Plant genotype and rhizobia strain combinations strongly influence the transcriptome under heavy metal stress conditions in Medicago truncatula

Sharma, Reena; Chakraborty, Sanhita; Bhat, Aditi; Clear, Michael; Xie, Meng; Pueyo, José J.; Paape, Timothy

doi:10.1016/j.stress.2025.100854

Plant genotype and rhizobia strain combinations strongly influence the transcriptome under heavy metal stress conditions in Medicago truncatula

Journal Article · Fri Apr 11 00:00:00 EDT 2025 · Plant Stress

DOI:https://doi.org/10.1016/j.stress.2025.100854· OSTI ID:2560730

Sharma, Reena ^[1]; Chakraborty, Sanhita ^[2]; Bhat, Aditi ^[1]; Clear, Michael ^[1]; ^[1]; Pueyo, José J. ^[3]; ^[4]

Brookhaven National Laboratory (BNL), Upton, NY (United States)
Texas A & M Univ., College Station, TX (United States)
Institute of Agricultural Sciences, Madrid (Spain); Consejo Superior de Investigaciones Cientificas (CSIC), Madrid (Spain)
Texas A & M Univ., College Station, TX (United States); US Department of Agriculture (USDA), College Station, TX (United States)

Heavy metals such as cadmium (Cd) and mercury (Hg) pose significant threats to plant health and food safety as they are absorbed from the environment. Legumes are generally considered sensitive to heavy metals but possess standing genetic variation for accumulation and tolerance to toxic ions. We conducted a transcriptomic analysis on hydroponically and soil grown Medicago truncatula plants to investigate gene expression responses to Cd and Hg exposure in roots, leaves, and nodules. By using plant genotypes with varying metal tolerance or accumulation levels, we observed distinct clustering of gene ontologies, indicating tissue-specific, genotype-specific, and metal-specific gene expression patterns. Considering the symbiotic relationship between legumes and nitrogen-fixing bacteria, we further examined plant phenotypes and transcriptomes of plant genotypes with contrasting Hg accumulation levels and inoculated them with high or low Hg-tolerant Sinorhizobium medicae strains that have presence-absence variation for a mercury reductase (Mer) operon. Host plants inoculated with the Hg-tolerant rhizobia strain possessing a Mer operon exhibited less reduction in nodule number and plant biomass. A smaller reduction in iron (Fe) distribution in nodules after Hg stress was measured using X-ray Fluorescence (XRF) imaging. Dual transcriptome (host plant and bacteria) analysis of nodules revealed a remarkable decrease in the number of differentially expressed genes (DEGs) and clustering of gene ontologies in plants inoculated with the Hg-tolerant rhizobia strain, including symbiosis related genes. This finding suggests that the Hg-tolerant rhizobia strain has the potential to mitigate Hg stress in host plants. Furthermore, we observed genotype by-genotype interactions between the high Hg accumulating plant genotype and the Hg-tolerant rhizobia strain. These findings provide insights into enhancing plant resilience in contaminated environments through optimizing legume-rhizobia interactions for heavy metal tolerance.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0012704

OSTI ID:: 2560730

Report Number(s):: BNL--228033-2025-JAAM

Journal Information:: Plant Stress, Journal Name: Plant Stress Vol. 16; ISSN 2667-064X

