Pangenomic context reveals the extent of intraspecific plant NLR evolution

Luisa C. Teasdale; Kevin D. Murray; Max Collenberg; Adrian Contreras-Garrido; Theresa Schlegel; Leon van Ess; Justina Jüttner; Christa Lanz; Oliver Deusch; Joffrey Fitz; Regina Mencia; Rosanne van Velthoven; Hajk Georg Drost; Detlef Weigel; Gautam Shirsekar

doi:10.1016/j.chom.2025.07.011

Pangenomic context reveals the extent of intraspecific plant NLR evolution

Luisa C. Teasdale
, Kevin D. Murray
, Max Collenberg
, Adrian Contreras-Garrido
, Theresa Schlegel
, Leon van Ess
, Justina Jüttner
, Christa Lanz
, Oliver Deusch
, Joffrey Fitz
, Regina Mencia
, Rosanne van Velthoven
, Hajk Georg Drost
, Detlef Weigel (Lead / Corresponding author)
, Gautam Shirsekar (Lead / Corresponding author)

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

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Abstract

Nucleotide-binding leucine-rich repeat (NLR) proteins are major components of the plant immune system, recognizing pathogen effectors and triggering defense responses. Because of the diversity of pathogen effector repertoires, NLRs have extraordinary sequence, structural, and regulatory variability. Although processes contributing to NLR diversity have been identified, the precise evolution of NLRs in their genomic context and along the multiple axes of diversity has been difficult to trace. We integrate genome-specific full-length transcript, homology, and transposable element information to annotate 3,789 NLRs in 17 diverse Arabidopsis thaliana accessions. We define 121 pangenomic NLR neighborhoods, which vary greatly in size, content, and complexity. NLRs are diverse across many axes, and multiple metrics are required to fully capture NLR variation. Based on these findings, we propose that diversity in diversity generation is fundamental to maintaining a functionally “adaptive” immune system in plants and that mechanistic studies should consider multiple axes of immune system diversity.

Original language	English
Pages (from-to)	1291-1305.e9
Journal	Cell Host and Microbe
Volume	33
Issue number	8
DOIs	https://doi.org/10.1016/j.chom.2025.07.011
Publication status	Published - 13 Aug 2025

Keywords

genome evolution
immunity
NLR
pangenome graphs
plant-pathogen interactions
TE

ASJC Scopus subject areas

Parasitology
Microbiology
Virology

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10.1016/j.chom.2025.07.011Licence: CC BY

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Teasdale et al., 2025, Cell Host & Microbe 33, 1291–1305 © 2025 The Author(s). Published by Elsevier Inc. https://doi.org/10.1016/j.chom.2025.07.011javascript:void(0);
Final published version, 8.74 MBLicence: CC BY

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Teasdale, L. C., Murray, K. D., Collenberg, M., Contreras-Garrido, A., Schlegel, T., van Ess, L., Jüttner, J., Lanz, C., Deusch, O., Fitz, J., Mencia, R., van Velthoven, R., Drost, H. G., Weigel, D., & Shirsekar, G. (2025). Pangenomic context reveals the extent of intraspecific plant NLR evolution. Cell Host and Microbe, 33(8), 1291-1305.e9. https://doi.org/10.1016/j.chom.2025.07.011

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title = "Pangenomic context reveals the extent of intraspecific plant NLR evolution",

abstract = "Nucleotide-binding leucine-rich repeat (NLR) proteins are major components of the plant immune system, recognizing pathogen effectors and triggering defense responses. Because of the diversity of pathogen effector repertoires, NLRs have extraordinary sequence, structural, and regulatory variability. Although processes contributing to NLR diversity have been identified, the precise evolution of NLRs in their genomic context and along the multiple axes of diversity has been difficult to trace. We integrate genome-specific full-length transcript, homology, and transposable element information to annotate 3,789 NLRs in 17 diverse Arabidopsis thaliana accessions. We define 121 pangenomic NLR neighborhoods, which vary greatly in size, content, and complexity. NLRs are diverse across many axes, and multiple metrics are required to fully capture NLR variation. Based on these findings, we propose that diversity in diversity generation is fundamental to maintaining a functionally “adaptive” immune system in plants and that mechanistic studies should consider multiple axes of immune system diversity.",

