Abstract
Aims
The mechanisms of weed resistance to herbicides are generally thought to include alteration of the target site, enhanced detoxification, and sequestration. Endophytes can promote plant growth and enhance tolerance to abiotic stress. To date, how endophytes affect weed resistance to herbicides has not been reported.
Methods
The dose-response tests performed on the derived seed batches in our study were used to test the toxicity of Polypogon fugax to quizalofop-p-ethyl. The endophytes were isolated, and the degradation rate of endophytes to quizalofop-p-ethyl was measured. The endophyte was inoculated onto the susceptible P. fugax using inoculation techniques. The effect of germicide on the toxicity of quizalofop-p-ethyl to the resistant P. fugax plants was observed.
Results
Resistance was confirmed in several tested P. fugax populations. Among them, the population collected from Qingshen County, Sichuan Province (QCSP) had the highest resistance index. The number and degradation rate of quizalofop-p-ethyl degrading endophytes was lower in the susceptible population than in the QCSP resistant population. The isolated KT4 strain from the QCSP population had the highest degradation rate. The 16S rDNA sequence of KT4 was identical to that of Sphingomonas sp. The treatments that contain inoculating endophytes KT4 enhanced the resistance to quizalofop-p-ethyl in the susceptible population. Treatments containing a combination of quizalofop-p-ethyl with either kasugamycin or jinggangmycin, which can kill or inhibit endophytes growth, reduced the resistance level of the QCSP population to quizalofop-p-ethyl.
Conclusions
This is the first report that endophytes can degrade quizalofop-p-ethyl to enhance resistance in P. fugax.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588. https://doi.org/10.1038/nbt960
Beckie HJ, Tardif FJ (2012) Herbicide cross resistance in weeds. Crop Protect 35:15–28. https://doi.org/10.1016/j.cropro.2011.12.018
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
Cheng DF, Guo ZJ, Riegler M, Xi ZY, Liang GW, Xu YJ (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5:13. https://doi.org/10.1186/s40168-017-0236-z
Dong W, Hou Y, Xi X, Wang F, Li Z, Ye X, Huang Y, Cui Z (2015) Biodegradation of fenoxaprop-ethyl by an enriched consortium and its proposed metabolic pathway. Int Biodeterior Biodegrad 97:159–167. https://doi.org/10.1016/j.ibiod.2014.10.009
Dupont PY, Eaton CJ, Wargent JJ, Fechtner S, Solomon P, Schmid J, Day RC, Scott B, Cox MP (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208:1227–1240. https://doi.org/10.1111/nph.13614
Edwards R, Hannah M (2014) Focus on weed control. Plant Physiol 166:1087–1089. https://doi.org/10.1104/pp.114.900496
Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302–310. https://doi.org/10.1111/j.1574-6941.2006.00121.x
Huan Z, Zhang H, Hou Z, Zhang S, Zhang Y, Liu W, Bi Y, Wang J (2011) Resistance level and metabolism of barnyard-grass (Echinochloa crusgalli (L.) Beauv.) populations to quizalofop-p-ethyl in Heilongjiang Province, China. Agric Sci China 10:1914–1922. https://doi.org/10.1016/s1671-2927(11)60192-2
Itoh H, Hori T, Sato Y, Nagayama A, Tago K, Hayatsu M, Kikuchi Y (2018) Infection dynamics of insecticide-degrading symbionts from soil to insects in response to insecticide spraying. ISME J 12:909–920. https://doi.org/10.1038/s41396-017-0021-9
Jabeen H, Iqbal S, Ahmad F, Afzal M, Firdous S (2016) Enhanced remediation of chlorpyrifos by ryegrass (Lolium multiflorum) and a chlorpyrifos degrading bacterial endophyte Mezorhizobium sp. HN3. Int J Phytorem 18:126–133. https://doi.org/10.1080/15226514.2015.1073666
Khan AL, Waqas M, Kang S-M, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung H-Y, Lee I-J (2014a) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695. https://doi.org/10.1007/s12275-014-4002-7
Khan Z, Roman D, Kintz T, delas Alas M, Yap R, Doty S (2014b) Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ Sci Technol 48:12221–12228. https://doi.org/10.1021/es503880t
Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622. https://doi.org/10.1073/pnas.1200231109
Kumar J, D’Souza SF (2010) An optical microbial biosensor for detection of methyl parathion using Sphingomonas sp. immobilized on microplate as a reusable biocomponent. Biosens Bioelectron 26:1292–1296. https://doi.org/10.1016/j.bios.2010.07.016
Kumar A, Trefault N, Olaniran AO (2014) Microbial degradation of 2, 4-dichlorophenoxyacetic acid: insight into the enzymes and catabolic genes involved, their regulation and biotechnological implications. Crit Rev Microbiol 1–15
Li X, He J, Li S (2007) Isolation of a chlorpyrifos-degrading bacterium, Sphingomonas sp. strain Dsp-2, and cloning of the mpd gene. Res Microbiol 158:143–149. https://doi.org/10.1016/j.resmic.2006.11.007
Liu Y (2014) Ecological characteristics of Polypogon fugax and resistance to quizalofop-p-ethyl in rape(Brassica campestris) field. Hunan agricultural university, Changsha
Liu M, Luo K, Wang Y, Zeng A, Zhou X, Luo F, Bai L (2014) Isolation, identification and characteristics of an endophytic quinclorac degrading Bacterium Bacillus megaterium Q3. PLoS One 9:e108012. https://doi.org/10.1371/journal.pone.0108012
