Skip to main content

Advertisement

Log in

Histological and proteome analyses of Microbacterium foliorum-mediated decrease in arsenic toxicity in Melastoma malabathricum

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Arsenic (As) is an increasing threat across the globe, widely known as a non-threshold carcinogen, and it is reaching harmful values in several areas of the world. In this study, the effect of plant growth promoting bacteria (Microbacterium foliorum) on inorganic arsenic (Arsenate) phytoremediation by Melastoma malabathricum plants was investigated through histological analysis and proteome profiling of the M. malabathricum plants. Two-dimensional gel electrophoresis and transmission electron microscopy were used to conduct the proteome and histological analysis. When arsenic-treated cells were compared to untreated cells, substantial changes were found (1) severely altered the morphology of the cells, intensely disturbed; (2) the cell wall was thicker; (3) drastically changed the cytoplasm, the cells were polygonal in shape, different in size (scattered), and relatively dense. Compared to the control group, the ultra-structure of the root cells of the control group revealed intact cytoplasm, vacuole, and cell wall under exposure to As + bacteria that had a minor effect on the cell form. To further understand As + bacteria interaction, proteome profiling of the root cell was analyzed. The As-induced oxidative stress enrichment was confirmed by the up-regulation of tubulin, nucleoside diphosphate kinase, and major allergen during As + bacteria exposure It was observed that the profusion of proteins involved in defence, protein biogenesis, signaling, photosynthesis, nucleoside and energy metabolism was greater in As + bacteria as compared to the rooting out of As only. Overall, it can be obviously seen that the current study demonstrates the effectiveness of phytoremediation by M. foliorum on proteins involved and responsive pathways in dealing with As toxicity in M. malabathricum plant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agrawal GK, Jwa NS, Jung YH, Kim ST, Kim DW, Cho K, Shibato J, Rakwal R (2013) Rice proteomic analysis: sample preparation for protein identification. In Rice Protocols. Humana Press, Totowa, NJ, pp 151–184

  • Agrawal L, Gupta S, Mishra SK, Pandey G, Kumar S, Chauhan PS, Chakrabarty D, Nautiyal CS (2016) Elucidation of complex nature of PEG induced drought-stress response in rice root using comparative proteomics approach. Front Plant Sci 7:1466

    Article  PubMed  PubMed Central  Google Scholar 

  • Aguilar-Galvez A, Pedreschi R, Carpentier S, Chirinos R, García-Ríos D, Campos D (2020) Proteomic analysis of mashua (Tropaeolum tuberosum) tubers subjected to postharvest treatments. Food Chem 305:125485

    Article  CAS  PubMed  Google Scholar 

  • Ahammer L, Grutsch S, Wallner M, Ferreira F, Tollinger M (2017) NMR resonance assignments of a hypoallergenic isoform of the major birch pollen allergen Bet v 1. Biomol NMR Assign 11(2):231–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Alam P, Balawi TH, Altalayan FH, Ahanger MA, Ashraf M (2020) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemosphere 244:125480

    Article  CAS  PubMed  Google Scholar 

  • Ahmadpour P, Ahmadpour F, Mahmud TMM, Abdu A, Soleimani M, Tayefeh FH (2012) Phytoremediation of heavy metals: a green technology. Afr J Biotechnol 11(76):14036–14043

    CAS  Google Scholar 

  • Alcantara-Martinez N, Guizar S, Rivera-Cabrera F, Anicacio-Acevedo BE, Buendia-Gonzalez L, Volke-Sepulveda T (2016) Tolerance, arsenic uptake, and oxidative stress in Acacia farnesiana under arsenate-stress. Int J Phytoremediat 18(7):671–678

    Article  CAS  Google Scholar 

  • Alcántara-Martínez N, Figueroa-Martínez F, Rivera-Cabrera F, Gutiérrez-Sánchez G, Volke-Sepúlveda T (2018) An endophytic strain of Methylobacterium sp. increases arsenate tolerance in Acacia farnesiana (L.) Willd: a proteomic approach. Sci Total Environ 625:762–774

