bioRxiv Science⌕ Search

Biology subjects

Munos, S.

Publications and source records attributed to Munos, S..

7 recordsLinked to original sources

Genomic and eco-geographic features of locally adapted inversions in wild sunflowers

Chromosomal inversions are increasingly recognized as important drivers of local adaptation and ecological divergence because they suppress recombination and maintain adaptive allele combinations despite ongoing gene flow. However, the eco-evolutionary conditions favouring the establishment of such indirectly adaptive inversions, as well as the genomic features that distinguish them from other inversions remain incompletely understood. In this study, we investigated these questions in a wild sunflower system comprising two species: Helianthus debilis and Helianthus praecox, which exhibit diverse ecotypes and varying degrees of geographic overlap across Texas and Florida in the USA. To resolve the evolutionary relationships between and within these species, and identify potentially adaptive inversions, we generated haplotype-resolved reference assemblies and integrated comparative and population genomic analyses. We identified three major genetic clusters that only partially corresponded to taxonomic classifications. We further detected 156 inversions across the genome, 11 of which showed signatures consistent with a role in local adaptation. Notably, nine of the 11 putatively adaptive inversions were found in sympatric Texas populations. Together with a similar enrichment of inversions in genome assemblies from sympatric versus allopatric populations, our results suggest that inversions are more likely to evolve in heterogeneous environments with ongoing gene flow than in allopatry. Lastly, locally adaptive inversions were generally larger, contained more genes, and showed greater sequence divergence between haplotypes than other types of inversions. Our findings provide empirical support for the role of gene flow in promoting inversion establishment and identify genomic characteristics associated with indirectly adaptive inversions.

evolutionary biology↗

Fine mapping and genomic analyses reveal a tandem kinase-pseudokinase candidate underlying OrDeb2-mediated resistance to Orobanche cumana in sunflower

Sunflower broomrape (Orobanche cumana Wallr.) is a holoparasitic weed that parasitizes sunflower (Helianthus annuus L.) and severely constrains yield. The OrDeb2 gene confers resistance to broomrape race G in the sunflower line DEB2. It has been previously located within a 1.38-Mbp physical region in the H. annuus XRQ reference genome that contains a cluster of receptor-like proteins and receptor-like kinases (RLKs). In this study, an OrDeb2 candidate has been proposed though high-resolution genetic and physical mapping, multi-allelic comparisons across resistant and susceptible lines, and exclusion of other potential candidates based on their function and genetic features. OrDeb2 was delimited to a 219.4-kbp region in the DEB2 genome assembly that contained six annotated protein-coding genes belonging to two groups: three small heat shock proteins (HSP20) and three RLKs. Given that the only sunflower broomrape resistance gene cloned to date encodes an RLK, the key role of RLKs in resistance to biotic stresses in plants, and the similar genetic features between RLK-type resistance genes and OrDeb2 as major dominant genes in gene-for-gene interactions, RLKs in the interval emerged as the most plausible candidates. Within them, the RLK-2 gene encoding a root-expressed full-length kinase-pseudokinase protein belonging to the tandem kinase proteins (TKPs) family was prioritized, because the other two RLKs corresponded to a truncated TKP with a stop codon within the kinase domain. RLK-2 also carried sequence variants unique to DEB2 relative to multiple susceptible genotypes. The results of this research reveal the potential role of TKP genes as new players in resistance to parasitic plants and provide a framework to dissect the genetic dialog between O. cumana and sunflower in gene-for-gene interactions.

plant biology↗

The penetration of sunflower root tissues by the parasitic plant Orobanche cumana Wallr. is intracellular

O_LIParasitic plants cause yield losses for important crops. Among these, Orobanche cumana Wallr, sunflower broomrape, is one of the major pests for sunflower. Previous studies stated that in most cases, the haustorium, a specific parasitic plant organ, penetrates host roots intercellularly. However, host cellular mechanisms involved during the parasitic cells penetration remained poorly described. C_LIO_LIWe investigated sunflower root cellular behavior during haustorium penetration using various microscopy approaches including live cell imaging of inoculated transgenic fluorescent sunflower roots. C_LIO_LIWe showed that the haustorium of O. cumana penetrated living sunflower root tissues, as a result of the degradation of the host cell wall and the formation of a new host trans-cellular apoplastic compartment for haustorium accommodation. Moreover, broomrape induced cell divisions in outer root tissues at very early stages of the interaction, leading to localized hypertrophy at the site of broomrape attachments. C_LIO_LIThese findings are a change of paradigm in the research field of parasitic plants. They extend host root intracellular accommodation mechanisms initially shown for symbiotic and pathogenic biotrophic fungi to parasitic plants. It paves the way for future understanding and development of resistance to parasitic plants. C_LI Key messageCombination of in vivo confocal, large field and transmission electron microscopy approaches revealed how intimate the relationship between the parasitic plant broomrape (Orobanche cumana Wallr.) and its sunflower host (Helianthus annus L.) is at very early stages of their interaction.

