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

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

doi:10.1016/j.molp.2022.01.003

Cited by 110 publications

(136 citation statements)

References 91 publications

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“…The number of pseudomolecule-scale genome assemblies of seed plants has rapidly increased in the last 20 years revealing their conserved and divergent architectural features (1)(2)(3)(4)(5). In addition, comparative analyses of deep and shallowly divergent seed plant genomes provided detailed insights into genome evolution and dynamics both at longer and shorter timescales (6,7, [16][17][18][19][20][8][9][10][11][12][13][14][15]. By contrast, structure and dynamics of seed-free plant genomes are little understood (2,5,21).…”

Section: Introductionmentioning

confidence: 99%

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

Kirbis¹,

Rahmatpour

Dong

et al. 2022

Preprint

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Background: While genome evolutionary processes of seed plants are intensively investigated, very little is known about seed-free plants in this respect. Here, we use one of the largest groups of seed-free plants, the mosses, and newly generated chromosome-scale genome assemblies to investigate three poorly known aspects of genome dynamics and their underlying processes in seed-free plants: (i) genome size variation, (ii) genomic collinearity/synteny, and (iii) gene set differentiation. Results: Comparative genomic analyses on the model moss Physcomitrium (Physcomitrella) patens and two genomes of Funaria hygrometrica reveal that, like in seed plants, genome size change (approx. 140 Mbp) is primarily due to transposable element expansion/contraction. Despite 60 million years of divergence, the genomes of P. patens and F. hygrometrica show remarkable chromosomal stability with the majority of homologous genes located in conserved collinear blocks. In addition, both genomes contain a relatively large set of lineage-specific genes with no detectible homologs in the other speciesʼ genome, suggesting a highly dynamic gene space fueled by the process of de novo gene birth and loss rather than by gene family diversification/duplication. Conclusions: These, combined with previous observations suggest that genome dynamics in mosses involves the coexistence of a collinear homologous and a highly dynamic species-specific gene sets. Besides its significance for understanding genome evolution, the presented chromosome-scale genome assemblies will provide a foundation for comparative genomic and functional studies in the Funariaceae, a family holding historical and contemporary model taxa in the evolutionary biology of mosses.

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Section: Introductionmentioning

confidence: 99%

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

Kirbis¹,

Rahmatpour

Dong

et al. 2022

Preprint

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“…This is the second publication in which QTL haplotype effects for vine maturity were connected to CDF1 alleles in a tetraploid mapping population. Hoopes et al (2022) analyzed a single F1 population with CDF1 parental genotypes 1111 x 1223, and we have extended the method to a multi-parental population. Our determination of the CDF1 allelic series 3 > 2 > 1 for early maturity agrees with the results of Hoopes et al (2022).…”

Section: Discussionmentioning

confidence: 99%

“…The software IGV (Robinson et al 2011) was used to visualize the alignments and count CDF1 allele read depth. A multiple sequence alignment of CDF1 alleles from a tetraploid potato pan-genome (Hoopes et al 2022) was performed using MUSCLE v3.8 (Edgar 2004; Madeira et al 2019), and the percent identity matrix was used for UPGMA hierarchical clustering with hclust in R (R Core Team 2021).…”

Section: Methodsmentioning

confidence: 99%

The genetic architectures of vine and skin maturity in tetraploid potato

Caraza-Harter

Endelman

2022

Preprint

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As with most crops, maturity is a critical trait for potato production and therefore breeding. In this study, both vine and skin maturity, which refer to foliar senescence and adherence of the tuber periderm, respectively, were measured in breeding populations (N = 586) over a two-year period. It is well established that S. tuberosum Cyclin DOF Factor 1 (CDF1) affects vine maturity, but this is the first study to quantify its effect on skin maturity, using linked markers discovered through genome-wide association studies (GWAS). Skin maturity had slightly less genomic heritability than vine maturity (0.41 vs. 0.47), and the importance of CDF1 was considerably less for skin maturity, accounting for only 39% of the additive variance vs. 70% for vine maturity. Using path analysis, the additive genetic correlation between the two maturity traits was estimated at 0.65, of which 0.51 was attributed to CDF1. Within the GWAS panel was a half-diallel population derived from three parents, which was analyzed by joint linkage mapping. Based on the estimated effects of the parental haplotypes and prior knowledge of the allelic series for CDF1, the CDF1 allele for each haplotype was predicted and ultimately confirmed through whole-genome sequencing. The ability to connect statistical alleles from QTL models with biological alleles based on DNA sequencing represents a new milestone in genomics-assisted breeding for tetraploid species.

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“…Thousands of potato cultivars exists and most of them are tetraploid (2n = 4x = 48; FAO, 2008 ). However, chromosome level genome assemblies for tetraploid potato clones became only recently available ( Hoopes et al, 2022 ), after the analyses for this study were finalized. Instead, we used four tuber-bearing diploid potato clones belonging to cultivated, non-cultivated, and wild potato species for which chromosome-level genome assemblies are available.…”

Section: Methodsmentioning

confidence: 99%

Genetic Divergence of Lineage-Specific Tandemly Duplicated Gene Clusters in Four Diploid Potato Genotypes

Bonthala

Stich

2022

Front. Plant Sci.

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Potato (Solanum tuberosum L.) is the most important non-grain food crop. Tandem duplication significantly contributes to genome evolution. The objectives of this study were to (i) identify tandemly duplicated genes and compare their genomic distributions across potato genotypes, (ii) investigate the bias in functional specificities, (iii) explore the relationships among coding sequence, promoter and expression divergences associated with tandemly duplicated genes, (iv) examine the role of tandem duplication in generating and expanding lineage-specific gene families, (v) investigate the evolutionary forces affecting tandemly duplicated genes, and (vi) assess the similarities and differences with respect to above mentioned aspects between cultivated genotypes and their wild-relative. In this study, we used well-annotated and chromosome-scale de novo genome assemblies of multiple potato genotypes. Our results showed that tandemly duplicated genes are abundant and dispersed through the genome. We found that several functional specificities, such as disease resistance, stress-tolerance, and biosynthetic pathways of tandemly duplicated genes were differentially enriched across multiple potato genomes. Our results indicated the existence of a significant correlation among expression, promoter, and protein divergences in tandemly duplicated genes. We found about one fourth of tandemly duplicated gene clusters as lineage-specific among multiple potato genomes, and these tended to localize toward centromeres and revealed distinct selection signatures and expression patterns. Furthermore, our results showed that a majority of duplicated genes were retained through sub-functionalization followed by genetic redundancy, while only a small fraction of duplicated genes was retained though neo-functionalization. The lineage-specific expansion of gene families by tandem duplication coupled with functional bias might have significantly contributed to potato’s genotypic diversity, and, thus, to adaption to environmental stimuli.

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

Cited by 110 publications

References 91 publications

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

The genetic architectures of vine and skin maturity in tetraploid potato

Genetic Divergence of Lineage-Specific Tandemly Duplicated Gene Clusters in Four Diploid Potato Genotypes

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