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  • 1. Batista-Santos, Paula
    et al.
    Duro, Nuno
    Rodrigues, Ana P.
    Semedo, Jose N.
    Alves, Paula
    da Costa, Mario
    Graca, Ines
    Pais, Isabel P.
    Scotti-Campos, Paula
    Lidon, Fernando C.
    Leitao, Antonio E.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ribeiro-Barros, Ana I.
    Ramalho, Jose C.
    Is salt stress tolerance in Casuarina glauca Sieb. ex Spreng. associated with its nitrogen-fixing root-nodule symbiosis? An analysis at the photosynthetic level2015In: Plant physiology and biochemistry (Paris), ISSN 0981-9428, E-ISSN 1873-2690, Vol. 96, p. 97-109Article in journal (Refereed)
    Abstract [en]

    Casuarina glauca is an actinorhizal tree which establishes root-nodule symbiosis with N-2-fixing Frankia bacteria. This plant is commonly found in saline zones and is widely used to remediate marginal soils and prevent desertification. The nature of its ability to survive in extreme environments and the extent of Frankia contribution to stress tolerance remain unknown. Thus, we evaluated the ability of C. glauca to cope with salt stress and the influence of the symbiosis on this trait. To this end, we analysed the impact of salt on plant growth, mineral contents, water relations, photosynthetic-related parameters and nonstructural sugars in nodulated vs. non-nodulated plants. Although the effects on photosynthesis and stomatal conductance started to become measurable in the presence of 200 mM NaCl, photochemical (e.g., photosynthetic electron flow) and biochemical (e.g., activity of photosynthetic enzymes) parameters were only strongly impaired when NaCl levels reached 600 mM. These results indicate the maintenance of high tissue hydration under salt stress, probably associated with enhanced osmotic potential. Furthermore, the maintenance of photosynthetic assimilation potential (A(max)), together with the increase in the quantum yield of down-regulated energy dissipation of PSII (Y-NPQ), suggested a down-regulation of photosynthesis instead of photo-damaging effects. A comparison of the impact of increasing NaCl levels on the activities of photosynthetic (RubisCO and ribulose-5 phosphate kinase) and respiratory (pyruvate kinase and NADH-dependent malate dehydrogenase) enzymes vs. photosynthetic electron flow and fluorescence parameters, revealed that biochemical impairments are more limiting than photochemical damage. Altogether, these results indicate that, under controlled conditions, C glauca tolerates high NaCl levels and that this capacity is linked to photosynthetic adjustments.

  • 2. Berry, Alison M.
    et al.
    Mendoza-Herrera, Alberto
    Guo, Ying-Yi
    Hayashi, Jennifer
    Persson, Tomas
    Stockholm University, Faculty of Science, Department of Botany.
    Barabote, Ravi
    Demchenko, Kirill
    Zhang, Shuxiao
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    New perspectives on nodule nitrogen assimilation in actinorhizal symbioses2011In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 38, no 8-9, p. 645-652Article, review/survey (Refereed)
    Abstract [en]

    Nitrogen-fixing root nodules are plant organs specialised for symbiotic transfer of nitrogen and carbon between microsymbiont and host. The organisation of nitrogen assimilation, storage and transport processes is partitioned at the subcellular and tissue levels, in distinctive patterns depending on the symbiotic partners. In this review, recent advances in understanding of actinorhizal nodule nitrogen assimilation are presented. New findings indicate that Frankia within nodules of Datisca glomerata (Presl.) Baill. carries out both primary nitrogen assimilation and biosynthesis of arginine, rather than exporting ammonium. Arginine is a typical storage form of nitrogen in plant tissues, but is a novel nitrogen carrier molecule in root nodule symbioses. Thus Frankia within D. glomerata nodules exhibits considerable metabolic independence. Furthermore, nitrogen reassimilation is likely to take place in the host in the uninfected nodule cortical cells of this root nodule symbiosis, before amino acid export to host sink tissues via the xylem. The role of an augmented pericycle in carbon and nitrogen exchange in root nodules deserves further attention in actinorhizal symbiosis, and further highlights the importance of a comprehensive, structure-function approach to understanding function in root nodules. Moreover, the multiple patterns of compartmentalisation in relation to nitrogen flux within root nodules demonstrate the diversity of possible functional interactions between host and microsymbiont that have evolved in the nitrogen-fixing clade.

  • 3. Carro, Lorena
    et al.
    Persson, Tomas
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pujic, Petar
    Alloisio, Nicole
    Fournier, Pascale
    Boubakri, Hasna
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Normand, Philippe
    Organic acids metabolism in Frankia alni2016In: Symbiosis, ISSN 0334-5114, E-ISSN 1878-7665, Vol. 70, no 1, p. 37-48Article in journal (Refereed)
    Abstract [en]

    Trophic exchanges constitute the bases of the symbiosis between the nitrogen-fixing actinomycete Frankia and its host plant Alnus, but the identity of the compounds exchanged is still poorly known. In the current work, previously published transcriptomic studies of Alnus nodules and of symbiotic Frankia were reexamined for TCA cycle related genes. The bacterial TCA enzyme genes were all upregulated, especially the succinyl-CoA synthase and the citrate synthase while on the plant side, none was significantly modified in nodules relative to non-inoculated roots. A preliminary metabolomics approach permitted to see that citrate, 2-oxoglutarate, succinate, malate and fumarate were all more abundant (FC (Fold change) = 5-70) in mature nitrogen-fixing nodules than in roots. In the evaluation of the uptake and metabolism of these organic acids, a significant change was observed in the morphology of nitrogen fixing vesicles in vitro: the dicarboxylates malate, succinate and fumarate induced the formation of larger vesicles than was the case with propionate. Moreover, the production of spores was also modified depending on the organic acid present. The assays showed that most C4 dicarboxylates were taken up while C6 tricarboxylates were not and citrate even partially blocked catabolism of reserve carbon. Tests were performed to determine if the change in membrane permeability induced by Ag5, a peptide previously shown to modify the membranes of Frankia, increased the uptake of specific organic acids. No effect was observed with citrate while an increase in nitrogen fixation was seen with propionate.

  • 4. Demchenko, K.
    et al.
    Zdyb, Anna
    Stockholm University, Faculty of Science, Department of Botany.
    Feussner, I.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Analysis of the subcellular localisation of lipoxygenase in legume and actinorhizal nodules2012In: Plant Biology, ISSN 1435-8603, E-ISSN 1438-8677, Vol. 14, no 1, p. 56-63Article in journal (Refereed)
    Abstract [en]

    Plant lipoxygenases (LOXs; EC 1.13.11.12) catalyse the oxygenation of polyunsaturated fatty acids, linoleic (18:2) and a-linolenic acid (18:3(n-3)) and are involved in processes such as stress responses and development. Depending on the regio-specificity of a LOX, the incorporation of molecular oxygen leads to formation of 9- or 13-fatty acid hydroperoxides, which are used by LOX itself as well as by members of at least six different enzyme families to form a series of biologically active molecules, collectively called oxylipins. The best characterised oxylipins are the jasmonates: jasmonic acid (JA) and its isoleucine conjugate that are signalling compounds in vegetative and propagative plant development. In several types of nitrogen-fixing root nodules, LOX expression and/or activity is induced during nodule development. Allene oxide cyclase (AOC), a committed enzyme of the JA biosynthetic pathway, has been shown to localise to plastids of nodules of one legume and two actinorhizal plants, Medicago truncatula, Datisca glomerata and Casuarina glauca, respectively. Using an antibody that recognises several types of LOX interspecifically, LOX protein levels were compared in roots and nodules of these plants, showing no significant differences and no obvious nodule-specific isoforms. A comparison of the cell-specific localisation of LOXs and AOC led to the conclusion that (i) only cytosolic LOXs were detected although it is generally assumed that the (13S)-hydroperoxy a-linolenic acid for JA biosynthesis is produced in the plastids, and (ii) in cells of the nodule vascular tissue that contain AOC, no LOX protein could be detected.

