Mitochondrial copper and phosphate transporter specificity was defined early in the evolution of eukaryotes

Abstract
Data availability
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Abstract

The mitochondrial carrier family protein SLC25A3 transports both copper and phosphate in mammals yet in Saccharomyces cerevisiae the transport of these substrates is partitioned across two paralogs: PIC2 and MIR1. To understand the ancestral state of copper and phosphate transport in mitochondria, we explored the evolutionary relationships of PIC2 and MIR1 orthologs across the eukaryotic tree of life. Phylogenetic analyses revealed that PIC2-like and MIR1-like orthologs are present in all major eukaryotic supergroups, indicating an ancient gene duplication created these paralogs. To link this phylogenetic signal to protein function, we used structural modelling and site-directed mutagenesis to identify residues involved in copper and phosphate transport. Based on these analyses, we generated a L175A variant of mouse SLC25A3 that retains the ability to transport copper but not phosphate. This work highlights the utility of using an evolutionary framework to uncover amino acids involved in substrate recognition by mitochondrial carrier family proteins.

Data availability

All data generated or analyzed during this study are included in the manuscript, supplemental file, and available on GenBank.

The following previously published data sets were used

1. Abrahamsen
2. M.S.
3. Templeton
4. T.J.
5. Enomoto
6. S.
7. Abrahante
8. J.E.
9. Zhu
10. G.
11. Lancto
12. C.A.
13. Deng
14. M.
15. Liu
16. C.
17. Widmer
18. G.
19. Tzipori
20. S.
21. Buck
22. G.A.
23. Xu
24. P.
25. Bankier
26. A.T.
27. Dear
28. P.H.
29. Konfortov
30. B.A.
31. Spriggs
32. H.F.
33. Iyer
34. L.
35. Anantharaman
36. V.
37. Aravind
38. L. and Kapur
39. V.
(2004) ASM16534v1 - representative genome
GCA_000165345.1.

https://www.ncbi.nlm.nih.gov/assembly/GCF_000165345.1
1. Aury
2. J.-M.
3. Jaillon
4. O.
5. Duret
6. L.
7. Noel
8. B.
9. Jubin
10. C.
11. Porcel
12. B.M.
13. Segurens
14. B.
15. Daubin
16. V.
17. Anthouard
18. V.
19. Aiach
20. N.
21. Arnaiz
22. O.
23. Billaut
24. A.
25. Beisson
26. J.
27. Blanc
28. I.
29. Bouhouche
30. K.
31. Camara
32. F.
33. Duharcourt
34. S.
35. Guigo
36. R.
37. Gogendeau
38. D.
39. Katinka
40. M.
41. Keller
42. A.-M.
43. Kissmehl
44. R.
45. Klotz
46. C.
47. Koll
48. F.
49. Le Mouel
50. A.
51. Lepere
52. C.
53. Malinsky
54. S.
55. Nowacki
56. M.
57. Nowak
58. J.K.
59. Plattner
60. H.
61. Poulain
62. J.
63. Ruiz
64. F.
65. Serrano
66. V.
67. Zagulski
68. M.
69. Dessen
70. P.
71. Betermier
72. M.
73. Weissenbach
74. J.
75. Scarpelli
76. C.
77. Schachter
78. V.
79. Sperling
80. L.
81. Meyer
82. E.
83. Cohen
84. J. and Wincker
85. P.
(2006) ASM16542v1
GCA_000165425.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000165425.1
1. El-Sayed
2. N.
3. Caler
4. E.
5. Inman
6. J.
7. Amedeo
8. P.
9. Hass
10. B.
11. Wortman
12. J.
13. Gardner
14. M.
15. Fernandez-Robledo
16. J.A. and Vasta
17. G.R.
(2008) JCVI_PMG_1.0
GCA_000006405.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000006405.1
1. Plasmodium falciparum Genome Sequencing Consortium
(2016) GCA_000002765
GCA_000002765.5.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002765.5
1. Bidwell
2. S.
3. Michalis
4. H.M.
5. Zafar
6. N.
7. Joardar
8. V.
9. Miao
10. W.
11. Russ
12. C.
13. Eisen
14. J.
15. Wu
16. M.
17. Wu
18. D.
19. Nierman
20. W.
21. Orias
22. E.
23. Delcher
24. A.
25. Salzberg
26. S. and Coyne
27. R.
(2009) JCVI-TTA1-2.2
GCA_000189635.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000189635.1
1. Lorenzi
2. H.
3. Caler
4. E.
5. Galinsky
6. K.
7. Schobel
8. S. and Paulsen
9. I.
(2013) TGA4
GCA_000006565.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000006565.2
1. Clarke
2. M.
3. Lohan
4. A.J.
5. Liu
6. B.
7. Lagkouvardos
8. I.
9. Roy
10. S.
11. Zafar
12. N.
13. Bertelli
14. C.
15. Schilde
16. C.
17. Kianianmomeni
18. A.
19. Burglin
20. T.R.
21. Frech
22. C.
23. Turcotte
24. B.
25. Kopec
26. K.O.
27. Synnott
28. J.M.
29. Choo
30. C.
31. Paponov
32. I.
33. Finkler
34. A.
35. Soon Heng Tan
36. C.
37. Hutchins
38. A.P.
39. Weinmeier
40. T.
41. Rattei
42. T.
43. Chu
44. J.S.
45. Gimenez
46. G.
47. Irimia
48. M.
49. Rigden
50. D.J.
51. Fitzpatrick
52. D.A.
53. Lorenzo-Morales
54. J.
55. Bateman
56. A.
57. Chiu
58. C.H.
59. Tang
60. P.
61. Hegemann
62. P.
63. Fromm
64. H.
65. Raoult
66. D.
67. Greub
68. G.
69. Miranda-Saavedra
70. D.
71. Chen
72. N.
73. Nash
74. P.
75. Ginger
76. M.L.
77. Horn
78. M.
79. Schaap
80. P.
81. Caler
82. L. and Loftus
83. B.
(2013) Acastellanii.strNEFF v1
GCA_000313135.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000313135.1
1. The Dictyostelium discoideum Sequencing Consortium
(2005) Dictyostelium discoideum AX4
GCA_000004695.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000004695.1
1. The Broad Institute Genome Sequencing Platform
(2010) TheTra_May2010
GCA_000142905.1 .

