Functional bisporangiate cones in Pinus johannis (Pinaceae): Implications for the evolution of bisexuality in seed plants

Premise of study: Bisexuality (male and female function in one structure) has been reported as a key innovation of angiosperms. Although there are several reports of "teratological" bisporangiate (bisexual) cones in gymnosperms, there have been none on the viability of their ovules and pollen. Analyses of the development and arrangement of female and male structures on bisporangiate cones of Pinus johannis enables us to gain insight on the origin of bisexuality in seed plants, for both angiosperms and gymnosperms. Methods: Viability of bisporangiate cones was assayed by performing manual crosses and using anatomical and histological methods. Key results: We determined that bisporangiate cones of P. johannis produce functional pollen and ovules. Male and female organs occupy basal and apical positions, respectively, the same positions found in almost all bisporangiate strobili in gymnosperms and bisexual flowers in angiosperms. Conclusions: The viability and spatial distribution of female and male organs of bisporangiate cones and their frequent occurrence in gymnosperms suggest a common mechanism in all seed plants for the production of bisporangiate structures. This idea is further supported by the presence of homologous genes for sexual organ identity in gymnosperms and angiosperms as reported by other authors. The lack of bisporangiate structure in gymnosperms may be primarily due to selection to avoid inbreeding rather than to genetic constraint.