Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (7): 1469-1478.doi: 10.3864/j.issn.0578-1752.2022.07.017


Distribution Characteristics of Prophage in Multidrug Resistant Escherichia coli as well as Its Induction and Isolation

LIU Jiao(),LIU Chang,CHEN Jin,WANG MianZhi,XIONG WenGuang,ZENG ZhenLing()   

  1. South China Agriculture University/Guangdong Provincial Key Laboratory of Veterinary Pharmaceutics Development and Safety Evaluation/National Risk Assessment Laboratory for Antimicrobial Resistance of Animal Original Bacteria, Guangzhou 510642
  • Received:2021-02-06 Accepted:2021-09-30 Online:2022-04-01 Published:2022-04-18
  • Contact: ZhenLing ZENG;


【Objective】 This study investigated the distribution characteristics of prophage in multi-drug resistant Escherichia coli, induction and isolation, as well as the prevalence of drug resistance and virulence genes in prophage, so as to provide a scientific basis for the study of prophage-mediated resistance genes in the spread of bacteria. 【Method】 131 multi-drug resistant E. coli isolating from poultry origin in Guangdong Province from 2018 to 2019 were selected in the laboratory for nucleic acid extraction and whole-genome sequencing. The results of second-generation sequencing were assembled and spliced into a whole-genome sequence and uploaded to the phage. The PHASTER network database was compared and analyzed with the existing phage genome sequences in the database. Drug resistance genes and virulence genes were compared on the CGE database, and then the distribution of drug resistance genes and virulence genes on the prophage were obtained. The mild phage was induced by mitomycin C, separated and purified by using the double-layer plate method. 【Result】 The results of the drug sensitivity test of 131 strains of Escherichia coli showed that the drug resistance rates of ampicillin, tetracycline, florfenicol and compound trimethoprim were all more than 90%, followed by cephalosporin antibiotics, gentamicin, ciprofloxacin, meropenem and colistin with all around 50%, and the resistance rate of tigecycline reached 0.2%. All strains showed multi-drug resistance, and they were all multi-drug resistant Escherichia coli. A total of 736 prophage fragments were detected in 131 strains of multi-drug resistant E. coli, including 329 complete prophage, 66 suspicious phages and 341 incomplete phage, which matched with 40, 20 and 52 known database phage species in different percentages, respectively. The gene sequence of the complete prophage showed that it matched the known phage species better, and the sequence similarity was the highest, with an average of 58.53%. The average number of prophages in 131 strains of E. coli was 5.6, and the average total content was 152.4 kb. Prophage genome accounted for 0.58% to 5.87% of its host genome, with 3.0% being the dominant. The length of the prophage genome ranged from 2.8 to 107.9 kb, and the 13.0 kb prophage had the highest frequency, accounting for 9.1% of all prophages. CGE comparison results showed that the genomes of 131 strains of multi-drug-resistant E. coli detected resistance genes mdf (A), lnu (G) and mcr-1 in 18 prophage sequences. The detected numbers of mdf (A), lnu (G) and mcr-1 were 16, 1, and 1, respectively. 71 strains of multi-drug resistant E. coli prophage carried 6 different virulence genes, and some strains carried 2 or 3 virulence genes. There were 62 prophages carrying the telomerase RNA gene terC, 16 prophages carrying the serum survival increasing gene iss, and the outer membrane protease ompT, among which the adhesin gene iha, the cvaC gene and the ABC transporter gene mchF were at 2, 2, 1, and 1, respectively. Mcr-a gene were detected in prophage of 1 strain multi-drug resistant Escherichia coli. The mdf (A) gene and terC gene were the most common resistance genes and virulence genes in prophage, respectively. The results of mild phage induction experiments showed that the success rate of prophage induction was 84.0%, but the probability of plaque appearance was still relatively low. 【Conclusion】Prophages were widely distributed in multi-drug resistant E. coli and carried a variety of resistance genes and virulence genes. Mild phages had a high induction rate, and have the risk of horizontal transmission of resistance genes and virulence genes, and need to be strengthened and sustained monitor.

