Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance

Hübner, Sariel; Bercovich, Natalia; Todesco, Marco; Mandel, Jennifer R.; Odenheimer, Jens; Ziegler, Emanuel; Lee, Joon S.; Baute, Gregory J.; Owens, Gregory L.; Grassa, Christopher J.; Ebert, Daniel; Ostevik, Katherine L.; Moyers, Brook T.; Yakimowski, Sarah B.; Masalia, Rishi R.; Gao, Lexuan; Ćalić, Irina; Bowers, John E.; Kane, Nolan C.; Swanevelder, Dirk; Kubach, Timo; Muños, Stéphane; Langlade, Nicolas B.; Burke, John M.; Rieseberg, Loren H.

doi:10.1038/s41477-018-0329-0

Cited by 180 publications

(190 citation statements)

References 60 publications

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“…For these comparisons, there was significant variation in F ST values and the highest values were concentrated in chromosome 10 and, to a less extent, chromosomes 8 and 13 (Figure ). The patterns of divergence are similar to those reported previously between restorer and maintainer lines based on a less complete reference sequence (Hubner et al., ). However, differentiation relative to OPVs was not reported in the previous study, so the directionality of change could not be inferred.…”

Section: Resultsmentioning

confidence: 99%

“…Although evidence of different pan‐genome gene content between inbred lines in sunflowers was recently shown (Hubner et al., ), the role of introgression in gene loss has not been previously appreciated. Missing genes may play a role in linkage drag, which is a concern to breeders when wild relatives are employed for improvement (Curwen‐McAdams & Jones, ).…”

Section: Discussionmentioning

confidence: 99%

“…The gene also colocalizes within the best supported downy mildew QTL reported by Hubner et al. (). The correlation of gene presence and introgression may suggest that presence–absence variation is segregating within both cultivars and wild relatives.…”

Section: Discussionmentioning

confidence: 99%

“…Most relevant to this study are a large sampling of restorer (96 samples) and maintainer varieties (127) and OPVs (9) from which they have been derived. This whole population was sequenced to a target of 5–20× coverage on the Illumina platform (Table ), although aligned median read depth ranged from 1.6 to 19 (median 4.5) (Hubner et al., ).…”

Section: Methodsmentioning

confidence: 99%

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Genomic sequence and copy number evolution during hybrid crop development in sunflowers

Owens

Baute

Hübner

2018

Evolutionary Applications

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Hybrid crops, an important part of modern agriculture, rely on the development of male and female heterotic gene pools. In sunflowers, heterotic gene pools were developed through the use of crop‐wild relatives to produce cytoplasmic male sterile female and branching, fertility restoring male lines. Here, we use genomic data from a diversity panel of male, female, and open‐pollinated lines to explore the genetic changes brought during modern improvement. We find the male lines have diverged most from their open‐pollinated progenitors and that genetic differentiation is concentrated in chromosomes, 8, 10 and 13, due to introgressions from wild relatives. Ancestral variation from open‐pollinated varieties almost universally evolved in parallel for both male and female lines suggesting little or no selection for heterotic overdominance. Furthermore, we show that gene content differs between the male and female lines and that differentiation in gene content is concentrated in high F ST regions. This means that the introgressions that brought branching and fertility restoration to the male lines, brought with them different gene content from the ancestral haplotypes, including the removal of some genes. Although we find no evidence that gene complementation genomewide is responsible for heterosis between male and female lines, several of the genes that are largely absent in either the male or female lines are associated with pathogen defense, suggesting complementation may be functionally relevant for crop breeders.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Genomic sequence and copy number evolution during hybrid crop development in sunflowers

Owens

Baute

Hübner

2018

Evolutionary Applications

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“…In plants, many species-centered projects are genotyping collections of individuals, for which different phenotypes can then be measured and analyzed. These include hundreds or thousands of strains from Arabidopsis thaliana , rice, maize, tomato, sunflower, and several other species (1001Genomes Consortium, 2016Bukowski et al, 2018;Hübner et al, 2018;Tieman et al, 2017;Wang et al, 2018) .…”

