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Title: Reprogramming sphingolipid glycosylation is required for endosymbiont persistence in Medicago truncatula

Journal Article · · Current Biology

Plant endosymbiosis relies on the development of specialized membranes that encapsulate the endosymbiont and facilitate nutrient exchange. However, the identity and function of lipids within these membrane interfaces is largely unknown. Here, we identify GLUCOSAMINE INOSITOL PHOSPHORYLCERAMIDE TRANSFERASE1 (GINT1) as a sphingolipid glycosyltransferase highly expressed in Medicago truncatula root nodules and roots colonized by arbuscular mycorrhizal (AM) fungi and further demonstrate that this enzyme functions in the synthesis of N-acetyl-glucosamine-decorated glycosyl inositol phosphoryl ceramides (GIPCs) in planta. MtGINT1 expression was developmentally regulated in symbiotic tissues associated with the development of symbiosome and periarbuscular membranes. RNAi silencing of MtGINT1 did not affect overall root growth but strongly impaired nodulation and AM symbiosis, resulting in the senescence of symbiosomes and arbuscules. Our results indicate that, although M. truncatula root sphingolipidome predominantly consists of hexose-decorated GIPCs, local reprogramming of GIPC glycosylation by MtGINT1 is required for the persistence of endosymbionts within the plant cell.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); JSPS KAKENHI
Grant/Contract Number:
AC02-05CH11231; DGE 1106400; 17K15411; 26292190
OSTI ID:
1777615
Alternate ID(s):
OSTI ID: 1783142
Journal Information:
Current Biology, Journal Name: Current Biology Vol. 31 Journal Issue: 11; ISSN 0960-9822
Publisher:
ElsevierCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (68)

