Skip to main content Accessibility help
×
Home
Hostname: page-component-564cf476b6-2jsqd Total loading time: 0.244 Render date: 2021-06-22T02:17:33.132Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

Empirical investigation of mutation rate for herbicide resistance

Published online by Cambridge University Press:  28 May 2019

Federico A. Casale
Affiliation:
Graduate Student, University of Illinois, Urbana, IL, USA
Darci A. Giacomini
Affiliation:
Research Assistant Professor, University of Illinois, Urbana, IL, USA
Patrick J. Tranel
Affiliation:
Professor, University of Illinois, Urbana, IL, USA
Corresponding
E-mail address:

Abstract

In a predictable natural selection process, herbicides select for adaptive alleles that allow weed populations to survive. These resistance alleles may be available immediately from the standing genetic variation within the population or may arise from immigration via pollen or seeds from other populations. Moreover, because all populations are constantly generating new mutant genotypes by de novo mutations, resistant mutants may arise spontaneously in any herbicide-sensitive weed population. Recognizing that the relative contribution of each of these three sources of resistance alleles influences what strategies should be applied to counteract herbicide-resistance evolution, we aimed to add experimental information to the resistance evolutionary framework. Specifically, the objectives of this experiment were to determine the de novo mutation rate conferring herbicide resistance in a natural plant population and to test the hypothesis that the mutation rate increases when plants are stressed by sublethal herbicide exposure. We used grain amaranth (Amaranthus hypochondriacus L.) and resistance to acetolactate synthase (ALS)-inhibiting herbicides as a model system to discover spontaneous herbicide-resistant mutants. After screening 70.8 million plants, however, we detected no spontaneous resistant genotypes, indicating the probability of finding a spontaneous ALS-resistant mutant in a given sensitive population is lower than 1.4 × 10−8. This empirically determined upper limit is lower than expected from theoretical calculations based on previous studies. We found no evidence that herbicide stress increased the mutation rate, but were not able to robustly test this hypothesis. The results found in this study indicate that de novo mutations conferring herbicide resistance might occur at lower frequencies than previously expected.

Type
Research Article
Copyright
© Weed Science Society of America, 2019 

Access options

Get access to the full version of this content by using one of the access options below.