    Article  PubMed  CAS  Google Scholar 

  • Ali B, Huang CR, Qi ZY, Ali S, Daud MK, Geng XX, Liu HB, Zhou WJ (2013) 5-Aminolevulinic acid ameliorates cadmium-induced morphological, biochemical, and ultrastructural changes in seedlings of oilseed rape. Environ Sci Pollut Res 20(10):7256–7267

    Article  CAS  Google Scholar 

  • Alka S, Shahir S, Ibrahim N, Chai TT, Bahari ZM, Abd Manan F (2020) The role of plant growth promoting bacteria on arsenic removal: a review of existing perspectives. Environ Technol Innov 17:100602

    Article  Google Scholar 

  • Alka S, Shahir S, Ibrahim N, Ndejiko MJ, Vo DVN, Abd Manan F (2021) Arsenic removal technologies and future trends: a mini review. J Clean Prod 278:123805

  • Bahari ZM, Ibrahim Z, Jaafar J, Shahir S (2017) Draft genome sequence of Arsenic-resistant Microbacterium sp. strain SZ1 isolated from Arsenic-bearing gold ores. Genome Announc 5(43):2

  • Barberini L, Noto A, Saba L, Palmas F, Fanos V, Dessì A, Zavattoni M, Fattuoni C, Mussap M (2016) Multivariate data validation for investigating primary HCMV infection in pregnancy. Data Brief 9:220–230

    Article  PubMed  PubMed Central  Google Scholar 

  • Behrendt U, Ulrich A, Schumann P (2001) Description of Microbacterium foliorum sp. nov. and Microbacterium phyllosphaerae sp. nov., isolated from the phyllosphere of grasses and the surface litter after mulching the sward, and reclassification of Aureobacterium resistens (Funke et al. 1998) as Microbacterium resistens comb. nov. Int J Syst Evol Microbiol 51(4):1267–1276

    Article  CAS  PubMed  Google Scholar 

  • Bijlsma S, Bobeldijk I, Verheij ER, Ramaker R, Kochhar S, Macdonald IA, Van Ommen B, Smilde AK (2006) Large-scale human metabolomics studies: a strategy for data (pre-) processing and validation. Anal Chem 78(2):567–574

    Article  CAS  PubMed  Google Scholar 

  • Bilal S, Shahzad R, Khan AL, Al-Harrasi A, Kim CK, Lee IJ (2019) Phytohormones enabled endophytic Penicillium funiculosum LHL06 protects Glycine max L. from synergistic toxicity of heavy metals by hormonal and stress-responsive proteins modulation. J Hazard Mater 379:120824

    Article  CAS  PubMed  Google Scholar 

  • Bona E, Scarafoni A, Marsano F, Boatti L, Copetta A, Massa N, Gamalero E, D’Agostino G, Cesaro P, Cavaletto M, Berta G (2016) Arbuscular mycorrhizal symbiosis affects the grain proteome of Zea mays: a field study. Sci Rep 6:26439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruno LB, Karthik C, Ma Y, Kadirvelu K, Freitas H, Rajkumar M (2020) Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing-thermotolerant plant growth promoting bacteria. Chemosphere 244:

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekhar C, Ray JG (2019) Lead accumulation, growth responses and biochemical changes of three plant species exposed to soil amended with different concentrations of lead nitrate. Ecotoxicol Environ Saf 171:26–36

    Article  CAS  PubMed  Google Scholar 

  • Chauhan R, Awasthi S, Indoliya Y, Chauhan AS, Mishra S, Agrawal L, Srivastava S, Dwivedi S, Singh PC, Mallick S, Chauhan PS (2020) Transcriptome and proteome analyses reveal selenium mediated amelioration of arsenic toxicity in rice (Oryza sativa L.). J Hazard Mater 390:122122

    Article  CAS  PubMed  Google Scholar 

  • Corretto E, Antonielli L, Sessitsch A, Kidd P, Weyens N, Brader G (2015) Draft genome sequences of 10 Microbacterium spp., with emphasis on heavy metal-contaminated environments. Genome Announc 3(3):e00432-e1415