  • 5. Demchenko, Kirill N.
    et al.
    Voitsekhovskaja, Olga V.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Plasmodesmata without callose and calreticulin in higher plants - open channels for fast syrnplastic transport?2014In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 5Article in journal (Refereed)
    Abstract [en]

    Plasmodesmata (PD) represent membrane-lined channels that link adjacent plant cells across the cell wall. PD of higher plants contain a central tube of endoplasmic reticulum (ER) called desmotubule. Membrane and lumen proteins seem to be able to move through the desmotubule, but most transport processes through PD occur through the cytoplasmic annulus (Brunkard (Bale 2013). Calreticulin (CRT), a highly conserved Ca2+-binding protein found in all multicellular eukaryotes, predominantly located in the ER, was shown to localize to PD, though not all PD accumulate CRT. In nitrogen-fixing actinorhizal root nodules of the Australian tree Casuarina glauca, the primary walls of infected cells containing the microsymbiont become lignified upon infection. TEM analysis of these nodules showed that during the differentiation of infected cells, PD connecting infected cells, and connecting infected and adjacent uninfected cells, were reduced in number as well as diameter (Schubert eta, 2013). In contrast with PD connecting young infected cells, and most PD connecting mature infected and adjacent uninfected cells, PD connecting mature infected cells did not accumulate CRT. Furthermore, as shown here, these PD were not associated with callose, and based on their diameter, they probably had lost their desmotubules. We speculate that either this is a slow path to PD degradation, or that the loss of callose accumulation and presumably also desmotubules leads to the PD becoming open channels and improves metabolite exchange between cells.

  • 6.
    Demina, Irina V.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ng, Liang J. P.
    Division of Plant Science, Research School of Biology, Australian National University, Linnaeus Way, ACT 0200 Canberra, Australia.
    van der Graaff, Eric
    Department of Plant Physiology, Karl-Franzens-Universität Graz, 8010 Graz, Austria.
    Roitsch, Thomas
    Department of Plant Physiology, Karl-Franzens-Universität Graz, 8010 Graz, Austria.
    Mathesius, Ulrike
    Division of Plant Science, Research School of Biology, Australian National University, Linnaeus Way, ACT 0200 Canberra, Australia.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Auxins and cytokinins in roots, hairy roots and nodules of the actinorhizal plant Datisca glomerata and the model legume Medicago truncatulaManuscript (preprint) (Other academic)
  • 7.
    Demina, Irina V.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Cysteine-rich peptide genes are expressed in the infected nodule cells of the actinorhizal plant Datisca glomerataManuscript (preprint) (Other academic)
  • 8.
    Demina, Irina V.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Persson, Tomas
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Santos, Patricia
    Plaszczyca, Marian
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Comparison of the Nodule vs. Root Transcriptome of the Actinorhizal Plant Datisca glomerata: Actinorhizal Nodules Contain a Specific Class of Defensins2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 8, p. e72442-Article in journal (Refereed)
    Abstract [en]

    Actinorhizal root nodule symbioses are very diverse, and the symbiosis of Datisca glomerata has previously been shown to have many unusual aspects. In order to gain molecular information on the infection mechanism, nodule development and nodule metabolism, we compared the transcriptomes of D. glomerata roots and nodules. Root and nodule libraries representing the 3'-ends of cDNAs were subjected to high-throughput parallel 454 sequencing. To identify the corresponding genes and to improve the assembly, Illumina sequencing of the nodule transcriptome was performed as well. The evaluation revealed 406 differentially regulated genes, 295 of which (72.7%) could be assigned a function based on homology. Analysis of the nodule transcriptome showed that genes encoding components of the common symbiosis signaling pathway were present in nodules of D. glomerata, which in combination with the previously established function of SymRK in D. glomerata nodulation suggests that this pathway is also active in actinorhizal Cucurbitales. Furthermore, comparison of the D. glomerata nodule transcriptome with nodule transcriptomes from actinorhizal Fagales revealed a new subgroup of nodule-specific defensins that might play a role specific to actinorhizal symbioses. The D. glomerata members of this defensin subgroup contain an acidic C-terminal domain that was never found in plant defensins before.

  • 9. Duro, Nuno
    et al.
    Batista-Santos, Paula
    da Costa, Mario
    Maia, Rodrigo
    Castro, Isabel V.
    Ramos, Margarida
    Ramalho, Jose C.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Maguas, Cristina
    Ribeiro-Barros, Ana
    The impact of salinity on the symbiosis between Casuarina glauca Sieb. ex Spreng. and N-2-fixing Frankia bacteria based on the analysis of Nitrogen and Carbon metabolism2016In: Plant and Soil, ISSN 0032-079X, E-ISSN 1573-5036, Vol. 398, no 1-2, p. 327-337Article in journal (Refereed)
    Abstract [en]

    Casuarina glauca is an actinorhizal plant that establishes root-nodule symbiosis with N-2-fixing bacteria of the genus Frankia. This plant is highly recalcitrant to extreme environmental conditions such as salinity and drought. The aim of this study was to evaluate the impact of salt stress on the symbiotic relationship between C. glauca and Frankia Thr, focusing on N and C metabolism. Symbiotic and non-symbiotic plants were exposed to 0, 200, 400 and 600 mM NaCl. The following analyses were performed: stable carbon (delta C-13) and nitrogen (delta N-15) isotope signature; nitrogenase activity in nodules (acetylene reduction assay); and gene expression of a set of genes involved in nodule infection and N/C metabolism (qRT-PCR). Data were analysed using two-way ANOVA. Salt stress induced an enrichment in delta C-13 and delta N-15, reflecting a negative impact of salt in the relative water content and N-2 fixation, respectively. Furthermore, nitrogenase activity in nodules was insignificant already at 200 mM NaCl, consistent with the expression patterns of nifH as well as of plant genes involved in nodule induction and metabolism. The ability of C. glauca to thrive under highly saline environments is not dependent on the symbiosis with Frankia.

  • 10. Evkaikina, Anastasiia I.
    et al.
    Berke, Lidija
    Romanova, Marina A.
    Proux-Wéra, Estelle
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Stockholm University, Science for Life Laboratory (SciLifeLab). Swedish University of Agricultural Sciences, Sweden.
    Ivanova, Alexandra N.
    Rydin, Catarina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Voitsekhovskaja, Olga V.
    The Huperzia selago Shoot Tip Transcriptome Sheds New Light on the Evolution of Leaves2017In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 9, p. 2444-2460Article in journal (Refereed)
    Abstract [en]

    Lycopodiophyta-consisting of three orders, Lycopodiales, Isoetales and Selaginellales, with different types of shoot apical meristems (SAMs)-form the earliest branch among the extant vascular plants. They represent a sister group to all other vascular plants, from which they differ in that their leaves are microphylls-that is, leaves with a single, unbranched vein, emerging from the protostele without a leaf gap-not megaphylls. All leaves represent determinate organs originating on the flanks of indeterminate SAMs. Thus, leaf formation requires the suppression of indeterminacy, that is, of KNOX transcription factors. In seed plants, this is mediated by different groups of transcription factors including ARP and YABBY. We generated a shoot tip transcriptome of Huperzia selago (Lycopodiales) to examine the genes involved in leaf formation. Our H. selago transcriptome does not contain any ARP homolog, although transcriptomes of Selaginella spp. do. Surprisingly, we discovered a YABBY homolog, although these transcription factors were assumed to have evolved only in seed plants. The existence of a YABBY homolog in H. selago suggests that YABBY evolved already in the common ancestor of the vascular plants, and subsequently was lost in some lineages like Selaginellales, whereas ARP may have been lost in Lycopodiales. The presence of YABBY in the common ancestor of vascular plants would also support the hypothesis that this common ancestor had a simplex SAM. Furthermore, a comparison of the expression patterns of ARP in shoot tips of Selaginella kraussiana (Harrison CJ, et al. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434(7032): 509-514.) and YABBY in shoot tips of H. selago implies that the development of microphylls, unlike megaphylls, does not seem to depend on the combined activities of ARP and YABBY. Altogether, our data show that Lycopodiophyta are a diverse group; so, in order to understand the role of Lycopodiophyta in evolution, representatives of Lycopodiales, Selaginellales, as well as of Isoetales, have to be examined.