Footnotes

Associate Editor: Marie A. Jasieniuk, University of California, Davis

References

Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796815CrossRefGoogle Scholar
Bagavathiannan, MV, Norsworthy, JK, Smith, KL, Neve, P (2013) Modeling the evolution of glyphosate resistance in barnyardgrass (Echinochloa crus-galli) in cotton-based production systems of the midsouthern United States. Weed Technol 27:475487CrossRefGoogle Scholar
Baltensperger, DD, Weber, LE, Nelson, LA (1992) Registration of ‘Plainsman’ grain amaranth. Crop Sci 32:15101511CrossRefGoogle Scholar
Bashir, T, Sailer, C, Gerber, F, Loganathan, N, Bhoopalan, H, Eichenberger, C, Grossniklaus, U, Baskar, R (2014) Hybridization alters spontaneous mutation rates in a parent-of-origin-dependent fashion in Arabidopsis. Plant Physiol 165:424437CrossRefGoogle Scholar
Burgos, NR, Tranel, PJ, Streibig, JC, Davis, VM, Shaner, D, Norsworthy, JK, Ritz, C (2013) Review: confirmation of resistance to herbicides and evaluation of resistance levels. Weed Sci 61:420CrossRefGoogle Scholar
Délye, C, Deulvot, C, Chauvel, B (2013a) DNA Analysis of herbarium specimens of the grass weed Alopecurus myosuroides reveals herbicide resistance pre-dated herbicides. PLoS ONE 8:e75117, doi: 10.1371/journal.pone.0075117CrossRefGoogle ScholarPubMed
Délye, C, Jasieniuk, M, Le, C,orre, V (2013b) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649658CrossRefGoogle ScholarPubMed
Doganlar, ZB (2012) Quizalofop-p-ethyl-induced phytotoxicity and genotoxicity in Lemna minor and Lemna gibba. J Environ Sci Health Part A Toxic-Hazard Subst Environ Eng 47:16311643CrossRefGoogle ScholarPubMed
Doyle, JJ, Doyle, JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:1315Google Scholar
Filkowski, J, Besplug, J, Burke, P, Kovalchuk, I, Kovalchuk, O (2003) Genotoxicity of 2, 4-D and dicamba revealed by transgenic Arabidopsis thaliana plants harboring recombination and point mutation markers. Mutat Res 542:2332CrossRefGoogle ScholarPubMed
Filkowski, J, Kovalchuk, O, Kovalchuk, I (2004) Dissimilar mutation and recombination rates in Arabidopsis and tobacco. Plant Sci 166:265272CrossRefGoogle Scholar
Foes, MJ, Liu, L, Tranel, PJ, Wax, LM, Stoller, EW (1998) A biotype of waterhemp (Amaranthus rudis) resistant to triazine and ALS herbicides. Weed Sci 46:514520CrossRefGoogle Scholar
Foes, MJ, Liu, L, Vigue, G, Stoller, EW, Wax, LM, Tranel, PJ (1999) A kochia (Kochia scoparia) biotype resistant to triazine and ALS-inhibiting herbicides. Weed Sci 47:2027CrossRefGoogle Scholar
Gressel, J (2011) Low pesticide rates may hasten the evolution of resistance by increasing mutation frequencies. Pest Manag Sci 67:253257CrossRefGoogle ScholarPubMed
Gressel, J, Levy, AA (2009) Stress, mutators, mutations and stress resistance. Pages 471484 in Pareek, A, Sopory, SK, Bohnert, HJ, Govindjee, eds. Abiotic Stress Adaptation in Plants. Dordrecht, Netherlands: SpringerCrossRefGoogle Scholar
Heap, IM (2014) Global perspective of herbicide-resistant Weeds. Pest Manag Sci 70:13061315CrossRefGoogle ScholarPubMed
Heap, IM (2018) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: March 27, 2018Google Scholar
Jasieniuk, M, Brûlé-Babel, AL, Morrison, IN (1996) The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176193CrossRefGoogle Scholar
Jiang, C, Mithani, A, Belfield, EJ, Mott, R, Hurst, LD, Harberd, NP (2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res 24:18211829CrossRefGoogle ScholarPubMed
Llewellyn, RS, Powles, SB (2001) High levels of herbicide resistance in rigid ryegrass (Lolium rigidum) in the wheat belt of Western Australia. Weed Technol 15:242248CrossRefGoogle Scholar
Mimura, M, Ono, K, Goka, K, Hara, T (2013) Standing variation boosted by multiple sources of introduction contributes to the success of the introduced species, Lotus corniculatus. Biol Invasions 15:27432754CrossRefGoogle Scholar
Murphy, BP, Plewa, DE, Phillippi, E, Bissonnette, SM, Tranel, PJ (2017) A quantitative assay for Amaranthus palmeri identification. Pest Manag Sci 73:22212224CrossRefGoogle ScholarPubMed
Neve, P, Norsworthy, JK, Smith, KL, Zelaya, IA (2010) Modelling evolution and management of glyphosate resistance in Amaranthus palmeri. Weed Res 51:99112CrossRefGoogle Scholar
Norsworthy, JK, Ward, SM, Shaw, DR, Llewellyn, RS, Nichols, RL, Webster, TM, Bradley, KW, Frisvold, G, Powles, DB, Burgos, NR, Witt, WW, Barrett, M (2012) Reducing the risks of herbicide resistance: best management practices and recommendations. Weed Sci 60:3162CrossRefGoogle Scholar
Ossowski, S, Schneeberger, K, Lucas-Lledo, JI, Warthmann, N, Clark, RM, Shaw, RG, Weigel, D, Lynch, M (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:9294CrossRefGoogle ScholarPubMed
Patzoldt, WL, Tranel, PJ (2007) Multiple ALS mutations confer herbicide resistance in waterhemp (Amaranthus tuberculatus). Weed Sci 55:421428CrossRefGoogle Scholar
Plewa, MJ (1985) Mutation testing with maize. Basic Life Sci 34:323328Google Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347CrossRefGoogle ScholarPubMed
Preston, C, Powles, SB (2002) Evolution of herbicide resistance in weeds: initial frequency of target site-based resistance to acetolactate synthase-inhibiting herbicides in Lolium rigidum. Heredity 88:813CrossRefGoogle ScholarPubMed
Renton, M, Busi, R, Neve, P, Thornby, D, Vila-Aiub, M (2014) Herbicide resistance modelling: past, present and future. Pest Manag Sci 70:13941404CrossRefGoogle ScholarPubMed
Schmitz, RJ, Schultz, MD, Lewsey, MG, Malley, RCO, Urich, MA, Libiger, O, Schork, NJ, Ecker, JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369373CrossRefGoogle ScholarPubMed
Stannard, ME, Fay, PK (1987) Selection of alfalfa seedlings for tolerance to chlorsulfuron. WSSA Abstracts 27:61Google Scholar
Trucco, F, Hager, AG, Tranel, PJ (2006) Acetolactate synthase mutation conferring imidazolinone-specific herbicide resistance in Amaranthus hybridus. J Plant Physiol 163:475479CrossRefGoogle ScholarPubMed
Trucco, F, Jeschke, MR, Rayburn, AL, Tranel, PJ (2005) Promiscuity in weedy amaranths: high frequency of female tall waterhemp (Amaranthus tuberculatus) × smooth pigweed (A. hybridus) hybridization under field conditions. Weed Sci 53:4654CrossRefGoogle Scholar
Yang, S, Wang, L, Huang, J, Zhang, X, Yuan, Y, Chen, JQ, Hurst, LD, Tian, D (2015) Parent-progeny sequencing indicates higher mutation rates in heterozygotes. Nature 523:463467CrossRefGoogle ScholarPubMed
Yao, Y, Kovalchuk, I (2011) Abiotic stress leads to somatic and heritable changes in homologous recombination frequency, point mutation frequency and microsatellite stability in Arabidopsis plants. Mutat Res 707:6166CrossRefGoogle ScholarPubMed
Yu, Q, Powles, SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:13401350CrossRefGoogle ScholarPubMed
6
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Empirical investigation of mutation rate for herbicide resistance
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Empirical investigation of mutation rate for herbicide resistance
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Empirical investigation of mutation rate for herbicide resistance
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *