DOCSLIB.ORG

Iron Transport Across Symbiotic Membranes of Nitrogen-Fixing Legumes

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Iron Transport Across Symbiotic Membranes of Nitrogen-Fixing Legumes International Journal of Molecular Sciences Review Iron Transport across Symbiotic Membranes of Nitrogen-Fixing Legumes David A. Day 1,* and Penelope M. C. Smith 2 1 College of Science and Engineering, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia 2 School of Life Sciences, La Trobe University, Melbourne, VIC 3083, Australia; [email protected] * Correspondence: David.Day@flinders.edu.au Abstract: Iron is an essential nutrient for the legume-rhizobia symbiosis and nitrogen-fixing bac- teroids within root nodules of legumes have a very high demand for the metal. Within the infected cells of nodules, the bacteroids are surrounded by a plant membrane to form an organelle-like structure called the symbiosome. In this review, we focus on how iron is transported across the symbiosome membrane and accessed by the bacteroids. Keywords: legumes; nitrogen fixation; symbiosomes; iron 1. Introduction Iron is an essential nutrient for cell function and plants have developed specialised mechanisms for mobilising, absorbing and storing the metal. Cellular iron homeostasis is important because iron is toxic when present in excess. Symbiotically grown legumes have a particularly high requirement for iron and low iron severely retards their growth and their ability to fix atmospheric nitrogen [1,2]. Legumes form a symbiosis with nitrogen-fixing soil bacteria (rhizobia) that enables the plants to utilize atmospheric nitrogen for growth. Infection of the legume root by rhizobia Citation: Day, D.A.; Smith, P.M.C. results in the formation of specialized organs called nodules that provide the microaerobic Iron Transport across Symbiotic conditions required for operation of the bacterium’s nitrogenase enzyme. The establishment Membranes of Nitrogen-Fixing of the nodule begins with signaling between the plant root and the rhizobia, and results Legumes. Int. J. Mol. Sci. 2021, 22, 432. https://doi.org/10.3390/ in the bacteria colonizing root hairs. An infection thread is formed from invagination of ijms22010432 the root cell wall and the bacteria travel through the infection thread into the root cortex where nodule formation is initiated. Eventually, in response to unknown signals, the wall Received: 15 December 2020 of the infection thread and that of root cortex cells are degraded and the rhizobia released Accepted: 31 December 2020 into the cells. Within the nodule infected cells, the rhizobia are enclosed in a plant-derived Published: 4 January 2021 membrane to form an organelle-like compartment called the symbiosome (Figure1). Within this symbiosome the rhizobia differentiate into their symbiotic form, the bacteroid, which Publisher’s Note: MDPI stays neu- begin to fix nitrogen to ammonia via the enzyme nitrogenase. The symbiosome membrane tral with regard to jurisdictional clai- (SM) effectively controls the exchange of metabolites between the symbiotic partners. The ms in published maps and institutio- SM, although originating from the plasma membrane of infected nodule cells, evolves nal affiliations. over the course of nodule organogenesis to become a new and specialized membrane containing symbiosis-specific proteins synthesized from plant nuclear genes (see [3–5] for recent reviews). Mature nodules are composed of an infection zone, which contains both infected and Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. uninfected cells, surrounded by layers of cortical cells (3,5). Nutrients are transported This article is an open access article to the nodule via the vasculature, which terminates in the cortex. Nodules are generally distributed under the terms and con- considered as two distinct types, determinate and indeterminate. Determinate nodules, ditions of the Creative Commons At- such as those on soybean and Lotus japonicus, are spherical and clearly divided into the tribution (CC BY) license (https:// central infected zone and the outer cortex. Cells in the infected zone contain bacteroids creativecommons.org/licenses/by/ all at approximately the same developmental stage. Indeterminate nodules, on the other 4.0/). hand, have an elongated or branched shape and have a persistent meristem that remains Int. J. Mol. Sci. 2021, 22, 432. https://doi.org/10.3390/ijms22010432 