Serendipita indica Drives Sulfur-Related Microbiota in Enhancing Growth of Hyperaccumulator Sedum alfredii and Facilitating Soil Cadmium Remediation

Qiao, Yabei; Lin, Zhi; Li, Luxi; Jiang, Wei; Ge, Jun; Chen, Jiuzhou; Lu, Lingli; Tian, Shengke

doi:10.1021/acs.est.4c01418

Serendipita indica Drives Sulfur-Related Microbiota in Enhancing Growth of Hyperaccumulator Sedum alfredii and Facilitating Soil Cadmium Remediation

Journal Article · Thu Aug 08 00:00:00 EDT 2024 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.4c01418· OSTI ID:2567003

Qiao, Yabei ^[1]; Lin, Zhi ^[1]; Li, Luxi ^[2]; Jiang, Wei ^[3]; Ge, Jun ^[1]; Chen, Jiuzhou ^[1]; Lu, Lingli ^[1]; ^[1]

Zhejiang Univ., Hangzhou (China)
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Xianghu Laboratory, Hangzhou (China)

Endophytic fungus Serendipita indica can bolster plant growth and confer protection against various biotic and abiotic stresses. However, S. indica -reshaped rhizosphere microecology interactions and root-soil interface processes in situ at the submicrometer scale remain poorly understood. Here, we combined amplicon sequencing and high-resolution nano X-ray fluorescence (nano-XRF) imaging of the root-soil interface to reveal cadmium (Cd) rhizosphere processes. S. indica can successfully colonize the roots of Sedum alfredii Hance, which induces a remarkable increase in shoot biomass by 211.32% and Cd accumulation by 235.72%. Nano-XRF images showed that S. indica colonization altered the Cd distribution in the rhizosphere and facilitated the proximity of more Cd and sulfur (S) to enter the roots and transport to the shoot. Furthermore, the rhizosphere-enriched microbiota demonstrated a more stable network structure after the S. indica inoculation. Keystone species were strongly associated with growth promotion and Cd absorption. For example, Comamonadaceae are closely related to the organic acid cycle and S bioavailability, which could facilitate Cd and S accumulation in plants. Meanwhile, Sphingomonadaceae could release auxin and boost plant biomass. In summary, we construct a mutualism system for beneficial fungi and hyperaccumulation plants, which facilitates high-efficient remediation of Cd-contaminated soils by restructuring the rhizosphere microbiota.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Key Research and Development Program of China; National Natural Science Foundation of China (NSFC); Natural Science Foundation of Zhejiang Province; Science and Technology Department of Zhejiang Province; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2567003

Journal Information:: Environmental Science and Technology, Journal Name: Environmental Science and Technology Journal Issue: 33 Vol. 58; ISSN 1520-5851; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (114)

ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants: Growth promoting rhizobacteria from tropical rice Bal, Himadri Bhusan; Das, Subhasis; Dangar, Tushar K. Journal of Basic Microbiology, Vol. 53, Issue 12 https://doi.org/10.1002/jobm.201200445	journal	May 2013
Hypoproduction of erythropoietin contributes to anemia in chronic cadmium intoxication: clinical study on Itai-itai disease in Japan Horiguchi, Hyogo; Teranishi, Hidetoyo; Niiya, Kenji Archives of Toxicology, Vol. 68, Issue 10 https://doi.org/10.1007/BF03208342	journal	October 1994
Oxidation of Elemental Sulfur by Fusarium solani Strain THIF01 Harboring Endobacterium Bradyrhizobium sp. Li, Xian Shu; Sato, Tsutomu; Ooiwa, Yuji Microbial Ecology, Vol. 60, Issue 1 https://doi.org/10.1007/s00248-010-9699-1	journal	June 2010
Effect of endophytic fungus Piriformospora indica and PEG-induced water stress on maximum root growth pressure and elongation rate of maize Hosseini, Fatemeh; Mosaddeghi, Mohammad Reza; Dexter, Anthony Roger Plant and Soil, Vol. 435, Issue 1-2 https://doi.org/10.1007/s11104-018-03909-7	journal	December 2018
Changes in gas exchange, root growth, and biomass accumulation of Platycladus orientalis seedlings colonized by Serendipita indica Wu, Chu; Wei, Qiao; Deng, Jing Journal of Forestry Research, Vol. 30, Issue 4 https://doi.org/10.1007/s11676-018-0712-8	journal	June 2018
Soil beneficial bacteria and their role in plant growth promotion: a review Hayat, Rifat; Ali, Safdar; Amara, Ummay Annals of Microbiology, Vol. 60, Issue 4 https://doi.org/10.1007/s13213-010-0117-1	journal	August 2010
High concentrations of bioavailable heavy metals impact freshwater sediment microbial communities Ni, Caiying; Horton, Dean J.; Rui, Junpeng Annals of Microbiology, Vol. 66, Issue 3 https://doi.org/10.1007/s13213-015-1189-8	journal	December 2015
Piriformospora indica: A Novel Plant Growth-Promoting Mycorrhizal Fungus Varma, Ajit; Bakshi, Madhunita; Lou, Binggan Agricultural Research, Vol. 1, Issue 2 https://doi.org/10.1007/s40003-012-0019-5	journal	May 2012
A putative cyclin, SiPHO80 from root endophytic fungus Serendipita indica regulates phosphate homeostasis, salinity and heavy metal toxicity tolerance Loha, Anita; Kashyap, Arun Kumar; Sharma, Pooja Biochemical and Biophysical Research Communications, Vol. 507, Issue 1-4 https://doi.org/10.1016/j.bbrc.2018.11.053	journal	December 2018
Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils Ma, Y.; Prasad, M. N. V.; Rajkumar, M. Biotechnology Advances, Vol. 29, Issue 2 https://doi.org/10.1016/j.biotechadv.2010.12.001	journal	March 2011
Uptake and allocation of selected metals by dominant vegetation in Poyang Lake wetland: From rhizosphere to plant tissues Xu, Jinying; Zheng, Lilin; Xu, Ligang CATENA, Vol. 189 https://doi.org/10.1016/j.catena.2020.104477	journal	June 2020
Endophytic bacteria and their potential to enhance heavy metal phytoextraction Rajkumar, Mani; Ae, Noriharu; Freitas, Helena Chemosphere, Vol. 77, Issue 2 https://doi.org/10.1016/j.chemosphere.2009.06.047	journal	September 2009
Biomethylation and volatilization of arsenic by the marine microalgae Ostreococcus tauri Zhang, Si-Yu; Sun, Guo-Xin; Yin, Xi-Xiang Chemosphere, Vol. 93, Issue 1 https://doi.org/10.1016/j.chemosphere.2013.04.063	journal	September 2013
Effect of alkyl polyglucoside and nitrilotriacetic acid combined application on lead/pyrene bioavailability and dehydrogenase activity in co-contaminated soils Chen, Tingru; Liu, Xiaoyan; Zhang, Xinying Chemosphere, Vol. 154 https://doi.org/10.1016/j.chemosphere.2016.03.127	journal	July 2016
Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives Sarwar, Nadeem; Imran, Muhammad; Shaheen, Muhammad Rashid Chemosphere, Vol. 171 https://doi.org/10.1016/j.chemosphere.2016.12.116	journal	March 2017
