应用古DNA技术探究发酵微生物的适应、演化和驯化历史

doi:10.16288/j.yczz.22-057

[an error occurred while processing this directive]

Hereditas(Beijing) ›› 2022, Vol. 44 ›› Issue (5): 414-423.doi: 10.16288/j.yczz.22-057

• Review • Previous Articles Next Articles

Exploration of adaptation, evolution and domestication of fermentation microorganisms by applying ancient DNA technology

Zequan Zheng^1,^2,³(), Qiaomei Fu^1,^2,³, Yichen Liu¹()

1. Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
3. CAS Center for Excellence in Life and Paleoenvironment, Beijing 100044, China

Received:2022-03-06 Revised:2022-04-10 Online:2022-05-20 Published:2022-04-19
Contact: Liu Yichen E-mail:zhengzequqn18@mails.ucas.ac.cn;yichen.liu@ivpp.ac.cn
Supported by:
Supported by the National Natural Science Foundation of China(41925009);Chinese Academy of Sciences, and the Ministry of Finance of the People's Republic of China Nos(YSBR-019,XDB26000000);Chinese Academy of Sciences, and the Ministry of Finance of the People's Republic of China Nos(XDB26000000)

Abstract

Abstract:

Fermentation production is the most primitive application of microorganisms by humans, which is of great significance in human history. However, due to the lack of molecular evidence, the history of human fermentation production and the evolution and domestication of fermentation microorganisms remain to be further investigated. Taking wine and fermented dairy, the two most common types of fermented foods as examples, we introduce the archaeology evidence of fermented foods and the evolution and domestication of fermented microorganisms, introduce the research status of paleomicrobiology and fermented paleomicroorganisms, and explore the feasibility and challenges of the research of ancient fermented microorganisms applying microbial ancient DNA technology, as well as the application potential of ancient DNA capture technology in this field.

Key words: fermentation, microorganism, ancient DNA, evolution

Zequan Zheng, Qiaomei Fu, Yichen Liu. Exploration of adaptation, evolution and domestication of fermentation microorganisms by applying ancient DNA technology[J]. Hereditas(Beijing), 2022, 44(5): 414-423.