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 432 2 of 8 throughout the life of the nodule. Indeterminate nodules are segmented into distinct developmental zones: a meristematic zone at the tip, an invasion zone where the invading Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 8 rhizobia are released, a transition zone where the rhizobia differentiate into bacteroids, a nitrogen fixation zone, and a zone of senescence closest to the root. Figure 1. (A) nodules on the root of a soybean plant. (B) detail of infected cells. V = vacuole; Figure 1. (A) nodules on the root of a soybean plant. (B) detail of infected cells. V = vacuole; as = air as = air space; uc = uninfected cell; ic = infected cell; pbm = peribacteroid membrane, now known as space; uc = uninfected cell; ic = infected cell; pbm = peribacteroid membrane, now known as the the symbiosome membrane; bact = bacteroid. symbiosome membrane; bact = bacteroid. Nitrogen fixing legume nodules have a very high requirement for iron and nodule ironMature content isnodules higher are than composed any of the of other an plantinfection organs zone, [4,6 –which8]. Iron contains is an essential both infected cofactor andfor nitrogenase,uninfected cells, the nitrogen-fixingsurrounded by enzyme,layers of as cortical well as cells respiratory (3,5). Nutrients chain components are trans- portedand other to the essential nodule enzymes via the vasculature, in bacteroids which [9]. It terminates is also required in the forcortex. the infectedNodules cells’are generallymitochondrial considered respiratory as two chain distinct components types, determinate and for the synthesisand indeterminate. of leghemoglobin Determinate in the nodules,infected cells,such as which those is on essential soybean for and the transportLotus japonicus of oxygen, are tospherical the bacteroids and clearly [8–10 divided]. Given intothat the leghemoglobin central infected is present zone and in mM the concentrationsouter cortex. Cells in the in infectedthe infected cell cytosolzone contain [10,11] bacteroidsand that infected all at approximately cells in a mature the same soybean developmental nodule contain stage. up Indeterminate to 12,000 mitochondria nodules, peron thecell other [12] andhand, as have many an as elongated 50,000 bacteroids or branched [13,14 shape], then and the have requirement a persistent for meristem iron in nodule that remainscells is enormous. throughout the life of the nodule. Indeterminate nodules are segmented into distinctNitrogen developmental fixation zones: has been a meristematic studied extensively zone at the in tip, a number an invasion of different zone where legumes, the invadingincluding rhizobia the model are plants released,Medicago a transition truncatula zoneand whereLotus the japonicus rhizobia, and differentiate important cropsinto bacteroids,such as soybean a nitrogen and pea.fixation Iron zone, is most and likely a zone imported of senescence into the closest nodule to asthe ferric root. citrate via the xylemNitrogen [15 ,16fixing] and legume subsequently nodules must have cross a very a number high requirement of cell layers for to reachiron and the infectednodule ironcells content [17]. Both is higher symplastic than any and of apoplastic the other routesplant organs are utilized [4,6–8]. for Iron this is transport an essential [15 ].co- A factormember for ofnitrogenase, the NRAMP the family nitrogen-fixing in M. truncatula enzyme,, MtNRAMP1, as well as catalyses respiratory ferrous chain iron compo- uptake nentsinto infectedand other cells essential [18], possibly enzymes acting in bacteroids in concert [9]. with It Multidrugis also required and Toxic for the Compound infected cells’Extrusion mitochondrial protein 67 respiratory (MtMATE67), chain which compon catalyzesents and citrate for effluxthe synthesis and appears of leghemoglo- to enhance biniron in uptake the infected by infected cells, which cells [19 is]. essential In this review, for the wetransport focus on of theoxygen subsequent to the bacteroids events during [8– 10].which Given iron that within leghemoglobin nodule infected is present cells is in transported mM concentrations into the symbiosomes in the infected for cell delivery cytosol to [10,11]the bacteroids. and that infected cells in a mature soybean nodule contain up to 12,000 mito- chondria per cell [12] and as many as 50,000 bacteroids [13,14], then