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Environmental Implications of Herbicide Resistance: Soil Biology and Ecology

Published online by Cambridge University Press:  20 January 2017

Robert J. Kremer
Robert J. Kremer*
Affiliation:
USDA-ARS and Adjunct Professor, Department of Soil, Environmental & Atmospheric Sciences, University of Missouri, 302 Natural Resources Building, Columbia, MO 65211
*
Corresponding author's E-mail: bob.kremer@ars.usda.gov
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Abstract

Soil microbial community structure and activity are linked to plant communities. Weeds may alter their soil environment, selecting for specific rhizosphere microbial communities. Rhizosphere modification occurs for many crop and horticultural plants. However, impacts of weeds in agroecosystems on soil biology and ecology have received less attention because effective weed management practices were developed to minimize their impacts on crop production. The recent development of herbicide resistance (HR) in several economically important weeds leading to widespread infestations in crop fields treated with a single herbicide has prompted a re-evaluation of the effects of weed growth on soil biology and ecology. The objective of this article is to review the potential impacts of herbicide-resistant weeds on soil biological and ecological properties based on reports for crops, weeds, and invasive plants. Persistent weed infestations likely establish extensive root systems and release various plant metabolites through root exudation. Many exudates are selective for specific soil microbial groups mediating biochemical and nutrient acquisition processes. Exudates may stimulate development of microbial groups beneficial to weed but detrimental to crop growth or beneficial to both. Changes in symbiotic and associative microbial interactions occur, especially for arbuscular mycorrhizal fungi (AMF) that are important in plant uptake of nutrients and water, and protecting from phytopathogens. Mechanisms used by weeds to disrupt symbioses in crops are not clearly described. Many herbicide-resistant weeds including Amaranthus and Chenopodium do not support AMF symbioses, potentially reducing AMF propagule density and establishment with crop plants. Herbicides applied to control HR weeds may compound effects of weeds on soil microorganisms. Systemic herbicides released through weed roots may select microbial groups that mediate detrimental processes such as nutrient immobilization or serve as opportunistic pathogens. Understanding complex interactions of weeds with soil microorganisms under extensive infestations is important in developing effective management of herbicide-resistant weeds.

Keywords

Glyphosatedeleterious rhizobacteriamicrobial ecologymycorrhizaerhizodepositionrhizospheresoil microbial communitysystemic herbicidestransgenic crops
Type
Symposium
Information
Weed Science , Volume 62 , Issue 2 , June 2014 , pp. 415 - 426
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Abbas, HK, Barrentine, WL (1995) Alternaria helianthi and imazaquin for control of imazaquin susceptible and resistant cocklebur (Xanthium strumarium) biotypes. Weed Sci. 43:425–428 Google Scholar
Aldrich, RJ, Kremer, RJ (1997) Principles in Weed Management. Ames, IA Iowa State University Press. 455 pGoogle Scholar
Altman, J, Campbell, CL (1977) Effect of herbicides on plant disease. Annu Rev Phytopathol. 15:361–385 Google Scholar
Anderson, RC, Anderson, MR, Bauer, JT, Slater, M, Herold, J, Baumhardt, P, Borowicz, V (2010) Effect of removal of garlic mustard (Alliaria petiolata, Brassicaceae) on arbuscular mycorrhizal fungi inoculum potential in forest soils. Open Ecol J. 3:41–47 Google Scholar
Averill, C, Finzi, A (2013) Plant regulation of microbial enzyme production in situ. Soil Biol Biochem. 56:49–52 Google Scholar
Bais, HP, Weir, TL, Perry, LG, Gilroy, SL, Vivanco, JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol. 57:233–266 Google Scholar
Bassett, IJ, Crompton, CW (1978) The biology of Canadian weeds. 32. Chenopodium album L. Can J Plant Sci. 58:106l–1072 Google Scholar
Berg, G, Smalla, K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol. 68:1–13 Google Scholar