Figures/Tables 2

References 65

[1]	Joshi VK, Pandey A. Biotechnology: Food Fermentations, Vol. I. Educational Publishers and Distributors, New Delhi, 1999, 1-24.
[2]	McGovern PE, Zhang JZ, Tang JG, Zhang ZQ, Hall GR, Moreau RA, Nuñez A, Butrym ED, Richards MP, Wang CS, Cheng GS, Zhao ZJ, Wang CS. Fermented beverages of pre- and proto-historic China. Proc Natl Acad Sci USA, 2004, 101(51):17593-17598. doi: 10.1073/pnas.0407921102
[3]	Salque M, Bogucki PI, Pyzel J, Sobkowiak-Tabaka I, Grygiel R, Szmyt M, Evershed RP. Earliest evidence for cheese making in the sixth millennium bc in northern Europe. Nature, 2013, 493(7433):522-525. doi: 10.1038/nature11698
[4]	Farnworth ER. Handbook of Fermented Functional Foods, Second Edition. CRC Press, 2008.
[5]	Yong FM, Wood BJB. Microbiology and biochemistry of soy sauce fermentation. Adv Appl Microbiol, 1974, 17:157-194.
[6]	Beddows CG. Fermented fish and fish products. In: Microbiology of Fermented Foods, Vol. 2. Wood BJB, Ed. Elsevier Applied Sci. Publ., London, 1985: 1-40.
[7]	Pederson CS. Microbiology of Food Fermentations. The AVI Publ. Co., Connecticut, 1971: 1-274.
[8]	Purugganan MD, Fuller DQ. The nature of selection during plant domestication. Nature, 2009, 457(7231):843-848. doi: 10.1038/nature07895
[9]	Driscoll CA, Macdonald DW, O’Brien SJ. From wild animals to domestic pets, an evolutionary view of domestication. Proc Natl Acad Sci USA, 2009, 106(Suppl 1):9971-9978. doi: 10.1073/pnas.0901586106
[10]	Arning N, Wilson DJ. The past, present and future of ancient bacterial DNA. Microb Genom, 2020, 6(7): mgen000384.
[11]	Warinner C, Rodrigues JMF, Vyas R, Trachsel C, Shved N, Grossmann J, Radini A, Hancock Y, Tito RY, Fiddyment S, Speller C, Hendy J, Charlton S, Luder HU, Salazar-García DC, Eppler E, Seiler R, Hansen LH, Castruita JAS, Barkow-Oesterreicher S, Teoh KY, Kelstrup CD, Olsen JV, Nanni P, Kawai T, Willerslev E, von Mering C, Lewis CM, Collins MJ, Gilbert MTP, Rühli F, Cappellini E. Pathogens and host immunity in the ancient human oral cavity. Nat Genet, 2014, 46(4):336-344. doi: 10.1038/ng.2906
[12]	Sabin S, Yeh HY, Pluskowski A, Clamer C, Mitchell PD, Bos KI. Estimating molecular preservation of the intestinal microbiome via metagenomic analyses of latrine sediments from two medieval cities. Philos Trans R Soc Lond B Biol Sci, 2020, 375(1812):20190576. doi: 10.1098/rstb.2019.0576
[13]	Lugli GA, Milani C, Mancabelli L, Turroni F, Ferrario C, Duranti S, van Sinderen D, Ventura M. Ancient bacteria of the Ötzi's microbiome: a genomic tale from the Copper Age. Microbiome, 2017, 5(1):5. doi: 10.1186/s40168-016-0221-y
[14]	Cavalieri D, McGovern PE, Hartl DL, Mortimer R, Polsinelli M. Evidence for S. cerevisiae fermentation in ancient wine. J Mol Evol, 2003, 57 Suppl 1: S226-S232. doi: 10.1007/s00239-003-0031-2
[15]	Blanco-Zubiaguirre L, Olivares M, Castro K, Carrero JA, García-Benito C, García-Serrano JÁ, Pérez-Pérez J, Pérez-Arantegui J. Wine markers in archeological potteries: detection by GC-MS at ultratrace levels. Anal Bioanal Chem, 2019, 411(25):6711-6722. doi: 10.1007/s00216-019-02044-1 pmid: 31372702
