Published May 2, 2013
Microorganisms in Weed Control Strategies A. C. Kennedy and R. .L Kremer
Research Question
Study Approach
Applied Questions
Alternative weed management is one of the critical factors limiting optimum crop yield; however, excess herbicide use can negatively affect our groundwater and environment. Alternative weed management strategies 'are needed as the use of synthetic chemical herbicides becomes more restricted. Biological weed control arises from the fact that biotic factors significantly influence the distribution, abundance, and competitive abilities of plant species. Biological control offers an alternative means of suppressing weed growth and establishment. Biocontrol is successful when the weed, the pathogen, and environment are associated in such a manner that weed control or suppression is possible (Fig. 1). Questions arise as to the type of management systems that will favor biocontrol by increasing the successful interaction of these three components. Currently, more than 100 pathogens have been identified as having the potential for weed biocontrol, and the research on biological control agents continues to increase. The three main strategies for biological control are the classical, augmentative, and integrated management approaches for weed suppression. What types of biological control agents exist?
Most of the research on microbial control of weeds has concentrated on fbngal plant pathogens for broadleaf weed control. Most notable is the use of rust fungi and mycoherbicides commercially available under the trade names of DeVine, Collego, and BioMal. The success of these commercial mycoherbicides indicates the potential for the use of microorganisms in weed control technology. Several other pathogens representing a wide range of fungal classes are being investigated for their biocontrol potential as well. The role of bacteria in weed control also is being explored, although their potential contribution often is overlooked. Will formulations enhance biocontrol?
The delivery and survival of biocontrol agents are critical to the success of weed suppression. Formulations protect the microorganism, enhance their growth or survival in soil or on the leaf, and deliver viable and active biocontrol agents. There is a range of formulations using varying substrates, including wheat bran, alginate, vermiculite and montmorillonite, polyacrylimide and carrageenan pellets, and several synthetic polymers that can be used in both liquid or solid fermentation. Diversity with respect to type of biocontrol agent and its temperature and moisture requirements for germination, infection colonization, and sporulation requires that a variety of formulations be developed and used.
.
How can interactions with other stresses be used in biocontrol? The compatibility and synergistic effects of microbial and chemical herbicide interactions will assist in the integration of biological control agents with synthetic chemical herbicides for improved weed management strategies. Combinations of biological control agents and reduced rates of chemicals may improve control and broaden the spectra of control. The concept of multiple stresses as a means of plant suppression needs further study, whether that be microbeherbicide or microbe/other growth regulators to increase activity, selectivity, or spectrum of control. Full scientific article from which this summary was written begins on page 480 of this issue.
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I
Do weed-suppressive soils exist? The changes in microbial communities readily observed with changes in management and weed-suppressive communities may exist and can be altered with management. In biologically based weed management, weed-suppressive soils can be an important component in weed control. Management of these soils could enhance weed suppression. Microbial activity of the indigenous organisms could contribute to the depletion of the weed seed bank and can be managed for greater weed seed decay. Native biocontrol agents can be used and enhanced for weed control. What are the future considerations to implementation of biocontrol?
There are many challenges ahead for the use of microbes for weed control. Future research endeavors should address the discovery, ecology, mechanisms of action, molecular investigations, and fermentation and delivery technologies. The research on microbial-based biological weed control has demonstrated the potential for use of naturally occurring plant-suppressive microbes as a novel, nonchemical approach for suppressing and reducing weeds. Microbes can have a profound effect on plant growth, and thus must be considered in weed management strategies. Ecologically based approaches, such as biological weed control, which take into consideration all components, including the weed, the biocontrol agent, and the environment, will result in the greatest success.
Fig. 1. The interaction among the weed, the pathogen, and the environment that results in biological weed control.
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Microorganisms in Weed Control Strategies A. C. Kennedy* and R. J. Kremer Alternative weed management strategies are needed to expand the capability of weed control as weed pressures continue to limit optimum yield, and as the use of synthetic chemical herbicides for weed control becomes more restricted. Biological control of weeds is based on the premise that biotic factors influence the distribution, abundance, and competitive abilities of plant species. Biological control is one alternative means of suppressing weed growth and establishment. More than 100 microorganisms have been identified as having the potential for weed biocontrol. There are, however, a number of problems with using these agents that must be solved, including limited host spectrum, lack of consistency across environments, and slow or inadequate weed suppression. It has been shown that soil microorganisms are capable of suppressing weeds in the field. It is imperative to develop an understanding of these soil microbes and their ecology so that they may be used to benefit agriculture, especially for weed management. Further study is required so that they may be produced efficiently and used effectively in weed management strategies.