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Heavy Metal Toxicity and the Environment Tchounwou, Paul B.; Yedjou, Clement G.; Patlolla, Anita K. Experientia Supplementum https://doi.org/10.1007/978-3-7643-8340-4_6	book	January 2012
Duckweed: a potential phytosensor for heavy metals Sharma, Reena; Lenaghan, Scott C. Plant Cell Reports, Vol. 41, Issue 12 https://doi.org/10.1007/s00299-022-02913-7	journal	August 2022
Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils Nonnoi, Francesca; Chinnaswamy, Appunu; García de la Torre, Vanesa S. Applied Soil Ecology, Vol. 61 https://doi.org/10.1016/j.apsoil.2012.06.004	journal	October 2012
The biochemistry of environmental heavy metal uptake by plants: Implications for the food chain Peralta-Videa, Jose R.; Lopez, Martha Laura; Narayan, Mahesh The International Journal of Biochemistry & Cell Biology, Vol. 41, Issue 8-9 https://doi.org/10.1016/j.biocel.2009.03.005	journal	August 2009
Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants Clemens, S. Biochimie, Vol. 88, Issue 11 https://doi.org/10.1016/j.biochi.2006.07.003	journal	November 2006
Light-sensitive short hypocotyl genes confer symbiotic nodule identity in the legume Medicago truncatula Lee, Tak; Orvosova, Martina; Batzenschlager, Morgane Current Biology, Vol. 34, Issue 4 https://doi.org/10.1016/j.cub.2024.01.018	journal	February 2024
Cadmium-tolerant bacteria reduce the uptake of cadmium in rice: Potential for microbial bioremediation Siripornadulsil, Surasak; Siripornadulsil, Wilailak Ecotoxicology and Environmental Safety, Vol. 94 https://doi.org/10.1016/j.ecoenv.2013.05.002	journal	August 2013
Rapid screening of Medicago truncatula germplasm for mercury tolerance at the seedling stage García de la Torre, Vanesa S.; Coba de la Peña, Teodoro; Lucas, M. Mercedes Environmental and Experimental Botany, Vol. 91 https://doi.org/10.1016/j.envexpbot.2013.03.004	journal	July 2013
Heavy metals in food crops: Health risks, fate, mechanisms, and management Rai, Prabhat Kumar; Lee, Sang Soo; Zhang, Ming Environment International, Vol. 125 https://doi.org/10.1016/j.envint.2019.01.067	journal	April 2019
Metal tolerance mechanisms in plants and microbe-mediated bioremediation Narayanan, Mathiyazhagan; Ma, Ying Environmental Research, Vol. 222 https://doi.org/10.1016/j.envres.2023.115413	journal	April 2023
Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants Yadav, S. K. South African Journal of Botany, Vol. 76, Issue 2 https://doi.org/10.1016/j.sajb.2009.10.007	journal	April 2010
Whole-genome landscape of Medicago truncatula symbiotic genes Pecrix, Yann; Staton, S. Evan; Sallet, Erika Nature Plants, Vol. 4, Issue 12 https://doi.org/10.1038/s41477-018-0286-7	journal	November 2018
A legume kinesin controls vacuole morphogenesis for rhizobia endosymbiosis Zhang, Xiaxia; Wang, Qi; Wu, Jingxia Nature Plants, Vol. 8, Issue 11 https://doi.org/10.1038/s41477-022-01261-4	journal	October 2022
Iron distribution through the developmental stages of Medicago truncatula nodules Rodríguez-Haas, Benjamín; Finney, Lydia; Vogt, Stefan Metallomics, Vol. 5, Issue 9 https://doi.org/10.1039/c3mt00060e	journal	January 2013
Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula Branca, A.; Paape, T. D.; Zhou, P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 42 https://doi.org/10.1073/pnas.1104032108	journal	September 2011
Optimizing Rhizobium- legume symbioses by simultaneous measurement of rhizobial competitiveness and N ₂ fixation in nodules Mendoza-Suárez, Marcela A.; Geddes, Barney A.; Sánchez-Cañizares, Carmen Proceedings of the National Academy of Sciences, Vol. 117, Issue 18 https://doi.org/10.1073/pnas.1921225117	journal	April 2020
Heavy Metal Detoxification in Plants: Phytochelatin Biosynthesis and Function Cobbett, Christopher S. IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Vol. 51, Issue 3 https://doi.org/10.1080/152165401753544250	journal	March 2001
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis Brunetti, Patrizia; Zanella, Letizia; De Paolis, Angelo Journal of Experimental Botany, Vol. 66, Issue 13 https://doi.org/10.1093/jxb/erv185	journal	April 2015