[16]	Pecci A, Giorgi G, Salvini L, Cau Ontiveros MÁ. Identifying wine markers in ceramics and plasters using gas chromatography-mass spectrometry. Experimental and archaeological materials. J Archaeol Sci, 2013, 40(1):109-115. doi: 10.1016/j.jas.2012.05.001
[17]	Rageot M, Mötsch A, Schorer B, Bardel D, Winkler A, Sacchetti F, Chaume B, Casa PD, Buckley S, Cafisso S, Fries-Knoblach J, Krausse D, Hoppe T, Stockhammer P, Spiteri C. New insights into Early Celtic consumption practices: organic residue analyses of local and imported pottery from Vix-Mont Lassois. PLoS One, 2019, 14(6):e0218001. doi: 10.1371/journal.pone.0218001
[18]	Shevchenko A, Yang YM, Knaust A, Thomas H, Jiang HE, Lu EG, Wang CS, Shevchenko A. Proteomics identifies the composition and manufacturing recipe of the 2500-year old sourdough bread from Subeixi cemetery in China. J Proteomics, 2014, 105:363-371. doi: 10.1016/j.jprot.2013.11.016 pmid: 24291353
[19]	Henderson JS, Joyce RA, Hall GR, Hurst WJ, McGovern PE. Chemical and archaeological evidence for the earliest cacao beverages. Proc Natl Acad Sci USA, 2007, 104(48):18937-18940. doi: 10.1073/pnas.0708815104
[20]	Mcgovern PE. Ancient wine: the search for the origins of viniculture. Economic Botany, 2003, 58:488. doi: 10.1663/0013-0001(2004)058[0488:DFABRE]2.0.CO;2
[21]	Mcgovern P, Jalabadze M, Batiuk S, Callahan MP, Smith KE, Hall GR, Kvavadze E, Maghradze D, Rusishvili N, Bouby L, Failla O, Cola G, Mariani L, Boaretto E, Bacilieri R, This P, Wales N, Lordkipanidze D. Early Neolithic wine of Georgia in the South Caucasus. Proc Natl Acad Sci USA, 2017, 114(48):E10309-E10318.
[22]	McGovern PE, Mirzoian A, Hall GR. Ancient Egyptian herbal wines. Proc Natl Acad Sci USA, 2009, 106(18):7361-7366. doi: 10.1073/pnas.0811578106
[23]	Manzano E, Cantarero S, García A, Adroher A, Vílchez JL. A multi-analytical approach applied to the archaeological residues in Iberian glasses. Earliest evidences on the consumption of fermented beverages in votive rituals. Microchem J, 2016, 129:286-292. doi: 10.1016/j.microc.2016.07.006
[24]	Mcclure SB, Magill C, Podrug E, Moore AMT, Harper TK, Culleton BJ, Kennett DJ, Freeman KHF. Fatty acid specific δ13C values reveal earliest Mediterranean cheese production 7,200 years ago. PLoS One, 2018, 13(9):e0202807. doi: 10.1371/journal.pone.0202807
[25]	Yang YM, Shevchenko A, Knaust A, Abuduresule I, Li WY, Hu XJ, Wang CS, Shevchenko A. Proteomics evidence for kefir dairy in Early Bronze Age China. J Archaeol Sci, 2014, 45:178-186. doi: 10.1016/j.jas.2014.02.005
[26]	Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, Merlevede A, Roncoroni M, Voordeckers K, Miraglia L, Teiling C, Steffy B, Taylor M, Schwartz A, Richardson T, White C, Baele G, Maere S, Verstrepen KJ. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell, 2016, 166(6): 1397-1410.e16. doi: 10.1016/j.cell.2016.08.020
[27]	Marsit S, Sanchez I, Galeote V, Dequin S. Horizontally acquired oligopeptide transporters favour adaptation of Saccharomyces cerevisiae wine yeast to oenological environment. Environ Microbiol, 2016, 18(4):1148-1161. doi: 10.1111/1462-2920.13117
[28]	Pérez-Ortín J, Querol A, Puig S, Barrio E. Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res, 2002, 12(10):1533-1539. pmid: 12368245