Molecular composition and development of the plant with the peribacteroid membrane of pea root nodules journal July 1991
Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation journal May 2012
Lipids of plant membrane rafts journal July 2012
A high-throughput inducible RNAi vector for plants journal November 2005
An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis journal November 2015
Differential Expression of a Glycosyl Inositol Phospholipid Antigen on the Peribacteroid Membrane during Pea Nodule Development journal January 1995
Cell adhesion in Arabidopsis thaliana is mediated by ECTOPICALLY PARTING CELLS 1 - a glycosyltransferase (GT64) related to the animal exostosins: Glycosyltransferase mediates plant cell adhesion journal June 2005
Differential Localization of Carbohydrate Epitopes in Plant Cell Walls in the Presence and Absence of Arbuscular Mycorrhizal Fungi journal May 1996
Prepenetration Apparatus Assembly Precedes and Predicts the Colonization Patterns of Arbuscular Mycorrhizal Fungi within the Root Cortex of Both Medicago truncatula and Daucus carota   journal May 2008
Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? journal December 2005
NODULES WITH ACTIVATED DEFENSE 1 is required for maintenance of rhizobial endosymbiosis in Medicago truncatula journal June 2016
Characterization of Lipid Rafts from Medicago truncatula Root Plasma Membranes: A Proteomic Study Reveals the Presence of a Raft-Associated Redox System journal March 2007
A Mycorrhizal-Specific Ammonium Transporter from Lotus japonicus Acquires Nitrogen Released by Arbuscular Mycorrhizal Fungi journal March 2009
The role of the cell wall compartment in mutualistic symbioses of plants journal June 2014
Immunocytochemical location of hydroxyproline rich glycoproteins at the interface between a mycorrhizal fungus and its host plants journal February 1991
Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant journal June 2017
Synthesis and Function of Complex Sphingolipid Glycosylation journal June 2020
Glycosphingolipid metabolism in cell fate specification journal December 2018
Live-Cell Imaging Reveals Periarbuscular Membrane Domains and Organelle Location in Medicago truncatula Roots during Arbuscular Mycorrhizal Symbiosis journal August 2009
A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi journal September 2002
Molecular characterization and targeted quantitative profiling of the sphingolipidome in rice journal September 2016
Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins journal December 2017
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize journal May 2017
A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1 journal April 2017
Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization journal October 2008
Identification of a Sphingolipid α-Glucuronosyltransferase That Is Essential for Pollen Function in Arabidopsis journal August 2014
Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone journal February 2013
EXO70I Is Required for Development of a Sub-domain of the Periarbuscular Membrane during Arbuscular Mycorrhizal Symbiosis journal August 2015
A set of fluorescent protein-based markers expressed from constitutive and arbuscular mycorrhiza-inducible promoters to label organelles, membranes and cytoskeletal elements in Medicago truncatula journal December 2014
Characterization of the targeted nuclear accumulation of GFP within the cells of transgenic plants journal September 1997
A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis journal January 2013
Single-Chain β- d -Glycopyranosylamides of Unsaturated Fatty Acids: Self-Assembly Properties and Applications to Artificial Cell Development journal April 2019
Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development: Arbuscule-containing and non-colonized cortical cells journal November 2011
Sphingolipids and Plant Defense/Disease: The “Death” Connection and Beyond journal January 2012
How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza journal January 2012
Breakdown of phospholipids in mild alkaline hydrolysis journal January 1963
Symbiotic Fungi Control Plant Root Cortex Development through the Novel GRAS Transcription Factor MIG1 journal October 2016
High-Throughput Construction of Intron-Containing Hairpin RNA Vectors for RNAi in Plants journal May 2012
GIPC: Glycosyl Inositol Phospho Ceramides, the major sphingolipids on earth journal March 2016
Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis journal November 2016
GLUCOSAMINE INOSITOLPHOSPHORYLCERAMIDE TRANSFERASE1 (GINT1) Is a GlcNAc-Containing Glycosylinositol Phosphorylceramide Glycosyltransferase journal May 2018
Structural signatures in EPR3 define a unique class of plant carbohydrate receptors journal July 2020
GmN70 and LjN70. Anion Transporters of the Symbiosome Membrane of Nodules with a Transport Preference for Nitrate journal March 2005
An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula journal January 2013
Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant journal September 2015
Transport processes of the legume symbiosome membrane journal December 2014
Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense journal February 2002
Production of hydroxycinnamoyl anthranilates from glucose in Escherichia coli journal January 2013
A systematic simulation of the effect of salicylic acid on sphingolipid metabolism journal March 2015
Disruption of the ceramide synthase LOH1 causes spontaneous cell death in Arabidopsis thaliana journal August 2011
Revisiting Plant Plasma Membrane Lipids in Tobacco: A Focus on Sphingolipids journal October 2015
Two Medicago truncatula Half-ABC Transporters Are Essential for Arbuscule Development in Arbuscular Mycorrhizal Symbiosis journal May 2010
Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity journal December 2013
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation journal July 2007
Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis journal January 2017
Abnormal Glycosphingolipid Mannosylation Triggers Salicylic Acid–Mediated Responses in Arabidopsis journal May 2013
Arbuscular Mycorrhizal Fungi Elicit a Novel Intracellular Apparatus in Medicago truncatula Root Epidermal Cells before Infection journal November 2005
Accumulation of phosphoinositides in distinct regions of the periarbuscular membrane journal November 2018
Sphingolipids and the formation of sterol-enriched ordered membrane domains journal December 2006
Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals journal May 1996
Differential Effect of Plant Lipids on Membrane Organization journal February 2015
A symbiosis‐dedicated SYNTAXIN OF PLANTS 13II isoform controls the formation of a stable host–microbe interface in symbiosis journal April 2016
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing journal February 2014
Multiple Exocytotic Markers Accumulate at the Sites of Perifungal Membrane Biogenesis in Arbuscular Mycorrhizas journal December 2011
Biochemical characterization of symbiosome membrane proteins fromMedicago truncatula root nodules journal February 2004
Toluidine blue: A review of its chemistry and clinical utility journal January 2012
Plant sphingolipids: function follows form journal June 2013