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 »
- Authors:
-
- Univ. of Turin (Italy). Dept. of Life Sciences and Systems Biology
- 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)
- 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)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- 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 Laboratory (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. doi: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 = {Mon Mar 09 00:00:00 EDT 2020},
month = {Mon Mar 09 00:00:00 EDT 2020}
}
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Works referenced in this record:
Identification and Comparative Analysis of Cadmium Tolerance-Associated miRNAs and Their Targets in Two Soybean Genotypes
journal, December 2013
- Fang, Xiaolong; Zhao, Yunyun; Ma, Qibin
- PLoS ONE, Vol. 8, Issue 12
Response to cadmium in higher plants
journal, April 1999
- Sanità di Toppi, L.; Gabbrielli, R.
- Environmental and Experimental Botany, Vol. 41, Issue 2
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
Origin, Biogenesis, and Activity of Plant MicroRNAs
journal, February 2009
- Voinnet, Olivier
- Cell, Vol. 136, Issue 4
Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review)
journal, November 2006
- Bertin, G.; Averbeck, D.
- Biochimie, Vol. 88, Issue 11
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
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
Biogenesis, Turnover, and Mode of Action of Plant MicroRNAs
journal, July 2013
- Rogers, K.; Chen, X.
- The Plant Cell, Vol. 25, Issue 7
Genome-wide analysis of thiourea-modulated salinity stress-responsive transcripts in seeds of Brassica juncea: identification of signalling and effector components of stress tolerance
journal, August 2010
- Srivastava, A. K.; Ramaswamy, N. K.; Suprasanna, P.
- Annals of Botany, Vol. 106, Issue 5
Model systems to unravel the molecular mechanisms of heavy metal tolerance in the ericoid mycorrhizal symbiosis
journal, December 2015
- Daghino, Stefania; Martino, Elena; Perotto, Silvia
- Mycorrhiza, Vol. 26, Issue 4
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
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
Structural Biology of the Major Facilitator Superfamily Transporters
journal, June 2015
- Yan, Nieng
- Annual Review of Biophysics, Vol. 44, Issue 1
Phytochelatins and Their Roles in Heavy Metal Detoxification
journal, July 2000
- Cobbett, Christopher S.
- Plant Physiology, Vol. 123, Issue 3
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
Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice
journal, May 2012
- Sasaki, Akimasa; Yamaji, Naoki; Yokosho, Kengo
- The Plant Cell, Vol. 24, Issue 5
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
Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress
journal, June 2005
- Ouziad, Fouad; Hildebrandt, Ulrich; Schmelzer, Elmon
- Journal of Plant Physiology, Vol. 162, Issue 6
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
Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.)
journal, September 2013
- Pang, Kaiyuan; Li, Yanjiao; Liu, Menghan
- Gene, Vol. 526, Issue 2
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
Common and metal-specific proteomic responses to cadmium and zinc in the metal tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn
journal, January 2015
- Chiapello, M.; Martino, E.; Perotto, S.
- Metallomics, Vol. 7, Issue 5
The SlZRT1 Gene Encodes a Plasma Membrane-Located ZIP (Zrt-, Irt-Like Protein) Transporter in the Ectomycorrhizal Fungus Suillus luteus
journal, November 2017
- Coninx, Laura; Thoonen, Anneleen; Slenders, Eli
- Frontiers in Microbiology, Vol. 8
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
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
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
Yeast expression of mammalian Onzin and fungal FCR1 suggests ancestral functions of PLAC8 proteins in mitochondrial metabolism and DNA repair
journal, April 2019
- Daghino, Stefania; Di Vietro, Luigi; Petiti, Luca
- Scientific Reports, Vol. 9, Issue 1
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
The role of ectomycorrhizas in heavy metal stress tolerance of host plants
journal, December 2014
- Luo, Zhi-Bin; Wu, Chenhan; Zhang, Chao
- Environmental and Experimental Botany, Vol. 108
The Biology of Mycorrhiza in the Ericaceae. Viii. the role of Mycorrhizal Infection in Heavy Metal Resistance
journal, June 1982
- Bradley, R.; Burt, A. J.; Read, D. J.
- New Phytologist, Vol. 91, Issue 2
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004
- Apel, Klaus; Hirt, Heribert
- Annual Review of Plant Biology, Vol. 55, Issue 1
Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete Hebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis
journal, July 2015
- Doré, Jeanne; Perraud, Marie; Dieryckx, Cindy
- New Phytologist, Vol. 208, Issue 4
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
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
Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus
journal, October 2017
- Meng, Jin Guo; Zhang, Xian Duo; Tan, Shang Kun
- BioMetals, Vol. 30, Issue 6
Arbuscular mycorrhizal fungus modulates the phytotoxicity of Cd via combined responses of enzymes, thiolic compounds, and essential elements in the roots of Phragmites australis
journal, November 2017
- Huang, Xiaochen; Wang, Li; Ma, Fang
- Chemosphere, Vol. 187
The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s)
journal, November 2010
- Turlapati, Phanikanth V.; Kim, Kye-Won; Davin, Laurence B.
