Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts

被引:115
作者
Hacquard, Stephane [1 ]
Kracher, Barbara [1 ]
Maekawa, Takaki [1 ]
Vernaldi, Saskia [1 ]
Schulze-Lefert, Paul [1 ]
van Themaat, Emiel Ver Loren [1 ]
机构
[1] Max Planck Inst Plant Breeding Res, Dept Plant Microbe Interact, D-50829 Cologne, Germany
关键词
comparative genomics; fungal genetics; obligate biotrophy; plant-microbe interactions; effector-triggered immunity; RESISTANCE GENES; DIFFERENTIAL EXPRESSION; OBLIGATE BIOTROPHY; PLANT-CELL; EVOLUTION; FUNGI; LOCUS; POPULATION; VIRULENCE; PROFILES;
D O I
10.1073/pnas.1306807110
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
Barley powdery mildew, Blumeria graminis f. sp. hordei (Bgh), is an obligate biotrophic ascomycete fungal pathogen that can grow and reproduce only on living cells of wild or domesticated barley (Hordeum sp.). Domestication and deployment of resistant barley cultivars by humans selected for amplification of Bgh isolates with different virulence combinations. We sequenced the genomes of two European Bgh isolates, A6 and K1, for comparative analysis with the reference genome of isolate DH14. This revealed a mosaic genome structure consisting of large isolate-specific DNA blocks with either high or low SNP densities. Some of the highly polymorphic blocks likely accumulated SNPs for over 10,000 years, well before the domestication of barley. These isolate-specific blocks of alternating monomorphic and polymorphic regions imply an exceptionally large standing genetic variation in the Bgh population and might be generated and maintained by rare outbreeding and frequent clonal reproduction. RNA-sequencing experiments with isolates A6 and K1 during four early stages of compatible and incompatible interactions on leaves of partially immunocompromised Arabidopsis mutants revealed a conserved Bgh transcriptional program during pathogenesis compared with the natural host barley despite similar to 200 million years of reproductive isolation of these hosts. Transcripts encoding candidate-secreted effector proteins are massively induced in successive waves. A specific decrease in candidate-secreted effector protein transcript abundance in the incompatible interaction follows extensive transcriptional reprogramming of the host transcriptome and coincides with the onset of localized host cell death, suggesting a host-inducible defense mechanism that targets fungal effector secretion or production.
引用
收藏
页码:E2219 / E2228
页数:10
相关论文
共 76 条
[51]   Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage [J].
Raffaele, Sylvain ;
Farrer, Rhys A. ;
Cano, Liliana M. ;
Studholme, David J. ;
MacLean, Daniel ;
Thines, Marco ;
Jiang, Rays H. Y. ;
Zody, Michael C. ;
Kunjeti, Sridhara G. ;
Donofrio, Nicole M. ;
Meyers, Blake C. ;
Nusbaum, Chad ;
Kamoun, Sophien .
SCIENCE, 2010, 330 (6010) :1540-1543
[52]   Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance [J].
Ridout, Christopher J. ;
Skamnioti, Pari ;
Porritt, Oliver ;
Sacristan, Soledad ;
Jones, Jonathan D. G. ;
Brown, James K. M. .
PLANT CELL, 2006, 18 (09) :2402-2414
[53]   Integrative genomics viewer [J].
Robinson, James T. ;
Thorvaldsdottir, Helga ;
Winckler, Wendy ;
Guttman, Mitchell ;
Lander, Eric S. ;
Getz, Gad ;
Mesirov, Jill P. .
NATURE BIOTECHNOLOGY, 2011, 29 (01) :24-26
[54]   Coevolution between a Family of Parasite Virulence Effectors and a Class of LINE-1 Retrotransposons [J].
Sacristan, Soledad ;
Vigouroux, Marielle ;
Pedersen, Carsten ;
Skamnioti, Pari ;
Thordal-Christensen, Hans ;
Micali, Cristina ;
Brown, James K. M. ;
Ridout, Christopher J. .
