Recent advances and application in whole-genome multiple displacement amplification

Naiyun Long , Yi Qiao , Zheyun Xu , Jing Tu , Zuhong Lu

Quant. Biol. ›› 2020, Vol. 8 ›› Issue (4) : 279 -294.

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Quant. Biol. ›› 2020, Vol. 8 ›› Issue (4) : 279 -294. DOI: 10.1007/s40484-020-0217-2
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Recent advances and application in whole-genome multiple displacement amplification

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Abstract

Background: The extremely small amount of DNA in a cell makes it difficult to study the whole genome of single cells, so whole-genome amplification (WGA) is necessary to increase the DNA amount and enable downstream analyses. Multiple displacement amplification (MDA) is the most widely used WGA technique.

Results: Compared with amplification methods based on PCR and other methods, MDA renders high-quality DNA products and better genome coverage by using phi29 DNA polymerase. Moreover, recently developed advanced MDA technologies such as microreactor MDA, emulsion MDA, and micro-channel MDA have improved amplification uniformity. Additionally, the development of other novel methods such as TruePrime WGA allows for amplification without primers.

Conclusion: Here, we reviewed a selection of recently developed MDA methods, their advantages over other WGA methods, and improved MDA-based technologies, followed by a discussion of future perspectives. With the continuous development of MDA and the successive update of detection technologies, MDA will be applied in increasingly more fields and provide a solid foundation for scientific research.

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Keywords

whole genome amplification / multiple displacement amplification / improved MDA-based approaches

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Naiyun Long, Yi Qiao, Zheyun Xu, Jing Tu, Zuhong Lu. Recent advances and application in whole-genome multiple displacement amplification. Quant. Biol., 2020, 8(4): 279-294 DOI:10.1007/s40484-020-0217-2

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References

[1]

Feinerman, O., Veiga, J., Dorfman, J. R., Germain, R. N. and Altan-Bonnet, G. (2008) Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science, 321, 1081–1084

[2]

Hoey, T. (2010) Drug resistance, epigenetics, and tumor cell heterogeneity. Sci. Transl. Med., 2, 28ps19

[3]

Yan, L., Huang, L., Xu, L., Huang, J., Ma, F., Zhu, X., Tang, Y., Liu, M., Lian, Y., Liu, P., (2015) Live births after simultaneous avoidance of monogenic diseases and chromosome abnormality by next-generation sequencing with linkage analyses. Proc. Natl. Acad. Sci. U.S.A., 112, 15964–15969

[4]

Ni, X., Zhuo, M., Su, Z., Duan, J., Gao, Y., Wang, Z., Zong, C., Bai, H., Chapman, A. R., Zhao, J., (2013) Reproducible copy number variation patterns among single circulating tumor cells of lung cancer patients. Proc. Natl. Acad. Sci. USA, 110, 21083–21088

[5]

Zhang, L., Cui, X., Schmitt, K., Hubert, R., Navidi, W., and Arnheim, N. (1992) Whole genome amplification from a single cell: implications for genetic analysis. Proc. Natl. Acad. Sci. USA, 89, 5847–5851

[6]

Telenius, H., Carter, N. P., Bebb, C. E., Nordenskjöld, M., Ponder, B. A. J. and Tunnacliffe, A. (1992) Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics, 13, 718–725

[7]

Lizardi, P. M., Huang, X., Zhu, Z., Bray-Ward, P., Thomas, D. C. and Ward, D. C. (1998) Mutation detection and single-molecule counting using isothermal rolling-circle amplification. Nat. Genet., 19, 225–232

[8]

Dean, F. B., Hosono, S., Fang, L., Wu, X., Faruqi, A. F., Bray-Ward, P., Sun, Z., Zong, Q., Du, Y., Du, J., (2002) Comprehensive human genome amplification using multiple displacement amplification. Proc. Natl. Acad. Sci. USA, 99, 5261–5266

[9]

Zong, C., Lu, S., Chapman, A. R. and Xie, X. S. (2012) Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science, 338, 1622–1626

[10]

Chen, C., Xing, D., Tan, L., Li, H., Zhou, G., Huang, L. and Xie, X. S. (2017) Single-cell whole-genome analyses by Linear Amplification via Transposon Insertion (LIANTI). Science, 356, 189–194

[11]