  • 11. Fortunato, Ana
    et al.
    Santos, Patricia
    Graca, Ines
    Gouveiva, Maria Manuela
    Martins, Sandra Marina
    Pinto Ricardo, Candido Pereira
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany. Växtfysiologi.
    Ribeiro, Ana Isabel
    Isolation and characterization of cgchi3, a nodule-specific gene from Casuarina glauca encoding a class III chitinase2007In: Physiologia Plantarum, ISSN 0031-9317, Vol. 130, no 3, p. 418-426Article in journal (Refereed)
    Abstract [en]

    Chitinases (EC 3.2.1.14) catalyse the hydrolysis of chitin, a homopolymer of beta-1,4-linked N-acetyl-D-glucosamine residues. Plant chitinases are involved in a wide variety of processes; in particular, their expression has been found to be enhanced in symbiotic and pathogenic plant-microbe interactions. During this work we have cloned and characterized a gene encoding a class III chitinase from actinorhizal nodules of Casuarina glauca (cgchi3). CGCHI3 was found to be encoded by a single gene that was specifically activated in nodules as compared with uninoculated control roots and leaves. The expression of this gene was further enhanced in nodules after salicylic acid treatment and completely repressed after wounding. In situ hybridisation analysis revealed that cgchi3 is an early nodulin gene, being expressed in the meristem and in the uninfected cortical cells of young nodules. Based on the obtained results we suggest that this gene is involved in nodule development. This is the first report on a class III chitinase coding gene that is specifically activated during actinorhizal symbiosis.

  • 12. Griesmann, Maximilian
    et al.
    Chang, Yue
    Liu, Xin
    Song, Yue
    Haberer, Georg
    Crook, Matthew B.
    Billault-Penneteau, Benjamin
    Lauressergues, Dominique
    Keller, Jean
    Imanishi, Leandro
    Roswanjaya, Yuda Purwana
    Kohlen, Wouter
    Pujic, Petar
    Battenberg, Kai
    Alloisio, Nicole
    Liang, Yuhu
    Hilhorst, Henk
    Salgado, Marco G.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Hocher, Valerie
    Gherbi, Hassen
    Svistoonoff, Sergio
    Doyle, Jeff J.
    He, Shixu
    Xu, Yan
    Xu, Shanyun
    Qu, Jing
    Gao, Qiang
    Fang, Xiaodong
    Fu, Yuan
    Normand, Philippe
    Berry, Alison M.
    Wall, Luis G.
    Ane, Jean-Michel
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Xu, Xun
    Yang, Huanming
    Spannagl, Manuel
    Mayer, Klaus F. X.
    Wong, Gane Ka-Shu
    Parniske, Martin
    Delaux, Pierre-Marc
    Cheng, Shifeng
    Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis2018In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 361, no 6398, article id 1743Article in journal (Refereed)
  • 13. Ilina, Elena L.
    et al.
    Logachov, Anton A.
    Laplaze, Laurent
    Demchenko, Nikolay P.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Demchenko, Kirill N.
    Composite Cucurbita pepo plants with transgenic roots as a tool to study root development2012In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 110, no 2, p. 479-489Article in journal (Refereed)
    Abstract [en]

    In most plant species, initiation of lateral root primordia occurs above the elongation zone. However, in cucurbits and some other species, lateral root primordia initiation and development takes place in the apical meristem of the parental root. Composite transgenic plants obtained by Agrobacterium rhizogenes-mediated transformation are known as a suitable model to study root development. The aim of the present study was to establish this transformation technique for squash. The auxin-responsive promoter DR5 was cloned into the binary vectors pKGW-RR-MGW and pMDC162-GFP. Incorporation of 5-ethynyl-2-deoxyuridine (EdU) was used to evaluate the presence of DNA-synthesizing cells in the hypocotyl of squash seedlings to find out whether they were suitable for infection. Two A. rhizogenes strains, R1000 and MSU440, were used. Roots containing the respective constructs were selected based on DsRED1 or green fluorescent protein (GFP) fluorescence, and DR5::Egfp-gusA or DR5::gusA insertion, respectively, was verified by PCR. Distribution of the response to auxin was visualized by GFP fluorescence or -glucuronidase (GUS) activity staining and confirmed by immunolocalization of GFP and GUS proteins, respectively. Based on the distribution of EdU-labelled cells, it was determined that 6-day-old squash seedlings were suited for inoculation by A. rhizogenes since their root pericycle and the adjacent layers contain enough proliferating cells. Agrobacterium rhizogenes R1000 proved to be the most virulent strain on squash seedlings. Squash roots containing the respective constructs did not exhibit the hairy root phenotype and were morphologically and structurally similar to wild-type roots. The auxin response pattern in the root apex of squash resembled that in arabidopsis roots. Composite squash plants obtained by A. rhizogenes-mediated transformation are a good tool for the investigation of root apical meristem development and root branching.

  • 14. Normand, Philippe
    et al.
    Nguyen, Thanh Van
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Battenberg, Kai
    Berry, Alison M.
    Vanden Heuvel, Brian
    Fernandez, Maria P.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Proposal of 'Candidatus Frankia californiensis', the uncultured symbiont in nitrogen-fixing root nodules of a phylogenetically broad group of hosts endemic to western North America2017In: International Journal of Systematic and Evolutionary Microbiology, ISSN 1466-5026, E-ISSN 1466-5034, Vol. 67, no 10, p. 3706-3715Article in journal (Refereed)
    Abstract [en]

    The genus Frankia comprises a group of nitrogen-fixing actinobacteria that form root-nodule symbioses with perennial dicotyledonous plants in the nitrogen-fixing clade. These bacteria have been characterized phylogenetically and grouped into four clusters (clusters 1-4). Cluster 2 contains mostly uncultured strains that induce nodules on species of the genera Datisca (Datiscaceae), Coriaria (Coriariaceae), Ceanothus (Rhamnaceae) and several genera in the family Rosaceae (Cercocarpus, Chamaebatia, Dryas, Purshia), all of which except members of the genus Coriaria are present within the California Floristic Province (CFP) or neighbouring areas of western North America. Those strains occurring in western North America are genetically very closely related to one another, and genetically distinct from strains characterized from other locales. We hereby propose to create a 'Candidatus Frankia californiensis' species for those cluster 2 strains of the genus Frankia with both high genetic similarity and a geographical distribution in or near the CFP.

  • 15.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Actinorhizal symbioses2011In: Ecological Aspects of Nitrogen Metabolism in Plants / [ed] Polacco JC, Todd CD, Hoboken: Wiley-Blackwell, 2011, p. 117-137Chapter in book (Other academic)
  • 16.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Nodules and oxygen2008In: Plant Biotechnology, ISSN 1342-4580, Vol. 25, no 3, p. 299-307Article, review/survey (Other (popular science, discussion, etc.))
    Abstract [en]

    In root nodule symbioses, bacterial microsymbionts are hosted inside plant cells and supply the host plant with

    the products of biological nitrogen fixation, rendering it independent of soil nitrogen sources. Two types of such interactions

    are known, legume/rhizobia symbioses involving several alpha- and beta-proteobacterial genera, collectively called rhizobia,

    and members of the Leguminosae (Fabaceae) family, and actinorhizal symbioses involving members of the Gram-positive

    actinomycetous genus Frankia and a diverse group of plants from 25 genera from eight different families, collectively called

    actinorhizal plants, with one exception trees or woody shrubs.

