Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi

Yogesh K. Gupta; Francismar C. Marcelino-Guimarães; Cécile Lorrain; Andrew Farmer; Sajeet Haridas; Everton Geraldo Capote Ferreira; Valéria S. Lopes-Caitar; Liliane Santana Oliveira; Emmanuelle Morin; Stephanie Widdison; Connor Cameron; Yoshihiro Inoue; Kathrin Thor; Kelly Robinson; Elodie Drula; Bernard Henrissat; Kurt LaButti; Aline Mara Rudsit Bini; Eric Paget; Vasanth Singan; Christopher Daum; Cécile Dorme; Milan van Hoek; Antoine Janssen; Lucie Chandat; Yannick Tarriotte; Jake Richardson; Bernardo do Vale Araújo Melo; Alexander H.J. Wittenberg; Harrie Schneiders; Stephane Peyrard; Larissa Goulart Zanardo; Valéria Cristina Holtman; Flavie Coulombier-Chauvel; Tobias I. Link; Dirk Balmer; André N. Müller; Sabine Kind; Stefan Bohnert; Louisa Wirtz; Cindy Chen; Mi Yan; Vivian Ng; Pierrick Gautier; Maurício Conrado Meyer; Ralf Thomas Voegele; Qingli Liu; Igor V. Grigoriev; Uwe Conrath; Sérgio H. Brommonschenkel; Marco Loehrer; Ulrich Schaffrath; Catherine Sirven; Gabriel Scalliet; Sébastien Duplessis; H. Peter van Esse

doi:10.1038/s41467-023-37551-4

Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi

Yogesh K. Gupta, Francismar C. Marcelino-Guimarães, Cécile Lorrain, Andrew Farmer, Sajeet Haridas, Everton Geraldo Capote Ferreira, Valéria S. Lopes-Caitar, Liliane Santana Oliveira, Emmanuelle Morin, Stephanie Widdison, Connor Cameron, Yoshihiro Inoue, Kathrin Thor, Kelly Robinson, Elodie Drula, Bernard Henrissat, Kurt LaButti, Aline Mara Rudsit Bini, Eric Paget, Vasanth SinganChristopher Daum, Cécile Dorme, Milan van Hoek, Antoine Janssen, Lucie Chandat, Yannick Tarriotte, Jake Richardson, Bernardo do Vale Araújo Melo, Alexander H.J. Wittenberg, Harrie Schneiders, Stephane Peyrard, Larissa Goulart Zanardo, Valéria Cristina Holtman, Flavie Coulombier-Chauvel, Tobias I. Link, Dirk Balmer, André N. Müller, Sabine Kind, Stefan Bohnert, Louisa Wirtz, Cindy Chen, Mi Yan, Vivian Ng, Pierrick Gautier, Maurício Conrado Meyer, Ralf Thomas Voegele, Qingli Liu, Igor V. Grigoriev, Uwe Conrath, Sérgio H. Brommonschenkel, Marco Loehrer, Ulrich Schaffrath, Catherine Sirven, Gabriel Scalliet, Sébastien Duplessis, H. Peter van Esse^*

^*Corresponding author for this work

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Abstract

With >7000 species the order of rust fungi has a disproportionately large impact on agriculture, horticulture, forestry and foreign ecosystems. The infectious spores are typically dikaryotic, a feature unique to fungi in which two haploid nuclei reside in the same cell. A key example is Phakopsora pachyrhizi, the causal agent of Asian soybean rust disease, one of the world's most economically damaging agricultural diseases. Despite P. pachyrhizi's impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. Here, we sequence three independent P. pachyrhizi genomes and uncover a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. We study the incursion and dominant impact of these TEs on the genome and show how they have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity.