Serpentine endophytic bacterium Pseudomonas azotoformans ASS1 accelerates phytoremediation of soil metals under drought stress Ma, Ying; Rajkumar, Mani; Moreno, António Chemosphere, Vol. 185 https://doi.org/10.1016/j.chemosphere.2017.06.135	journal	October 2017
Effects of endophytes inoculation on rhizosphere and endosphere microecology of Indian mustard (Brassica juncea) grown in vanadium-contaminated soil and its enhancement on phytoremediation Wang, Liang; Lin, Hai; Dong, Yingbo Chemosphere, Vol. 240 https://doi.org/10.1016/j.chemosphere.2019.124891	journal	February 2020
Endophyte Pseudomonas putida enhanced Trifolium repens L. growth and heavy metal uptake: A promising in-situ non-soil cover phytoremediation method of nonferrous metallic tailing Liu, Chenjing; Lin, Hai; Li, Bing Chemosphere, Vol. 272 https://doi.org/10.1016/j.chemosphere.2021.129816	journal	June 2021
Phytoremediation of cadmium-contaminated sediment using Hydrilla verticillata and Elodea canadensis harbor two same keystone rhizobacteria Pedosphaeraceae and Parasegetibacter Yuan, Qiusheng; Wang, Peifang; Wang, Xun Chemosphere, Vol. 286 https://doi.org/10.1016/j.chemosphere.2021.131648	journal	January 2022
Enhancing phytoremediation of soils polluted with heavy metals Gavrilescu, Maria Current Opinion in Biotechnology, Vol. 74 https://doi.org/10.1016/j.copbio.2021.10.024	journal	April 2022
Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity Shahabivand, Saleh; Parvaneh, Azar; Aliloo, Ali Asghar Ecotoxicology and Environmental Safety, Vol. 145 https://doi.org/10.1016/j.ecoenv.2017.07.064	journal	November 2017
Ecological responses of bacterial assembly and functions to steep Cd gradient in a typical Cd-contaminated farmland ecosystem Deng, Yan; Fu, Shaodong; Sarkodie, Emmannuel Konadu Ecotoxicology and Environmental Safety, Vol. 229 https://doi.org/10.1016/j.ecoenv.2021.113067	journal	January 2022
Phytoremediation: Mechanisms, plant selection and enhancement by natural and synthetic agents Kafle, Arjun; Timilsina, Anil; Gautam, Asmita Environmental Advances, Vol. 8 https://doi.org/10.1016/j.envadv.2022.100203	journal	July 2022
The Cd phytoextraction potential of hyperaccumulator Sedum alfredii-oilseed rape intercropping system under different soil types and comprehensive benefits evaluation under field conditions Cao, Xuerui; Wang, Xiaozi; Lu, Min Environmental Pollution, Vol. 285 https://doi.org/10.1016/j.envpol.2021.117504	journal	September 2021
Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica Zuccaro, Alga; Basiewicz, Magdalena; Zurawska, Magdalena Fungal Genetics and Biology, Vol. 46, Issue 8 https://doi.org/10.1016/j.fgb.2009.03.009	journal	August 2009
Effects of inoculation of biosurfactant-producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil Sheng, Xiafang; He, Linyan; Wang, Qingya Journal of Hazardous Materials, Vol. 155, Issue 1-2 https://doi.org/10.1016/j.jhazmat.2007.10.107	journal	June 2008
Bioremediation of Cd-DDT co-contaminated soil using the Cd-hyperaccumulator Sedum alfredii and DDT-degrading microbes Zhu, Zhi-qiang; Yang, Xiao-e; Wang, Kai Journal of Hazardous Materials, Vol. 235-236 https://doi.org/10.1016/j.jhazmat.2012.07.033	journal	October 2012
Effects of sulfur application on cadmium bioaccumulation in tobacco and its possible mechanisms of rhizospheric microorganisms Li, Xuanzhen; Yu, Hao; Sun, Xiaowei Journal of Hazardous Materials, Vol. 368 https://doi.org/10.1016/j.jhazmat.2018.12.099	journal	April 2019
Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review Riaz, Muhammad; Kamran, Muhammad; Fang, Yizeng Journal of Hazardous Materials, Vol. 402 https://doi.org/10.1016/j.jhazmat.2020.123919	journal	January 2021
Remediation of soils co-contaminated with cadmium and dichlorodiphenyltrichloroethanes by king grass associated with Piriformospora indica: Insights into the regulation of root excretion and reshaping of rhizosphere microbial community structure Li, Dong; Zheng, Xiaoxiao; Lin, Li Journal of Hazardous Materials, Vol. 422 https://doi.org/10.1016/j.jhazmat.2021.126936	journal	January 2022
