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Birgitta Bergman - One of the best experts on this subject based on the ideXlab platform.
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The Gunnera Symbiosis: DNA Restriction Fragment Length Polymorphism and Protein
2016Co-Authors: Comparisons Of Nostoc Symbionts, William J. Z Immerman, Birgitta BergmanAbstract:Abstract. Cyanobacteria separated from symbiosis with several species of the angiosperm Gunnera were comparatively characterized and corre-lated with the locales and taxonomy of their host plants. All were identified as strains of Nostoc. Protein profiles and DNA restriction fragment length polymorphisms (from hybridizations with heterologous n/JH and glnA probes) determined that three of the four cyanobacteria from Gunnera grown at one site in Sweden, each from a different host species, were very similar or identical. Plants of one species, G. manicata, grown in a second location at the site were infected with a different cyanobiont. Among five isolates from two species of Gunnera, collected in the same locale in New Zealand, three subgroups were documented. Isolates from three different Gunnera species grown in separate locations in the United States were each uniquely different. None of the cyanobacteria differed in the molecular weights of their glutamine synthetase and Fe-nitrogenase proteins. The diversity and accessibility of compatible Nostoc populations present in the soil micro-environment, ot a critical selective factor required by Gunnera, were concluded to be a major determinant in symbiont selection
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why does Gunnera do it and other angiosperms don t an evolutionary perspective on the Gunnera nostoc symbiosis
2008Co-Authors: Bruce Osborne, Birgitta BergmanAbstract:The Gunnera–Nostoc symbiosis is an enigmatic plant–cyanobacterial symbiosis: the only known angiosperm–cyanobacterial symbiosis. We postulate that this symbiosis, together with perhaps all other plant–cyanobacterial symbioses, was more important in the geological past and was a response to a unique suite of environmental conditions that are uncommon today. Phylogenetic analyses indicate a distinct origin for the evolution of the Gunnera–Nostoc symbiosis within the angiosperms, although we suggest that this symbiosis may share more common features with both rhizobial and Frankia symbioses than might have been expected. Whilst we can only speculate on the evolutionary drivers that led to the establishment of the Gunnera–Nostoc symbiosis, there is plausible evidence that this could have been related to low oxygen-induced nitrogen deficiency. There is even evidence that low oxygen conditions can induce a number of factors that could be related to the establishment of plant–bacterial symbioses (rhizobia and Frankia). A particularly important goal for the future is the identification of the origin and development of specialised Gunnera glands, which are the conduit through which cyanobacteria enter cortical tissue. Currently we have little understanding of the functional or evolutionary significance of this structure. Far from being glands, in the strictest sense, there is evidence for an origin associated with adventitious root formation, a feature that also has parallels with nodule formation in legumes. This requires more detailed investigation.
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The Gunnera— Nostoc Symbiosis
Biology & Environment: Proceedings of the Royal Irish Academy, 2002Co-Authors: Birgitta Bergman, Bruce OsborneAbstract:Among angiosperms, a restricted number of plants are capable of forming symbioses with nitrogen fixing organisms. The best-studied examples of symbiosis are those between legumninous plants and nitrogen-fixing rhizobia. Although cyanobacteria are the most potent nitrogen-fixing microsymbionts in terms of variations in the taxonomy of the hosts, ranging from fungi to higher plants, extant cyanobacterial symbioses encompass only one an giosperm family. This monogeneric family, the Gunneraceae, has an unclear taxonomic affiliation. It comprises about 50 species, which show great variation in size. The larger, rhubarb-like, stand forming species (up to 6m high) are typical of areas ranging from Hawaii to Central America and South America, whereas smaHer, more slender species are found in New Zealand, South-East Asia and the southernmost parts of South America. The eleven endemic species of New Zealand are all small, often < 10cm high, and form stolons, whereas the larger species are rhizomatous. The natural distribution of Gunnera is restricted to the southern hemisphere, but naturalised Gunnera (G. tinctoria) is now known from some European sites, for instance the west coast of Ireland, south-western England, northern France and the Azores. A characteristic of all Gunnera species is their preference for wet and humid areas. Ever since cyanobacteria were discovered in side cells of Gunnera at the end of the nineteenth century, they have been classified as belonging to the genus Nostoc. This is a widespread and globally common filamentous genus capable of advanced cell differentiation. Under nitrogen limitation, het erocysts (sites for the nitrogen-fixing enzyme intro genase) are formed, constituting 5-10% of the total cell population, whereas other adverse conditions may give rise to motile hormogonia or resting spores (akinetes). The differentiation of hormogo nia (the de facto infection units in symbioses) and heterocysts is crucial to the formation of the Gunnera symbioses. Although possibly restricted to the genus Nostoc, several species and strains are capable of forming symbioses with Gunnera, including those compatible with plants such as liverworts and cycads. These aspects of cyano bacterial specificity in symbioses are fairther discussed by Rasmussen and Johansson (this volume).