Conserved but Attenuated Parental Gene Expression in Allopolyploids: Constitutive Zinc Hyperaccumulation in the Allotetraploid Arabidopsis kamchatica Paape, Timothy; Hatakeyama, Masaomi; Shimizu-Inatsugi, Rie Molecular Biology and Evolution, Vol. 33, Issue 11 https://doi.org/10.1093/molbev/msw141	journal	July 2016
2021 update on ATP-binding cassette (ABC) transporters: how they meet the needs of plants Do, Thanh Ha Thi; Martinoia, Enrico; Lee, Youngsook Plant Physiology, Vol. 187, Issue 4 https://doi.org/10.1093/plphys/kiab193	journal	May 2021
Salt Stress Enhances Early Symbiotic Gene Expression in Medicago truncatula and Induces a Stress-Specific Set of Rhizobium-Responsive Genes Chakraborty, Sanhita; Driscoll, Heather E.; Abrahante, Juan E. Molecular Plant-Microbe Interactions®, Vol. 34, Issue 8 https://doi.org/10.1094/MPMI-01-21-0019-R	journal	August 2021
At the crossroads of salinity and rhizobium-legume symbiosis Chakraborty, Sanhita; Harris, Jeanne Marie Molecular Plant-Microbe Interactions® https://doi.org/10.1094/MPMI-09-21-0231-FI	journal	March 2022
The Signal Peptide of the Medicago truncatula Modular Nodulin MtNOD25 Operates as an Address Label for the Specific Targeting of Proteins to Nitrogen-Fixing Symbiosomes Hohnjec, Natalija; Lenz, Frauke; Fehlberg, Vera Molecular Plant-Microbe Interactions®, Vol. 22, Issue 1 https://doi.org/10.1094/MPMI-22-1-0063	journal	January 2009
Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont Batstone, Rebecca T.; Burghardt, Liana T.; Heath, Katy D. Proceedings of the Royal Society B: Biological Sciences, Vol. 289, Issue 1978 https://doi.org/10.1098/rspb.2022.0477	journal	July 2022
Functional Association of Arabidopsis CAX1 and CAX3 Is Required for Normal Growth and Ion Homeostasis Cheng, Ning-Hui; Pittman, Jon K.; Shigaki, Toshiro Plant Physiology, Vol. 138, Issue 4 https://doi.org/10.1104/pp.105.061218	journal	July 2005
A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis Jardinaud, Marie-Françoise; Boivin, Stéphane; Rodde, Nathalie Plant Physiology, Vol. 171, Issue 3 https://doi.org/10.1104/pp.16.00711	journal	May 2016
An Iron-Activated Citrate Transporter, MtMATE67, Is Required for Symbiotic Nitrogen Fixation Kryvoruchko, Igor S.; Routray, Pratyush; Sinharoy, Senjuti Plant Physiology, Vol. 176, Issue 3 https://doi.org/10.1104/pp.17.01538	journal	December 2017
Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation Roy, Sonali; Liu, Wei; Nandety, Raja Sekhar The Plant Cell, Vol. 32, Issue 1 https://doi.org/10.1105/tpc.19.00279	journal	October 2019
The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury Park, Jiyoung; Song, Won‐Yong; Ko, Donghwi The Plant Journal, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04789.x	journal	October 2011
Medicago truncatula Ferroportin2 mediates iron import into nodule symbiosomes Escudero, Viviana; Abreu, Isidro; Tejada‐Jiménez, Manuel New Phytologist, Vol. 228, Issue 1 https://doi.org/10.1111/nph.16642	journal	May 2020
Forging a symbiosis: transition metal delivery in symbiotic nitrogen fixation González‐Guerrero, Manuel; Navarro‐Gómez, Cristina; Rosa‐Núñez, Elena New Phytologist, Vol. 239, Issue 6 https://doi.org/10.1111/nph.19098	journal	June 2023
Transcriptome Response to Heavy Metals in Sinorhizobium meliloti CCNWSX0020 Reveals New Metal Resistance Determinants That Also Promote Bioremediation by Medicago lupulina in Metal-Contaminated Soil Lu, Mingmei; Jiao, Shuo; Gao, Enting Applied and Environmental Microbiology, Vol. 83, Issue 20 https://doi.org/10.1128/AEM.01244-17	journal	October 2017
The UDP-Glycosyltransferase (UGT) Superfamily: New Members, New Functions, and Novel Paradigms Meech, Robyn; Hu, Dong Gui; McKinnon, Ross A. Physiological Reviews, Vol. 99, Issue 2 https://doi.org/10.1152/physrev.00058.2017	journal	April 2019
Molecular Mechanism of Heavy Metal Toxicity and Tolerance in Plants: Central Role of Glutathione in Detoxification of Reactive Oxygen Species and Methylglyoxal and in Heavy Metal Chelation Hossain, Mohammad Anwar; Piyatida, Pukclai; da Silva, Jaime A. Teixeira Journal of Botany, Vol. 2012 https://doi.org/10.1155/2012/872875	journal	April 2012
