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Tandem kinase proteins across the plant kingdom

Nature Genetics volume 57, pages 254–262 (2025)Cite this article

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Abstract

Plant pathogens pose a continuous threat to global food production. Recent discoveries in plant immunity research unveiled a unique protein family characterized by an unusual resistance protein structure that combines two kinase domains. This study demonstrates the widespread occurrence of tandem kinase proteins (TKPs) across the plant kingdom. An examination of 104 plant species’ genomes uncovered 2,682 TKPs. The majority (95.6%) of these kinase domains are part of the receptor-like kinase–Pelle family, which is crucial for cell surface responses in plant immunity. Notably, 90% of TKPs comprise dual kinase domains, with over 50% being pseudokinases. Over 56% of these proteins harbor 127 different integrated domains, and over 47% include a transmembrane domain. TKP pseudokinases and/or integrated domains probably serve as decoys, engaging with pathogen effectors to trigger plant immunity. The TKP Atlas we created sheds light on the mechanisms of TKP convergent molecular evolution and potential function.

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Fig. 1: A taxonomic tree of 104 plant species was used to generate the TKP Atlas showcasing the number of TKPs.
Fig. 2: Prediction, composition and diversity of kinase and PKDs across 104 plant genomes.
Fig. 3: Integrated domain prevalence and position relative to protein KDs across 104 plant genomes.
Fig. 4: Variety of full domain compositions of tandem kinase among 104 plant species.
Fig. 5: Phylogenetic trees of all T. aestivum tandem kinases with two domains from DLSV family.
Fig. 6: Multidimensional scaling analyses of all tandem kinases with two KDs from two RLK–Pelle subfamilies from all studied species.

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Data availability

We have published a fasta file with all found TKPs on the Zenodo platform with a link: https://doi.org/10.5281/zenodo.13384335 (ref. 53).

Code availability

We have published our code on the Zenodo platform with a link: https://doi.org/10.5281/zenodo.11118417 (ref. 54).

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Acknowledgements

The authors thank O. Borzov, A. Korol, T. Krugman and L. Govta from the Institute of Evolution at the University of Haifa for their professional and moral support. T.F. was supported by the United States-Israel Binational Science Foundation (2019654), the US-Israel Binational Agricultural Research and Development Fund (US-5191-19C and US-5515-22C) and the Israel Science Foundation (grants 1366/18 and 2342/18). A.F. was supported by the EU COST INDEPH (CA16212). G.C. and T.F. were supported by the United States National Science Foundation (1937855) and the United States Department of Agriculture (2020-67013-32577). G.C. was supported by a grant from the National Institutes of Health (R35GM136402).

Author information

Authors and Affiliations

  1. Institute of Evolution, University of Haifa, Haifa, Israel

    Tamara Reveguk, Andrii Fatiukha, Evgenii Potapenko, Hanan Sela, Valentyna Klymiuk, Yinghui Li & Tzion Fahima

  2. Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel

    Tamara Reveguk, Andrii Fatiukha, Evgenii Potapenko, Valentyna Klymiuk, Yinghui Li & Tzion Fahima

  3. Crop Development Centre and Department of Plant Sciences, University of Saskatchewan, Saskatoon, Saskatchewan, Canada

    Andrii Fatiukha, Valentyna Klymiuk & Curtis Pozniak

  4. Laboratory of the Structural Biology of the Cell (BIOC), École Polytechnique, Paris, France

    Ivan Reveguk

  5. Triticeae Research Institute, Sichuan Agricultural University, Chengdu, China

    Yinghui Li

  6. Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland

    Thomas Wicker

  7. Department of Plant Pathology, University of California, Davis, CA, USA

    Gitta Coaker

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  1. Tamara Reveguk
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Contributions

T.F. conceived the overall research concept. A.F. and T.W. developed the pipeline for searching the TKPs, which A.F. used with the genomes of 104 plants. T.F., A.F., V.K., H.S., Y.L., G.C., T.R., E.P. and C.P. designed the experimental approach. E.P., T.R. and I.R. analyzed the TKPs data. T.R. and H.S. conducted the phylogenetic and multidimensional scaling analyses. V.K. and Y.L. contributed to discussions and provided valuable advice on interpreting the research findings. T.R., T.F. and G.C. wrote the initial version of the manuscript. All authors contributed to subsequent versions and have read and approved the manuscript.

Corresponding authors

Correspondence to Gitta Coaker or Tzion Fahima.

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Nature Genetics thanks Manuel Spannagl and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Domain diversity and proportion of TKPs identified from predicted proteomes.

a, The proportion of TKPs compared to the total proteome size. b, TKPs containing two to five kinase domains and their family membership.

Extended Data Fig. 2 Genomic position of TKPs on chromosomes of cereal species.

a, Aegilops tauschii 2n = 2x = 14, DD; b, Triticum urartu 2n = 2x = 14, AA; c, Triticum turgidum subsp. durum 2n = 4x = 28, AABB; d, Triticum turgidum subsp. dicoccoides 2n = 4x = 28, AABB; e, Triticum aestivum 2n = 6x = 42, AABBDD; f, Triticum spelta 2n = 6x = 42, AABBDD. Yellow lines indicate the TKPs positions.

Extended Data Fig. 3 A tree with the nine species having the most abundant number of TKPs.

Bars demonstrate the presence/absence of a transmembrane region (TM), a signal peptide (SP) and at least one integrated (nonkinase) domain (ID). The tree represents taxonomy, created using the ete toolkit v3.1.2, showcasing total TKP counts as a bar chart. This tree illustrates qualitative branching patterns, excluding distance information.

Extended Data Fig. 4 Distance histogram calculated on domain sequences with matching family annotations.

a, For TKPs with two domains from the RLK–Pelle Lec family. b, For TKPs with two domains from RLK–Pelle DLSV family. Pairwise distances were calculated for sequences from two subfamilies by dist.alignment function from seqinr (version 4.2-16) R package.

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Supplementary Information

Supplementary Note and Supplementary Tables 1–5.

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Reveguk, T., Fatiukha, A., Potapenko, E. et al. Tandem kinase proteins across the plant kingdom. Nat Genet 57, 254–262 (2025). https://doi.org/10.1038/s41588-024-02032-x

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