W
EED MANAGEMENT is one of the critical factors limiting crop yield in agricultural systems; however, excess herbicide use can negatively affect our groundwater and environment. Pesticide use in the USA has increased annually (USDA-ERS, 1993), with herbicide use comprising the largest share of all pesticides used (Gianessi and Puffer, 1991; Bridges, 1994). Public awareness and concern has also increased. Alternative weed management strategies are needed as the use of synthetic chemical herbicides for weed control becomes more restricted. These factors led us to consider alternative means of weed management such as biological control. The diversity of soil microbes is high, although our knowledge of them is limited. A gram of soil may contain up to 4000 different bacterial species (Torsvik et al., 1990). It has been estimated that up to 1 million different bacterial species may exist on earth (American Society for Microbiology, 1994). Less than 1% of the microbial inhabitants of the earth are known or are in culture collections (Hawksworth, 1991). Although microbes are responsible for nutrient cycling, residue decomposition, maintenance of soil structure, and more, the total hctioning of microorganisms in an agroecosystem is largely unknown. The present use and potential applications of these microorganisms must be considered in pest management strategies. The objectives of this manuscript are to illustrate the ongoing research on
microbes for weed management and to identify approaches to expand the role of microbes in biological weed control.
BIOLOGICAL CONTROL Biological control uses natural enemies to control such pests as insects, pathogens, and weeds.Biologica1 control can be defined as “the action of parasites, predators, or pathogens in maintaining another organism’s population density at a lower average than would occur in their absence” (DeBach, 1964). Another broader definition includes all forms of intervention and is stated as “the use of natural or modified organisms, genes, or gene products to reduce the effects of undesirable organisms (pests), and to favor desirable organisms such as crops, trees, animals, and beneficial insects and microorganisms” (Cook, 1987). Biological weed control takes advantage of biotic factors that influence the distribution, abundance, and competitive abilities of plant species. Biological control offers an alternative to herbicides as a means of suppressing weed growth and establishment. Biocontrol is successful when the weed, the biocontrol agent, and environment interact in such a manner that weed control or suppression occurs (Fig. 1). The challenge ahead is to develop management systems that favor biocontrol by increasing the interaction of these three components. This can be achieved by altering the ecology and increasing the survival of the biocontrol agent, increasing the susceptibility of the weed, or altering the environment to enhance biocontrol potential. Currently, more than 100 biocontrol agents have been identified as having the potential for weed biocontrol (Table 1) and the research on biological control agents continues. Researchers have to develop an understanding of microbes and the soil and phyllosphere ecology of microbes, so that they may be used to benefit weed management and agriculture. The three main strategies for biological control are the classical, inundative, and integrated management approaches for weed suppression (DeBach, 1964; TeBeest, 1991). The classical approach involves the importation of exotics or the use of natural enemies for release, dissemination, and self-perpetuation on target pests. Insects and rust fungi have
Pathogen Escape
A.C. Kennedy, USDA-ARS, Pullman, WA 99164-6421; R.J. Kremer, USDA-ARS, Columbia, MO 6521 1. Contribution 9504-1 1 from the USDA-ARS in cooperation with the Washington State Univ. College of Agric. and Home Econ. Agric. Res. Cent., Pullman, and Univ. of Missouri Agronomy Dep., Columbia. Received 27 Apr. 1995. *Corresponding author (
[email protected]). Published in J. Prod. Agric. 9:48&485 (1996).
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PATHOGEN
Fig. 1. The interaction among the weed, the pathogen, and the environment that results in biological weed control.
Table 2. Select microbial weed control projects.
