Genetic basis and dual adaptive role of floral pigmentation in sunflowers.

Variation in floral displays, both between and within species, has been long known to be shaped by the mutualistic interactions that plants establish with their pollinators. However, increasing evidence suggests that abiotic selection pressures influence floral diversity as well. Here, we analyse the genetic and environmental factors that underlie patterns of floral pigmentation in wild sunflowers. While sunflower inflorescences appear invariably yellow to the human eye, they display extreme diversity for patterns of ultraviolet pigmentation, which are visible to most pollinators. We show that this diversity is largely controlled by cis-regulatory variation affecting a single MYB transcription factor, HaMYB111, through accumulation of ultraviolet (UV)-absorbing flavonol glycosides in ligules (the 'petals' of sunflower inflorescences). Different patterns of ultraviolet pigments in flowers are strongly correlated with pollinator preferences. Furthermore, variation for floral ultraviolet patterns is associated with environmental variables, especially relative humidity, across populations of wild sunflowers. Ligules with larger ultraviolet patterns, which are found in drier environments, show increased resistance to desiccation, suggesting a role in reducing water loss. The dual role of floral UV patterns in pollinator attraction and abiotic response reveals the complex adaptive balance underlying the evolution of floral traits.

Flowers are an important part of how many plants reproduce. Their distinctive colours, shapes and patterns attract specific pollinators, but they can also help to protect the plant from predators and environmental stresses. Many flowers contain pigments that absorb ultraviolet (UV) light to display distinct UV patterns ­ although invisible to the human eye, most pollinators are able to see them. For example, when seen in UV, sunflowers feature a 'bullseye' with a dark centre surrounded by a reflective outer ring. The sizes and thicknesses of these rings vary a lot within and between flower species, and so far, it has been unclear what causes this variation and how it affects the plants. To find out more, Todesco et al. studied the UV patterns in various wild sunflowers across North America by considering the ecology and molecular biology of different plants. This revealed great variation between the UV patterns of the different sunflower populations. Moreover, Todesco et al. found that a gene called HaMYB111 is responsible for the diverse UV patterns in the sunflowers. This gene controls how plants make chemicals called flavonols that absorb UV light. Flavonols also help to protect plants from damage caused by droughts and extreme temperatures. Todesco et al. showed that plants with larger bullseyes had more flavonols, attracted more pollinators, and were better at conserving water. Accordingly, these plants were found in drier locations. This study suggests that, at least in sunflowers, UV patterns help both to attract pollinators and to control water loss. These insights could help to improve pollination ­ and consequently yield ­ in cultivated plants, and to develop plants with better resistance to extreme weather. This work also highlights the importance of combining biology on small and large scales to understand complex processes, such as adaptation and evolution.

Massive haplotypes underlie ecotypic differentiation in sunflowers.

Species often include multiple ecotypes that are adapted to different environments1. However, it is unclear how ecotypes arise and how their distinctive combinations of adaptive alleles are maintained despite hybridization with non-adapted populations2-4. Here, by resequencing 1,506 wild sunflowers from 3 species (Helianthus annuus, Helianthus petiolaris and Helianthus argophyllus), we identify 37 large (1-100 Mbp in size), non-recombining haplotype blocks that are associated with numerous ecologically relevant traits, as well as soil and climate characteristics. Limited recombination in these haplotype blocks keeps adaptive alleles together, and these regions differentiate sunflower ecotypes. For example, haplotype blocks control a 77-day difference in flowering between ecotypes of the silverleaf sunflower H. argophyllus (probably through deletion of a homologue of FLOWERING LOCUS T (FT)), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, frequently associated with structural variants and often appear to represent introgressions from other-possibly now-extinct-congeners. These results highlight a pervasive role of structural variation in ecotypic adaptation.

Intraspecific genetic divergence within Helianthus niveus and the status of two new morphotypes from Mexico.

PREMISE: Collecting and characterizing the genetic diversity of wild relatives of crops can contribute importantly to sustainable crop production and food security. Wild sunflower, Helianthus niveus, occurs in arid regions in western North America and is partially cross-compatible with the cultivated sunflower (H. annuus). We assessed phylogenetic relationships and patterns of genetic divergence among three previously described subspecies (subsp. niveus, subsp. canescens, and subsp. tephrodes) as well as two new morphotypes of H. niveus recently discovered in extreme drought and dune habitats in Baja California, Mexico. METHODS: We measured 50 plants growing in a common garden for 27 morphological traits and conducted principal component analysis to assess patterns of phenotypic variation. Genome size of each accession was determined using flow cytometry. Pollen viability of first generation hybrids between taxa was tested to infer the strength of intrinsic postzygotic reproductive barriers. Finally, genotyping-by-sequencing data were used to investigate the genetic structure and phylogenetic relationships among the previously described subspecies and new morphotypes. RESULTS: The intraspecific genetic and phenotypic divergence of H. niveus populations closely tracks their geographical distribution. Subspecies niveus is phenotypically, genetically, and reproductively distinct from the other two subspecies and has a larger genome. Therefore, H. niveus as currently circumscribed should be considered to contain two distinct species, H. niveus and H. tephrodes. ABBA-BABA tests revealed substantial introgression between subsp. canescens and its sympatric congener H. petiolaris, which might contribute to their morphological similarities. The two new morphotypes collected in Mexico represent local ecotypes of subsp. niveus that occur in extreme drought and dune environments. Mantel tests showed a strong positive correlation between genetic and geographic distances. CONCLUSIONS: We conclude that geographic isolation is primarily responsible for intraspecific genomic divergence within H. niveus, while patterns of phenotypic variation appear to have been shaped by ecological selection and interspecific introgression.