Original language	English
Article number	1835
Journal	Nature Communications
Volume	14
Number of pages	16
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-023-37551-4
Publication status	Published - 2023

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Gupta, Y. K., Marcelino-Guimarães, F. C., Lorrain, C., Farmer, A., Haridas, S., Ferreira, E. G. C., Lopes-Caitar, V. S., Oliveira, L. S., Morin, E., Widdison, S., Cameron, C., Inoue, Y., Thor, K., Robinson, K., Drula, E., Henrissat, B., LaButti, K., Bini, A. M. R., Paget, E., ... van Esse, H. P. (2023). Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi. Nature Communications, 14, Article 1835. https://doi.org/10.1038/s41467-023-37551-4

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title = "Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi",

abstract = "With >7000 species the order of rust fungi has a disproportionately large impact on agriculture, horticulture, forestry and foreign ecosystems. The infectious spores are typically dikaryotic, a feature unique to fungi in which two haploid nuclei reside in the same cell. A key example is Phakopsora pachyrhizi, the causal agent of Asian soybean rust disease, one of the world's most economically damaging agricultural diseases. Despite P. pachyrhizi's impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. Here, we sequence three independent P. pachyrhizi genomes and uncover a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. We study the incursion and dominant impact of these TEs on the genome and show how they have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity.",

author = "Gupta, {Yogesh K.} and Marcelino-Guimar{\~a}es, {Francismar C.} and C{\'e}cile Lorrain and Andrew Farmer and Sajeet Haridas and Ferreira, {Everton Geraldo Capote} and Lopes-Caitar, {Val{\'e}ria S.} and Oliveira, {Liliane Santana} and Emmanuelle Morin and Stephanie Widdison and Connor Cameron and Yoshihiro Inoue and Kathrin Thor and Kelly Robinson and Elodie Drula and Bernard Henrissat and Kurt LaButti and Bini, {Aline Mara Rudsit} and Eric Paget and Vasanth Singan and Christopher Daum and C{\'e}cile Dorme and {van Hoek}, Milan and Antoine Janssen and Lucie Chandat and Yannick Tarriotte and Jake Richardson and Melo, {Bernardo do Vale Ara{\'u}jo} and Wittenberg, {Alexander H.J.} and Harrie Schneiders and Stephane Peyrard and Zanardo, {Larissa Goulart} and Holtman, {Val{\'e}ria Cristina} and Flavie Coulombier-Chauvel and Link, {Tobias I.} and Dirk Balmer and M{\"u}ller, {Andr{\'e} N.} and Sabine Kind and Stefan Bohnert and Louisa Wirtz and Cindy Chen and Mi Yan and Vivian Ng and Pierrick Gautier and Meyer, {Maur{\'i}cio Conrado} and Voegele, {Ralf Thomas} and Qingli Liu and Grigoriev, {Igor V.} and Uwe Conrath and Brommonschenkel, {S{\'e}rgio H.} and Marco Loehrer and Ulrich Schaffrath and Catherine Sirven and Gabriel Scalliet and S{\'e}bastien Duplessis and {van Esse}, {H. Peter}",

year = "2023",

doi = "10.1038/s41467-023-37551-4",

language = "English",

volume = "14",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

}

Gupta, YK, Marcelino-Guimarães, FC, Lorrain, C, Farmer, A, Haridas, S, Ferreira, EGC, Lopes-Caitar, VS, Oliveira, LS, Morin, E, Widdison, S, Cameron, C, Inoue, Y, Thor, K, Robinson, K, Drula, E, Henrissat, B, LaButti, K, Bini, AMR, Paget, E, Singan, V, Daum, C, Dorme, C, van Hoek, M, Janssen, A, Chandat, L, Tarriotte, Y, Richardson, J, Melo, BDVA, Wittenberg, AHJ, Schneiders, H, Peyrard, S, Zanardo, LG, Holtman, VC, Coulombier-Chauvel, F, Link, TI, Balmer, D, Müller, AN, Kind, S, Bohnert, S, Wirtz, L, Chen, C, Yan, M, Ng, V, Gautier, P, Meyer, MC, Voegele, RT, Liu, Q, Grigoriev, IV, Conrath, U, Brommonschenkel, SH, Loehrer, M, Schaffrath, U, Sirven, C, Scalliet, G, Duplessis, S & van Esse, HP 2023, 'Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi', Nature Communications, vol. 14, 1835. https://doi.org/10.1038/s41467-023-37551-4

TY - JOUR

T1 - Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi

AU - Gupta, Yogesh K.

