An unusual tandem kinase fusion protein confers leaf rust resistance in wheat

Yajun Wang; Michael Abrouk; Spyridon Gourdoupis; Dal Hoe Koo; Miroslava Karafiátová; István Molnár; Kateřina Holušová; Jaroslav Doležel; Naveenkumar Athiyannan; Emile Cavalet-Giorsa; Łukasz Jaremko; Jesse Poland; Simon G. Krattinger

doi:10.1038/s41588-023-01401-2

An unusual tandem kinase fusion protein confers leaf rust resistance in wheat

Yajun Wang, Michael Abrouk, Spyridon Gourdoupis, Dal Hoe Koo, Miroslava Karafiátová, István Molnár, Kateřina Holušová, Jaroslav Doležel, Naveenkumar Athiyannan, Emile Cavalet-Giorsa, Łukasz Jaremko, Jesse Poland, Simon G. Krattinger^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

43 Scopus citations

Abstract

The introgression of chromosome segments from wild relatives is an established strategy to enrich crop germplasm with disease-resistance genes¹. Here we use mutagenesis and transcriptome sequencing to clone the leaf rust resistance gene Lr9, which was introduced into bread wheat from the wild grass species Aegilops umbellulata ². We established that Lr9 encodes an unusual tandem kinase fusion protein. Long-read sequencing of a wheat Lr9 introgression line and the putative Ae. umbellulata Lr9 donor enabled us to assemble the ~28.4-Mb Lr9 translocation and to identify the translocation breakpoint. We likewise cloned Lr58, which was reportedly introgressed from Aegilops triuncialis ³, but has an identical coding sequence compared to Lr9. Cytogenetic and haplotype analyses corroborate that the two genes originate from the same translocation event. Our work sheds light on the emerging role of kinase fusion proteins in wheat disease resistance, expanding the repertoire of disease-resistance genes for breeding.

Original language	English (US)
Pages (from-to)	914-920
Number of pages	7
Journal	Nature Genetics
Volume	55
Issue number	6
DOIs	https://doi.org/10.1038/s41588-023-01401-2
State	Published - Jun 2023

Bibliographical note

Funding Information:
We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubská, R. Šperková and J. Weiserová (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. Cápál (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant ‘AEGILWHEAT’ (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures.

Funding Information:
We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubská, R. Šperková and J. Weiserová (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. Cápál (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant ‘AEGILWHEAT’ (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures.

Publisher Copyright:
© 2023, The Author(s).

ASJC Scopus subject areas

Genetics

Access to Document

10.1038/s41588-023-01401-2

Cite this

@article{fbb4dfb17ab34394b112be2ff9f81fcd,

title = "An unusual tandem kinase fusion protein confers leaf rust resistance in wheat",

abstract = "The introgression of chromosome segments from wild relatives is an established strategy to enrich crop germplasm with disease-resistance genes 1. Here we use mutagenesis and transcriptome sequencing to clone the leaf rust resistance gene Lr9, which was introduced into bread wheat from the wild grass species Aegilops umbellulata 2. We established that Lr9 encodes an unusual tandem kinase fusion protein. Long-read sequencing of a wheat Lr9 introgression line and the putative Ae. umbellulata Lr9 donor enabled us to assemble the ~28.4-Mb Lr9 translocation and to identify the translocation breakpoint. We likewise cloned Lr58, which was reportedly introgressed from Aegilops triuncialis 3, but has an identical coding sequence compared to Lr9. Cytogenetic and haplotype analyses corroborate that the two genes originate from the same translocation event. Our work sheds light on the emerging role of kinase fusion proteins in wheat disease resistance, expanding the repertoire of disease-resistance genes for breeding.",

author = "Yajun Wang and Michael Abrouk and Spyridon Gourdoupis and Koo, {Dal Hoe} and Miroslava Karafi{\'a}tov{\'a} and Istv{\'a}n Moln{\'a}r and Kate{\v r}ina Holu{\v s}ov{\'a} and Jaroslav Dole{\v z}el and Naveenkumar Athiyannan and Emile Cavalet-Giorsa and {\L}ukasz Jaremko and Jesse Poland and Krattinger, {Simon G.}",

note = "Funding Information: We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubsk{\'a}, R. {\v S}perkov{\'a} and J. Weiserov{\'a} (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. C{\'a}p{\'a}l (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant {\textquoteleft}AEGILWHEAT{\textquoteright} (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. Funding Information: We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubsk{\'a}, R. {\v S}perkov{\'a} and J. Weiserov{\'a} (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. C{\'a}p{\'a}l (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant {\textquoteleft}AEGILWHEAT{\textquoteright} (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = jun,

doi = "10.1038/s41588-023-01401-2",

language = "English (US)",

volume = "55",

pages = "914--920",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "6",

}

TY - JOUR

T1 - An unusual tandem kinase fusion protein confers leaf rust resistance in wheat

AU - Wang, Yajun

AU - Abrouk, Michael

AU - Gourdoupis, Spyridon

AU - Koo, Dal Hoe

AU - Karafiátová, Miroslava

AU - Molnár, István

AU - Holušová, Kateřina

AU - Doležel, Jaroslav

AU - Athiyannan, Naveenkumar

AU - Cavalet-Giorsa, Emile

AU - Jaremko, Łukasz

AU - Poland, Jesse

AU - Krattinger, Simon G.