Key words: prophage, Escherichia coli, induction, distribution characteristics, resistance genes

Fig. 1

Results of antimicrobial susceptibility test AMP, Ampicillin; CTX, Cefotaxime; CAZ, ceftazidime; MEM, Meropenem; GEN, Gentamicin; AMI, amikacin; TET, tetracycline; TIG, tigecycline; FLR, Florfenicol; CL, Colistin; CIP, Ciprofloxacin; SXT, Cotrimoxazole"

Fig. 2

The length contribution percentage of the prophage prophage to its host genome"

Fig. 3

Probability distribution of with different genomic lengths"

Fig. 4

Percentage of similarity between pre-phage and known database phage genomes"

Fig. 5

Distribution of drug resistance genes on prophages"

Fig. 6

Distribution of virulence genes in prophages"

[1] SALMOND G P C, FINERAN P C. A century of the phage: Past, present and future. Nature Reviews Microbiology, 2015, 13(12):777-786. doi: 10.1038/nrmicro3564.
doi: 10.1038/nrmicro3564
[2] HOBBS Z, ABEDON S T. Diversity of phage infection types and associated terminology: The problem with ‘Lytic or lysogenic'. FEMS Microbiology Letters, 2016, 363(7):47. doi: 10.1093/femsle/fnw047.
doi: 10.1093/femsle/fnw047
[3] MAVRICH T N, CASEY E, OLIVEIRA J, BOTTACINI F, JAMES K, FRANZ C M A P, LUGLI G A, NEVE H, VENTURA M, HATFULL G F, MAHONY J, VAN SINDEREN D. Characterization and induction of prophages in human gut-associated Bifidobacterium hosts. Scientific Reports, 2018, 8(1):12772. doi: 10.1038/s41598-018-31181-3.
doi: 10.1038/s41598-018-31181-3
[4] TORRES-BARCELÓ C. The disparate effects of bacteriophages on antibiotic-resistant bacteria. Emerging Microbes & Infections, 2018, 7(1):168. doi: 10.1038/s41426-018-0169-z.
doi: 10.1038/s41426-018-0169-z
[5] SCHMIEGER H, SCHICKLMAIER P. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiology Letters, 1999, 170(1):251-256. doi: 10.1111/j.1574-6968.1999.tb13381.x.
doi: 10.1111/j.1574-6968.1999.tb13381.x
[6] DAVIES E V, JAMES C E, WILLIAMS D, O'BRIEN S, FOTHERGILL J L, HALDENBY S, PATERSON S, WINSTANLEY C, BROCKHURST M A. Temperate phages both mediate and drive adaptive evolution in pathogen biofilms. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(29):8266-8271. doi: 10.1073/pnas.1520056113.
doi: 10.1073/pnas.1520056113
[7] CHEN J, QUILES-PUCHALT N, CHIANG Y N, BACIGALUPE R, FILLOL-SALOM A, CHEE M S J, FITZGERALD J R, PENADÉS J R. Genome hypermobility by lateral transduction. Science, 2018, 362(6411):207-212. doi: 10.1126/science.aat5867.
doi: 10.1126/science.aat5867
[8] SONG W, STEENSEN K, THOMAS T. HgtSIM: A simulator for horizontal gene transfer (HGT) in microbial communities. PeerJ, 2017, 5:e4015. doi: 10.7717/peerj.4015.
doi: 10.7717/peerj.4015
[9] VON WINTERSDORFF C J, PENDERS J, VAN NIEKERK J M, MILLS N D, MAJUMDER S, VAN ALPHEN L B, SAVELKOUL P H, WOLFFS P F. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Frontiers in Microbiology, 2016, 7:173. doi: 10.3389/fmicb.2016.00173.
doi: 10.3389/fmicb.2016.00173
[10] LERMINIAUX N A, CAMERON A D S. Horizontal transfer of antibiotic resistance genes in clinical environments. Canadian Journal of Microbiology, 2019, 65(1):34-44. doi: 10.1139/cjm-2018-0275.
doi: 10.1139/cjm-2018-0275