[29]	Warringer J, Zörgö E, Cubillos FA, Zia A, Gjuvsland A, Simpson JT, Forsmark A, Durbin R, Omholt SW, Louis EJ, Liti G, Moses A, Blomberg A. Trait variation in yeast is defined by population history. PLoS Genet, 2011, 7(6):e1002111. doi: 10.1371/journal.pgen.1002111
[30]	Fijarczyk A, Hénault M, MaRsit S, Charron G, Fischborn T, Nicole-Labrie L, Landry CR. The genome sequence of the Jean-Talon strain, an archeological beer yeast from Québec, reveals traces of adaptation to specific brewing conditions. G3 (Bethesda), 2020, 10(9):3087-3097. doi: 10.1534/g3.120.401149
[31]	Legras J-L, Galeote V, Bigey F, Camarasa C, Marsit S, Nidelet T, Sanchez I, Couloux A, Guy J, Franco-Duarte R, Marcet-Houben M, Gabaldon T, Schuller D, Sampaio JP, Dequin S. Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Mol Biol Evol, 2018, 35(7):1712-1727. doi: 10.1093/molbev/msy066
[32]	Erny C, Raoult P, Alais A, Butterlin G, Delobel P, Matei- Radoi F, Casaregola S, Legras JL. Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the Northern European wine-making environment. Appl Environ Microbiol, 2012, 78(9):3256-3265. doi: 10.1128/AEM.06752-11
[33]	Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, Nielly-Thibault L, Leducq JB, Landry CR, Gonçalves P, Rosa CA, Sampaio JP. Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biol Evol, 2016, 8(2):317-329. doi: 10.1093/gbe/evv263 pmid: 26782936
[34]	Price CE, Zeyniyev A, Kuipers OP, Kok J. From meadows to milk to mucosa-adaptation of Streptococcus and Lactococcus species to their nutritional environments. FEMS Microbiol Rev, 2012, 36(5):949-971. doi: 10.1111/j.1574-6976.2011.00323.x
[35]	Cavanagh D, Fitzgerald GF, McAuliffe O. From field to fermentation: the origins of Lactococcus lactis and its domestication to the dairy environment. Food Microbiol, 2015, 47:45-61. doi: 10.1016/j.fm.2014.11.001 pmid: 25583337
[36]	Wels M, Siezen R, van Hijum S, Kelly WJ, Bachmann H. Comparative genome analysis of Lactococcus lactis indicates niche adaptation and resolves genotype/phenotype disparity. Front Microbiol, 2019, 10:4. doi: 10.3389/fmicb.2019.00004
[37]	G-Alegrı́a E, López I, Ruiz JI, Sáenz J, Fernández E, Zarazaga M, Dizy M, Torres C, Ruiz-Larrea F. High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiol Lett, 2004, 230(1):53-61. pmid: 14734166
[38]	Bartowsky EJ, Borneman AR. Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine. Appl Microbiol Biotechnol, 2011, 92(3):441-447. doi: 10.1007/s00253-011-3546-2 pmid: 21870044
[39]	Lorentzen MP, Campbell-Sills H, Jorgensen TS, Nielsen TK, Coton M, Coton E, Hansen L, Lucas PM. Expanding the biodiversity of Oenococcus oeni through comparative genomics of apple cider and kombucha strains. BMC Genomics, 2019, 20(1):330. doi: 10.1186/s12864-019-5692-3 pmid: 31046679
[40]	Cooper A, Poinar HN. Ancient DNA: do it right or not at all. Science, 2000, 289(5482):1139. pmid: 10970224
[41]	Briggs AW, Stenzel U, Meyer M, Krause J, Kircher M, Pääbo S. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res, 2010, 38(6):e87. doi: 10.1093/nar/gkp1163
[42]	Dabney J, Meyer M, Pääbo S. Ancient DNA damage. Cold Spring Harb Perspect Biol, 2013, 5(7):a012567.
[43]	Sawyer S, Krause J, Guschanski K, Savolainen V, Pääbo S. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS One, 2012, 7(3):e34131. doi: 10.1371/journal.pone.0034131