Table 1. The status of microbial weed control projects. ~
Weeds targeted Microorganisms studied Surveys underway Lab/greenhouse tests Field tests Commercialized
1982t
19897
1995
35 54
67 I09 13 29 36 7
107 150 50 50
1 12 18
2
45 4
t From Charudattan, 1991. been successful classical approaches to weed control. The addition of a virulent strain to suppress weeds is known as the inundative or bioherbicide approach. The biocontrol agent is not self-sustainingand must be applied to the target host every season. The last approach, the integrative approach, is a broad approach and not yet well-defined, which involves management of weed-suppressive soils, including practices to conserve or enhance native enemies of weeds. An effective biological control agent should possess certain characteristics. Most importantly, biological control agents must first have a fairly narrow host specificity or selectively suppress a target organism without adversely affecting nontarget species. A host range has to be broad enough to include similar weed species; too narrow a host range, however, can limit the use and marketability of the final product. Suppression of the pest does not necessarily have to be 100% to be effective. Secondly, the agent must survive and function in the environment. It is very easy to find antagonistic relationships in the lab, but often these relationships do not persist in field situations under varying environmental conditions. Survival of the introduced microbes is critical and is controlled by physical constraints, competition with other microbes, and growth on the seed, leaf, and root. The microorganism must survive and proliferate on the leaf or in the soil and tolerate fluctuations in moisture and temperature. Formulation and application technology can be developed to enhance survival and bioactivity of biocontrol microorganisms. Thirdly, the biocontrol agent must suppress the target organism at a critical point in its growth. Weed characteristics are critical to biocontrol success. These include factors that influence seed, root, or leaf colonization; infection by the biocontrol organism; and the competition of the weed with the crop. Information on economic suppression and the biological interaction with herbicides and other stresses is also needed. Finally, the biological control procedure must be practical, economical, and compatible with other methods of weed control. FUNGAL BIOLOGICAL CONTROL AGENTS Most of the research on microbial control of weeds has concentrated on hngal plant pathogens for broadleaf weed control. Most notable are the use of the rust fungi (Puccinia juceue Otth.) for the control of diffuse knapweed (Centuuriu dfffusa Lam.) (Mortensen, 1986; Watson and Clement, 1986), and Puccinia chondrillinu Bubak & Syd. for skeleton weed (Chondrillajuncea L.) (Cullen et al., 1973) control. A limited number of fungal biocontrol agents of weeds formulated as mycoherbicides have been commercially developed under the trade names of DeVine (Phytophthorapalmivora),
Trade name
Microorganism
Weed
Crop
Reference
Stranglervine, Citrus Ridings, 1986 DeVine Phytophthora palmivora milkweed vine Northern Rice, Daniel et al., 1973 Collego Colletonichum gloesporioides jointvetch soybean Sicklepod Soybean Walker & Boyette, CAAST Alternaria cassiae &peanut 1985 BioMal Colletotrichum Roundleaf Lentil, Mortensen, 1988 mallow small grains gleosporioides sp. Malvae
Collego (Colletotrichum gloeosporioides f. sp. aeschynomene), and BioMal (Table 2). DeVine is being used to control stranglervine [Morrenia odorata (H. and A.) Lindl.] in citrus (Ridings, 1986) and Collego (Daniel et al., 1973) is used for the control of northern jointvetch [Aeschynomene virginica (L) B.S.P.] (Templeton, 1982) in rice (Otyza sativa L.) and soybean [Glycine mux (L.) Merr.]. BioMal was recently registered for the control of round leaf mallow (Mulvapusilla) (Mortensen, 1988) in small grains and lentil (Lens culinaris Medikus). CASST (Alternaria cassiae) is a mycoherbicide for the control of sickle pod (Cassia obtusifolia L.) in soybean and peanut (Arachis hypogaea)(Walker and Boyette, 1985). The success of these commercial mycoherbicides indicates the potential for the use of microorganisms in modem weed control technology. At this time, however, these products are not being marketed as widely as had been expected due to limited acreage of the host weed. Their lack of acceptance and limited use illustrate the problems facing biocontrol agents. Several additional agents representing a wide range of fungal classes are being investigated for their biocontrol potential. These include Colletotrichum coccodes for the control of eastern black nightshade (Solanum ptycanthum Dun.)(Andersen and Walker, 1985) and Fusarium lateritium to suppress prickly sida (Sida spinosa L.) and velvetleaf (Abutilon theophrusti Medikus)(Boyette and Walker, 1985). Phomopsis convolvulus has been investigated for the control of field bindweed (Convolvulus arvensis L.) (OrmenoNunez et at., 1988) and Bipolaris sorghicola has been studied for johnsongrass (Sorghum halepense L.Pers.)( Winder and Van Dyke, 1989) control. Programs also investigate Alternaria crasse for control of jimsonweed (Datura stramonium L.) and Sclerotiniu sclerotiorum (Lib.) de Bary for control of Canada thistle [Cirsium arvense (L.) Scop.], spotted knapweed (Centauria maculosas Lam.), and dandelion (Taraxacum oficinale Weber) (Brosten and Sands, 1986; Miller et al., 1989; Riddle et al., 1991). The list of fungi for potential biocontrol agents is extensive and only a portion of those being studied are mentioned here. The development of commercially acceptable bioherbicides requires further understanding of the interactions among the plant, microorganisms and the environment. BACTERIAL BIOLOGICAL CONTROL AGENTS Bacteria have a role in weed control, although their potential contribution often is overlooked (Kremer and Kennedy, 1996). Bacteria exert a subtle yet profound effect on plant growth. While most fungal biological control agents are foliarly applied and rely on infection and disease, J. Prod. Agric., Vol. 9, no. 4, 1996 481
