Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T05:30:29.408Z Has data issue: false hasContentIssue false

Germinability and seed biochemical properties of susceptible and non–target site herbicide-resistant blackgrass (Alopecurus myosuroides) subpopulations exposed to abiotic stresses

Published online by Cambridge University Press:  20 January 2020

Zahra Ghazali
Affiliation:
Graduate Student, Department of Agronomy, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran
Eshagh Keshtkar*
Affiliation:
Assistant Professor, Department of Agronomy, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran
Majid AghaAlikhani
Affiliation:
Professor, Department of Agronomy, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran
Per Kudsk
Affiliation:
Professor, Department of Agroecology, Aarhus University, Slagelse, Denmark
*
Author for correspondence: Eshagh Keshtkar, Department of Agronomy, Tarbiat Modares University, P.O. Box 14115-111, 1497713111 Tehran, Iran. Email: [email protected]

Abstract

Quantifying the level of ecophysiological, biochemical, and agronomical fitness of herbicide-resistant (R) and herbicide-susceptible (S) weeds is useful for understanding the evolutionary development of herbicide resistance, but also for implementing herbicide-resistance management strategies. Although germination is a key fitness component in the life cycle of weeds, germinability of S and R weeds has rarely been evaluated under stressful conditions. Germinability traits of S and non–target site resistant subpopulations of blackgrass (Alopecurus myosuroides Huds.) sharing closely related genetic background were tested under salinity, drought stress, and accelerated seed-aging (i.e., exposed to 100% relative humidity at 45 C from 0 to 134 h) conditions. In addition, the activity of three antioxidant enzymes and protein concentration of accelerated aged seeds of the subpopulations were studied. There were no differences in maximum seed germination (Gmax) and time to 50% germination between the two subpopulations under optimum conditions. However, under salinity, drought stress, and accelerated aging conditions, there were differences between the subpopulations. The salinity, drought, and accelerated aging treatments reducing Gmax of the S subpopulation by 50% were 18 dS m−1, 0.75 MPa, and 90 h, respectively, while for the R subpopulation the corresponding values were 15 dS m−1, 0.66 MPa, and 67 h. No differences were found in the activity of the antioxidant enzymes and the content of protein between non-aged seeds of the subpopulations. The aging treatments reducing the activity of catalase and superoxide dismutase enzymes by 50% were 118 and 82 h for the S subpopulation, respectively, while they were 54 and 58 h for the R subpopulation. In contrast, there were no differences in the effect of the aging treatments on the peroxidase activity and protein content between subpopulations. The results provided clear evidence that the non–target site resistant loci of blackgrass is associated with fitness costs under environmental stress.

Type
Research Article
Copyright
© Weed Science Society of America, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Te-Ming Paul Tseng, Mississippi State University