[44]	Llamas B, Valverde G, Fehren-Schmitz L, Weyrich LS, Cooper A, Haak W. From the field to the laboratory: controlling DNA contamination in human ancient DNA research in the high-throughput sequencing era. Sci Technol Archaeol Res, 2017, 3(1):1-14.
[45]	Chan JZM, Sergeant MJ, Lee OYC, Minnikin DE, Besra GS, Pap I, Spigelman M, Donoghue HD, Pallen MJ. Metagenomic analysis of Tuberculosis in a mummy. N Engl J Med, 2013, 369(3):289-290. doi: 10.1056/NEJMc1302295
[46]	Schuenemann VJ, Avanzi C, Krause-Kyora B, Seitz A, Herbig A, Inskip S, Bonazzi M, Reiter E, Urban C, Pedersen DD, Taylor GM, Singh P, Stewart GR, Velemínský P, Likovsky J, Marcsik A, Molnár E, Pálfi G, Mariotti V, Riga A, Belcastro MG, Boldsen JL, Nebel A, Mays S, Donoghue HD, Zakrzewski S, Benjak A, Nieselt K, Cole ST, Krause J. Ancient genomes reveal a high diversity of Mycobacterium leprae in medieval Europe. PLoS Pathog, 2018, 14(5):e1006997. doi: 10.1371/journal.ppat.1006997
[47]	Zhou ZM, Lundstrøm I, Tran-Dien A, Duchêne S, Alikhan NF, Sergeant MJ, Langridge G, Fotakis AK, Nair S, Stenøien HK, Hamre SS, Casjens S, Christophersen A, Quince C, Thomson NR, Weill FX, Ho SYW, Gilbert MTP, Achtman M. Pan-genome analysis of ancient and modern Salmonella enterica demonstrates genomic stability of the Invasive Para C lineage for Millennia. Curr Biol, 2018, 28(15): 2420-2428.e10. doi: 10.1016/j.cub.2018.05.058
[48]	Schuenemann VJ, Lankapalli AK, Barquera R, Nelson EA, Hernández DI, Alonzo VA, Bos KI, Morfín LM, Herbig A, Krause J. Historic Treponema pallidum genomes from Colonial Mexico retrieved from archaeological remains. PLoS Negl Trop Dis, 2018, 12(6):e0006447. doi: 10.1371/journal.pntd.0006447
[49]	Keller M, Spyrou MA, Scheib CL, Neumann GU, Kröpelin A, Haas-Gebhard B, Päffgen B, Haberstroh J, Lacomba ARI, Raynaud C, Cessford C, Durand R, Stadler P, Nägele K, Bates JS, Trautmann B, Inskip SA, Peters J, Robb JE, Kivisild T, Castex D, McCormick M, Bos KI, Harbeck M, Herbig A, Krause J. AncientYersinia pestis genomes from across Western Europe reveal early diversification during the First Pandemic (541-750). Proc Natl Acad Sci USA, 2019, 116(25):12363-12372. doi: 10.1073/pnas.1820447116
[50]	Adler CJ, Dobney K, Weyrich LS, Kaidonis J, Walker AW, Haak W, Bradshaw CJA, Townsend G, Sołtysiak A, Alt KW, Parkhill J, Cooper A. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet, 2013, 45(4):450-455. doi: 10.1038/ng.2536
[51]	Warinner C, Herbig A, Mann A, Yates JAF, Weiß CL, Burbano HA, Orlando L, Krause J. A robust framework for microbial archaeology. Annu Rev Genomics Hum Genet, 2017, 18:321-356. doi: 10.1146/annurev-genom-091416-035526
[52]	Campana MG, Robles García N, Rühli FJ, Tuross N. False positives complicate ancient pathogen identifications using high-throughput shotgun sequencing. BMC Res Notes, 2014, 7:111. doi: 10.1186/1756-0500-7-111
[53]	Weiß CL, Gansauge MT, Aximu-Petri A, Meyer M, Burbano HA. Mining ancient microbiomes using selective enrichment of damaged DNA molecules. BMC Genomics, 2020, 21(1):432. doi: 10.1186/s12864-020-06820-7