https://www.ncbi.nlm.nih.gov/assembly/GCA_000142905.1
1. The Arabidopsis Information Resource (TAIR)
(2018) TAIR10.1
GCA_000001735.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000001735.2
1. Merchant
2. S.S.
3. Prochnik
4. S.E.
5. Vallon
6. O.
7. Harris
8. E.H.
9. Karpowicz
10. S.J.
11. Witman
12. G.B.
13. Terry
14. A.
15. Salamov
16. A.
17. Fritz-Laylin
18. L.K.
19. Marechal-Drouard
20. L.
21. Marshall
22. W.F.
23. Qu
24. L.H.
25. Nelson
26. D.R.
27. Sanderfoot
28. A.A.
29. Spalding
30. M.H.
31. Kapitonov
32. V.V.
33. Ren
34. Q.
35. Ferris
36. P.
37. Lindquist
38. E.
39. Shapiro
40. H.
41. Lucas
42. S.M.
43. Grimwood
44. J.
45. Schmutz
46. J.
47. Cardol
48. P.
49. Cerutti
50. H.
51. Chanfreau
52. G.
53. Chen
54. C.L.
55. Cognat
56. V.
57. Croft
58. M.T.
59. Dent
60. R.
61. Dutcher
62. S.
63. Fernandez
64. E.
65. Fukuzawa
66. H.
67. Gonzalez-Ballester
68. D.
69. Gonzalez-Halphen
70. D.
71. Hallmann
72. A.
73. Hanikenne
74. M.
75. Hippler
76. M.
77. Inwood
78. W.
79. Jabbari
80. K.
81. Kalanon
82. M.
83. Kuras
84. R.
85. Lefebvre
86. P.A.
87. Lemaire
88. S.D.
89. Lobanov
90. A.V.
91. Lohr
92. M.
93. Manuell
94. A.
95. Meier
96. I.
97. Mets
98. L.
99. Mittag
100. M.
101. Mittelmeier
102. T.
103. Moroney
104. J.V.
105. Moseley
106. J.
107. Napoli
108. C.
109. Nedelcu
110. A.M.
111. Niyogi
112. K.
113. Novoselov
114. S.V.
115. Paulsen
116. I.T.
117. Pazour
118. G.
119. Purton
120. S.
121. Ral
122. J.P.
123. Riano-Pachon
124. D.M.
125. Riekhof
126. W.
127. Rymarquis
128. L.
129. Schroda
130. M.
131. Stern
132. D.
133. Umen
134. J.
135. Willows
136. R.
137. Wilson
138. N.
139. Zimmer
140. S.L.
141. Allmer
142. J.
143. Balk
144. J.
145. Bisova
146. K.
147. Chen
148. C.J.
149. Elias
150. M.
151. Gendler
152. K.
153. Hauser
154. C.
155. Lamb
156. M.R.
157. Ledford
158. H.
159. Long
160. J.C.
161. Minagawa
162. J.
163. Page
164. M.D.
165. Pan
166. J.
167. Pootakham
168. W.
169. Roje
170. S.
171. Rose
172. A.
173. Stahlberg
174. E.
175. Terauchi
176. A.M.
177. Yang
178. P.
179. Ball
180. S.
181. Bowler
182. C.
183. Dieckmann
184. C.L.
185. Gladyshev
186. V.N.
187. Green
188. P.
189. Jorgensen
190. R.
191. Mayfield
192. S.
193. Mueller-Roeber
194. B.
195. Rajamani
196. S.
197. Sayre
198. R.T.
199. Brokstein
200. P.
201. Dubchak
202. I.
203. Goodstein
204. D.
205. Hornick
206. L.
207. Huang
208. Y.W.
209. Jhaveri
210. J.
211. Luo
212. Y.
213. Martinez
214. D.
215. Ngau
216. W.C.
217. Otillar
218. B.
219. Poliakov
220. A.
221. Porter
222. A.
223. Szajkowski
224. L.
225. Werner
226. G.
227. Zhou
228. K.
229. Grigoriev
230. I.V.
231. Rokhsar
232. D.S. and Grossman
233. A.R."
(2014) Chlamydomonas reinhardtii (green algae), v3.0
GCA_000002595.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002595.2
1. Micromonas genome consortium
(2009) ASM9098v2
GCA_000090985.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000090985.2
1. International Rice Genome Sequencing Project
(2009) The IRGSP pseudomolecules (Build 4.0)
GCF_000005425.2.

