Codon optimization underpins generalist parasitism in fungi

Abstract
Data availability
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Abstract

The range of hosts that parasites can infect is a key determinant of the emergence and spread of disease. Yet the impact of host range variation on the evolution of parasite genomes remains unknown. Here, we show that codon optimization underlies genome adaptation in broad host range parasite. We found that the longer proteins encoded by broad host range fungi likely increase natural selection on codon optimization in these species. Accordingly, codon optimization correlates with host range across the fungal kingdom. At the species level, biased patterns of synonymous substitutions underpin increased codon optimization in a generalist but not a specialist fungal pathogen. Virulence genes were consistently enriched in highly codon-optimized genes of generalist but not specialist species. We conclude that codon optimization is related to the capacity of parasites to colonize multiple hosts. Our results link genome evolution and translational regulation to the long term persistence of generalist parasitism.

Data availability

The following data sets were generated

(2016) Sclerotinia sclerotiorum isolates genome sequence
Publicly available at the NCBI BioProject (accession no: PRJNA342788).

https://www.ncbi.nlm.nih.gov/bioproject/342788

The following previously published data sets were used

1. James TY
2. Pelin A
3. Bonen L
4. Ahrendt S
5. Sain D
6. Corradi N
7. Stajich JE
(2013) Rozella allomycis genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Rozal1_1/Rozal1_1.download.html
1. Ma LJ
2. Ibrahim AS
3. Skory C
4. Grabherr MG
5. Burger G
6. Butler M
7. Elias M
8. Idnurm A
9. Lang BF
10. Sone T
11. Abe A
12. Calvo SE
13. Corrochano LM
14. Engels R
15. Fu J
16. Hansberg W
17. Kim JM
18. Kodira CD
19. Koehrsen MJ
20. Liu B
21. Miranda-Saavedra D
22. O'Leary S
23. Ortiz-Castellanos L
24. Poulter R
25. Rodriguez-Romero J
26. Ruiz-Herrera J
27. Shen YQ
28. Zeng Q
29. Galagan J
30. Birren BW
31. Cuomo CA
32. Wickes BL
(2009) Rhizopus oryzae genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Rhior3/Rhior3.home.html
1. Cornman RS
2. Chen YP
3. Schatz MC
4. Street C
5. Zhao Y
6. Desany B
7. Egholm M
8. Hutchison S
9. Pettis JS
10. Lipkin WI
11. Evans JD
(2009) Nosema ceranae genome sequence
Publicly available at the EBI European Nucleotide Archive (accession no: GCA_000988165.1).

http://www.ebi.ac.uk/ena/data/view/GCA_000988165.1
(2010) Encephalitozoon intestinalis genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Encin1
1. Batrachochytrium dendrobatidis Sequencing Project
2. Broad Institute of Harvard and MIT
(2016) Batrachochytrium dendrobatidis genome sequence
Publicly available at www.broadinstitute.org.

https://www.broadinstitute.org/annotation/genome/batrachochytrium_dendrobatidis/MultiDownloads.html
1. Chang Y
2. Wang S
3. Sekimoto S
4. Aerts AL
5. Choi C
6. Clum A
7. LaButti KM
8. Lindquist EA
9. Yee Ngan C
10. Ohm RA
11. Salamov AA
12. Grigoriev IV
13. Spatafora JW
14. Berbee ML
(2015) Gonapodya prolifera genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Ganpr1/Ganpr1.download.html
(2010) Sporisorium reilianum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Spore1
1. Zhu Z
2. Zhang S
3. Liu H
4. Shen H
5. Lin X
6. Yang F
7. Zhou YJ
8. Jin G
9. Ye M
10. Zou H
11. Zhao ZK
(2012) Rhodotorula toruloides genome sequence
Publicly available at genome.jgi.doe.gov.

https://cdn.elifesciences.org/articles/22472/ttp://genome.jgi.doe.gov/Rhoto1/Rhoto1.home.html
1. Duplessis S
2. Cuomo CA
3. Lin YC
4. Aerts A
5. Tisserant E
6. Veneault-Fourrey C
7. Joly DL
8. Hacquard S
9. Amselem J
10. Cantarel BL
11. Chiu R
12. Coutinho PM
13. Feau N
14. Field M
15. Frey P
16. Gelhaye E
17. Goldberg J
18. Grabherr MG
19. Kodira CD
20. Kohler A
21. KÃ1/4es U
22. Lindquist EA
23. Lucas SM
24. Mago R
25. Mauceli E
26. Morin E
27. Murat C
28. Pangilinan JL
29. Park R
30. Pearson M
31. Quesneville H
32. Rouhier N
33. Sakthikumar S
34. Salamov AA
35. Schmutz J
36. Selles B
37. Shapiro H
38. Tanguay P
39. Tuskan GA
40. Henrissat B
41. Van de Peer Y
42. RouzÃ{copyright
43. serif} P
44. Ellis JG
45. Dodds PN
46. Schein JE
47. Zhong S
48. Hamelin RC
49. Grigoriev IV
50. Szabo LJ
51. Martin F.
(2011) Melampsora larici-populina genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Mellp2_3
1. Puccinia Group Sequencing Project
2. Broad Institute of Harvard and MIT
(2016) Puccinia triticina genome sequence
Publicly available at www.broadinstitute.org.