Huang, L., Ma, F., Chapman, A., Lu, S. and Xie, X. S. (2015) Single-cell whole-genome amplification and sequencing: methodology and applications. Annu. Rev. Genomics Hum. Genet., 16, 79–102

[12]

Gawad, C., Koh, W. and Quake, S. R. (2016) Single-cell genome sequencing: current state of the science. Nat. Rev. Genet., 17, 175–188

[13]

Detter, J. C., Jett, J. M., Lucas, S. M., Dalin, E., Arellano, A. R., Wang, M., Nelson, J. R., Chapman, J., Lou, Y., Rokhsar, D., (2002) Isothermal strand-displacement amplification applications for high-throughput genomics. Genomics, 80, 691–698

[14]

Fu, Y., Li, C., Lu, S., Zhou, W., Tang, F., Xie, X. S. and Huang, Y. (2015) Uniform and accurate single-cell sequencing based on emulsion whole-genome amplification. Proc. Natl. Acad. Sci. USA, 112, 11923–11928

[15]

Ballantyne, K. N., van Oorschot, R. A. H., John Mitchell, R. and Koukoulas, I. (2006) Molecular crowding increases the amplification success of multiple displacement amplification and short tandem repeat genotyping. Anal. Biochem., 355, 298–303

[16]

de Cesare, G., Nascetti, A. and Caputo, D. (2015) Amorphous silicon p-i-n structure acting as light and temperature sensor. Sensors (Basel), 15, 12260–12272

[17]

Bruijns, B. B., Costantini, F., Lovecchio, N., Tiggelaar, R. M., Di Timoteo, G., Nascetti, A., de Cesare, G., Gardeniers, J. G. E. and Caputo, D. (2019) On-chip real-time monitoring of multiple displacement amplification of DNA. Sens. Actuators B Chem., 293, 16–22

[18]

Li, X. Y., Du, Y. C., Zhang, Y. P. and Kong, D. M. (2017) Dual functional Phi29 DNA polymerase-triggered exponential rolling circle amplification for sequence-specific detection of target DNA embedded in long-stranded genomic DNA. Sci. Rep., 7, 6263

[19]

Toley, B. J., Covelli, I., Belousov, Y., Ramachandran, S., Kline, E., Scarr, N., Vermeulen, N., Mahoney, W., Lutz, B. R. and Yager, P. (2015) Isothermal strand displacement amplification (iSDA): a rapid and sensitive method of nucleic acid amplification for point-of-care diagnosis. Analyst (Lond.), 140, 7540–7549

[20]

Blanco, L., Bernad, A., Lázaro, J. M., Martín, G., Garmendia, C. and Salas, M. (1989) Highly efficient DNA synthesis by the phage phi 29 DNA polymerase. Symmetrical mode of DNA replication. J. Biol. Chem., 264, 8935–8940

[21]

Handyside, A. H., Robinson, M. D., Simpson, R. J., Omar, M. B., Shaw, M. A., Grudzinskas, J. G. and Rutherford, A. (2004) Isothermal whole genome amplification from single and small numbers of cells: a new era for preimplantation genetic diagnosis of inherited disease. Mol. Hum. Reprod., 10, 767–772

[22]

Banér, J., Nilsson, M., Mendel-Hartvig, M. and Landegren, U. (1998) Signal amplification of padlock probes by rolling circle replication. Nucleic Acids Res., 26, 5073–5078

[23]

Krzywkowski, T., Kühnemund, M., Wu, D. and Nilsson, M. (2018) Limited reverse transcriptase activity of phi29 DNA polymerase. Nucleic Acids Res., 46, 3625–3632

[24]

Coskun, S. and Alsmadi, O. (2007) Whole genome amplification from a single cell: a new era for preimplantation genetic diagnosis. Prenat. Diagn., 27, 297–302

[25]

Spits, C., Le Caignec, C., De Rycke, M., Van Haute, L., Van Steirteghem, A., Liebaers, I. and Sermon, K. (2006) Optimization and evaluation of single-cell whole-genome multiple displacement amplification. Hum. Mutat., 27, 496–503

[26]

del Prado, A., Rodríguez, I., Lázaro, J. M., Moreno-Morcillo, M., de Vega, M. and Salas, M. (2019) New insights into the coordination between the polymerization and 3′-5′ exonuclease activities in f29 DNA polymerase. Sci. Rep., 9, 923