https://www.ncbi.nlm.nih.gov/assembly/GCF_000005425.2
1. S Douglas 1
2. S Zauner
3. M Fraunholz
4. M Beaton
5. S Penny
6. L T Deng
7. X Wu
8. M Reith
9. T Cavalier-Smith
10. U G Maier
(2001) ASM297v1
GCA_000002975.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002975.1
(2011) ASM272v2
GCA_000002725.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002725.2
1. "Fritz-Laylin
2. L.K.
3. Prochnik
4. S.E.
5. Ginger
6. M.L.
7. Dacks
8. J.B.
9. Carpenter
10. M.L.
11. Field
12. M.C.
13. Kuo
14. A.
15. Paredez
16. A.
17. Chapman
18. J.
19. Pham
20. J.
21. Shu
22. S.
23. Neupane
24. R.
25. Cipriano
26. M.
27. Mancuso
28. J.
29. Tu
30. H.
31. Salamov
32. A.
33. Lindquist
34. E.
35. Shapiro
36. H.
37. Lucas
38. S.
39. Grigoriev
40. I.V.
41. Cande
42. W.Z.
43. Fulton
44. C.
45. Rokhsar
46. D.S. and Dawson
47. S.C."
(2010) Naegleria gruberi strain NEG-M, v1.0
GCA_000004985.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000004985.1
(2009) ASM21029v1
GCA_000210295.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000210295.1
1. Hovde
2. B.T.
3. Starkenburg
4. S.R. and Cattolico
5. R.A.
(2015) Ctobinv2
GCA_001275005.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_001275005.1
1. Emiliania huxleyi Annotation Consortium
(2013) Emiliana huxleyi CCMP1516 main genome assembly v1.0
GCA_000372725.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000372725.1
1. Morrison
2. H.G.
3. McArthur
4. A.G.
5. Gillin
6. F.D.
7. Aley
8. S.B.
9. Adam
10. R.D.
11. Olsen
12. G.J.
13. Best
14. A.A.
15. Cande
16. W.Z.
17. Chen
18. F.
19. Cipriano
20. M.J.
21. Davids
22. B.J.
23. Dawson
24. S.C.
25. Elmendorf
26. H.G.
27. Hehl
28. A.B.
29. Holder
30. M.E.
31. Huse
32. S.M.
33. Kim
34. U.U.
35. Lasek-Nesselquist
36. E.
37. Manning
38. G.
39. Nigam
40. A.
41. Nixon
42. J.E.
43. Palm
44. D.
45. Passamaneck
46. N.E.
47. Prabhu
48. A.
49. Reich
50. C.I.
51. Reiner
52. D.S.
53. Samuelson
54. J.
55. Svard
56. S.G. and Sogin
57. M.L.
(2019) UU_WB_2.1
GCA_000002435.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002435.2
1. Xu
2. F.
3. Jimenez-Gonzalez
4. A.
5. Einarsson
6. E.
7. Astvaldsson
8. A.
9. Peirasmaki
10. D.
11. Eckmann
12. L.
13. Andersson
14. J.O.
15. Svard
16. S.G. and Jerlstrom-Hultqvist
17. J.
(2019) UU_GM_1.1
GCA_006247105.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_006247105.1
1. Tanifuji
2. G.
3. Takabayashi
4. S.
5. Kume
6. K.
7. Takagi
8. M.
9. Nakayama
10. T.
11. Kamikawa
12. R.
13. Inagaki
14. Y. and Hashimoto
15. T.
(2018) KIPB_1.0
GCA_003568945.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_003568945.1
1. Xu
2. F.
3. Jerlstrom-Hultqvist
4. J.
5. Einarsson
6. E.
7. Astvaldsson
8. A.
9. Svard
10. S.G. and Andersson
11. J.O.
(2013) SSK3.0
