Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism

Pietro D. Spanu; James C. Abbott; Joelle Amselem; Timothy A. Burgis; Darren M. Soanes; Kurt  Stüber; Emiel Ver Loren van Themaat; James K.M.  Brown; Sarah A. Butcher; Sarah J. Gurr; Marc-Henri Lebrun; Christopher J. Ridout; Paul Schulze-Lefert; Nicholas J. Talbot; Nahal Ahmadinejad; Christian Ametz; Geraint R. Barton; Mariam Benjdia; Przemyslaw Bidzinski; Laurence V. Bindschedler; Maike Both; Marin T. Brewer; Lance  Cadle-Davidson; Molly M. Cadle-Davidson; Jerome Collemare; Rainer Cramer; Omer Frenkel; Dale Godfrey; James Harriman; Claire Hoede; Brian C. King; Sven Klages; Jochen Kleemann; Daniela Knoll; Prasanna S. Koti; Jonathan Kreplak; Francisco J. López-Ruiz; Xunli Lu; Takaki Maekawa; Siraprapa Mahanil; Cristina Micali; Michael G.  Milgroom; Giovanni Montana; Sandra Noir; Richard J. O'Connell; Simone Oberhaensli; Francis Parlange; Carsten Pedersen; Hadi Quesneville; Richard Reinhardt; Matthias  Rott; Soledad Sacristán; Sarah M. Schmidt; Moritz Schön; Pari Skamnioti; Hans Sommer; Amber Stephens; Hiroyuki Takahara; Hans Thordal-Christensen; Marielle Vigouroux; Ralf Weßling; Thomas Wicker; Ralph Panstruga

doi:10.1126/science.1194573

Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism

Pietro D. Spanu, James C. Abbott, Joelle Amselem, Timothy A. Burgis, Darren M. Soanes, Kurt Stüber, Emiel Ver Loren van Themaat, James K.M. Brown , Sarah A. Butcher, Sarah J. Gurr, Marc-Henri Lebrun, Christopher J. Ridout, Paul Schulze-Lefert, Nicholas J. Talbot, Nahal Ahmadinejad, Christian Ametz, Geraint R. Barton, Mariam Benjdia, Przemyslaw Bidzinski, Laurence V. BindschedlerMaike Both, Marin T. Brewer, Lance Cadle-Davidson, Molly M. Cadle-Davidson, Jerome Collemare, Rainer Cramer, Omer Frenkel, Dale Godfrey, James Harriman, Claire Hoede, Brian C. King, Sven Klages, Jochen Kleemann, Daniela Knoll, Prasanna S. Koti, Jonathan Kreplak, Francisco J. López-Ruiz, Xunli Lu, Takaki Maekawa, Siraprapa Mahanil, Cristina Micali, Michael G. Milgroom, Giovanni Montana, Sandra Noir, Richard J. O'Connell, Simone Oberhaensli, Francis Parlange, Carsten Pedersen, Hadi Quesneville, Richard Reinhardt, Matthias Rott, Soledad Sacristán, Sarah M. Schmidt, Moritz Schön, Pari Skamnioti, Hans Sommer, Amber Stephens, Hiroyuki Takahara, Hans Thordal-Christensen, Marielle Vigouroux, Ralf Weßling, Thomas Wicker, Ralph Panstruga

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Abstract

Powdery mildews are phytopathogens whose growth and reproduction are entirely dependent on living plant cells. The molecular basis of this life-style, obligate biotrophy, remains unknown. We present the genome analysis of barley powdery mildew, Blumeria graminis f.sp. hordei (Blumeria), as well as a comparison with the analysis of two powdery mildews pathogenic on dicotyledonous plants. These genomes display massive retrotransposon proliferation, genome-size expansion, and gene losses. The missing genes encode enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, probably reflecting their redundancy in an exclusively biotrophic life-style. Among the 248 candidate effectors of pathogenesis identified in the Blumeria genome, very few (less than 10) define a core set conserved in all three mildews, suggesting thatmost effectors represent species-specific adaptations.

