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

Authors: HOOPES, G - Michigan State University; MENG, X - University Of Minnesota; HAMILTON, J - Michigan State University; ACHAKKAGARI, S - McGill University - Canada; DE ALVES FREITAS GUE, F - Wageningen University And Research Center; BOLGER, M - Ibg-4 Bioinformatics; COOMBS, J - Michigan State University; ESSELINK, D - Wageningen University And Research Center; KAISER, N - Michigan State University; KODDE, L - Wageningen University And Research Center; KYRIAKIDOU, M - McGill University - Canada; LAVRIJSSEN, B - Wageningen University And Research Center; VAN LIESHOUT, N - Wageningen University And Research Center; SHEREDA, R - Michigan State University; TUTTLE, H - University Of Minnesota; VAILLANCOURT, B - Michigan State University; WOOD, J - Michigan State University; DE BOER, J - Averis Seeds Bv; BORNOWSKI, N - Michigan State University; BOURKE, P - Wageningen University And Research Center; DOUCHES, D - Michigan State University; VAN ECK, H - Wageningen University And Research Center; ELLIS, D - International Potato Center; Feldman, Max; GARDNER, K - Agriculture And Agri-Food Canada; HOPMAN, J - Averis Seeds Bv; JIANG, J - Michigan State University; DE JONG, W - Cornell University; KUHL, J - University Of Idaho; Novy, Richard - Rich; OOME, S - Hzpc Research Bv; SATHUVALLI, V - Oregon State University; TAN, E - University Of Maine; URSUM, R - Hzpc Research Bv; VALES, M - Texas A&M University; VINING, K - Oregon State University; VISSER, R - Wageningen University And Research Center; VOSSEN, J - Wageningen University And Research Center; YENCHO, C - North Carolina State University; Anglin, Noelle; BACHEM, C - Wageningen University And Research Center; ENDELMAN, J - University Of Wisconsin; SHANNON, L - University Of Minnesota; STROMVIK, M - McGill University - Canada; TAI, H - Agriculture And Agri-Food Canada; USADEL, B - Ibg-4 Bioinformatics; BUELL, C - Michigan State University; FINKERS, R - Wageningen University And Research Center

Submitted to: Molecular Plant
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/7/2022
Publication Date: 1/10/2022
Citation: Hoopes, G., Meng, X., Hamilton, J.P., Achakkagari, S.R., De Alves Freitas Guesdes, F., Bolger, M.E., Coombs, J.J., Esselink, D., Kaiser, N.R., Kodde, L., Kyriakidou, M., Lavrijssen, B., van Lieshout, N., Shereda, R., Tuttle, H.K., Vaillancourt, B., Wood, J.C., de Boer, J.M., Bornowski, N., Bourke, P., Douches, D., van Eck, H.J., Ellis, D., Feldman, M.J., Gardner, K.M., Hopman, J.C., Jiang, J., De Jong, W.S., Kuhl, J.C., Novy, R.G., Oome, S., Sathuvalli, V., Tan, E.H., Ursum, R.A., Vales, M.I., Vining, K., Visser, R.G., Vossen, J., Yencho, C., Anglin, N.L., Bachem, C.W., Endelman, J.B., Shannon, L.M., Stromvik, M.V., Tai, H.H., Usadel, B., Buell, C.R., Finkers, R. 2022. Phased, chromosome-scale genome assemblies of tetraploid potato reveal a complex genome, transcriptome, and predicted proteome landscape underpinning genetic diversity. Molecular Plant. 15(3):520-536. https://doi.org/10.1016/j.molp.2022.01.003.
DOI: https://doi.org/10.1016/j.molp.2022.01.003

Interpretive Summary: Cultivated potato has a very complex genetic constitution with four copies of chromosomes and a high level of genetic diversity, making its genetic analysis and the development of a blueprint of its assemblage of chromosomes a significant challenge. In this study, the assemblage of chromosomes, transcribed genes, and cellular organelles for six potato cultivars were sequenced, assembled, and phased. The six cultivars chosen for this study, are important in the European and the North American markets allowing a comparison of the genetic basis for market class traits and the similarities among them. Sequence data from 20 wild potato species were also utilized to examine if DNA from them had been incorporated into cultivated potato. All wild species examined had signatures within the cultivated material suggesting significant gene exchange over time. The data obtained allowed an assessment of the genetic variability and chromosomal structural variation in cultivars which demonstrated high genetic diversity, dysfunctional alleles, and significant wild species integration. The data reinforces the notion that potato has a complex assemblage of chromosomes, perhaps the most complex analyzed and released to date among cultivated crops.

Technical Abstract: Cultivated potato is a clonally propagated autotetraploid species with a highly heterogenous genome. Construction of phased, chromosome-scale assemblies of multiple cultivars 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 resulting proteome distributed across the homologous chromosomes. Wild species introgressions further contribute to allelic diversity demonstrating ancestral introgressions prior to modern breeding efforts. As an autotetraploid that undergoes limited meiosis, dysfunctional and deleterious alleles are not purged and nearly a quarter of loci bore mutations predicted to have high negative impact on protein function complicating breeder’s efforts to reduce genetic load. The locus StCDF1 controls maturity and analysis of six tetraploid genomes revealed eight allelic variants, of which, allele dosage was correlated maturity. Knowledge of the complexity of a tetraploid genome with its embedded deleterious and dysfunctional alleles will be key to constructing diploid potato homozygous for favorable alleles that can then be combined in an F1 hybrid to capture heterosis.