  • 17.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Bogusz, Didier
    Ribeiro, Ana
    Berry, Alison M.
    Progress on research on actinorhizal plants2011In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 38, no 8-9, p. 633-638Article, review/survey (Refereed)
    Abstract [en]

    In recent years, our understanding of the plant side of actinorhizal symbioses has evolved rapidly. No homologues of the common nod genes from rhizobia were found in the three Frankia genomes published so far, which suggested that Nod factor-like molecules would not be used in the infection of actinorhizal plants by Frankia. However, work on chimeric transgenic plants indicated that Frankia Nod factor equivalents signal via the same transduction pathway as rhizobial Nod factors. The role of auxin in actinorhizal nodule formation differs from that in legume nodulation. Great progress has been made in the analysis of pathogenesis-related and stress-related gene expression in nodules. Research on nodule physiology has shown the structural and metabolic diversity of actinorhizal nodules from different phylogenetic branches. The onset of large-scale nodule transcriptome analysis in different actinorhizal systems will provide access to more information on the symbiosis and its evolution.

  • 18.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Demchenko, Kirill N.
    The diversity of actinorhizal symbiosis2012In: Protoplasma, ISSN 0033-183X, E-ISSN 1615-6102, Vol. 249, no 4, p. 967-979Article, review/survey (Refereed)
    Abstract [en]

    Filamentous aerobic soil actinobacteria of the genus Frankia can induce the formation of nitrogen-fixing nodules on the roots of a diverse group of plants from eight dicotyledonous families, collectively called actinorhizal plants. Within nodules, Frankia can fix nitrogen while being hosted inside plant cells. Like in legume/rhizobia symbioses, bacteria can enter the plant root either intracellularly through an infection thread formed in a curled root hair, or intercellularly without root hair involvement, and the entry mechanism is determined by the host plant species. Nodule primordium formation is induced in the root pericycle as for lateral root primordia. Mature actinorhizal nodules are coralloid structures consisting of multiple lobes, each of which represents a modified lateral root without a root cap, a superficial periderm and with infected cells in the expanded cortex. In this review, an overview of nodule induction mechanisms and nodule structure is presented including comparisons with the corresponding mechanisms in legume symbioses.

  • 19.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Jacobsen, Karin
    Alloisio, Nicole
    Ford Denison, R Ford
    Klein, M
    Tjepkema, John D
    Winzer, Thilo
    Sirrenberg, A
    Guan, Changhui
    Berry, Alison M
    Truncated Hemoglobins in Actinorhizal Nodules of Datisca glomerata.2007In: Plant Biol (Stuttg), ISSN 1435-8603, Vol. 9, no 6, p. 776-785Article in journal (Other academic)
    Abstract [en]

    Three types of hemoglobins exist in higher plants, symbiotic, non-symbiotic, and truncated hemoglobins. Symbiotic (class II) hemoglobins play a role in oxygen supply to intracellular nitrogen-fixing symbionts in legume root nodules, and in one case (Parasponia sp.), a non-symbiotic (class I) hemoglobin has been recruited for this function. Here we report the induction of a host gene, Dgtrhb1, encoding a truncated hemoglobin in Frankia-induced nodules of the actinorhizal plant Datisca glomerata Induction takes place specifically in cells infected by the microsymbiont, prior to the onset of bacterial nitrogen fixation. A bacterial gene (Frankia trHbO) encoding a truncated hemoglobin with O (2)-binding kinetics suitable for the facilitation of O (2) diffusion ( ) is also expressed in symbiosis. Nodule oximetry confirms the presence of a molecule that binds oxygen reversibly in D. glomerata nodules, but indicates a low overall hemoglobin concentration suggesting a local function. Frankia TrHbO is likely to be responsible for this activity. The function of the D. glomerata truncated hemoglobin is unknown; a possible role in nitric oxide detoxification is suggested.

  • 20.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Newton, William E.
    Nitrogen-fixing Actinorhizal Symbioses2008Book (Other academic)
  • 21.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Sprent, Janet I.
    Comparison between actinorhizal and legume symbioses2008In: Nitrogen-fixing Actinorhizal Symbioses, Springer, Dordrecht , 2008, p. 261-288Chapter in book (Other academic)
  • 22.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Steinbüchel, Alexander
    Prokaryotic symbionts in plants2009Collection (editor) (Other academic)
  • 23.
    Pawlowski, Katharina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Zdyb, Anna
    Stockholm University, Faculty of Science, Department of Botany.
    Demchenko, Kirill
    Hause, Bettina
    Heumann, Jan
    Feussner, Ivo
    Grzeganek, Peter
    Göbel, Cornelia
    Mrosk, Cornelia
    Jasmonate biosynthesis in legume and actinorhizal nodules2011In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 189, no 2, p. 568-579Article in journal (Refereed)
    Abstract [en]

    • Jasmonic acid (JA) is a plant signalling compound that has been implicated in theregulation of mutualistic symbioses. In order to understand the spatial distributionof JA biosynthetic capacity in nodules of two actinorhizal species, Casaurina glauca and Datisca glomerata, and one legume, Medicago truncatula, we determined thelocalization of allene oxide cyclase (AOC) which catalyses a committed step inJA biosynthesis. In all nodule types analysed, AOC was detected exclusively inuninfected cells.

    • The levels of JA were compared in the roots and nodules of the three plantspecies. The nodules and noninoculated roots of the two actinorhizal species, andthe root systems of M. truncatula, noninoculated or nodulated with wild-type Sinorhizobium meliloti or with mutants unable to fix nitrogen, did not showsignificant differences in JA levels. However, JA levels in all plant organs examined increased significantly on mechanical disturbance.

    • To study whether JA played a regulatory role in the nodules of M. truncatula, composite plants containing roots expressing an MtAOC1-sense or MtAOC1-RNAi construct were inoculated with S. meliloti. Neither an increase nor reductionin AOC levels resulted in altered nodule formation.

    • These data suggest that jasmonates are not involved in the development andfunction of root nodules.

  • 24.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Battenberg, Kai
    Demina, Irina V.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Vigil-Stenman, Theoden
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Heuvel, Brian Vanden
    Pujic, Petar
    Facciotti, Marc T.
    Wilbanks, Elizabeth G.
    O'Brien, Anna
    Fournier, Pascale
    Hernandez, Maria Antonia Cruz
    Herrera, Alberto Mendoza
    Medigue, Claudine
    Normand, Philippe
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Berry, Alison M.
    Candidatus Frankia Datiscae Dg1, the Actinobacterial Microsymbiont of Datisca glomerata, Expresses the Canonical nod Genes nodABC in Symbiosis with Its Host Plant2015In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 5, article id e0127630Article in journal (Refereed)
    Abstract [en]

    Frankia strains are nitrogen-fixing soil actinobacteria that can form root symbioses with actinorhizal plants. Phylogenetically, symbiotic frankiae can be divided into three clusters, and this division also corresponds to host specificity groups. The strains of cluster II which form symbioses with actinorhizal Rosales and Cucurbitales, thus displaying a broad host range, show suprisingly low genetic diversity and to date can not be cultured. The genome of the first representative of this cluster, Candidatus Frankia datiscae Dg1 (Dg1), a microsymbiont of Datisca glomerata, was recently sequenced. A phylogenetic analysis of 50 different housekeeping genes of Dg1 and three published Frankia genomes showed that cluster II is basal among the symbiotic Frankia clusters. Detailed analysis showed that nodules of Datisca glomerata, independent of the origin of the inoculum, contain several closely related cluster II Frankia operational taxonomic units. Actinorhizal plants and legumes both belong to the nitrogen-fixing plant clade, and bacterial signaling in both groups involves the common symbiotic pathway also used by arbuscular mycorrhizal fungi. However, so far, no molecules resembling rhizobial Nod factors could be isolated from Frankia cultures. Alone among Frankia genomes available to date, the genome of Dg1 contains the canonical nod genes nodA, nodB and nodC known from rhizobia, and these genes are arranged in two operons which are expressed in Datisca glomerata nodules. Furthermore, Frankia Dg1 nodC was able to partially complement a Rhizobium leguminosarum A34 nodC::Tn5 mutant. Phylogenetic analysis showed that Dg1 Nod proteins are positioned at the root of both alpha- and beta-rhizobial NodABC proteins. NodA-like acyl transferases were found across the phylum Actinobacteria, but among Proteobacteria only in nodulators. Taken together, our evidence indicates an Actinobacterial origin of rhizobial Nod factors.

