Ecology, Evolution and Behavior, Plant Biological Sciences
Research Interests
Evolution of mutualism (especially legumes and rhizobia); implications of past and ongoing evolution for agriculture.
Statement
How does evolution based on "selfish genes" maintain cooperation? We are trying to answer this question for rhizobia, symbiotic bacteria that infect legume plants like alfalfa or soybean and (to varying extents) supply them with nitrogen. Fixing nitrogen is costly for rhizobia, so why haven't rhizobia that supply their plant hosts with nitrogen (indirectly benefiting competing rhizobia infecting the same plant) been completely displaced by "ineffective" rhizobia? Why are ineffective rhizobia common enough to be a problem in some soils but not others? This research may lead to practical applications, such as legume crops that selectively enrich the soil with the most-beneficial local strains of rhizobia. This research may also be relevant to other cases where symbiosis breaks down, as in coral bleaching. As time allows, I also hope to explore other applications of modern evolutionary theory, pursuing some of the ideas in our paper on Darwinian Agriculture. To pursue my research objectives, I have often had to develop new tools, including mechanistic computer models and noninvasive scientific instruments, such as the nodule oximeter or a laser-scanner measure green leaf area index in the field.
Selected Publications
Kiers, E.T., R.A. Rousseau, and R.F. Denison. 2006. Measured sanctions: legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evolutionary Ecology Research 8:1077-1086.
R.F. Denison and E.T. Kiers. 2004. Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiology Letters 237:187-193.
Martini, E.A., J.S. Buyer, D.C. Bryant, T.K. Hartz, and R.F. Denison. 2004. Yield increases during the organic transition: improving soil quality or increasing experience? Field Crops Research 86:255-266.
Kiers, E.T., R.A. Rousseau, S.A. West, and R.F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.
Kinraide, T.B., and R.F. Denison. 2003. Strong inference, the way of science. American Biology Teacher 65:419-424.
Denison, R.F., E.T. Kiers, and S.A. West. 2003. Darwinian Agriculture: When can humans find solutions beyond the reach of natural selection? Quarterly Review of Biology 78:145-168.
Denison, R.F., C. Bledsoe, M. Kahn, F. O'Gara, E.L. Simms,and L.S. Thomashow. 2003. Cooperation in the rhizosphere and the "free rider" problem. Ecology 84:838-845.
Denison, R.F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156:567-576.
From 1993 through 2002, R. FORD DENISON taught crop ecology and conducted research at the University of California, Davis, on topics ranging from agricultural sustainability to the evolution of cooperation between microbes and plants. For most of this time, he directed "the world's youngest 100-year experiment" (LTRAS.ucdavis.edu), tracking the long-term trends that determine agricultural sustainability. His work on symbiotic nitrogen fixation, a possible alternative to nitrogen fertilizers, has led to a patent and publications in journals from Natureto Field Crops Research. One recent paper, "Darwinian Agriculture: When Can Humans Find Solutions Beyond the Reach of Natural Selection?" points out some limitations both of agricultural biotechnology and of agriculture that mimics natural ecosystems. He has been interviewed on National Public Radio, Science Update (AAAS), and DeutschlandRadio and has been an invited speaker at international meetings and at institutions from Japan's National Agricultural Research Center to the Scripps Institute of Oceanography. He was educated at Harvard, Evergreen, and Cornell, where he earned a Ph.D. in Crop Science, with postdoctoral and sabbatical research at UC Davis, UCLA, Queen's University (Ontario), Welsh Plant Breeding Station (Aberystwyth), and University of Minnesota. His research has been supported by NSF, USDA, and California's Agricultural Experiment Station. This web page was last updated May 2005, when he moved to the University of Minnesota.
Teaching
PLB 142. Ecology of Crop Systems (4) II. Denison. Lecture, 3 hours; discussion, 1 hour. Prerequisite: Agricultural Systems and Environment 2 or Biological Sciences 1C; Math 16A or Physics 1A, or consent of instructor. Ecological processes governing the structure and behavior of managed ecosystems. Emphasis on mechanistic and systems views of the physical environment, photosynthetic productivity, competition, adaptation, nutrient cycling, energy relations and contemporary issues such as climate change.