the requirement for iron2. Studies in nodule with cells Isolated is enormous. Symbiosomes NitrogenMost studies fixation have has utilised been soybean studied nodules extensively because in ofa number the relative of easedifferent of symbiosome legumes, includingpurification the frommodel this plants species. Medicago Initial truncatula experiments and Lotus showed japonicus that isolated, and important symbiosomes crops suchaccumulate as soybean ferric and iron pea. when Iron presented is most likely with ferricimported citrate into [20 the,21 ],nodule and that as ferric this involves citrate via the theconcomitant xylem [15,16] uptake and of subsequently citrate [21]. However, must cross the a ironnumber was notof cell taken layers up byto thereach bacteroids the in- fectedwithin cells and [17]. remained Both symplastic in the symbiosome and apoplastic space [routes20]. Another
Load more

Recommended publications
  • Transport in Plants and in Root Nodules
    DEVELOPMENT OF SPECIALIZED TRANSPORT PATHWAYS IN PISUM SATIVUM ROOT NODULES by Cherish A. Warner A dissertation submitted to the Faculty of the University of Delaware in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Sciences Fall 2018 © 2018 Cherish A. Warner All Rights Reserved DEVELOPMENT OF SPECIALIZED TRANSPORT PATHWAYS IN PISUM SATIVUM ROOT NODULES by Cherish A. Warner Approved: __________________________________________________________ E. Fidelma Boyd, Ph.D. Chair of the Department of Biological Sciences Approved: __________________________________________________________ John Pelesko, Ph.D. Interim Dean of the College of Arts and Sciences Approved: __________________________________________________________ Douglas J. Doren, Ph.D. Interim Vice Provost for Graduate and Professional Education I certify that I have read this dissertation and that in my opinion it meets the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy. Signed: __________________________________________________________ D. Janine Sherrier, Ph.D. Professor in charge of dissertation I certify that I have read this dissertation and that in my opinion it meets the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy. Signed: __________________________________________________________ Jeffrey L. Caplan, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy. Signed: __________________________________________________________ Diane Herson, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.
    [Show full text]
  • Cellular and Molecular Aspects of Cnidarian-Algal Associations
    AN ABSTRACT OF THE THESIS OF Jodi A. Schwarz for the degree of Doctor of Philosophy in Zoology presented on October 18, 2002. Title: Cellular and Molecular Aspects of Cnidarian-Algal Associations Redacted for Privacy Abstract approved: Virginia M. Weis Intracellular symbioses between cnidarians and dinoflagellates from the genus Symbiodinium are widespread throughout the marine environment. These associations are ecologically significant, especially in tropical waters where symbiotic interactions between corals and Symbiodinium culminate in the formation of limestone reefs. This thesis focuses on cellular and molecular aspects of the symbiosis, specifically the initiation of the symbiosis and characterization of a host gene, sym32, that is believed to function in the symbiosis. Sym32 was originally identified as a differentially expressed protein in symbiotic vs. aposymbiotic individuals of the sea anemone, Anthopleura elegantissima. Based on its deduced amino acid sequence, sym32 belongs to a family of cell adhesion proteins that play roles in cell recognition in a diverse array of organisms. Chapter 2 examines the process by which a new cnidarian host acquires its first symbionts. Larvae of the scleractinian coral Fungia scutaria, which are initially aposymbiotic, acquired symbionts while feeding. Symbionts that entered the larval gastric cavity with food were subsequently taken into host gastrodermal cells by phagocytosis. Chapter 3 describes immunolocalization of sym32 in A. elegantissima tentacles. In aposymbiotic tentacles, sym32 was localized to vesicles within the host gastrodermal cells. Symbiotic tentacles lacked sym32-containing vesicles. Instead, sym32 was present among the membranes that enclose the symbionts within host cells. Western blots of proteins fromSymbiodiniumrevealed a 45/48kD doublet that cross-reacts with anti-sym32 antiserum.