  • 25.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Benson, David R.
    Normand, Philippe
    Vanden Heuvel, Brian
    Pujic, Petar
    Chertkov, Olga
    Teshima, Hazuki
    Bruce, David C.
    Detter, Chris
    Tapia, Roxanne
    Han, Shunsheng
    Han, James
    Woyke, Tanja
    Pitluck, Sam
    Pennacchio, Len
    Nolan, Matt
    Ivanova, Natalia
    Pati, Amrita
    Land, Miriam L.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Berry, Alison M.
    Genome Sequence of "Candidatus Frankia datiscae" Dg1, the Uncultured Microsymbiont from Nitrogen-Fixing Root Nodules of the Dicot Datisca glomerata2011In: Journal of Bacteriology, ISSN 0021-9193, E-ISSN 1098-5530, Vol. 193, no 24, p. 7017-7018Article in journal (Refereed)
    Abstract [en]

    Members of the noncultured clade of Frankia enter into root nodule symbioses with actinorhizal species from the orders Cucurbitales and Rosales. We report the genome sequence of a member of this clade originally from Pakistan but obtained from root nodules of the American plant Datisca glomerata without isolation in culture.

  • 26.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Demina, Irina V.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Vanden Heuvel, Brian
    Department of Biology, Colorado State University, Pueblo 16, CO 81001, USA.
    Pujic, Petar
    Université Lyon 1, Université de Lyon, CNRS, Ecologie Microbienne UMR5557, Cedex 69622 Villeurbanne, France.
    Fournier, Pascale
    Université Lyon 1, Université de Lyon, CNRS, Ecologie Microbienne UMR5557, Cedex 69622 Villeurbanne, France.
    Normand, Philippe
    Université Lyon 1, Université de Lyon, CNRS, Ecologie Microbienne UMR5557, Cedex 69622 Villeurbanne, France.
    Médigue, Claudine
    Génoscope, Evry, France.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Berry, Alison M.
    Department of Plant Sciences, University of California, Davis, CA 95616, USA.
    Candidatus Frankia datiscae Dg1, the actinobacterial symbiont of Datisca glomerata, is a member of the basal clade of symbiotic frankiae and expresses the common nod genesManuscript (preprint) (Other academic)
  • 27.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Nguyen, Thanh Van
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Alloisio, Nicole
    Pujic, Petar
    Berry, Alison M.
    Normand, Philippe
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D-glomerata change N-transport forms when nodulated?2016In: Symbiosis, ISSN 0334-5114, E-ISSN 1878-7665, Vol. 70, no 1, p. 149-157Article in journal (Refereed)
    Abstract [en]

    To gain more insight in nitrogen metabolism in actinorhizal nodules, a comparison between the N metabolite profiles in roots vs. nodules was initiated for one host plant from the best-examined order of actinorhizal plants, Fagales, A. glutinosa (Betulaceae), a temperate tree, and one host plant from the Cucurbitales order, Datisca glomerata (Datiscaceae). For both symbioses, the symbiotic transcriptomes have been published and can be used to assess the expression of genes representing specific metabolic pathways in nodules. The amino acid profiles of roots in this study suggest that A. glutinosa transported aspartate, glutamate and citrulline in the xylem, a combination of nitrogenous solutes not published previously for this species. The amino acid profiles of D. glomerata roots depended on whether the plants were nodulated or grown on nitrate; roots of nodulated plants contained increased amounts of arginine. Although bacterial transcriptome data showed no symbiotic auxotrophy for branched chain amino acids (leucine, isoleucine, valine) in either symbiosis, D. glomerata nodules contained comparatively high levels of these amino acids. This might represent a response to osmotic stress.

  • 28.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Vanden Heuvel, B.
    Pujic, P.
    Normand, P.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Berry, A.
    Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, uses Nod factors for the infection of its host plantManuscript (preprint) (Other academic)
  • 29.
    Persson, Tomas
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Wilbanks, E.F.
    Alloisio, N.
    Guo, Y.
    Barabote, R.
    Pujic, P.
    Facciotti, M.
    Mendoza-Herrera, A.
    Normand, P.
    Berry, A.M.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Amino acid metabolism in roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: γ-aminobutyric acid and β-alanine are important metabolitesManuscript (preprint) (Other academic)
    Abstract [en]

    Roots and nodules of the actinorhizal plants Alnus glutinosa and Datisca glomerata, as well as Frankia alni ACN14a grown in minimal and ammonium supplemented media, were analyzed for amino acid profiles. To analyze nitrogen and carbon metabolism, the transcriptome in nodules of the microsymbiont of D. glomerata, Frankia datiscae Dg1, was sequenced and compared with transcriptome data from symbiotic F. alni ACN14a (Alloisio et al. 2011). The amino acid profile of A. glutinosa roots suggests that Citrulline, Asparagine and Glutamine are transported in the xylem. Moreover, the comparatively high concentration of γ-aminobutyric acid in A. glutinosa roots suggest that this compound has a function in plant nitrogen metabolism. γ-aminobutyric acid could, as was suggested for the legume symbiosis, act as a signal factor for the plant nitrogen status to symbiotic Frankia. It could also be imported by the bacteria as a carbon and nitrogen source. Moreover, the expression of the gene for the enzyme catalyzing β-Alanine synthesis was elevated in both Frankia strains in symbiosis. Elevated concentrations of β-Alanine in nodules of D. glomerata and A. glutinosa compared to roots suggest that β-Alanine is produced by the bacteria in large amounts, possibly as a storage compound for Coenzyme A production.

  • 30.
    Plaszczyca, Malgorzata
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Manns, Isabel
    Albrecht von Haller Institute for Plant Sciences, Plant Biochemistry, Göttingen University, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany .
    Schröter, Eric
    Albrecht von Haller Institute for Plant Sciences, Plant Biochemistry, Göttingen University, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany .
    Guan, Changhui
    Department of Molecular Biology, Wageningen University, Dreijenlaan 3, 6703 HA Wageningen, The Netherlands.
    Santos, Patricia
    Stockholm University, Faculty of Science, Department of Botany.
    Demchenko, Kirill
    Komarov Botanical Institute, Russian Academy of Sciences, 2, Professor Popova ul., 197376 St. Petersburg, Russia .
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    A natriuretic peptide is formed at high levels in actinorhizal nodules of Alnus glutinosaManuscript (preprint) (Other academic)
    Abstract [en]

    Plant homologues of mammalian natriuretic peptides (Plant Natriuretic Peptides, PNPs, also called γ-expansins as they represent expansins lacking the third exon/C-terminal domain) are small apoplastic proteins that have been associated with various biotic and abiotic stresses. Here, the characterization of PNP from Alnus glutinosa is described that is expressed at high levels in actinorhizal root nodules induced by nitrogen-fixing Frankia, and at very low levels during fruit development. In order to determine the function of this PNP in nodules, the cDNA was expressed in transgenic tobacco under control of the CaMV35S promoter. The results reveal a very slight increase in resistance to oxidative/nitrosative stress. Based on the occurrence of PNPs in different types of nitrogen-fixing root nodules and the oxidative/nitrosative stress these nodule types are exposed to, we hypothesize that Ag67 is involved in the response to nitric oxide.

