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Do microorganisms influence seed-bank dynamics?

Published online by Cambridge University Press:  20 January 2017

Joanne C. Chee-Sanford ,
Martin M. Williams II ,
Adam S. Davis  and
Gerald K. Sims
Martin M. Williams II
Affiliation:
United States Department of Agriculture—Agricultural Research Service, Invasive Weed Management Research, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801
Adam S. Davis
Affiliation:
United States Department of Agriculture—Agricultural Research Service, Invasive Weed Management Research, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801
Gerald K. Sims
Affiliation:
United States Department of Agriculture—Agricultural Research Service, Invasive Weed Management Research, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801
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Abstract

Reduction of seed-bank persistence is an important goal for weed management systems. Recent interest in more biological-based weed management strategies has led to closer examination of the role of soil microorganisms. Incidences of seed decay with certain weed species occur in the laboratory; however, their persistence in soil indicates the presence of yet-unknown factors in natural systems that regulate biological mechanisms of seed antagonism by soil microorganisms. A fundamental understanding of interactions between seeds and microorganisms will have important implications for future weed management systems targeting seed banks. Laboratory studies demonstrate susceptibility to seed decay among weed species, ranging from high (velvetleaf) to very low (giant ragweed). Microscopic examinations revealed dense microbial assemblages formed whenever seeds were exposed to soil microorganisms, regardless of whether the outcome was decay. Microbial communities associated with seeds of four weed species (woolly cupgrass, jimsonweed, Pennsylvania smartweed, and velvetleaf) were distinct from one another. The influence of seeds on microbial growth is hypothesized to be due to nutritional and surface-attachment opportunities. Data from velvetleaf seeds suggests that diverse assemblages of bacteria can mediate decay, whereas fungal associations may be more limited and specific to weed species. Though microbial decay of seeds presents clear opportunities for weed biocontrol, limited success is met when introducing exogenous microorganisms to natural systems. Alternatively, a conservation approach that promotes the function of indigenous natural enemies through habitat or cultural management may be more promising. A comprehensive ecological understanding of the system is needed to identify methods that enhance the activities of microorganisms. Herein, we provide a synthesis of the relevant literature available on seed microbiology; we describe some of the major challenges and opportunities encountered when studying the in situ relationships between seeds and microorganisms, and present examples from studies by the ARS Invasive Weed Management Unit.

Keywords

Giant ragweed, Ambrosia trifida L.jimsonsweed, Datura stramonium L.Pennsylvania smartweed, Polygonum pensylvanicum L.velvetleaf, Abutilon theophrasti Medic.woolly cupgrass, Eriochloa gracilis (Fourn) A. S. HitchcSeed–microorganism interactionweed seed decaysoil microbiologymicrobial communitiesseed-bank ecologymultitrophic systemsintegrated weed management
Type
Symposium
Information
Weed Science , Volume 54 , Issue 3 , June 2006 , pp. 575 - 587
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Amann, R., Fuchs, B. M., and Behrens, S. 2001. The identification of microorganisms by fluorescence in situ hybridisation. Curr. Opin. Biotechnol 12:231–236.Google Scholar
Anderson, I. C. and Cairney, J. W. G. 2004. Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ. Microbiol 6:769–779.CrossRefGoogle ScholarPubMed