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isolation of host plant induced cdnas from nostoc sp strain pcc 9229 forming symbiosis with the angiosperm Gunnera spp
Symbiosis, 2001Co-Authors: Anton Liaimer, Andrey Matveyev, Birgitta BergmanAbstract:The identification of three genes differentially expressed in a symbiotically competent cyanobacterium during an early stage of its infection of the angiosperm Gunnera is reported. The symbiotic isolate Nostoc sp. PCC 9229 was treated for 6 and 16 hours with the carbohydrate rich mucilage excreted by Gunnera stem glands, the infection organ known to possess multiple induction potential. Subtractive unique cDNA libraries were constructed. The cyanobacterial clones,identified after screening the libraries were tentatively termed hieA, hieB and hieC. The clones were specifically expressed in response to the secreted Gunnera gland mucilage as shown by RT-PCR. Analysis of the deduced amino acid sequences suggest that hieA encodes a putative precursor of a pheromone-like signalling peptide; hieB encodes an outer membrane or secreted glycoprotein, possibly involved in cell-identification, and the product of hieC is probably involved in adaptation to the acidic environment offered by the mucilage. The nucleotide sequences are deposited in GenBank (accession numbers AF291436, AF293349, AF292396). The potential role of these clones in symbiosis is discussed.
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cyanobacterial diversity in geographically related and distant host plants of the genus Gunnera
Archives of Microbiology, 2000Co-Authors: Malin Nilsson, Birgitta Bergman, Ulla RasmussenAbstract:The diversity among 45 cyanobacterial isolates from 11 different Gunnera species originating from different geographical areas was examined. By means of polymerase chain reaction (PCR) fingerprinting with short tandemly repeated repetitive (STRR) sequences as primers, ten groups of symbiotic cyanobacteria and five unique isolates not belonging to a particular group were identified. Most groups were restricted to one geographical area, indicating a limited distribution of related cyanobacterial strains. An extensive cyanobacterial diversity was found both within and between the 11 different Gunnera species. Within a particular plant and even within the same stem gland, more than one cyanobacterial strain at a time could be present. These results indicate a low specificity in Gunnera-Nostoc symbiosis.
Livia Wanntorp - One of the best experts on this subject based on the ideXlab platform.