https://www.broadinstitute.org/annotation/genome/puccinia_group/MultiDownloads.html
1. Duplessis S
2. Cuomo CA
3. Lin YC
4. Aerts A
5. Tisserant E
6. Veneault-Fourrey C
7. Joly DL
8. Hacquard S
9. Amselem J
10. Cantarel BL
11. Chiu R
12. Coutinho PM
13. Feau N
14. Field M
15. Frey P
16. Gelhaye E
17. Goldberg J
18. Grabherr MG
19. Kodira CD
20. Kohler A
21. KÃ1/4es U
22. Lindquist EA
23. Lucas SM
24. Mago R
25. Mauceli E
26. Morin E
27. Murat C
28. Pangilinan JL
29. Park R
30. Pearson M
31. Quesneville H
32. Rouhier N
33. Sakthikumar S
34. Salamov AA
35. Schmutz J
36. Selles B
37. Shapiro H
38. Tanguay P
39. Tuskan GA
40. Henrissat B
41. Van de Peer Y
42. RouzÃ{copyright
43. serif} P
44. Ellis JG
45. Dodds PN
46. Schein JE
47. Zhong S
48. Hamelin RC
49. Grigoriev IV
50. Szabo LJ
51. Martin F
(2011) Puccinia graminis genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Pucgr2
1. Loftus BJ
2. Fung E
3. Roncaglia P
4. Rowley D
5. Amedeo P
6. Bruno D
7. Vamathevan J
8. Miranda M
9. Anderson IJ
10. Fraser JA
11. Allen JE
12. Bosdet IE
13. Brent MR
14. Chiu R
15. Doering TL
16. Donlin MJ
17. D'Souza CA
18. Fox DS
19. Grinberg V
20. Fu J
21. Fukushima M
22. Haas BJ
23. Huang JC
24. Janbon G
25. Jones SJ
26. Koo HL
27. Krzywinski MI
28. Kwon-Chung JK
29. Lengeler KB
30. Maiti R
31. Marra MA
32. Marra RE
33. Mathewson CA
34. Mitchell TG
35. Pertea M
36. Riggs FR
37. Salzberg SL
38. Schein JE
39. Shvartsbeyn A
40. Shin H
41. Shumway M
42. Specht CA
43. Suh BB
44. Tenney A
45. Utterback TR
46. Wickes BL
47. Wortman JR
48. Wye NH
49. Kronstad JW
50. Lodge JK
51. Heitman J
52. Davis RW
53. Fraser CM
54. Hyman RW
(2005) Cryptococcus neoformans genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Cryne_JEC21_1/Cryne_JEC21_1.download.html
1. Floudas D
2. Binder M
3. Riley R
4. Barry K
5. Blanchette RA
6. Henrissat B
7. Martinez AT
8. Otillar R
9. Spatafora JW
10. Yadav JS
11. Aerts A
12. Benoit I
13. Boyd A
14. Carlson A
15. Copeland A
16. Coutinho PM
17. de Vries RP
18. Ferreira P
19. Findley K
20. Foster B
21. Gaskell J
22. Glotzer D
23. Gorecki P
24. Heitman J
25. Hesse C
26. Hori C
27. Igarashi K
28. Jurgens JA
29. Kallen N
30. Kersten P
31. Kohler A
32. Kues U
33. Kumar TK
34. Kuo A
35. LaButti K
36. Larrondo LF
37. Lindquist E
38. Ling A
39. Lombard V
40. Lucas S
41. Lundell T
42. Martin R
43. McLaughlin DJ
44. Morgenstern I
45. Morin E
46. Murat C
47. Nagy LG
48. Nolan M
49. Ohm RA
50. Patyshakuliyeva A
51. Rokas A
52. Ruiz-Duenas FJ
53. Sabat G
54. Salamov A
55. Samejima M
56. Schmutz J
57. Slot JC
58. St John F
59. Stenlid J
60. Sun H
61. Sun S
62. Syed K
63. Tsang A
64. Wiebenga A
65. Young D
66. Pisabarro A
67. Eastwood DC
68. Martin F
69. Cullen D
70. Grigoriev IV
71. Hibbett DS.
(2012) Wolfiporia cocos genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi-psf.org/Wolco1/Wolco1.home.html
1. Cubeta MA
2. Thomas E
3. Dean RA
4. Jabaji S
5. Neate SM
6. Tavantzis S
7. Toda T
8. Vilgalys R
9. Bharathan N
10. Fedorova-Abrams N
11. Pakala SB
12. Pakala SM
13. Zafar N
14. Joardar V
15. Losada L
16. Nierman WC.
(2014) Rhizoctonia solani genome sequence
Publicly available at the EBI European Nucleotide Archive (accession no:GCA_000524645.1).

