Inbreeding depression confers reduced fitness among the offspring of genetic relatives. As a clonally propagated crop, potato (Solanum tuberosum L.) suffers from severe inbreeding depression; however, the genetic basis of inbreeding depression in potato is largely unknown. To gain insight into inbreeding depression in potato, we evaluated the mutation burden in 151 diploid potatoes and obtained 344,831 predicted deleterious substitutions. The deleterious mutations in potato are enriched in the pericentromeric regions and are line specific. Using three F2 populations, we identified 15 genomic regions with severe segregation distortions due to selection at the gametic and zygotic stages. Most of the deleterious recessive alleles affecting survival and growth vigor were located in regions with high recombination rates. One of these deleterious alleles is derived from a rare mutation that disrupts a gene required for embryo development. This study provides the basis for genome design of potato inbred lines.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
American Journal of Potato Research Open Access 14 October 2022
aBIOTECH Open Access 15 September 2022
Genome Biology Open Access 07 September 2022
Subscribe to Nature+
Get immediate online access to Nature and 55 other Nature journal
Subscribe to Journal
Get full journal access for 1 year
only $6.58 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
The pipeline of parent-independent genotyping in potato was written using custom Python scripts. All codes are available from the corresponding author upon request.
The sequencing data that support the findings of this study have been deposited in the Sequence Read Archive (SRA) under accession PRJNA471783. The deleterious mutations datasets are available from the following ftp link: ftp://ftp.agis.org.cn/~zhangchunzhi/.
Darwin, C. The Effects of Cross and Self Fertilization in the Vegetable Kingdom (John Murray, London, 1876).
Ramu, P. et al. Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation. Nat. Genet. 49, 959–963 (2017).
Vreugdenhil, D. et al. Potato Biology and Biotechnology: Advances and Perspectives (Elsevier Science, Amsterdam, 2007).
Lindhout, P. et al. Towards F1 hybrid seed potato breeding. Potato Res. 54, 301–312 (2011).
Li, Y., Li, G., Li, C., Qu, D. & Huang, S. Prospects of diploid hybrid breeding in potato. Chin. Potato 27, 96–99 (2013).
Jansky, S. H. et al. Reinventing potato as a diploid inbred line–based crop. Crop Sci. 56, 1412–1422 (2016).
Remington, D. L. & O’Malley, D. M. Evaluation of major genetic loci contributing to inbreeding depression for survival and early growth in a selfed family of Pinus taeda. Evolution 54, 1580–1589 (2000).
Chen, Z. J. Genomic and epigenetic insights into the molecular bases of heterosis. Nat. Rev. Genet. 14, 471–482 (2013).
Charlesworth, D. & Willis, J. H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).
Takayama, S. & Isogai, A. Self-incompatibility in plants. Annu. Rev. Plant Biol. 56, 467–489 (2005).
Vaser, R., Adusumalli, S., Leng, S. N., Sikic, M. & Ng, P. C. SIFT missense predictions for genomes. Nat. Protoc. 11, 1–9 (2016).
Haddrill, P. R., Halligan, D. L., Tomaras, D. & Charlesworth, B. Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome. Biol. 8, R18 (2007).
Mackay, T. F. C. et al. The Drosophila melanogaster Genetic Reference Panel. Nature 482, 173–178 (2012).
Rodgers-Melnick, E. et al. Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc. Natl Acad. Sci. USA 112, 3823–3828 (2015).
McMulen, M. D. et al. Genetic properties of the maize nested association mapping population. Science 327, 737–740 (2009).
Bonierbale, M. W., Plaisted, R. L. & Tanksley, S. D. RFLP maps based on a common set of clones reveals modes of chromosomal evolution in potato and tomato. Genetics 120, 1095–1103 (1988).
Gebhardt, C. et al. RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor. Appl. Genet. 83, 49–57 (1991).
Jacobs, J. M. E. et al. A genetic map of potato (Solanum tuberosum) integrating molecular markers including transposons and classical markers. Theor. Appl. Genet. 91, 289–300 (1995).
Felcher, K. J. et al. Integration of two diploid potato linkage maps with the potato genome sequence. PLoS ONE 7, e36347 (2012).
Endelman, J. B. & Jansky, S. H. Genetic mapping with an inbred line-derived F2 population in potato. Theor. Appl. Genet. 129, 935–943 (2016).
Kloosterman, B. et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495, 246–250 (2013).
Zourelidou, M. et al. The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136, 627–636 (2009).
Koizumi, K., Wu, S., MacRae-Crerar, A. & Gallagher, K. L. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr. Biol. 21, 1559–1564 (2011).
Hosaka, K. & Hanneman, R. E. Jr. Genetics of self-compatibility in a self-incompatible wild diploid potato species Solanum chacoense. 2. Localization of an S locus inhibitor (Sli) gene on the potato genome using DNA markers. Euphytica 103, 265–271 (1998).
Ye, M. et al. Generation of self-compatible diploid potato by knockout of S-RNase. Nat. Plants 4, 651–654 (2018).
Sharma, S. K. et al. Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. Genes Genomes Genet. 3, 2031–2047 (2013).
Van Ooijen, J. W. Joinmap4: Software for the Calculation of Genetic Linkage Maps in Experimental Populations (Kyazma BV, Wageningen, 2006).
Takagi, H. et al. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 74, 174–183 (2013).