GCA_000497125.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000497125.1
1. Treitli
2. S.C.
3. Kolisko
4. M.
5. Husnik
6. F.
7. Keeling
8. P. and Hampl
9. V.
(2019) CUV_Sstr_1.0
GCA_008636045.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_008636045.1
1. Kuo
2. D.
(2018) ASM289133v1
GCA_002891335.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_002891335.1
1. Benchimol
2. M.
3. Almeida
4. L.G.
5. Vasconcelos
6. A.T.
7. Perreira-Neves
8. A.
9. Rosa
10. I.A.
11. Tasca
12. T.
13. Bogo
14. M.R. and de Souza
15. W.
(2016) ASM183968v1
GCA_001839685.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_001839685.1
1. Srivastava
2. M.
3. Simakov
4. O.
5. Chapman
6. J.
7. Fahey
8. B.
9. Gauthier
10. M.E.
11. Mitros
12. T.
13. Richards
14. G.S.
15. Conaco
16. C.
17. Dacre
18. M.
19. Hellsten
20. U.
21. Larroux
22. C.
23. Putnam
24. N.H.
25. Stanke
26. M.
27. Adamska
28. M.
29. Darling
30. A.
31. Degnan
32. S.M.
33. Oakley
34. T.H.
35. Plachetzki
36. D.C.
37. Zhai
38. Y.
39. Adamski
40. M.
41. Calcino
42. A.
43. Cummins
44. S.F.
45. Goodstein
46. D.M.
47. Harris
48. C.
49. Jackson
50. D.J.
51. Leys
52. S.P.
53. Shu
54. S.
55. Woodcroft
56. B.J.
57. Vervoort
58. M.
59. Kosik
60. K.S.
61. Manning
62. G.
63. Degnan
64. B.M. and Rokhsar
65. D.S.
(2010) Amphimedon queenslandica v1.0
GCA_000090795.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000090795.1
1. The Broad Institute Genome Sequencing Platform
(2013) C_owczarzaki_V2
GCA_000151315.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000151315.2
1. Genome Reference Consortium
(2017) Genome Reference Consortium Zebrafish Build 11
GCA_000002035.4.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002035.4
1. The FlyBase Consortium
(2014) Release 6 plus ISO1 MT
GCA_000001215.4.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000001215.4
1. The Broad Institute Genomics Platform
(2014) Font_alba_ATCC_38817_V2
GCA_000388065.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000388065.2
1. Genome Reference Consortium
(2010) GRCh37.p2
GCA_000001405.3.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000001405.3
1. King
2. N.
3. Westbrook
4. M.J.
5. Young
6. S.L.
7. Kuo
8. A.
9. Abedin
10. M.
11. Chapman
12. J.
13. Fairclough
14. S.
15. Hellsten
16. U.
17. Isogai
18. Y.
19. Letunic
20. I.
21. Marr
22. M.
23. Pincus
24. D.
25. Putnam
26. N.
27. Rokas
28. A.
29. Wright
30. K.J.
31. Zuzow
32. R.
33. Dirks
34. W.
35. Good
36. M.
37. Goodstein
38. D.
39. Lemons
40. D.
41. Li
42. W.
43. Lyons
44. J.B.
45. Morris
46. A.
47. Nichols
48. S.
49. Richter
50. D.J.
51. Salamov
52. A.
53. Sequencing
54. J.G.
55. Bork
56. P.
57. Lim
58. W.A.
59. Manning
60. G.
61. Miller
62. W.T.
63. McGinnis
64. W.
65. Shapiro
66. H.
67. Tjian
68. R.