[54]	Ginolhac A, Rasmussen M, Gilbert MTP, Willerslev E, Orlando L. mapDamage: testing for damage patterns in ancient DNA sequences. Bioinformatics, 2011, 27(15):2153-2155. doi: 10.1093/bioinformatics/btr347
[55]	Hübler R, Key FM, Warinner C, Bos KI, Krause J, Herbig A. HOPS: automated detection and authentication of pathogen DNA in archaeological remains. Genome Biol, 2019, 20(1):280. doi: 10.1186/s13059-019-1903-0 pmid: 31842945
[56]	Rollo F, Luciani S, Marota I, Olivieri C, Ermini L. Persistence and decay of the intestinal microbiota’s DNA in glacier mummies from the Alps. J Archaeol Sci, 2007, 34(8):1294-1305. doi: 10.1016/j.jas.2006.10.019
[57]	Ziesemer KA, Mann AE, Sankaranarayanan K, Schroeder H, Ozga AT, Brandt BW, Zaura E, Waters-Rist A, Hoogland M, Salazar-García DC, Aldenderfer M, Speller C, Hendy J, Weston DA, MacDonald SJ, Thomas GH, Collins MJ, Lewis CM, Hofman C, Warinner C. Intrinsic challenges in ancient microbiome reconstruction using 16S rRNA gene amplification. Sci Rep, 2015, 5:16498. doi: 10.1038/srep16498 pmid: 26563586
[58]	Bidle KD, Lee S, Marchant DR, Falkowski PG. Fossil genes and microbes in the oldest ice on Earth. Proc Natl Acad Sci USA, 2007, 104(33):13455-13460. doi: 10.1073/pnas.0702196104
[59]	Fu QM, Meyer M, Gao X, Stenzel U, Burbano HA, Kelso J, Pääbo S. DNA analysis of an early modern human from Tianyuan Cave, China. Proc Natl Acad Sci USA, 2013, 110(6):2223-2227. doi: 10.1073/pnas.1221359110
[60]	Burbano HA, Green RE, Maricic T, Lalueza-Fox C, de la Rasilla M, Rosas A, Kelso J, Pollard KS, Lachmann M, Pääbo S. Analysis of human accelerated DNA regions using archaic hominin genomes. PLoS One, 2012, 7(3):e32877. doi: 10.1371/journal.pone.0032877
[61]	Burbano HA, Hodges E, Green RE, Briggs AW, Krause J, Meyer M, Good JM, Maricic T, Johnson PLF, Xuan ZY, Rooks M, Bhattacharjee A, Brizuela L, Albert FW, de la Rasilla M, Fortea J, Rosas A, Lachmann M, Hannon GJ, Pääbo S. Targeted investigation of the Neandertal genome by array-based sequence capture. Science, 2010, 328(5979):723-725. doi: 10.1126/science.1188046 pmid: 20448179
[62]	Avila-Arcos MC, Cappellini E, Romero-Navarro JA, Wales N, Moreno-Mayar JV, Rasmussen M, Fordyce SL, Montiel R, Vielle-Calzada JP, Willerslev E, Gilbert MTP. Application and comparison of large-scale solution-based DNA capture-enrichment methods on ancient DNA. Sci Rep, 2011, 1:74. doi: 10.1038/srep00074 pmid: 22355593
[63]	Slon V, Hopfe C, Weiß CL, Mafessoni F, de la Rasilla M, Lalueza-Fox C, Rosas A, Soressi M, Knul MV, Miller R, Stewart JR, Derevianko AP, Jacobs Z, Li B, Roberts RG, Shunkov MV, de Lumley H, Perrenoud C, Gušić I, Kućan Ž, Rudan P, Aximu-Petri A, Essel E, Nagel S, Nickel B, Schmidt A, Prüfer K, Kelso J, Burbano HA, Pääbo S, Meyer M. Neandertal and Denisovan DNA from Pleistocene sediments. Science, 2017, 356(6338):605-608. doi: 10.1126/science.aam9695
[64]	Rivera-Perez JI, Santiago-Rodriguez TM, Toranzos GA. Paleomicrobiology: a snapshot of ancient microbes and approaches to forensic microbiology. Microbiol Spectr, 2016, 4(4).
[65]	Donoghue HD, Spigelman M, Greenblatt CL, Lev-Maor G, Bar-Gal GK, Matheson C, Vernon K, Nerlich AG, Zink AR. Tuberculosis: from prehistory to Robert Koch, as revealed by ancient DNA. Lancet Infect Dis, 2004, 4(9):584-592. pmid: 15336226