    Article  PubMed  PubMed Central  Google Scholar 

  • Dadrasnia A, Pariatamby A (2016) Phyto-enhanced remediation of soil co-contaminated with lead and diesel fuel using biowaste and Dracaena reflexa: a laboratory study. Waste Manag Res 34(3):246–253

    Article  CAS  PubMed  Google Scholar 

  • Das S, Jean JS, Kar S, Chou ML, Chen CY (2014) Screening of plant growth-promoting traits in arsenic-resistant bacteria isolated from agricultural soil and their potential implication for arsenic bioremediation. J Hazard Mater 272:112–120

    Article  CAS  PubMed  Google Scholar 

  • Del Giudice I, Limauro D, Pedone E, Bartolucci S, Fiorentino G (2013) A novel arsenate reductase from the bacterium Thermus thermophilus HB27: its role in arsenic detoxification. Biochim Biophys Acta (BBA) Proteins Proteom 834(10):2071–2079

    Article  CAS  Google Scholar 

  • Dixit G, Singh AP, Kumar A, Dwivedi S, Deeba F, Kumar S, Suman S, Adhikari B, Shukla Y, Trivedi PK, Trivedi PK (2015) Sulfur alleviates arsenic toxicity by reducing its accumulation and modulating proteome, amino acids and thiol metabolism in rice leaves. Sci Rep 5:16205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farnese FS, Oliveira JA, Paiva EA, Menezes-Silva PE, da Silva AA, Campos FV, Ribeiro C (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516

    PubMed  PubMed Central  Google Scholar 

  • Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, Zhou W (2016) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25(2):350–366

    Article  CAS  PubMed  Google Scholar 

  • Farooq MA, Zhang K, Islam F, Wang J, Athar HU, Nawaz A, Ullah Zafar Z, Xu J, Zhou W (2018a) Physiological and iTRAQ-based quantitative proteomics analysis of methyl jasmonate-induced tolerance in Brassica napus under arsenic stress. Proteomics 18(10):1700290

    Article  CAS  Google Scholar 

  • Farooq MA, Islam F, Yang C, Nawaz A, Gill RA, Ali B, Song W, Zhou W (2018b) Methyl jasmonate alleviates arsenic-induced oxidative damage and modulates the ascorbate–glutathione cycle in oilseed rape roots. Plant Growth Regul 84(1):135–148

    Article  CAS  Google Scholar 

  • Fru EC, Callac N, Posth NR, Argyraki A, Ling YC, Ivarsson M, Broman C, Kilias SP (2018) Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments. Biogeochemistry 141(1):41–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu HL, Meng Y, Ordóñez E, Villadangos AF, Bhattacharjee H, Gil JA, Mateos LM, Rosen BP (2009) Properties of arsenite efflux permeases (Acr3) from Alkaliphilus metalliredigens and Corynebacterium glutamicum. J Biol Chem 284(30):19887–19895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh A, Pramanik K, Bhattacharya S, Mondal S, Ghosh SK, Ghosh PK, Maiti TK (2021) Abatement of arsenic-induced phytotoxic effects in rice seedlings by an arsenic-resistant Pantoea dispersa strain. Environ Sci Pollut Res 28(17):21633–21649

    Article  CAS  Google Scholar 

  • Gupta P, Kumar V, Usmani Z, Rani R, Chandra A, Gupta VK (2020a) Implications of plant growth promoting Klebsiella sp. CPSB4 and Enterobacter sp. CPSB49 in luxuriant growth of tomato plants under chromium stress. Chemosphere 240:124944

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Rani R, Chandra A, Kumar V (2018) Potential applications of Pseudomonas sp. (strain CPSB21) to ameliorate Cr6+ stress and phytoremediation of tannery effluent contaminated agricultural soils. Sci Rep 8(1):1–10

    Article  Google Scholar 

  • Gupta S, Mishra SK, Misra S, Pandey V, Agrawal L, Nautiyal CS, Chauhan PS (2020b) Revealing the complexity of protein abundance in chickpea root under drought-stress using a comparative proteomics approach. Plant Physiol Biochem 15:88–102

    Article  CAS  Google Scholar 

  • Hackstadt AJ, Hess AM (2009) Filtering for increased power for microarray data analysis. BMC Bioinform 10(1):11