Barns, S. M., Takala, S. L., and Kuske, C. R. 1999. Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl. Environ. Microbiol 65:1731–1737.CrossRefGoogle ScholarPubMed
Baskin, C. and Baskin, J. 1998. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. San: Diego: Academic.Google Scholar
Baskin, C. C. and Baskin, J. M. 2006. The natural history of soil seed banks of arable land. Weed Sci 54:549–557.Google Scholar
Baskin, J. M. and Baskin, C. C. 2000. Evolutionary considerations of claims for physical dormancy-break by microbial action and abrasion by soil particles. Seed Sci. Res 10:409–413.Google Scholar
Benech-Arnold, R. L., Sánchez, R. A., Forcella, F., Kruk, B. C., and Ghersa, C. M. 2000. Environmental control of dormancy in weed seed banks in soil. Field Crops Res 67:105–122.Google Scholar
Booth, B. D., Murphy, S. D., and Swanton, C. J. 2003. Weed Ecology in Natural and Agricultural Systems. Cambridge, MA: CABI.Google Scholar
Borneman, J. and Hartin, R. J. 2000. PCR primers that amplify fungal rRNA genes from environmental samples. Appl. Environ. Microbiol 66:4356–4360.CrossRefGoogle ScholarPubMed
Broekaert, W. F., Terras, F. R. G., Cammue, B. P. A., and Osborn, R. W. 1995. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108:1353–1358.CrossRefGoogle ScholarPubMed
Buhler, D. D. and Hartzler, R. G. 2001. Emergence and persistence of seed of velvetleaf, common waterhemp, woolly cupgrass, and giant foxtail. Weed Sci 49:230–235.Google Scholar
Buhler, D. D., Hartzler, R. G., and Forcella, F. 1998. Weed seed bank dynamics: implications to weed management. J. Crop Product 1:145–168.Google Scholar
Buhler, D. and Hoffman, M. 1999. Andersen's Guide to Practical Methods of Propagating Weeds & Other Plants. Lawrence, KS: Weed Science Society of America.Google Scholar
Buhler, D. D., Kohler, K. A., and Thompson, R. L. 2001. Weed seed bank dynamics during a five-year crop rotation. Weed Technol 15:170–176.CrossRefGoogle Scholar
Céspedes, R., González, B., and Vicuña, R. 1997. Characterization of a bacterial consortium degrading the lignin model compound vanillyl-D-glucopyranoside. J. Basic Microbiol 3:175–180.Google Scholar
Chandramohan, S., Charudattan, R., Sonoda, R. M., and Singh, M. 2002. Field evaluation of a fungal pathogen mixture for the control of seven weedy grasses. Weed Sci 50:204–213.CrossRefGoogle Scholar
Chee-Sanford, J. C., Connor, L. M., and Holman, T. J. 2003. Characterization of weed seed decay activities mediated by natural soil microbial populations. in Abstracts of the 103rd General Meeting of the American Society for Microbiology. Washington, D.C.: ASM Press. Available at http://www.asm.org/memonly/abstracts/AbstractView.asp?AbstractID=78618.Google Scholar
Chee-Sanford, J. C., Connor, L. M., Holman, T. J., Williams, M. M. II, and Sims, G. K. 2004. Interactions between microorganisms and weed seeds: implications for the microbial ecology of seed banks. Page 292 in Abstracts of the 10th International Symposium on Microbial Ecology ISME-10: Microbial planet: subsurface to space.Google Scholar
Davis, A. S. 2006. When does it make sense to target the weed seed bank? Weed Sci 54:558–565.Google Scholar
Davis, A. S., Dixon, P. M., and Liebman, M. 2004. Using matrix models to determine cropping system effects on annual weed demography. Ecol. Appl 14:655–668.CrossRefGoogle Scholar
de Boer, W., Folman, L. B., Summerbell, R. C., and Boddy, L. 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev 29:795–811.Google Scholar
Diaz, E. 2004. Bacterial degradation of aromatic pollutants: a paradigm of metabolic versatility. Int. Microbiol 7:173–180.Google Scholar
Ellis, R. J., Thompson, I. P., and Bailey, M. J. 1995. Metabolic profiling as a means of characterizing plant-associated microbial communities. FEMS Microbiol. Ecol 16:9–18.CrossRefGoogle Scholar