Increase of P and Cd bioavailability in the rhizosphere by endophytes promoted phytoremediation efficiency of Phytolacca acinosa Liu, Chenjing; Lin, Hai; Dong, Yingbo Journal of Hazardous Materials, Vol. 431 https://doi.org/10.1016/j.jhazmat.2022.128546	journal	June 2022
Enhanced Cd efflux capacity and physiological stress resistance: The beneficial modulations of Metarhizium robertsii on plants under cadmium stress Jiang, Xiaohan; Dai, Jin; Zhang, Xing Journal of Hazardous Materials, Vol. 437 https://doi.org/10.1016/j.jhazmat.2022.129429	journal	September 2022
Challenges and opportunities for improving the environmental quality of cadmium-contaminated soil in China Yang, Jun; Hu, Ruqing; Zhao, Chen Journal of Hazardous Materials, Vol. 445 https://doi.org/10.1016/j.jhazmat.2022.130560	journal	March 2023
Piriformospora indica alter root-associated microbiome structure to enhance Artemisia annua L. tolerance to arsenic Rahman, Saeed ur; Khalid, Muhammad; Hui, Nan Journal of Hazardous Materials, Vol. 457 https://doi.org/10.1016/j.jhazmat.2023.131752	journal	September 2023
Piriformospora indica colonization enhances remediation of cadmium and chromium co-contaminated soils by king grass through plant growth promotion and rhizosphere microecological regulation Zhang, Kailu; Zhang, Haixiang; Xie, Can Journal of Hazardous Materials, Vol. 462 https://doi.org/10.1016/j.jhazmat.2023.132728	journal	January 2024
Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis Fesel, Philipp H.; Zuccaro, Alga Current Opinion in Microbiology, Vol. 32 https://doi.org/10.1016/j.mib.2016.05.008	journal	August 2016
Microbial eco-evolutionary dynamics in the plant rhizosphere Fields, Bryden; Friman, Ville-Petri Current Opinion in Microbiology, Vol. 68 https://doi.org/10.1016/j.mib.2022.102153	journal	August 2022
Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars Ji, Sang Hye; Gururani, Mayank Anand; Chun, Se-Chul Microbiological Research, Vol. 169, Issue 1 https://doi.org/10.1016/j.micres.2013.06.003	journal	January 2014
Application of random matrix theory to biological networks Luo, Feng; Zhong, Jianxin; Yang, Yunfeng Physics Letters A, Vol. 357, Issue 6 https://doi.org/10.1016/j.physleta.2006.04.076	journal	September 2006
Structural development and assembly patterns of the root-associated microbiomes during phytoremediation Chen, Yanmei; Ding, Qiaobei; Chao, Yuanqing Science of The Total Environment, Vol. 644 https://doi.org/10.1016/j.scitotenv.2018.07.095	journal	December 2018
Successive phytoextraction alters ammonia oxidation and associated microbial communities in heavy metal contaminated agricultural soils Luo, Jipeng; Liu, Yuying; Tao, Qi Science of The Total Environment, Vol. 664 https://doi.org/10.1016/j.scitotenv.2019.01.315	journal	May 2019
Soil application of manganese sulfate could reduce wheat Cd accumulation in Cd contaminated soil by the modulation of the key tissues and ionomic of wheat Wang, Yale; Xu, Yingming; Liang, Xuefeng Science of The Total Environment, Vol. 770 https://doi.org/10.1016/j.scitotenv.2021.145328	journal	May 2021
Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.) Belimov, A. A.; Hontzeas, N.; Safronova, V. I. Soil Biology and Biochemistry, Vol. 37, Issue 2 https://doi.org/10.1016/j.soilbio.2004.07.033	journal	February 2005
Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi Fomina, M. A.; Alexander, I. J.; Colpaert, J. V. Soil Biology and Biochemistry, Vol. 37, Issue 5 https://doi.org/10.1016/j.soilbio.2004.10.013	journal	May 2005
The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils Sessitsch, Angela; Kuffner, Melanie; Kidd, Petra Soil Biology and Biochemistry, Vol. 60 https://doi.org/10.1016/j.soilbio.2013.01.012	journal	May 2013
Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils Wood, Jennifer L.; Tang, Caixian; Franks, Ashley E. Soil Biology and Biochemistry, Vol. 103 https://doi.org/10.1016/j.soilbio.2016.08.021	journal	December 2016
