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Convergent reduction of immune receptor repertoires during plant adaptation to diverse special lifestyles and habitats

Nature Plants volume 11, pages 248–262 (2025)Cite this article

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Abstract

Plants deploy cell-surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding site–leucine-rich repeat receptors (NLRs) to recognize pathogens. However, how plant immune receptor repertoires evolve in responding to changed pathogen burdens remains elusive. Here we reveal the convergent reduction of NLR repertoires in plants with diverse special lifestyles/habitats (SLHs) encountering low pathogen burdens. Furthermore, a parallel but milder reduction of PRR genes in SLH species was observed. The reduction of PRR and NLR genes was attributed to both increased gene loss and decreased gene duplication. Notably, pronounced loss of immune receptors was associated with the complete absence of signalling components from the enhanced disease susceptibility 1 (EDS1) and the resistance to powdery mildew 8 (RPW8)-NLR (RNL) families. In addition, evolutionary pattern analysis suggested that the conserved toll/interleukin-1 receptor (TIR)-only proteins might function tightly with EDS1/RNL. Taken together, these results reveal the hierarchically adaptive evolution of the two-tiered immune receptor repertoires during plant adaptation to diverse SLHs.

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Fig. 1: Identification and classification of immune receptor genes across 808 angiosperm genomes.
Fig. 2: Concerted contraction of NLR gene number among SLH species.
Fig. 3: Concerted contraction of the LRR-RLK XII and LRR-RLPID+4LRR genes among SLH species.
Fig. 4: Evolutionary patterns of immune pathway signalling components.
Fig. 5: Presence/absence mode of immune signalling candidates in species lacking EDS1 family genes.
Fig. 6: Schematic diagram illustrating the hierarchically adaptive evolution of two-tiered immune receptor genes during diverse ecological specialization.

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Data availability

With reference to PlaBI (https://www.plabipd.de/pubplant_cladogram1.html), we collected accessions of sequenced plant genomes that have been published in peer-reviewed journals. Accordingly, the annotated proteomes of 808 angiosperm genomes were downloaded from publicly available databases, such as NCBI (https://www.ncbi.nlm.nih.gov/assembly/), NGDC (https://ngdc.cncb.ac.cn/gwh/), CNGBdb (https://db.cngb.org/), Phytozome (https://phytozome-next.jgi.doe.gov/), CoGe (https://genomevolution.org/coge/), GigaDB (http://gigadb.org/), Ensembl Plants (http://plants.ensembl.org/index.html) and Plant GARDEN (https://plantgarden.jp/en/index). The complete list of species taxa, references and download links is curated in Supplementary Table 1. The information on the sequencing, assembly and annotation of each genome retrieved from the N3 database (http://ibi.zju.edu.cn/N3database/)96, original publications and deposited databases is also curated in Supplementary Table 1. The protein sequences of the PRR, NLR, EDS1, cTIR, TNP and MLKL genes from 808 angiosperms that were identified and classified in this study have been deposited in AirDB (https://efg.nju.edu.cn/AirDB/). Source data are provided with this paper.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32270241 and 32070243 to Z.-Q.S., 32170218 to J.-Q.C., and 32172089 to Y.-M.Z.), the NSFC-FDCT Grant (32461160254 to J.-Q.C.), the Jiangsu Agricultural Science and Technology Independent Innovation Fund (CX(23)3116 to Z.-Q.S.), and the National Postdoctoral Science Foundation of China (2022M721558 and 2024T170408 to Y.L.). Y.L. was supported by the Jiangsu Excellent Postdoctoral Funding (2022ZB45), and Z.-Q.S. was supported by the Outstanding Young Teacher of ‘QingLan Project’ of Jiangsu Province. We thank W.-L. Wu for providing the cartoon elements in Fig. 6.

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Author notes

  1. These authors contributed equally: Sai-Xi Li, Yang Liu.

Authors and Affiliations

  1. State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, China

    Sai-Xi Li, Yang Liu, Jian-Qun Chen & Zhu-Qing Shao

  2. Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, China

    Yan-Mei Zhang

  3. Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Nanjing, China

    Yan-Mei Zhang

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  1. Sai-Xi Li
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Contributions

Z.-Q.S. and J.-Q.C. conceived and designed the research. S.-X.L., Y.L. and Y.-M.Z. obtained and analysed the data. S.-X.L. and Z.-Q.S. interpreted the data. S.-X.L. constructed the database. S.-X.L. drafted the manuscript. Z.-Q.S. and J.-Q.C. revised the manuscript.