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evolutionary persistence in Gunnera and the contribution of southern plant groups to the tropical andes biodiversity hotspot
PeerJ, 2018Co-Authors: Bengt Oxelman, Christine D Bacon, Francisco J Velasquezpuentes, Luis Felipe Hinojosa, Thomas Schwartz, Bernard E Pfeil, Mary T K Arroyo, Livia WanntorpAbstract:Several studies have demonstrated the contribution of northern immigrants to the flora of the tropical Andes-the world's richest and most diverse biodiversity hotspot. However, much less is known about the biogeographic history and diversification of Andean groups with southern origins, although it has been suggested that northern and southern groups have contributed roughly equally to the high Andean (i.e., paramo) flora. Here we infer the evolutionary history of the southern hemisphere plant genus Gunnera, a lineage with a rich fossil history and an important ecological role as an early colonising species characteristic of wet, montane environments. Our results show striking contrasts in species diversification, where some species may have persisted for some 90 million years, and whereas others date to less than 2 Ma since origination. The outstanding longevity of the group is likely linked to a high degree of niche conservatism across its highly disjunct range, whereby Gunnera tracks damp and boggy soils in cool habitats. Colonisation of the northern Andes is related to Quaternary climate change, with subsequent rapid diversification appearing to be driven by their ability to take advantage of environmental opportunities. This study demonstrates the composite origin of a mega-diverse biota.
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phylogenetic relationships of Gunnera based on nuclear ribosomal dna its region rbcl and rps16 intron sequences
Systematic Botany, 2009Co-Authors: Livia Wanntorp, Hans-erik Wanntorp, Mari KallersjoAbstract:Abstract A previous analysis of two chloroplast gene regions, rbcL and the rps16 intron, showed a clear phylogenetic pattern in Gunnera. However, these regions were not informative enough to completely resolve the phylogeny. In this study the nuclear ITS region was sequenced for 24 specimens representing 22 species of Gunnera. 223 characters out of 819 were informative and supported the same monophyletic groups as the chloroplast gene regions. Because of its greater information content, the ITS region identified additional well-supported clades. In an analysis based on the three gene regions together, 272 characters out of 3154 were informative. The results show that the South American annual, G. herteri is sister to all other species. The African G. perpensa is well-supported as sister to the remaining species, which form two well-defined clades, one with the Malayan G. macrophylla as sister to subgenus Milligania from New Zealand and Tasmania. In the other clade, the South American subgenus Misandra is ...
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Gunnera MORAE (GunneraCEAE), A NEW SPECIES FROM COLOMBIA
Caldasia, 2006Co-Authors: Livia Wanntorp, Jens KlackenbergAbstract:A Colombian species of Gunnera, G. morae L. Wanntorp & Klackenberg, previously mistakenly identified as Gunnera manicata Linden ex Andre, is presented and described. Molecular phylogenetic studies as well as morphological evidence have shown this plant to be different from the Brazilian true G. manicata.
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evolution of floral characters in Gunnera Gunneraceae
Systematic Botany, 2006Co-Authors: Louis P. Ronse De Craene, Livia WanntorpAbstract:Floral morphology of 16 species of Gunnera representing all six subgenera is examined and described using scanning electron microscopy (SEM). The evolution of 19 flower morphological characters is discussed. Eight of these characters are optimized on a current phylogenetic tree. Character evolution tends to be generally continuous over different clades and several parallel evolutionary patterns of floral reduction can be identified within the family. At one extreme stand species such as G. manicata and G. perpensa with mainly bisexual flowers bearing well-developed sepals and petals, and at the other stand species such as G. magellanica and G. herteri with perianthless staminate flowers, and pistillate flowers with only gynoecia and sepals. In between one finds a range of flower morphologies, bisexual or not, with petals and sepals present or absent, or discernable as reduced organs. Character-state reconstruction and morphological evidence suggest that flowers in Gunneraceae were bisexual in origin with a reduction leading to simple unisexual flowers. Among the examined characters, absence of reduced organs in the other gender, spathulate petals in the staminate flower, long styles, and the presence of well-developed bracts are typical for species of subg. Milligania. Basally connected sepal lobes with a strongly swollen base and reduced blade is found in all species of Panke and in G. magellanica (subg. Misandra). Selected synapomorphies are consistent with the deep phylogenetic division of Gunnera between the New and Old Worlds.