http://www.ebi.ac.uk/ena/data/view/GCA_000524645.1
1. Eastwood DC
2. Floudas D
3. Binder M
4. Majcherczyk A
5. Schneider P
6. Aerts A
7. Asiegbu FO
8. Baker SE
9. Barry K
10. Bendiksby M
11. Blumentritt M
12. Coutinho PM
13. Cullen D
14. de Vries RP
15. Gathman A
16. Goodell B
17. Henrissat B
18. Ihrmark K
19. Kauserud H
20. Kohler A
21. LaButti K
22. Lapidus A
23. Lavin JL
24. Lee YH
25. Lindquist E
26. Lilly W
27. Lucas S
28. Morin E
29. Murat C
30. Oguiza JA
31. Park J
32. Pisabarro AG
33. Riley R
34. Rosling A
35. Salamov A
36. Schmidt O
37. Schmutz J
38. Skrede I
39. Stenlid J
40. Wiebenga A
41. Xie X
42. Kues U
43. Hibbett DS
44. Hoffmeister D
45. Hogberg N
46. Martin F
47. Grigoriev IV
48. Watkinson SC
(2011) Serpula lacrymans genome sequence
Publicly available at genome.jgi-psf.org.

http://genome.jgi-psf.org/SerlaS7_9_2/SerlaS7_9_2.home.html
1. Meinhardt LW
2. Costa GG
3. Thomazella DP
4. Teixeira PJ
5. Carazzolle MF
6. Schuster SC
7. Carlson JE
8. Guiltinan MJ
9. Mieczkowski P
10. Farmer A
11. Ramaraj T
12. Crozier J
13. Davis RE
14. Shao J
15. Melnick RL
16. Pereira GA
17. Bailey BA
(2014) Moniliophthora roreri genome sequence
Publicly available at www.ncbi.nlm.nih.gov.elis.tmu.edu.tw.