PBI 225. Methods and Instrumentation for Crop and Soil Science (3) III. Denison, Hsiao, Hartz, Mitchell, Pettygrove, Scow & van Kessel. Lecture, 1 hour; discussion, 1 hour; laboratory, 3 hours. Prerequisite: Basic knowledge of plant physiology, soil science, chemistry and physics. Theory and practice of in situ sampling and instrumentation methods for crop science and related aspects of soil science (e.g. moisture and fertility) and laboratory analysis. Not offered every year.
Featured speaker at workshop "Education for Sustainable Agriculture," California State University, Chico, March 26, 1999.
Agroecology Seminar Series (Winter 1999 and 2000) and student participatory seminars.
Research
How does evolution based on "selfish genes" maintain cooperation? We are trying to answer this question for rhizobia, symbiotic bacteria that infect legume plants like alfalfa or soybean and (to varying extents) supply them with nitrogen. Fixing nitrogen is costly for rhizobia, so why haven't rhizobia that supply their plant hosts with nitrogen (indirectly benefiting competing rhizobia infecting the same plant) been completely displaced by "ineffective" rhizobia? Why are ineffective rhizobia common enough to be a problem in some soils but not others? This research may lead to practical applications, such as legume crops that selectively enrich the soil with the most-beneficial local strains of rhizobia. This research may also be relevant to other cases where symbiosis breaks down, as in coral bleaching. As time allows, I also hope to explore other applications of modern evolutionary theory, pursuing some of the ideas in our paper on Darwinian Agriculture. Steve Kaffka has replaced me as Director of LTRAS, but I remain interested in scientific approaches to the problem of long-term sustainability, especially that of agriculture. To pursue my research objectives, I have often had to develop new tools, including mechanistic computer models and noninvasive scientific instruments, such as the nodule oximeter or a laser-scanner (at right) to measure green leaf area index in the field.
Physical changes associated with stress-induced changes in nodule oxygen permeability. 12/99-12/01. USDA/NRI.
Long-Term Sustainability of Irrigated Agriculture. 9/96-9/98. USDA/NRI.
Developing Site-Specific Farming Information for Cropping Systems in California. Calif. Fertilizer Research & Education Program.
Real-time Educational Monitoring Of The Environment (REMOTE). UC Instructional Use of Computers program.
Patent
Method and Apparatus for Measuring Oxygen Concentration and its Subsequent Use in Estimating Nitrogen Fixation in Plants. D.B. Layzell, S. Hunt, G. Palmer, R.F. Denison. #5,096,294.
Publications
E.T. Kiers, S.A. West, and R.F. Denison. 2005? Maintaining cooperation in the legume-rhizobia symbiosis: identifying selection pressures and mechanisms. In: J. Sprent and E. James (eds.) Leguminous Symbioses. Kluwer Academic Publishers (in press).
Kong, A.Y., J. Six, D.C. Bryant, R.F. Denison, and C. van Kessel. 2005. The relationship between carbon input, aggregation, and soil organic carbon stabilization in sustainable cropping systems. Soil Science Society of America Journal (in press).
R.F. Denison and E.T. Kiers. 2005. Sustainable crop nutrition: constraints and opportunities. In: M. Broadley (ed.) Plant Nutritional Genomics. Blackwell.
Denison, R.F., D.C. Bryant, and T.E. Kearney. 2004. Crop yields over the first nine years of LTRAS, a long-term comparison of field crop systems in a Mediterranean climate. Field Crops Research 86:267-277.
Martini, E.A., J.S. Buyer, D.C. Bryant, T.K. Hartz, and R.F. Denison. 2004. Yield increases during the organic transition: improving soil quality or increasing experience?Field Crops Research 86:255-266.
Okano, Y., K.R. Hristova, C. Leutenegger, L. Jackson, R.F. Denison, B. Gebreyesus, D. LeBauer, and K.M. Scow. 2004. Effects of ammonium on the population size of ammonia-oxidizing bacteria in soil -- Application of real-time PCR. Applied and Environmental Microbiology 70:1008-1016.