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Correspondence to Jian-Qun Chen or Zhu-Qing Shao.

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Extended data

Extended Data Fig. 1 Comparison of PRR gene numbers identified in this study with previous publications.

a Comparison of IR-RLK gene number in this study with all RLK gene number in Li et al. (RGAugury)43 for the corresponding species. b Comparison of LRR-RLK gene number in this study with LRR-RLK gene number in Yin et al. (HMMER, deepTMHMM)44 for the corresponding species. c Comparison of LRR-RLK XII gene number in this study with LRR-RLK XII gene number in Dufayard et al. (HMMER, TMHMM, TopPred)45 for the corresponding species. d Comparison of IR-RLP gene number in this study with all RLP gene number in Li et al. (RGAugury)43 for the corresponding species. Each scatter plot contains the linear regression trend (solid line), 95% confidence interval (dark gray shade), 95% prediction interval (light gray shade), and Pearson's correlation coefficient with two-sided test. Two-sided Wilcoxon matched-pairs signed-ranks tests were conducted for boxplots (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range).

Extended Data Fig. 2 Comparison of NLR gene numbers identified in this study with previous publications.

a Comparison of NLR gene number in this study with the NLR gene number in Li et al. (RGAugury)43 for the corresponding species. b Comparison of NLR gene number in this study with NLR gene number in Baggs et al. (NLR-Annotator)41 for the corresponding species. c Comparison of NLR gene number in this study with NLR gene number in Krourelis et al. (NLRtracker)46 for the corresponding species. d Comparison of NLR gene number in this study with NLR gene number in Qin et al. (HMMER, MAFFT, Fasttree)47 for the corresponding species. Each scatter plot contains the linear regression trend (solid line), 95% confidence interval (dark gray shade), 95% prediction interval (light gray shade), and Pearson's correlation coefficient with two-sided test. Two-sided Wilcoxon matched-pairs signed-ranks tests were conducted for boxplots (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range).

Extended Data Fig. 3 Correlations between genome size, CDS number, and immune receptor gene number.

The diagonal boxes include histograms representing the distributions of genome sizes (Mb), CDS numbers, and gene numbers of NLR, LRR-RLK XII, and LRR-RLPID+4LRR from 808 angiosperms, respectively. The bottom left boxes contain the scatter plots between genome sizes, CDS numbers, and immune receptor gene numbers from 808 angiosperms, with the solid lines representing the linear trends and the light blue shades representing 95% confidence intervals. The top right boxes provide the corresponding values of the Pearson correlation coefficient (Pearson’s r) with two-sided statistical test (***: P < 0.001).

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Extended Data Fig. 4 Evaluation of the impact of genome quality and species domestication on NLR comparison.

a NLR gene number in SLH and non-SLH species under similar metrics of genome sequencing [third-generation sequencing (TGS), next-generation sequencing (NGS), and Sanger], assembly [chromosome-level and non-chromosome-level; contig N50 size (the length of the shortest contig at 50% of the total assembly length)], and annotation [benchmarking universal single-copy orthologs (BUSCO)]. The distribution of NLR gene numbers is represented by the boxplot (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range; outliers not shown). The SLH species and non-SLH species are indicated in salmon and blue, respectively. Pairwise significance was determined by two-sided Mann‒Whitney U test between SLH and non-SLH angiosperms (****: P < 0.0001). Species lacking the information of genome quality (for example contig N50) were not included in this analysis. b NLR gene number in SLH, wild, and domesticated species. The distribution of NLR gene numbers is represented by the boxplot (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range; outliers not shown). Pairwise significance was determined by two-sided Mann‒Whitney U test between SLH and non-SLH angiosperms, respectively (ns: P > 0.05; ****: P < 0.0001).

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Extended Data Fig. 5 Comparison of NLR gene number between SLH and non-SLH species within the same family.

