Genetic battle of the sexes plays out in cukes and melons

Two new genetic insights could make plants’ sex more convenient for the people growing and eating them.

Genes that keep a plant from fertilizing itself can be transferred successfully from one species to another across an unexpectedly wide evolutionary gap, says Noni Franklin-Tong of the University of Birmingham in England. And research on melons and cucumbers shows how the interplay of three main genes controls the shifts between unisexual and bisexual blooms, says Abdelhafid Bendahmane of the INRA French national agricultural labs in Évry.  

The new papers, both in the Nov. 6 Science, sharpen the understanding of plants’ control over how sexual organs develop and function in individual blooms. Even though textbook diagrams show male and female flower parts snugged into a single blossom, plants vary enormously in terms of sex and blooms, with important implications for agriculture. For certain crops, people now emasculate bloom after bloom by hand to make sure that seeds will be true hybrids instead of self-fertilized offspring, for example. Tweaking genes that guide plant sexual encounters could ease the production of hybrid seeds, Franklin-Tong says.

For about three decades, she has worked with the wild Papaver rhoeas, a fixture of commemorations of soldiers who died in World War I. The poppy has a robust self-incompatibility system built into its flowers that involves comparing his-and-hers versions of a particular protein. If the (male) pollen’s version of the protein matches receptive sites on the flower’s female stigma — indicating that both proteins probably came from same plant — the female tissue signals the pollen to commit cell suicide, and no seed forms.

At least two other protocols for self-incompatibility have evolved among plants. Self-chastity for flowers reduces the risks of inbreeding, which can dim the vigor of offspring. But the heightened incompatibility raises the risk that a bloom won’t find enough suitable pollen to make as many seeds as it could.

Franklin-Tong and colleagues decided to try coaxing the poppy’s self-chastity system to work in a plant group with a very different protocol. Plain curiosity, or “some crazy bit of stupidity” as she puts it, inspired the attempt to transfer poppy self-incompatibility to the mustard family’s Arabidopsis thaliana.

The little white-flowered Arabidopsis, popular in laboratories, doesn’t have its own self-incompatibility system and can in fact self-fertilize. But relatives in the mustard family use an unpoppylike system. That system blocks selfie seeds with different cell chemistry and puts the receptive identity-checking site on male parts instead of female parts.

Over several years, the team coaxed both male and female tissue of A. thaliana to turn on genes transferred from the poppy. The researchers now finally present results from whole plants. The transfer “worked like a dream,” Franklin-Tong concludes. So when she asked how long ago the poppy and mustard ancestors had diverged, she was startled to discover they had parted ways more than 140 million years ago. The transferred genetic pieces had succeeded in preventing self-fertilization in a very different plant.

“An important result,” says Spencer Barrett of the University of Toronto, who has also studied the evolution of self-incompatibility systems. “To my knowledge it has not been done before.”

Of course, harnessing such solutions in crops would be useful only if genetically modified plants prove acceptable to people who buy the harvest, Bendahmane of INRA points out.

His own work on how flowers control their sex could do more than reduce the need for hand emasculation. For most crops, from apples to zucchini, the female organs grow into what’s harvested. The more female flowers a plant can be coaxed to make, the bigger the yield, he says.

On the individual melon plants his lab works with, flowers with only female organs sprout on young side branches diverging from the main spine of the vine. Elsewhere, flowers are all male. Now Bendahmane’s lab and Israeli colleagues have pieced together how an individual melon plant orchestrates such sexual differences.

The interplay of three genes turned on or off in different configurations can create the variety, the team reports. For a female melon blossom, researchers found that a gene called CmACS11 turns on in the sap-carrying cells in the plant’s phloem plumbing that runs through side branches. This gene suppresses a macho gene (CmWIP1) that would otherwise drive flowers there to grow up male. And a third gene (CmACS-7), turning on in the side branches’ emerging female sex organs, completes the effect by suppressing formation of male sex organs in their bloom.

In other parts of the plant, with the go-female gene ACS11 turned off, the go-male gene kicks on, and there’s no female organ tissue with gene activity that prevents male organs. And when a mutation disables the third gene in the trio, flowers can grow up bisexual — with organs of both sexes inside the same flower. With genes for one sex suppressing the other’s, “it’s a war,” Bendahmane says.

The shenanigans of these genes suggest evolutionary scenarios for how plant ancestors with one configuration of flower sexes gave rise to quite different arrangements, Bendahmane says. And plants have certainly switched their arrangements over the eons of green history. The species that now segregate male and female functions on different individuals, as people do, tend to have bisexual ancestry. Now geneticists are a little closer to understanding, and tinkering with, plant history.