Kiers, E.T., R.A. Rousseau, S.A. West, and R.F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81. Widely covered in scientific and popular press.
Denison, R.F., C. Bledsoe, M. Kahn, F. O'Gara, E.L. Simms,and L.S. Thomashow. 2003. Cooperation in the rhizosphere and the "free rider" problem. Ecology 84:838-845.
Kiers, E.T., S.A. West & R.F. Denison. 2002. Mediating mutualisms: the influence of farm management practices on the evolutionary maintenance of symbiont cooperation. Journal of Applied Ecology 39:745-754.
West, S.A., E.T. Kiers, I. Pen & R.F. Denison. 2002. Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? Journal of Evolutionary Biology 15:830-837.
Hasegawa, H., D.C. Bryant, and R.F. Denison. 2000. Testing CERES model predictions of crop growth and N dynamics, in cropping systems with leguminous green manures in a Mediterranean climate. Field Crops Res. 67:239-255.
Hasegawa, H.,J.M. Labavitch, A.M. McGuire, D.C. Bryant, and R.F. Denison. 1999. Testing CERES model predictions of N release from legume cover crop residue. Field Crops Res. 63:255-267.
Plant, R.E., A. Mermer, G.S. Pettygrove, M.P. Vayssieres, J.A. Young, R.O. Miller, L.F. Jackson, R.F. Denison, and K. Phelps. 1999. Factors underlying grain yield spatial variability in three irrigated wheat fields. ASAE Transactions 42:1187-1202.
Serraj, R., V. Vadez, R.F. Denison, and T.R. Sinclair. 1999. Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol. 119:289-296.
McGuire, A.M., D.C. Bryant, and R.F. Denison. 1998. Wheat yields, nitrogen uptake, and soil moisture following winter legume cover crop vs. fallow. Agron. J. 90:404-410.
Denison, R.F. 1998. Decreased oxygen permeability: a universal stress response in legume root nodules. Bot. Acta 111:191-192.
Jacobsen, K.R., R.A. Rousseau, and R.F. Denison. 1998. Tracing the path of oxygen into birdsfoot trefoil and alfalfa nodules using iodine vapor. Bot. Acta. 111:193-203. (cover article)
Pettygrove,G.S., S.K. Upadhyaya, M.G. Pelletier, T.K. Hartz, R.E. Plant, and R.F. Denison. 1998. Tomato yield - color infrared photograph relationships. Proc. 4th Intl. Conf. Precision Agric., St. Paul, MN.
Arrese-Igor,C., A.J. Gordon, F.R. Minchin, and R.F. Denison. 1998. Nitrate entry and nitrite formation in the infected region of soybean nodules. J. Exp. Bot. 9:41-48.
Miller, R.O., G.S. Pettygrove, R.F. Denison, L. Jackson, M. Cahn, R. Plant, T. Kearney. 1998. Site specific relationships between flag leaf nitrogen, SPAD meter values and grain protein in irrigated wheat. Commun. Soil Sci. Plant Anal. 9:1381-1382.
Denison, R.F., and R. Russotti. 1997. Field estimates of green leaf area index using laser-induced chlorophyll fluorescence. Field Crops Res. 52:143-150.
Denison, R.F. 1997. Minimizing errors in LAI estimates from laser-probe inclined-point quadrats. Field Crops Res. 51:231-240.
Denison, R.F. 1997. Review of "Long-Term Experiments in Agricultural and Ecological Sciences." Field Crops Res. 54:74-75.
Shimada, S., R. Rousseau, and R.F. Denison. 1997. Wavelength options for monitoring leghemoglobin oxygenation gradients in intact legume root nodules. J. Exp. Bot. 48:1251-1258. (cover article)
Denison, R.F., R.O. Miller, D. Bryant, A. Abshahi, and W.E. Wildman. 1996. Image processing extracts more information from color infrared aerial photos.Calif. Agric. 50(3):9-13 (cover article) Denison, R.F., and B.L. Harter. 1995. Nitrate effects on nodule oxygen permeability and leghemoglobin Nodule oximetry and computer modeling.Plant Physiol. 107:1355-1364.