Fenner, M. 1995. Ecology of seed banks. Pages 507–528 in Kigel, J. and Galili, G. (eds.), Seed Development and Germination. New York: Marcel Dekker.Google Scholar
Forney, L. J., Zhou, X., and Brown, C. J. 2004. Molecular microbial ecology: land of the one-eyed king. Curr. Opin. Microbiol 7:210–220.CrossRefGoogle ScholarPubMed
Fries, M. R., Zhou, J-Z., Chee-Sanford, J. C., and Tiedje, J. M. 1994. Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl. Environ. Microbiol 60:2802–2810.Google Scholar
Garbeva, P., van Veen, J. A., and van Elsas, J. D. 2004. Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu. Rev. Phytopathol 42:243–270.Google Scholar
Ghersa, C. M. and Martínez-Ghersa, M. A. 2000. Ecological correlates of weed seed size and persistence in the soil under different tilling systems: implications for weed management. Field Crops Res 67:141–148.Google Scholar
Gibson, J. and Harwood, C. S. 2002. Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu. Rev. Microbiol 56:345–369.Google Scholar
Guérif, J., Richard, G., Dürr, C., Machet, J. M., Recous, S., and Roger-Estrade, J. 2001. A review of tillage effects on crop residue management, seedbed conditions and seedling establishment. Soil Tillage Res 61:13–32.CrossRefGoogle Scholar
Girvan, M. S., Bullimore, J., Ball, A. S., Pretty, J. N., and Osborn, A. M. 2004. Responses of active bacterial and fungal communities in soils under winter wheat to different fertilizer and pesticide regimens. Appl. Environ. Microbiol 70:2692–2701.Google Scholar
Haas, D. and Keel, C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol 41:117–153.Google Scholar
Johansson, J. F., Paul, L. R., and Finlay, R. D. 2004. Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol 48:1–13.Google Scholar
Johnsen, K., Jacobsen, C. S., Torsvik, V., and Sørensen, J. 2001. Pesticide effects on bacterial diversity in agricultural soils—a review. Biol. Fert. Soils 33:443–453.Google Scholar
Kennedy, A. C. 1999. Soil microorganisms for weed management. J. Crop Product 2:123–138.Google Scholar
Kennedy, A. C. and Kremer, R. J. 1996. Microorganisms in weed control strategies. J. Product. Agric 9:480–485.Google Scholar
Kitts, C. L. 2001. Terminal restriction fragment patterns: a tool for comparing microbial communities and assessing community dynamics. Curr. Issues Intest. Microbiol 2:17–25.Google Scholar
Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70.Google Scholar
Kremer, R. J. 1986. Antimicrobial activity of velvetleaf (Abutilon theophrasti) seeds. Weed Sci 34:617–622.Google Scholar
Kremer, R. J. 1993. Management of weed seed banks with microorganisms. Ecol. Appl 3:42–52.Google Scholar
Kremer, R. J. and Schulte, L. K. 1989. Influence of chemical treatment and Fusarium oxysporum on velvetleaf. Weed Technol 3:369–374.Google Scholar
Lewis, W. J., van Lenteren, J. C., Phatak, S. C., and Tumlison, J. H. 1997. A total system approach to sustainable pest management. Proc. Nat. Acad. Sci 94:12243–12248.CrossRefGoogle ScholarPubMed
Lord, N. S., Kaplan, C. W., Shank, P., Kitts, C. L., and Elrod, S. L. 2002. Assessment of fungal diversity using terminal restriction fragment (TRF) pattern analysis: comparison of 18S and ITS ribosomal regions. FEMS Microbiol. Ecol 42:327–337.CrossRefGoogle ScholarPubMed
Lu, Y., Lueders, T., Friedrich, M. W., and Conrad, R. 2005. Detecting active methanogenic populations on rice roots using stable isotope probing. Environ. Microbiol 7:326–336.Google Scholar
Lueders, T., Wagner, B., Claus, P., and Friedrich, M. W. 2004. Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ. Microbiol 6:60–72.Google Scholar
Lueschen, W. E., Andersen, R. N., Hoverstad, T. R., and Kanne, B. R. 1993. Seventeen years of cropping systems and tillage affect velvetleaf (Abutilon theophrasti) seed longevity. Weed Sci 41:82–86.Google Scholar