Section: Introductionmentioning

confidence: 99%

Finding genetic variants in plants without complete genomes

Voichek¹,

Weigel²

2019

Preprint

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Structural variants and presence/absence polymorphisms are common in plant genomes, yet they are routinely overlooked in genome-wide association studies (GWAS). Here, we expand the genetic variants detected in GWAS to include major deletions, insertions, and rearrangements. We first use raw sequencing data directly to derive short sequences, k -mers, that mark a broad range of polymorphisms independently of a reference genome. We then link k -mers associated with phenotypes to specific genomic regions. Using this approach, we re-analyzed 2,000 traits measured in Arabidopsis thaliana, tomato , and maize populations. Associations identified with k -mers recapitulate those found with single-nucleotide polymorphisms (SNPs), however, with stronger statistical support. Moreover, we identified new associations with structural variants and with regions missing from reference genomes.Our results demonstrate the power of performing GWAS before linking sequence reads to specific genomic regions, which allow detection of a wider range of genetic variants responsible for phenotypic variation.Here, we present an efficient method for k -mer-based GWAS and compare it directly to the conventional SNP-based approach on more than 2,000 phenotypes from three plant species with different genome and population characteristics -A. thaliana , maize and tomato. Most variants identified by SNPs can be detected with k -mers (and vice versa), but k -mers having stronger statistical support.For k -mer-only hits, we demonstrate how different strategies can be used to infer their genomic context, including large structural variants, sequences missing from the reference genome, and organeller variants. Lastly, we compute population structure directly from k -mers, enabling the analysis of species with poor quality or without a reference genome. In summary, we have inverted the conventional approach of building a genome, using it to find population variants, and only then associating variants with phenotypes. In contrast, we begin by associating sequencing reads with phenotypes, and only then infer the genomic context of these sequences. We posit that this change of order is especially effective in plant species, for which defining the full population-level genetic variation based on reference genomes remains highly challenging. Schneeberger et al., 2009) . While traditional GWAS methods will benefit from these technological improvements, so will k -mer based approaches, which will be able to use tags spanning larger genomic distances. Therefore, we posit that for GWAS purposes, k -mer based approaches are ideal because they minimize arbitrary choices when classifying alleles and because they capture more, almost optimal, information from raw sequencing data. 578

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Candidate pathway association and genome‐wide association approaches reveal alternative genetic architectures of carotenoid content in cultivated sunflower (Helianthus annuus)

Dowell,

Mason

2023

Appl Plant Sci

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PremiseThe explosion of available genomic data poses significant opportunities and challenges for genome‐wide association studies. Current approaches via linear mixed models (LMM) are straightforward but prevent flexible assumptions of an a priori genomic architecture, while Bayesian sparse LMMs (BSLMMs) allow this flexibility. Complex traits, such as specialized metabolites, are subject to various hierarchical effects, including gene regulation, enzyme efficiency, and the availability of reactants.MethodsTo identify alternative genetic architectures, we examined the genetic architecture underlying the carotenoid content of an association mapping panel of Helianthus annuus individuals using multiple BSLMM and LMM frameworks.ResultsThe LMMs of genome‐wide single‐nucleotide polymorphisms (SNPs) identified a single transcription factor responsible for the observed variations in the carotenoid content; however, a BSLMM of the SNPs with the bottom 1% of effect sizes from the results of the LMM identified multiple biologically relevant quantitative trait loci (QTLs) for carotenoid content external to the known (annotated) carotenoid pathway. A candidate pathway analysis (CPA) suggested a β‐carotene isomerase to be the enzyme with the highest impact on the observed carotenoid content within the carotenoid pathway.DiscussionWhile traditional LMM approaches suggested a single unknown transcription factor associated with carotenoid content variation in sunflower petals, BSLMM proposed several QTLs with interpretable biological relevance to this trait. In addition, the CPA allowed for the dissection of the regulatory vs. biosynthetic genetic architectures underlying this metabolic trait.

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Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance

Cited by 180 publications

References 60 publications

Genomic sequence and copy number evolution during hybrid crop development in sunflowers

Genomic sequence and copy number evolution during hybrid crop development in sunflowers

Finding genetic variants in plants without complete genomes

Candidate pathway association and genome‐wide association approaches reveal alternative genetic architectures of carotenoid content in cultivated sunflower (Helianthus annuus)

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