The Battle of the Sexes: The Gene That Female-Sterilizes Kiwifruit Flowers
By Céline Caseys
The Faulty Gender Concept
Do you think that gender in humans is self-evident? Maybe yes, maybe not so much. Wait to read about plants!
When thinking about gender it seems simple: there is male and female. Human men have XY chromosomes and women have XX. But even in humans, it can get a bit fuzzy. What makes male or female is in fact a complex interplay of genetics, development, and sometimes environment (Bachtrog et al., 2014).
What about organisms without distinct sexes? An organism with both male and female reproductive organs, a hermaphrodite, seems unusual. This may read as a shocking fact but most flowers are hermaphrodites. If you don’t believe me look at the flowers below.
Flowers are Hermaphrodites… Except When They’re Not
Flowering plants with distinct sexes (male and female on different plants) are super rare. It happens in approximately 5% of all flowering plants. It probably evolved independently in various plant families. Each of these plant species with distinct sexes represents a chance for biologists to understand the molecular mechanisms and strategies that result in flowers with only one or both types of reproductive organs.
If you wonder whether the plants you eat have distinct sexes: asparagus, pistachio, papaya, persimmon, and kiwifruits all have distinct sexes. Most of the other fruits and veggies you eat are yummy hermaphrodites.
What Makes a Male Flower in Kiwifruit
Takashi Akagi and colleagues took on the challenge of identifying the genes that make male and female kiwifruit flowers distinct. Their findings about the male part of the story were published recently in The Plant Cell (Akagi et al., 2018).
Kiwifruit is interesting not only because of its commercial importance but also because all species closely related to kiwifruit have distinct sexes. Thus it appears to be an ancient trait. Indeed, the authors calculated that distinct sexes appeared about 20 millions years ago in the genus Actinidia before the evolution of the different kiwifruit species that exist today.
Morphologically, female kiwifruit flowers look deceptive. They look like hermaphrodites, with both male and female organs, but the male organs produce sterile pollen. On different plants, male flowers produce fertile pollen but have reduced and sterile carpels, the female structures containing ovules. The researchers know so far how to explain the morphological difference in male flowers and therefore the origin of female sterility.
For finding the sex genes, the researchers sequenced both male and female individuals. Comparing whole genomic sequences showed general differences in the genome between genders and allowed for the description of the general location of sex-determining genes. They were found on a small area of a chromosome; a bit like finding a tiny island in the middle of the wavy and dangerous ocean.
To identify which of the genes present on “this island” is making male kiwifruit flowers “male only”, the researchers analyzed the gene expression profile of young flower tissue to see which genes are being turned on, or expressed, specifically in these organs. This analysis revealed the specific role of a gene that the authors beautifully named “Shy Girl”, because when this gene is expressed, it is as if the female part of the flower wants to remain hidden.
Shy Girl, the Gene That Female-Sterilizes Male Flowers
Shy Girl encodes a male-specific cytokinin response regulator. This is a receptor protein that detects cytokinin, a plant hormone involved in plant growth, and relays orders to regulate the growth of nearby cells. This regulator is expressed specifically at the surface of the sterile carpel in male flowers. As shown functionally in Arabidopsis and Nicotiana transgenic plants, the activity of this protein stops carpel development resulting in female sterility. Thus it is a negative regulator: when present it prevents cytokinin from initiating the development of carpels.
In short, the male flowers seem to have all the genes necessary to create the female structure, but evolved a gene that blocks the construction process. This repressing behaviour is not limited to kiwifruit. In asparagus, both sex organs start developing but later in the development one degenerates (Harkess et al., 2017). In Persimmon (Akagi et al., 2016) and papaya (Aryal and Ming 2014), development is further influenced by epigenetics, adding a layer of flexibility. In other words, distinct genders in plants are fragile and subtle, like the flowers themselves.
Department of Plant Sciences
University of California, Davis
Akagi, T., Henry, I.M., Ohtani, H., Morimoto, Y., Beppu, K., Kataoka, I., and Tao, R. (2018). A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit. Plant Cell https://doi.org/10.1105/tpc.17.00787.