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An accumulation of genetic variation and selection across the disease-related genes during apple domestication

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Abstract

Although human-imposed selection is known to have altered plant traits during crop domestication, the effect of selection on host susceptibility or resistance is not well understood. Moreover, the domestication of perennial tree fruit crops, unlike annual crops, was driven by hybridization, clonal propagation, and selection of desirable phenotypes, which could confound the accurate assessment of domestication-associated effects on host resistance or susceptibility genes. We studied the effects of domestication on disease-related nucleotide-binding leucine-rich repeat (NLR) genes by combining phylogenetic, haplotype, and selection signature analysis using sequence data from Golden Delicious double haploid (GDDH13 v.1.1) apple genome and 80 resequenced domesticated and wild Malus accessions. The NLR gene family in the GDDH13 v.1.1 apple genome constituted 546 genes that showed expansion mainly through proximal (39.1%) and dispersed (29.5%) duplications. The genome duplication (WGD) within Rosaceae, affecting the Malus lineage, is also evident in the NLR genes. The NLR genes are found in genomic regions associated with previously detected disease resistance-related quantitative trait loci (QTL) for apple scab, fire blight, powdery mildew, and blue mold. A genomic diversity analysis identified that the NLR genes in domesticated apples (Malus domestica) have more variation (average πdom=4.01 × 10−3) than their main progenitor, wild M. sieversii (average πsie=2.95 × 10−3) and M. sylvestris (average πsyl=2.11 × 10−3), which hybridized with M. domestica during the domestication process. These results suggest evidence of selection on disease-related genes associated with domestication of apple. An increased diversity across NLR genes in the domesticated germplasm may be attributed to their diverse geographical origins and distinct pedigrees, together with selection for disease resistance during domestication. The NLR genes under selection can provide opportunities to explore their role in disease resistance in apples.

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Data availability

All the data is provided within the manuscript and as supplemental files. The apple genome sequence variants were published previously (Duan et al. 2017).

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Acknowledgements

We acknowledge Zhangjun Fei from Boyce Thompson Institute for providing the apple genome sequence variants file (Duan et al. 2017).

Funding

This research was supported by the New York State’s USDA Specialty Crop Block Grant Program’s grant #SCG-18-008, managed by the New York Farm Viability Institute and New York State’s Department of Agriculture and Markets.

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Authors and Affiliations

  1. Plant Pathology and Plant-Microbe Biology Section, Cornell University, Geneva, NY, USA

    Jugpreet Singh & Awais Khan

  2. College of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, Jiangsu, China

    Manyi Sun & Jun Wu

  3. Crop Genome Informatics Laboratory, Corn Insects and Crop Genetics Research Unit, USDA-ARS, Ames, IA, 50011, USA

    Steven B. Cannon

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  1. Jugpreet Singh
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  2. Manyi Sun
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  3. Steven B. Cannon
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  4. Jun Wu
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  5. Awais Khan
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Contributions

J.S. and A.K. conceived and designed the original research; A.K. supervised the research; J.S. and M.S. performed gene family characterization and duplication analysis; J.S. and S.B.C. performed the phylogenetic analysis; J.S. performed the diversity and selection analysis with input from A.K.; J.S. wrote the first draft of the manuscript. All authors contributed towards improving the manuscript and have read and approved the final version of the manuscript.

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Correspondence to Awais Khan.

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The authors declare no competing interests.

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Communicated by C. Rellstab

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Supplemental figure S1

A bar plot showing the distribution of nonsynonymous (Ka) to synonymous (Ks) ratio for the NLR genes in apple. The x-axis represents individual NLR gene (bar) and y-axis represents the Ka/Ks ratios for these genes. (PNG 1740 kb)

High resolution image (TIFF 9275 kb)

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Singh, J., Sun, M., Cannon, S.B. et al. An accumulation of genetic variation and selection across the disease-related genes during apple domestication. Tree Genetics & Genomes 17, 29 (2021). https://doi.org/10.1007/s11295-021-01510-1

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