Blackshaw, RE, Brandt, RN, Janzen, HH, Entz, T (2004) Weed species response to phosphorus fertilization. Weed Sci. 52:406–412 Google Scholar
Boyetchko, SM (1996) Impact of soil microorganisms on weed biology and ecology. Phytoprotection. 77:41–56 Google Scholar
Boyetchko, SM, Mortensen, K (1993) Use of rhizobacteria as biological control agents of downy brome. Pages 443–448 in Proceedings of the 1993 Soils & Crops Workshop. Saskatoon, Saskatchewan, Canada University of Saskatchewan Google Scholar
Brinecombe, MJ, De Leij, FA, Lynch, JM (2001) The effect of root exudates on rhizosphere microbial populations. Pages 95–140 in Pinton, R, Varanini, Z, and Nannipieri, P, eds, The Rhizosphere. New York Marcel Dekker Google Scholar
Bulgarelli, D, Rott, M, Schlaeppi, K, van Themaat, T, Ahmadinejad, N, Assenza, F, Rauf, P, Huettel, R, Reinhardt, E, Schmelzer, J, Peplies, FO, Gloeckner, R, Amann, T, Eickhorst, T, Schulze-Lefert, P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 488:91–95 Google Scholar
Chee-Sanford, JC (2008) Weed seeds as nutritional resources for soil Ascomycota and characterization of specific associations between plant and fungal species. Biol Fert Soils. 44:763–771 Google Scholar
Cipollini, D, Rigsby, CM, Barto, EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol. 38:714–727 Google Scholar
Connick, WJ Jr., Bradow, JM, Legendre, MG (1989) Identification and bioactivity of volatile allelochemicals from amaranth residues. J Agric Food Chem. 37:792–796 Google Scholar
Coupland, D, Casely, JC (1979) Presence of 14C activity in root exudates and guttation fluid from Agropyron repens treated with 14C-labelled glyphosate. New Phytol. 83:17–22 Google Scholar
Cregut, M, Piutti, S, Vong, PC, Slezack-Deschaumes, S, Crovisier, I, Benizri, E (2009) Density, structure, and diversity of the cultivable arylsulfatase-producing bacterial community in the rhizosphere of field-grown rape and barley. Soil Biol Biochem. 41:704–710 Google Scholar
Davis, AS, Hill, JD, Chase, CD, Johanns, AM, Liebman, M (2012) Increasing cropping system diversity balances productivity, profitability and environmental health. PLoS ONE. 7:e47149 Google Scholar
Davis, RG, Johnson, WC, Wood, FO (1967) Weed root profiles. Agron J. 59:555–556 Google Scholar
DeAngelis, KM, Lindow, SE, Firestone, MK (2008) Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbiol Ecol. 66:197–207 Google Scholar
DeAngelis, KM, Brodie, EL, DeSantis, TZ, Anderso, GL, Lindow, SE, Firestone, MK (2009) Selective progressive response of soil microbial community to wild oat roots. ISME Journal. 3:168–178 Google Scholar
Dick, RP, Lorenz, N, Wojno, M, Lane, M (2010) Microbial dynamics in soils under long-term glyphosate tolerant cropping systems. Pages 153–156 in Gilkes, RJ, Prakongkep, N, eds. Proceedings of the 19th World Congress of Soil Science. Brisbane, Australia CSIRO Google Scholar
Druille, M, Cabello, MN, Omacini, M, Golluscio, RM (2013) Glyphosate reduces spore viability and root colonization of arbuscular mycorrhizal fungi. Appl Soil Ecol. 64:99–103 Google Scholar
Dunfield, KE, Germida, JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically-modified canola (Brassica napus). Appl Environ Microbiol. 69:7310–7318 Google Scholar
Ehrenfeld, JG, Ravit, B, Elgersma, K (2005) Feedback in the plant-soil system. Annu Rev Environ Res. 30:75–115 Google Scholar
Forcella, F (2014) Short- and full-season soybean in stale seedbeds versus rolled-crimped winter rye mulch. Renew Agri Food Syst. 29:92–99 Google Scholar
Garbeva, P, van Veen, JA, van Elsas, JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type implications for disease suppressiveness. Annu Rev Phytopathol. 42:243–270 Google Scholar
Gonzalez-Torralva, F, Cruz-Hipolito, H, Bastida, F, Mulleder, N, Smeda, RJ, de Prado, R (2010) Differential susceptibility to glyphosate among Conyza weed species in Spain. J Agric Food Chem. 58:4361–4366 Google Scholar
Greaves, MP, Sargent, JA (1986) Herbicide-induced microbial invasion of plant roots. Weed Sci. 34(Suppl 1):50–53 Google Scholar
Herman, RA, Price, WD (2013) Unintended compositional changes in genetically modified (GM) crops: 20 years of research. J Agric Food Chem. 61:11695–11701 Google Scholar