ftp://ftp.ncbi.nlm.nih.gov/genomes/all/GCA/000/488/995/GCA_000488995.1_M_roreri_MCA_2997_v1/
1. Martin F
2. Aerts A
3. AhrÃ{copyright
4. serif}n D
5. Brun A
6. Danchin EG
7. Duchaussoy F
8. Gibon J
9. Kohler A
10. Lindquist E
11. Pereda V
12. Salamov A
13. Shapiro HJ
14. Wuyts J
15. Blaudez D
16. BuÃ{copyright
17. serif}e M
18. Brokstein P
19. CanbÃ¤ck B
20. Cohen D
21. Courty PE
22. Coutinho PM
23. Delaruelle C
24. Detter JC
25. Deveau A
26. DiFazio S
27. Duplessis S
28. Fraissinet-Tachet L
29. Lucic E
30. Frey-Klett P
31. Fourrey C
32. Feussner I
33. Gay G
34. Grimwood J
35. Hoegger PJ
36. Jain P
37. Kilaru S
38. LabbÃ{copyright
39. serif} J
40. Lin YC
41. LeguÃ{copyright
42. serif} V
43. Le Tacon F
44. Marmeisse R
45. Melayah D
46. Montanini B
47. Muratet M
48. Nehls U
49. Niculita-Hirzel H
50. Oudot-Le Secq MP
51. Peter M
52. Quesneville H
53. Rajashekar B
54. Reich M
55. Rouhier N
56. Schmutz J
57. Yin T
58. Chalot M
59. Henrissat B
60. KÃ1/4es U
61. Lucas S
62. Van de Peer Y
63. Podila GK
64. Polle A
65. Pukkila PJ
66. Richardson PM
67. RouzÃ{copyright
68. serif} P
69. Sanders IR
70. Stajich JE
71. Tunlid A
72. Tuskan G
73. Grigoriev IV
(2008) Laccaria bicolor genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Lacbi2
1. Morin E
2. Kohler A
3. Baker AR
4. Foulongne-Oriol M
5. Lombard V
6. Nagy LG
7. Ohm RA
8. Patyshakuliyeva A
9. Brun A
10. Aerts AL
11. Bailey AM
12. Billette C
13. Coutinho PM
14. Deakin G
15. Doddapaneni H
16. Floudas D
17. Grimwood J
18. Hilden K
19. Kues U
20. Labutti KM
21. Lapidus A
22. Lindquist EA
23. Lucas SM
24. Murat C
25. Riley RW
26. Salamov AA
27. Schmutz J
28. Subramanian V
29. Wosten HA
30. Xu J
31. Eastwood DC
32. Foster GD
33. Sonnenberg AS
34. Cullen D
35. de Vries RP
36. Lundell T
37. Hibbett DS
38. Henrissat B
39. Burton KS
40. Kerrigan RW
41. Challen MP
42. Grigoriev IV
43. Martin F
(2012) Agaricus bisporus genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Agabi_varbisH97_2/Agabi_varbisH97_2.download.html
(2013) Taphrina deformans genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Tapde1_1
1. Martin F
2. Aerts A
3. AhrÃ{copyright
4. serif}n D
5. Brun A
6. Danchin EG
7. Duchaussoy F
8. Gibon J
9. Kohler A
10. Lindquist E
11. Pereda V
12. Salamov A
13. Shapiro HJ
14. Wuyts J
15. Blaudez D
16. BuÃ{copyright
17. serif}e M
18. Brokstein P
19. CanbÃ¤ck B
20. Cohen D
21. Courty PE
22. Coutinho PM
23. Delaruelle C
24. Detter JC
25. Deveau A
26. DiFazio S
27. Duplessis S
28. Fraissinet-Tachet L
29. Lucic E
30. Frey-Klett P
31. Fourrey C
32. Feussner I
33. Gay G
34. Grimwood J
35. Hoegger PJ
36. Jain P
37. Kilaru S
38. LabbÃ{copyright
39. serif} J
40. Lin YC
41. LeguÃ{copyright
42. serif} V
43. Le Tacon F
44. Marmeisse R
45. Melayah D
46. Montanini B
47. Muratet M
48. Nehls U
49. Niculita-Hirzel H
50. Oudot-Le Secq MP
51. Peter M
52. Quesneville H
53. Rajashekar B
54. Reich M
55. Rouhier N
56. Schmutz J
57. Yin T
58. Chalot M
59. Henrissat B
60. KÃ1/4es U
61. Lucas S
62. Van de Peer Y
63. Podila GK
64. Polle A
65. Pukkila PJ
66. Richardson PM
67. RouzÃ{copyright
68. serif} P
69. Sanders IR
70. Stajich JE
71. Tunlid A
72. Tuskan G
73. Grigoriev IV
(2008) Tuber melanosporum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Tubme1
(2012) Penicillium digitatum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Tubme1
1. Nierman WC
2. Pain A
3. Anderson MJ
4. Wortman JR
5. Kim HS
6. Arroyo J
7. Berriman M
8. Abe K
9. Archer DB
10. Bermejo C
11. Bennett J
12. Bowyer P
13. Chen D
14. Collins M
15. Coulsen R
16. Davies R
17. Dyer PS
18. Farman M
19. Fedorova N
20. Fedorova N
21. Feldblyum TV
22. Fischer R
23. Fosker N
24. Fraser A
25. Garcia JL
26. Garcia MJ
27. Goble A
28. Goldman GH
29. Gomi K
30. Griffith-Jones S
31. Gwilliam R
32. Haas B
33. Haas H
34. Harris D
35. Horiuchi H
36. Huang J
37. Humphray S
38. Jimenez J
39. Keller N
40. Khouri H
41. Kitamoto K
42. Kobayashi T
43. Konzack S
44. Kulkarni R
45. Kumagai T
46. Lafon A
47. Latge JP
48. Li W
49. Lord A
50. Lu C
51. Majoros WH
52. May GS
53. Miller BL
54. Mohamoud Y
55. Molina M
56. Monod M
57. Mouyna I
58. Mulligan S
59. Murphy L
60. O'Neil S
61. Paulsen I
62. Penalva MA
63. Pertea M
64. Price C
65. Pritchard BL
66. Quail MA
67. Rabbinowitsch E
68. Rawlins N
69. Rajandream MA
70. Reichard U
71. Renauld H
72. Robson GD
73. Rodriguez de Cordoba S
74. Rodriguez-Pena JM
75. Ronning CM
76. Rutter S
77. Salzberg SL
78. Sanchez M
79. Sanchez-Ferrero JC
80. Saunders D
81. Seeger K
82. Squares R
83. Squares S
84. Takeuchi M
85. Tekaia F
86. Turner G
87. Vazquez de Aldana CR
88. Weidman J
89. White O
90. Woodward J
91. Yu JH
92. Fraser C
93. Galagan JE
94. Asai K
95. Machida M
96. Hall N
97. Barrell B
98. Denning DW
(2005) Aspergillus fumigatus genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Aspfu1/Aspfu1.home.html
1. Hane JK
2. Lowe RG
3. Solomon PS
4. Tan KC
5. Schoch CL
6. Spatafora JW
7. Crous PW
8. Kodira C
9. Birren BW
10. Galagan JE
11. Torriani SF
12. McDonald BA
13. Oliver RP
(2007) Stagonospora nodorum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Stano2
1. Ohm RA
2. Feau N
3. Henrissat B
4. Schoch CL
5. Horwitz BA
6. Barry KW
7. Condon BJ
8. Copeland AC
9. Dhillon B
10. Glaser F
11. Hesse CN
12. Kosti I
13. LaButti K
14. Lindquist EA
15. Lucas S
16. Salamov AA
17. Bradshaw RE
18. Ciuffetti L
19. Hamelin RC
20. Kema GH
21. Lawrence C
22. Scott JA
23. Spatafora JW
24. Turgeon BG
25. de Wit PJ
26. Zhong S
27. Goodwin SB
28. Grigoriev IV
(2012) Alternaria brassicicola genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Altbr1/Altbr1.download.html
1. Manning VA
2. Pandelova I
3. Dhillon B
4. Wilhelm LJ
5. Goodwin SB
6. Berlin AM
7. Figueroa M
8. Freitag M
9. Hane JK
10. Henrissat B
11. Holman WH
12. Kodira CD
13. Martin J
14. Oliver RP
15. Robbertse B
16. Schackwitz W
17. Schwartz DC
18. Spatafora JW
19. Turgeon BG
20. Yandava C
21. Young S
22. Zhou S
23. Zeng Q
24. Grigoriev IV
25. Ma LJ
26. Ciuffetti LM
(2013) Pyrenophora tritici-repentis genome sequence
Publicly available at genome.jgi.doe.gov.