    [Show full text]
  • 330, 329, 357 Acquired/Secondary
    j689 Index a acute/chronic pulmonary Acanthamoeba castellanii 152 histoplasmosis 567 acid-fast staining 327 ACV trafficking 248 acquired immune deficiency syndrome adaptive immune system 217 (AIDS) 330, 329, 357 – antigen processing 225–230 acquired/secondary mutualistic – B cells, antibodies and immunity endosymbionts 553–554 224–225 þ actin-associated proteins 131 – CD4 TH1 217–220 actin-based motility system 440, 435 – cells of 217–225 þ – process 435 – cytotoxic CD8 T lymphocytes 221–222 actin-binding proteins (ABPs) 126, 127 – natural killer T lymphocytes 222–223 – coronin 337 – regulatory T cells 223–224 – filamin 130 – T cell receptors 225 – SipA 379 – ab T cells 217 actin cytoskeleton 126, 135 – gd TCRT lymphocytes 222 – background 126 – TH2 lymphocytes 217–220 – – – disruption 135 TH17 lymphocytes 220 221 actin-dependent process 132 adaptive virulence mechanisms 27 – phagocytosis 289 adenylate kinase 133 actin depolymerization factor (ADF) 127 ADP-actin 129 actin filament 129 ADP-Pi-bound monomers 126 actin interactions 128 ADP-ribosylation factor 1(Arf1) 71 – binding 128 ADP transporter 133 – nucleation 128 Aerobacter aerogenes 21 actin monomers 127 Afipia felis 237, 239, 240, 242, 248, see also cat actin nucleation assay, schematic scratch disease presentation 130 – containing phagosome 240, 241, 242, 249, actin polymerization process 116, 129, 243, 251 247 – immunology 251–252 – inhibitor 399 – intracellular bacterium 239 – machinery, lipophosphoglycan (LPG)- – intracellular fate determination 246–248 mediated retention 590 – low-efficiency uptake pathway 242–243 actin-recruiting protein 277 – macrophages 246 actin-remodeling proteins 118 – uptake/intracellular compartmentation actin-rich bacteria-containing membrane, model 240, 248 formation 402 Agrobacterium tumefaciens 311, 575 actin system 126 – Cre recombinase reporter assay 311 Intracellular Niches of Microbes.
    [Show full text]
  • Understanding the Intracellular Niche in Cnidariansymbiodinium Symbioses: Parasites Lead the Way J.A
    UNDERSTANDING THE INTRACELLULAR NICHE IN CNIDARIANSYMBIODINIUM SYMBIOSES: PARASITES LEAD THE WAY J.A. Schwarz To cite this version: J.A. Schwarz. UNDERSTANDING THE INTRACELLULAR NICHE IN CNIDARIANSYMBIO- DINIUM SYMBIOSES: PARASITES LEAD THE WAY. Vie et Milieu / Life & Environment, Obser- vatoire Océanologique - Laboratoire Arago, 2008, pp.141-151. hal-03246111 HAL Id: hal-03246111 https://hal.sorbonne-universite.fr/hal-03246111 Submitted on 2 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE ET MILIEU - LIFE AND ENVIRONMENT, 2008, 58 (2): 141-151 UNDERSTANDING THE INTRACELLULAR NICHE IN CNIDARIAN- SYMBIODINIUM SYMBIOSES: PARASITES LEAD THE WAY J. A. SCHWARZ Biology Department, Vassar College, 124 Raymond Avenue, Poughkeepsie, NY 12604, USA [email protected] SYMBIOSIS ABSTRACT. – Most scleractinian corals and many other cnidarians host intracellular photosyn- CORAL CNIDARIAN thetic dinoflagellate symbionts. The symbionts contribute to host metabolism and skeletogene- SYMBIODINIUM sis to such extent that this symbiosis is well recognized for its contribution in creating the coral PHAGOCYTOSIS reef ecosystem. However, the significance of this animal-microeukaryote association as the only HOST-MICROBE INTERACTION widespread infection of animal cells by a mutualistic microeukaryote has yet to be explored.
    [Show full text]
  • 2010.-Hungria-MLI.Pdf
    Mohammad Saghir Khan l Almas Zaidi Javed Musarrat Editors Microbes for Legume Improvement SpringerWienNewYork Editors Dr. Mohammad Saghir Khan Dr. Almas Zaidi Aligarh Muslim University Aligarh Muslim University Fac. Agricultural Sciences Fac. Agricultural Sciences Dept. Agricultural Microbiology Dept. Agricultural Microbiology 202002 Aligarh 202002 Aligarh India India [email protected] [email protected] Prof. Dr. Javed Musarrat Aligarh Muslim University Fac. Agricultural Sciences Dept. Agricultural Microbiology 202002 Aligarh India [email protected] This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machines or similar means, and storage in data banks. Product Liability: The publisher can give no guarantee for all the information contained in this book. The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. # 2010 Springer-Verlag/Wien Printed in Germany SpringerWienNewYork is a part of Springer Science+Business Media springer.at Typesetting: SPI, Pondicherry, India Printed on acid-free and chlorine-free bleached paper SPIN: 12711161 With 23 (partly coloured) Figures Library of Congress Control Number: 2010931546 ISBN 978-3-211-99752-9 e-ISBN 978-3-211-99753-6 DOI 10.1007/978-3-211-99753-6 SpringerWienNewYork Preface The farmer folks around the world are facing acute problems in providing plants with required nutrients due to inadequate supply of raw materials, poor storage quality, indiscriminate uses and unaffordable hike in the costs of synthetic chemical fertilizers.
