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Full-genome identification and characterization of NBS-encoding disease resistance genes in wheat

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Abstract

Host resistance is the most economical, effective and ecologically sustainable method of controlling diseases in crop plants. In bread wheat, despite the high number of resistance loci that have been cataloged to date, only few have been cloned, underlying the need for genomics-guided investigations capable of providing a prompt and acute knowledge on the identity of effective resistance genes that can be used in breeding programs. Proteins with a nucleotide-binding site (NBS) encoded by the major plant disease resistance (R) genes play an important role in the responses of plants to various pathogens. In this study, a comprehensive analysis of NBS-encoding genes within the whole wheat genome was performed, and the genome scale characterization of this gene family was established. From the recently published wheat genome sequence, we used a data mining and automatic prediction pipeline to identify 580 complete ORF candidate NBS-encoding genes and 1,099 partial-ORF ones. Among complete gene models, 464 were longer than 200 aa, among them 436 had less than 70 % of sequence identity to each other. This gene models set was deeply characterized. (1) First, we have analyzed domain architecture and identified, in addition to typical domain combinations, the presence of particular domains like signal peptides, zinc fingers, kinases, heavy-metal-associated and WRKY DNA-binding domains. (2) Functional and expression annotation via homology searches in protein and transcript databases, based on sufficient criteria, enabled identifying similar proteins for 60 % of the studied gene models and expression evidence for 13 % of them. (3) Shared orthologous groups were defined using NBS-domain proteins of rice and Brachypodium distachyon. (4) Finally, alignment of the 436 NBS-containing gene models to the full set of scaffolds from the IWGSC’s wheat chromosome survey sequence enabled high-stringence anchoring to chromosome arms. The distribution of the R genes was found balanced on the three wheat sub-genomes. In contrast, at chromosome scale, 50 % of members of this gene family were localized on 6 of the 21 wheat chromosomes and ~22 % of them were localized on homeologous group 7. The results of this study provide a detailed analysis of the largest family of plant disease resistance genes in allohexaploid wheat. Some structural traits reported had not been previously identified and the genome-derived data were confronted with those stored in databases outlining the functional specialization of members of this family. The large reservoir of NBS-type genes presented and discussed will, firstly, form an important framework for marker-assisted improvement of resistance in wheat, and, secondly, open up new perspectives for a better understanding of the evolution dynamics of this gene family in grass species and in polyploid systems.

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Acknowledgments

We gratefully acknowledge Jacques-Déric Rouault (Laboratoire Evolution, Génome et Spéciation, CNRS, Gif sur Yvette, France) for providing training; Abdelkader Aïnouche and Malika-Lily Aïnouche (UMR-CNRS Ecobio, Université de Rennes-1, France) for useful discussion and manuscript revision, and Rafika Challouf (Institut National des Sciences et Technologies de la Mer, INSTM, Monastir, Tunisia) for providing help in computational analyses. This study was financially supported by the Tunisian Ministry of Higher Education and Scientific Research.

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Unité de Recherche “Génomique des Insectes Ravageurs des Cultures d’intérêt agronomique” (GIRC, UR11ES10), Faculté des Sciences de Tunis, Université de Tunis El Manar, El Manar, 2092, Tunis, Tunisia

    Dhia Bouktila, Yosra Khalfallah, Yosra Habachi-Houimli, Maha Mezghani-Khemakhem, Mohamed Makni & Hanem Makni

  2. Institut Supérieur de Biotechnologie de Béja (ISBB), Université de Jendouba, Avenue Habib Bourguiba, 9000, Béja, Tunisia

    Dhia Bouktila

  3. Institut Supérieur de l’Animation pour la Jeunesse et la Culture (ISAJC), Université de Tunis, Bir-El-Bey, Tunisia

    Hanem Makni

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  1. Dhia Bouktila
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Correspondence to Dhia Bouktila.

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Communicated by: S. Hohmann.

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Bouktila, D., Khalfallah, Y., Habachi-Houimli, Y. et al. Full-genome identification and characterization of NBS-encoding disease resistance genes in wheat. Mol Genet Genomics 290, 257–271 (2015). https://doi.org/10.1007/s00438-014-0909-2

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  • DOI: https://doi.org/10.1007/s00438-014-0909-2

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