Lyons, J. I., Newell, S. Y., Buchan, A., and Moran, M. A. 2003. Diversity of ascomycete laccase gene sequences in a southeastern U.S. salt marsh. Microb. Ecol 45:270–281.Google Scholar
Marsh, T. L. 1999. Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. Curr. Opin. Microbiol 2:323–327.Google Scholar
Martin-Laurent, F., Piutti, S., Hallet, S., Wagschal, I., Philippot, L., Catroux, G., and Soulas, G. 2003. Monitoring of atrazine treatment on soil bacterial, fungal and atrazine-degrading communities by quantitative competitive PCR. Pest. Manage. Sci 59:259–268.Google Scholar
Martínez, A. T., Speranza, M., Ruiz-Dueñas, F. J., Ferreira, P., Camarero, S., Guillén, F., Martínez, M. J., Gutiérrez, A., and del Río, J. C. 2005. Biodegradaton of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int. Microbiol 8:195–204.Google Scholar
Meisert, A., Schulz, D., and Lehmann, H. 1999. Structural features underlying hardseededness in Geraniaceae . Plant Biol 1:311–314.CrossRefGoogle Scholar
Mills, K. E. and Bever, J. D. 1998. Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601.Google Scholar
Misra, S. 2005. Engineering broad-spectrum disease resistance. in Information systems for biotechnology news report, p. 3–6, October.Google Scholar
Mummey, D. L. and Stahl, P. D. 2004. Analysis of soil whole- and inner-microaggregate bacterial communities. Microb. Ecol 48:41–50.Google Scholar
Muyzer, G. 1999. DGGE/TGGE a method for identifying genes from natural ecosystems. Curr. Opin. Microbiol 2:317–322.Google Scholar
Nelson, E. B. 2004. Microbial dynamics and interactions in the spermosphere. Annu. Rev. Phytopathol 42:271–309.Google Scholar
Nunan, N., Wu, K., Young, I. M., Crawford, J. W., and Ritz, K. 2002. In situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil. Microb. Ecol 44:296–305.CrossRefGoogle Scholar
Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734–740.Google Scholar
Paerl, H. W. and Steppe, T. F. 2003. Scaling up: the next challenge in environmental microbiology. Environ. Microbiol 5:1025–1038.CrossRefGoogle ScholarPubMed
Quimby, P. C. Jr., DeLoach, C. J., Wineriter, S. A., Goolsby, J. A., Sobhian, R., Boyette, C. D., and Abbas, H. K. 2003. Biological control of weeds: research by the United States Department of Agriculture— Agricultural Research Service: selected case studies. Pest Manage. Sci 59:671–680.Google Scholar
Reeves, R. G. 1936. Comparative anatomy of the seeds of cottons and other malvaceous plants. I. Malveae and Ureneae. Am. J. Bot 23:291–296.CrossRefGoogle Scholar
Reuss, S. A., Buhler, D. D., and Gunsolus, J. L. 2001. Effects of soil depth and aggregate size on weed seed distribution and viability in a silt loam soil. Appl. Soil Ecol 16:209–217.Google Scholar
Rodriguez-Zaragoza, S. 1994. Ecology of free-living amoebae. Crit. Rev. Microbiol 20:225–241.Google Scholar
Roger-Estrade, J., Colbach, N., Leterme, P., Richard, G., and Caneill, J. 2001. Modelling vertical and lateral weed seed movements during mouldboard ploughing with a skim-coulter. Soil Till. Res 63:35–49.Google Scholar
Rondon, M. R., Goodman, R. M., and Handelsman, J. 1999. The earth's bounty: assessing and accessing soil microbial diversity. Trends Biotechnol 17:403–409.CrossRefGoogle ScholarPubMed
Schafer, M. and Kotanen, P. M. 2004. Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35.Google Scholar
Sessitsch, A., Weilharter, A., Gerzabek, M. H., Kirchmann, H., and Kandeler, E. 2001. Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl. Environ. Microbiol 67:4215–4224.Google Scholar
Shingler, V. 2003. Integrated regulation in response to aromatic compounds: from signal sensing to attractive behavior. Environ. Microbiol 5:1226–1241.CrossRefGoogle Scholar
Simon, H. M., Smith, K. P., Dodsworth, J. A., Guenthner, B., Handelsman, J., and Goodman, R. M. 2001. Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere. Appl. Environ. Microbiol 67:514–520.Google Scholar