http://www.broadinstitute.org/annotation/genome/pyrenophora_tritici_repentis
1. de Wit PJ
2. van der Burgt A
3. Okmen B
4. Stergiopoulos I
5. Abd-Elsalam KA
6. Aerts AL
7. Bahkali AH
8. Beenen HG
9. Chettri P
10. Cox MP
11. Datema E
12. de Vries RP
13. Dhillon B
14. Ganley AR
15. Griffiths SA
16. Guo Y
17. Hamelin RC
18. Henrissat B
19. Kabir MS
20. Jashni MK
21. Kema G
22. Klaubauf S
23. Lapidus A
24. Levasseur A
25. Lindquist E
26. Mehrabi R
27. Ohm RA
28. Owen TJ
29. Salamov A
30. Schwelm A
31. Schijlen E
32. Sun H
33. van den Burg HA
34. van Ham RC
35. Zhang S
36. Goodwin SB
37. Grigoriev IV
38. Collemare J
39. Bradshaw RE
(2012) Dothistroma septosporum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Dotse1/Dotse1.home.html
1. Ohm RA
2. Feau N
3. Henrissat B
4. Schoch CL
5. Horwitz BA
6. Barry KW
7. Condon BJ
8. Copeland AC
9. Dhillon B
10. Glaser F
11. Hesse CN
12. Kosti I
13. LaButti K
14. Lindquist EA
15. Lucas S
16. Salamov AA
17. Bradshaw RE
18. Ciuffetti L
19. Hamelin RC
20. Kema GH
21. Lawrence C
22. Scott JA
23. Spatafora JW
24. Turgeon BG
25. de Wit PJ
26. Zhong S
27. Goodwin SB
28. Grigoriev IV
(2012) Pseudocercospora fijiensis genome sequence
Publicly available at ftp.ncbi.nlm.nih.gov.

ftp://ftp.ncbi.nlm.nih.gov/genomes/all/GCA/000/340/215/GCA_000340215.1_Mycfi2/
1. Goodwin SB
2. M'barek SB
3. Dhillon B
4. Wittenberg AH
5. Crane CF
6. Hane JK
7. Foster AJ
8. Van der Lee TA
9. Grimwood J
10. Aerts A
11. Antoniw J
12. Bailey A
13. Bluhm B
14. Bowler J
15. Bristow J
16. van der Burgt A
17. Canto-Canche B
18. Churchill AC
19. Conde-Ferraez L
20. Cools HJ
21. Coutinho PM
22. Csukai M
23. Dehal P
24. De Wit P
25. Donzelli B
26. van de Geest HC
27. van Ham RC
28. Hammond-Kosack KE
29. Henrissat B
30. Kilian A
31. Kobayashi AK
32. Koopmann E
33. Kourmpetis Y
34. Kuzniar A
35. Lindquist E
36. Lombard V
37. Maliepaard C
38. Martins N
39. Mehrabi R
40. Nap JP
41. Ponomarenko A
42. Rudd JJ
43. Salamov A
44. Schmutz J
45. Schouten HJ
46. Shapiro H
47. Stergiopoulos I
48. Torriani SF
49. Tu H
50. de Vries RP
51. Waalwijk C
52. Ware SB
53. Wiebenga A
54. Zwiers LH
55. Oliver RP
56. Grigoriev IV
57. Kema GH
(2011) Zymoseptoria tritici genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Mycgr3/Mycgr3.home.html
1. de Wit PJ
2. van der Burgt A
3. Okmen B
4. Stergiopoulos I
5. Abd-Elsalam KA
6. Aerts AL
7. Bahkali AH
8. Beenen HG
9. Chettri P
10. Cox MP
11. Datema E
12. de Vries RP
13. Dhillon B
14. Ganley AR
15. Griffiths SA
16. Guo Y
17. Hamelin RC
18. Henrissat B
19. Kabir MS
20. Jashni MK
21. Kema G
22. Klaubauf S
23. Lapidus A
24. Levasseur A
25. Lindquist E
26. Mehrabi R
27. Ohm RA
28. Owen TJ
29. Salamov A
30. Schwelm A
31. Schijlen E
32. Sun H
33. van den Burg HA
34. van Ham RC
35. Zhang S
36. Goodwin SB
37. Grigoriev IV
38. Collemare J
39. Bradshaw RE
(2012) Passalora fulva genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Clafu1
1. Spanu PD
2. Abbott JC
3. Amselem J
4. Burgis TA
5. Soanes DM
6. StÃ1/4ber K
7. Ver Loren van Themaat E
8. Brown JK
9. Butcher SA
10. Gurr SJ
11. Lebrun MH
12. Ridout CJ
13. Schulze-Lefert P
14. Talbot NJ
15. Ahmadinejad N
16. Ametz C
17. Barton GR
18. Benjdia M
19. Bidzinski P
20. Bindschedler LV
21. Both M
22. Brewer MT
23. Cadle-Davidson L
24. Cadle-Davidson MM
25. Collemare J
26. Cramer R
27. Frenkel O
28. Godfrey D
29. Harriman J
30. Hoede C
31. King BC
32. Klages S
33. Kleemann J
34. Knoll D
35. Koti PS
36. Kreplak J
37. LÃ³pez-Ruiz FJ
38. Lu X
39. Maekawa T
40. Mahanil S
41. Micali C
42. Milgroom MG
43. Montana G
44. Noir S
45. O'Connell RJ
46. Oberhaensli S
47. Parlange F
48. Pedersen C
49. Quesneville H
50. Reinhardt R
51. Rott M
52. SacristÃ¡n S
53. Schmidt SM
54. SchÃ¶n M
55. Skamnioti P
56. Sommer H
57. Stephens A
58. Takahara H
59. Thordal-Christensen H
60. Vigouroux M
61. Wessling R
62. Wicker T
63. Panstruga R
(2010) Blumeria graminis genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Blugr1
1. Jones L
2. Riaz S
3. Morales-Cruz A
4. Amrine KC
5. McGuire B
6. Gubler WD
7. Walker MA
8. Cantu D
(2014) Erysiphe necator genome sequence
Publicly available at www.ncbi.nlm.nih.gov.

