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Genomic regions conferring resistance to multiple fungal pathogens in synthetic hexaploid wheat

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Abstract

Fungal diseases are among the most devastating biotic stresses and often cause significant losses in wheat production worldwide. A set of 173 synthetic hexaploid wheat (SHW) characterized for resistance against fungal pathogens that cause leaf, stem and yellow rusts, yellow leaf spot, Septoria nodorum and crown rot were used in genome-wide association study (GWAS). Diversity Arrays Technology (DArT) and DArTSeq markers were employed for marker–trait association in which 74 markers associated with 35 quantitative trait loci (QTL) were found to be significantly linked with disease resistances using a unified mixed model (P = 10−3 to 10−5); Of these 15 QTL originated from D genome. Six markers on 1BL, 3BS, 4BL, 6B, and 6D conferred resistance to two diseases representing 10 of the 35 QTL. A further set of 147 SHW genotyped with DArT only markers validated 11 QTL detected in the previous 173 SHW. We also confirmed the presence of the gene Lr46/Yr29/Sr58/Pm39/Ltn2 on 1BL in the SHW germplasm. In addition, gene–gene interactions between significantly associated loci and all loci across the genome revealed five significant interactions at FDR <0.05. Two significant leaf rust and one stem rust interactions were thought to be synergistic, while another two QTL for yellow leaf spot involved antagonistic relations. To the best of our knowledge, this is the first GWAS for six fungal diseases using SHW. Identification of markers associated with disease resistance to one or more diseases represents an important resource for pyramiding favorable alleles and introducing multiple disease resistance from SHW accessions into current elite wheat cultivars.

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Abbreviations

MDR:

Multiple disease resistance

SHW:

Synthetic hexaploid wheat

MLM:

Mixed linear model

QTL:

Quantitative trait loci

GWAS:

Genome-wide association study

LD:

Linkage disequilibrium

Lr:

Leaf rust

Sr:

Stem rust

Yr:

Yellow rust

YLS:

Yellow leaf spot

SNG:

Septoria Nodorum glume blotch

SNL:

Septoria Nodorum leaf blotch

Cr:

Crown rot

DArT:

Diversity Arrays Technology

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Acknowledgments

The authors acknowledge financial support from the Grains Research and Development Corporation, International Centre for Agricultural Research in the Dry Areas (ICARDA), the International Maize and Wheat Improvement Centre (CIMMYT) and Department of Environment and Primary Industries, Victoria. They thank J. Wilson, M. S. McLean, S. P. Taylor, J. P. Thompson, H. S. Bariana, M. M. Shankar, and A. Milgate for their assistance with disease phenotyping.

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Authors and Affiliations

  1. International Centre for Agricultural Research in the Dry Areas (ICARDA), Rabat, Morocco

    Abdulqader Jighly, Manickavelu Alagu, Farid Makdis, Murari Singh & Francis C. Ogbonnaya

  2. Department of Economic Development, Jobs, Transport and Resources, AgriBio, Centre for Agribioscience, 5 Ring Road, Bundoora, VIC, 3083, Australia

    Abdulqader Jighly

  3. School of Applied Systems Biology, La Trobe University, Bundoora, VIC, 3083, Australia

    Abdulqader Jighly

  4. Kihara Institute for Biological Research, Yokohama City University, 641-12, Maioka, Yokohama, 2440813, Japan

    Manickavelu Alagu

  5. International Maize and Wheat Improvement Center (CIMMYT), Km. 45 Carretera México-Veracruz, Colonia El Batán, Texcoco, Edo. De México, 56130, Mexico

    Sukhwinder Singh

  6. Graham Centre for Agricultural Innovation (NSW Department of Primary Industries and Charles Sturt University), Wagga Wagga, NSW, 2650, Australia

    Livinus C. Emebiri

  7. Grains Research and Development Corporation, P.O. Box 5367, Kingston, ACT, 2604, Australia

    Francis C. Ogbonnaya

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  1. Abdulqader Jighly
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  2. Manickavelu Alagu
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  3. Farid Makdis
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  4. Murari Singh
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  5. Sukhwinder Singh
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  6. Livinus C. Emebiri
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  7. Francis C. Ogbonnaya
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Correspondence to Francis C. Ogbonnaya.

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11032_2016_541_MOESM1_ESM.xlsx

Table S1 List of the 320 synthetic hexaploid wheat genotypes used in this study, their pedigrees and their phenotypes scored from 1 (susceptible) to 9 (resistant) (XLSX 34 kb)

Table S2 The number of mapped DArT and DArTSeq markers on each wheat chromosome (DOCX 13 kb)

Table S3 The full genotypic data for both main and validation sets (XLSX 7994 kb)

Table S4 Genotypes of the associated marker for the main set (XLSX 69 kb)

Table S5 QTL detected when analyzing the validation and the main panels as one set (DOCX 13 kb)

11032_2016_541_MOESM6_ESM.png

Figure S1 Results of the response of 320 SHWs to each of the six diseases evaluated. YLS = yellow leaf spot, Cr = crown rot, Lr = leaf rust, Sr = stem rust, Yr = yellow rust, SNL = Stagonospora nodorum leaf blotch, SNG = Stagonospora nodorum glume blotch. S = susceptible, MS = moderately susceptible, MR = moderately resistant, and R = resistant (PNG 2 kb)

Figure S2 Pseudo-heritability estimation inferred from the mixed model for the studied traits (PDF 58 kb)

Figure S3 Map position of both DArT (red) and DArTSeq (black) markers on wheat genome (PNG 8 kb)

11032_2016_541_MOESM9_ESM.png

Figure S4 Phylogenetic tree of the 320 SHWs, red genotypes represent the main set while blue genotypes represent the validation set (PNG 123 kb)

Figure S5 Kinship relations for the 320 SHWs (PNG 314 kb)

11032_2016_541_MOESM11_ESM.png

Figure S6 Scatter plot for the genetic distance against R2 value for each pair of markers on the same chromosome (LD decay) for a) whole genome; b) genome A; c) genome B; d) genome D. Red lines represent the LOESS second degree smoothing while the blue horizontal lines represents the R2 cut off 0.2 (PNG 199 kb)

Figure S7 Inter-chromosomal R2 values for each pair of markers for each genome (PNG 2 kb)

11032_2016_541_MOESM13_ESM.pdf

Figure S8 Manhattan and QQ plots for studied traits. Cr = crown rot, Lr = leaf rust, Sr = stem rust, Yr = yellow rust, SNL = Stagonospora nodorum leaf blotch, SNG = Stagonospora nodorum glume blotch and YLS = yellow leaf spot. Chromosomes were numbered starting from the homoeologous chromosome group one to seven with within group order of A, B and D genome, respectively. Chromosome 22 represents the unmapped markers (PDF 1379 kb)

11032_2016_541_MOESM14_ESM.png

Figure S9 The average disease score (the allelic effect) for the alleles of the markers with multiple associations. For the 6D QTL, we used only the marker 1126778 (PNG 42 kb)

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Jighly, A., Alagu, M., Makdis, F. et al. Genomic regions conferring resistance to multiple fungal pathogens in synthetic hexaploid wheat. Mol Breeding 36, 127 (2016). https://doi.org/10.1007/s11032-016-0541-4

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