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Gunnera morae Gunneraceae a new species from colombia Gunnera morae Gunneraceae una nueva especie para colombia
2006Co-Authors: Livia Wanntorp, Jens KlackenbergAbstract:A Colombian species of Gunnera, G. morae L. Wanntorp & Klackenberg, previously mistakenly identified as Gunnera manicata Linden ex Andre, is presented and described. Molecular phylogenetic studies as well as morphological evidence have shown this plant to be different from the Brazilian true G. manicata.
E Soderback - One of the best experts on this subject based on the ideXlab platform.
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the nostoc Gunnera symbiosis carbon fixation and translocation
Physiologia Plantarum, 1993Co-Authors: E Soderback, Birgitta BergmanAbstract:The in vitro specific activity of ribulose-1,5-bisphosphate carboxylase (Rubisco; EC 4. 1. 1. 39) and the dark and light in vivo CO2 fixation activities were determined in the cyanobiont of Gunnera. Compared to the free-living isolate Nostoc PCC 9231, the in vitro Rubisco activity was high, while the in vivo CO2 fixation was very low. Light did not significantly influence CO2 fixation if the cyanobiont was left in the sliced Gunnera tissues, while a small light stimulation was found for CO2 fixation of the freshly-isolated cyanobiont. The adjacent non-infected Gunnera tissue showed a very low CO2 fixation. A rapid translocation of fixed 14CO2 from leaves towards apical parts of the plant was apparent, in particular to the symbiotic tissue. The 14C label appeared mainly in soluble form in this tissue and was rapidly catabolised as shown by 14C chase experiments. Also, short-term experiments revealed that maximum 14C accumulation occurred in the symbiotic tissue showing the highest rates of nitrogen fixation (Soderback et al. 1990), about 10–15 mm from the plant apex. The data were taken to indicate that there is a modification in the photosynthetic light reaction of the cyanobiont and that the cyanobiont lives heterotrophically in the dark on photo-synthate rapidly delivered from nearby leaves of the host plant.
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the nostoc Gunnera symbiosis
New Phytologist, 1992Co-Authors: Birgitta Bergman, Christina Johansson, E SoderbackAbstract:Gunnera L. develops a complex and intimate symbiosis with N2 -fixing cyanobacteria of the genus Nostoc, which renders the plant independent of combined nitrogen. The Nostoc-Gunnera symbiosis exhibits unique features compared to other cyanobacterial-plant symbioses: it is for example the only one that involves a flowering plant (angiosperm), the cyanobacterium infects specialized gland organs located on the stems of the host and once it has passed into the interior of the gland the cyanobacterium also enters the Gunnera cells where it starts to differentiate the highest frequency of heterocysts (the N2 -fixing cells) recorded in any cyanobacterial population. Gunnera has attracted scientific attention also for the following reasons: the genus has a peculiar geographic distribution of its subgenera and species in the Southern Hemisphere. It differs morphologically and anatomically from related plants and also shows an anomalous polystelic vascular system (polystely). This review gives an updated account of present knowledge concerning the Nostoc-Gunnera symbiosis. Emphasis will be on the development of the symbiotic tissue (the gland), the structure and function of the prokaryotic N2 -fixing cyanobacterium, the infection process and on the relationship between the pro- and eukaryotic partners prior to and following the establishment of symbiosis. CONTENTS Summary 379 I. Introduction 379 II. The Gunner a plant 380 III. The microsymbiont(s) 383 IV. The symbiosis 384 V. The gland 385 VI. The infection process 388 VII. Specificity 391 VIII. Impacts on the cyanobiont 392 IX. N2 fixation and release 393 X. Photosynthesis 396 XI. Concluding remarks 397 Acknowledgements 398 References 398.