[27]

Xu, M. (2015) Patent CN 104560950A

[28]

Huang, W., Cai, H., Wei, S., Bo, X. and Li, F. (2016) MDAGenera: an efficient and accurate simulator for multiple displacement amplification. In: Intelligent Computing Theories and Application, Huang, D.S., Bevilacqua, V., Premaratne, P. (eds.),pp. 258–267. Springer, Cham

[29]

Tenaglia, E., Imaizumi, Y., Miyahara, Y. and Guiducci, C. (2018) Isothermal multiple displacement amplification of DNA templates in minimally buffered conditions using phi29 polymerase. Chem. Commun. (Camb.), 54, 2158–2161

[30]

Wang, G., Brennan, C., Rook, M., Wolfe, J. L., Leo, C., Chin, L., Pan, H., Liu, W. H., Price, B. and Makrigiorgos, G. M. (2004) Balanced-PCR amplification allows unbiased identification of genomic copy changes in minute cell and tissue samples. Nucleic Acids Res., 32, e76

[31]

Bergen, A. W., Haque, K. A., Qi, Y., Beerman, M. B., Garcia-Closas, M., Rothman, N. and Chanock, S. J. (2005) Comparison of yield and genotyping performance of multiple displacement amplification and OmniPlex whole genome amplified DNA generated from multiple DNA sources. Hum. Mutat., 26, 262–270

[32]

Lovmar, L., Fredriksson, M., Liljedahl, U., Sigurdsson, S. and Syvänen, A. C. (2003) Quantitative evaluation by minisequencing and microarrays reveals accurate multiplexed SNP genotyping of whole genome amplified DNA. Nucleic Acids Res., 31, e129

[33]

Hawkins, T. L., Detter, J. C. and Richardson, P. M. (2002) Whole genome amplification–applications and advances. Curr. Opin. Biotechnol., 13, 65–67

[34]

Lasken, R. S., Egholm, M. and Alsmadi, O. A. (2004) Patent US 9487823B2

[35]

Theunissen, G. M. G., Rolf, B., Gibb, A. and Jäger, R. (2017) DNA profiling of sperm cells by using micromanipulation and whole genome amplification. Forensic Sci. International. Genet. Suppl. Ser., 6, e497–e499

[36]

Lasken, R. S. (2013) Single-cell sequencing in its prime. Nat. Biotechnol., 31, 211–212

[37]

de Bourcy, C. F., De Vlaminck, I., Kanbar, J. N., Wang, J., Gawad, C. and Quake, S. R. (2014) A quantitative comparison of single-cell whole genome amplification methods. PLoS One, 9, e105585

[38]

Liu, W., Zhang, H., Hu, D., Lu, S. and Sun, X. (2018) The performance of MALBAC and MDA methods in the identification of concurrent mutations and aneuploidy screening to diagnose beta-thalassaemia disorders at the single- and multiple-cell levels. J. Clin. Lab. Anal., 32, e22267

[39]

del Rey, J., Vidal, F., Ramírez, L., Borràs, N., Corrales, I., Garcia, I., Martinez-Pasarell, O., Fernandez, S. F., Garcia-Cruz, R., Pujol, A., (2018) Novel Double Factor PGT strategy analyzing blastocyst stage embryos in a single NGS procedure. PLoS One, 13, e0205692

[40]

He, F., Zhou, W., Cai, R., Yan, T. and Xu, X. (2018) Systematic assessment of the performance of whole-genome amplification for SNP/CNV detection and β-thalassemia genotyping. J. Hum. Genet., 63, 407–416

[41]

Li, C., Yu, Z., Fu, Y., Pang, Y. and Huang, Y. (2017) Single-cell-based platform for copy number variation profiling through digital counting of amplified genomic DNA fragments. ACS Appl. Mater. Interfaces, 9, 13958–13964

[42]

Pan, X. and Liang, X. (2014) Principle of whole genome amplification technology and its progress. Biotechnology Bulletin, 12, 47–54, in Chinese

[43]

Hou, Y., Fan, W., Yan, L., Li, R., Lian, Y., Huang, J., Li, J., Xu, L., Tang, F., Xie, X. S., (2013) Genome analyses of single human oocytes. Cell, 155, 1492–1506

[44]