References

Aper, J, Cauwer, B, Roo, S, Lourenço, M, Fievez, V, Bulcke, R, Reheul, D (2014) Seed germination and viability of herbicide resistant and susceptible Chenopodium album populations after ensiling, digestion by cattle and manure storage. Weed Res 54:169177CrossRefGoogle Scholar
Bailly, C, Abdelilah, B, Françoise, C, Daniel, C (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97:104110CrossRefGoogle Scholar
Beauchamp, C, Fridovich, I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276287CrossRefGoogle Scholar
Beers, RF, Sizer, IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133140Google ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248254CrossRefGoogle ScholarPubMed
Clerkx, EJM, Blankestijn-De Vries, H, Ruys, GJ, Groot, SPC, Koornneef, M (2004) Genetic differences in seed longevity of various Arabidopsis mutants. Physiol Plant 121:448461CrossRefGoogle Scholar
Colbach, N, Dürr, C (2003) Effects of seed production and storage conditions on blackgrass (Alopecurus myosuroides) germination and shoot elongation. Weed Sci 51:708717CrossRefGoogle Scholar
Cousens, RD, Fournier-Level, A (2018) Herbicide resistance costs: what are we actually measuring and why? Pest Manag Sci 74:15391546CrossRefGoogle Scholar
Cousens, RD, Gill, GS, Speijers, EJ (1997) Comment: number of sample populations required to determine the effects of herbicide resistance on plant growth and fitness. Weed Res 37:14CrossRefGoogle Scholar
Dang, HT, Long, W, Malone, JM, Preston, C, Gill, G (2019) No apparent fitness costs associated with phytoene desaturase mutations conferred resistance to diflufenican and picolinafen in oriental mustard (Sisymbrium orientale L.). Pestic Biochem Physiol 155:5157CrossRefGoogle Scholar
Du, L, Bai, S, Li, Q, Qu, M, Yuan, G, Guo, W, Wang, J (2017) Effect of herbicide resistance endowing three ACCase mutations on seed germination and viability in American slough grass (Beckmannia syzigachne Steud. Fernald). Chil J Agric Res 77:142149CrossRefGoogle Scholar
Ebrahimi, E, Eslami, SV (2012) Effect of environmental factors on seed germination and seedling emergence of invasive Ceratocarpus arenarius. Weed Res 52:5059CrossRefGoogle Scholar
Florentine, S, Weller, S, King, A, Florentine, A, Dowling, K, Westbrooke, M, Chauhan, BS (2018) Seed germination response of a noxious agricultural weed Echium plantagineum to temperature, light, pH, drought stress, salinity, heat and smoke. Crop Pasture Sci 69:326333CrossRefGoogle Scholar
Forcella, F, Benech Arnold, RL, Sanchez, R, Ghersa, CM (2000) Modeling seedling emergence. Field Crops Res 67:123139CrossRefGoogle Scholar
Ghanizadeh, H, Harrington, KC (2019) Fitness costs associated with multiple resistance to dicamba and atrazine in Chenopodium album. Planta 249:787797CrossRefGoogle ScholarPubMed
Giannopolitis, CN, Ries, SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309314CrossRefGoogle ScholarPubMed
Gundel, PE, Martínez-Ghersa, MA, Ghersa, CM (2008) Dormancy, germination and ageing of Lolium multiflorum seeds following contrasting herbicide selection regimes. Eur J Agron 28:606613CrossRefGoogle Scholar
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed: Novembr 20, 2019Google Scholar
Hilton, HW (1957) Herbicide Tolerant Strains of Weeds. Honolulu: Hawaiian Sugar Planters’ Association. Annual Report. 69 pGoogle Scholar
Holm, L, Doll, J, Holm, E, Pancho, JV, Herberger, JP (1997) World Weeds: Natural Histories and Distribution. New York: Wiley. 1152 pGoogle Scholar
Holt, JS (1990) Fitness and Ecological Adaptability of Herbicide-Resistant Biotypes. Pages 419429in Green, MB, LeBaron, HM, Moberg, WK, eds. Managing Resistance to Agrochemicals: From Fundamental Research to Practical Strategies. Washington, DC: American Chemical SocietyCrossRefGoogle Scholar
Hothorn, T, Bretz, F, Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346363CrossRefGoogle ScholarPubMed
Hoveland, CS, Buchanan, GA (1973) Weed seed germination under simulated drought. Weed Science 21:322324CrossRefGoogle Scholar