[11] SHANG Y, LI D, HAO W, SCHWARZ S, SHAN X, LIU B, ZHANG S M, LI X S, DU X D. A prophage and two ICESa2603-family integrative and conjugative elements (ICEs) carrying optrA in Streptococcus suis. The Journal of Antimicrobial Chemotherapy, 2019, 74:2876-2879.
doi: 10.1093/jac/dkz309
[12] HÅFSTRÖM T, JANSSON D S, SEGERMAN B. Complete genome sequence of Brachyspira intermedia reveals unique genomic features in Brachyspira species and phage-mediated horizontal gene transfer. BMC Genomics, 2011, 12(1):395. doi: 10.1186/1471-2164-12-395.
doi: 10.1186/1471-2164-12-395
[13] SHAABAN S, COWLEY L A, MCATEER S P, JENKINS C, DALLMAN T J, BONO J L, GALLY D L. Evolution of a zoonotic pathogen: Investigating prophage diversity in enterohaemorrhagic Escherichia coli O157 by long-read sequencing. Microbial Genomics, 2016, 2(12):e000096. doi: 10.1099/mgen.0.000096.
doi: 10.1099/mgen.0.000096
[14] PLEŠKA M, LANG M, REFARDT D, LEVIN B R, GUET C C. Phage-host population dynamics promotes prophage acquisition in bacteria with innate immunity. Nature Ecology & Evolution, 2018, 2(2):359-366. doi: 10.1038/s41559-017-0424-z.
doi: 10.1038/s41559-017-0424-z
[15] GOH S, HUSSAIN H, CHANG B J, EMMETT W, RILEY T V, MULLANY P. Phage ϕC2 mediates transduction of Tn6215, encoding erythromycin resistance, between Clostridium difficile strains. mBio, 2013, 4(6):e00840-e00813. doi: 10.1128/mbio.00840-13.
doi: 10.1128/mbio.00840-13
[16] LOHB, CHEN J, MANOHAR P, YU Y, HUA X, LEPTIHN S. A biological inventory of prophages in A. baumannii genomes reveal distinct distributions in classes, length, and genomic positions. Woqumaid, 2020, 11:579802.
[17] COLAVECCHIO A, CADIEUX B, LO A, GOODRIDGE L D. Bacteriophages contribute to the spread of antibiotic resistance genes among foodborne pathogens of the Enterobacteriaceae family-A review. Frontiers in Microbiology, 2017, 8:1108. doi: 10.3389/fmicb.2017.01108.
doi: 10.3389/fmicb.2017.01108
[18] MOHAN RAJ J R, VITTAL R, HUILGOL P, BHAT U, KARUNASAGAR I. T4-like Escherichia coli phages from the environment carry blaCTX-M. Letters in Applied Microbiology, 2018, 67(1):9-14. doi: 10.1111/lam.12994.
doi: 10.1111/lam.12994
[19] ZINDER N D, LEDERBERG J. Genetic exchange in Salmonella. Journal of Bacteriology, 1952, 64(5):679-699. doi: 10.1128/jb.64.5.679-699.1952.
doi: 10.1128/jb.64.5.679-699.1952 pmid: 12999698
[20] MAHONY J, VAN SINDEREN D. The impact and applications of phages in the food industry and agriculture. Viruses, 2020, 12(2):210. doi: 10.3390/v12020210.
doi: 10.3390/v12020210
[21] ANDERSSON D I, HUGHES D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nature Reviews Microbiology, 2010, 8(4):260-271. doi: 10.1038/nrmicro2319.
doi: 10.1038/nrmicro2319
[22] COLOMER-LLUCH M, IMAMOVIC L, JOFRE J, MUNIESA M. Bacteriophages carrying antibiotic resistance genes in fecal waste from cattle, pigs, and poultry. Antimicrobial Agents and Chemotherapy, 2011, 55(10):4908-4911. doi: 10.1128/aac.00535-11.
doi: 10.1128/aac.00535-11
[23] COLOMER-LLUCH M, JOFRE J, MUNIESA M. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS ONE, 2011, 6(3). doi: 10.1371/journal.pone.0017549.
doi: 10.1371/journal.pone.0017549
[24] LEKUNBERRI I, SUBIRATS J, BORREGO C M, BALCÁZAR J L. Exploring the contribution of bacteriophages to antibiotic resistance. Enviromental Pollution, 2017, 220(pt b):981-984. doi: 10.1016/j.envpol.2016.11.059.