    Article  Google Scholar 

  • Hall JÁ (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11

    Article  CAS  PubMed  Google Scholar 

  • Huang WL, Wu FL, Huang HY, Huang WT, Deng CL, Yang LT, Huang ZR, Chen LS (2020) Excess copper-induced alterations of protein profiles and related physiological parameters in citrus leaves. Plants 9(3):291

    Article  CAS  PubMed Central  Google Scholar 

  • Irshad S, Xie Z, Mehmood S, Nawaz A, Ditta A, Mahmood Q (2021) Insights into conventional and recent technologies for arsenic bioremediation: a systematic review. Environ Sci Pollut Res 28(15):18870–18892

    Article  Google Scholar 

  • Khan DH, Duckett JG, Frankland B, Kirkham JB (1984) An X-ray microanalytical study of the distribution of cadmium in roots of Zea mays L. J Plant Physiol 115(1):19–28

    Article  CAS  PubMed  Google Scholar 

  • Khan KY, Ali B, Stoffella PJ, Cui X, Yang X, Guo Y (2020) Study amino acid contents, plant growth variables and cell ultrastructural changes induced by cadmium stress between two contrasting cadmium accumulating cultivars of Brassica rapa ssp. chinensis L. (pak choi). Ecotoxicol Environ Saf 200:110748

    Article  CAS  PubMed  Google Scholar 

  • Kleinknecht L, Wang F, Stübe R, Philippar K, Nickelsen J, Bohne AV (2014) RAP, the sole octotricopeptide repeat protein in Arabidopsis, is required for chloroplast 16S rRNA maturation. Plant Cell 26(2):777–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteom 74(8):1301–1322

    Article  CAS  Google Scholar 

  • Lindsay ER, Maathuis FJ (2017) New molecular mechanisms to reduce arsenic in crops. Trends Plant Sci 22(12):1016–1026

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Huang R, Hu X, Jia Y, Li J, Luo J, Liu Q, Luo L, Liu G, Chen Z (2019) Physiological responses and proteomic changes reveal insights into Stylosanthes response to manganese toxicity. BMC Plant Biol 19(1):212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Long R, Li M, Zhang T, Kang J, Sun Y, Yang Q (2019) Comparative proteomic analysis reveals differential root proteins in Medicago sativa and Medicago truncatula in response to salt stress. In: de Bruijn FJ (ed) The model legume Medicago truncatula. Wiley, New York, pp 1102–1111

    Google Scholar 

  • Luzarowski M, Kosmacz M, Sokolowska E, Jasińska W, Willmitzer L, Veyel D, Skirycz A (2017) Affinity purification with metabolomic and proteomic analysis unravels diverse roles of nucleoside diphosphate kinases. J Exp Bot 68(13):3487–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moussi CJ (2020) Transforming growth factor-beta targets Formin-like 2 for Angiopoietin-like 4 secretion during the epithelial mesenchymal transition. Doctoral dissertation, Philipps-Universität Marburg

  • Mukherjee G, Saha C, Naskar N, Mukherjee A, Mukherjee A, Lahiri S, Majumder AL, Seal A (2018) An endophytic bacterial consortium modulates multiple strategies to improve arsenic phytoremediation efficacy in Solanum nigrum. Sci Rep 8(1):6979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137(2):611–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira BRM, de Almeida AAF, Pirovani CP, Barroso JP, Neto CHDC, Santos NA, Ahnert D, Baligar VC, Mangabeira PAO (2020) Mitigation of Cd toxicity by Mn in young plants of cacao, evaluated by the proteomic profiles of leaves and roots. Ecotoxicology 29(3):340–358

    Article  CAS  PubMed  Google Scholar 

  • Pandey AS, Sharma E, Jain N, Singh B, Burman N, Khurana JP (2018) A rice bZIP transcription factor, OsbZIP16, regulates abiotic stress tolerance when over-expressed in Arabidopsis. J Plant Biochem Biotechnol 27(4):393–400

    Article  CAS  Google Scholar 

  • Pandey N, Manjunath K, Sahu K (2020) Screening of plant growth promoting attributes and arsenic remediation efficacy of bacteria isolated from agricultural soils of Chhattisgarh. Arch Microbiol 202(3):567–578