    [Show full text]
  • Ménage-À-Trois: the Amoeba Nuclearia Sp. from Lake Zurich with Its Ecto- and Endosymbiotic Bacteria
    Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2014 Ménage-à-trois: The amoeba Nuclearia sp. from Lake Zurich with its ecto- and endosymbiotic bacteria Dirren, Sebastian ; Salcher, Michaela M ; Blom, J F ; Schweikert, M ; Posch, T Abstract: We present a fascinating triad relationship between a eukaryotic amoeba and its two bac- terial symbionts. The morphological characteristics of the amoeba allowed for a confident assignment to the genus Nuclearia (Opisthokonta, Nucleariidae), but species identification resulted in an ambigu- ous result. Sequence analysis indicated an affiliation to the species N. thermophila, however, several morphological features contradict the original description. Amoebal isolates were cultured for several years with their preferred food source, the microcystin-producing harmful cyanobacterium Planktothrix rubescens. Symbioses of the amoeba with ecto- and endosymbiotic bacteria were maintained over this period. Several thousand cells of the ectosymbiont are regularly arranged inside a layer of extracellular polymeric substances produced by the amoeba. The ectosymbiont was identified as Paucibacter tox- inivorans (Betaproteobacteria), which was originally isolated by enrichment with microcystins. We found indications that our isolated ectosymbiont indeed contributed to toxin-degradation. The endosymbiont (Gammaproteobacteria, 15-20 bacteria per amoeba) is enclosed in symbiosomes inside the host cytoplasm and represents probably an obligate
    [Show full text]
  • Transgenic Approaches to Study Nodulation in the Model Legume, Lotus Japonicus
    University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 12-2003 Transgenic Approaches to Study Nodulation in the Model Legume, Lotus japonicus Crystal Bickley McAlvin University of Tennessee - Knoxville Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Microbiology Commons Recommended Citation McAlvin, Crystal Bickley, "Transgenic Approaches to Study Nodulation in the Model Legume, Lotus japonicus. " PhD diss., University of Tennessee, 2003. https://trace.tennessee.edu/utk_graddiss/2151 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Crystal Bickley McAlvin entitled "Transgenic Approaches to Study Nodulation in the Model Legume, Lotus japonicus." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Microbiology. Dr. Gary Stacey, Major Professor We have read this dissertation and recommend its acceptance: Dr. Beth Mullin, Dr. Jeff Becker, Dr. Albrecht VonArnim, Dr. Pam Small Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) To the Graduate Council: I am submitting herewith a dissertation written by Crystal Bickley McAlvin entitled “Transgenic approaches to study nodulation in the model legume, Lotus japonicus”.
    [Show full text]
  • For a Nodule-Specific Cysteine Proteinase (Nitrogen Rixation/Ahlus Gluinosa/Differential Screening/Nodulin) M
    Proc. Nati. Acad. Sci. USA Vol. 91, pp. 9891-9895, October 1994 Plant Biology Differential gene expression in an actinorhizal symbiosis: Evidence for a nodule-specific cysteine proteinase (nitrogen rixation/Ahlus gluinosa/differential screening/nodulin) M. P. GOETTING-MINESKY AND B. C. MULLIN Graduate Program in Plant Physiology and Genetics, Department of Botany, Center for Legume Research, University of Tennessee, Knoxville, TN 37996-1100 Communicated by Robert H. Burris, July 5, 1994 ABSTRACT Nodules formed on the roots of actinorhizal nitrogen. Alteration of lateral root morphology by the sym- plants as a consequence of nitrogen-fixing symbioses with the biosis results in the characteristic lobed nodules ofAlnus (3, actinomycete Frankia appear to result from modification ofthe 4). developmental pathway that leads to lateral root formation. In the Rhizobium4egume symbioses, plant proteins ex- Presently no information exists about factors that control this pressed specifically in nitrogen-fixing root nodules have been developmental switch or, until now, about genes that are observed and classified, according to time of expression, as differentially expressed as a result of an altered developmental early and late nodulins (5). Early nodulins, thought to func- pathway. Differential screening of an Alnus glutinosa nodule tion in bacterial invasion of the root and in nodule organo- cDNA library revealed altered levels of gene expression in genesis, may be expressed as a host response to one or more nodules as compared with roots and allowed isolation of host bacterial signals or as a response to altered host hormone plant nodule-specific cDNA sequences. The deduced amino levels. Late nodulins are considered to be involved in estab- acid sequence of one full-length cDNA, AgNOD-CP1, repre- lishment and maintenance ofa nodule environment favorable sents a nodule-specific cysteine proteinase similar to cysteine for nitrogen reduction and ammonium assimilation and may proteinases of the papain superfamily.