http://www.ncbi.nlm.nih.gov/Traces/wgs/?val=JNVN01#contigs
1. van Kan JA
2. Stassen JH
3. Mosbach A
4. van der Lee TA
5. Faino L
6. Farmer AD
7. Papasotiriou D
8. Zhou S
9. Seidl MF
10. Cottam E
11. Edel D
12. Hahn M
13. Schwartz DC
14. Dietrich RA
15. Widdison S
16. Scalliet G
(2016) Botrytis cinerea genome sequence
Publicly available at fungi.ensembl.org.

http://fungi.ensembl.org/Botrytis_cinerea/Info/Index
1. Kohler A
2. Kuo A
3. Nagy LG
4. Morin E
5. Barry KW
6. Buscot F
7. Canback B
8. Choi C
9. Cichocki N
10. Clum A
11. Colpaert J
12. Copeland A
13. Costa MD
14. Dore J
15. Floudas D
16. Gay G
17. Girlanda M
18. Henrissat B
19. Herrmann S
20. Hess J
21. Hogberg N
22. Johansson T
23. Khouja HR
24. LaButti K
25. Lahrmann U
26. Levasseur A
27. Lindquist EA
28. Lipzen A
29. Marmeisse R
30. Martino E
31. Murat C
32. Ngan CY
33. Nehls U
34. Plett JM
35. Pringle A
36. Ohm RA
37. Perotto S
38. Peter M
39. Riley R
40. Rineau F
41. Ruytinx J
42. Salamov A
43. Shah F
44. Sun H
45. Tarkka M
46. Tritt A
47. Veneault-Fourrey C
48. Zuccaro A
49. Tunlid A
50. Grigoriev IV
51. Hibbett DS
52. Martin F
(2015) Oidiodendron maius genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Oidma1
1. Geomyces destructans Sequencing Project
2. Broad Institute of Harvard and MIT
(2016) Pseudogymnoascus destructans genome sequence
licly available at www.broadinstitute.org.