Original language	English
Journal	Science
Volume	330
Issue number	6010
Pages (from-to)	1543-1546
Number of pages	4
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.1194573
Publication status	Published - 10 Dec 2010

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Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stüber, K., Themaat, E. V. L. V., Brown , J. K. M., Butcher, S. A., Gurr, S. J., Lebrun, M-H., Ridout, C. J., Schulze-Lefert, P., Talbot, N. J., Ahmadinejad, N., Ametz, C., Barton, G. R., Benjdia, M., Bidzinski, P., ... Panstruga, R. (2010). Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science, 330(6010), 1543-1546 . https://doi.org/10.1126/science.1194573

Spanu, PD, Abbott, JC, Amselem, J, Burgis, TA, Soanes, DM, Stüber, K, Themaat, EVLV, Brown , JKM, Butcher, SA, Gurr, SJ, Lebrun, M-H, Ridout, CJ, Schulze-Lefert, P, Talbot, NJ, Ahmadinejad, N, Ametz, C, Barton, GR, Benjdia, M, Bidzinski, P, Bindschedler, LV, Both, M, Brewer, MT, Cadle-Davidson, L, Cadle-Davidson, MM, Collemare, J, Cramer, R, Frenkel, O, Godfrey, D, Harriman, J, Hoede, C, King, BC, Klages, S, Kleemann, J, Knoll, D, Koti, PS, Kreplak, J, López-Ruiz, FJ, Lu, X, Maekawa, T, Mahanil, S, Micali, C, Milgroom, MG, Montana, G, Noir, S, O'Connell, RJ, Oberhaensli, S, Parlange, F, Pedersen, C, Quesneville, H, Reinhardt, R, Rott, M, Sacristán, S, Schmidt, SM, Schön, M, Skamnioti, P, Sommer, H, Stephens, A, Takahara, H, Thordal-Christensen, H, Vigouroux, M, Weßling, R, Wicker, T & Panstruga, R 2010, 'Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism', Science, vol. 330, no. 6010, pp. 1543-1546 . https://doi.org/10.1126/science.1194573

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title = "Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism",

abstract = "Powdery mildews are phytopathogens whose growth and reproduction are entirely dependent on living plant cells. The molecular basis of this life-style, obligate biotrophy, remains unknown. We present the genome analysis of barley powdery mildew, Blumeria graminis f.sp. hordei (Blumeria), as well as a comparison with the analysis of two powdery mildews pathogenic on dicotyledonous plants. These genomes display massive retrotransposon proliferation, genome-size expansion, and gene losses. The missing genes encode enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, probably reflecting their redundancy in an exclusively biotrophic life-style. Among the 248 candidate effectors of pathogenesis identified in the Blumeria genome, very few (less than 10) define a core set conserved in all three mildews, suggesting thatmost effectors represent species-specific adaptations.",

author = "Spanu, {Pietro D.} and Abbott, {James C.} and Joelle Amselem and Burgis, {Timothy A.} and Soanes, {Darren M.} and Kurt St{\"u}ber and Themaat, {Emiel Ver Loren van} and Brown, {James K.M.} and Butcher, {Sarah A.} and Gurr, {Sarah J.} and Marc-Henri Lebrun and Ridout, {Christopher J.} and Paul Schulze-Lefert and Talbot, {Nicholas J.} and Nahal Ahmadinejad and Christian Ametz and Barton, {Geraint R.} and Mariam Benjdia and Przemyslaw Bidzinski and Bindschedler, {Laurence V.} and Maike Both and Brewer, {Marin T.} and Lance Cadle-Davidson and Cadle-Davidson, {Molly M.} and Jerome Collemare and Rainer Cramer and Omer Frenkel and Dale Godfrey and James Harriman and Claire Hoede and King, {Brian C.} and Sven Klages and Jochen Kleemann and Daniela Knoll and Koti, {Prasanna S.} and Jonathan Kreplak and L{\'o}pez-Ruiz, {Francisco J.} and Xunli Lu and Takaki Maekawa and Siraprapa Mahanil and Cristina Micali and Milgroom, {Michael G.} and Giovanni Montana and Sandra Noir and O'Connell, {Richard J.} and Simone Oberhaensli and Francis Parlange and Carsten Pedersen and Hadi Quesneville and Richard Reinhardt and Matthias Rott and Soledad Sacrist{\'a}n and Schmidt, {Sarah M.} and Moritz Sch{\"o}n and Pari Skamnioti and Hans Sommer and Amber Stephens and Hiroyuki Takahara and Hans Thordal-Christensen and Marielle Vigouroux and Ralf We{\ss}ling and Thomas Wicker and Ralph Panstruga",

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doi = "10.1126/science.1194573",

language = "English",

volume = "330",

pages = "1543--1546 ",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6010",

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TY - JOUR

T1 - Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism

AU - Spanu, Pietro D.