Hirsch, PR, Mauchline, TH (2012) Mutualism: plant-microorganism interactions. Pages 43–55 in Ogilvie, LA, Hirsch, PR, eds. Microbial Ecological Theory. Norfolk, United Kingdom Caister Academic Press Google Scholar
Jordan, NR, Aldrich-Wolfe, L, Huerd, SC, Larson, DL, Muehlbauer, G (2012) Soil-occupancy effects of invasive and native grassland plant species on composition and diversity of mycorrhizal associations. Invasive Plant Sci Manage. 5:494–505 Google Scholar
Jordan, NR, Zhang, J, Huerd, S (2000) Arbuscular-mycorrhizal fungi: potential roles in weed management. Weed Res. 40:397–410 Google Scholar
Kennedy, AC, Elliott, LF, Young, FL, Douglas, CL (1991) Rhizobacteria suppressive to the weed downy brome. Soil Sci Soc Am J. 55:722–727 Google Scholar
Kering, MK, Lukaaszewska, K, Blevins, DG (2009) Manganese requirement for optimum photosynthesis and growth in NAD-malic enzyme C-4 species. Plant Soil. 316:217–226 Google Scholar
Kim, S-J, Kremer, RJ (2005) Scanning and transmission electron microscopy of root colonization of morningglory (Ipomoea spp.) seedlings by rhizobacteria. Symbiosis. 39:117–124 Google Scholar
Kloepper, JW, Ryu, CM, Zhang, S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology. 94:1259–1266 Google Scholar
Kremer, RJ (1986) Microorganisms associated with velvetleaf (Abutilon theophrasti) seeds on the soil surface. Weed Sci. 34:233–236 Google Scholar
Kremer, RJ (1987) Identity and properties of bacteria inhabiting seeds of selected broadleaf weed species. Microb Ecol. 14:29–37 Google Scholar
Kremer, RJ (1993) Management of weed seed banks with microorganisms. Ecol Appl. 3:42–52 Google Scholar
Kremer, RJ, Begonia, MFT, Stanley, L, Lanham, ET (1990) Characterization of rhizobacteria associated with weed seedlings. Appl Environ Microbiol. 56:1649–1655 Google Scholar
Kremer, RJ, Means, NE, Kim, SJ (2005) Glyphosate affects soybean root exudation and rhizosphere microorganisms. Intern J Environ Anal Chem. 15:1165–1174 Google Scholar
Kumar, R, Pandey, S, Pandey, A (2006) Plant roots and carbon sequestration. Curr Sci. 91:885–890 Google Scholar
LaBarge, GA, Kremer, RJ (1989) Effects of velvetleaf plant residues on seedling growth and soil microbial activity. Bull Environ Contam Toxicol. 43:421–427 Google Scholar
Lehman, RM, Taheri, WI, Osborne, SL, Buyer, JS, Douds, DD Jr., 2012) Fall cover cropping can increase arbuscular mycorrhizae in soils supporting intensive agricultural production. Appl Soil Ecol. 61:300–304 Google Scholar
Li, J, Kremer, RJ (2000) Rhizobacteria associated with weed seedlings in different cropping systems. Weed Sci. 48:734–741 Google Scholar
Li, J, Kremer, RJ (2006) Growth response of weed and crop seedlings to deleterious rhizobacteria. Biol Contr. 39:58–65 Google Scholar
Li, M, Yu, Q, Vila-Aiub, M, Powles, SB (2013) ALS herbicide resistance mutations in Raphanus raphanistrum: evaluation of pleiotropic effects on vegetative growth and ALS activity. Pest Manage Sci. 69:689–695 Google Scholar
Lynch, JM, Whipps, JM (1990) Substrate flow in the rhizosphere. Plant Soil. 129:1–10 Google Scholar
Marschner, P (2012) Rhizosphere biology. Pages 369–388 in Marschner, P, ed. Mineral Nutrition of Higher Plants. San Diego Elsevier Google Scholar
Mijangos, I, Becerril, JM, Albizu, I, Epeide, L, Garbisu, C (2009) Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and –independent methodologies. Soil Biol Biochem. 41:505–513 Google Scholar
Mortensen, DA, Egan, JF, Maxwell, BD, Ryan, MR, Smith, RG (2012) Navigating a critical juncture for sustainable weed management. BioScience. 62:75–84 Google Scholar
Norsworthy, JK, Ward, SM, Shaw, DR, Llewellyn, RS, Nichols, RL, Webster, TM, Bradley, KM, Frisvold, G, Powles, SB, Burgos, NR, William, WW, Barrett, M (2012) Reducing the risks of herbicide resistance: best management practices and recommendations. Weed Sci Special Issue. 31–62 Google Scholar
Postic, J, Cosic, J, Vrandecic, K, Jurkovic, D, Saleh, AA, Leslie, JF (2012) Diversity of Fusarium species isolated from weeds and plant debris in Croatia. J Pathol. 161:76–81 Google Scholar