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the nostoc Gunnera magellanica symbiosis phycobiliproteins carboxysomes and rubisco in the cyanobiont
Physiologia Plantarum, 1992Co-Authors: E Soderback, Birgitta BergmanAbstract:In the nitrogen fixing symbiosis between Nostoc and the angiosperm Gunnera, the cyanobiont is found in stem glands and is thought to have a heterotrophic mode of nutrition. To investigate whether the photosynthetic machinery in the cyanobiont is down-regulated in the symbiosis, the presence of the phycobiliproteins, phycoerythrin and phycocyanin, and ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco, EC 4.1.1.39) in cyanobionts of Gunnera magellanica Lam. and in a free-living (cultured) isolate of the cyanobacterium was studied by immunoelectron microscopy. Carboxysomes were numerous in all vegetative cells (ca 3.5 per cell section), and on an area basis they showed a high Rubisco label compared to the cytoplasm; but recalculation on a volume basis demonstrated that the carboxysomal fraction of Rubisco decreased in the cyanobiont along the plant stem. Along the whole Gunnera stem both types of phycobiliproteins were present in the symbiotic Nostoc and in amounts equivalent to or above those detected in the free-living isolate. As the symbiotic Nostoc is located intracellularly, out of reach of light in the plant stem, the findings indicate a lack of regulation of the photosynthetic protein synthesis in the symbiotic state.
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developmental patterns in the nostoc Gunnera symbiosis
1992Co-Authors: E SoderbackAbstract:Gunneraceae is an angiosperm family comprising about 60 species scattered in the southern hemisphere. All members of the family develop a nitrogen-fixing symbiosis with intracellularly located Nost ...
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the nostoc Gunnera magellanica symbiosis developmental patterns related to nitrogen fixation
1991Co-Authors: E Soderback, Peter Lindblad, Birgitta BergmanAbstract:Several parameters in the development of the nitrogen-fixing Nostoc-Gunnera magellanica symbiosis were studied. All parameters studied showed a developmental profile from young towards older symbiotic tissues, with the highest activities and most functional symbiosis located in relatively young parts of the plant. After leaf shedding of the plant the symbiotic cells showed signs of degeneration, and nitrogenase activity declined gradually to zero.
Catherine Damerval - One of the best experts on this subject based on the ideXlab platform.
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Combining Phylogenetic and Syntenic Analyses for Understanding the Evolution of TCP ECE Genes in
2016Co-Authors: Helene L Citerne, Martine Le Guilloux, Julie Sannier, Sophie Nadot, Catherine DamervalAbstract:TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the γ event. Genomic comparisons in Arabidopsis thaliana and Solanum lycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegia coerulea an
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combining phylogenetic and syntenic analyses for understanding the evolution of tcp ece genes in eudicots
PLOS ONE, 2013Co-Authors: Helene L Citerne, Martine Le Guilloux, Julie Sannier, Sophie Nadot, Catherine DamervalAbstract:TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the γ event. Genomic comparisons in Arabidopsis thaliana and Solanum lycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegia coerulea and Nelumbo nucifera suggests that the two TCP ECE paralogs in these species are also derived from large-scale duplications. TCP ECE loci from basal eudicots share many features with the three main core eudicot loci, and allow us to infer the makeup of the ancestral eudicot locus.
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combining phylogenetic and syntenic analyses for understanding the evolution of tcp ece genes in eudicots
PLOS ONE, 2013Co-Authors: Helene L Citerne, Martine Le Guilloux, Julie Sannier, Sophie Nadot, Catherine DamervalAbstract:TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the γ event. Genomic comparisons in Arabidopsis thaliana and Solanum lycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegia coerulea and Nelumbo nucifera suggests that the two TCP ECE paralogs in these species are also derived from large-scale duplications. TCP ECE loci from basal eudicots share many features with the three main core eudicot loci, and allow us to infer the makeup of the ancestral eudicot locus.
Bruce Osborne - One of the best experts on this subject based on the ideXlab platform.