A scaling normalization method for differential expression analysis of RNA-seq data Robinson, Mark D.; Oshlack, Alicia Genome Biology, Vol. 11, Issue 3, Article No. R25 https://doi.org/10.1186/gb-2010-11-3-r25	journal	March 2010
Horizontal gene transfer of the Mer operon is associated with large effects on the transcriptome and increased tolerance to mercury in nitrogen-fixing bacteria Bhat, Aditi; Sharma, Reena; Desigan, Kumaran BMC Microbiology, Vol. 24, Issue 1 https://doi.org/10.1186/s12866-024-03391-5	journal	July 2024
The UDP-glucose: glycoprotein glucosyltransferase (UGGT), a key enzyme in ER quality control, plays a significant role in plant growth as well as biotic and abiotic stress in Arabidopsis thaliana Blanco-Herrera, Francisca; Moreno, Adrián A.; Tapia, Rodrigo BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0525-2	journal	May 2015
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Plant ABC Transporters Kang, Joohyun; Park, Jiyoung; Choi, Hyunju The Arabidopsis Book, Vol. 9 https://doi.org/10.1199/tab.0153	journal	January 2011
The Five AhMTP1 Zinc Transporters Undergo Different Evolutionary Fates towards Adaptive Evolution to Zinc Tolerance in Arabidopsis halleri Shahzad, Zaigham; Gosti, Françoise; Frérot, Hélène PLoS Genetics, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pgen.1000911	journal	April 2010
Genome-Wide Association Studies Identify Heavy Metal ATPase3 as the Primary Determinant of Natural Variation in Leaf Cadmium in Arabidopsis thaliana Chao, Dai-Yin; Silva, Adriano; Baxter, Ivan PLoS Genetics, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pgen.1002923	journal	September 2012
Mutualism and Adaptive Divergence: Co-Invasion of a Heterogeneous Grassland by an Exotic Legume-Rhizobium Symbiosis Porter, Stephanie S.; Stanton, Maureen L.; Rice, Kevin J. PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0027935	journal	December 2011
Candidate Genes and Genetic Architecture of Symbiotic and Agronomic Traits Revealed by Whole-Genome, Sequence-Based Association Genetics in Medicago truncatula Stanton-Geddes, John; Paape, Timothy; Epstein, Brendan PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0065688	journal	May 2013
ATP binding cassette transporters and uridine diphosphate glycosyltransferases are ancient protein families that evolved roles in herbicide resistance through exaptation Caygill, Samuel; Dolan, Liam PLOS ONE, Vol. 18, Issue 9 https://doi.org/10.1371/journal.pone.0287356	journal	September 2023
Genomic Signature of Adaptation to Climate in Medicago truncatula Yoder, Jeremy B.; Stanton-Geddes, John; Zhou, Peng Genetics, Vol. 196, Issue 4 https://doi.org/10.1534/genetics.113.159319	journal	January 2014
Microbial Diversity of Mer Operon Genes and Their Potential Rules in Mercury Bioremediation and Resistance Naguib, Martha M.; El-Gendy, Ahmed O.; Khairalla, Ahmed S. The Open Biotechnology Journal, Vol. 12, Issue 1 https://doi.org/10.2174/1874070701812010056	journal	April 2018
Genome-Wide Identification and Expression Analysis of Metal Tolerance Protein Gene Family in Medicago truncatula Under a Broad Range of Heavy Metal Stress El-Sappah, Ahmed H.; Elbaiomy, Rania G.; Elrys, Ahmed S. Frontiers in Genetics, Vol. 12 https://doi.org/10.3389/fgene.2021.713224	journal	September 2021
The Mercury Resistance Operon: From an Origin in a Geothermal Environment to an Efficient Detoxification Machine Boyd, Eric S.; Barkay, Tamar Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00349	journal	January 2012
Phyto-microbiome to mitigate abiotic stress in crop plants Singh, Anamika; Mazahar, Samina; Chapadgaonkar, Shilpa Samir Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1210890	journal	August 2023
Iron: an essential micronutrient for the legume-rhizobium symbiosis Brear, Ella M.; Day, David A.; Smith, Penelope M. C. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00359	journal	January 2013
Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics Singh, Samiksha; Parihar, Parul; Singh, Rachana Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01143	journal	February 2016
Transition Metal Transport in Plants and Associated Endosymbionts: Arbuscular Mycorrhizal Fungi and Rhizobia González-Guerrero, Manuel; Escudero, Viviana; Saéz, Ángela Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01088	journal	July 2016