69. Grigoriev
70. I.V. and Rokhsar
71. D.
(2007) Monosiga brevicollis MX1 (choanoflagellates) v1.0
GCA_000002865.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002865.1
1. Galagan
2. J.E.
3. Calvo
4. S.E.
5. Borkovich
6. K.A.
7. Selker
8. E.U.
9. Read
10. N.D.
11. Jaffe
12. D.
13. FitzHugh
14. W.
15. Ma
16. L.J.
17. Smirnov
18. S.
19. Purcell
20. S.
21. Rehman
22. B.
23. Elkins
24. T.
25. Engels
26. R.
27. Wang
28. S.
29. Nielsen
30. C.B.
31. Butler
32. J.
33. Endrizzi
34. M.
35. Qui
36. D.
37. Ianakiev
38. P.
39. Bell-Pedersen
40. D.
41. Nelson
42. M.A.
43. Werner-Washburne
44. M.
45. Selitrennikoff
46. C.P.
47. Kinsey
48. J.A.
49. Braun
50. E.L.
51. Zelter
52. A.
53. Schulte
54. U.
55. Kothe
56. G.O.
57. Jedd
58. G.
59. Mewes
60. W.
61. Staben
62. C.
63. Marcotte
64. E.
65. Greenberg
66. D.
67. Roy
68. A.
69. Foley
70. K.
71. Naylor
72. J.
73. Stange-Thomann
74. N.
75. Barrett
76. R.
77. Gnerre
78. S.
79. Kamal
80. M.
81. Kamvysselis
82. M.
83. Mauceli
84. E.
85. Bielke
86. C.
87. Rudd
88. S.
89. Frishman
90. D.
91. Krystofova
92. S.
93. Rasmussen
94. C.
95. Metzenberg
96. R.L.
97. Perkins
98. D.D.
99. Kroken
100. S.
101. Cogoni
102. C.
103. Macino
104. G.
105. Catcheside
106. D.
107. Li
108. W.
109. Pratt
110. R.J.
111. Osmani
112. S.A.
113. DeSouza
114. C.P.
115. Glass
116. L.
117. Orbach
118. M.J.
119. Berglund
120. J.A.
121. Voelker
122. R.
123. Yarden
124. O.
125. Plamann
126. M.
127. Seiler
128. S.
129. Dunlap
130. J.
131. Radford
132. A.
133. Aramayo
134. R.
135. Natvig
136. D.O.
137. Alex
138. L.A.
139. Mannhaupt
140. G.
141. Ebbole
142. D.J.
143. Freitag
144. M.
145. Paulsen
146. I.
147. Sachs
148. M.S.
149. Lander
150. E.S.
151. Nusbaum
152. C. and Birren
153. B.
(2013) NC12
GCA_000182925.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000182925.2
1. Ma
2. L.J.
3. Ibrahim
4. A.S.
5. Skory
6. C.
7. Grabherr
8. M.G.
9. Burger
10. G.
11. Butler
12. M.
13. Elias
14. M.
15. Idnurm
16. A.
17. Lang
18. B.F.
19. Sone
20. T.
21. Abe
22. A.
23. Calvo
24. S.E.
25. Corrochano
26. L.M.
27. Engels
28. R.
29. Fu
30. J.
31. Hansberg
32. W.
33. Kim
34. J.M.
35. Kodira
36. C.D.
37. Koehrsen
38. M.J.
39. Liu
40. B.
41. Miranda-Saavedra
42. D.
43. O'Leary
44. S.
45. Ortiz-Castellanos
46. L.
47. Poulter
48. R.
49. Rodriguez-Romero
50. J.
51. Ruiz-Herrera
52. J.
53. Shen
54. Y.Q.
55. Zeng
56. Q.
57. Galagan
58. J.
59. Birren
60. B.W.
61. Cuomo
62. C.A. and Wickes
63. B.L.
(2009) RO3
GCA_000149305.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000149305.1
1. Frasergen bioinfomatics
(2018) ASM308665v1
GCA_003086655.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_003086655.1
1. The Broad Institute Genome Sequencing Platform
(2015) S_punctatus_V1
GCA_000182565.2 .