The phylogenetic tree of SLH species within each family is extracted from Supplementary Fig. 1. Clades of Orchidaceae (n = 10), Poaceae (n = 85), Salicaceae (n = 14), Fabaceae (n = 51), Brassicaceae (n = 44), Amaranthaceae (n = 12), and Solanaceae (n = 45) are indicated in alternate color stripes superimposed on the species tree. The NLR gene number is represented by the bar plot, with SLH species indicated in color as Fig. 2a and the average of non-SLH species in each family indicated in gray. Pairwise significance was determined by two-sided one sample Wilcoxon signed-rank test between each SLH plant and its non-SLH relatives within the same family, respectively (ns: P > 0.05; *: P < 0.05; **: P < 0.01; ***: P < 0.001; ****: P < 0.0001).

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Extended Data Fig. 6 Evaluation of the impact of genome quality and species domestication on LRR-RLK XII and LRR-RLPID+4LRR comparison.

a LRR-RLK XII and LRR-RLPID+4LRR gene number in SLH and non-SLH species under similar metrics of genome sequencing [third-generation sequencing (TGS), next-generation sequencing (NGS), and Sanger], assembly [chromosome-level and non-chromosome-level; contig N50 size (the length of the shortest contig at 50% of the total assembly length)], and annotation [benchmarking universal single-copy orthologs (BUSCO)]. The distribution of LRR-RLK XII and LRR-RLPID+4LRR gene numbers is represented by the boxplot (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range; outliers not shown). The SLH species and non-SLH species are indicated in salmon and blue, respectively. Pairwise significance was determined by two-sided Mann‒Whitney U test between SLH and non-SLH angiosperms (***: P < 0.001; ****: P < 0.0001). Species lacking the information of genome quality (for example contig N50) were not included in this analysis. b LRR-RLK XII and LRR-RLPID+4LRR gene number in SLH, wild, and domesticated species. The distribution of LRR-RLK XII and LRR-RLPID+4LRR gene numbers is represented by the boxplot (centre line: median; box limits: upper and lower quartiles; whiskers: 1.5x interquartile range; outliers not shown). Pairwise significance was determined by two-sided Mann‒Whitney U test between SLH and non-SLH angiosperms, respectively (ns: P > 0.05; ****: P < 0.0001).

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Extended Data Fig. 7 Comparison of LRR-RLK XII and LRR-RLPID+4LRR gene number between SLH and non-SLH species within the same family.

The phylogenetic tree of SLH species within each family is extracted from Supplementary Fig. 1. Clades of Orchidaceae (n = 10), Poaceae (n = 85), Salicaceae (n = 14), Fabaceae (n = 51), Brassicaceae (n = 44), Amaranthaceae (n = 12), and Solanaceae (n = 45) are indicated in alternate color stripes superimposed on the species tree. The LRR-RLK XII (a) and LRR-RLPID+4LRR (b) gene number is represented by the bar plot, with SLH species indicated in color as Fig. 3a and the average of non-SLH species in each family indicated in gray. Pairwise significance was determined by two-sided one sample Wilcoxon signed-rank test between each SLH plant and its non-SLH relatives within the same family, respectively (ns: P > 0.05; *: P < 0.05; **: P < 0.01; ***: P < 0.001; ****: P < 0.0001).

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Extended Data Fig. 8 Distribution of RNL and EDS1 family genes across 808 angiosperms.

The phylogenetic tree of 808 angiosperm species is corresponding to Supplementary Fig. 1. The numbers of RNL (NRG1 and ADR1) and EDS1 family (EDS1, SAG101 and PAD4) genes are represented by the heatmap. The color key is shown at the bottom, with white indicating no detectable gene.

Extended Data Fig. 9 Distribution of cTIR, TNP, and MLKL genes across 808 angiosperms.

The phylogenetic tree of 808 angiosperm species is corresponding to Supplementary Fig. 1. The numbers of cTIR, TNP, and MLKL genes are represented by the heatmap. The color key is shown at the bottom, with white indicating no detectable gene.

Extended Data Fig. 10 Presence/absence mode of PTI and ETI pathway components in species lacking EDS1 family genes.

The presence and absence of the PTI and ETI pathway components are indicated by the solid and open circles, respectively, with the color of the circles reflecting presence of the components of ETI (orange) or PTI (green).

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Li, SX., Liu, Y., Zhang, YM. et al. Convergent reduction of immune receptor repertoires during plant adaptation to diverse special lifestyles and habitats. Nat. Plants 11, 248–262 (2025). https://doi.org/10.1038/s41477-024-01901-x

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