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

Marco Todesco,Gregory L Owens,Jean-Sébastien Légaré,Natalia Bercovich,Loren H Rieseberg,Benjamin K Blackman,Óscar Dorado Ruiz,Lufiani L Madilao,Mojtaba Jahani,Ivana Imerovski,Srinidhi V Holalu,Amy Kim

doi:10.7554/elife.72072

Abstract

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.

Highlights

The diversity in colour and colour patterns found in flowers is one of the most extraordinary examples of adaptive variation in the plant world
We measured floral UV patterns in 1589 H. annuus individuals derived from 110 distinct natural populations and 351 H. petiolaris individuals from 40 populations, grown in common garden
Together with the observation that the strongest genome-wide association study (GWAS) association with ligule ultraviolet proportion (LUVp) fell in the promoter region of HaMYB111, these results suggest that differences in the effect of the ‘small’ and ‘large’ alleles of this gene on floral UV pigmentation are not due to differences in protein function, but rather to differences in gene expression

Summary

Introduction

The diversity in colour and colour patterns found in flowers is one of the most extraordinary examples of adaptive variation in the plant world. Pollinator visitation and preference (Brock et al, 2016; Horth et al, 2014; Rae and Vamosi, 2013; Sheehan et al, 2016) Besides their importance for pollinator attraction, patterns of UV-a bsorbing pigments in flowers have increasingly been recognized to have a role in responses to other biotic and abiotic factors, including defence against insect herbivory (Gronquist et al, 2001), protection against UV radiation (Koski and Ashman, 2015; Koski et al, 2020), and adaptation to different temperatures (Koski and Ashman, 2016; Koski et al, 2020). We explore the diversity of floral UV pigmentation in wild sunflowers and the genetic mechanisms and environmental factors that shape this variation

Results and discussion

10 Promoter: p35SCaMV pAtMYB111 c Leaf e 2000

Conclusions

Materials and methods

Funding Funder