https://www.ncbi.nlm.nih.gov/assembly/GCA_000182565.2
1. The Sea Urchin Genome Project
(2019) Spur_5.0
GCA_000002235.4.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000002235.4
1. Kamper
2. J.
3. Kahmann
4. R.
5. Bolker
6. M.
7. Ma
8. L.J.
9. Brefort
10. T.
11. Saville
12. B.J.
13. Banuett
14. F.
15. Kronstad
16. J.W.
17. Gold
18. S.E.
19. Muller
20. O.
21. Perlin
22. M.H.
23. Wosten
24. H.A.
25. de Vries
26. R.
27. Ruiz-Herrera
28. J.
29. Reynaga-Pena
30. C.G.
31. Snetselaar
32. K.
33. McCann
34. M.
35. Perez-Martin
36. J.
37. Feldbrugge
38. M.
39. Basse
40. C.W.
41. Steinberg
42. G.
43. Ibeas
44. J.I.
45. Holloman
46. W.
47. Guzman
48. P.
49. Farman
50. M.
51. Stajich
52. J.E.
53. Sentandreu
54. R.
55. Gonzalez-Prieto
56. J.M.
57. Kennell
58. J.C.
59. Molina
60. L.
61. Schirawski
62. J.
63. Mendoza-Mendoza
64. A.
65. Greilinger
66. D.
67. Munch
68. K.
69. Rossel
70. N.
71. Scherer
72. M.
73. Vranes
74. M.
75. Ladendorf
76. O.
77. Vincon
78. V.
79. Fuchs
80. U.
81. Sandrock
82. B.
83. Meng
84. S.
85. Ho
86. E.C.
87. Cahill
88. M.J.
89. Boyce
90. K.J.
91. Klose
92. J.
93. Klosterman
94. S.J.
95. Deelstra
96. H.J.
97. Ortiz-Castellanos
98. L.
99. Li
100. W.
101. Sanchez-Alonso
102. P.
103. Schreier
104. P.H.
105. Hauser-Hahn
106. I.
107. Vaupel
108. M.
109. Koopmann
110. E.
111. Friedrich
112. G.
113. Voss
114. H.
115. Schluter
116. T.
117. Margolis
118. J.
119. Platt
120. D.
121. Swimmer
122. C.
123. Gnirke
124. A.
125. Chen
126. F.
127. Vysotskaia
128. V.
129. Mannhaupt
130. G.
131. Guldener
132. U.
133. Munsterkotter
134. M.
135. Haase
136. D.
137. Oesterheld
138. M.
139. Mewes
140. H.W.
141. Mauceli
142. E.W.
143. DeCaprio
144. D.
145. Wade
146. C.M.
147. Butler
148. J.
149. Young
150. S.
151. Jaffe
152. D.B.
153. Calvo
154. S.
155. Nusbaum
156. C.
157. Galagan
158. J. and Birren
159. B.W.
(2015) Umaydis521_2.0
GCA_000328475.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000328475.2
1. Glockner
2. G.
3. Hulsmann
4. N.
5. Schleicher
6. M.
7. Noegel
8. A.A.
9. Eichinger
10. L.
11. Gallinger
12. C.
13. Pawlowski
14. J.
15. Sierra
16. R.
17. Euteneuer
18. U.
19. Pillet
20. L.
21. Moustafa
22. A.
23. Platzer
24. M.
25. Groth
26. M.
27. Szafranski
28. K. and Schliwa
29. M.
(2013) Reti_assembly1.0
GCA_000512085.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000512085.1
1. Collen
2. J.
3. Porcel
4. B.
5. Carre
6. W.
7. Ball
8. S.G.
9. Chaparro
10. C.
11. Tonon
12. T.
13. Barbeyron
14. T.
15. Michel
16. G.
17. Noel
18. B.
19. Valentin
20. K.
21. Elias
22. M.
23. Artiguenave
24. F.
25. Arun
26. A.
27. Aury
28. J.M.
29. Barbosa-Neto
30. J.F.
31. Bothwell
32. J.H.
33. Bouget
34. F.Y.
35. Brillet
36. L.
37. Cabello-Hurtado
38. F.
39. Capella-Gutierrez
40. S.
41. Charrier
42. B.
43. Cladiere
44. L.
45. Cock
46. J.M.
47. Coelho
48. S.M.
49. Colleoni
50. C.
51. Czjzek
52. M.
53. Da Silva
54. C.
55. Delage
56. L.
57. Denoeud
58. F.
59. Deschamps
60. P.
61. Dittami
62. S.M.
63. Gabaldon
64. T.
65. Gachon
66. C.M.
67. Groisillier
68. A.
69. Herve
70. C.
71. Jabbari
72. K.
73. Katinka
74. M.
75. Kloareg
76. B.
77. Kowalczyk
78. N.
79. Labadie
80. K.
81. Leblanc
82. C.
83. Lopez
84. P.J.
85. McLachlan
86. D.H.
87. Meslet-Cladiere
88. L.
89. Moustafa
90. A.
91. Nehr
92. Z.
93. Nyvall Collen
94. P.
95. Panaud
96. O.
97. Partensky