AU - Marcelino-Guimarães, Francismar C.

AU - Lorrain, Cécile

AU - Farmer, Andrew

AU - Haridas, Sajeet

AU - Ferreira, Everton Geraldo Capote

AU - Lopes-Caitar, Valéria S.

AU - Oliveira, Liliane Santana

AU - Morin, Emmanuelle

AU - Widdison, Stephanie

AU - Cameron, Connor

AU - Inoue, Yoshihiro

AU - Thor, Kathrin

AU - Robinson, Kelly

AU - Drula, Elodie

AU - Henrissat, Bernard

AU - LaButti, Kurt

AU - Bini, Aline Mara Rudsit

AU - Paget, Eric

AU - Singan, Vasanth

AU - Daum, Christopher

AU - Dorme, Cécile

AU - van Hoek, Milan

AU - Janssen, Antoine

AU - Chandat, Lucie

AU - Tarriotte, Yannick

AU - Richardson, Jake

AU - Melo, Bernardo do Vale Araújo

AU - Wittenberg, Alexander H.J.

AU - Schneiders, Harrie

AU - Peyrard, Stephane

AU - Zanardo, Larissa Goulart

AU - Holtman, Valéria Cristina

AU - Coulombier-Chauvel, Flavie

AU - Link, Tobias I.

AU - Balmer, Dirk

AU - Müller, André N.

AU - Kind, Sabine

AU - Bohnert, Stefan

AU - Wirtz, Louisa

AU - Chen, Cindy

AU - Yan, Mi

AU - Ng, Vivian

AU - Gautier, Pierrick

AU - Meyer, Maurício Conrado

AU - Voegele, Ralf Thomas

AU - Liu, Qingli

AU - Grigoriev, Igor V.

AU - Conrath, Uwe

AU - Brommonschenkel, Sérgio H.

AU - Loehrer, Marco

AU - Schaffrath, Ulrich

AU - Sirven, Catherine

AU - Scalliet, Gabriel

AU - Duplessis, Sébastien

AU - van Esse, H. Peter

PY - 2023

Y1 - 2023

N2 - With >7000 species the order of rust fungi has a disproportionately large impact on agriculture, horticulture, forestry and foreign ecosystems. The infectious spores are typically dikaryotic, a feature unique to fungi in which two haploid nuclei reside in the same cell. A key example is Phakopsora pachyrhizi, the causal agent of Asian soybean rust disease, one of the world's most economically damaging agricultural diseases. Despite P. pachyrhizi's impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. Here, we sequence three independent P. pachyrhizi genomes and uncover a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. We study the incursion and dominant impact of these TEs on the genome and show how they have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity.

AB - With >7000 species the order of rust fungi has a disproportionately large impact on agriculture, horticulture, forestry and foreign ecosystems. The infectious spores are typically dikaryotic, a feature unique to fungi in which two haploid nuclei reside in the same cell. A key example is Phakopsora pachyrhizi, the causal agent of Asian soybean rust disease, one of the world's most economically damaging agricultural diseases. Despite P. pachyrhizi's impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. Here, we sequence three independent P. pachyrhizi genomes and uncover a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. We study the incursion and dominant impact of these TEs on the genome and show how they have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity.

U2 - 10.1038/s41467-023-37551-4

DO - 10.1038/s41467-023-37551-4

M3 - Journal article

C2 - 37005409

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

M1 - 1835

ER -

Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi

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