- Planta, Vol. 233, Issue 3
The Oligopeptide Transporters: A Small Gene Family with a Diverse Group of Substrates and Functions?
journal, May 2011
- Lubkowitz, Mark
- Molecular Plant, Vol. 4, Issue 3
Laccases Direct Lignification in the Discrete Secondary Cell Wall Domains of Protoxylem
journal, August 2014
- Schuetz, M.; Benske, A.; Smith, R. A.
- PLANT PHYSIOLOGY, Vol. 166, Issue 2
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
Parlez-vous effectors?: Editorial
journal, August 2010
- Martin, Francis
- New Phytologist, Vol. 187, Issue 4
Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc
journal, September 1994
- Patra, Jita; Lenka, Maheswar; Panda, Brahma B.
- New Phytologist, Vol. 128, Issue 1
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
Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants
journal, November 2006
- Clemens, S.
- Biochimie, Vol. 88, Issue 11
P HYTOCHELATINS AND M ETALLOTHIONEINS : Roles in Heavy Metal Detoxification and Homeostasis
journal, June 2002
- Cobbett, Christopher; Goldsbrough, Peter
- Annual Review of Plant Biology, Vol. 53, Issue 1
Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants
journal, June 2004
- Pinto, A.; Mota, A.; Devarennes, A.
- Science of The Total Environment, Vol. 326, Issue 1-3
The Structure and Function of the Ericoid Mycorrhizal Root
journal, April 1996
- Read, D.
- Annals of Botany, Vol. 77, Issue 4
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
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
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
Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions
journal, December 2003
- Cairney, J. W. G.; Meharg, A. A.
- European Journal of Soil Science, Vol. 54, Issue 4
A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: Ligninolytic enzyme regulation in Pleurotus ostreatus
journal, November 2017
- Feldman, Daria; Kowbel, David J.; Glass, N. Louise
- Scientific Reports, Vol. 7, Issue 1
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
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
microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis: Post-transcriptional control of superoxide dismutases
journal, February 2010
- Beauclair, Linda; Yu, Agnès; Bouché, Nicolas
- The Plant Journal, Vol. 62, Issue 3
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
Evolution and function of phytochelatin synthases
journal, February 2006
- Clemens, Stephan
- Journal of Plant Physiology, Vol. 163, Issue 3
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance
journal, July 2006
- Sunkar, Ramanjulu; Kapoor, Avnish; Zhu, Jian-Kang
- The Plant Cell, Vol. 18, Issue 8
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
Mechanisms of metal toxicity in plants
journal, January 2016
- Küpper, Hendrik; Andresen, Elisa
- Metallomics, Vol. 8, Issue 3
Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants
journal, December 2014
- Das, Kaushik; Roychoudhury, Aryadeep
- Frontiers in Environmental Science, Vol. 2
MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives
journal, August 2013
- Gupta, O. P.; Sharma, P.; Gupta, R. K.
- Plant Molecular Biology, Vol. 84, Issue 1-2
The American cranberry: first insights into the whole genome of a species adapted to bog habitat
journal, January 2014
- Polashock, James; Zelzion, Ehud; Fajardo, Diego
- BMC Plant Biology, Vol. 14, Issue 1
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
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
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
Analysis and characterization of cultivable extremophilic hydrolytic bacterial community in heavy-metal-contaminated soils from the Atacama Desert and their biotechnological potentials
journal, July 2012
- Moreno, M. L.; Piubeli, F.; Bonfá, M. R. L.
- Journal of Applied Microbiology, Vol. 113, Issue 3
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
Ericoid mycorrhizal fungi from heavy metal polluted soils: their identification and growth in the presence of zinc ions
journal, March 2000
- Martino, Elena; Turnau, Katarzyna; Girlanda, Mariangela
- Mycological Research, Vol. 104, Issue 3
Copper homeostasis: Tansley review
journal, April 2009
- Burkhead, Jason L.; Gogolin Reynolds, Kathryn A.; Abdel-Ghany, Salah E.
- New Phytologist, Vol. 182, Issue 4
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
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
The Structure and Function of the Ericoid Mycorrhizal Root
journal, April 1996
- Read, D.
- Annals of Botany, Vol. 77, Issue 4
The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s)
journal, November 2010
- Turlapati, Phanikanth V.; Kim, Kye-Won; Davin, Laurence B.
- Planta, Vol. 233, Issue 3
Model systems to unravel the molecular mechanisms of heavy metal tolerance in the ericoid mycorrhizal symbiosis
journal, December 2015
- Daghino, Stefania; Martino, Elena; Perotto, Silvia
- Mycorrhiza, Vol. 26, Issue 4
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
Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus
journal, October 2017
- Meng, Jin Guo; Zhang, Xian Duo; Tan, Shang Kun
- BioMetals, Vol. 30, Issue 6
MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives
journal, August 2013
- Gupta, O. P.; Sharma, P.; Gupta, R. K.
