The <i>Gunnera manicata—Nostoc</i> Symbiosis: Is the Red Stipulate Tissue Symbiogenetic?

Abstract

All species of the angiosperm genus Gunnera form an intracellular symbiosis with hormogonium-pro ducing strains of Nostoc cyanobacteria. Gunnera is the only angiosperm genus known to enter symbi otic associations with cyanobacteria capable of fixing nitrogen. Unlike most symbioses, the Gun nera cyanobacterial associations are intracellular (Bergman et al. 1992). Of the 45 species of Gun nera, the smaller species are typically aquatic, whereas the larger species tend to occupy high-al titude cliff faces and stream banks (Osborne et al. 1991). Free-living Nostoc cyanobacteria live in the moist soils of the Gunnera habitats. They form long photosynthetic filaments that bear nitrogen-fixing heterocysts interspersed among the cells. The port of entry for Nostoc into Gunnera is via the unique glands present at the base of each leaf petiole in all Gunnera species (Bergman et al. 1992). Aseriate photoautotrophic Nostoc filaments that bear heterocysts are induced to differentiate into motile, heterocyst-free hormogonia filaments by various compounds present in the mucus secreted by the Gunnera gland tissue. The Nostoc hormogonia respond to a chemical signal and glide down the extracellular channels of the Gunnera gland, against the direction of both gland mucilage production and their usual positive phototaxis, to enter the Gunnera cortical cells. In the dark, Nostoc cells become heterotrophic, intracellular sym bionts. They rely on Gunnera for photosynthates, and the fixed nitrogen from their now re-differen tiated heterocysts is assimilated by the plant tissue. 'Whereas all Gunnera species, small and large, bear Nostoc-infecting glands, only the larger Gunnera species possess clusters of large red stipules that abundantly surround glands at the base of each leaf petiole (P1. IA-C). They are more distinc tively distributed, pigmented, mucous-laden and conspicuous than other plant stipules. We concur that the term 'stipule' (rather than bract or leaf bud) is the most accurate one for these structures. The focus of Gunnera-Nostoc symbiosis research is on the process by which Nostoc infects the Gunnera gland, not on the presence of Nostoc on the plant tissue surrounding the gland. Such an emphasis causes the stipulate tissue on the larger Gunnera species to be ignored in the literature, as it is often removed from the plant by researchers who have studied the gland tissue buried beneath.