  • 31.
    Rashidi, Behnoosh
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Mehrabi, Sara
    Stockholm University, Faculty of Science, Department of Botany.
    Demchenko, Kirill
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    The Casuarina glauca metallothionein I promoter in nodulated transgenic hairy roots of the actinorhizal plant Datisca glomerata2011In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 38, no 8-9, p. 728-737Article in journal (Refereed)
    Abstract [en]

    The activity of the promoter of a metallothionein gene expressed in actinorhizal nodules of Casuarina glauca Sieber ex Spreng., CgMT1, has previously been analysed in Casaurinaceae and in tobacco (Nicotiana tabacum L.), Arabidopsis and rice. In all these plants, the promoter showed high activity in the root cortex and epidermis, making it a useful tool for the expression of transgenes. Therefore, its activity was now analysed in transgenic root systems of Datisca glomerata (C. Presl) Baill, an actinorhizal plant from a different phylogenetic group than C. glauca, using the same CgMT1:: GUS fusion as in previous studies. However, in contrast with all other plant species examined previously, the CgMT1:: GUS construct showed no activity at all in D. glomerata hairy roots: the expression pattern in nodules resembled that found in C. glauca nodules. This is probably due to the changed hormone balance in hairy roots since experiments on the CgMT1:: GUS construct in transgenic Arabidopsis showed that CgMT1 promoter activity was repressed by auxin or cytokinin, respectively. Yet, in hairy roots of the model legume Lotus japonicus L. induced by the same Agrobacterium rhizogenes strain, the CgMT1 promoter was active in roots and not in nodules. These results indicate that although the expression of pRi T-DNA genes leads to changes in root hormone balance, these changes do not abolish the differences in phytohormone levels or sensitivity between plant species. Therefore, gene expression data obtained using transgenic hairy root systems have to be viewed with care, not only due to the disturbed hormone balance, but also because the effects of the pRI-T-DNA genes can differ between species.

  • 32. Ribeiro, Ana
    et al.
    Berry, Alison M.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Santos, Patricia
    Actinorhizal plants2011In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 38, no 8-9, p. v-VIIArticle, review/survey (Refereed)
    Abstract [en]

    Actinorhizal plants are a group of taxonomically diverse angiosperms with remarkable economic and ecological significance. Most actinorhizal plants are able to thrive under extreme adverse environmental conditions as well as to fix atmospheric nitrogen due to their capacity to establish root nodule symbioses with Frankia bacteria. This special issue of Functional Plant Biology is dedicated to actinorhizal plant research, covering part of the work presented at the 16th International Meeting on Frankia and Actinorhizal Plants, held on 5-8 September 2010, in Oporto, Portugal. The papers (4 reviews and 10 original articles) give an overall picture of the status of actinorhizal plant research and the imposed challenges, covering several aspects of the symbiosis, ecology and molecular tools.

  • 33. Ribeiro, Ana
    et al.
    Graca, Ines
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Santos, Patricia
    Actinorhizal plant defence-related genes in response to symbiotic Frankia2011In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 38, no 8-9, p. 639-644Article, review/survey (Refereed)
    Abstract [en]

    Actinorhizal plants have become increasingly important as climate changes threaten to remake the global landscape over the next decades. These plants are able to grow in nutrient-poor and disturbed soils, and are important elements in plant communities worldwide. Besides that, most actinorhizal plants are capable of high rates of nitrogen fixation due to their capacity to establish root nodule symbiosis with N(2)-fixing Frankia strains. Nodulation is a developmental process that requires a sequence of highly coordinated events. One of these mechanisms is the induction of defence-related events, whose precise role in a symbiotic interaction remains to be elucidated. This review summarises what is known about the induction of actinorhizal defence-related genes in response to symbiotic Frankia and their putative function during symbiosis.

  • 34. Ribeiro-Barros, Ana I.
    et al.
    da Costa, Mário
    Duro, Nuno
    Graça, Inês
    Batista-Santos, Paula
    Jorge, Tiago F.
    Lidon, Fernando C.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    António, Carla
    Ramalho, José C.
    An integrated approach to understand the mechanisms underlying salt stress tolerance in Casuarina glauca and its relation with nitrogen-fixing Frankia Thr2016In: Symbiosis, ISSN 0334-5114, E-ISSN 1878-7665, Vol. 70, no 1, p. 111-116Article in journal (Refereed)
    Abstract [en]

    Salinity is one of the most wide spread abiotic stresses affecting agricultural productivity, with an impact on more than 800 million hectares worldwide. A promising solution for the recovery of saline soils encompasses the use of actinorhizal plants, a group of perennial dicotyledonous angiosperms including species highly resilient to extreme environmental conditions. These plants are able to establish root-nodule symbiosis with N-2-fixing actinobacteria of the genus Frankia. In this review, we discuss the main physiological and biochemical mechanisms underlying salt tolerance in the model Casuarina glauca supplemented with chemical nitrogen or obtaining it from symbiotic Frankia. In the first part, an overview of the impact of increasing NaCl concentrations in photosynthesis, antioxidative system and membrane integrity is presented. The second part addresses the effect of salt stress in the symbiosis between C. glauca and Frankia strain Thr. Preliminary results from analyses of the branchlets proteome and nodule metabolome are presented as well.

  • 35.
    Santos, Patricia
    et al.
    ITQB/UNL, Oueiras, Portugal.
    Fortunato, Ana
    ITQB/UNL, Oueiras, Portugal.
    Graca, Ines
    ITQB/UNL, Oueiras, Portugal.
    Martins, Sandra Marina
    ITQB/UNL, Oueiras, Portugal.
    Gouveia, Maria Manuela
    Departamento de Biologia and Centro de Estudos da Macaronésia, Universidade da Madeira, Funchal, Portugal .
    Auguy, Florence
    IRD Montpellier, Montpellier, France.
    Bogusz, Didier
    IRD Montpellier, Montpellier, France.
    Ricardo, Cândido Pereira Pinto
    ITQB/UNL, Oueiras, Portugal.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Ribeiro, Ana
    ITQB/UNL, Oueiras, Portugal.
    Characterization of four defense-related genes up-regulatedin root nodules of Casuarina glauca2010In: Symbiosis, ISSN 0334-5114, E-ISSN 1878-7665, Vol. 50, p. 25-35Article in journal (Refereed)
    Abstract [en]

    Actinorhizal plants are capable of high rates ofnitrogen fixation, due to their capacity to establish a rootnodulesymbiosis with N2-fixing actinomycetes of the genus Frankia. Nodulation is an ontogenic process whichrequires a sequence of highly coordinated events. One of these mechanisms is the induction of defense-relatedevents, whose precise role during nodulation is largelyunknown. In order to contribute to the clarification of the involvement of defense-related genes during actinorhizal root-nodule symbiosis, we have analysed the differential expression of several genes with putative defense-relatedfunctions in Casuarina glauca nodules versus non inoculatedroots. Four genes encoding a chitinase (CgChi1), a glutathione S-transferase (CgGst), a hairpin-inducible protein (CgHin1) and a peroxidase (CgPox4) were found to be up-regulated in mature nodules compared to roots. In order to find out to which extend were the encoded proteins involved in nodule protection, development or both, generegulation studies in response to SA and wounding as wellas phylogenetic analysis of the protein sequences wereperformed. These were further characterized through expression studies after SA-treatment and wounding, and by phylogenetic analysis. We suggest that CgChi1 andCgGst are involved in defense or microsymbiont controland CgPox4 is involved in nodule development. For CgHin1 the question “defense, development or both” remains open.

  • 36.
    Santos, Patricia
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Fortunato, Ana
    Ribeiro, Ana
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Chitinases in root nodules2008In: Plant Biotechnology, ISSN 1342-4580, Vol. 25, no 3, p. 299-307Article, review/survey (Other (popular science, discussion, etc.))
    Abstract [en]

    The abundance of chitinases in plants is surprising in view of the fact that plants do not contain chitin.

    However, plant chitinases have been shown to play a role in defense, growth and developmental processes. They are also

    involved in plant-bacterial symbioses. Two groups of plants, legumes and actinorhizal plants, are able to enter root-nodule

    symbioses with nitrogen fixing bacteria, rhizobia and Frankia strains, respectively, and plant chitinases are involved in these

    interactions. None of these bacteria contain chitin in their cell walls but rhizobia produce chitinaceous signal factors. To find

    out whether symbiosis-related chitinases belonged to phylogenetically distinct subgroups, a phylogenetic analysis was

    performed including all chitinases of one dicot, Arabidopsis, and one monocot, rice. The results show that conserved class

    I- and class III-chitinases were recruited in both types of root nodule symbioses. Since no chitinaceous signal molecules are

    formed by Frankia, a role of chitinases in the control of microbial signaling is unlikely. Alternative roles of chitinases in

    root nodules are discussed.

