Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis

被引:487
作者
Martin, Francis [1 ]
Kohler, Annegret [1 ]
Murat, Claude [1 ]
Balestrini, Raffaella [2 ,3 ]
Coutinho, Pedro M. [4 ,5 ]
Jaillon, Olivier [6 ,7 ,8 ]
Montanini, Barbara [9 ]
Morin, Emmanuelle [1 ]
Noel, Benjamin [6 ,7 ,8 ]
Percudani, Riccardo [9 ]
Porcel, Bettina [6 ,7 ,8 ]
Rubini, Andrea [10 ]
Amicucci, Antonella [11 ]
Amselem, Joelle [12 ]
Anthouard, Veronique [6 ,7 ,8 ]
Arcioni, Sergio [10 ]
Artiguenave, Francois [6 ,7 ,8 ]
Aury, Jean-Marc [6 ,7 ,8 ]
Ballario, Paola [13 ,14 ]
Bolchi, Angelo [9 ]
Brenna, Andrea [13 ,14 ]
Brun, Annick [1 ]
Buee, Marc [1 ]
Cantarel, Brandi [4 ,5 ]
Chevalier, Gerard [15 ]
Couloux, Arnaud [6 ,7 ,8 ]
Da Silva, Corinne [6 ,7 ,8 ]
Denoeud, France [6 ,7 ,8 ]
Duplessis, Sebastien [1 ]
Ghignone, Stefano [2 ,3 ]
Hilselberger, Benoit [12 ]
Iotti, Mirco [16 ]
Marcais, Benoit [1 ]
Mello, Antonietta [2 ,3 ]
Miranda, Michele [17 ]
Pacioni, Giovanni [18 ]
Quesneville, Hadi [12 ]
Riccioni, Claudia [10 ]
Ruotolo, Roberta [9 ]
Splivallo, Richard [19 ]
Stocchi, Vilberto
Tisserant, Emilie [1 ]
Viscomi, Arturo Roberto [9 ]
Zambonelli, Alessandra [16 ]
Zampieri, Elisa [2 ,3 ]
Henrissat, Bernard [4 ,5 ]
Lebrun, Marc-Henri [20 ]
Paolocci, Francesco [10 ]
Bonfante, Paola [2 ,3 ]
Ottonello, Simone [9 ]
机构
[1] Nancy Univ, UMR 1136, INRA, F-54280 Champenoux, France
[2] Univ Turin, Dipartimento Biol Vegetale, I-10125 Turin, Italy
[3] Univ Turin, CNR, Ist Protez Piante, Sez Torino, I-10125 Turin, Italy
[4] Univ Aix Marseille 1, CNRS, UMR6098, F-13288 Marseille, France
[5] Univ Aix Marseille 2, CNRS, UMR6098, F-13288 Marseille, France
[6] CEA, IG, F-91057 Evry, France
[7] CNRS, UMR 8030, F-91057 Evry, France
[8] Univ Evry, F-91057 Evry, France
[9] Univ Parma, Dipartmento Biochim & Biol Mol, I-43100 Parma, Italy
[10] CNR, IGV, Unita Organizzat Supporto Perugia, I-06128 Perugia, Italy
[11] Univ Urbino, Dipartimento Sci Biomol, I-61029 Urbino, PU, Italy
[12] INRA, Unite Rech Genom Info, F-78000 Versailles, France
[13] Univ Roma La Sapienza, Dipartimento Genet & Biol Mol, I-00185 Rome, Italy
[14] Univ Roma La Sapienza, CNR, IBPM, I-00185 Rome, Italy
[15] Univ Blaise Pascal, INRA Clermont Theix, INRA, UMR Ameliorat & Sante Plantes, F-63122 St Genes Champanelle, France
[16] Univ Bologna, Dipartimento Protez Valorizzaz Agroalimentare, I-40126 Bologna, Italy
[17] Univ Aquila, Dipartimento Biol Base & Applicata, I-67100 Laquila, Italy
[18] Univ Aquila, Dipartimento Sci Ambientali, I-67100 Laquila, Italy
[19] Univ Gottingen, D-37077 Gottingen, Germany
[20] INRA Grignon, INRA, UMR BIOGER CPP, F-78850 Thiverval Grignon, France
关键词
FUNGAL; INSIGHTS;
D O I
10.1038/nature08867