many bacterial biological control agents are soil applied and rely on suppression of the weed seedling. A wide variety of these bacteria were found to inhibit velvetleaf, morning glory (Ipomoea spp.), cocklebur (Xanthiumstrumarium L.), pigweed (Amaranthus spp.), lambsquarters (Chenopodium spp.), smartweed (Polygonum spp.), and jimsonweed (Kremer, 1986b; Kremer et al., 1990). The potential of deleterious rhizobacteria for biological weed control has been reported for broadleaf weeds (Kremer, 1986b; Kremer et al., 1990) and the grass weeds downy brome (Bromus tectorum L.)(Kennedy et al., 1991),japanese brome (Bromusjaponicus L.)(Harris and Stahlman, 1995) and jointed goatgrass (Aegilops cylindrica Host.) (Kennedy et al., 1992b). These deleterious rhizobacteria have been used for the control of downy brome in the field (Kennedy et al., 1991). Deleterious rhizobacteria that specifically inhibit various grass weeds, but do not affect the crop, have been isolated from soil (Kennedy et al., 1991; Kennedy et al., 1992b). They inhibit plant growth by the production of plant-suppressive compounds (Tranel et al., 1993). These bacteria are excellent biological control agents, in part, because they are aggressive colonizers of the roots and residue, often comprising up to 95% of the total bacteria on the plant root (Stroo et al., 1988; Kennedy et al., 1992a). These bacteria can function as a direct delivery system for the natural plantsuppressive compounds they produce. Bacteria appear to have a place in biological weed control, but further investigation is required. FORMULATIONS
The delivery and survival of biocontrol agents are critical to successfd weed suppression. Formulations protect the microorganism, enhance their growth and survival in soil or on the leaf, and deliver viable and active biocontrol agents. There is a range of formulations using varying substrates, including wheat bran, alginate, vermiculite and montmorillonite, polyacrylimide and carrageenan pellets, and several synthetic polymers that can be used in both liquid and solid fermentation (Fravel and Lewis, 1992; Quimby et al., 1989). Protection of the agent would increase efficacy because the dew period is critical for fungal growth and survival is the key to bacterial and fungal biocontrol efficacy (Boyette et al., 1991). A peat inoculum formulated with velvetleaf-suppressive rhizobacteria was effective at reducing velvetleaf emergence in greenhouse and field studies (Begonia, 1989). Diversity with respect to type of biocontrol agent and its temperature and moisture requirements for germination, infection, colonization, sporulation, and overall performance requires that a variety of formulations be developed and used. INTERACTIONS
The compatibility and synergistic effects of microbial and chemical herbicide interactions will assist in the integration of biological control agents and synthetic chemical herbicides for improved weed management strategies. Combinations of biocontrol agents and chemical herbicides (at reduced rates) may improve and broaden the spectra of control (Charudattan and De Loach, 1988). Integration of 482
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stresses has been demonstrated for velvetleaf control using the fungal pathogen Fusarium oxysporum and chemical herbicides (Kremer and Schulte, 1989). Colonization of wheat roots by Pseudomonas spp. was increased when plants were treated with a herbicide (Greaves and Sargent, 1986). Plant pathogens combined with insects achieve greater weed control. The use of insects as either vectors of biocontrol agents or the fbngal biocontrol agent combined with a seed-feeding insect increased weed control compared with either method alone (Kremer and Spencer, 1989). The concept of multiple stresses by microbeherbicide or microbe/other growth regulators as a means of plant suppression requires m e r study. A combination of the biological control agent and reduced rates of herbicides may significantly reduce the infestations of weeds and may act synergistically with herbicides to increase activity, selectivity, or spectrum of control by the microbial agent. WEED-SUPPRESSIVE SOILS
The changes in microbial communities are readily observed with changes in management (Kennedy and Smith, 1995) and weed suppressive communities may be altered with management as well. In biologically based weed management, weed-suppressive soils can be an important component of weed management by enhancing weed suppression (Kremer, 1986a; Roberts et al., 1986; Kirkpatrick and Bazzaz, 1979). Microbial activity of indigenous organisms could contribute to the depletion of the weed seed bank (Fig. 2) (Kremer, 1993) and can be managed for greater weed seed decay. Native biocontrol agents can be used and enhanced for weed control. This is no easy task, in that the soil system is quite complex. A diversity of biocontrol agents residing within the soil, a diverse population of target weeds, and environmental variables all contribute to the development of microbial populations that could, in various ways, suppress weed growth. The number of weed-suppressive bacteria in soil varies with management, which may influence the competitive ability of the weed, and thus may be a useful consideration in developing biological control agents (Kennedy, 1990, unpublished data). The horizonation of residue and microbial activity in some systems, such as no-till, establishes areas of increased seed decay potential within the residue zone, thereby exhibiting increased weed-suppression potential relative to other soil microsites. FUTURE CONSIDERATIONS
There are many challenges ahead for the use of microbes for weed control. Future research endeavors should address the following areas: Discovery. The diversity of microorganisms and our lack of understanding of this diversity suggests that many biological control agents are yet to be discovered. With the development of each new agent and host, new concepts and problems will arise, increasing our understanding of plantmicrobe interactions and the acceptance of microorganisms for weed control. Ecology. A more complete understanding of the ecology of the introduced microbe is imperative to increasing sur-
ture, temperature, and radiation sensitivities may be reduced through formulation technology.
