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

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.

Large-scale bioinformatic analysis of the regulation of the disease resistance NBS gene family by microRNAs in Poaceae

“…For H. vulgare and T. aestivum, 318 and 580 NBS-type gene models previously predicted from the whole genome shotgun sequence assembly of barley cv. Bowman and the LCG assembly of T. aestivum, respectively [15] were used in this study. From both sets, we have selected 257 barley and 286 wheat NBS gene models, following examination of the conservation of core NBS with MEME.…”

“…Studies of the NBS gene family have been performed in many monocot and dicot plant species, such as Arabidopsis [7], rice [8], Medicago truncatula [9], Poplar [10], grape [11], sorghum [12], Lotus japonica [13], Brassica rapa [14], Triticum aestivum [15], Brachypodium distachyon [16] and Hordeum vulgare (Y. Habachi-Houimli, Y. Khalfallah, H. Makni, M. Makni, D. Bouktila, unpublished data). All results have shown that the size of this gene family differs in each species.…”

Strategies for transferring resistance into wheat: from wide crosses to GM cassettes

“…Negotiating this terrain is no simple task. Wheat is no exception and contains ∼600 NB-LRRs ( Bouktila et al, 2014 ; IWGSC, 2014 ), although this is most likely an underestimate because short read sequencing technologies lack the discriminatory power to assemble such large gene families. An accurate, high-throughput, and cost-efficient long-read technology is required to overcome this limitation.…”

Rapid evolutionary dynamics in a 2.8‐Mb chromosomal region containing multiple prolamin and resistance gene families in Aegilops tauschii

“…The evolution of NLR and RLK gene sequences in plant genomes is very dynamic. Comparative genomic analyses have indicated that plant genomes encode hundreds of NLR and RLK genes (Meyers et al ., ; Afzal et al ., ; Bouktila et al ., ). Apparently, both whole genome and segmental duplications have contributed to the large family number of these R genes (Meyers et al ., ).…”