Ibrahim, EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:3846CrossRefGoogle ScholarPubMed
Javaid, MM, Tanveer, A (2014) Germination ecology of Emex spinosa and Emex australis, invasive weeds of winter crops. Weed Res 54:565575CrossRefGoogle Scholar
Jensen, SM, Andreasen, C, Streibig, JC, Keshtkar, E, Ritz, C (2017) A note on the analysis of germination data from complex experimental designs. Seed Sci Res 27:321327CrossRefGoogle Scholar
Kar, M, Mishra, D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315319CrossRefGoogle ScholarPubMed
Keshtkar, E, Abdolshahi, R, Sasanfar, H, Zand, E, Beffa, R, Dayan, FE, Kudsk, P (2019) Assessing fitness costs from a herbicide-resistance management perspective: a review and insight. Weed Sci 67:137148CrossRefGoogle Scholar
Keshtkar, E, Kordbacheh, F, Mesgaran, MB, Mashhadi, HR, Alizadeh, HM (2009) Effects of the sowing depth and temperature on the seedling emergence and early growth of wild barley (Hordeum spontaneum) and wheat. Weed Biol Manag 9:1019CrossRefGoogle Scholar
Keshtkar, E, Mathiassen, SK, Beffa, R, Kudsk, P (2017a) Seed germination and seedling emergence of blackgrass (Alopecurus myosuroides) as affected by non–target site herbicide resistance. Weed Science 65:732742CrossRefGoogle Scholar
Keshtkar, E, Mathiassen, SK, Kudsk, P (2017b) No Vegetative and fecundity fitness cost associated with acetyl-coenzyme A carboxylase non-target-site resistance in a black-grass (Alopecurus myosuroides Huds) population. Front Plant Sci 8, doi: 10.3389/fpls.2017.02011CrossRefGoogle Scholar
Keshtkar, E, Mathiassen, SK, Moss, SR, Kudsk, P (2015) Resistance profile of herbicide-resistant Alopecurus myosuroides (black-grass) populations in Denmark. Crop Prot 69:8389CrossRefGoogle Scholar
Lee, YP, Baek, K-H, Lee, H-S, Kwak, S-S, Bang, J-W, Kwon, S-Y (2010) Tobacco seeds simultaneously over-expressing Cu/Zn-superoxide dismutase and ascorbate peroxidase display enhanced seed longevity and germination rates under stress conditions. J Exp Bot 61:24992506CrossRefGoogle ScholarPubMed
Li, X-h, Jiang, D-m, Li, X-l, Zhou, Q-l, Xin, J (2011) Effects of salinity and desalination on seed germination of six annual weed species. J For Res 22:475CrossRefGoogle Scholar
Long, RL, Gorecki, MJ, Renton, M, Scott, JK, Colville, L, Goggin, DE, Commander, LE, Westcott, DA, Cherry, H, Finch-Savage, WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev Camb Philos Soc 90:3159CrossRefGoogle ScholarPubMed
Long, RL, Panetta, FD, Steadman, KJ, Probert, R, Bekker, RM, Brooks, S, Adkins, SW (2008) Seed persistence in the field may be predicted by laboratory-controlled aging. Weed Sci 56:523528CrossRefGoogle Scholar
Lutman, PJW, Moss, SR, Cook, S, Welham, SJ (2013) A review of the effects of crop agronomy on the management of Alopecurus myosuroides. Weed Res 53:299313CrossRefGoogle Scholar
Maréchal, P, Henriet, F, Vancutsem, F, Bodson, B (2012) Ecological review of black-grass (Alopecurus myosuroides Huds.) propagation abilities in relationship with herbicide resistance. Biotechnol Agron Soc Environ 16:103113Google Scholar
Matzrafi, M, Seiwert, B, Reemtsma, T, Rubin, B, Peleg, Z (2016) Climate change increases the risk of herbicide-resistant weeds due to enhanced detoxification. Planta 244:12171227CrossRefGoogle ScholarPubMed
Michel, BE, Kaufmann, MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51:914916CrossRefGoogle ScholarPubMed
Moncaleano-Escandon, J, Silva, BCF, Silva, SRS, Granja, JAA, Alves, MCJL, Pompelli, MF (2013) Germination responses of Jatropha curcas L. seeds to storage and aging. Ind Crops Prod 44:684690CrossRefGoogle Scholar
Osipitan, OA, Dille, JA (2017) Fitness outcomes related to glyphosate resistance in kochia (Kochia scoparia): what life history stage to examine? Front Plant Sci 8, doi: 10.3389/fpls.2017.01090CrossRefGoogle ScholarPubMed
Pedersen, BP, Neve, P, Andreasen, C, Powles, SB (2007) Ecological fitness of a glyphosate-resistant Lolium rigidum population: growth and seed production along a competition gradient. Bas Appl Ecol 8:258268CrossRefGoogle Scholar