Transformation of organic and inorganic sulfur– adding perspectives to new players in soil and rhizosphere Santana, Margarida M.; Dias, Teresa; Gonzalez, Juan M. Soil Biology and Biochemistry, Vol. 160 https://doi.org/10.1016/j.soilbio.2021.108306	journal	September 2021
Integrated Life Cycle Assessment for Sustainable Remediation of Contaminated Agricultural Soil in China Jin, Yuanliang; Wang, Liuwei; Song, Yinan Environmental Science & Technology, Vol. 55, Issue 17 https://doi.org/10.1021/acs.est.1c02535	journal	August 2021
Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance Luo, Jipeng; Gu, Shaohua; Guo, Xinyu Environmental Science & Technology, Vol. 56, Issue 18 https://doi.org/10.1021/acs.est.1c08832	journal	September 2022
Unique Rhizosphere Micro-characteristics Facilitate Phytoextraction of Multiple Metals in Soil by the Hyperaccumulating Plant Sedum alfredii Hou, Dandi; Wang, Kai; Liu, Ting Environmental Science & Technology, Vol. 51, Issue 10 https://doi.org/10.1021/acs.est.6b06531	journal	April 2017
Rhizosphere Bacteria Mobilize Zn for Hyperaccumulation by Thlaspi caerulescens Whiting, Steven N.; de Souza, Mark P.; Terry, Norman Environmental Science & Technology, Vol. 35, Issue 15 https://doi.org/10.1021/es001938v	journal	August 2001
Spatial Imaging and Speciation of Lead in the Accumulator Plant Sedum alfredii by Microscopically Focused Synchrotron X-ray Investigation Tian, Shengke; Lu, Lingli; Yang, Xiaoe Environmental Science & Technology, Vol. 44, Issue 15 https://doi.org/10.1021/es903921t	journal	August 2010
Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance) Yang, X. E.; Long, X. X.; Ye, H. B. Plant and Soil, Vol. 259, Issue 1/2 https://doi.org/10.1023/B:PLSO.0000020956.24027.f2	journal	February 2004
Crystal structure of a eukaryotic phosphate transporter Pedersen, Bjørn P.; Kumar, Hemant; Waight, Andrew B. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12042	journal	March 2013
How does multiple testing correction work? Noble, William S. Nature Biotechnology, Vol. 27, Issue 12 https://doi.org/10.1038/nbt1209-1135	journal	December 2009
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Erosion reduces soil microbial diversity, network complexity and multifunctionality Qiu, Liping; Zhang, Qian; Zhu, Hansong The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00913-1	journal	March 2021
Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion Wen, Tao; Yuan, Jun; He, Xiaoming Horticulture Research, Vol. 7, Issue 1 https://doi.org/10.1038/s41438-020-00380-3	journal	October 2020
Soil bacterial networks are less stable under drought than fungal networks de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05516-7	journal	August 2018
Nutrient supply controls the linkage between species abundance and ecological interactions in marine bacterial communities Dai, Tianjiao; Wen, Donghui; Bates, Colin T. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-021-27857-6	journal	January 2022
Pervasive associations between dark septate endophytic fungi with tree root and soil microbiomes across Europe Netherway, Tarquin; Bengtsson, Jan; Buegger, Franz Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-023-44172-4	journal	January 2024
Core microbiomes for sustainable agroecosystems Toju, Hirokazu; Peay, Kabir G.; Yamamichi, Masato Nature Plants, Vol. 4, Issue 5 https://doi.org/10.1038/s41477-018-0139-4	journal	April 2018
Plant–microbiome interactions: from community assembly to plant health Trivedi, Pankaj; Leach, Jan E.; Tringe, Susannah G. Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0412-1	journal	August 2020
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non‐hyperaccumulator Thlaspi ochroleucum Shen, Z. G.; Zhao, F. J.; McGRATH, S. P. Plant, Cell & Environment, Vol. 20, Issue 7 https://doi.org/10.1046/j.1365-3040.1997.d01-134.x	journal	July 1997
