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Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
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6

View of a Microbial Ecologist

STEVE LINDOW

University of California, Berkeley

Microbial ecology principles will be important in any future efforts to practice ecologically based pest management. It is clear we lack a complete understanding of a number of important issues relating to interactions between pests and crop plants as well as between pests and other microorganisms. It will be important to determine the mechanisms of interaction between microorganisms in order to know the potential for ecologically based pest management as well as the degree to which it has been achieved. A lack of understanding of these interactions limits our ability to understand the processes that occur during our efforts to implement ecologically based pest management. Unless a more thorough understanding of the ecological principals dictating microbial and plant interactions is obtained, efforts to achieve ecologically based pest management will remain empirical and will lack transferability between systems. On the other hand, by understanding particular model systems in which ecologically based management can be successfully implemented, it should be possible to develop common strategies and practices by which pest management can be relied upon in the future. Examples of important ecological principles that will need to be understood, as well as recent attempts to obtain information in these areas, will now be presented.

One of the most powerful and dramatic recent applications of technology to microbial ecology has been to address questions of population structure and population genetics. Until recently, we lacked tools to differentiate between

Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
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individuals in populations of the groups of microorganisms that operate either as pest microorganisms or as biological control agents. For this reason, it was previously impossible to know whether a population of a target pest was genetically homogeneous, and therefore might be expected to react similarly to a biological control agent, or was genetically diverse and requiring more complex strategies of management such as in the deployment of plant disease resistance genes. One of the more important tools for implementing ecologically based pest management is that of the effective deployment of plant disease resistance genes. Because of a gene-for-gene relationship between resistance genes in a host plant and avirulence genes in a plant pathogen, it is important to understand the population genetics of the plant pathogen as well as processes that could lead to changes in the genetic structure of the population, since changes could lead the pathogen to overcome plant disease resistance. Because of the ease with which plant pathogens can now be spread around the world by human activities, we need to be knowledgeable about pathogen diversity throughout the globe to be able to deploy plant disease resistance genes in a way in which resistance will be durable. A good example of a detailed examination of a plant pest population has recently come from the laboratory of Dr. Jan Leach of Kansas State University, who studied the bacterial plant pathogen Xanthomonas oryzae, one of the most important pathogens of cultivated crops (George et al.,1997; Raymundo et al., 1999). Her analysis of the populations of this pathogen in a variety of tropical regions where rice is grown showed that the pathogen had apparently been spread widely to rice grain regions but that local variation in a pathogen population also can occur. This information is clearly applicable to regional and local plant breeding efforts to develop disease resistant rice cultivars in that it elucidates the need to include a wide variety of pathogen genotypes in selection schemes to anticipate introduction of novel pathogenic strains.

Knowledge of the population structure of soilborne pathogens is also important in implementing biocontrol procedures. For example, the soilborne plant pathogenic fungus Armillaria mellea, which can attack the subterranean parts of a variety of woody plants, has recently become a prominent disease problem in pear orchards in California. The recurrence of this disease might be associated with changes in cultural practices such as irrigation or fertilization but the introduction of novel virulent strains of the pathogen could not be ruled out without a better understanding of the population structure of the pathogen in the orchards. However, David Rizzo of the University of California at Davis was able to ascertain, using molecular techniques, that a limited number of genotypes of pathogen occur within a given orchard, and that large contiguous areas of trees are apparently infected by clonal representatives of a given strain of the plant pathogen, apparently originating from infections of native tree species hundreds of years ago (Rizzo et al.,1998). Thus, it appears that changes in cultural practices, perhaps increased amounts or altered times of irrigation in recent years, have stimulated a preexisting pathogen within the orchards. Without an understanding of the pathogen structure within these orchards, such conclusions would have been impossible and a focus of disease management based on cultural practices could not have been made.

Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×

The role of microorganisms in common cultural practices for pest management such as crop rotation and soil amendments can now be better understood using molecular biological tools. For example, it has frequently been observed that the incorporation of green plant residues (green manures) into soils can decrease the severity of diseases caused by soilborne plant pathogens such as Verticillium dahlia. Clearly, the introduction of large amounts of plant material into soils could have many effects on the composition and behavior of soil microorganisms. Although numerous descriptions of changes in soil microorganisms have been provided, it has been recognized through the work of Oen Huisman and James Davis (and others) that a common feature of soil microorganisms in sites that have become resistant to disease due to the addition of green manures is an increase in microbial activity (Davis et al., 1996). Increased microbial activity might logically be associated with increased production of antibiotics and other biologically active compounds in the soil. Without the direct measurements of microbial activity that are now possible, statements about the potential involvement of microbial communities and negative interactions with soilborne plant pathogens would remain hypothetical.

One of the most striking and influential contributions of molecular microbial ecology to the study of pest management has been to better define the composition of microbial communities in a given habitat. It is deplorable that only less than about 1 percent of the soil microorganisms found in agricultural soils can be cultured and hence studied. It seems likely that many of the unculturable microorganisms play an important role in the disease process and in maintaining plant health. While few advances in our ability to culture soilborne microorganisms have been made, it is now possible to obtain a direct assessment of their diversity and identity. Culture-independent methods of identifying microorganisms, for example, by amplification of common molecules such as 16S rRNA genes, has made it possible to identify microorganisms present in a sample. Such studies, when applied to soil microorganisms, reveal incredible levels of diversity among the unculturable microorganisms. For example, a study by Dr. Eric Tripplet of the University of Wisconsin revealed not only that high levels of diversity are found in agricultural soils but that different microorganisms are found in disturbed agricultural soils compared to undisturbed forest soils (Borneman and Triplett, 1997). Although we remain far from the goal of being able to specifically manipulate microbial communities in soils, tools are now available to assess impacts of agricultural practices such as cultivation and crop rotation.