Chu, W. K., Edge, P., Lee, H. S., Bansal, V., Bafna, V., Huang, X. and Zhang, K. (2017) Ultraaccurate genome sequencing and haplotyping of single human cells. Proc. Natl. Acad. Sci. U.S.A., 114, 12512–12517

[45]

Blainey, P. C. and Quake, S. R. (2011) Digital MDA for enumeration of total nucleic acid contamination. Nucleic Acids Res., 39, e19

[46]

Wang, W., Ren, Y., Lu, Y., Xu, Y., Crosby, S. D., Di Bisceglie, A. M. and Fan, X. (2017) Template-dependent multiple displacement amplification for profiling human circulating RNA. Biotechniques, 63, 21–27

[47]

Guria, A., Velayudha Vimala Kumar, K., Srikakulam, N., Krishnamma, A., Chanda, S., Sharma, S., Fan, X. and Pandi, G. (2019) Circular RNA profiling by Illumina sequencing via template-dependent multiple displacement amplification. BioMed Res. Int., 2019, 2756516

[48]

Picher, Á. J., Budeus, B., Wafzig, O., Krüger, C., García-Gémez, S., Martínez-Jimónez, M. I., Díaz-Talavera, A., Weber, D., Blanco, L. and Schneider, A. (2016) TruePrime is a novel method for whole-genome amplification from single cells based on TthPrimPol. Nat. Commun., 7, 13296

[49]

Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J. F., Darling, A., Malfatti, S., Swan, B. K., Gies, E. A., (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature, 499, 431–437

[50]

Stepanauskas, R., Fergusson, E. A., Brown, J., Poulton, N. J., Tupper, B., Labonté J. M., Becraft, E. D., Brown, J. M., Pachiadaki, M. G., Povilaitis, T., (2017) Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles. Nat. Commun., 8, 84

[51]

Gawad. , C., Easton, J. and Gonzalez-pena, V. (2019) Patent WO 2019/148119 A1

[52]

Marcy, Y., Ishoey, T., Lasken, R. S., Stockwell, T. B., Walenz, B. P., Halpern, A. L., Beeson, K. Y., Goldberg, S. M. D. and Quake, S. R. (2007) Nanoliter reactors improve multiple displacement amplification of genomes from single cells. PLoS Genet., 3, 1702–1708

[53]

Gole, J., Gore, A., Richards, A., Chiu, Y. J., Fung, H. L., Bushman, D., Chiang, H. I., Chun, J., Lo, Y. H. and Zhang, K. (2013) Massively parallel polymerase cloning and genome sequencing of single cells using nanoliter microwells. Nat. Biotechnol., 31, 1126–1132

[54]

Hosokawa, M., Nishikawa, Y., Kogawa, M. and Takeyama, H. (2017) Massively parallel whole genome amplification for single-cell sequencing using droplet microfluidics. Sci. Rep., 7, 5111–5199

[55]

Sidore, A. M., Lan, F., Lim, S. W. and Abate, A. R. (2016) Enhanced sequencing coverage with digital droplet multiple displacement amplification. Nucleic Acids Res., 44, e66

[56]

Rhee, M., Light, Y. K., Meagher, R. J. and Singh, A. K. (2016) Digital Droplet Multiple Displacement Amplification (ddMDA) for whole genome sequencing of limited DNA samples. PLoS One, 11, e0153699

[57]

Chen, Z., Fu, Y., Zhang, F., Liu, L., Zhang, N., Zhou, D., Yang, J., Pang, Y. and Huang, Y. (2016) Spinning micropipette liquid emulsion generator for single cell whole genome amplification. Lab Chip, 16, 4512–4516

[58]

Fu, Y., Zhang, F., Zhang, X., Yin, J., Du, M., Jiang, M., Liu, L., Li, J., Huang, Y. and Wang, J. (2019) High-throughput single-cell whole-genome amplification through centrifugal emulsification and eMDA. Commun. Biol., 2, 147

[59]

Kim, S. C., Premasekharan, G., Clark, I. C., Gemeda, H. B., Paris, P. L. and Abate, A. R. (2017) Measurement of copy number variation in single cancer cells using rapid-emulsification digital droplet MDA. Microsyst. Nanoeng., 3, 17018

[60]

Chen, Z., Liao, P., Zhang, F., Jiang, M., Zhu, Y. and Huang, Y. (2017) Centrifugal micro-channel array droplet generation for highly parallel digital PCR. Lab Chip, 17, 235–240

