Katharina Pawlowski

Nitrogen is the element that most often limits plant growth. Only prokaryotes that can form the nitrogenase enzyme complex can reduce air dinitrogen to ammonia and thereby bring it from the atmosphere into the biosphere. Plants that can enter a root nodule symbiosis with nitrogen-fixing soil bacteria are independent of soil nitrogen, i.e. fertilizer. In root nodules, the microsymbionts are hosted within plant cells, fix dinitrogen and deliver the products of nitrogen fixation to the host plant, while the host plant supplies them with carbon sources. Only plants belonging to a particular group, the so-called Fabid clade (but not all of them), are able to establish a root nodule symbiosis. Two groups of microsymbionts are involved in these symbioses – rhizobia with legumes and with Parasponia sp. from the Cannabaceae family, and Frankia strains with actinorhizal plants. Actinorhizal plants - mostly trees or woody shrubs - belong to eight different families from three different orders (Fagales, Rosales and Cucurbitales; look here for details).

Evolution of root nodule symbioses

The question arises which common feature of these plants represents the precondition that allowed the evolution of a root nodule symbiosis. Therefore, we compare root nodule symbioses from different branches of the Fabid clade in order to identify the common vs. family-specific features. The wide phylogenetic range of actinorhizal plant means that there is significant diversity among symbioses involving host plants from different families (see here). We are working on different plant species:

Legumes:

Medicago truncatula - model legume, indeterminate nodules, intracellular infection by Sinorhizobium meliloti

Lotus japonicus - model legume, determinate nodules, intracellular infection by Mesorhizobium loti

Actinorhizal plants:

Casuarina glauca (swamp oak) - Australian tree, intracellular infection by Frankia cluster-1c

Alnus glutinosa (black alder) - Northern hemisphere tree, intracellular infection by Frankia cluster-1a

Coriaria spp. - shrubs, distributed in Mediterranean, Northern India/Pakistan/Nepal, China, Japan, Taiwan, Philippines, Papua New Guinea, New Zealand, South America, pathway of infection by Frankia cluster-2 under examination

Datisca glomerata (Durango root) - Northwest American suffruticose plant, pathway of infection by Frankia cluster-2 under examination

Ceanothus thyrsiflorus – Northwest American shrub, intercellular infection by Frankia cluster-2

On the microbsymbiont side, in contrast with rhizobia, Frankia strains are monophyletic. Phylogenetically, there are four Frankia clusters, three of which representing facultative symbionts while cluster IV contains only non-symbiotic strains. Genome sizes differ strongly between strains from different clusters (cluster I genomes are ca. 7.5 MB in size except for the subgroup that nodulates Casuarinaceae which with 5.3 – 5.7 MB shows stronger genome reduction, cluster II genomes (5.3-5.6 MB) also show strong genome reduction, while clusters III (9-10 MB) and IV (ca. 10 MB) have the largest genome). Host range is correlated with phylogeny – e.g., members of cluster I nodulate actinorhizal Fagales (with the exception of Gymnostoma sp. (Casuarinaceae) and Myrica sp. (Myricaceae), members of cluster II nodule actinorhizal Cucurbitales and from the Rosales the actinorhizal Rosaceae and Ceanothus sp. (Rhamnaceae). Members of cluster III nodulate actinorhizal members of two Rosales families (Elaeagnaceae and Rhamnaceae with the exception of Ceanothus sp.) and the outlier genera of the actinorhizal Fagales, Gymnostoma sp. and Myrica sp. However, as a rule a member of a particular cluster cannot nodulate all host plants of said cluster.

            Phylogenetically, cluster II is basal to all other Frankia clusters (see here). So far, only one member of this cluster could be cultured, and this one, in contrast with all other known Frankia strains, is alkaliphile (see here). We are particularly interested in the evolution of cluster II and its host plants.

Projects (people from SU underlined):

• Comparison of Frankia cluster II genomes from different areas (Fede Berckx, Hsiao-Han Lin, Cyndi Mae Bandong, Jessica Simbahan, Luis Gabriel Wall, Than Van Nguyen, Daniel Wibberg, Jörn Kalinowski)
• Control of the microsymbiont by the plant in nodules of Datisca glomerata: characterization of nodule-specific cysteine-rich peptides (Irina Demina, Marco Salgado)
• What is the carbon source provided by Datisca glomerata to its microsymbiont? (Marco Salgado, Irina Demina, Fede Berckx, Nadia Binte Obaid, Sabine Zimmermann)
• Mechanism of stable internal accommodation of Frankia in actinorhizal nodules of Casuarina glauca and Datisca glomerata (Behnoosh Rashidi, Kirill Demchenko)
• Conservation of transcription factors involved in nodule development: activity of nodule-specific promoters in heterologous systems (Behnoosh Rashidi, Sara Mehrabi, Kirill Demchenko, Patricia Santos, Beth Mullin)
• Differentiation of infected cells in Datisca glomerata: transcriptome analysis using laser capture microdissection (Nadia Binte Obaid, Irina Demina, Marco Salgado, Nicole Gaude, Franziska Krajinski, Max Griesmann, Christoph Ziegenhain, Wolfgang Enard)
• Comparison of nodule development and differentiation in two host plants of cluster-2 Frankia, Datisca glomerata and Ceanothus thyrsiflorus (Thanh Van Nguyen, Marco Salgado, Fede Berckx, Rolf Hilker, Daniel Wibberg, Jörn Kalinowski, Kai Battenberg, Alison Berry)
• Metabolomics of actinorhizal nodules (Tomas Persson, Thanh Van Nguyen, Fede Berckx, Stefano Papazian, Benedicte Albrectsen, Alison Berry, Nicole Alloisio, Philippe Normand)
• Auxin and Datisca glomerata nodules (Irina Demina, Pooja Jha Maity, Anurupa Nagchowdhury, Marco Salgado, Ulrike Mathesius)

Group members (current):

• Nadia Binte Obaid (PhD student)
• Ciara Morrison (MSc student)
• Matilda Sandin (MSc student)

Former group members:

• Anna Maria Zdyb (PhD) (now: Institute of Genetics, Technical University Dresden, Zellescher Weg 20b, 01062 Dresden, Germany)
• Małgorzata Płaszczyca (PhD) (now: Rybnik, Poland)
• Patricia Santos (PostDoc) (now: Department of Biochemistry and Molecular Biology, University of Nevada, Reno 89557, NV, USA)
• Behnoosh Rashidi (PhD) (now: Copenhagen, Denmark)
• Sara Mehrabi (MSc) (now: Department of Ecology and Genetics, Evolutionary Biology, Norbyvägen 18D, 752 36 Uppsala, Sweden)
• Tomas Persson (PhD) (now: Department for Mathematics and Science Education, Stockholm University)
• Stefano Papazian (MSc) (now: Exposomics, SciLifeLab, Stockholm, Sweden)
• Irina V. Demina (PhD) (now: patent lawyer at BRANN AB, Uppsala, Sweden)
• Anurupa Nagchowdhury (MSc) (now: Karolinska Institutet, Stockholm, Sweden)
• Pooja Jha Maity (PostDoc) (Department of Botany, Ramjas College, University of Delhi, Delhi 110 007, India)
• Xiaoyun Gong (MSc) (now: Genetics, LMU Munich, Biocenter, Großhaderner Str. 4, 82152 Martinsried, Germany)
• Thanh Van Nguyen (PhD) (Novogene Europe, Uppsala, Sweden)
• Marco Guedes Salgado (PhD) (now: Institute of Biotechnology HiLIFE, Helsinki University, Viikinkaari 5d, 00790 Helsinki, Finland)
• Nadia Binte Obaid (MSc) (now: PhD student in the same group)
• Emilia Regazzoni (MSc) (now: Research Engineer at SciLifeLab, Solnavägen 9, Biomedicum, 17165 Solna, Sweden)
• András Patyi (MSc) (now: Department of Crop Sciences, FIBL, Ackerstrasse 113, CH-5070 Frick, Switzerland
• Fede Berckx (PhD) (now: Department of Crop Production Ecology, SLU Uppsala, Ekologicentrum, Ulls väg 16, 756 51 Uppsala, Sweden)

Funding (currently):

VR

External collaborations:

• Paul Dahlin (Agroscope, Research Division, Plant Protection, Phytopathology and Zoology in Fruit and Vegetable
  Production, 8820 Wädenswil, Switzerland)
• Martin Parniske (Genetics, LMU Munich, Biocenter, Großhaderner Str. 4, 82152 Martinsried, Germany)
• Kirill Demchenko (Laboratory of Plant Anatomy & Morphology, V.L. Komarov Botanical Institute, Russian Academy of Sciences, 2 Prof. Popov Street, St.-Petersburg 197376, St.-Petersburg, Russia)
• Olga Voitsekhovskaja (Department of Plant Physiologial Ecology, V.L. Komarov Botanical Institute, Russian Academy of Sciences, 2 Prof. Popov Street, 197376 St. Petersburg, Russia)
• Daniel Wibberg and Jörn Kalinowski (CeBiTec, Bielefeld University, Universitätsstr. 25, 33615 Bielefeld, Germany)
• Rolf Hilker (Department of Bioinformatics and Systems Biology, Justus-Liebig University Giessen, Heinrich-Buff-Ring 58, 35392 Giessen, Germany)
• Anita Sellstedt (Department of Physiological Botany, Umeå University, 901 87 Umeå, Sweden)
• Pooja Jha Maity (Department of Botany, University of Delhi, Delhi 110 007, India)
• Patricia Santos and Dylan Kosma (Department of Biochemistry and Molecular Biology, University of Nevada, Reno 89557, NV, USA)
• Petar Pujic, Nicole Alloisio and Philippe Normand (Ecologie Microbienne, Universite Lyon 1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne Cedex, France)
• Sabine Zimmermann (Biochimie et Physiologie Moleéculaire des Plantes, UMR 5004 CNRS/INRA/SupAgro/UM2, Campus INRA/SupAgro, 2 Place Viala, 34060 Montpellier Cedex 2, France)
• Ana Ribeiro-Barros (ECO-BIO/IICT, Quinta do Marquês, 2784-505 Oeiras, Portugal)
• Ulrike Mathesius (Division of Plant Science, Research School of Biology, Australian National University, Canberra ACT 2601, Australia)
• Didier Bogusz and Claudine Franche (IRD Montpellier, France)
• Beth Mullin (Department of Botany, University of Tennessee, Knoxville, TN 37996-1100, USA)
• Franziska Krajinski (Institute of Biology, Applied and General Botany Lab, Leipzig University, Johannisallee 21-23, 04103 Leipzig, Germany)
• Christoph Ziegenhain and Wolfgang Enard (Anthropology and Human Genetics, Department Biology II, Faculty of Biology, Ludwig-Maximilians University Munich, Großhaderner Straße 2, 82152 Martinsried, Germany)
• Marcel Bucher (Botanical Institute, Cologne Biocenter, Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, 50674 Cologne, Germany)

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