    [Show full text]
  • Srsymrk, a Plant Receptor Essential for Symbiosome Formation
    SrSymRK, a plant receptor essential for symbiosome formation Ward Capoen*, Sofie Goormachtig*, Riet De Rycke, Katrien Schroeyers, and Marcelle Holsters† Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium Communicated by Marc C. E. Van Montagu, Ghent University, Ghent, Belgium, May 23, 2005 (received for review March 31, 2005) The symbiosis between legumes and rhizobia is essential for the domains bind peptidoglycan or chitin (10, 11); hence, plant nitrogen input into the life cycle on our planet. New root organs, LysM-receptor-like kinases are good candidates for NF binding the nodules, are established, which house N2-fixing bacteria inter- and perception. nalized into the host cell cytoplasm as horizontally acquired or- In addition, other NF signal transduction elements act down- ganelles, the symbiosomes. The interaction is initiated by bacterial stream from the LysM-receptor-like kinases, because the cor- invasion via epidermal root hair curling and cell division in the responding mutants still respond to NFs by root hair swelling, but cortex, both triggered by bacterial nodulation factors. Of the no longer show a root hair curling (RHC) response. In Medicago several genes involved in nodule initiation that have been identi- truncatula, the Dmi1, Dmi2, and Dmi3 (12) genes encode a fied, one encodes the leucine-rich repeat-type receptor kinase putative ligand-gated cation channel, a leucine-rich repeat SymRK. In SymRK mutants of Lotus japonicus or its orthologs in (LRR)-type receptor kinase, and a putative calcium and cal- Medicago sp. and Pisum sativum, nodule initiation is arrested at the modulin-dependent protein kinase, respectively (13–15).
    [Show full text]
  • Binding NPC2 Proteins in Coral-Algal Symbiosis
    RESEARCH ARTICLE Sterol transfer by atypical cholesterol- binding NPC2 proteins in coral-algal symbiosis Elizabeth Ann Hambleton1*, Victor Arnold Shivas Jones1, Ira Maegele1, David Kvaskoff2, Timo Sachsenheimer2, Annika Guse1* 1Centre for Organismal Studies (COS), Universita¨ t Heidelberg, Heidelberg, Germany; 2Heidelberg University Biochemistry Center (BZH), Universita¨ t Heidelberg, Heidelberg, Germany Abstract Reef-building corals depend on intracellular dinoflagellate symbionts that provide nutrients. Besides sugars, the transfer of sterols is essential for corals and other sterol-auxotrophic cnidarians. Sterols are important cell components, and variants of the conserved Niemann-Pick Type C2 (NPC2) sterol transporter are vastly up-regulated in symbiotic cnidarians. Types and proportions of transferred sterols and the mechanism of their transfer, however, remain unknown. Using different pairings of symbiont strains with lines of Aiptasia anemones or Acropora corals, we observe both symbiont- and host-driven patterns of sterol transfer, revealing plasticity of sterol use and functional substitution. We propose that sterol transfer is mediated by the symbiosis-specific, non-canonical NPC2 proteins, which gradually accumulate in the symbiosome. Our data suggest that non-canonical NPCs are adapted to the symbiosome environment, including low pH, and play an important role in allowing corals to dominate nutrient-poor shallow tropical seas worldwide. DOI: https://doi.org/10.7554/eLife.43923.001 *For correspondence: [email protected]. de (EAH); Introduction [email protected]. de (AG) Many plants and animals cultivate symbioses with microorganisms for nutrient exchange. Cnidarians, such as reef-building corals and anemones, establish an ecologically critical endosymbiosis with pho- Competing interests: The tosynthetic dinoflagellate algae (Douglas, 2010) (family Symbiodiniaceae)(LaJeunesse et al., 2018).