viva1 and efficacy, and thus improving the effectiveness of biological control agents. Survival of the microbe is critical to the success of the agent. Weed ecology also should be considered in biocontrol. Mechanisms. Knowledge of the structure and mode of action of each plant-suppressive compound is imperative to understanding the mechanisms of inhibition so that microorganisms can be manipulated to enhance compound activity and specificity. Molecular Investigations. Molecular investigations will uncover the genetic basis of virulence and host specificity and broaden our understanding of the range of diversity in biocontrol agents (Kennedy, 1995). Genetic manipulation of the microbes may increase metabolite production, regulate host specificity or host range, and regulate production of the plant-suppressivecompounds. This regulation will allow the control of expression of plant-suppressive genes by specific promoters or under specific environmental conditions. Fermentation und Delivery Technology.A greater understanding of the factors involved in efficient commercial inoculum production is needed for the practical, economical production of microbial biocontrol agents. The shelf life of the organism in the finished product also demands consideration. A greater understanding of the ecological constraints of each system, the weed, and the microbe will foster development of delivery systems or formulations that will reduce the impact of the biotic and abiotic forces and increase the viability, efficacy, and ease of application. Many of the problems affecting survival of the bacterium, such as mois-
SUMMARY Research on microbial-based biological weed control has demonstrated the potential for use of naturally occurring, plant-suppressive microbes as a novel, nonchemical approach for suppressing weeds and reducing weed interference. Microbes can have a profound effect on plant growth, and thus must be considered in weed management strategies. Microbial weed control agents should significantly reduce crop production costs, the need for tillage, and synthetic chemical herbicide use. These reductions will, in turn, increase profits, while reducing erosion and contamination of surface and ground water. The biological control alternative to weed management uses natural biocontrol agent/ plant interactions, and plant/plant competition. Biological systems, however, need special management considerations to enhance their activity and achieve a reduction in weed growth. Development of management approaches for weedsuppressive soils to take advantage of naturally occurring communities of soil microbes is an urgent need. Microbes are a tool in sustainable systems to be used in concert with other weed management techniques, such as cultural practices and herbicide application. Suppression of weeds by multiple stresses may be more successful than relying on a single means of control. Biological control agents will not replace herbicides, rather these agents can be used with
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I N T EG R AT IO N:
1 Seed-attacking
1
chemicals
.
insects
-1-
Weed seeds on parent plants
_.
i ____-__
Growt h-regulating chemicals
-
I.___
-I n d u ce s s e e d imbibition -Stimulates s e e d exudation
R educes s e e d number R educes s e e d v i a b i l i t y Pr edispose s e e d to microbial a t t a c k
/
=
\
Ch e mo taxis
I
WEED SEED BANK
I
Exudation
De teri o ra t ion R esistance
Fig. 2. Relationships of microorganisms and weed seeds in the soil environment. (Modified from Kremer,1993).
J. Prod. Agric., Vol. 9, no. 4, 1996 483
reduced levels of synthetic chemicals for economic suppression of weeds. Biological control demands an understanding of the ecology of the system, its participants, and their plant specificity. Ecologically based approaches, such as biological weed control, which take into consideration all components, including the weed, the biocontrol agent, and the environment, will result in the greatest success for pest management in sustainable systems. ACKNOWLEDGMENTS Trade names and company names are included for the benefit of the reader and do not imply endorsement or preferential treatment of the product by the USDA, Washington State University, or the University of Missouri. All programs and services of the USDA are offered on a nondiscriminatory basis without regard to race, color, national origin, religion, sex, age, marital status, or handicap.
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