Denison, R.F., and T.B. Kinraide. 1995. Oxygen-induced membrane depolarizations in legume root nodules: possible evidence for an osmoelectrical mechanism controlling nodule gas permeability. Plant Physiol. 108:235-240
Denison, R.F. 1995. Agricultural soil and crop practices. McGraw-Hill Yearbook of Science and Technology, pp. 6-9.
Denison, R.F., J.F. Witty, and F.R. Minchin. 1992. Reversible O2-inhibition of nitrogenase activity in attached soybean nodules. Plant Physiol. 100:1863-1868.
Denison, R.F., S. Hunt, and D.B. Layzell. 1992. Nitrogenase activity, nodule respiration, and O2 permeability following detopping of alfalfa and birdsfoot trefoil. Plant Physiol. 98:894-900.
Denison, R.F. 1992. Mathematical modeling of oxygen diffusion and respiration in legume root nodules. Plant Physiol. 98:901-907.
Denison, R.F., andD.B. Layzell. 1991. Measurement of legume nodule respiration and O2 permeability by noninvasive spectrophotometry of leghemoglobin. Plant Physiol. 96:137-143.
Denison, R.F., D.L. Smith, T. Legros, and D.B. Layzell. 1991. Noninvasive measurement of internal oxygen concentration in field-grown soybean nodules. Agron. J. 83:166-169.
Denison, R.F., and H.D. Perry. 1990. Seasonal growth rate patterns for orchardgrass and tall fescue on the Appalachian Plateau. Agron. J. 82:869-873.
Denison, R.F., J.M. Fedders, and C.B.S. Tong. 1990. Amyloglucosidase digestion can overestimate starch content of plants. Agron. J. 82:361-364.
Denison, R.F. 1989. Implications of competitive inhibition in the acetylene reduction assay for dinitrogen fixation. Ann. Bot. 64:167-169.
Denison, R.F., and P.S. Nobel. 1988. Growth of Agave deserti without current photosynthesis. Photosynthetica 22:51-57.
Denison, R.F., P.R. Weisz, and T.R. Sinclair. 1988. Oxygen supply to nodules as a limiting factor for symbiotic nitrogen fixation. p. 767-776. In: R.J. Summerfield (ed.) World Crops: Cool Season Food Legumes. Kluwer Academic Publishers, Dordrecht.
Weisz, P.R., R.F. Denison, and T.R. Sinclair. 1985. Response to drought stress of nitrogen fixation (acetylene reduction) rates by field-grown soybeans. Plant Physiol. 78:525-530.
Sinclair, T.R., P.R. Weisz, and R.F. Denison. 1985. Oxygen limitation to nitrogen fixation in soybean nodules. p. 797-806. In: R. Shibles (ed.) Proceedings, World Soybean Conf. III. Westview Press, Boulder.
Denison, R.F., and T.R. Sinclair. 1985. Diurnal and seasonal variation in dinitrogen fixation (acetylene reduction) rates by field-grown soybeans. Agron. J. 77:679-684.
Denison, R.F., P.R. Weisz, and T.R. Sinclair. 1985. Variability among plants in dinitrogen fixation Agron. J.77:947-950.
Denison, R.F., P.R. Weisz, and T.R. Sinclair. 1983. Analysis of acetylene reduction rates of soybean nodules at low acetylene concentrations.Plant Physiol. 73:648-651.
Denison, R.F., T.R. Sinclair, R.W. Zobel, M.N. Johnson, and G.M. Drake. 1983. A nondestructive field assay for soybean nitrogen fixation by acetylene reduction. Plant Soil 70:173-182.
Denison, R.F. 1979. A 2K Symbolic Assembler for the 6502. Self-published manual recently reincarnated on the web.
Denison, R., B. Caldwell, B. Bormann, L. Eldred, C. Swanberg, and S. Anderson. 1976. The effects of acid rain on nitrogen fixation in western Washington coniferous forests. Water Air Soil Pollut. 8:21-34.
Ecology, Evolution and Behavior University of Minnesota 1987 Upper Buford Circle St. Paul, MN 55108 E-mail:First five letters of my last name + 036 + umn.edu (you know where to put the @)