98. F.
99. Poulain
100. J.
101. Rensing
102. S.A.
103. Rousvoal
104. S.
105. Samson
106. G.
107. Symeonidi
108. A.
109. Weissenbach
110. J.
111. Zambounis
112. A.
113. Wincker
114. P. and Boyen
115. C.
(2013) ASM35022v2
GCA_000350225.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000350225.2
1. National Institute of Genetics
2. Japan
(2007) ASM9120v1
GCA_000091205.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000091205.1
1. Lee
2. J.
(2019) P_purpureum_CCMP1328_Hybrid_assembly
GCA_008690995.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_008690995.1
1. Wincker
2. P.
(2010) ASM15166v1
GCA_000151665.1.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000151665.1
1. Bowler
2. C.
3. Allen
4. A.E.
5. Badger
6. J.H.
7. Grimwood
8. J.
9. Jabbari
10. K.
11. Kuo
12. A.
13. Maheswari
14. U.
15. Martens
16. C.
17. Maumus
18. F.
19. Otillar
20. R.P.
21. Rayko
22. E.
23. Salamov
24. A.
25. Vandepoele
26. K.
27. Beszteri
28. B.
29. Gruber
30. A.
31. Heijde
32. M.
33. Katinka
34. M.
35. Mock
36. T.
37. Valentin
38. K.
39. Verret
40. F.
41. Berges
42. J.A.
43. Brownlee
44. C.
45. Cadoret
46. J.P.
47. Chiovitti
48. A.
49. Choi
50. C.J.
51. Coesel
52. S.
53. De Martino
54. A.
55. Detter
56. J.C.
57. Durkin
58. C.
59. Falciatore
60. A.
61. Fournet
62. J.
63. Haruta
64. M.
65. Huysman
66. M.J.
67. Jenkins
68. B.D.
69. Jiroutova
70. K.
71. Jorgensen
72. R.E.
73. Joubert
74. Y.
75. Kaplan
76. A.
77. Kroger
78. N.
79. Kroth
80. P.G.
81. La Roche
82. J.
83. Lindquist
84. E.
85. Lommer
86. M.
87. Martin-Jezequel
88. V.
89. Lopez
90. P.J.
91. Lucas
92. S.
93. Mangogna
94. M.
95. McGinnis
96. K.
97. Medlin
98. L.K.
99. Montsant
100. A.
101. Oudot-Le Secq
102. M.P.
103. Napoli
104. C.
105. Obornik
106. M.
107. Parker
108. M.S.
109. Petit
110. J.L.
111. Porcel
112. B.M.
113. Poulsen
114. N.
115. Robison
116. M.
117. Rychlewski
118. L.
119. Rynearson
120. T.A.
121. Schmutz
122. J.
123. Shapiro
124. H.
125. Siaut
126. M.
127. Stanley
128. M.
129. Sussman
130. M.R.
131. Taylor
132. A.R.
133. Vardi
134. A.
135. von Dassow
136. P.
137. Vyverman
138. W.
139. Willis
140. A.
141. Wyrwicz
142. L.S.
143. Rokhsar
144. D.S.
145. Weissenbach
146. J.
147. Armbrust
148. E.V.
149. Green
150. B.R.
151. Van de Peer
152. Y. and Grigoriev
153. I.V.
(2008) ASM15095v2
GCA_000150955.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000150955.2
1. Armbrust
2. E.V.
3. Berges
4. J.A.
5. Bowler
6. C.
7. Green
8. B.R.
9. Martinez
10. D.
11. Putnam
12. N.H.
13. Zhou
14. S.
15. Allen
16. A.E.
17. Apt
18. K.E.
19. Bechner
20. M.
21. Brzezinski
22. M.A.
23. Chaal
24. B.K.
25. Chiovitti
26. A.
27. Davis
28. A.K.
29. Demarest
30. M.S.
31. Detter
32. J.C.
33. Glavina
34. T.
35. Goodstein
36. D.
37. Hadi
38. M.Z.
39. Hellsten
40. U.
41. Hildebrand
42. M.
43. Jenkins
44. B.D.
45. Jurka
46. J.
47. Kapitonov
48. V.V.
49. Kroger
50. N.
51. Lau
52. W.W.
53. Lane
54. T.W.
55. Larimer
56. F.W.
57. Lippmeier
58. J.C.
59. Lucas
60. S.
61. Medina
62. M.
63. Montsant
64. A.
65. Obornik
66. M.
67. Parker
68. M.S.
69. Palenik
70. B.
71. Pazour
72. G.J.
73. Richardson
74. P.M.
75. Rynearson
76. T.A.
77. Saito
78. M.A.
79. Schwartz
80. D.C.
81. Thamatrakoln
82. K.
83. Valentin
84. K.
85. Vardi
86. A.
87. Wilkerson
88. F.P. and Rokhsar
89. D.S.
(2009) ASM14940v2
GCA_000149405.2.