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biological flora of the british isles Gunnera tinctoria
Journal of Ecology, 2013Co-Authors: Margherita Gioria, Bruce OsborneAbstract:Summary 1. This account presents information on all aspects of the biology of Gunnera tinctoria (Molina) Mirb. (G. chilensis Lam.; G. scabra Ruix & Pav.; G. pilosa Kunth) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characters, herbivores and disease, history and conservation. 2. Gunnera tinctoria is a gynomonoecious, clonal, perennial herb that is naturalized in parts of Britain, becoming invasive in parts of Ireland and, more recently, Scotland. It occurs where winter temperatures are mild, and precipitation and humidity are high. Gunnera tinctoria is native to South America, predominantly in the Andean region of Chile and Colombia, and probably in parts of Argentina, ranging from sea level to c. 2000 m a.s.l. 3. Typical habitats in Britain and Ireland include stream and river banks, lake and pond margins, coastal cliffs, as well as disturbed areas, such as roadsides, quarries and ditches. In its native range it occurs predominantly on the banks of rivers and streams, on coastal cliffs and within canopy gaps or at the margins of temperate-humid rain forests. 4. Gunnera tinctoria occurs on a variety of substrates, mainly on alluvial or colluvial soils derived from volcanic material or on thin gley soils of marine origin. In Ireland, it occurs naturally on soils with a pH ranging from 4.6 to 6.2 and has been cultivated in soils with a pH up to 7. Soil moisture content and soil organic matter vary greatly, although it rarely colonizes highly organic soils such as peat. It is susceptible to even mild water deficits at all stages of development, and its seedlings are also sensitive to waterlogged conditions. 5. Gunnera tinctoria produces large numbers of seeds and also spreads clonally, by a horizontal rhizome system. It is wind pollinated, although insect pollination has been reported in New Zealand. Seeds are likely to be predominantly water and/or bird dispersed. In its invasive range, it can form a large and persistent soil seed bank. Recruitment from seeds seems to be important for its initial establishment, while vegetative propagation is the main means of expansion, leading to dense clonal stands. Long-distance seed dispersal seems to be central to the colonization of new areas, although the transport of vegetative propagules may also be important. 6. Gunnera tinctoria is a strong competitor in its invasive range, particularly in wet, humid environments. Its competitive ability arises from its large stature, the persistence of its seeds and rhizomes and a capacity for fixing nitrogen through a unique intracellular symbiosis with cyanobacteria (Nostoc) that may be particularly important for supporting the rapid growth of established plants early in the spring.
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why does Gunnera do it and other angiosperms don t an evolutionary perspective on the Gunnera nostoc symbiosis
2008Co-Authors: Bruce Osborne, Birgitta BergmanAbstract:The Gunnera–Nostoc symbiosis is an enigmatic plant–cyanobacterial symbiosis: the only known angiosperm–cyanobacterial symbiosis. We postulate that this symbiosis, together with perhaps all other plant–cyanobacterial symbioses, was more important in the geological past and was a response to a unique suite of environmental conditions that are uncommon today. Phylogenetic analyses indicate a distinct origin for the evolution of the Gunnera–Nostoc symbiosis within the angiosperms, although we suggest that this symbiosis may share more common features with both rhizobial and Frankia symbioses than might have been expected. Whilst we can only speculate on the evolutionary drivers that led to the establishment of the Gunnera–Nostoc symbiosis, there is plausible evidence that this could have been related to low oxygen-induced nitrogen deficiency. There is even evidence that low oxygen conditions can induce a number of factors that could be related to the establishment of plant–bacterial symbioses (rhizobia and Frankia). A particularly important goal for the future is the identification of the origin and development of specialised Gunnera glands, which are the conduit through which cyanobacteria enter cortical tissue. Currently we have little understanding of the functional or evolutionary significance of this structure. Far from being glands, in the strictest sense, there is evidence for an origin associated with adventitious root formation, a feature that also has parallels with nodule formation in legumes. This requires more detailed investigation.
