Phased, chromosome-scale genome assemblies of tetraploid potato reveal a complex genome, transcriptome, and predicted proteome landscape underpinning genetic diversity

Genevieve Hoopes, Xiaoxi Meng, John P. Hamilton, Sai Reddy Achakkagari, Fernanda de Alves Freitas Guesdes, Marie E. Bolger, Joseph J. Coombs, Danny Esselink, Natalie R. Kaiser, Linda Kodde, Maria Kyriakidou, Brian Lavrijssen, Natascha van Lieshout, Rachel Shereda, Heather K. Tuttle, Brieanne Vaillancourt, Joshua C. Wood, Jan M. de Boer, Nolan Bornowski, Peter BourkeDavid Douches, Herman J. van Eck, Dave Ellis, Max J. Feldman, Kyle M. Gardner, Johannes C.P. Hopman, Jiming Jiang, Walter S. De Jong, Joseph C. Kuhl, Richard G. Novy, Stan Oome, Vidyasagar Sathuvalli, Ek Han Tan, Remco A. Ursum, M. Isabel Vales, Kelly Vining, Richard G.F. Visser, Jack Vossen, G. Craig Yencho, Noelle L. Anglin, Christian W.B. Bachem, Jeffrey B. Endelman, Laura M. Shannon, Martina V. Strömvik, Helen H. Tai, Björn Usadel, C. Robin Buell, Richard Finkers

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Cultivated potato is a clonally propagated autotetraploid species with a highly heterogeneous genome. Phased assemblies of six cultivars including two chromosome-scale phased genome assemblies revealed extensive allelic diversity, including altered coding and transcript sequences, preferential allele expression, and structural variation that collectively result in a highly complex transcriptome and predicted proteome, which are distributed across the homologous chromosomes. Wild species contribute to the extensive allelic diversity in tetraploid cultivars, demonstrating ancestral introgressions predating modern breeding efforts. As a clonally propagated autotetraploid that undergoes limited meiosis, dysfunctional and deleterious alleles are not purged in tetraploid potato. Nearly a quarter of the loci bore mutations are predicted to have a high negative impact on protein function, complicating breeder's efforts to reduce genetic load. The StCDF1 locus controls maturity, and analysis of six tetraploid genomes revealed that 12 allelic variants of StCDF1 are correlated with maturity in a dosage-dependent manner. Knowledge of the complexity of the tetraploid potato genome with its rampant structural variation and embedded deleterious and dysfunctional alleles will be key not only to implementing precision breeding of tetraploid cultivars but also to the construction of homozygous, diploid potato germplasm containing favorable alleles to capitalize on heterosis in F1 hybrids.

Original languageEnglish (US)
Pages (from-to)520-536
Number of pages17
JournalMolecular Plant
Volume15
Issue number3
DOIs
StatePublished - Mar 7 2022

Bibliographical note

Funding Information:
We acknowledge financial support from AAFC-Génome Québec GQ-AAC-2019-2 to M.V.S., Agriculture and Agri-Food Canada Genomics Research and Development Initiative grant number J-002367 to H.H.T. and K.M.G., Compute Canada, Research Portals and Platforms (RPP) award to M.V.S, Compute Canada, Resources for Research Groups (RRG) award to M.V.S., DFG Germany's Excellence Strategy (EXC-2048/1–Project 390686111) to B.U., Dutch TKI top-sector project Novel genetic and genomic tools for polyploid crops (project numbers BO-26.03-009-004 and BO-50-002-022) to P.M.B., European Union's Horizon 2020 research and innovation programme under grant agreement no 862858 (ADAPT) to C.W.B.B., Germany Ministry of Education and Research BMBF FKZ031A536C to B.U., Germany Ministry of Education and Research BMBF FKZ031A536C to M.E.B., GIZ on behalf of the of the Federal Ministry for Economic Cooperation and Development, Germany to D. Ellis and N.L.A., National Science Foundation (IOS 2140176) to C.R.B., National Science Foundation NRT-IMPACTS fellowship (1828149) to N.B., NC Agricultural Research Service to G.C.Y., NC State University to G.C.Y., NSF IOS-1929982 to C.R.B., NWO-domein Toegepaste en Technische Wetenschappen MAMY project ID 16889 to C.W.B.B. and N.L., Potato Variety Management Institute to K.V. and V.S., State of Minnesota, Minnesota Department of Agriculture to L.M.S., the United States-Israel Binational Agricultural Research and Development Funds IS-5038-17C and IS-5317-20C to J.J., Texas A & M University to M.I.V., The Clen P. and Emma L. Atchley Potato Research Faculty Excellence Endowment to J.C.K., University of Maine to E.H.T., USDA AFRI NIFA Pre-doctoral Fellowship project 2019-07160 to N.R.K., USDA Multistate Research Funds accession 1004958 to W.S.D.J., USDA Hatch Act 2019-03162 to C.R.B., USDA NIFA 2020-67034-31731 to G.H., USDA-NIFA 2016-34141-25707 to L.M.S., USDA-NIFA-SCRI 2019-51181-30021 to L.M.S., Dutch TKI top-sector project Genetics Assisted Assembly of Complex Genomes (project number BO-68-001-033-WPR), LWV20.112 Application of sequence-based multi-allelic markers in genetics and breeding of polyploids (project number BO-68-001-042-WPR), and Wageningen UR Plant Breeding to R.F., Wageningen UR Plant Breeding to R.G.F.V., and Washington State Potato Commission to M.J.F. We would like to thank Emily McCoy and Martin Lague for assistance with data analysis.