doi: 10.1016/j.envpol.2016.11.059
[25] SHOUSHA A, AWAIWANONT N, SOFKA D, SMULDERS F J, PAULSEN P, SZOSTAK M P, HUMPHREY T, HILBERT F. Bacteriophages isolated from chicken meat and the horizontal transfer of antimicrobial resistance genes. Applied and Environmental Microbiology, 2015, 81(14):4600-4606. doi: 10.1128/aem.00872-15.
doi: 10.1128/aem.00872-15
[26] NOVICK R P, CHRISTIE G E, PENAD S J R. The phage-related chromosomal islands of Gram-positive bacteria. Nature Reviews Microbiology, 2010, 8:541-551.
doi: 10.1038/nrmicro2393
[27] VARGA M, KUNTOVÁ L, PANTŮČEK R, MAŠLAŇOVÁ I, RŮŽIČKOVÁ V, DOŠKAŘ J. Efficient transfer of antibiotic resistance plasmids by transduction within methicillin-resistant Staphylococcus aureus USA300 clone. FEMS Microbiology Letters, 2012, 332(2):146-152. doi: 10.1111/j.1574-6968.2012.02589.x.
doi: 10.1111/j.1574-6968.2012.02589.x
[28] MAZAHERI NEZHAD FARD R, BARTON M D, HEUZENROEDER M W. Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Letters in Applied Microbiology, 2011, 52(6):559-564. doi: 10.1111/j.1472-765x.2011.03043.x.
doi: 10.1111/j.1472-765x.2011.03043.x
[29] DEDRICK R M, JACOBS-SERA D, BUSTAMANTE C A, GARLENA R A, MAVRICH T N, POPE W H, REYES J C, RUSSELL D A, ADAIR T, ALVEY R, et al. Prophage-mediated defence against viral attack and viral counter-defence. Nature Microbiology, 2017, 2:16251.
doi: 10.1038/nmicrobiol.2016.251
[30] TRAN P M, FEISS M. φSa3mw Prophage as a Molecular Regulatory Switch of Staphylococcus aureus β -Toxin Production. 2019, 201(14):e00766-18. doi: 10.1128/JB.00766-18.
doi: 10.1128/JB.00766-18
[31] OGATA S, SUENAGA H, HAYASHIDA S. A temperate phage of Streptomyces azureus. Applied and Environmental Microbiology, 1985, 49(1):201-204. doi: 10.1128/aem.49.1.201-204.1985.
doi: 10.1128/aem.49.1.201-204.1985
[32] JOFRE J, MUNIESA M. Bacteriophage isolation and characterization: phages of Escherichia coli. Methods in Molecular Biology (Clifton, N J), 2020, 2075:61-79. doi: 10.1007/978-1-4939-9877-7_4.
doi: 10.1007/978-1-4939-9877-7_4
[33] ARNDT D, MARCU A, LIANG Y, WISHART D S. PHAST, PHASTER and PHASTEST: Tools for finding prophage in bacterial genomes. Briefings in Bioinformatics, 2019, 20(4):1560-1567. doi: 10.1093/bib/bbx121.
doi: 10.1093/bib/bbx121
[34] WANG D, LIANG H, CHEN J, MOU Y, QI Y. Structural and environmental features of novel mdfA variant and mdfA genes in recombinant regions of Escherichia coli. Microbial Drug Resistance (Larchmont, N Y), 2014, 20(5):392-398. doi: 10.1089/mdr.2013.0201.
doi: 10.1089/mdr.2013.0201
[35] BATTAGLIOLI E J, BAISA G A, WEEKS A E, SCHROLL R A, HRYCKOWIAN A J, WELCH R A. Isolation of generalized transducing bacteriophages for uropathogenic strains of Escherichia coli. Applied and Environmental Microbiology, 2011, 77(18):6630-6635. doi: 10.1128/aem.05307-11.
doi: 10.1128/aem.05307-11
[36] ZHANG A, CALL D R, BESSER T E, LIU J, JONES L, WANG H, DAVIS M A. Β-lactam resistance genes in bacteriophage and bacterial DNA from wastewater, river water, and irrigation water in Washington State. Water Research, 2019, 161:335-340. doi: 10.1016/j.watres.2019.06.026.
