic E, Klett PF, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Hirzel HN, Le Secq MPO, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Peer YV, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé 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
Masson D, Kreis TE (1993) Identification and molecular characterization of E-MAP -115, a novel microtubule-associated protein predominantly expressed in epithelial cells. J Cell Biol 123:357–371
Menotta M, Amicucci A, Sisti D, Gioacchini AM, Stocchi V (2004) Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad. and Tilia Americana L. Curr Genet 46:158–165
Moon BY, Ho ZC, Sue GR, Chock PB, Earl RS (1994) On the protective mechanism of the thiol-specific antioxidant enzyme against the oxidative damage of biomacromolecules. J Biol Chem 269:1621–1626
Morel M, Jacob C, Kohler A, Johansson T, Martin F, Charlot M, Brun A (2005) Indentification of genes differentially expressed in extraradical mycelium and ectomycorrizal roots during Paxillus involutus–Petula pendula ectomycorrhizal symbiosis. Appl Environ Microbiol 71:382–391
Nehls U, Mikolajewski S, Ecke M, Hampp R (1999) Identification and expression analysis of two fungal cDNA regulated by ectomycorrhiza and fruit body formation. New Phytol 144:195–202
Ntambi JM, Buhrow SA, Kaestner KH, Christy RJ, Sibley E, Kelly TJ Jr, Lane MD (1988) Differentiation-induced gene expression in 3T3-Ll preadipocytes. Characterization of a differentially expressed gene encoding steaoryl-coa desaturase. J Biol Chem 263:17291–17300
Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48–54
Podila GK, Zheng J, Balasubramanian S, Sundaram S, Hiremath S, Brand JH, Hymes MJ (2002) Fungal gene expression in early symbiotic interactions between Laccaria bicolor and red pine. Plant Soil 244:117–128
Poinssot B, Vandelle E, Bentéjac M, Adrian M, Levis C, Brygoo Y, Garin J, Sicilia F, Thévenot PC, Pugin A (2003) The Endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe Interact 16:553–564
Polidori E, Agostini D, Zeppa S, Potenza L, Palma F, Sisti D, Stocchi V (2002) Identification of differentially expressed cDNA clones in Tilia platiphyllos-Tuber borchii ectomycorrhizae using a differential screening approach. Mol Genet Genomics 266:858–864
Porter TN, Li Y, Raushel FM (2004) Mechanism of the dihydroorotase reaction. Biochemistry 43:16285–16292
Punt PJ, Van Gemeren IA, Drint-Kuijvenhoven J, Hessing JGM, Van Muijlwijk-Harteveld GM, Beijersbergen A, Verrips CT, Van Den Hondel CAMJJ (1998) Analysis of the role of the gene bipA, encoding the major endoplasmic reticulum chaperone protein the secretion of homologous and heterologous proteins in black Aspergilli. Appl Microbiol Biotechnol 50:447–454
Rehling P, Model K, Brandner K, Kovermann P, Sickmann A, Meyer HE, Kühlbrandt W, Wagner R, Truscott KN, Pfanner N (2003) Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science 299:1747–1751
Santos B, Snyder M (2005) Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J Cell Biol 136:95–110
Schmid J, Amrhein N (1995) Molecular organization of the shikimate pathway in higher plants. Phytochemistry 39:737–749
Seroussi F, Pan HQ, Kedra D, Roe BA, Dumanski JP (1998) Caracterization of human NIPSNAP1 gene from 22q12: a member of novel gene family. Gene 212:13–20
Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H1-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353–1362
Silver S, Misra TK, Laddaga RA (1989) DNA sequence analysis of bacterial toxic heavy metal resistances. Biol Trace Elem Res 21:145–163
Slater S, Houmiel KL, Tran M, Mitski TA, Taylor NB, Padgette SR, Gruys KJ (1998) Multiple b-ketothiolases mediate poly(b-hydroxyalkanoate) copolymer synthesis in Ralstonia eutropha. J Bacteriol 180:1979–1987
Smith CV, Huang C, Miczak A, Russell DG, Sacchettini JC, Bentrup KH (2003) Biochemical and structural studies of malate synthase from Mycobacterium tuberculosis. J Biol Chem 278:1735–1743
Sundaram S, Kim SJ, Suzuki H, Mcquattie CJ, Hiremath ST, Podila G (2001) Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol Plant Microbe Interact 14:618–628
Szczepaneck T, Lazowska J (1996) Replacement of two non-adjacent amino acid in the S. serevisiae bi2 intron-incoded RNA maturase is sufficient to gain a homing- endonuclease activity. Eur Mol Biol Organ J 15:3758–3767
Tagu D, Nasse B, Martin F (1996) Cloning and caracterization of hydrophobins-enconding cDNAs from the ectomycorrhizal Basidiomycete Pisolithus tinctorius. Gene 168:93–97
Tagu D, De Bellis R, Balestrini R, De Vries OMH, Piccolli G, Stocchi V, Bonfante P, Martin F (2001) Immuno localization of hydrophobin HYDPt-1 from de ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots. New Phytol 149:127–135
Tasto JJ, Morrell JL, Gould KL (2003) An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J Cell Biol 160:1093–1103
Tatsumi A, Shoji J, Kikuma T, Arioka M, Kitamoto K (2007) Aggregation of endosomal-vacuolar compartments in the Aovps24-deleted strain in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 362:474–479
Timonen S, Peterson L (2002) Cytoskeletons in mycorrhizal symbioss. Plant Soil 244:199–210
Timonen S, Söderström B, Raudaskoski M (1996) Dynamics of cytosckeletal proteins in developing pine ectomycorriza. Mycorrhiza 6:423–429
Velten J, Oliver MJ (2001) Tr288, a rehydrin with a dehydrin twist. Plant Mol Biol 45:713–722
Voiblet C, Duplessis S, Encelot L, Martin F (2001) Identifications of symbiosis-reguleted genes in Eucalyptus globulus-Pisolitus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant J 25:181–191
Wilkinson CRM, Wallace M, Morphew M, Perry P, Allshire R, Javerzat JP, Mcintosh JR, Gordon C (1998) Localization of the 26S proteasome during mitosis and meiosis in fission yeast. EMBO J 17:6465–6476
Wösten HAB, Vocht ML (2000) Hydrophobins, the fungal coat unravelled. Biochim Biophys Acta 1469:79–86
Yamagata S (1989) Roles of O-acetyl-l-homoserine sulfhydrylases in micro-organisms. Biochimie 71:1125–1143
Yu YB (2002) Coiled-coils: stability, specificity, and drug delivery potential. Adv Drug Deliv Rev 54:1113–1129
Zahner HA, Harkins JE, Pringle JR (1996) Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae. Mol Cell Biol 16:1857–1870
Zaretsky M, Sitrit Y, Mills D, Roth-Bejerano N, Kagan-Zur V (2006) Differential expression of fungal genes at preinfection and mycorrhiza establishment between Terfezia boudieri isolates and Cistus incanus hairy root clones. New Phytol 171:837–846
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Acioli-Santos, B., Vieira, H.E.E., Lima, C.E.P., Maia, L.C. (2011). The Molecular Ectomycorrhizal Fungus Essence in Association: A Review of Differentially Expressed Fungal Genes During Symbiosis Formation. In: Rai, M., Varma, A. (eds) Diversity and Biotechnology of Ectomycorrhizae. Soil Biology, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-15196-5_5
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