Evidence map›Paper›PMID 26839128›Full record

ArticlePlant physiology2016

Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns.

Zhu-Qing Shao, Jia-Yu Xue, Ping Wu, Yan-Mei Zhang, Yue Wu, Yue-Yu Hang, Bin Wang, Jian-Qun Chen

Open access · greenAbstract read
In one paragraph

Article in Plant physiology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 178 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
178citing papers in PubMed, 1 pooled it
50.0field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

178 citing papers in PubMed, 1 synthesis or guideline pooled it, 330 citations in OpenAlex.

  1. Pooled it
  2. Review
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  5. Article
  6. Article
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  8. Article
  9. Article
  10. Plant NLRs are getting into higher-order architectures.The Plant journal : for cell and molecular biology · 2026
    Review
  11. Review
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  14. Dissection of Cell Death Induction byLife (Basel, Switzerland) · 2026
    Article
  15. Article
  16. Pan-NLRome ofFrontiers in plant science · 2026
    Article
  17. Article
  18. Article
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  20. Article

118 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

8 authors at 2 institutions in 1 country.

Zhu-Qing ShaoState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Jia-Yu XueState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Ping WuState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Yan-Mei ZhangState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Yue WuState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Yue-Yu HangState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.).
Bin WangState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.) chenjq@nju.edu.cn binwang@nju.edu.cn.
Jian-Qun ChenState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210023, China (Z.-Q.S., P.W., Y.-M.Z., Y.W., B.W., J.-Q.C.); andInstitute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China (J.-Y.X., Y.-M.Z., Y.-Y.H.) chenjq@nju.edu.cn binwang@nju.edu.cn.
Nanjing University · CNChinese Academy of Sciences · CN

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

Abstract

Nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes make up the largest plant disease resistance gene family (R genes), with hundreds of copies occurring in individual angiosperm genomes. However, the expansion history of NBS-LRR genes during angiosperm evolution is largely unknown. By identifying more than 6,000 NBS-LRR genes in 22 representative angiosperms and reconstructing their phylogenies, we present a potential framework of NBS-LRR gene evolution in the angiosperm. Three anciently diverged NBS-LRR classes (TNLs, CNLs, and RNLs) were distinguished with unique exon-intron structures and DNA motif sequences. A total of seven ancient TNL, 14 CNL, and two RNL lineages were discovered in the ancestral angiosperm, from which all current NBS-LRR gene repertoires were evolved. A pattern of gradual expansion during the first 100 million years of evolution of the angiosperm clade was observed for CNLs. TNL numbers remained stable during this period but were eventually deleted in three divergent angiosperm lineages. We inferred that an intense expansion of both TNL and CNL genes started from the Cretaceous-Paleogene boundary. Because dramatic environmental changes and an explosion in fungal diversity occurred during this period, the observed expansions of R genes probably reflect convergent adaptive responses of various angiosperm families. An ancient whole-genome duplication event that occurred in an angiosperm ancestor resulted in two RNL lineages, which were conservatively evolved and acted as scaffold proteins for defense signal transduction. Overall, the reconstructed framework of angiosperm NBS-LRR gene evolution in this study may serve as a fundamental reference for better understanding angiosperm NBS-LRR genes.

Indexed as

Evolution, MolecularGenes, PlantGenetic VariationArabidopsisBase SequenceBinding SitesExonsIntronsMagnoliopsidaNLR ProteinsNucleotide MotifsPhylogenySpecies SpecificityNLR Proteins

Identifiers

PMID26839128
PMCPMC4825152
OpenAlexW2269502061

What OpenQuestion holds

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.