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Title: Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus

Abstract

The success of Ericaceae in stressful habitats enriched in heavy metals has been ascribed to the distinctive abilities of their mycorrhizal fungal partners to withstand heavy metal stress and to enhance metal tolerance in the host plant. Whereas heavy metal tolerance has been extensively investigated in some ericoid mycorrhizal (ERM) fungi, the molecular and cellular mechanisms that extend tolerance to the host plant are currently unknown. Here, we show a reduced Cd content in Cd-exposed mycorrhizal roots of Vaccinium myrtillus colonized by a metal tolerant isolate of the fungus Oidiodendron maius as compared to non-mycorrhizal roots. To better understand this phenotype, we applied Next Generation Sequencing technologies to analyze gene expression in V. myrtillus and O. maius Zn grown under normal and Cd-stressed conditions, in the free living and in the mycorrhizal status. The results clearly showed that Cd had a stronger impact on plant gene expression than symbiosis, whereas fungal gene expression was mainly regulated by symbiosis. The higher abundance of transcripts coding for stress related proteins in non-mycorrhizal roots may be related to the higher Cd content. Regulated plant metal transporters have been identified that may play a role in reducing Cd content in mycorrhizal roots exposed tomore » this metal.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [3];  [4];  [5];  [5];  [6];  [3]
  1. Univ. of Turin (Italy). Dept. of Life Sciences and Systems Biology
  2. Univ. of Turin (Italy). Dept. of Life Sciences and Systems Biology; Université de Lorraine, INRAE, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est Nancy, Champenoux (France)
  3. Univ. of Turin (Italy). Dept. of Life Sciences and Systems Biology
  4. Université de Lorraine, INRAE, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est Nancy, Champenoux (France)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Université de Lorraine, INRAE, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est Nancy, Champenoux (France); Beijing Forestry University, Beijing (China). Beijing Advanced Innovation Center for Tree Breeding by Molecular Design
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1628186
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
Microbiology; Cd tolerance, transcriptomics; ericoid mycorrhiza; Oidiodendron maius, Vaccinium myrtillus

Citation Formats

Casarrubia, Salvatore, Martino, Elena, Daghino, Stefania, Kohler, Annegret, Morin, Emmanuelle, Khouja, Hassine-Radhouane, Murat, Claude, Barry, Kerrie W., Lindquist, Erika A., Martin, Francis M., and Perotto, Silvia. Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus. United States: N. p., 2020. Web. https://doi.org/10.3389/fmicb.2020.00341.
Casarrubia, Salvatore, Martino, Elena, Daghino, Stefania, Kohler, Annegret, Morin, Emmanuelle, Khouja, Hassine-Radhouane, Murat, Claude, Barry, Kerrie W., Lindquist, Erika A., Martin, Francis M., & Perotto, Silvia. Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus. United States. https://doi.org/10.3389/fmicb.2020.00341
Casarrubia, Salvatore, Martino, Elena, Daghino, Stefania, Kohler, Annegret, Morin, Emmanuelle, Khouja, Hassine-Radhouane, Murat, Claude, Barry, Kerrie W., Lindquist, Erika A., Martin, Francis M., and Perotto, Silvia. Mon . "Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus". United States. https://doi.org/10.3389/fmicb.2020.00341. https://www.osti.gov/servlets/purl/1628186.
@article{osti_1628186,
title = {Modulation of Plant and Fungal Gene Expression Upon Cd Exposure and Symbiosis in Ericoid Mycorrhizal Vaccinium myrtillus},
author = {Casarrubia, Salvatore and Martino, Elena and Daghino, Stefania and Kohler, Annegret and Morin, Emmanuelle and Khouja, Hassine-Radhouane and Murat, Claude and Barry, Kerrie W. and Lindquist, Erika A. and Martin, Francis M. and Perotto, Silvia},
abstractNote = {The success of Ericaceae in stressful habitats enriched in heavy metals has been ascribed to the distinctive abilities of their mycorrhizal fungal partners to withstand heavy metal stress and to enhance metal tolerance in the host plant. Whereas heavy metal tolerance has been extensively investigated in some ericoid mycorrhizal (ERM) fungi, the molecular and cellular mechanisms that extend tolerance to the host plant are currently unknown. Here, we show a reduced Cd content in Cd-exposed mycorrhizal roots of Vaccinium myrtillus colonized by a metal tolerant isolate of the fungus Oidiodendron maius as compared to non-mycorrhizal roots. To better understand this phenotype, we applied Next Generation Sequencing technologies to analyze gene expression in V. myrtillus and O. maius Zn grown under normal and Cd-stressed conditions, in the free living and in the mycorrhizal status. The results clearly showed that Cd had a stronger impact on plant gene expression than symbiosis, whereas fungal gene expression was mainly regulated by symbiosis. The higher abundance of transcripts coding for stress related proteins in non-mycorrhizal roots may be related to the higher Cd content. Regulated plant metal transporters have been identified that may play a role in reducing Cd content in mycorrhizal roots exposed to this metal.},
doi = {10.3389/fmicb.2020.00341},
journal = {Frontiers in Microbiology},
number = ,
volume = 11,
place = {United States},
year = {2020},
month = {3}
}