An X-ray diffraction microscope at the Advanced Photon Source Cai, Z.; Lai, B.; Xiao, Y. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:200300020	journal	March 2003
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets Vogt, S. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:20030160	journal	March 2003
The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield Waller, F.; Achatz, B.; Baltruschat, H. Proceedings of the National Academy of Sciences, Vol. 102, Issue 38 https://doi.org/10.1073/pnas.0504423102	journal	September 2005
Modularity and community structure in networks Newman, M. E. J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 23 https://doi.org/10.1073/pnas.0601602103	journal	May 2006
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition Almario, Juliana; Jeena, Ganga; Wunder, Jörg Proceedings of the National Academy of Sciences, Vol. 114, Issue 44 https://doi.org/10.1073/pnas.1710455114	journal	October 2017
Piriformospora indica enhances freezing tolerance and post-thaw recovery in Arabidopsis by stimulating the expression of CBF genes Jiang, Wei; Pan, Rui; Wu, Chu Plant Signaling & Behavior, Vol. 15, Issue 4 https://doi.org/10.1080/15592324.2020.1745472	journal	March 2020
Molecular mechanisms of Piriformospora indica mediated growth promotion in plants Kundu, Anish; Vadassery, Jyothilakshmi Plant Signaling & Behavior, Vol. 17, Issue 1 https://doi.org/10.1080/15592324.2022.2096785	journal	July 2022
Regulatory mechanisms of sulfur metabolism affecting tolerance and accumulation of toxic trace metals and metalloids in plants Sun, Sheng-Kai; Chen, Jie; Zhao, Fang-Jie Journal of Experimental Botany, Vol. 74, Issue 11 https://doi.org/10.1093/jxb/erad074	journal	March 2023
Molecular evolution and interaction of 14-3-3 proteins with H+-ATPases in plant abiotic stresses Jiang, Wei; He, Jing; Babla, Mohammad Journal of Experimental Botany, Vol. 75, Issue 3 https://doi.org/10.1093/jxb/erad414	journal	October 2023
Plant responses to potassium deficiencies: a role for potassium transport proteins Ashley, M. K.; Grant, M.; Grabov, A. Journal of Experimental Botany, Vol. 57, Issue 2 https://doi.org/10.1093/jxb/erj034	journal	December 2005
Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii Lu, L. -l.; Tian, S. -k.; Yang, X. -e Journal of Experimental Botany, Vol. 59, Issue 11 https://doi.org/10.1093/jxb/ern174	journal	June 2008
Uptake, sequestration and tolerance of cadmium at cellular levels in the hyperaccumulator plant species Sedum alfredii Tian, Shengke; Xie, Ruohan; Wang, Haixin Journal of Experimental Botany, Vol. 68, Issue 9 https://doi.org/10.1093/jxb/erx112	journal	April 2017
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Effects of Cadmium Treatment on the Uptake and Translocation of Sulfate inArabidopsis thaliana Yamaguchi, Chisato; Takimoto, Yuki; Ohkama-Ohtsu, Naoko Plant and Cell Physiology, Vol. 57, Issue 11 https://doi.org/10.1093/pcp/pcw156	journal	September 2016
Sulfur transfer from the endophytic fungus Serendipita indica improves maize growth and requires the sulfate transporter SiSulT Narayan, Om Prakash; Verma, Nidhi; Jogawat, Abhimanyu The Plant Cell, Vol. 33, Issue 4 https://doi.org/10.1093/plcell/koab006	journal	January 2021
Piriformospora indica recruits host-derived putrescine for growth promotion in plants Kundu, Anish; Mishra, Shruti; Kundu, Pritha Plant Physiology, Vol. 188, Issue 4 https://doi.org/10.1093/plphys/kiab536	journal	November 2021
An endophytic fungus,Piriformospora indica, enhances drought tolerance of trifoliate orange by modulating the antioxidant defense system and composition of fatty acids Cao, Jin-Li; He, Wan-Xia; Zou, Ying-Ning Tree Physiology, Vol. 43, Issue 3 https://doi.org/10.1093/treephys/tpac126	journal	October 2022