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

发酵食品类别	食品举例	考古发现或文献记载的最早生产地点和时间	参考文献
乳制品	各类酸奶和乳酪,如Dahi、Kefir、Kumys等	西亚地区,约公元前6000年	[3]
谷物和豆制品	各类面包、发酵面饼,以及酱油、味噌等	东亚地区,约公元前1000年	[5]
植物根茎制品	Gari、Fufu等非洲地区传统食品	-	-
果蔬制品	酒精饮料,以及Sauerkraut、Kimchi等一些腌制蔬菜	中国,约公元前7000年	[2]
鱼制品	鱼露、鱼酱和一些腌制鱼	欧洲地区,公元前500年至公元500年	[6]
肉制品	一些腌制肉(猪肉、牛肉等)和香肠	中国,约公年前1500年	[7]

Exploration of adaptation, evolution and domestication of fermentation microorganisms by applying ancient DNA technology

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 2

References 65

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Chaofan Xing, Mintao Wang, Lei Wang, Xin Shen. Progress on the mechanism of left-right asymmetrical patterning in bilaterians [J]. Hereditas(Beijing), 2023, 45(6): 488-500.
[2]	Mingliang Jiang, Hong Lang, Xiaonan Li, Ye Zu, Jing Zhao, Shenling Peng, Zhen Liu, Zongxiang Zhan, Zhongyun Piao. Progress on plant orphan genes [J]. Hereditas(Beijing), 2022, 44(8): 682-694.
[3]	Wanjing Ping, Yichen Liu, Qiaomei Fu. Exploring the evolution of archaic humans through sedimentary ancient DNA [J]. Hereditas(Beijing), 2022, 44(5): 362-369.
[4]	Shanshan Gao, Jinliang Li, Jiani Yang, Tong Zhou, Rui Liu, Xiaoping Wang, Li Yu. Progresses on adaptive evolution of gliding and flying ability in mammals [J]. Hereditas(Beijing), 2022, 44(1): 46-58.
[5]	Shan Li, Yunzhi Huang, Xueying Liu, Xiangdong Fu. Genetic improvement of nitrogen use efficiency in crops [J]. Hereditas(Beijing), 2021, 43(7): 629-641.
[6]	Hengxing Ba, Pengfei Hu, Chunyi Li. Progress on deer genome research [J]. Hereditas(Beijing), 2021, 43(4): 308-322.
[7]	Menggang Lv, Aijia Liu, Qingwei Li, Peng Su. Progress on the origin, function and evolutionary mechanism of RHR transcription factor family [J]. Hereditas(Beijing), 2021, 43(3): 215-225.
[8]	Yuxing Zhang, Hong Wu, Li Yu. Progress on coat color regulation mechanism and its association with the adaptive evolution in mammals [J]. Hereditas(Beijing), 2021, 43(2): 118-133.
[9]	Yigao Zhu, Jun Li, Yue Pang, Qingwei Li. Lamprey: an important animal model of evolution and disease research [J]. Hereditas(Beijing), 2020, 42(9): 847-857.
[10]	Linan Zhao, Na Wang, Guoliang Yang, Xianbin Su, Zeguang Han. A method for reliable detection of genomic point mutations based on single-cell target-sequencing [J]. Hereditas(Beijing), 2020, 42(7): 703-712.
[11]	Fengyue Hu, Kejian Wang. The STEME system: a novel tool for directed evolution in vivo [J]. Hereditas(Beijing), 2020, 42(3): 231-235.
[12]	Lianchao Tang, Feng Gu. Next-generation CRISPR-Cas for genome editing: focusing on the Cas protein and PAM [J]. Hereditas(Beijing), 2020, 42(3): 236-249.
[13]	Zhichao Mei, Zhujun Wei, Jiahui Yu, Fengdan Ji, Linan Xie. Multi-omics association analysis revealed the role and mechanism of epialleles in environmental adaptive evolution of Arabidopsis thaliana [J]. Hereditas(Beijing), 2020, 42(3): 321-331.
[14]	Wei Peng, Mengjie Feng, Hao Chen, Baoyu Han. Progress on genome sequencing of Dipteran insects [J]. Hereditas(Beijing), 2020, 42(11): 1093-1109.
[15]	Xiaoli Shi,Yilin He,Hongqing Ling. Progress on wheat A genome illustration and its evolutional analysis [J]. Hereditas(Beijing), 2019, 41(9): 836-844.