    Article  CAS  PubMed  Google Scholar 

  • Patek-Mohd NN, Abdu A, Jusop S, Abdul-Hamid H, Karim M, Nazrin M, Akbar MH, Jamaluddin AS (2018) Potentiality of Melastoma malabathricum as phytoremediators of soil contaminated with sewage sludge. Sci Agricola 75(1):27–35

    Article  CAS  Google Scholar 

  • Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, Inuganti A, Griss J, Mayer G, Eisenacher M, Pérez E (2019) The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res 47(D1):D442–D450

    Article  CAS  PubMed  Google Scholar 

  • Rabello AR, Guimarães CM, Rangel PH, da Silva FR, Seixas D, de Souza E, Brasileiro AC, Spehar CR, Ferreira ME, Mehta  (2008) Identification of drought-responsive genes in roots of upland rice (Oryza sativa L). BMC Genom 9(1):485

    Article  CAS  Google Scholar 

  • Rajoo K, Abdu A, Singh D, Abdul-Hamid H, Jusop S, Zhen W (2013) Heavy metal uptake and translocation by Dipterocarpus verrucosus from sewage sludge contaminated soil. Am J Environ Sci 9(3):259–268

    Article  Google Scholar 

  • Salekdeh GH, Komatsu S (2007) Crop proteomics: aim at sustainable agriculture of tomorrow. Proteomics 7(16):2976–2996

    Article  CAS  PubMed  Google Scholar 

  • Samrana S, Ali A, Muhammad U, Azizullah A, Ali H, Khan M, Naz S, Khan MD, Zhu S, Chen J (2020) Physiological, ultrastructural, biochemical, and molecular responses of glandless cotton to hexavalent chromium (Cr6+) exposure. Environ Pollut 266:115394

    Article  CAS  PubMed  Google Scholar 

  • Sengupta D, Kannan M, Reddy AR (2011) A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek. Planta 233(6):1111–1127

    Article  CAS  PubMed  Google Scholar 

  • Song F, Qi D, Liu X, Kong X, Gao Y, Zhou Z, Wu Q (2015) Proteomic analysis of symbiotic proteins of Glomus mosseae and Amorpha fruticosa. Sci Rep 5:18031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squibb KS, Fowler BA (1983) The toxicity of arsenic and its compounds. In: Fowler BA (ed) Biological and environmental effects of arsenic, pp 233–269

  • Srivastava S, Suprasanna P, D’Souza SF (2011) Redox state and energetic equilibrium determine the magnitude of stress in Hydrilla verticillata upon exposure to arsenate. Protoplasma 248(4):805–815

    Article  CAS  PubMed  Google Scholar 

  • Štefanić PP, Jarnević M, Cvjetko P, Biba R, Šikić S, Tkalec M, Cindrić M, Letofsky-Papst I, Balen B (2019) Comparative proteomic study of phytotoxic effects of silver nanoparticles and silver ions on tobacco plants. Environ Sci Pollut Res 26(22):22529–22550

    Article  CAS  Google Scholar 

  • Subba P, Kumar R, Gayali S, Shekhar S, Parveen S, Pandey A, Datta A, Chakraborty S, Chakraborty N (2013) Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar. Proteomics 13(12–13):1973–1992

    Article  CAS  PubMed  Google Scholar 

  • Tantray AY, Ali HM, Ahmad A (2020) Analysis of proteomic profile of contrasting phosphorus responsive rice cultivars grown under phosphorus deficiency. Agronomy 10(7):1028

    Article  CAS  Google Scholar 

  • Titah HS, Abdullah SRS, Mushrifah I, Anuar N, Basri H, Mukhlisin M (2013) Effect of applying rhizobacteria and fertilizer on the growth of Ludwigia octovalvis for arsenic uptake and accumulation in phytoremediation. Ecol Eng 58:303–313

    Article  Google Scholar 

  • Tlustoš P, Goessler W, Száková J, Balík J (2002) Arsenic compounds in leaves and roots of radish grown in soil treated by arsenite, arsenate and dimethylarsinic acid. Appl Organomet Chem 16(4):216–220