Serendipita Fungi Modulate the Switchgrass Root Transcriptome to Circumvent Host Defenses and Establish a Symbiotic Relationship Ray, Prasun; Guo, Yingqing; Chi, Myoung-Hwan Molecular Plant-Microbe Interactions®, Vol. 34, Issue 10 https://doi.org/10.1094/MPMI-04-21-0084-R	journal	October 2021
Fast algorithm for detecting community structure in networks Newman, M. E. J. Physical Review E, Vol. 69, Issue 6 https://doi.org/10.1103/PhysRevE.69.066133	journal	June 2004
Physiological Characterization of Root Zn2+ Absorption and Translocation to Shoots in Zn Hyperaccumulator and Nonaccumulator Species of Thlaspi Lasat, M. M.; Baker, Ajm.; Kochian, L. V. Plant Physiology, Vol. 112, Issue 4 https://doi.org/10.1104/pp.112.4.1715	journal	December 1996
Piriformospora indica-a mutualistic basidiomycete with an exceptionally large plant host range: Mutualistic root symbiosis Qiang, Xiaoyu; Weiss, Michael; Kogel, Karl-Heinz Molecular Plant Pathology, Vol. 13, Issue 5 https://doi.org/10.1111/j.1364-3703.2011.00764.x	journal	November 2011
Plant-rhizobacteria interactions alleviate abiotic stress conditions: Plant-rhizobacteria interactions Dimkpa, Christian; Weinand, Tanja; Asch, Folkard Plant, Cell & Environment, Vol. 32, Issue 12 https://doi.org/10.1111/j.1365-3040.2009.02028.x	journal	August 2009
Piriformospora indica affects plant growth by auxin production Sirrenberg, Anke; Göbel, Cornelia; Grond, Stephanie Physiologia Plantarum, Vol. 131, Issue 4 https://doi.org/10.1111/j.1399-3054.2007.00983.x	journal	December 2007
Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria – evolution of the Sox sulfur oxidation enzyme system Meyer, Birte; Imhoff, Johannes F.; Kuever, Jan Environmental Microbiology, Vol. 9, Issue 12 https://doi.org/10.1111/j.1462-2920.2007.01407.x	journal	December 2007
The role of Variovorax and other Comamonadaceae in sulfur transformations by microbial wheat rhizosphere communities exposed to different sulfur fertilization regimes Schmalenberger, Achim; Hodge, Sarah; Bryant, Anna Environmental Microbiology, Vol. 10, Issue 6 https://doi.org/10.1111/j.1462-2920.2007.01564.x	journal	February 2008
UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi: Methods Kõljalg, Urmas; Larsson, Karl-Henrik; Abarenkov, Kessy New Phytologist, Vol. 166, Issue 3 https://doi.org/10.1111/j.1469-8137.2005.01376.x	journal	March 2005
Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri Zhao, F. J.; Jiang, R. F.; Dunham, S. J. New Phytologist, Vol. 172, Issue 4 https://doi.org/10.1111/j.1469-8137.2006.01867.x	journal	September 2006
Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii Lu, Lingli; Tian, Shengke; Zhang, Jie New Phytologist, Vol. 198, Issue 3 https://doi.org/10.1111/nph.12168	journal	February 2013
Sebacinales – one thousand and one interactions with land plants Weiß, Michael; Waller, Frank; Zuccaro, Alga New Phytologist, Vol. 211, Issue 1 https://doi.org/10.1111/nph.13977	journal	February 2016
Spatial imaging reveals the pathways of Zn transport and accumulation during reproductive growth stage in almond plants Xie, Ruohan; Zhao, Jianqi; Lu, Lingli Plant, Cell & Environment, Vol. 44, Issue 6 https://doi.org/10.1111/pce.14037	journal	April 2021
A review of green remediation strategies for heavy metal contaminated soil Wang, Liuwei; Rinklebe, Jörg; Tack, Filip M. G. Soil Use and Management, Vol. 37, Issue 4 https://doi.org/10.1111/sum.12717	journal	March 2021
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
Coordination between microbiota and root endodermis supports plant mineral nutrient homeostasis Salas-González, Isai; Reyt, Guilhem; Flis, Paulina Science, Vol. 371, Issue 6525 https://doi.org/10.1126/science.abd0695	journal	November 2020
Improved Selection of Internal Transcribed Spacer-Specific Primers Enables Quantitative, Ultra-High-Throughput Profiling of Fungal Communities Bokulich, Nicholas A.; Mills, David A. Applied and Environmental Microbiology, Vol. 79, Issue 8 https://doi.org/10.1128/AEM.03870-12	journal	February 2013