Singh, B. K., Millard, P., Whiteley, A. S., and Murrell, J. C. 2004. Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393.Google Scholar
Smit, E., Leeflang, P., Glandorf, B., van Elsas, J. D., and Wernars, K. 1999. Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl. Environ. Microbiol 65:2614–21.Google Scholar
Smit, E., Leeflang, P., Gommans, S., Van Den Broek, J., Van Mil, S., and Wernars, K. 2001. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl. Environ. Microbiol 67:2284–2291.Google Scholar
Smith, K. P. and Goodman, R. M. 1999. Host variation for interactions with beneficial plant-associated microbes. Annu. Rev. Phytopathol 37:473–491.CrossRefGoogle ScholarPubMed
Somers, E., Vanderleyden, J., and Srinivasan, M. 2004. Rhizosphere bacterial signalling: a love parade beneath our feet. Curr. Rev. Microbiol 30:205–240.Google Scholar
Tannock, G. W. 1995. Normal Microflora: An Introduction to Microbes Inhabiting the Human Body. London: Chapman & Hall.Google Scholar
ten Have, R. and Teunissen, P. J. M. 2001. Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem. Rev 101:3397–3413.CrossRefGoogle ScholarPubMed
Thorn, R. G. 1997. The fungi in soil. Pages 63–108 in van Elsas, J. D., Trevors, J. T., and Wellington, E. M. H. (eds.), Modern Soil Microbiology. New York: Marcel Dekker.Google Scholar
Tiedje, J. M., Cho, J. C., Murray, A., Treves, D., Xia, B., and Zhou, J. 2001. Soil teeming with life: new frontiers for soil science. Pages 393–412 in Rees, R. M., Ball, B. C., Watson, C. A., and Campbell, C. D. (eds.), Sustainable Management of Soil Organic Matter. New York: Oxford University Press.Google Scholar
Torsvik, V., Goksøyr, J., and Daae, F. L. 1990. High diversity in DNA of soil bacteria. Appl. Environ. Microbiol 56:782–787.Google Scholar
Torsvik, V. and Øvreås, L. 2002. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol 5:240–245.Google Scholar
van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., and Sanders, I. R. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.Google Scholar
van der Meer, J. R., de Vos, W. M., Harayama, S., and Zehnder, A. J. B. 1992. Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol. Rev 56:677–694.Google Scholar
van Elsas, J. D., Duarte, G. F., Keijzer-Wolters, A., and Smit, E. 2000. Analysis of the dynamics of fungal communities in soil via fungal-specific PCR of soil DNA followed by denaturing gradient gel electrophoresis. J. Microbiol. Methods 43:133–151.Google Scholar
van Elsas, J. D., Trevors, J. T., and Wellington, E. M. H. (eds.). 1997. Modern Soil Microbiology. New York: Marcel Dekker.Google Scholar
von Wintzingerode, F., Goebel, U. B., and Stackebrandt, E. 1997. Determination of microbial diversity in environmental samples—pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev 21:213–229.CrossRefGoogle ScholarPubMed
Waksman, S. A. 1927. Principles of soil microbiology. Baltimore: Williams and Wilkins.Google Scholar
Ward, D. M., Weller, R., and Bateson, M. M. 1990. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65.Google Scholar
Westerman, P. R., Liebman, M., Heggenstaller, A. H., and Forcella, F. 2006. Integrating measurements of seed availability and removal to estimate weed seed losses due to predation. Weed Sci 54:566–574.Google Scholar
Woese, C. R. 1987. Bacterial evolution. Microbiol. Rev 51:221–271.Google Scholar
Ye, R. W., Wang, T., Bedzyk, L., and Croker, K. M. 2001. Applications of DNA microarrays in microbial systems. J. Microbiol. Methods 47:257–272.Google Scholar
Zhou, J., Xia, B., Treves, D. S., Wu, L-Y., Marsh, T. L., O'Neill, R. V., Palumbo, A. V., and Tiedje, J. M. 2002. Spatial and resource factors influencing high microbial diversity in soil. Appl. Environ. Microbiol 68:326–334.Google Scholar