http://www.broadinstitute.org/annotation/genome/Geomyces_destructans/MultiHome.html
1. Dean RA
2. Talbot NJ
3. Ebbole DJ
4. Farman ML
5. Mitchell TK
6. Orbach MJ
7. Thon M
8. Kulkarni R
9. Xu JR
10. Pan H
11. Read ND
12. Lee YH
13. Carbone I
14. Brown D
15. Oh YY
16. Donofrio N
17. Jeong JS
18. Soanes DM
19. Djonovic S
20. Kolomiets E
21. Rehmeyer C
22. Li W
23. Harding M
24. Kim S
25. Lebrun MH
26. Bohnert H
27. Coughlan S
28. Butler J
29. Calvo S
30. Ma LJ
31. Nicol R
32. Purcell S
33. Nusbaum C
34. Galagan JE
35. Birren BW
(2005) Magnaporthe oryzae genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Maggr1
1. Berka RM
2. Grigoriev IV
3. Otillar R
4. Salamov A
5. Grimwood J
6. Reid I
7. Ishmael N
8. John T
9. Darmond C
10. Moisan MC
11. Henrissat B
12. Coutinho PM
13. Lombard V
14. Natvig DO
15. Lindquist E
16. Schmutz J
17. Lucas S
18. Harris P
19. Powlowski J
20. Bellemare A
21. Taylor D
22. Butler G
23. de Vries RP
24. Allijn IE
25. van den Brink J
26. Ushinsky S
27. Storms R
28. Powell AJ
29. Paulsen IT
30. Elbourne LD
31. Baker SE
32. Magnuson J
33. Laboissiere S
34. Clutterbuck AJ
35. Martinez D
36. Wogulis M
37. de Leon AL
38. Rey MW
39. Tsang A
(2011) Myceliophthora thermophila genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Spoth2/Spoth2.download.html
1. Berka RM
2. Grigoriev IV
3. Otillar R
4. Salamov A
5. Grimwood J
6. Reid I
7. Ishmael N
8. John T
9. Darmond C
10. Moisan MC
11. Henrissat B
12. Coutinho PM
13. Lombard V
14. Natvig DO
15. Lindquist E
16. Schmutz J
17. Lucas S
18. Harris P
19. Powlowski J
20. Bellemare A
21. Taylor D
22. Butler G
23. de Vries RP
24. Allijn IE
25. van den Brink J
26. Ushinsky S
27. Storms R
28. Powell AJ
29. Paulsen IT
30. Elbourne LD
31. Baker SE
32. Magnuson J
33. Laboissiere S
34. Clutterbuck AJ
35. Martinez D
36. Wogulis M
37. de Leon AL
38. Rey MW
39. Tsang A
(2011) Chaetomium globosum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Chagl_1
(2015) Verticilium dahliae genome sequence
Publicly available at www.ncbi.nlm.nih.gov.

http://www.ncbi.nlm.nih.gov/genome/?term=GCA_000952015.1
1. O'Connell RJ
2. Thon MR
3. Hacquard S
4. Amyotte SG
5. Kleemann J
6. Torres MF
7. Damm U
8. Buiate EA
9. Epstein L
10. Alkan N
11. Altmuller J
12. Alvarado-Balderrama L
13. Bauser CA
14. Becker C
15. Birren BW
16. Chen Z
17. Choi J
18. Crouch JA
19. Duvick JP
20. Farman MA
21. Gan P
22. Heiman D
23. Henrissat B
24. Howard RJ
25. Kabbage M
26. Koch C
27. Kracher B
28. Kubo Y
29. Law AD
30. Lebrun MH
31. Lee YH
32. Miyara I
33. Moore N
34. Neumann U
35. Nordstrom K
36. Panaccione DG
37. Panstruga R
38. Place M
39. Proctor RH
40. Prusky D
41. Rech G
42. Reinhardt R
43. Rollins JA
44. Rounsley S
45. Schardl CL
46. Schwartz DC
47. Shenoy N
48. Shirasu K
49. Sikhakolli UR
50. Stuber K
51. Sukno SA
52. Sweigard JA
53. Takano Y
54. Takahara H
55. Trail F
56. van der Does HC
57. Voll LM
58. Will I
59. Young S
60. Zeng Q
61. Zhang J
62. Zhou S
63. Dickman MB
64. Schulze-Lefert P
65. Ver Loren van Themaat E
66. Ma LJ
67. Vaillancourt LJ
(2012) Colletotrichum higginsianum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/Colhi1/Colhi1.home.html
1. Colletotrichum Sequencing Project
2. Broad Institute of Harvard and MIT
(2016) Colletotrichum graminicola genome sequence
Publicly available at www.broadinstitute.org.

http://www.broadinstitute.org/annotation/genome/colletotrichum_group/MultiHome.html
1. de Bekker C
2. Ohm RA
3. Loreto RG
4. Sebastian A
5. Albert I
6. Merrow M
7. Brachmann A
8. Hughes DP
(2015) Ophiocordyceps unilateralis genome sequence
Publicly available at www.ncbi.nlm.nih.gov.