N1 - Funding Information: We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubská, R. Šperková and J. Weiserová (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. Cápál (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant ‘AEGILWHEAT’ (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. Funding Information: We are grateful to L. Zou (KAUST) for technical assistance, Y. Zhou (KAUST) and H.I. Ahmed (KAUST) for discussions on bioinformatics analyses and the KAUST Bioscience Core Lab for sequencing support. We thank Z. Dubská, R. Šperková and J. Weiserová (Institute of Experimental Botany) for the preparation of chromosome samples for flow cytometry, M. Said and P. Cápál (Institute of Experimental Botany) for chromosome 2B sorting and J. Raupp from the Wheat Genetics Resource Center for providing germplasm. We thank J. A. Kolmer from the USDA-ARS Cereal Disease Laboratory, St. Paul, MN, for providing P. triticina isolate MNPSD. We thank P. Lu from IGDB, CAS, for providing TKP sequences for phylogenetic analysis. This publication is based upon work supported by the King Abdullah University of Science and Technology (KAUST) Office of Sponsored Research (OSR) under Award OSR-CRG2018-3768. D.K. was supported by WGRC/IUCRC and NSF (grant 1822162). I.M. received support from the Marie Curie Fellowship grant ‘AEGILWHEAT’ (H2020-MSCA-IF-2016-746253) and from the Hungarian National Research, Development and Innovation Office (K135057). M.K., K.H. and J.D. received support from the ERDF project 'Plants as a tool for sustainable global development' (CZ.02.1.01/0.0/0.0/16_019/0000827). Computational resources were supplied by the project 'e-Infrastruktura CZ' (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. Publisher Copyright: © 2023, The Author(s).

PY - 2023/6

Y1 - 2023/6

N2 - The introgression of chromosome segments from wild relatives is an established strategy to enrich crop germplasm with disease-resistance genes 1. Here we use mutagenesis and transcriptome sequencing to clone the leaf rust resistance gene Lr9, which was introduced into bread wheat from the wild grass species Aegilops umbellulata 2. We established that Lr9 encodes an unusual tandem kinase fusion protein. Long-read sequencing of a wheat Lr9 introgression line and the putative Ae. umbellulata Lr9 donor enabled us to assemble the ~28.4-Mb Lr9 translocation and to identify the translocation breakpoint. We likewise cloned Lr58, which was reportedly introgressed from Aegilops triuncialis 3, but has an identical coding sequence compared to Lr9. Cytogenetic and haplotype analyses corroborate that the two genes originate from the same translocation event. Our work sheds light on the emerging role of kinase fusion proteins in wheat disease resistance, expanding the repertoire of disease-resistance genes for breeding.

AB - The introgression of chromosome segments from wild relatives is an established strategy to enrich crop germplasm with disease-resistance genes 1. Here we use mutagenesis and transcriptome sequencing to clone the leaf rust resistance gene Lr9, which was introduced into bread wheat from the wild grass species Aegilops umbellulata 2. We established that Lr9 encodes an unusual tandem kinase fusion protein. Long-read sequencing of a wheat Lr9 introgression line and the putative Ae. umbellulata Lr9 donor enabled us to assemble the ~28.4-Mb Lr9 translocation and to identify the translocation breakpoint. We likewise cloned Lr58, which was reportedly introgressed from Aegilops triuncialis 3, but has an identical coding sequence compared to Lr9. Cytogenetic and haplotype analyses corroborate that the two genes originate from the same translocation event. Our work sheds light on the emerging role of kinase fusion proteins in wheat disease resistance, expanding the repertoire of disease-resistance genes for breeding.

UR - http://www.scopus.com/inward/record.url?scp=85160034677&partnerID=8YFLogxK

U2 - 10.1038/s41588-023-01401-2

DO - 10.1038/s41588-023-01401-2

M3 - Article

C2 - 37217716

AN - SCOPUS:85160034677

SN - 1061-4036

VL - 55

SP - 914

EP - 920

JO - Nature Genetics

JF - Nature Genetics

IS - 6

ER -

An unusual tandem kinase fusion protein confers leaf rust resistance in wheat

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this