  • 37. Schubert, Maria
    et al.
    Koteyeva, Nouria K.
    Wabnitz, Philipp W.
    Santos, Patricia
    Stockholm University, Faculty of Science, Department of Botany.
    Büttner, Michael
    Sauer, Norbert
    Demchenko, Kirill
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata2011In: Planta, ISSN 0032-0935, E-ISSN 1432-2048, Vol. 233, no 1, p. 139-152Article in journal (Refereed)
    Abstract [en]

    To understand carbon partitioning in roots and nodules of Datisca glomerata, activities of sucrose-degrading enzymes and sugar transporter expression patterns were analyzed in both organs, and plasmodesmal connections between nodule cortical cells were examined by transmission electron microscopy. The results indicate that in nodules, the contribution of symplastic transport processes is increased in comparison to roots, specifically in infected cells which develop many secondary plasmodesmata. Invertase activities are dramatically reduced in nodules as compared to roots, indicating that here the main enzyme responsible for the cleavage of sucrose is sucrose synthase. A high-affinity, low-specificity monosaccharide transporter whose expression is induced in infected cells prior to the onset of bacterial nitrogen fixation, and which has an unusually low pH optimum and may be involved in turgor control or hexose retrieval during infection thread growth.

  • 38. Schubert, Maria
    et al.
    Koteyeva, Nouria K.
    Zdyb, Anna
    Stockholm University, Faculty of Science, Department of Botany.
    Santos, Patricia
    Stockholm University, Faculty of Science, Department of Botany. ECO‐BIO/Tropical Research Institute, Portugal.
    Voitsekhovskaja, Olga V.
    Demchenko, Kirill N.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany. Göttingen University, Germany.
    Lignification of cell walls of infected cells in Casuarina glauca nodules that depend on symplastic sugar supply is accompanied by reduction of plasmodesmata number and narrowing of plasmodesmata2013In: Physiologia Plantarum: An International Journal for Plant Biology, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 147, no 4, p. 524-540Article in journal (Refereed)
    Abstract [en]

    The oxygen protection system for the bacterial nitrogen-fixing enzyme complex nitrogenase in actinorhizal nodules of Casuarina glauca resembles that of legume nodules: infected cells contain large amounts of the oxygen-binding protein hemoglobin and are surrounded by an oxygen diffusion barrier. However, while in legume nodules infected cells are located in the central tissue, actinorhizal nodules are composed of modified lateral roots with infected cells in the expanded cortex. Since an oxygen diffusion barrier around the entire cortex would also block oxygen access to the central vascular system where it is required to provide energy for transport processes, here each individual infected cell is surrounded with an oxygen diffusion barrier. In order to assess the effect of these oxygen diffusion barriers on oxygen supply for energy production for transport processes, apoplastic and symplastic sugar transport pathways in C. glauca nodules were examined. The results support the idea that sugar transport to and within the nodule cortex relies to a large extent on the less energy-demanding symplastic mechanism. This is in line with the assumption that oxygen access to the nodule vascular system is substantially restricted. In spite of this dependence on symplastic transport processes to supply sugars to infected cells, plasmodesmal connections between infected cells, and to a lesser degree with uninfected cells, were reduced during the differentiation of infected cells.

  • 39. Schubert, Maria
    et al.
    Melnikova, Anna N
    Mesecke, Nikola
    Zubkova, Elena K
    Fortte, Rocco
    Batashev, Denis R
    Barth, Inga
    Sauer, Norbert
    Gamalei, Yuri V
    Mamushina, Natalia S
    Tietze, Lutz F
    Voitsekhovskaja, Olga V
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Two novel disaccharides, rutinose and methylrutinose, are involved in carbon metabolism in Datisca glomerata2010In: Planta, ISSN 0032-0935, E-ISSN 1432-2048, Vol. 231, no 3, p. 507-521Article in journal (Refereed)
    Abstract [en]

    Datisca glomerata forms nitrogen-fixing root nodules in symbiosis with soil actinomycetes from the genus Frankia. Analysis of sugars in roots, nodules and leaves of D. glomerata revealed the presence of two novel compounds that were identified as alpha-L: -rhamnopyranoside-(1 --> 6)-D: -glucose (rutinose) and alpha-L: -rhamnopyranoside-(1 --> 6)-1-O-beta-D: -methylglucose (methylrutinose). Rutinose has been found previously as a/the glycoside part of several flavonoid glycosides, e.g. rutin, also of datiscin, the main flavonoid of Datisca cannabina, but had not been reported as free sugar. Time course analyses suggest that both rutinose and methylrutinose might play a role in transient carbon storage in sink organs and, to a lesser extent, in source leaves. Their concentrations show that they can accumulate in the vacuole. Rutinose, but not methylrutinose, was accepted as a substrate by the tonoplast disaccharide transporter SUT4 from Arabidopsis. In vivo (14)C-labeling and the study of uptake of exogenous sucrose and rutinose from the leaf apoplast showed that neither rutinose nor methylrutinose appreciably participate in phloem translocation of carbon from source to sink organs, despite rutinose being found in the apoplast at significant levels. A model for sugar metabolism in D. glomerata is presented.

  • 40. Scotti-Campos, Paula
    et al.
    Duro, Nuno
    da Costa, Mário
    Pais, Isabel P.
    Rodrigues, Ana P.
    Batista-Santos, Paula
    Semedo, José N.
    Leitão, A. Eduardo
    Lidon, Fernando C.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ramalho, José C.
    Ribeiro-Barros, Ana I.
    Antioxidative ability and membrane integrity in salt-induced responses of Casuarina glauca Sieber ex Spreng. in symbiosis with N-2-fixing Frankia Thr or supplemented with mineral nitrogen2016In: Journal of plant physiology (Print), ISSN 0176-1617, E-ISSN 1618-1328, Vol. 196-197, p. 60-69Article in journal (Refereed)
    Abstract [en]

    The actinorhizal tree Casuarina glauca tolerates extreme environmental conditions, such as high salinity. This species is also able to establish a root-nodule symbiosis with N-2-fixing bacteria of the genus Frankia. Recent studies have shown that C. glauca tolerance to high salt concentrations is innate and linked to photosynthetic adjustments. In this study we have examined the impact of increasing NaCl concentrations (200, 400 and 600 mM) on membrane integrity as well as on the control of oxidative stress in branchlets of symbiotic (NOD+) and non-symbiotic (KNO3+) C. glauca. Membrane selectivity was maintained in both plant groups at 200 mM NaCl, accompanied by an increase in the activity of antioxidative enzymes (superoxide dismutase, ascorbate peroxidase, glutathione reductase and catalase). Regarding cellular membrane lipid composition, linolenic acid (C18:3) showed a significant decline at 200 mM NaCl in both NOD+ and KNO3+ plants. In addition, total fatty acids (TFA) and C18:2 also decreased in NOD+ plants at this salt concentration, resulting in malondialdehyde (MDA) production. Such initial impact at 200 mM NaCl is probably due to the fact that NOD+ plants are subjected to a double stress, i.e., salinity and low nitrogen availability. At 400 mM NaCl a strong reduction of TFA and C18:3 levels was observed in both plant groups. This was accompanied by a decrease in the unsaturation degree of membrane lipids in NOD+. However, in both NOD+ and KNO3+ lipid modifications were not reflected by membrane leakage at 200 or 400 mM, suggesting acclimation mechanisms at the membrane level. The fact that membrane selectivity was impaired only at 600 mM NaCl in both groups of plants points to a high tolerance of C. glauca to salt stress independently of the symbiotic relation with Frankia.