http://www.ncbi.nlm.nih.gov/nuccore/LAZP00000000.1/
1. Xiao G
2. Ying SH
3. Zheng P
4. Wang ZL
5. Zhang S
6. Xie XQ
7. Shang Y
8. St Leger RJ
9. Zhao GP
10. Wang C
11. Feng MG
(2012) Beauveria bassiana genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Beaba1
1. Ma LJ
2. van der Does HC
3. Borkovich KA
4. Coleman JJ
5. Daboussi MJ
6. Di Pietro A
7. Dufresne M
8. Freitag M
9. Grabherr M
10. Henrissat B
11. Houterman PM
12. Kang S
13. Shim WB
14. Woloshuk C
15. Xie X
16. Xu JR
17. Antoniw J
18. Baker SE
19. Bluhm BH
20. Breakspear A
21. Brown DW
22. Butchko RA
23. Chapman S
24. Coulson R
25. Coutinho PM
26. Danchin EG
27. Diener A
28. Gale LR
29. Gardiner DM
30. Goff S
31. Hammond-Kosack KE
32. Hilburn K
33. Hua-Van A
34. Jonkers W
35. Kazan K
36. Kodira CD
37. Koehrsen M
38. Kumar L
39. Lee YH
40. Li L
41. Manners JM
42. Miranda-Saavedra D
43. Mukherjee M
44. Park G
45. Park J
46. Park SY
47. Proctor RH
48. Regev A
49. Ruiz-Roldan MC
50. Sain D
51. Sakthikumar S
52. Sykes S
53. Schwartz DC
54. Turgeon BG
55. Wapinski I
56. Yoder O
57. Young S
58. Zeng Q
59. Zhou S
60. Galagan J
61. Cuomo CA
62. Kistler HC
63. Rep M
(2010) Fusarium graminearum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Fusgr1
1. Gao Q
2. Jin K
3. Ying SH
4. Zhang Y
5. Xiao G
6. Shang Y
7. Duan Z
8. Hu X
9. Xie XQ
10. Zhou G
11. Peng G
12. Luo Z
13. Huang W
14. Wang B
15. Fang W
16. Wang S
17. Zhong Y
18. Ma LJ
19. Zhao GP
20. Pei Y
21. Feng MG
22. Xia Y
23. Wang C
(2011) Metarhizium acridum genome sequence
Publicly available at genome.jgi.doe.gov.

http://genome.jgi.doe.gov/pages/dynamicOrganismDownload.jsf?organism=Metac1
(2013) Zymoseptoria tritici variant call file
Publicly available at fungi.ensembl.org.

http://fungi.ensembl.org/Zymoseptoria_tritici/Info/Index
1. Amselem J
2. Cuomo CA
3. van Kan JA
4. Viaud M
5. Benito EP
6. Couloux A
7. Coutinho PM
8. de Vries RP
9. Dyer PS
10. Fillinger S
11. Fournier E
12. Gout L
13. Hahn M
14. Kohn L
15. Lapalu N
16. Plummer KM
17. Pradier JM
18. QuÃvillon E
19. Sharon A
20. Simon A
21. ten Have A
22. Tudzynski B
23. Tudzynski P
24. Wincker P
25. Andrew M
26. Beever RE
27. Benoit I
28. Bouzid O
29. Brault B
30. Chen Z
31. Choquer M
32. CollÃmare J
33. Cotton P
34. Danchin EG
35. Da Silva C
36. Gautier A
37. Giraud C
38. Giraud T
39. Gonzalez C
40. GÃldener U
41. Henrissat B
42. Howlett BJ
43. Kodira C
44. Kretschmer M
45. Lappartient A
46. Leroch M
47. Levis C
48. Mauceli E
49. NeuvÃglise C
50. Oeser B
51. Pearson M
52. Poulain J
53. Poussereau N
54. Quesneville H
55. Rascle C
56. Schumacher J
57. SÃgurens B
58. Sexton A
59. Silva E
60. Sirven C
61. Soanes DM
62. Talbot NJ
63. Templeton M
64. Yandava C
65. Yarden O
66. Zeng Q
67. Rollins JA
68. Lebrun MH
69. Dickman M
(2011) Gene expression data for Botrytis cinerea
Publicly available at urgi.versailles.inra.fr.

http://urgi.versailles.inra.fr/Data/Transcriptome
1. Farr DF
2. Rossman AY
(2016) List of hosts for fungal plant pathogens
Publicly available at nt.ars-grin.gov.

http://nt.ars-grin.gov/fungaldatabases/fungushost/FungusHost.cfm

Article and author information

Author details

Thomas Badet

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

Competing interests
The authors declare that no competing interests exist.
Remi Peyraud

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet Tolosan, France

Competing interests
The authors declare that no competing interests exist.
Malick Mbengue

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

Competing interests
The authors declare that no competing interests exist.
Olivier Navaud

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

Competing interests
The authors declare that no competing interests exist.
Mark Derbyshire

Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia

Competing interests
The authors declare that no competing interests exist.
Richard P Oliver

Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia

Competing interests
The authors declare that no competing interests exist.
Adelin Barbacci

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3156-272X
Sylvain Raffaele

Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

For correspondence
sylvain.raffaele@toulouse.inra.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2442-9632

Funding

European Research Council (ERC-StG 336808)

Thomas Badet
Remi Peyraud
Malick Mbengue
Olivier Navaud
Sylvain Raffaele

Labex TULIP (ANR-10-LABX-41; ANR-11-IDEX-0002-02)

Thomas Badet
Remi Peyraud
Malick Mbengue
Olivier Navaud
Adelin Barbacci
Sylvain Raffaele

Australian grains research and development corporation

Mark Derbyshire
Richard P Oliver

Curtin University of Technology

Mark Derbyshire
Richard P Oliver

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

Claus O Wilke, The University of Texas at Austin, United States

Version history

Received: October 18, 2016
Accepted: January 28, 2017
Accepted Manuscript published: February 3, 2017 (version 1)
Version of Record published: February 17, 2017 (version 2)
Version of Record updated: February 24, 2017 (version 3)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.