McGuinness MC, Mazurkiewicz V, Brennan E, Dowling DN (2007) Dechlorination of pesticides by a specific bacterial glutathione S-transferase, BphKLB400: potential for bioremediation. Eng Life Sci 7:611–615. https://doi.org/10.1002/elsc.200720218
Mirzahosseini Z, Shabani L, Sabzalian MR, Sharifi-Tehrani M (2014) Neotyphodium endophytes may increase tolerance to Ni in tall fescue. Eur J Soil Biol 63:33–40. https://doi.org/10.1016/j.ejsobi.2014.05.004
Newman DJ, Cragg GM (2015) Endophytic and epiphytic microbes as “sources” of bioactive agents. Front Chem 3. https://doi.org/10.3389/fchem.2015.00034
Shaw LJ, Burns RG (2004) Enhanced mineralization of [U-14C] 2, 4-dichlorophenoxyacetic acid in soil from the rhizosphere of Trifolium pratense. Appl Environ Microbiol 70:4766–4774
Sheng X, Chen X, He L (2008) Characteristics of an endophytic pyrene-degrading bacterium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int Biodeterior Biodegrad 62:88–95. https://doi.org/10.1016/j.ibiod.2007.12.003
Sorensen SR, Ronen Z, Aamand J (2001) Isolation from agricultural soil and characterization of a Sphingomonas sp. able to mineralize the phenylurea herbicide isoproturon. Appl Environ Microbiol 67:5403–5409. https://doi.org/10.1128/AEM.67.12.5403-5409.2001
Sørensen SR, Juhler RK, Aamand J (2013) Degradation and mineralisation of diuron by Sphingomonas sp. SRS2 and its potential for remediating at a realistic μg L−1 diuron concentration. Pest Manag Sci 69:1239–1244. https://doi.org/10.1002/ps.3490
Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260:214–216. https://doi.org/10.1126/science.8097061
Tang W, Zhou FY, Chen J, Zhou XG (2014) Resistance to ACCase-inhibiting herbicides in an Asia minor bluegrass (Polypogon fugax) population in China. Pestic Biochem Physiol 108:16–20. https://doi.org/10.1016/j.pestbp.2013.11.001
Tetard-Jones C, Edwards R (2016) Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci 72:203–209. https://doi.org/10.1002/ps.4147
Thom ER, Popay AJ, Hume DE, Fletcher LR (2013) Evaluating the performance of endophytes in farm systems to improve farmer outcomes–a review. Crop Pasture Sci 63:927–943
Vila Aiub MM, Ghersa CM (2001) The role of fungal endophyte infection in the evolution of Lolium multiflorum resistance to diclofop-methyl. Weed Res 41:265–274. https://doi.org/10.1046/j.1365-3180.2001.00236.x
Vila-Aiub M, Martinez-Ghersa MA, Ghersa C (2003) Evolution of herbicide resistance in weeds: vertically transmitted fungal endophytes as genetic entities. Evol Ecol 17:441–456. https://doi.org/10.1023/B:EVEC.0000005580.19018.fb
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391. https://doi.org/10.1073/pnas.0504423102
Wang JC, Xue C, Song Y, Wang L, Huang QW, Shen QR (2016) Wheat and rice growth stages and fertilization regimes alter soil bacterial community structure, But Not Diversity. Front Microbiol 7. https://doi.org/10.3389/Fmicb.2016.01207
Werren JH (2012) Symbionts provide pesticide detoxification. Proc Natl Acad Sci U S A 109:8364–8365. https://doi.org/10.1073/pnas.1206194109
Xia X, Sun B, Gurr GM, Vasseur L, Xue M, You M (2018) Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front Microbiol. https://doi.org/10.3389/fmicb.2018.00025
Yao L, Jia X, Zhao J, Cao Q, Xie X, Yu L, He J, Tao Q (2015) Degradation of the herbicide dicamba by two sphingomonads via different O-demethylation mechanisms. Int Biodeterior Biodegrad 104:324–332. https://doi.org/10.1016/j.ibiod.2015.06.016
Ying H, Jingquan L, YouXiaoyan WW, Tao P, Junjie S (2018) Isolation and identification of quizalofop-p-ethyl-degrading strain Bacillus subtilis H and its degradation characteristics. China Environ Sci 38:1466–1472
Yu FB, Shan SD, Luo LP, Guan LB, Qin H (2013) Isolation and characterization of a Sphingomonas sp strain F-7 degrading fenvalerate and its use in bioremediation of contaminated soil. J Environ Sci Heal, Part B 48:198–207. https://doi.org/10.1080/03601234.2013.730299
Zhang J, Sun J-Q, Yuan Q-Y, Li C, Yan X, Hong Q, Li S-P (2011) Characterization of the propanil biodegradation pathway in Sphingomonas sp. Y57 and cloning of the propanil hydrolase gene prpH. J Hazard Mater 196:412–419. https://doi.org/10.1016/j.jhazmat.2011.09.040
Zhang H, Li M, Li J, Wang G, Li F, Xu D, Liu Y, Xiong M (2017) A key esterase required for the mineralization of quizalofop-p-ethyl by a natural consortium of Rhodococcus sp. JT-3 and Brevundimonas sp. JT-9. J Hazard Mater 327:1–10. https://doi.org/10.1016/j.jhazmat.2016.12.038
Acknowledgments
We sincerely thank Mr. Mark Euqene Reynolds for the English editing of the manuscript.
Funding
This work was supported by the Natural Science Foundation of Hunan Province (2019JJ50270), the Scientific Research Project of Education Department of Hunan Province (19A231), and the Science and Technology Plan Projects of Hunan Province (2016JC2029).
Author information
Authors and Affiliations
Corresponding author
Additional information
Editorial Responsibility: Stéphane Compant
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, K., Luo, K., Mao, A. et al. Endophytes enhance Asia minor bluegrass (Polypogon fugax) resistance to quizalofop-p-ethyl. Plant Soil 450, 373–384 (2020). https://doi.org/10.1007/s11104-020-04509-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04509-0