    Article  CAS  Google Scholar 

  • Van den Berg RA, Hoefsloot HC, Westerhuis JA, Smilde AK, van der Werf MJ (2006) Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genom 7(1):142

    Article  CAS  Google Scholar 

  • Vezza ME, Nicotra MFO, Agostini E, Talano MA (2020) Biochemical and molecular characterization of arsenic response from Azospirillum brasilense Cd, a bacterial strain used as plant inoculant. Environ Sci Pollut Res 27(2):2287–2300

    Article  CAS  Google Scholar 

  • Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8(7):1470–1489

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Chen X, Xu X, Lu C, Zhang W, Zhao FJ (2018) Arsenate induced chlorosis 1/translocon at the outer envelope membrane of chloroplasts 132 protects chloroplasts from arsenic toxicity. Plant Physiol 178(4):1568–1583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheelock ÅM, Wheelock CE (2013) Trials and tribulations of ‘omics data analysis: assessing quality of SIMCA-based multivariate models using examples from pulmonary medicine. Mol BioSyst 9(11):2589–2596

    Article  CAS  PubMed  Google Scholar 

  • Worley B, Powers R (2013) Multivariate analysis in metabolomics. Curr Metabolomics 1(1):92–107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43(W1):W251–W257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan Y, Zhang X, Zheng X, Apaliya MT, Yang Q, Zhao L, Xu W, Feng L, Ma M, Zhu YG, Zhang H (2018) Control of postharvest blue mold decay in pears by Meyerozyma guilliermondii and its effects on the protein expression profile of pears. Postharvest Biol Technol 136:124–131

    Article  CAS  Google Scholar 

  • Zaheer IE, Ali S, Saleem MH, Imran M, Alnusairi GS, Alharbi BM, Riaz M, Abbas Z, Rizwan M, Soliman MH (2020) Role of iron–lysine on morpho-physiological traits and combating chromium toxicity in rapeseed (Brassica napus L.) plants irrigated with different levels of tannery wastewater. Plant Physiol Biochem 155:70–84

    Article  CAS  PubMed  Google Scholar 

  • Zeng X, Pang L, Chen Y, Kong X, Chen J, Tian X (2020) Bacteria Sphingobium yanoikuyae Sy 310 enhances accumulation capacity and tolerance of cadmium in Salix matsudana Koidz roots. Environ Sci Pollut Res 27(16):19764–19773

    Article  CAS  Google Scholar 

  • Zhang X, Wu F, Gu N, Yan X, Wang K, Dhanasekaran S, Gu X, Zhao L, Zhang H (2020) Postharvest biological control of Rhizopus rot and the mechanisms involved in induced disease resistance of peaches by Pichia membranefaciens. Postharvest Biol Technol 163:111146

    Article  CAS  Google Scholar 

  • Zhou C, Huang M, Li Y, Luo J, Cai L (2016) Changes in subcellular distribution and antioxidant compounds involved in Pb accumulation and detoxification in Neyraudia reynaudiana. Environ Sci Pollut Res 23(21):21794–21804

    Article  CAS  Google Scholar 

  • Zvobgo G, LwalabaWaLwalaba J, Sagonda T, Mapodzeke JM, Muhammad N, Shamsi IH, Zhang G (2018) Phosphate alleviates arsenate toxicity by altering expression of phosphate transporters in the tolerant barley genotypes. Ecotoxicol Environ Saf 147:832–839

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the Ministry of Higher Education Malaysia (Fundamental Research Grant Scheme, FRGS No. R.J130000.7854.5F102), Universiti Teknologi Malaysia (Geran Universiti Penyelidikan GUP TIER 1 No. Q.J130000.2545.17H14), and University Industry Research Laboratory, Universiti Teknologi Malaysia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fazilah Abd Manan.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alka, S., Shahir, S., Ibrahim, N. et al. Histological and proteome analyses of Microbacterium foliorum-mediated decrease in arsenic toxicity in Melastoma malabathricum. 3 Biotech 11, 336 (2021). https://doi.org/10.1007/s13205-021-02864-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-021-02864-y

Keywords

Navigation