[61]

Li, J., Lu, N., Shi, X., Qiao, Y., Chen, L., Duan, M., Hou, Y., Ge, Q., Tao, Y., Tu, J., (2017) 1D-reactor decentralized MDA for uniform and accurate whole genome amplification. Anal. Chem., 89, 10147–10152

[62]

Li, J., Lu, N., Tao, Y., Duan, M., Qiao, Y., Xu, Y., Ge, Q., Bi, C., Fu, J., Tu, J., (2018) Accurate and sensitive single-cell-level detection of copy number variations by micro-channel multiple displacement amplification (mcMDA). Nanoscale, 10, 17933–17941

[63]

Zhu, D., Yan, Y., Lei, P., Shen, B., Cheng, W., Ju, H. and Ding, S. (2014) A novel electrochemical sensing strategy for rapid and ultrasensitive detection of Salmonella by rolling circle amplification and DNA-AuNPs probe. Anal. Chim. Acta, 846, 44–50

[64]

Bowers, R. M., Kyrpides, N. C., Stepanauskas, R., Harmon-Smith, M., Doud, D., Reddy, T. B. K., Schulz, F., Jarett, J., Rivers, A. R., Eloe-Fadrosh, E. A., (2017) Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol., 35, 725–731

[65]

Liu, Y., Yao, J. and Walther-Antonio, M. (2019) Whole genome amplification of single epithelial cells dissociated from snap-frozen tissue samples in microfluidic platform. Biomicrofluidics, 13, 034109

[66]

Chen, M., Zhang, J., Zhao, J., Chen, T., Liu, Z., Cheng, F., Fan, Q. and Yan, J. (2020) Comparison of CE- and MPS-based analyses of forensic markers in a single cell after whole genome amplification. Forensic Sci. Int. Genet., 45, 102211

[67]

Bruijns, B., Veciana, A., Tiggelaar, R. and Gardeniers, H. (2019) Cyclic olefin copolymer microfluidic devices for forensic applications. Biosensors (Basel), 9, 85

[68]

Lipinski, K. A., Barber, L. J., Davies, M. N., Ashenden, M., Sottoriva, A. and Gerlinger, M. (2016) Cancer evolution and the limits of predictability in precision cancer medicine. Trends Cancer, 2, 49–63

[69]

Xu, X., Hou, Y., Yin, X., Bao, L., Tang, A., Song, L., Li, F., Tsang, S., Wu, K., Wu, H., (2012) Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell, 148, 886–895

[70]

Hou, Y., Song, L., Zhu, P., Zhang, B., Tao, Y., Xu, X., Li, F., Wu, K., Liang, J., Shao, D., (2012) Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell, 148, 873–885

[71]

Wang, Y., Waters, J., Leung, M. L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., Liang, H., (2014) Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature, 512, 155–160

[72]

Liu, H. E., Triboulet, M., Zia, A., Vuppalapaty, M., Kidess-Sigal, E., Coller, J., Natu, V. S., Shokoohi, V., Che, J., Renier, C., (2017) Workflow optimization of whole genome amplification and targeted panel sequencing for CTC mutation detection. NPJ Genom. Med., 2, 34

[73]

Edwards, A., Civitello, A., Hammond, H. A. and Caskey, C. T. (1991) DNA typing and genetic mapping with trimeric and tetrameric tandem repeats. Am. J. Hum. Genet., 49, 746–756

[74]

Deleye, L., Vander Plaetsen, A. S., Weymaere, J., Deforce, D. and Van Nieuwerburgh, F. (2018) Short tandem repeat analysis after whole genome amplification of single B-lymphoblastoid cells. Sci. Rep., 8, 1255

[75]

Michikawa, Y., Sugahara, K., Suga, T., Ohtsuka, Y., Ishikawa, K., Ishikawa, A., Shiomi, N., Shiomi, T., Iwakawa, M. and Imai, T. (2008) In-gel multiple displacement amplification of long DNA fragments diluted to the single molecule level. Anal. Biochem., 383, 151–158

[76]

Deleye, L., Gansemans, Y., De Coninck, D., Van Nieuwerburgh, F., and Deforce, D (2018) Massively parallel sequencing of micro-manipulated cells targeting a comprehensive panel of disease-causing genes: A comparative evaluation of upstream whole-genome amplification methods. PLoS One, 13, e0196334

