Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

Valentina Klymiuk; Elitsur Yaniv; Lin Huang; Dina Raats; Andrii Fatiukha; Shisheng Chen; Lihua Feng; Zeev Frenkel; Tamar Krugman; Gabriel Lidzbarsky; Wei Chang; Marko J. Jääskeläinen; Christian Schudoma; Lars Paulin; Pia Laine; Harbans Bariana; Hanan Sela; Kamran Saleem; Chris Khadgi Sørensen; Mogens S. Hovmøller; Assaf Distelfeld; Boulos Chalhoub; Jorge Dubcovsky; Abraham B. Korol; Alan H. Schulman; Tzion Fahima

doi:10.1038/s41467-018-06138-9

Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

Valentina Klymiuk, Elitsur Yaniv, Lin Huang, Dina Raats, Andrii Fatiukha, Shisheng Chen, Lihua Feng, Zeev Frenkel, Tamar Krugman, Gabriel Lidzbarsky, Wei Chang, Marko J. Jääskeläinen, Christian Schudoma, Lars Paulin, Pia Laine, Harbans Bariana, Hanan Sela, Kamran Saleem, Chris Khadgi Sørensen, Mogens S. HovmøllerAssaf Distelfeld, Boulos Chalhoub, Jorge Dubcovsky, Abraham B. Korol, Alan H. Schulman, Tzion Fahima

Department of Evolutionary and Environmental Biology

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

Abstract

Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.

Original language	English
Article number	3735
Journal	Nature Communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-06138-9
State	Published - 1 Dec 2018

Bibliographical note

Funding Information:
This research was supported by the European Community Framework projects BioEx-ploit (CT-2005-513949) and TriticeaeGenome (FP7-212019), the COST Actions TritiGen (FA0604), SUSTAIN (FA1208), and Impact of Nuclear Domains on Gene Expression and Plant Traits (INDEPTH, CA16212), the CSC-IT Center for Science (Finland), the Israel Science Foundation (1719/08), and the US-Israel Binational Agricultural Research and Development Fund (IS-4628-13, US-4916-16). We thank the International Wheat Genome Sequencing Consortium (IWGSC) for providing access to unpublished wheat genome sequences and the Global Yellow Rust Gene Bank for providing Pst races. We also thank P. Auvinen, P.C. Bailey, S. Barinova, H. Belcram, A. Dahan, Z. Gerechter-Amitai, A. Grama, M. Iso-Kokkila, T. Kis-Papo, D. Lewinsohn, U.S. Lönnqvist, A. Malik, Y. Manisterski, I. Manov, H. Miah, A.-M. Narvanto, M.L. Neufeld, K. Neufeld, Y. Ronin, O. Rybak, J. Shanir, N. Sher, O.-P. Smolander, and J. Tanskanen.

Publisher Copyright:
© 2018, The Author(s).

ASJC Scopus subject areas

Chemistry (all)
Biochemistry, Genetics and Molecular Biology (all)
Physics and Astronomy (all)

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Klymiuk, V., Yaniv, E., Huang, L., Raats, D., Fatiukha, A., Chen, S., Feng, L., Frenkel, Z., Krugman, T., Lidzbarsky, G., Chang, W., Jääskeläinen, M. J., Schudoma, C., Paulin, L., Laine, P., Bariana, H., Sela, H., Saleem, K., Sørensen, C. K., ... Fahima, T. (2018). Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nature Communications, 9(1), Article 3735. https://doi.org/10.1038/s41467-018-06138-9

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title = "Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family",

abstract = "Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.",

author = "Valentina Klymiuk and Elitsur Yaniv and Lin Huang and Dina Raats and Andrii Fatiukha and Shisheng Chen and Lihua Feng and Zeev Frenkel and Tamar Krugman and Gabriel Lidzbarsky and Wei Chang and J{\"a}{\"a}skel{\"a}inen, {Marko J.} and Christian Schudoma and Lars Paulin and Pia Laine and Harbans Bariana and Hanan Sela and Kamran Saleem and S{\o}rensen, {Chris Khadgi} and Hovm{\o}ller, {Mogens S.} and Assaf Distelfeld and Boulos Chalhoub and Jorge Dubcovsky and Korol, {Abraham B.} and Schulman, {Alan H.} and Tzion Fahima",