AU - Abbott, James C.

AU - Amselem, Joelle

AU - Burgis, Timothy A.

AU - Soanes, Darren M.

AU - Stüber, Kurt

AU - Themaat, Emiel Ver Loren van

AU - Brown , James K.M.

AU - Butcher, Sarah A.

AU - Gurr, Sarah J.

AU - Lebrun, Marc-Henri

AU - Ridout, Christopher J.

AU - Schulze-Lefert, Paul

AU - Talbot, Nicholas J.

AU - Ahmadinejad, Nahal

AU - Ametz, Christian

AU - Barton, Geraint R.

AU - Benjdia, Mariam

AU - Bidzinski, Przemyslaw

AU - Bindschedler, Laurence V.

AU - Both, Maike

AU - Brewer, Marin T.

AU - Cadle-Davidson, Lance

AU - Cadle-Davidson, Molly M.

AU - Collemare, Jerome

AU - Cramer, Rainer

AU - Frenkel, Omer

AU - Godfrey, Dale

AU - Harriman, James

AU - Hoede, Claire

AU - King, Brian C.

AU - Klages, Sven

AU - Kleemann, Jochen

AU - Knoll, Daniela

AU - Koti, Prasanna S.

AU - Kreplak, Jonathan

AU - López-Ruiz, Francisco J.

AU - Lu, Xunli

AU - Maekawa, Takaki

AU - Mahanil, Siraprapa

AU - Micali, Cristina

AU - Milgroom, Michael G.

AU - Montana, Giovanni

AU - Noir, Sandra

AU - O'Connell, Richard J.

AU - Oberhaensli, Simone

AU - Parlange, Francis

AU - Pedersen, Carsten

AU - Quesneville, Hadi

AU - Reinhardt, Richard

AU - Rott, Matthias

AU - Sacristán, Soledad

AU - Schmidt, Sarah M.

AU - Schön, Moritz

AU - Skamnioti, Pari

AU - Sommer, Hans

AU - Stephens, Amber

AU - Takahara, Hiroyuki

AU - Thordal-Christensen, Hans

AU - Vigouroux, Marielle

AU - Weßling, Ralf

AU - Wicker, Thomas

AU - Panstruga, Ralph

PY - 2010/12/10

Y1 - 2010/12/10

N2 - Powdery mildews are phytopathogens whose growth and reproduction are entirely dependent on living plant cells. The molecular basis of this life-style, obligate biotrophy, remains unknown. We present the genome analysis of barley powdery mildew, Blumeria graminis f.sp. hordei (Blumeria), as well as a comparison with the analysis of two powdery mildews pathogenic on dicotyledonous plants. These genomes display massive retrotransposon proliferation, genome-size expansion, and gene losses. The missing genes encode enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, probably reflecting their redundancy in an exclusively biotrophic life-style. Among the 248 candidate effectors of pathogenesis identified in the Blumeria genome, very few (less than 10) define a core set conserved in all three mildews, suggesting thatmost effectors represent species-specific adaptations.

AB - Powdery mildews are phytopathogens whose growth and reproduction are entirely dependent on living plant cells. The molecular basis of this life-style, obligate biotrophy, remains unknown. We present the genome analysis of barley powdery mildew, Blumeria graminis f.sp. hordei (Blumeria), as well as a comparison with the analysis of two powdery mildews pathogenic on dicotyledonous plants. These genomes display massive retrotransposon proliferation, genome-size expansion, and gene losses. The missing genes encode enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, probably reflecting their redundancy in an exclusively biotrophic life-style. Among the 248 candidate effectors of pathogenesis identified in the Blumeria genome, very few (less than 10) define a core set conserved in all three mildews, suggesting thatmost effectors represent species-specific adaptations.

U2 - 10.1126/science.1194573

DO - 10.1126/science.1194573

M3 - Journal article

C2 - 21148392

SN - 0036-8075

VL - 330

SP - 1543

EP - 1546

JO - Science

JF - Science

IS - 6010

ER -

Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism

Abstract

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