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nitrogen deprivation stimulates symbiotic gland development in Gunnera manicata
Plant Physiology, 2005Co-Authors: Wanling Chiu, Gerald A Peters, Germain Levieille, Patrick C Still, Sarah M Cousins, Bruce Osborne, Jeff ElhaiAbstract: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.
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uptake and metabolism of glucose in the nostoc Gunnera symbiosis
New Phytologist, 2002Co-Authors: Kevin Black, Richard Parsons, Bruce OsborneAbstract:Summary • The transition of Nostoc colonies from free-living to symbiotic conditions, in the Nostoc–Gunnera association, involves increased heterocyst frequency and a reliance on carbon imported from the host for metabolic processes, including N2 fixation. • Here the uptake of a glucose analogue, 3-[14C]-O-methyl-glucose (14C-OMG), in freshly isolated symbiotic and free-living Nostoc cells was characterized. In situ isotope enrichment coupled with GC–MS was used to elucidate the primary pathway(s) of 1-[13C]-glucose metabolism in the Nostoc–Gunnera symbiosis. • The characteristics of 14C-OMG uptake by symbiotic clusters suggested a respiratory driven process mediated by a hexose transporter. However, uptake by various Nostoc isolates decreased with increasing heterocyst frequency and was specifically associated with vegetative cells. In isolated and symbiotically intact Nostoc cells, 1-[13C]-glucose was imported and converted to various intermediates of the incomplete citric acid cycle, glycolysis and N2-assimilating pathways. Labelling profiles indicated that C metabolism was altered in infected, but not in uninfected, rhizome tissue. • Although it has been proposed that cyanobacteria such as Nostoc metabolise glucose using enzymes of the oxidative pentose phosphate cycle, our results suggest that glucose is also metabolised via glycolysis as well as the incomplete citric acid cycle in symbiotic cells.
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The Gunnera— Nostoc Symbiosis
Biology & Environment: Proceedings of the Royal Irish Academy, 2002Co-Authors: Birgitta Bergman, Bruce OsborneAbstract:Among angiosperms, a restricted number of plants are capable of forming symbioses with nitrogen fixing organisms. The best-studied examples of symbiosis are those between legumninous plants and nitrogen-fixing rhizobia. Although cyanobacteria are the most potent nitrogen-fixing microsymbionts in terms of variations in the taxonomy of the hosts, ranging from fungi to higher plants, extant cyanobacterial symbioses encompass only one an giosperm family. This monogeneric family, the Gunneraceae, has an unclear taxonomic affiliation. It comprises about 50 species, which show great variation in size. The larger, rhubarb-like, stand forming species (up to 6m high) are typical of areas ranging from Hawaii to Central America and South America, whereas smaHer, more slender species are found in New Zealand, South-East Asia and the southernmost parts of South America. The eleven endemic species of New Zealand are all small, often < 10cm high, and form stolons, whereas the larger species are rhizomatous. The natural distribution of Gunnera is restricted to the southern hemisphere, but naturalised Gunnera (G. tinctoria) is now known from some European sites, for instance the west coast of Ireland, south-western England, northern France and the Azores. A characteristic of all Gunnera species is their preference for wet and humid areas. Ever since cyanobacteria were discovered in side cells of Gunnera at the end of the nineteenth century, they have been classified as belonging to the genus Nostoc. This is a widespread and globally common filamentous genus capable of advanced cell differentiation. Under nitrogen limitation, het erocysts (sites for the nitrogen-fixing enzyme intro genase) are formed, constituting 5-10% of the total cell population, whereas other adverse conditions may give rise to motile hormogonia or resting spores (akinetes). The differentiation of hormogo nia (the de facto infection units in symbioses) and heterocysts is crucial to the formation of the Gunnera symbioses. Although possibly restricted to the genus Nostoc, several species and strains are capable of forming symbioses with Gunnera, including those compatible with plants such as liverworts and cycads. These aspects of cyano bacterial specificity in symbioses are fairther discussed by Rasmussen and Johansson (this volume).