Koressaar, T. & Remm, M. Enhancements and modifications of primer design program Primers. Bioinformatics 23, 1289–1291 (2007).
We thank J. Yan and F. Tian for critical reading of the manuscript; G. Zhu for discussions and project coordination; Z. Peng, X. Xu, and S. Feng for phenotyping and genetic transformation; and Z. Wang, W. Xiao, and D. Zhang from Yinmore Group for greenhouse assistance. This work was supported by the Agricultural Science and Technology Innovation Program (ASTIP-CAAS to S.H.), the Agricultural Science and Technology Innovation Program Cooperation and Innovation Mission (CAAS-XTCX2016 to S.H.), Advanced Technology Talents in Yunnan Province (2013HA025 to S.H.), and National Natural Science Foundation of China (31601360 to C.Z.). This work was also supported by the Ministry of Agriculture and Rural Affairs of PRC and the Shenzhen municipal (The Peacock Plan KQTD2016113010482651 to S.H.) and Dapeng district governments.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Integrated supplementary information
a, The five stages of flower development in PG6226. The numbers indicate the days from flowering. Scale bar, 0.5 cm. b, Relative expression of S-RNase in the mixed carpels of flowers at five developmental stages. The blue dots represent the expression levels of three technical replicates, and the error bars represent the standard errors of three technical replicates. Differential expression was analyzed by t test
a–c, The distribution of deleterious substitutions in three parental clones, PG6226 (a), PG6235 (b), and PG6359 (c). The x axis indicates the physical position. Red lines indicate the ratio between deleterious substitutions and synonymous mutations in each sliding window (window size, 5 Mb; step, 1 Mb), and black lines indicate the number of recombination events per 5 Mb. Gray-shaded boxes indicate the positions of pericentromeric regions
a, High-quality heterozygous SNPs in the F1 clone were extracted. b, The genotype of these SNPs in each F2 individual was identified from low-coverage sequencing data. The breakpoints between homozygous and heterozygous regions were deduced on the basis of the ratio of heterozygous SNPs to all SNPs in each window (window size, 1 Mb; step, 100 kb), and all SNPs in homozygous regions were extracted. c, The longest homozygous region or two overlapping homozygous regions that covered the whole chromosome were chosen as the reference fragments. All homozygous fragments were compared with the reference fragments and divided into two groups based on similarity to the reference fragment. d, Within each group, all SNPs with consensus at each locus were combined to construct the haplotype. e, The weighted value of genotype ‘b’ in each window was used to estimate the breakpoints of recombination. f, The genotype of a bin was defined on the basis of the weighted value of genotype ‘b’ in each bin. Blue, yellow, and gray indicate genotype ‘a’, ‘b’, and ‘h’, respectively. The same procedure was carried out for all 12 chromosomes
a–c, Bin maps of three selfing populations derived from PG6226 (a), PG6235 (b), and PG6359 (c). Yellow, blue, and gray bars indicate genotype b, a, and h, respectively. Red dashed lines represent the regions with a missing genotype in selfed progeny
a–c, The distribution of heterozygous SNPs in three F1 clones, PG6226 (a), PG6235 (b), and PG6359 (c). The x axis indicates physical position. The upper half of the y axis indicates the number of heterozygous SNPs in each sliding window (window size, 1 Mb; step, 100 kb), and the lower half indicates the average depth of the SNPs (window size, 1 Mb; step, 100 kb)
Supplementary Figure 6 Genetic mapping of the large-effect deleterious alleles affecting survival and growth vigor.
The delta SNP indexes between bulks with normal rooting versus abnormal rooting in the progeny of PG6226 (a), green seedlings and white seedlings in the progeny of PG6235 (b), normal leaves versus yellow-margined leaves in the progeny of PG6226 (c), normal leaves versus yellow leaves in the progeny of PG6359 (d), normal branching versus increased branching in the progeny of PG6235 (e), and normal branching versus strong vegetative growth in the progeny of PG6235 (f). The sliding window size is 1 Mb, and the step is 100 kb. The arrows indicate the positions of the target genes
Identify was calculated on the basis of the ratio of the same SNPs and total overlapping SNPs in the haplotype containing the ar1 allele between PG6226 and PG6235 (sliding window size, 5 Mb; step, 500 kb)
a–c, Frequency distributions of pollen viability in the selfing populations of PG6226 (a), PG6235 (b), and PG6359 (c). d, The segregation of tuber weight per plant in the selfing population of PG6226. The x axis represents the square root of tuber weight per plant. The arrows in a–d indicate the phenotype of the parental clones. Most progeny showed lower pollen viability and tuber yield than the parental clones. e–g, The delta indexes between bulks with high versus low pollen viability in the selfing populations of PG6226 (e), PG6235 (f), and PG6359 (g). h, The delta index between bulks with high and low tuber weight per plant. The sliding window size in e–h is 1 Mb, and the step size is 100 kb
About this article
Cite this article
Zhang, C., Wang, P., Tang, D. et al. The genetic basis of inbreeding depression in potato. Nat Genet 51, 374–378 (2019). https://doi.org/10.1038/s41588-018-0319-1
This article is cited by
Genome Biology (2022)
Nature Genetics (2022)
Grafting-induced transcriptome changes and long-distance mRNA movement in the potato/Datura stramonium heterograft system
Horticulture, Environment, and Biotechnology (2022)
American Journal of Potato Research (2022)