Glutathione S-Transferases: Role in Combating Abiotic Stresses Including Arsenic Detoxification in Plants Kumar, Smita; Trivedi, Prabodh K. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00751	journal	June 2018
MtMTP2-Facilitated Zinc Transport Into Intracellular Compartments Is Essential for Nodule Development in Medicago truncatula León-Mediavilla, Javier; Senovilla, Marta; Montiel, Jesús Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00990	journal	July 2018
Distinctive Patterns of Flavonoid Biosynthesis in Roots and Nodules of Datisca glomerata and Medicago spp. Revealed by Metabolomic and Gene Expression Profiles Gifford, Isaac; Battenberg, Kai; Vaniya, Arpana Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01463	journal	October 2018
Nicotianamine Synthase 2 Is Required for Symbiotic Nitrogen Fixation in Medicago truncatula Nodules Escudero, Viviana; Abreu, Isidro; del Sastre, Eric Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01780	journal	January 2020
Mercury-Tolerant Ensifer medicae Strains Display High Mercuric Reductase Activity and a Protective Effect on Nitrogen Fixation in Medicago truncatula Nodules Under Mercury Stress Arregui, Gabriela; Hipólito, Pablo; Pallol, Beatriz Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.560768	journal	January 2021
Cadmium-Tolerant and -Sensitive Cultivars Identified by Screening of Medicago truncatula Germplasm Display Contrasting Responses to Cadmium Stress García de la Torre, Vanesa S.; Coba de la Peña, Teodoro; Pueyo, José J. Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.595001	journal	March 2021
The Rhizobium-Legume Symbiosis: Co-opting Successful Stress Management Hawkins, Justin P.; Oresnik, Ivan J. Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.796045	journal	January 2022
Genome-Wide Association Study Reveals Complex Genetic Architecture of Cadmium and Mercury Accumulation and Tolerance Traits in Medicago truncatula Paape, Timothy; Heiniger, Benjamin; Santo Domingo, Miguel Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.806949	journal	January 2022
Flavonoid Accumulation Varies in Medicago truncatula in Response to Mercury Stress Alvarez-Rivera, Gerardo; Sanz, Aurora; Cifuentes, Alejandro Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.933209	journal	July 2022
Abiotic Stress and Reactive Oxygen Species: Generation, Signaling, and Defense Mechanisms Sachdev, Swati; Ansari, Shamim Akhtar; Ansari, Mohammad Israil Antioxidants, Vol. 10, Issue 2 https://doi.org/10.3390/antiox10020277	journal	February 2021
Harnessing Rhizobia to Improve Heavy-Metal Phytoremediation by Legumes Fagorzi, Camilla; Checcucci, Alice; diCenzo, George Genes, Vol. 9, Issue 11 https://doi.org/10.3390/genes9110542	journal	November 2018
Molecular Mechanisms of Metal Toxicity and Plant Tolerance Moustakas, Michael International Journal of Molecular Sciences, Vol. 24, Issue 9 https://doi.org/10.3390/ijms24097810	journal	April 2023
The Anatomical Basis of Heavy Metal Responses in Legumes and Their Impact on Plant–Rhizosphere Interactions Pandey, Arun K.; Zorić, Lana; Sun, Ting Plants, Vol. 11, Issue 19 https://doi.org/10.3390/plants11192554	journal	September 2022
Heavy Metal Induced Oxidative Stress Mitigation and ROS Scavenging in Plants Mansoor, Sheikh; Ali, Asif; Kour, Navneet Plants, Vol. 12, Issue 16 https://doi.org/10.3390/plants12163003	journal	August 2023
Heavy Metals and Pesticides Toxicity in Agricultural Soil and Plants: Ecological Risks and Human Health Implications Alengebawy, Ahmed; Abdelkhalek, Sara Taha; Qureshi, Sundas Rana Toxics, Vol. 9, Issue 3 https://doi.org/10.3390/toxics9030042	journal	February 2021

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59 BASIC BIOLOGICAL SCIENCES
Abiotic stress
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Medicago truncatula
Nodules
Sinorhizobium medicae
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Plant genotype and rhizobia strain combinations strongly influence the transcriptome under heavy metal stress conditions in Medicago truncatula

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