Photosynthetic Bradyrhizobia Are Natural Endophytes of the African Wild Rice Oryza breviligulata Chaintreuil, ClÃ¯Â¿Â½mence; Giraud, Eric; Prin, Yves Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5437-5447.2000	journal	December 2000
Comparative Genomic Analysis Reveals Habitat-Specific Genes and Regulatory Hubs within the Genus Novosphingobium Kumar, Roshan; Verma, Helianthous; Haider, Shazia mSystems, Vol. 2, Issue 3 https://doi.org/10.1128/mSystems.00020-17	journal	May 2017
Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods Clemens, Stephan; Ma, Jian Feng Annual Review of Plant Biology, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-arplant-043015-112301	journal	April 2016
Phytoremediation Pilon-Smits, Elizabeth Annual Review of Plant Biology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev.arplant.56.032604.144214	journal	June 2005
Molecular ecological network analyses Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-113	journal	January 2012
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation Agler, Matthew T.; Ruhe, Jonas; Kroll, Samuel PLOS Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pbio.1002352	journal	January 2016
Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica Zuccaro, Alga; Lahrmann, Urs; Güldener, Ulrich PLoS Pathogens, Vol. 7, Issue 10 https://doi.org/10.1371/journal.ppat.1002290	journal	October 2011
K+ Nutrition Exchange in the Serendipita-Arabidopsis Symbiosis: Study of the Fungal K+ Transporters Involved Conchillo, Lorena B.; Haro, Rosario; Benito, Begoña Frontiers in Ecology and Evolution, Vol. 9 https://doi.org/10.3389/fevo.2021.789371	journal	December 2021
Piriformospora indica: Potential and Significance in Plant Stress Tolerance Gill, Sarvajeet S.; Gill, Ritu; Trivedi, Dipesh K. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00332	journal	March 2016
Endophytic Fungi Piriformospora indica Mediated Protection of Host from Arsenic Toxicity Mohd, Shayan; Shukla, Jagriti; Kushwaha, Aparna S. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00754	journal	May 2017
Nitrogen and sulfur fertilizers promote the absorption of lead and cadmium with Salix integra Thunb. by increasing the bioavailability of heavy metals and regulating rhizosphere microbes Wang, Shaokun; Niu, Xiaoyun; Di, Dongliu Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.945847	journal	August 2022
Serendipita indica—A Review from Agricultural Point of View Saleem, Sana; Sekara, Agnieszka; Pokluda, Robert Plants, Vol. 11, Issue 24 https://doi.org/10.3390/plants11243417	journal	December 2022
Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions Hill, Terry W.; Kafer, Etta Fungal Genetics Reports, Vol. 48, Issue 1 https://doi.org/10.4148/1941-4765.1173	journal	September 2001
Cadmium stress tolerance in crop plants: Probing the role of sulfur Gill, Sarvajeet Singh; Tuteja, Narendra Plant Signaling & Behavior, Vol. 6, Issue 2 https://doi.org/10.4161/psb.6.2.14880	journal	February 2011

Similar Records

Uptake, sequestration and tolerance of cadmium at cellular levels in the hyperaccumulator plant species Sedum alfredii

Journal Article · Sat Apr 01 00:00:00 EDT 2017 · Journal of Experimental Botany · OSTI ID:1417381

Role of SaPCR2 in Zn Uptake in the Root Elongation Zone of the Zn/Cd Hyperaccumulator Sedum alfredii

Journal Article · Sun May 22 20:00:00 EDT 2022 · Life · OSTI ID:2469859

A Single Amino Acid Change in Nramp6 from Sedum Alfredii Hance Affects Cadmium Accumulation

Journal Article · Wed Apr 29 20:00:00 EDT 2020 · International Journal of Molecular Sciences (Online) · OSTI ID:1657942

Related Subjects

60 APPLIED LIFE SCIENCES
Endophytic fungus
Nano-XRF
Phytoremediation
Root-soil interface
in situ visualization

Serendipita indica Drives Sulfur-Related Microbiota in Enhancing Growth of Hyperaccumulator Sedum alfredii and Facilitating Soil Cadmium Remediation

Citation Formats

References (114)

Similar Records

Related Subjects