Funding Information:
We acknowledge financial support from AAFC-Génome Québec GQ-AAC-2019-2 to M.V.S., Agriculture and Agri-Food Canada Genomics Research and Development Initiative grant number J-002367 to H.H.T. and K.M.G., Compute Canada, Research Portals and Platforms (RPP) award to M.V.S, Compute Canada, Resources for Research Groups (RRG) award to M.V.S., DFG Germany’s Excellence Strategy (EXC-2048/1–Project 390686111 ) to B.U., Dutch TKI top-sector project Novel genetic and genomic tools for polyploid crops (project numbers BO-26.03-009-004 and BO-50-002-022 ) to P.M.B., European Union’s Horizon 2020 research and innovation programme under grant agreement no 862858 (ADAPT) to C.W.B.B., Germany Ministry of Education and Research BMBF FKZ031A536C to B.U., Germany Ministry of Education and Research BMBF FKZ031A536C to M.E.B., GIZ on behalf of the of the Federal Ministry for Economic Cooperation and Development , Germany to D. Ellis and N.L.A., National Science Foundation ( IOS 2140176 ) to C.R.B., National Science Foundation NRT-IMPACTS fellowship ( 1828149 ) to N.B., NC Agricultural Research Service to G.C.Y., NC State University to G.C.Y., NSF IOS-1929982 to C.R.B., NWO-domein Toegepaste en Technische Wetenschappen MAMY project ID 16889 to C.W.B.B. and N.L., Potato Variety Management Institute to K.V. and V.S., State of Minnesota , Minnesota Department of Agriculture to L.M.S., the United States-Israel Binational Agricultural Research and Development Funds IS-5038-17C and IS-5317-20C to J.J., Texas A & M University to M.I.V., The Clen P. and Emma L. Atchley Potato Research Faculty Excellence Endowment to J.C.K., University of Maine to E.H.T., USDA AFRI NIFA Pre-doctoral Fellowship project 2019-07160 to N.R.K., USDA Multistate Research Funds accession 1004958 to W.S.D.J., USDA Hatch Act 2019-03162 to C.R.B., USDA NIFA 2020-67034-31731 to G.H., USDA-NIFA 2016-34141-25707 to L.M.S., USDA-NIFA-SCRI 2019-51181-30021 to L.M.S., Dutch TKI top-sector project Genetics Assisted Assembly of Complex Genomes (project number BO-68-001-033-WPR ), LWV20.112 Application of sequence-based multi-allelic markers in genetics and breeding of polyploids (project number BO-68-001-042-WPR ), and Wageningen UR Plant Breeding to R.F., Wageningen UR Plant Breeding to R.G.F.V., and Washington State Potato Commission to M.J.F. We would like to thank Emily McCoy and Martin Lague for assistance with data analysis.

Publisher Copyright:
© 2022 The Author

Keywords

  • allele diversity
  • pan-genome
  • phased assembly
  • polyploid
  • potato
  • wild introgressions

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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