Molecular tools of microbial ecology now enable us to obtain a better insight into what microorganisms are doing while in their natural habitats. An understanding of microbial activities in situ will be required before we can hope to routinely manipulate systems to achieve pest management. It is now possible, for example, to determine the conditions in which a plant pathogen will express virulence traits. The plant pathogen Pseudomonas syringae pv. syringae, which causes a variety of diseases including a leaf and fruit spot of cherry, damages plants by its production of a phytotoxin. The genes for these toxins have now been cloned and work by Dr. Dennis Gross of Washington State University has demonstrated that such genes are not expressed except when the pathogen is

Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×

found associated with cherry (Mo et al.,1995). Furthermore, specific phenolic elicitors of gene expression when combined with sugar exudates found in host plants are sufficient to elicit toxin production (Quigley and Gross, 1994). Such detailed knowledge of pathogen behavior might form the basis for innovative strategies to evade the deleterious traits of plant pathogens by selective breeding to eliminate plant signals required for virulence.

Molecular genetic tools when applied to microbial ecology should enable us to better understand interactions between microorganisms that can confer biological control of important diseases. Whereas a number of microbial traits such as antibiotic production, chitinase production, and the production of iron-sequestering agents have all been implicated in biological control, in most cases we lack understanding of the expression of these traits in the habitats where biological control must occur. New tools have now been developed, however, that permit assessment of the level of expression of those genes implicated in biological control. For example, work by Dr. Joyce Loper of the US Department of Agriculture, Corvallis, OR, has clarified the role of iron siderophores in biological control. It was hypothesized that the rhizosphere of plants often lacks sufficient iron to allow unrestricted growth of plant pathogens prior to infection. Biological control agents, by acquiring iron in the infection court, might deprive plant pathogens of needed iron and thereby confer disease control by iron competition. By fusing iron-regulated genes involved in pyoverdine siderophore production with an ice nucleation reporter gene, Dr. Loper's group was able to demonstrate that available iron concentrations are moderately low in many soils but that iron availability in the rhizosphere was greatly dependent on the plant species itself (Loper and Henkels, 1997). This work provides a basis to predict those plant species and conditions under which control with an introduced siderophore-producing biological control agent would be expected to be maximally effective.

It is clear that a better understanding of microbial plant pests, as well as associated microorganisms that might be involved in their management, needs to be gained before ecologically based pest management schemes can be reliable. It is expected that the reliability of such management schemes will increase as we move from an empirically based protection strategy to one based on knowledge of the identity of the organisms and their activities in agricultural ecosystems.

REFERENCES

Borneman, J., and E.W. Triplett. 1997. Molecular microbial diversity in soils from eastern Amazonia: Evidence for unusual microorganisms and microbial population shifts associated with deforestation. Applied and Environmental Microbiology 63:2647–2653.

Davis, J.R., O.C. Huisman, D.T. Westermann, S.L. Hafez, D. Everson, L.H. Sorensen, and A.T. Schneider. 1996. Effects of green manures on Verticillium wilt of potato. Phytopathology 86:444–453.

Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×

George, M.L.C., M. Bustamam, S.T. Cruz, J.E. Leach, and R.J. Nelson. 1997. Movement of Xanthomonas oryzae pv. oryzae in southeast Asia detected using PCR-based DNA fingerprinting. Phytopathology 87:302–309.

Loper, J.E., and M.D. Henkels. 1997. Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Applied and Environmental Microbiology 63:99–105.

Mo, Y.-Y., M. Geibel, R.F. Bonsall, and D.C. Gross. 1995. Analysis of sweet cherry (Prunus avium 1.) leaves for plant signal molecules that activate the syrB gene required for synthesis of the phytotoxin, syringomycin, by Pseudomonas syringae pv syringae. Plant Physiology 107:603–612.

Quigley, N.B., and D.C. Gross. 1994. Syringomycin production among strains of Pseudomonas syringae pv. syringae: Conservation of the syrB and syr D genes and activation of phytotoxin production by plant signal molecules . Molecular Plant-Microbe Interactions 7:78–90.

Raymundo, A.K., A.M. Briones, E.Y. Ardales, M.T. Perez, L.C. Fernandez, J.E. Leach, T.W. Mew, M.A. Ynalvez, C.G. McLaren, and R.J. Nelson. 1999. Analysis of DNA polymorphism and virulence in Philippine strains of Xanthomonas oryzae pv. oryzicola. Plant Disease 83:434–440.

Rizzo, D.M., E.C. Whiting, and R.B. Elkins. 1998. Spatial distribution of Armillaria mellea in pear orchards. Plant Disease 82:1226–1231.

Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×
Page 32
Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×
Page 33
Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×
Page 34
Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×
Page 35
Suggested Citation:"6 View of a Microbial Ecologist." National Research Council. 2000. Professional Societies and Ecologically Based Pest Management: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/9888.
×
Page 36
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The National Research Council's (NRC) Board on Agriculture and Natural Resources invited professional societies associated with agriculture and ecology to participate in a two-day workshop to explore leadership and a common vision for ecologically based pest management (EBPM). These proceedings describe the challenges of and opportunities for EBPM discussed by participants in the workshop.

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