[77]

Edwards, R. G. and Gardner, R. L. (1967) Sexing of live rabbit blastocysts. Nature, 214, 576–577

[78]

Hellani, A., Coskun, S., Benkhalifa, M., Tbakhi, A., Sakati, N., Al-Odaib, A. and Ozand, P. (2004) Multiple displacement amplification on single cell and possible PGD applications. Mol. Hum. Reprod., 10, 847–852

[79]

Hellani, A., Coskun, S., Tbakhi, A. and Al-Hassan, S. (2005) Clinical application of multiple displacement amplification in preimplantation genetic diagnosis. Reprod. Biomed. Online, 10, 376–380

[80]

Lu, Y., Peng, H., Jin, Z., Cheng, J., Wang, S., Ma, M., Lu, Y., Han, D., Yao, Y., Li, Y., (2013) Preimplantation genetic diagnosis for a Chinese family with autosomal recessive Meckel-Gruber syndrome type 3 (MKS3). PLoS One, 8, e73245

[81]

Shen, X., Chen, D., Xu, Y., Fu, Y. and Zhou, C. (2019) Preimplantation genetic testing of achondroplasia by two haplotyping systems: short tandem repeats and single nucleotide polymorphism. Biochip J., 13, 165–173

[82]

Chen, L., Diao, Z., Xu, Z., Zhou, J., Yan, G. and Sun, H. (2017) The clinical application of NGS-based SNP haplotyping for PGD of Hb H disease. Syst Biol Reprod Med, 63, 212–217

[83]

Chen, S. C., Xu, X. L., Zhang, J. Y., Ding, G. L., Jin, L., Liu, B., Sun, D. M., Mei, C. L., Yang, X. N., Huang, H. F., (2016) Identification of PKD2 mutations in human preimplantation embryos in vitro using a combination of targeted next-generation sequencing and targeted haplotyping. Sci. Rep., 6, 25488

[84]

Konstantinidis, M., Prates, R., Goodall, N. N., Fischer, J., Tecson, V., Lemma, T., Chu, B., Jordan, A., Armenti, E., Wells, D., (2015) Live births following Karyomapping of human blastocysts: experience from clinical application of the method. Reprod. Biomed. Online, 31, 394–403

[85]

Thornhill, A. R., Handyside, A. H., Ottolini, C., Natesan, S. A., Taylor, J., Sage, K., Harton, G., Cliffe, K., Affara, N., Konstantinidis, M., (2015) Karyomapping-a comprehensive means of simultaneous monogenic and cytogenetic PGD: comparison with standard approaches in real time for Marfan syndrome. J. Assist. Reprod. Genet., 32, 347–356

[86]

Davison, M., Hall, E., Zare, R. and Bhaya, D. (2015) Challenges of metagenomics and single-cell genomics approaches for exploring cyanobacterial diversity. Photosynth. Res., 126, 135–146

[87]

Tu, J., Chen, L., Gao, S., Zhang, J., Bi, C., Tao, Y., Lu, N. and Lu, Z. (2019) Obtaining genome sequences of mutualistic bacteria in single Microcystis colonies. Int. J. Mol. Sci., 20, 5047

[88]

Parras-Moltó M., Rodríguez-Galet, A., Suárez-Rodríguez, P. and López-Bueno, A. (2018) Evaluation of bias induced by viral enrichment and random amplification protocols in metagenomic surveys of saliva DNA viruses. Microbiome, 6, 119

[89]

Brinkman, N. E., Villegas, E. N., Garland, J. L. and Keely, S. P. (2018) Reducing inherent biases introduced during DNA viral metagenome analyses of municipal wastewater. PLoS One, 13, e0195350

[90]

Hammond, M., Homa, F., Andersson-Svahn, H., Ettema, T. J. G. and Joensson, H. N. (2016) Picodroplet partitioned whole genome amplification of low biomass samples preserves genomic diversity for metagenomic analysis. Microbiome, 4, 52

[91]

Veltkamp, H. W., Akegawa Monteiro, F., Sanders, R., Wiegerink, R. and Lötters, J. (2020) Disposable DNA amplification chips with integrated low-cost heaters dagger. Micromachines (Basel), 11, 238

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