Primack, RB, Hyesoon, K (1989) Measuring fitness and natural selection in wild plant populations. Annu Rev Ecol Syst 20:367396CrossRefGoogle Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org. Accessed: November 20, 2019Google Scholar
Ritz, C, Baty, F, Streibig, JC, Gerhard, D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021CrossRefGoogle ScholarPubMed
Ritz, C, Pipper, CB, Streibig, JC (2013) Analysis of germination data from agricultural experiments. Eur J Agron 45:16CrossRefGoogle Scholar
Shariat, A, Assareh, MH, Ghamari-Zare, A (2017) Antioxidative responses of Eucalyptus camaldulensis to different concentrations of copper. J Plant Physiol Breed 7:4152Google Scholar
Shrestha, A, deSouza, LL, Yang, P, Sosnoskie, L, Hanson, BD (2018) Differential tolerance of glyphosate-susceptible and glyphosate-resistant biotypes of junglerice (Echinochloa colona) to environments during germination, growth, and intraspecific competition. Weed Sci 66:340346CrossRefGoogle Scholar
Siminis, CI, Kanellis, AK, Roubelakis-Angelakis, KA (1994) Catalase is differentially expressed in dividing and nondividing protoplasts. Plant Physiol 105:13751383CrossRefGoogle ScholarPubMed
Stéphane, C, Sandra, W, Carole, R, Florence, S, Bruno, C, Jean‐Philippe, G (2018) Effects of drought on weed emergence and growth vary with the seed burial depth and presence of a cover crop. Weed Biol Manag 18:1225Google Scholar
Streibig, JC, Rudemo, M, Jensen, JE (1993) Dose-response curves and statistical models. Pages 2955in Streibig, JC, Kudsk, P, eds. Herbicide Bioassays. Boca Raton, FL: CRC PressGoogle Scholar
Switzer, CM (1957) The existence of 2,4-D resistant strains of wild carrot. Pages 315318in Proceedings of the North Eastern Weed Control Conference. New York: Northeastern Weed Science SocietyGoogle Scholar
Tang, W, Xu, X, Shen, G, Chen, J (2015) Effect of environmental factors on germination and emergence of aryloxyphenoxy propanoate herbicide-resistant and -susceptible Asia minor bluegrass (Polypogon fugax). Weed Sci 63:669675CrossRefGoogle Scholar
Uddin, MN, Hossain, MA, Burritt, DJ (2016) Salinity and drought stress. Pages 86101in Ahmad, P, ed. Water Stress and Crop Plants. New York: Wiley-BlackwellCrossRefGoogle Scholar
Vanacker, H, Carver, TLW, Foyer, CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:11031114CrossRefGoogle ScholarPubMed
Viechtbauer, W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:148CrossRefGoogle Scholar
Vila-Aiub, MM, Goh, SS, Gaines, TA, Han, H, Busi, R, Yu, Q, Powles, SB (2014) No fitness cost of glyphosate resistance endowed by massive EPSPS gene amplification in Amaranthus palmeri. Planta 239:793801CrossRefGoogle ScholarPubMed
Vila-Aiub, MM, Neve, P, Powles, SB (2009) Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751–67CrossRefGoogle ScholarPubMed
Vila-Aiub, MM, Neve, P, Roux, F (2011) A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:386394CrossRefGoogle ScholarPubMed
Vila-Aiub, MM, Neve, P, Steadman, KJ, Powles, SB (2005) Ecological fitness of a multiple herbicide-resistant Lolium rigidum population: dynamics of seed germination and seedling emergence of resistant and susceptible phenotypes. J Appl Ecol 42:288298CrossRefGoogle Scholar
Vizantinopoulos, S, Katranis, N (1998) Management of blackgrass (Alopecurus myosuroides) in winter wheat in Greece. Weed Technol 12:484490CrossRefGoogle Scholar
Wang, T, Picard, JC, Tian, X, Darmency, H (2010) A herbicide-resistant ACCase 1781 Setaria mutant shows higher fitness than wild type. Heredity 105:394400CrossRefGoogle ScholarPubMed
Warwick, SI, Black, LD (1994) Relative fitness of herbicide-résistant and susceptible biotypes of weeds. Phytoprotection 75:3749CrossRefGoogle Scholar
Wu, X, Zhang, T, Pan, L, Wang, L, Xu, H, Dong, L (2016) Germination requirements differ between fenoxaprop-p-ethyl resistant and susceptible Japanese foxtail (Alopecurus japonicus) biotypes. Weed Sci 64:653663CrossRefGoogle Scholar