- Plant Molecular Biology, Vol. 84, Issue 1-2
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
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
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
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
Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants
journal, November 2006
- Clemens, S.
- Biochimie, Vol. 88, Issue 11
Origin, Biogenesis, and Activity of Plant MicroRNAs
journal, February 2009
- Voinnet, Olivier
- Cell, Vol. 136, Issue 4
Arbuscular mycorrhizal fungus modulates the phytotoxicity of Cd via combined responses of enzymes, thiolic compounds, and essential elements in the roots of Phragmites australis
journal, November 2017
- Huang, Xiaochen; Wang, Li; Ma, Fang
- Chemosphere, Vol. 187
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
The role of ectomycorrhizas in heavy metal stress tolerance of host plants
journal, December 2014
- Luo, Zhi-Bin; Wu, Chenhan; Zhang, Chao
- Environmental and Experimental Botany, Vol. 108
Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress
journal, June 2005
- Ouziad, Fouad; Hildebrandt, Ulrich; Schmelzer, Elmon
- Journal of Plant Physiology, Vol. 162, Issue 6
Evolution and function of phytochelatin synthases
journal, February 2006
- Clemens, Stephan
- Journal of Plant Physiology, Vol. 163, Issue 3
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
Response to cadmium in higher plants
journal, April 1999
- Sanità di Toppi, L.; Gabbrielli, R.
- Environmental and Experimental Botany, Vol. 41, Issue 2
Ericoid mycorrhizal fungi from heavy metal polluted soils: their identification and growth in the presence of zinc ions
journal, March 2000
- Martino, Elena; Turnau, Katarzyna; Girlanda, Mariangela
- Mycological Research, Vol. 104, Issue 3
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
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
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
A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: Ligninolytic enzyme regulation in Pleurotus ostreatus
journal, November 2017
- Feldman, Daria; Kowbel, David J.; Glass, N. Louise
- Scientific Reports, Vol. 7, Issue 1
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
Common and metal-specific proteomic responses to cadmium and zinc in the metal tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn
journal, January 2015
- Chiapello, M.; Martino, E.; Perotto, S.
- Metallomics, Vol. 7, Issue 5
Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions
journal, December 2003
- Cairney, J. W. G.; Meharg, A. A.
- European Journal of Soil Science, Vol. 54, Issue 4
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
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
Genome-wide analysis of thiourea-modulated salinity stress-responsive transcripts in seeds of Brassica juncea: identification of signalling and effector components of stress tolerance
journal, August 2010
- Srivastava, A. K.; Ramaswamy, N. K.; Suprasanna, P.
- Annals of Botany, Vol. 106, Issue 5
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
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
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
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
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
The Oligopeptide Transporters: A Small Gene Family with a Diverse Group of Substrates and Functions?
journal, May 2011
- Lubkowitz, Mark
- Molecular Plant, Vol. 4, Issue 3
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
Laccases Direct Lignification in the Discrete Secondary Cell Wall Domains of Protoxylem
journal, August 2014
- Schuetz, M.; Benske, A.; Smith, R. A.
- PLANT PHYSIOLOGY, Vol. 166, Issue 2
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance
journal, July 2006
- Sunkar, Ramanjulu; Kapoor, Avnish; Zhu, Jian-Kang
- The Plant Cell, Vol. 18, Issue 8
Biogenesis, Turnover, and Mode of Action of Plant MicroRNAs
journal, July 2013
- Rogers, K.; Chen, X.
- The Plant Cell, Vol. 25, Issue 7
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
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
Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc
journal, September 1994
- Patra, Jita; Lenka, Maheswar; Panda, Brahma B.
- New Phytologist, Vol. 128, Issue 1
Copper homeostasis: Tansley review
journal, April 2009
- Burkhead, Jason L.; Gogolin Reynolds, Kathryn A.; Abdel-Ghany, Salah E.
- New Phytologist, Vol. 182, Issue 4
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
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
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
journal, June 2004
- Apel, Klaus; Hirt, Heribert
- Annual Review of Plant Biology, Vol. 55, Issue 1
The American cranberry: first insights into the whole genome of a species adapted to bog habitat
journal, January 2014
- Polashock, James; Zelzion, Ehud; Fajardo, Diego
- BMC Plant Biology, Vol. 14, Issue 1
Identification and Comparative Analysis of Cadmium Tolerance-Associated miRNAs and Their Targets in Two Soybean Genotypes
journal, December 2013
- Fang, Xiaolong; Zhao, Yunyun; Ma, Qibin
- PLoS ONE, Vol. 8, Issue 12
Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants
journal, December 2014
- Das, Kaushik; Roychoudhury, Aryadeep
- Frontiers in Environmental Science, Vol. 2
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