doi: 10.1016/j.watres.2019.06.026
[37] CALERO-CÁCERES W, YE M, BALCÁZAR J L. Bacteriophages as environmental reservoirs of antibiotic resistance. Trends in Microbiology, 2019, 27(7):570-577. doi: 10.1016/j.tim.2019.02.008.
doi: 10.1016/j.tim.2019.02.008
[38] GARIN-FERNANDEZ A, PEREIRA-FLORES E, GLÖCKNER F O, WICHELS A. The North Sea Goes viral: Occurrence and distribution of North Sea bacteriophages. Marine Genomics, 2018, 41:31-41. doi: 10.1016/j.margen.2018.05.004.
doi: 10.1016/j.margen.2018.05.004
[39] WENDLING C C, REFARDT D, HALL A R. Fitness benefits to bacteria of carrying prophages and prophage-encoded antibiotic- resistance genes peak in different environments. BioRxiv, 2020. DOI: 10.1101/2020.03.13.990044.
doi: 10.1101/2020.03.13.990044
[40] LEKUNBERRI I, VILLAGRASA M, BALCÁZAR J L, BORREGO C M. Contribution of bacteriophage and plasmid DNA to the mobilization of antibiotic resistance genes in a river receiving treated wastewater discharges. The Science of the Total Environment, 2017, 601/602:206-209. doi: 10.1016/j.scitotenv.2017.05.174.
doi: 10.1016/j.scitotenv.2017.05.174
[41] WANG M, XIONG W, LIU P, XIE X, ZENG J, SUN Y, ZENG Z. Metagenomic insights into the contribution of phages to antibiotic resistance in water samples related to swine feedlot wastewater treatment. Frontiers in Microbiology, 2018, 9:2474. doi: 10.3389/fmicb.2018.02474.
doi: 10.3389/fmicb.2018.02474
[42] PAN Y, FANG Y, FENG Y, LYU N, CHEN L, LI J, XU X, ZHU B, HU Y. Discovery of mcr-3.1 gene carried by a prophage located in a conjugative IncA/C2 plasmid from a Salmonella Choleraesuis clinical isolate. The Journal of Infection, 2021, 82(3):414-451. doi: 10.1016/j.jinf.2020.09.036.
doi: 10.1016/j.jinf.2020.09.036
[43] LOH B, CHEN J, MANOHAR P, YU Y, HUA X, LEPTIHN S. A biological inventory of prophages in A. baumannii genomes reveal distinct distributions in classes, length, and genomic positions. Frontiers in Microbiology, 2020, 11:579802.
doi: 10.3389/fmicb.2020.579802
[44] HSU B B, WAY J C, SILVER P A. Stable neutralization of a virulence factor in bacteria using temperate phage in the mammalian gut. mSystems, 2020, 5.
[45] MOLINA F, SIMANCAS A, TABLA R, GÓMEZ A, ROA I, REBOLLO J E. Diversity and local coadaptation of Escherichia coli and coliphages from small ruminants. Frontiers in Microbiology, 2020, 11:564522. doi: 10.3389/fmicb.2020.564522.
doi: 10.3389/fmicb.2020.564522
[46] FRY B A. Conditions for the infection of Escherichia coli with lambda phage and for the establishment of lysogeny. Journal of General Microbiology, 1959, 21:676-684.
pmid: 13825457
[47] IMAMOVIC L, BALLESTÉ E, MARTÍNEZ-CASTILLO A, GARCÍA- ALJARO C, MUNIESA M. Heterogeneity in phage induction enables the survival of the lysogenic population. Environmental Microbiology, 2016, 18(3):957-969. doi: 10.1111/1462-2920.13151.
doi: 10.1111/1462-2920.13151
[48] RUIZ-CRUZ S, PARLINDUNGAN E, ERAZO GARZON A, ALQARNI M, LUGLI G A. Lysogenization of a lactococcal host with three distinct temperate phages provides homologous and heterologous phage resistance. Microorganisms, 2020, 8(11). doi. 10.3390/microorganisms8111685.
doi: 10.3390/microorganisms8111685
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