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author = "Teasdale, \{Luisa C.\} and Murray, \{Kevin D.\} and Max Collenberg and Adrian Contreras-Garrido and Theresa Schlegel and \{van Ess\}, Leon and Justina J{\"u}ttner and Christa Lanz and Oliver Deusch and Joffrey Fitz and Regina Mencia and \{van Velthoven\}, Rosanne and Drost, \{Hajk Georg\} and Detlef Weigel and Gautam Shirsekar",

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Teasdale, LC, Murray, KD, Collenberg, M, Contreras-Garrido, A, Schlegel, T, van Ess, L, Jüttner, J, Lanz, C, Deusch, O, Fitz, J, Mencia, R, van Velthoven, R, Drost, HG, Weigel, D & Shirsekar, G 2025, 'Pangenomic context reveals the extent of intraspecific plant NLR evolution', Cell Host and Microbe, vol. 33, no. 8, pp. 1291-1305.e9. https://doi.org/10.1016/j.chom.2025.07.011

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T1 - Pangenomic context reveals the extent of intraspecific plant NLR evolution

AU - Teasdale, Luisa C.

AU - Murray, Kevin D.

AU - Collenberg, Max

AU - Contreras-Garrido, Adrian

AU - Schlegel, Theresa

AU - van Ess, Leon

AU - Jüttner, Justina

AU - Lanz, Christa

AU - Deusch, Oliver

AU - Fitz, Joffrey

AU - Mencia, Regina

AU - van Velthoven, Rosanne

AU - Drost, Hajk Georg

AU - Weigel, Detlef

AU - Shirsekar, Gautam

PY - 2025/8/13

Y1 - 2025/8/13

N2 - Nucleotide-binding leucine-rich repeat (NLR) proteins are major components of the plant immune system, recognizing pathogen effectors and triggering defense responses. Because of the diversity of pathogen effector repertoires, NLRs have extraordinary sequence, structural, and regulatory variability. Although processes contributing to NLR diversity have been identified, the precise evolution of NLRs in their genomic context and along the multiple axes of diversity has been difficult to trace. We integrate genome-specific full-length transcript, homology, and transposable element information to annotate 3,789 NLRs in 17 diverse Arabidopsis thaliana accessions. We define 121 pangenomic NLR neighborhoods, which vary greatly in size, content, and complexity. NLRs are diverse across many axes, and multiple metrics are required to fully capture NLR variation. Based on these findings, we propose that diversity in diversity generation is fundamental to maintaining a functionally “adaptive” immune system in plants and that mechanistic studies should consider multiple axes of immune system diversity.

AB - Nucleotide-binding leucine-rich repeat (NLR) proteins are major components of the plant immune system, recognizing pathogen effectors and triggering defense responses. Because of the diversity of pathogen effector repertoires, NLRs have extraordinary sequence, structural, and regulatory variability. Although processes contributing to NLR diversity have been identified, the precise evolution of NLRs in their genomic context and along the multiple axes of diversity has been difficult to trace. We integrate genome-specific full-length transcript, homology, and transposable element information to annotate 3,789 NLRs in 17 diverse Arabidopsis thaliana accessions. We define 121 pangenomic NLR neighborhoods, which vary greatly in size, content, and complexity. NLRs are diverse across many axes, and multiple metrics are required to fully capture NLR variation. Based on these findings, we propose that diversity in diversity generation is fundamental to maintaining a functionally “adaptive” immune system in plants and that mechanistic studies should consider multiple axes of immune system diversity.

KW - genome evolution

KW - immunity

KW - NLR

KW - pangenome graphs

KW - plant-pathogen interactions

KW - TE

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AN - SCOPUS:105012840106

SN - 1931-3128

VL - 33

SP - 1291-1305.e9

JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 8

ER -

Pangenomic context reveals the extent of intraspecific plant NLR evolution

Abstract

Keywords

ASJC Scopus subject areas

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