    [Show full text]
  • Lineage Dynamics of the Endosymbiotic Cell Type in the Soft Coral Xenia
    Article Lineage dynamics of the endosymbiotic cell type in the soft coral Xenia https://doi.org/10.1038/s41586-020-2385-7 Minjie Hu1 ✉, Xiaobin Zheng1, Chen-Ming Fan1 ✉ & Yixian Zheng1 ✉ Received: 26 June 2019 Accepted: 28 April 2020 Many corals harbour symbiotic dinofagellate algae. The algae live inside coral cells in Published online: 17 June 2020 a specialized membrane compartment known as the symbiosome, which shares the photosynthetically fxed carbon with coral host cells while host cells provide Open access inorganic carbon to the algae for photosynthesis1. This endosymbiosis—which is Check for updates critical for the maintenance of coral reef ecosystems—is increasingly threatened by environmental stressors that lead to coral bleaching (that is, the disruption of endosymbiosis), which in turn leads to coral death and the degradation of marine ecosystems2. The molecular pathways that orchestrate the recognition, uptake and maintenance of algae in coral cells remain poorly understood. Here we report the chromosome-level genome assembly of a Xenia species of fast-growing soft coral3, and use this species as a model to investigate coral–alga endosymbiosis. Single-cell RNA sequencing identifed 16 cell clusters, including gastrodermal cells and cnidocytes, in Xenia sp. We identifed the endosymbiotic cell type, which expresses a distinct set of genes that are implicated in the recognition, phagocytosis and/or endocytosis, and maintenance of algae, as well as in the immune modulation of host coral cells. By coupling Xenia sp. regeneration and single-cell RNA sequencing, we observed a dynamic lineage progression of the endosymbiotic cells. The conserved genes associated with endosymbiosis that are reported here may help to reveal common principles by which diferent corals take up or lose their endosymbionts.
    [Show full text]
  • Transcription of ENOD8 in Medicago Truncatula Nodules Directs ENOD8 Esterase to Developing and Mature Symbiosomes
    MPMI Vol. 21, No. 4, 2008, pp. 404–410. doi:10.1094/ MPMI -21-4-0404. © 2008 The American Phytopathological Society e-Xtra* Transcription of ENOD8 in Medicago truncatula Nodules Directs ENOD8 Esterase to Developing and Mature Symbiosomes Laurent Coque,1 Purnima Neogi,1 Catalina Pislariu,1 Kimberly A. Wilson,1 Christina Catalano,2 Madhavi Avadhani,2 D. Janine Sherrier,2 and Rebecca Dickstein1 1University of North Texas, Department of Biological Sciences, Chestnut and Avenue C, Denton 76203-5220, U.S.A.; 2Department of Plant and Soil Sciences and Delaware Biotechnology Institute, University of Delaware, Newark 19711, U.S.A. Submitted 25 October 2007. Accepted 5 December 2007. In Medicago truncatula nodules, the soil bacterium Sino- attaching to root hairs, reorienting root hair cell wall growth, rhizobium meliloti reduces atmospheric dinitrogen into and forming a bacterial colony within a tightly curled root hair, nitrogenous compounds that the legume uses for its own rhizobia enter plant roots through plant-derived infection threads growth. In nitrogen-fixing nodules, each infected cell con- that traverse several cell layers. Ultimately, the rhizobia are de- tains symbiosomes, which include the rhizobial cell, the posited in nodule primordium cells in a process that resembles symbiosome membrane surrounding it, and the matrix endocytosis or phagocytosis. between the bacterium and the symbiosome membrane, A plasma membrane-derived membrane surrounds each bac- termed the symbiosome space. Here, we describe the local- terium and results in a new organelle-like compartment in the ization of ENOD8, a nodule-specific esterase. The onset of infected nodule cells termed the symbiosome. Within symbio- ENOD8 expression occurs at 4 to 5 days postinoculation, somes, coordinated division of rhizobia and the symbiosome before the genes that support the nitrogen fixation capa- membrane occurs.
    [Show full text]