Maternal factors have stronger effect on family sex ratio than nuclear factors in a trans-Atlantic cross of Silene vulgaris

ABSTRACT

Background: Sex determination in cyto-nuclear gynodioecious plants (those with females and hermaphrodites) is complex, with maternally inherited mitochondrial genes (CMS factors) causing male sterility and female phenotypes, and bi-parentally inherited nuclear genes (Rf) restoring male fertility, resulting in hermaphrodite phenotypes. Many gynodioecious species harbour multiple CMS and restoration factors.

Aims: We tested the hypothesis that these sex determination factors were matched between geographically proximal populations and mismatched between distant populations, with the prediction that crosses from populations from the same continents would produce relatively more hermaphrodites, and crosses across continents would produce relatively more females.

Methods: We measured the progeny sex ratios from reciprocal crosses among 10 families of Silene vulgaris from North America and Europe and sequenced the mitochondrial atp1 gene for each family.

Results: Our results were inconsistent with the prediction of a mismatch between geographically distant populations. Progeny sex ratios suggested that frequencies of male fertility restorer alleles had low variability worldwide.

Conclusions: Progeny sex ratios suggested at least four different matching CMS and restorer loci segregating within the cross and alluded to a cost of restoration. Our results support previous research indicating that both CMS and restorer types are maintained over long time periods.

KEYWORDS:

• Cytoplasmic male sterility
• gynodioecy
• male fertility restorer
• metapopulation
• population structure

Acknowledgements

We thank Brian Sanderson for discussions during the development of the manuscript and Ariana Graf for help in the greenhouse. We also thank Barbara Mable, Xavier Picó and five anonymous reviewers for insightful suggestions.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by the US National Science Foundation grant no. DEB 03-17115 and by the Ministry of Education, Youth and Sports of the Czech Republic (MSMT) grant KONTAKT II LH15075.

Notes on contributors

Matthew S. Olson

Matthew S. Olson's research focuses on the evolution of plant reproductive systems, local adaptation and adaptation in invasive species.

Helena Štorchová

Helena Štorchová is works in the field of cytoplasmic male sterility, mitochondrial genomics and the regulation of flowering.

Gary Houliston

Gary Houliston is interested in plant population genetics and breeding systems with a focus on biodiversity and biosecurity.

Jessica Armstrong

Jessica Armstrong is broadly interested in plant adaptation to Arctic environments, with specific focus on understanding the molecular and physiological mechanisms plants use to tolerate cold and their potential resilience to climate change.