https://www.ncbi.nlm.nih.gov/assembly/GCA_000149405.2

Article and author information

Author details

Xinyu Zhu

Biological Sciences, Auburn University, Auburn, United States

Competing interests
The authors declare that no competing interests exist.
Aren Boulet

Biochemistry, Microbiology and Immunology, University of Saskatchewan, Saskatoon, Canada

Competing interests
The authors declare that no competing interests exist.
Katherine M Buckley

Biological Sciences, Auburn University, Auburn, United States

Competing interests
The authors declare that no competing interests exist.
Casey B Phillips

Biological Sciences, Auburn University, Auburn, United States

Competing interests
The authors declare that no competing interests exist.
Micah G Gammon

Biological Sciences, Auburn University, Auburn, United States

Competing interests
The authors declare that no competing interests exist.
Laura E Oldfather

Biological Sciences, Auburn University, Auburn, United States

Competing interests
The authors declare that no competing interests exist.
Stanley A Moore

Biochemistry, Microbiology and Immunology, University Saskatchewan, Saskatoon, Canada

Competing interests
The authors declare that no competing interests exist.
Scot C Leary

Biochemistry, Microbiology and Immunology, University of Saskatchewan, Saskatoon, Canada

Competing interests
The authors declare that no competing interests exist.
Paul A Cobine

Biological Sciences, Auburn University, Auburn, United States

For correspondence
paul.cobine@auburn.edu

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6012-0985

Funding

National Institutes of Health (R01GM120211)

Scot C Leary
Paul A Cobine

National Science Foundation (EF 2021886)

Katherine M Buckley

Alabama Agricultural Experiment Station

Paul A Cobine

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

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