note = "Funding Information: This research was supported by the European Community Framework projects BioEx-ploit (CT-2005-513949) and TriticeaeGenome (FP7-212019), the COST Actions TritiGen (FA0604), SUSTAIN (FA1208), and Impact of Nuclear Domains on Gene Expression and Plant Traits (INDEPTH, CA16212), the CSC-IT Center for Science (Finland), the Israel Science Foundation (1719/08), and the US-Israel Binational Agricultural Research and Development Fund (IS-4628-13, US-4916-16). We thank the International Wheat Genome Sequencing Consortium (IWGSC) for providing access to unpublished wheat genome sequences and the Global Yellow Rust Gene Bank for providing Pst races. We also thank P. Auvinen, P.C. Bailey, S. Barinova, H. Belcram, A. Dahan, Z. Gerechter-Amitai, A. Grama, M. Iso-Kokkila, T. Kis-Papo, D. Lewinsohn, U.S. L{\"o}nnqvist, A. Malik, Y. Manisterski, I. Manov, H. Miah, A.-M. Narvanto, M.L. Neufeld, K. Neufeld, Y. Ronin, O. Rybak, J. Shanir, N. Sher, O.-P. Smolander, and J. Tanskanen. Publisher Copyright: {\textcopyright} 2018, The Author(s).",

year = "2018",

month = dec,

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doi = "10.1038/s41467-018-06138-9",

language = "English",

volume = "9",

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Klymiuk, V, Yaniv, E, Huang, L, Raats, D, Fatiukha, A, Chen, S, Feng, L, Frenkel, Z, Krugman, T, Lidzbarsky, G, Chang, W, Jääskeläinen, MJ, Schudoma, C, Paulin, L, Laine, P, Bariana, H, Sela, H, Saleem, K, Sørensen, CK, Hovmøller, MS, Distelfeld, A, Chalhoub, B, Dubcovsky, J, Korol, AB, Schulman, AH & Fahima, T 2018, 'Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family', Nature Communications, vol. 9, no. 1, 3735. https://doi.org/10.1038/s41467-018-06138-9

TY - JOUR

T1 - Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

AU - Klymiuk, Valentina

AU - Yaniv, Elitsur

AU - Huang, Lin

AU - Raats, Dina

AU - Fatiukha, Andrii

AU - Chen, Shisheng

AU - Feng, Lihua

AU - Frenkel, Zeev

AU - Krugman, Tamar

AU - Lidzbarsky, Gabriel

AU - Chang, Wei

AU - Jääskeläinen, Marko J.

AU - Schudoma, Christian

AU - Paulin, Lars

AU - Laine, Pia

AU - Bariana, Harbans

AU - Sela, Hanan

AU - Saleem, Kamran

AU - Sørensen, Chris Khadgi

AU - Hovmøller, Mogens S.

AU - Distelfeld, Assaf

AU - Chalhoub, Boulos

AU - Dubcovsky, Jorge

AU - Korol, Abraham B.

AU - Schulman, Alan H.

AU - Fahima, Tzion

N1 - Funding Information: This research was supported by the European Community Framework projects BioEx-ploit (CT-2005-513949) and TriticeaeGenome (FP7-212019), the COST Actions TritiGen (FA0604), SUSTAIN (FA1208), and Impact of Nuclear Domains on Gene Expression and Plant Traits (INDEPTH, CA16212), the CSC-IT Center for Science (Finland), the Israel Science Foundation (1719/08), and the US-Israel Binational Agricultural Research and Development Fund (IS-4628-13, US-4916-16). We thank the International Wheat Genome Sequencing Consortium (IWGSC) for providing access to unpublished wheat genome sequences and the Global Yellow Rust Gene Bank for providing Pst races. We also thank P. Auvinen, P.C. Bailey, S. Barinova, H. Belcram, A. Dahan, Z. Gerechter-Amitai, A. Grama, M. Iso-Kokkila, T. Kis-Papo, D. Lewinsohn, U.S. Lönnqvist, A. Malik, Y. Manisterski, I. Manov, H. Miah, A.-M. Narvanto, M.L. Neufeld, K. Neufeld, Y. Ronin, O. Rybak, J. Shanir, N. Sher, O.-P. Smolander, and J. Tanskanen. Publisher Copyright: © 2018, The Author(s).

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.

AB - Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.

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U2 - 10.1038/s41467-018-06138-9

DO - 10.1038/s41467-018-06138-9

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C2 - 30282993

AN - SCOPUS:85054325175

SN - 2041-1723

VL - 9

JO - Nature Communications

JF - Nature Communications

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ER -

Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

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