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Works referenced in this record:

Response to cadmium in higher plants
journal, April 1999


The OsNRAMP1 iron transporter is involved in Cd accumulation in rice
journal, June 2011

  • Takahashi, Ryuichi; Ishimaru, Yasuhiro; Senoura, Takeshi
  • Journal of Experimental Botany, Vol. 62, Issue 14
  • DOI: 10.1093/jxb/err136

Origin, Biogenesis, and Activity of Plant MicroRNAs
journal, February 2009


Plant Pleiotropic Drug Resistance Transporters: Transport Mechanism, Gene Expression, and Function: Plant PDR: Mechanism, expression, and function
journal, May 2014

  • Nuruzzaman, Mohammed; Zhang, Ru; Cao, Hong-Zhe
  • Journal of Integrative Plant Biology, Vol. 56, Issue 8
  • DOI: 10.1111/jipb.12196

Insights into the development of fungal biomarkers for metal ecotoxicity assessment: Case of Trametes versicolor exposed to copper
journal, April 2010

  • Lebrun, Jérémie D.; Trinsoutrot-Gattin, Isabelle; Laval, Karine
  • Environmental Toxicology and Chemistry, Vol. 29, Issue 4
  • DOI: 10.1002/etc.101

Biogenesis, Turnover, and Mode of Action of Plant MicroRNAs
journal, July 2013


Model systems to unravel the molecular mechanisms of heavy metal tolerance in the ericoid mycorrhizal symbiosis
journal, December 2015


Evidence of nickel (Ni) efflux in Ni-tolerant ectomycorhizal P isolithus albus isolated from ultramafic soil: Metal efflux in Ni-tolerant Pisolithus albus
journal, June 2014

  • Majorel, Clarisse; Hannibal, Laure; Ducousso, Marc
  • Environmental Microbiology Reports, Vol. 6, Issue 5
  • DOI: 10.1111/1758-2229.12176

Physiological and molecular mechanisms of heavy metal accumulation in nonmycorrhizal versus mycorrhizal plants
journal, November 2018

  • Shi, Wenguang; Zhang, Yuhong; Chen, Shaoliang
  • Plant, Cell & Environment, Vol. 42, Issue 4
  • DOI: 10.1111/pce.13471

Structural Biology of the Major Facilitator Superfamily Transporters
journal, June 2015


Phytochelatins and Their Roles in Heavy Metal Detoxification
journal, July 2000


Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris
journal, July 1981

  • Bradley, R.; Burt, A. J.; Read, D. J.
  • Nature, Vol. 292, Issue 5821
  • DOI: 10.1038/292335a0

Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice
journal, May 2012


Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots
journal, September 2013

  • Xu, Liang; Wang, Yan; Zhai, Lulu
  • Journal of Experimental Botany, Vol. 64, Issue 14
  • DOI: 10.1093/jxb/ert240

Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress
journal, June 2005


Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants
journal, February 2012

  • Khraiwesh, Basel; Zhu, Jian-Kang; Zhu, Jianhua
  • Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 2
  • DOI: 10.1016/j.bbagrm.2011.05.001

Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.)
journal, September 2013


How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution
journal, January 2011

  • Colpaert, Jan V.; Wevers, Jan H. L.; Krznaric, Erik
  • Annals of Forest Science, Vol. 68, Issue 1
  • DOI: 10.1007/s13595-010-0003-9

The SlZRT1 Gene Encodes a Plasma Membrane-Located ZIP (Zrt-, Irt-Like Protein) Transporter in the Ectomycorrhizal Fungus Suillus luteus
journal, November 2017


A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011


The NRAMP family of metal-ion transporters
journal, July 2006

  • Nevo, Yaniv; Nelson, Nathan
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 7
  • DOI: 10.1016/j.bbamcr.2006.05.007

Secretion of small proteins is species-specific within Aspergillus sp
journal, May 2016

  • Valette, Nicolas; Benoit-Gelber, Isabelle; Falco, Marcos Di
  • Microbial Biotechnology, Vol. 10, Issue 2
  • DOI: 10.1111/1751-7915.12361

Yeast expression of mammalian Onzin and fungal FCR1 suggests ancestral functions of PLAC8 proteins in mitochondrial metabolism and DNA repair
journal, April 2019


Expression of the Novel Wheat Gene TM20 Confers Enhanced Cadmium Tolerance to Bakers' Yeast
journal, April 2008

  • Kim, Yu-Young; Kim, Do-Young; Shim, Donghwan
  • Journal of Biological Chemistry, Vol. 283, Issue 23
  • DOI: 10.1074/jbc.m708947200

The role of ectomycorrhizas in heavy metal stress tolerance of host plants
journal, December 2014


The Biology of Mycorrhiza in the Ericaceae. Viii. the role of Mycorrhizal Infection in Heavy Metal Resistance
journal, June 1982


REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004


Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

The copper microRNAs
journal, October 2016


Defective Copper Transport in the copt5 Mutant Affects Cadmium Tolerance
journal, November 2014

  • Carrió-Seguí, Angela; Garcia-Molina, Antoni; Sanz, Amparo
  • Plant and Cell Physiology, Vol. 56, Issue 3
  • DOI: 10.1093/pcp/pcu180

The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s)
journal, November 2010


Laccases Direct Lignification in the Discrete Secondary Cell Wall Domains of Protoxylem
journal, August 2014


The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications
journal, October 2016

  • Ferrol, Nuria; Tamayo, Elisabeth; Vargas, Paola
  • Journal of Experimental Botany, Vol. 67, Issue 22
  • DOI: 10.1093/jxb/erw403

Parlez-vous effectors?: Editorial
journal, August 2010


Phenylpropanoid Biosynthesis
journal, January 2010


Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc
journal, September 1994


The Transporter Classification Database (TCDB): recent advances
journal, November 2015

  • Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1103

P HYTOCHELATINS AND M ETALLOTHIONEINS : Roles in Heavy Metal Detoxification and Homeostasis
journal, June 2002


Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants
journal, June 2004


The Structure and Function of the Ericoid Mycorrhizal Root
journal, April 1996


High-Affinity Manganese Uptake by the Metal Transporter NRAMP1 Is Essential for Arabidopsis Growth in Low Manganese Conditions
journal, March 2010

  • Cailliatte, Rémy; Schikora, Adam; Briat, Jean-François
  • The Plant Cell, Vol. 22, Issue 3
  • DOI: 10.1105/tpc.109.073023

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015

  • Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
  • Nature Genetics, Vol. 47, Issue 4
  • DOI: 10.1038/ng.3223

MicroRNAs as regulators in plant metal toxicity response
journal, January 2012

  • Mendoza-Soto, Ana B.; Sánchez, Federico; Hernández, Georgina
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00105

Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions
journal, December 2003


A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: Ligninolytic enzyme regulation in Pleurotus ostreatus
journal, November 2017


Cupredoxins—A study of how proteins may evolve to use metals for bioenergetic processes
journal, January 2011

  • Choi, Moonsung; Davidson, Victor L.
  • Metallomics, Vol. 3, Issue 2
  • DOI: 10.1039/c0mt00061b

The NRAMP6 metal transporter contributes to cadmium toxicity
journal, August 2009

  • Cailliatte, Rémy; Lapeyre, Bruno; Briat, Jean-François
  • Biochemical Journal, Vol. 422, Issue 2
  • DOI: 10.1042/bj20090655

miR408 is involved in abiotic stress responses in Arabidopsis
journal, October 2015

  • Ma, Chao; Burd, Shaul; Lers, Amnon
  • The Plant Journal, Vol. 84, Issue 1
  • DOI: 10.1111/tpj.12999

Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: An overview
journal, April 2013

  • Garg, N.; Bhandari, P.
  • Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, Vol. 148, Issue 4
  • DOI: 10.1080/11263504.2013.788096

Evolution and function of phytochelatin synthases
journal, February 2006


The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana
journal, January 2013

  • Gayomba, Sheena R.; Jung, Ha-il; Yan, Jiapei
  • Metallomics, Vol. 5, Issue 9
  • DOI: 10.1039/c3mt00111c

Mechanisms of metal toxicity in plants
journal, January 2016


Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants
journal, December 2014


MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives
journal, August 2013


The American cranberry: first insights into the whole genome of a species adapted to bog habitat
journal, January 2014


Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium
journal, July 2012

  • Zhou, Zhao Sheng; Song, Jian Bo; Yang, Zhi Min
  • Journal of Experimental Botany, Vol. 63, Issue 12
  • DOI: 10.1093/jxb/ers136

Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa)
journal, March 2011

  • Ding, Yanfei; Chen, Zhen; Zhu, Cheng
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err046

DNA repair systems as targets of cadmium toxicity
journal, June 2006

  • Giaginis, Constantinos; Gatzidou, Elisavet; Theocharis, Stamatios
  • Toxicology and Applied Pharmacology, Vol. 213, Issue 3
  • DOI: 10.1016/j.taap.2006.03.008

Genome-wide identification of rice class I metallothionein gene: tissue expression patterns and induction in response to heavy metal stress
journal, October 2012

  • Gautam, Neelam; Verma, Pankaj Kumar; Verma, Shikha
  • Functional & Integrative Genomics, Vol. 12, Issue 4
  • DOI: 10.1007/s10142-012-0297-9

Copper homeostasis: Tansley review
journal, April 2009


The biochemistry of environmental heavy metal uptake by plants: Implications for the food chain
journal, August 2009

  • Peralta-Videa, Jose R.; Lopez, Martha Laura; Narayan, Mahesh
  • The International Journal of Biochemistry & Cell Biology, Vol. 41, Issue 8-9
  • DOI: 10.1016/j.biocel.2009.03.005