Gunnera tinctoria: An Unusual Nitrogen-Fixing Invader

Osborne, Bruce; Doris, Fiona; Cullen, Ann; McDonald, R. N.; Campbell, Garret; Steer, Martin

doi:10.2307/1311412

Cited by 45 publications

(59 citation statements)

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“…Gunnera manicata). Even in the latter case, N 2 fixed by the symbiotic cyanobacteria, most likely in the form of NH 3 (Silvester et al, 1996), is able to fulfill the N needs of the plant (Osborne et al, 1991(Osborne et al, , 1992.In nature, Gunnera plants form symbioses with cyanobacteria belonging to the genus Nostoc (Bergman et al, 1992). Unlike other multicellular plant hosts, Gunnera harbors Nostoc intracellularly, surrounding the Nostoc filaments with a membrane most likely of plasma membrane origin (Silvester and McNamara, 1976;Johansson and Bergman, 1992).…”

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“…Subsequently, one new gland typically appears on the stem at the base of each new leaf. Under natural conditions, all of the glands are colonized by cyanobacteria (Bonnett, 1990;Osborne et al, 1991).Anatomical studies of several different Gunnera species have determined that a gland originates from a group of cells within the stem that resume mitotic activities after seedling establishment (Bonnett, 1990;Johansson and Bergman, 1992). Each progenitor cell produces an independent multicellular papilla that extends externally, eventually rupturing the epidermal layer.…”

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Nitrogen Deprivation Stimulates Symbiotic Gland Development in Gunnera manicata

et al. 2005

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Gunnera is the only genus of angiosperms known to host cyanobacteria and the only group of land plants that hosts cyanobacteria intracellularly. Motile filaments of cyanobacteria, known as hormogonia, colonize Gunnera plants through cells in the plant's specialized stem glands. It is commonly held that Gunnera plants always possess functional glands for symbiosis. We found, however, that stem gland development did not occur when Gunnera manicata plants were grown on nitrogen (N)-replete medium but, rather, was initiated at predetermined positions when plants were deprived of combined N. While N status was the main determinant for gland development, an exogenous carbon source (sucrose) accelerated the process. Furthermore, a high level of sucrose stimulated the formation of callus-like tissue in place of the gland under N-replete conditions. Treatment of plants with the auxin transport inhibitor 1-naphthylphthalamic acid prevented gland development on N-limited medium, most likely by preventing resource reallocation from leaves to the stem. Optimized conditions were found for in vitro establishment of the Nostoc-Gunnera symbiosis by inoculating mature glands with hormogonia from Nostoc punctiforme, a cyanobacterium strain for which the full genome sequence is available. In contrast to uninoculated plants, G. manicata plants colonized by N. punctiforme were able to continue their growth on N-limited medium. Understanding the nature of the Gunnera plant's unusual adaptation to an N-limited environment may shed light on the evolution of plant-cyanobacterium symbioses and may suggest a route to establish productive associations between N-fixing cyanobacteria and crop plants.Nitrogen (N)-fixing cyanobacteria enter into symbiotic associations with a phylogenetically diverse group of eukaryotes ranging from fungi to vascular plants (Rai et al., 2000). Gunnera is the only flowering plant genus known to host cyanobacteria (Bonnett, 1990;Bergman et al., 1992;Bergman and Osborne, 2002). Plants in the genus Gunnera are mainly distributed in the southern hemisphere with about 40 species, which includes small, stoloniferous species (e.g. Gunnera magellanica) and plants 6 to 8 ft in height (e.g. Gunnera manicata). Even in the latter case, N 2 fixed by the symbiotic cyanobacteria, most likely in the form of NH 3 (Silvester et al., 1996), is able to fulfill the N needs of the plant (Osborne et al., 1991(Osborne et al., , 1992.In nature, Gunnera plants form symbioses with cyanobacteria belonging to the genus Nostoc (Bergman et al., 1992). Unlike other multicellular plant hosts, Gunnera harbors Nostoc intracellularly, surrounding the Nostoc filaments with a membrane most likely of plasma membrane origin (Silvester and McNamara, 1976;Johansson and Bergman, 1992). The specialized glands on the Gunnera stem serve as entry points for Nostoc filaments. Gunnera glands are conspicuously red due to the accumulation of anthocyanins such as pelargonidin and cyanidin (G. Lanigan, K.G. Black, and B. Osborne, unpublished data). Shortly after ge...

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Nitrogen Deprivation Stimulates Symbiotic Gland Development in Gunnera manicata

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“…However, some Gunnera spp. has apparently escaped from botanical gardens and is even now invasive in Western Europe (Osborne et al, 1991;Osborne and Sprent, 2002). Naturally grown Gunnera plants are infected by cyanobacteria ( Figure 5), a phenomenon already observed at the end of the 19 th century (Reinke, 1872;1873;Jönsson, 1894;see Table 1).…”

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Cyanobacterial Associations

Bergman¹,

Rai²,

Rasmussen³

Associative and Endophytic Nitrogen-Fixing Bacteria and Cyanobacterial Associations

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Using soil seed banks to assess temporal patterns of genetic variation in invasive plant populations

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Gallagher

Vintró

et al. 2014

Ecology and Evolution

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Most research on the genetics of invasive plant species has focused on analyzing spatial differences among existing populations. Using a long-established Gunnera tinctoria population from Ireland, we evaluated the potential of using plants derived from seeds associated with different soil layers to track genetic variation through time. This species and site were chosen because (1) G. tinctoria produces a large and persistent seed bank; (2) it has been present in this locality, Sraheens, for ∼90 years; (3) the soil is largely undisturbed; and (4) the soil's age can be reliably determined radiometrically at different depths. Amplified fragment length polymorphic markers (AFLPs) were used to assess differences in the genetic structure of 75 individuals sampled from both the standing population and from four soil layers, which spanned 18 cm (estimated at ∼90 years based on 210Pb and 137Cs dating). While there are difficulties in interpreting such data, including accounting for the effects of selection, seed loss, and seed migration, a clear pattern of lower total allele counts, percentage polymorphic loci, and genetic diversity was observed in deeper soils. The greatest percentage increase in the measured genetic variables occurred prior to the shift from the lag to the exponential range expansion phases and may be of adaptive significance. These findings highlight that seed banks in areas with long-established invasive populations can contain valuable genetic information relating to invasion processes and as such, should not be overlooked.

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Gunnera tinctoria: An Unusual Nitrogen-Fixing Invader

Cited by 45 publications

References 38 publications

Nitrogen Deprivation Stimulates Symbiotic Gland Development in Gunnera manicata

Nitrogen Deprivation Stimulates Symbiotic Gland Development in Gunnera manicata

Cyanobacterial Associations

Using soil seed banks to assess temporal patterns of genetic variation in invasive plant populations

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