How female ferns make younger neighbors male

Precocious dames and nearby laggards split the job of making a hormone

Japanese climbing fern

BEHIND THE LEAVES  The Japanese climbing fern in its spore-making form (shown) will create a new generation of specialized, chemically adept sexual offspring that can masculinize their neighbors.

Doug Goldman/NPDT/NRCS/USDA

Female ferns off to a fast start toward sexual maturity do some unusual two-partner chemistry to turn their slow-developing neighbors into a convenient bevy of males.

Biologists have known since 1950 that the sexual forms of certain ferns release compounds that can masculinize nearby individuals into handy sources of sperm. Now a series of experiments on Japanese climbing ferns (Lygodium japonicum) reveals the odd way the plants can engineer neighbors’ sex, researchers report in the Oct. 24 Science.

Fern sex is not some flowery business with bees. The lacy fronds most familiar as ferns don’t have sex. Instead, the frond generation releases spores that sprout into a specialized sexual generation that looks nothing like the fronds. The gamete-mixing generation grows as fingernail-sized or smaller snippets of thin green tissue called prothalli.  These easy-to-overlook bits form eggs and swimming sperm, which unite to create a third generation, this time back to big, leafy fronds.

In Japanese climbing ferns, the first spores to germinate in a cloudlet of spores that wafts into a suitable spot tend to become female. These fast-start prothalli undergo a surge in producing enzymes that make a particular form of the widespread plant compounds called gibberellins, reports Miyako Ueguchi-Tanaka of Nagoya University in Japan and her colleagues.

fern offspring
SEXUAL GENERATION The easily overlooked offspring of the leafy generation of ferns, a female prothallus (left) of a Japanese climbing fern is about 2 millimeters wide and a male (right) is 5 millimeters. Arrows mark their respective sex organs. J. Tanaka et al/Science 2014

In the myriad forms of flowering plants, gibberellins act as hormones, driving growth and development. But the form that seeps out of the fern girls is inactive.

Why a fern would release inactive forms of gibberellin has been a puzzle, says plant molecular geneticist Tai-ping Sun of Duke University, who studies the compounds but was not involved in the research. It’s not just Japanese climbing ferns that do it. Of more than 10 fern species in which young females are known to masculinize nearby prothalli, the only signaling compounds detected have been inactive gibberellin forms.

The new paper solves that mystery. Japanese climbing fern prothalli pick up the inactive, hydrophobic form from water much more readily than they pick up the active form, the researchers found. And the prothalli getting off to a late start are producing a surge of some enzymes — different from those abundant in their precocious neighborshat — that turn the inactive compound into an active gibberellin that masculinizes them, the researchers found.

After tweaking by the recipient prothallus, it’s the same gibberellin molecule that’s active in seed plants, Sun notes. Another novelty of the paper, she says, is the “clever mechanism” that divides the manufacture of the masculinizer into two parts.

As far as they know, say Ueguchi-Tanaka and coauthor Makoto Matsuoka, also of Nagoya, this is the first example of plants using a partly formed hormone as a signal that the receiver puts the finishing touches on and uses.

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