PLOS ONE, 2009, 4 (10)
[55]   Ten things to know about oomycete effectors [J].
Schornack, Sebastian ;
Huitema, Edgar ;
Cano, Liliana M. ;
Bozkurt, Tolga O. ;
Oliva, Ricardo ;
van Damme, Mireille ;
Schwizer, Simon ;
Raffaele, Sylvain ;
Chaparro-Garcia, Angela ;
Farrer, Rhys ;
Segretin, Maria Eugenia ;
Bos, Jorunn ;
Haas, Brian J. ;
Zody, Michael C. ;
Nusbaum, Chad ;
Win, Joe ;
Thines, Marco ;
Kamoun, Sophien .
MOLECULAR PLANT PATHOLOGY, 2009, 10 (06) :795-803
[56]   Diversity at the Mla Powdery Mildew Resistance Locus from Cultivated Barley Reveals Sites of Positive Selection [J].
Seeholzer, Sabine ;
Tsuchimatsu, Takashi ;
Jordan, Tina ;
Bieri, Stephane ;
Pajonk, Simone ;
Yang, Wenxiang ;
Jahoor, Ahmed ;
Shimizu, Kentaro K. ;
Keller, Beat ;
Schulze-Lefert, Paul .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2010, 23 (04) :497-509
[57]   Use of within-array replicate spots for assessing differential expression in microarray experiments [J].
Smyth, GK ;
Michaud, J ;
Scott, HS .
BIOINFORMATICS, 2005, 21 (09) :2067-2075
[58]   Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism [J].
Spanu, Pietro D. ;
Abbott, James C. ;
Amselem, Joelle ;
Burgis, Timothy A. ;
Soanes, Darren M. ;
Stueber, Kurt ;
van Themaat, Emiel Ver Loren ;
Brown, James K. M. ;
Butcher, Sarah A. ;
Gurr, Sarah J. ;
Lebrun, Marc-Henri ;
Ridout, Christopher J. ;
Schulze-Lefert, Paul ;
Talbot, Nicholas J. ;
Ahmadinejad, Nahal ;
Ametz, Christian ;
Barton, Geraint R. ;
Benjdia, Mariam ;
Bidzinski, Przemyslaw ;
Bindschedler, Laurence V. ;
Both, Maike ;
Brewer, Marin T. ;
Cadle-Davidson, Lance ;
Cadle-Davidson, Molly M. ;
Collemare, Jerome ;
Cramer, Rainer ;
Frenkel, Omer ;
Godfrey, Dale ;
Harriman, James ;
Hoede, Claire ;
King, Brian C. ;
Klages, Sven ;
Kleemann, Jochen ;
Knoll, Daniela ;
Koti, Prasanna S. ;
Kreplak, Jonathan ;
Lopez-Ruiz, Francisco J. ;
Lu, Xunli ;
Maekawa, Takaki ;
Mahanil, Siraprapa ;
Micali, Cristina ;
Milgroom, Michael G. ;
Montana, Giovanni ;
Noir, Sandra ;
O'Connell, Richard J. ;
Oberhaensli, Simone ;
Parlange, Francis ;
Pedersen, Carsten ;
Quesneville, Hadi ;
Reinhardt, Richard .
SCIENCE, 2010, 330 (6010) :1543-1546
[59]   Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat [J].
Srichumpa, P ;
Brunner, S ;
Keller, B ;
Yahiaoui, N .
PLANT PHYSIOLOGY, 2005, 139 (02) :885-895
[60]   AUGUSTUS:: ab initio prediction of alternative transcripts [J].
Stanke, Mario ;
Keller, Oliver ;
Gunduz, Irfan ;
Hayes, Alec ;
Waack, Stephan ;
Morgenstern, Burkhard .
NUCLEIC ACIDS RESEARCH, 2006, 34 :W435-W439