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The Perigord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate today's truffle market(1,2). The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy produced by an ectomycorrhizal symbiont(3) endemic to calcareous soils in southern Europe. The worldwide demand for this truffle has fuelled intense efforts at cultivation. Identification of processes that condition and trigger fruit body and symbiosis formation, ultimately leading to efficient crop production, will be facilitated by a thorough analysis of truffle genomic traits. In the ectomycorrhizal Laccaria bicolor, the expansion of gene families may have acted as a 'symbiosis toolbox'(4). This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species(5). To get a better understanding of the biology and evolution of the ectomycorrhizal symbiosis, we report here the sequence of the haploid genome of T. melanosporum, which at similar to 125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for similar to 58% of the genome. In contrast, this genome only contains similar to 7,500 protein-coding genes with very rare multigene families. It lacks large sets of carbohydrate cleaving enzymes, but a few of them involved in degradation of plant cell walls are induced in symbiotic tissues. The latter feature and the upregulation of genes encoding for lipases and multicopper oxidases suggest that T. melanosporum degrades its host cell walls during colonization. Symbiosis induces an increased expression of carbohydrate and amino acid transporters in both L. bicolor and T. melanosporum, but the comparison of genomic traits in the two ectomycorrhizal fungi showed that genetic predispositions for symbiosis-'the symbiosis toolbox'-evolved along different ways in ascomycetes and basidiomycetes.
引用
收藏
页码:1033 / 1038
页数:6
相关论文
共 19 条
[1]   Trifling variation in truffles [J].
Bertault, G ;
Raymond, M ;
Berthomieu, A ;
Callot, G ;
Fernandez, D .
NATURE, 1998, 394 (6695) :734-734
[2]   The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics [J].
Cantarel, Brandi L. ;
Coutinho, Pedro M. ;
Rancurel, Corinne ;
Bernard, Thomas ;
Lombard, Vincent ;
Henrissat, Bernard .
NUCLEIC ACIDS RESEARCH, 2009, 37 :D233-D238
[3]   Evolution of fungal sex chromosomes [J].
Fraser, JA ;
Heitman, J .
MOLECULAR MICROBIOLOGY, 2004, 51 (02) :299-306
[4]   Genomics of the fungal kingdom: Insights into eukaryotic biology [J].
Galagan, JE ;
Henn, MR ;
Ma, LJ ;
Cuomo, CA ;
Birren, B .
GENOME RESEARCH, 2005, 15 (12) :1620-1631
[5]   RIP: the evolutionary cost of genome defense [J].
Galagan, JE ;
Selker, EU .
TRENDS IN GENETICS, 2004, 20 (09) :417-423
[6]  
Hall IR., 2007, TAMING TRUFFLE
[7]   The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses [J].
Hibbett, David S. ;
Matheny, P. Brandon .
BMC BIOLOGY, 2009, 7
[8]   The First Structure of a Glycoside Hydrolase Family 61 Member, Cel61B from Hypocrea jecorina, at 1.6 Å Resolution [J].
Karkehabadi, Saeid ;
Hansson, Henrik ;
Kim, Steve ;
Piens, Kathleen ;
Mitchinson, Colin ;
Sandgren, Mats .
JOURNAL OF MOLECULAR BIOLOGY, 2008, 383 (01) :144-154
[9]   Comparative genomics of enzymes in flavor-forming pathways from amino acids in lactic acid bacteria [J].
Liu, Mengjin ;
Nauta, Arjen ;
Francke, Christof ;
Siezen, Roland J. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2008, 74 (15) :4590-4600
[10]   The origins of genome complexity [J].
Lynch, M ;
Conery, JS .
SCIENCE, 2003, 302 (5649) :1401-1404