plant biology↗

The genomics of linkage drag in sunflower

Crop wild relatives represent valuable sources of alleles for crop improvement, including adaptation to climate change and emerging diseases. However, introgressions from wild relatives might have deleterious effects on desirable traits, including yield, due to linkage drag. Here we comprehensively analyzed the genomic and phenotypic impacts of wild introgressions into cultivated sunflower to estimate the impacts of linkage drag. First, we generated new reference sequences for seven cultivated and one wild sunflower genotype, as well as improved assemblies for two additional cultivars. Next, relying on previously generated sequences from wild donor species, we identified introgressions in the cultivated reference sequences, as well as the sequence and structural variants they contain. We then used a ridge regression model to test the effects of the introgressions on phenotypic traits in the cultivated sunflower association mapping population. We found that introgression has introduced substantial sequence and structural variation into the cultivated sunflower gene pool, including > 3,000 new genes. While introgressions reduced genetic load at protein-coding sequences and positively affected traits associated with abiotic stress resistance, they mostly had negative impacts on yield and quality traits. Introgressions found at high frequency in the cultivated gene pool had larger effects than low frequency introgressions, suggesting that the former likely were targeted by artificial selection. Also, introgressions from more distantly related species were more likely to be maladaptive than those from the wild progenitor of cultivated sunflower. Thus, pre-breeding efforts should focus, as far as possible, on closely related and fully compatible wild relatives.

genomics↗

Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower

Genes under balancing selection control phenotypes such as immunity, color or sex, but are difficult to identify. Self-incompatibility genes are under negative frequency-dependent selection, a special case of balancing selection, with up to 30 to 50 alleles segregating per population. We developed a method based on pooled Single-Molecule transcriptomics to identify balanced polymorphisms expressed in tissues of interest. We searched for multi-allelic, non-recombining genes causing self-incompatibility in wild sunflower (Helianthus annuus). A diversity scan in pistil identified a gene, Ha7650b,that displayed balanced polymorphism and colocalized with a quantitative trait locus for self-incompatibility. Unexpectedly, Ha7650b displayed gigantism (400 kb), which was caused by increase in intron size as a consequence of suppressed recombination. Ha7650b emerged after a whole-genome duplication (29 millions years ago) followed by tandem duplications and neofunctionalisation. Ha7650b shows expression, genetic location, genomic neighbourhood and predicted function that provide strong evidence that it is involved in self-incompatibility. Pooled Single-Molecule transcriptomics is an affordable and powerful new method that makes it possible to identify diversity and structural outliers simultaneously. It will allow a breakthrough in the discovery of self-incompatibility genes and other expressed genes under balancing selection.

evolutionary biology↗

Massive haplotypes underlie ecotypic differentiation in sunflowers

Species often include multiple ecotypes that are adapted to different environments. But how do ecotypes arise, and how are their distinctive combinations of adaptive alleles maintained despite hybridization with non-adapted populations? Re-sequencing of 1506 wild sunflowers from three species identified 37 large (1-100 Mbp), non-recombining haplotype blocks associated with numerous ecologically relevant traits, and soil and climate characteristics. Limited recombination in these regions keeps adaptive alleles together, and we find that they differentiate several sunflower ecotypes; for example, they control a 77 day difference in flowering between ecotypes of silverleaf sunflower (likely through deletion of a FLOWERING LOCUS T homolog), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, associated with polymorphic structural variants, and often appear to represent introgressions from other, possibly extinct, congeners. This work highlights a pervasive role of structural variation in maintaining complex ecotypic adaptation.

evolutionary biology↗

Comparison of GWAS models to identify non-additive genetic control of flowering time in sunflower hybrids

Genome-wide association studies are a powerful and widely used tool to decipher the genetic control of complex traits. One of the main challenges for hybrid crops, such as maize or sunflower, is to model the hybrid vigor in the linear mixed models, considering the relatedness between individuals. Here, we compared two additive and three non-additive association models for their ability to identify genomic regions associated with flowering time in sunflower hybrids. A panel of 452 sunflower hybrids, corresponding to incomplete crossing between 36 male lines and 36 female lines, was phenotyped in five environments and genotyped for 2,204,423 SNPs. Intra-locus effects were estimated in multi-locus models to detect genomic regions associated with flowering time using the different models. Thirteen quantitative trait loci were identified in total, two with both model categories and one with only non-additive models. A quantitative trait loci on LG09, detected by both the additive and non-additive models, is located near a GAI homolog and is presented in detail. Overall, this study shows the added value of non-additive modeling of allelic effects for identifying genomic regions that control traits of interest and that could participate in the heterosis observed in hybrids.

genetics↗