Genome-wide comparative analysis of NBS-encoding genes in four Gossypium species

Abstract

BackgroundNucleotide binding site (NBS) genes encode a large family of disease resistance (R) proteins in plants. The availability of genomic data of the two diploid cotton species, Gossypium arboreum and Gossypium raimondii, and the two allotetraploid cotton species, Gossypium hirsutum (TM-1) and Gossypium barbadense allow for a more comprehensive and systematic comparative study of NBS-encoding genes to elucidate the mechanisms of cotton disease resistance.ResultsBased on the genome assembly data, 246, 365, 588 and 682 NBS-encoding genes were identified in G. arboreum, G. raimondii, G. hirsutum and G. barbadense, respectively. The distribution of NBS-encoding genes among the chromosomes was nonrandom and uneven, and was tended to form clusters. Gene structure analysis showed that G. arboreum and G. hirsutum possessed a greater proportion of CN, CNL, and N genes and a lower proportion of NL, TN and TNL genes compared to that of G. raimondii and G. barbadense, while the percentages of RN and RNL genes remained relatively unchanged. The percentage changes among them were largest for TNL genes, about 7 times. Exon statistics showed that the average exon numbers per NBS gene in G. raimondii and G. barbadense were all greater than that in G. arboretum and G. hirsutum. Phylogenetic analysis revealed that the TIR-NBS genes of G. barbadense were closely related with that of G. raimondii. Sequence similarity analysis showed that diploid cotton G. arboreum possessed a larger proportion of NBS-encoding genes similar to that of allotetraploid cotton G. hirsutum, while diploid G. raimondii possessed a larger proportion of NBS-encoding genes similar to that of allotetraploid cotton G. barbadense. The synteny analysis showed that more NBS genes in G. raimondii and G. arboreum were syntenic with that in G. barbadense and G. hirsutum, respectively.ConclusionsThe structural architectures, amino acid sequence similarities and synteny of NBS-encoding genes between G. arboreum and G. hirsutum, and between G. raimondii and G. barbadense were the highest among comparisons between the diploid and allotetraploid genomes, indicating that G. hirsutum inherited more NBS-encoding genes from G. arboreum, while G. barbadense inherited more NBS-encoding genes from G. raimondii. This asymmetric evolution of NBS-encoding genes may help to explain why G. raimondii and G. barbadense are more resistant to Verticillium wilt, whereas G. arboreum and G. hirsutum are more susceptible to Verticillium wilt. The disease resistances of the allotetraploid cotton were related to their NBS-encoding genes especially in regard from which diploid progenitor they were derived, and the TNL genes may have a significant role in disease resistance to Verticillium wilt in G. raimondii and G. barbadense.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3682-x) contains supplementary material, which is available to authorized users.

Genome-Wide Identification of NBS-Encoding Resistance Genes in Sunflower (Helianthus annuus L.)

“…In C. sativus , 33 NBS genes were located in nine clusters [ 33 ]. The average number of NBS proteins per cluster in sunflower was approximately 2.7, lesser than ratios in Solanaceae species such as tomato (3.48), potato (4.65), pepper (3.44) [ 80 ], Brassicaceae species such as B. oleracea (3.04), B. rapa (2.7), A. thaliana (2.8) [ 5 ], Fabaceae species such as G. max (4), V. vinifera (6), M. truncatula (5) [ 16 ], Gossypium species such as G. arboretum (3.4), G. raimondii (5.5), G. hirsutum (5.3), and G. barbadense (3.5) [ 34 ]. Both segmental and tandem duplications are responsible for the formation of new clusters that generate intraspecific variation by processes such as unequal crossing over [ 9 , 14 , 81 ].…”

“… Note: Ha: Helianthus annuus ; At: Arabidopsis thaliana ; Gm: Glycine max ; Mt: Medicago truncatula ; Bo: Brassica oleracea ; Br: Brassica rapa ; Tc: Theobroma cacao ; Pt: Populus trichocarpa ; Vv: Vitis vinifera ; Ca: Cicer arietinum ; Cs: Cucumus sativus ; Pv: Phaseolus vulgaris ; Lj: Lotus japonicas ; Cc: Cajanus cajan ; Gs: Glycine soja ; Ga: Gossypium arboretum (* = this study, a = [ 5 ], b = [ 23 ], c = [ 24 ], d = [ 20 ], e = [ 33 ], f = [ 16 ], g = [ 34 ]). …”

“…With the increasing availability of plant genome sequences, R gene proteins have been identified in many plant species, such as A. thaliana [ 5 , 14 ]; Vaccinium spp. [ 19 ]; Amborella trichopoda , Musa acuminata , Phyllostachys heterocycla , Capsicum annuum , and Sesamum indicum by Shao et al 2016 [ 13 ]; Cicer arietinum [ 20 ]; Glycine max [ 21 , 22 , 23 , 24 ]; Oryza sativa [ 25 , 26 ]; Medicago truncatula [ 27 ]; Vitis vinifera and Populus trichocarpa by Yang et al 2008 [ 28 ]; Solanum tuberosum [ 29 ]; Brassica rapa and Brassica oleracea by Zhang et al 2016 [ 30 ]; Hordeum vulgare [ 31 ]; Setaria italica [ 32 ]; Theobroma cacao [ 5 ]; Populus trichocarpa [ 5 ]; V. vinifera [ 5 ]; Cucumis sativus [ 33 ]; Phaseolus vulgaris [ 16 , 24 ], Lotus japonicas , Cajanus cajan , Glycine soja by Zheng et al 2016 [ 16 ], Gossypium arboretum [ 34 ], etc. A recent study by Li et al 2016 [ 35 ] has identified NBS-encoding genes as well as receptor-like protein kinases (RLKs) and receptor-like proteins (RLPs), collectively called as Resistance Gene Analogs (RGAs), for 50 plant genomes using a RGAugury pipeline.…”

Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA-seq

“…Moreover, 12 circRNAs were commonly and differentially expressed in all the root comparisons ( Table 1 ), and the source gene of ghi_circ_000336, the Gh_D01G0335 gene, was annotated as an NBS family gene. The NBS gene family is the largest disease resistance gene family in plants and plays a central role in recognizing effectors from pathogens and in triggering downstream signalling during the plant response to pathogen invasion ( Yue et al, 2012 ; McHale et al, 2006 ; Zhao et al, 2017 ; Xiang et al, 2017 ). These results indicated that the NBS family genes in cotton may play a role in Verticillium wilt resistance and might be regulated by circRNAs in the disease-resistance process.…”

Heterologous Expression of the Cotton NBS-LRR Gene GbaNA1 Enhances Verticillium Wilt Resistance in Arabidopsis

“…Several NB-LRR genes have been identified to function as R genes in A. thaliana , including RPM1, RPS1, RPS2, RPS4 , and RPS5 ( Lee and Yeom, 2015 ). In cotton, the genome has an expanded repertoire of NBS-encoding genes ( Xiang et al, 2017 ), even notable in the diploid genome of G. raimondii that encodes more than 300 of these types of genes ( Paterson et al, 2012 ). Comparative genomic analysis showed that the NBS-encoding genes are significantly expanded in G. raimondii , which is nearly immune to Verticillium wilt, as compared to G. arboretum , which is susceptible to Verticillium wilt ( Li et al, 2014 ).…”