Powell, JR, Dunfield, KE (2007) Non-target impacts of genetically-modified, herbicide-resistant crops on soil microbial and faunal communities. Pages 127–137 in Gulden, RH, Swanton, CJ, eds. The First Decade of Herbicide-Resistant Crops in Canada. Topics in Canadian Weed Science, Vol. 4. Sainte Anne de Bellevue, Quebec Canadian Weed Science Society Google Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol. 61:317–347 Google Scholar
Rice, EL (1984) Allelopathy, 2nd ed. Orlando, FL Academic Press. 422 pGoogle Scholar
Rinaudo, V, Bàrberi, P, Giovannetti, M, van der Heijden, MGA (2010) Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil. 333:7–20 Google Scholar
Rosenbaum, KK, Miller, GL, Kremer, RJ, Bradley, KW (2014) Interactions between glyphosate, Fusarium infection of common waterhemp (Amaranthus rudis), and soil microbial abundance and diversity in soil collections from Missouri. Weed Sci. 62:71–82 Google Scholar
Schafer, JR, Hallett, SG, Johnson, WG (2012) Response of giant ragweed (Ambrosia trifida), horseweed (Conyza canadensis), and common lambsquarters (Chenopodium album) biotypes to glyphosate in the presence and absence of soil microorganisms. Weed Sci. 60:641–649 Google Scholar
Schafer, JR, Hallett, SG, Johnson, WG (2013) Soil microbial root colonization of glyphosate-treated giant ragweed (Ambrosia trifida), horseweed (Conyza canadensis), and common lambsquarters (Chenopodium album) biotypes. Weed Sci. 61:289–295 Google Scholar
Sellers, BA, Smeda, RJ, Johnson, WG, Kendig, JA, Ellersieck, MR (2003) Comparative growth of six Amaranthus species in Missouri. Weed Sci. 51:329–333 Google Scholar
Siqueira, JO, Muraleedharan, GN, Hammerschmidt, R, Safir, GR, Putnam, AR (1991) Significance of phenolic compounds in plant-microbial systems. Crit Rev Plant Sci. 10:63–121 Google Scholar
Skipper, HD, Ogg, AG Jr., Kennedy, AC (1996) Root biology of grasses and ecology of rhizobacteria for biological control. Weed Technol. 10:610–620 Google Scholar
Stinson, KA, Campbell, SA, Powell, JR, Wolfe, BE, Callaway, RM, Thelen, GC, Hallett, SG, Prati, D, Klironomos, JN (2006) Invasive plant suppresses growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. 4:e140 Google Scholar
Sturz, AV, Matheson, BG, Arsenault, W, Kimpinski, J, Christie, BR (2001) Weeds as a source of plant growth promoting rhizobacteria in agricultural soils. Can J Microbiol. 47:1013–1024 Google Scholar
Tranel, PJ, Riggins, CW, Bell, MS, Hager, AG (2011) Herbicide resistances in Amaranthus tuberculatus: a call for new options. J Agric Food Chem. 59:5808–5812 Google Scholar
Vaicekonyte, R, Keesing, F (2012) Effects of garlic mustard (Alliaria petiolata) removal on the abundance of entomopathogenic fungi. Invasive Plant Sci Manage. 5:323–329 Google Scholar
van der Putten, WH, Klironomos, JN, Wardle, DA (2007) Microbial ecology of biological invasions. ISMA Journal. 1:28–37 Google Scholar
van Overbeek, LS, Franke, AC, Nijhuis, EHM, Groenevel, RMW, da Rocha, UN, Lotz, LAP (2011) Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microb Ecol. 62:257–264 Google Scholar
Vatovec, C, Jordan, N, Huerd, S (2005) Responsiveness of certain agronomic weed species to arbuscular mycorrhizal fungi. Renew Agr Food Sys. 20:181–189 Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2005) Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol. 167:787–796 Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009) Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum . J Ecol. 97:772–780 Google Scholar
Walker, TS, Bais, HP, Grotewold, E, Vivanco, JM (2003) Root exudation and rhizosphere biology. Plant Physiol. 132:44–51 Google Scholar
Walsh, MJ, Owen, MJ, Powles, SB (2007) Frequency and distribution of herbicide resistance in Raphanus raphanistrum populations randomly collected across the Western Australian wheatbelt. Weed Res. 47:542–550 Google Scholar
Watrud, LS, King, G, Londo, JP, Colasanti, R, Smith, BM, Waschmann, RS, Lee, EH (2011) Changes in constructed Brassica communities treated with glyphosate drift. Ecol Appl. 21:525–538 Google Scholar
Weise, AF (1968) Rate of weed root elongation. Weed Sci. 16:11–13 Google Scholar
Willis, A, Rodrigues, BF, Harris, PJC (2013) The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci. 32:1–20 Google Scholar
Zimdahl, RL (1999) Fundamentals of Weed Science, 2nd ed. San Diego Academic Press. 556 pGoogle Scholar