  • 41. Sirrenberg, Anke
    et al.
    Goebel, Cornelia
    Grond, Stephanie
    Czempinski, Nadine
    Ratzinger, Astrid
    Karlovsky, Petr
    Santos, Patricia
    Stockholm University, Faculty of Science, Department of Botany.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Botany.
    Piriformospora indica affects plant growth by auxin production2007In: Physiologia Plantarum, Vol. 131, p. 581–589-Article in journal (Other (popular science, discussion, etc.))
    Abstract [en]

    Piriformospora indica has been shown to improve the growth of many plant species including Arabidopsis thaliana, but the mechanism by which this is achieved is still unclear. Arabidopsis root colonization by P. indica was examined in sterile culture on the medium of Murashige and Skoog. P. indica formed intracellular structures in Arabidopsis root epidermal cells and caused changes in root growth, leading to stunted and highly branched root systems. This effect was because of a diffusible factor and could be mimicked by IAA. In addition, P. indica was shown to produce IAA in liquid culture. We suggest that auxin production affecting root growth is responsible for, or at least contributes to, the beneficial effect of P. indica on its host plants.

  • 42. Tyutereva, Elena V.
    et al.
    Dobryakova, Ksenia S.
    Schiermeyer, Andreas
    Shishova, Maria F.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Demidchik, Vadim
    Reumann, Sigrun
    Voitsekhovskaja, Olga V.
    The levels of peroxisomal catalase protein and activity modulate the onset of cell death in tobacco BY-2 cells via reactive oxygen species levels and autophagy2018In: Functional Plant Biology, ISSN 1445-4408, E-ISSN 1445-4416, Vol. 45, no 1-2, p. 247-258Article in journal (Refereed)
    Abstract [en]

    In plant cells, peroxisomes participate in the metabolism of reactive oxygen species (ROS). One of the major regulators of cellular ROS levels-catalase (CAT)-occurs exclusively in peroxisomes. CAT activity is required for immunity-triggered autophagic programmed cell death (PCD). Autophagy has been recently demonstrated to represent a route for degradation of peroxisomes in plant cells. In the present study, the dynamics of the cellular peroxisome pool in tobacco BY-2 cell suspension cultures were used to analyse the effects of inhibition of basal autophagy with special attention to CAT activity. Numbers of peroxisomes per cell, levels of CAT protein and activity, cell viability, ROS levels and expression levels of genes encoding components of antioxidant system were analysed upon application of 3-methyladenine (3-MA), an inhibitor of autophagy, and/or aminotriazole (AT), an inhibitor of CAT. When applied separately, 3-MA and AT led to an increase in cell death, but this effect was attenuated by their simultaneous application. The obtained data suggest that both the levels of CAT protein in peroxisomes as well as CAT activity modulate the onset of cell death in tobacco BY-2 cells via ROS levels and autophagy.

  • 43.
    Van Nguyen, Thanh
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Wibberg, Daniel
    Battenberg, Kai
    Blom, Jochen
    Vanden Heuvel, Brian
    Berry, Alison M.
    Kalinowski, Jörn
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH2016In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 17, article id 796Article in journal (Refereed)
    Abstract [en]

    Background: The ability to establish root nodule symbioses is restricted to four different plant orders. Soil actinobacteria of the genus Frankia can establish a symbiotic relationship with a diverse group of plants within eight different families from three different orders, the Cucurbitales, Fagales and Rosales. Phylogenetically, Frankia strains can be divided into four clusters, three of which (I, II, III) contain symbiotic strains. Members of Cluster II nodulate the broadest range of host plants with species from four families from two different orders, growing on six continents. Two Cluster II genomes were sequenced thus far, both from Asia.

    Results: In this paper we present the first Frankia cluster II genome from North America (California), Dg2, which represents a metagenome of two major and one minor strains. A phylogenetic analysis of the core genomes of 16 Frankia strains shows that Cluster II the ancestral group in the genus, also ancestral to the non-symbiotic Cluster IV. Dg2 contains the canonical nod genes nodABC for the production of lipochitooligosaccharide Nod factors, but also two copies of the sulfotransferase gene nodH. In rhizobial systems, sulfation of Nod factors affects their host specificity and their stability.

    Conclusions: A comparison with the nod gene region of the previously sequenced Dg1 genome from a Cluster II strain from Pakistan shows that the common ancestor of both strains should have contained nodABC and nodH. Phylogenetically, Dg2 NodH proteins are sister to rhizobial NodH proteins. A glnA-based phylogenetic analysis of all Cluster II strains sampled thus far supports the hypothesis that Cluster II Frankia strains came to North America with Datisca glomerata following the Madrean-Tethyan pattern.

  • 44.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Liaimer, Anton
    Pederson, Eric
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Shapiro, Nicole
    Woyke, Tanja
    Altermark, Bjorn
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Weyman, Philip D.
    Dupont, Christopher L.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Genomic Changes Associated With the Evolutionary Transitions of Nostoc to a Plant Symtiont2018In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 5, p. 1160-1175Article in journal (Refereed)
    Abstract [en]

    Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic Glade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular Glade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate i-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell walls. These compounds could function as C-sources for members of the intracellular Glade. Molecular clock analysis indicated that the intracellular Glade emerged ca. 600 Ma, suggesting that intracellular Nostoc symbioses predate the origin of land plants and the emergence of their extant hosts.

  • 45.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pederson, Eric
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Shared and divergent genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiontManuscript (preprint) (Other academic)
    Abstract [en]

    The cyanobacteria belonging to the genus Nostoc comprise free-living strains but also facultative plant-symbionts. Symbiotic strains can enter into symbiosis with a taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here we compared the genomes derived from eleven symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, suggesting that this trait was most likely gained several times in the evolution of the Nostocales. Facultative symbiotic Nostoc strains showed enriched functions in the transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, amino acid and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains by a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell-walls. These compounds could function as C sources for members of the intracellular clade. Molecular clock analysis suggested that the intracellular clade emerged ~600 million years ago, which would predate the origin of land plants. This suggest that intracellular cyanobacterial symbioses may have even predated the emergence of extant terrestrial plants.

  • 46.
    Zdyb, Anna
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Georg-August-University, Germany.
    Salgado, Marco G.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Demchenko, Kirill N.
    Brenner, Wolfram G.
    Plaszczyca, Malgorzata
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Stumpe, Michael
    Herrfurth, Cornelia
    Feussner, Ivo
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Georg-August-University, Germany.
    Allene oxide synthase, allene oxide cyclase and jasmonic acid levels in Lotus japonicus nodules2018In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 1, article id e0190884Article in journal (Refereed)
    Abstract [en]

    Jasmonic acid (JA), its derivatives and its precursor cis-12-oxo phytodienoic acid (OPDA) form a group of phytohormones, the jasmonates, representing signal molecules involved in plant stress responses, in the defense against pathogens as well as in development. Elevated levels of JA have been shown to play a role in arbuscular mycorrhiza and in the induction of nitrogen-fixing root nodules. In this study, the gene families of two committed enzymes of the JA biosynthetic pathway, allene oxide synthase (AOS) and allene oxide cyclase (AOC), were characterized in the determinate nodule-forming model legume Lotus japonicus JA levels were to be analysed in the course of nodulation. Since in all L. japonicus organs examined, JA levels increased upon mechanical disturbance and wounding, an aeroponic culture system was established to allow for a quick harvest, followed by the analysis of JA levels in whole root and shoot systems. Nodulated plants were compared with non-nodulated plants grown on nitrate or ammonium as N source, respectively, over a five week-period. JA levels turned out to be more or less stable independently of the growth conditions. However, L. japonicus nodules formed on aeroponically grown plants often showed patches of cells with reduced bacteroid density, presumably a stress symptom. Immunolocalization using a heterologous antibody showed that the vascular systems of these nodules also seemed to contain less AOC protein than those of nodules of plants grown in perlite/vermiculite. Hence, aeroponically grown L. japonicus plants are likely to be habituated to stress which could have affected JA levels.

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