Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants
- *Center for Ecology and Evolutionary Biology, University of Oregon, 335 Pacific Hall, Eugene, OR 97403;
- †Center for Bioenvironmental Research, Environmental Endocrinology Laboratory, Tulane University, 1430 Tulane Avenue, New Orleans, LA 70112-2699;
- ‡Department of Biology, University of Louisville, Louisville, KY 40292;
- §University of Colorado, Boulder, CO 80309; and
- ¶Department of Medicine and Surgery, Hematology and Medical Oncology Section, Tulane University Medical School, 1430 Tulane Avenue, New Orleans, LA 70112-2699
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Edited by Christopher B. Field, Carnegie Institution of Washington, Stanford, CA, and approved May 8, 2007 (received for review January 8, 2007)
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Fig. 1.Pesticides inhibit recruitment of bacteria to host plant, delay nodulation, and reduce nitrogenase activity. Alfalfa seeds were inoculated with S. meliloti and treated with various environmental chemicals (at 5 × 10−6 M) at day 0. Alfalfa was harvested at 2, 4, and 6 weeks after inoculation, and the following were assayed: (A) The number of root nodules per plant was determined for each treatment group. At 2 weeks after inoculation, no nodules were present; (0) indicates no nodules present at weeks 4 and 6 for these treatment groups. At 4 and 6 weeks after inoculation, all treatment groups had significantly fewer nodules (as indicated by ∗) compared with the +Rhiz-positive control. (B) Nitrogenase activity was measured by using an acetylene reduction assay (32, 33). Five replicates per treatment per time point were assayed, and average nanomolar ethylene produced per minute per plant was calculated for each treatment group. At 3, 4, and 5 weeks after inoculation, nitrogenase activity was significantly reduced in all treatment groups (as indicated by ∗) compared with the +Rhiz-positive control. At 6 weeks after inoculation, nitrogenase activity of bisphenol A and pentachlorohenol treatment groups was significantly reduced (as indicated by #) compared with the +Rhiz-positive control. All results shown are mean values ± SEM for a minimum of three independent experiments. A one-way ANOVA with a Bonferroni correction for multiple tests was used to compare parameters of treatment groups (significant if P < 0.05).
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Fig. 2.Pesticide treatment reduces plant yield. (A) Plant yield was measured as dry weight in milligrams of plants (roots and shoots) for five replicates per treatment per time point, with initial weight of seeds subtracted. At 2 weeks after inoculation, plant yields of the uninoculated negative control (−Rhiz) and pentachlorophenol treatment groups were significantly reduced compared with all other treatment groups and the +Rhiz-positive control. Plant yields were significantly reduced for all treatment groups compared with the +Rhiz-positive control at 4 weeks after inoculation. At 6 weeks after inoculation, plant yields of all treatment groups, except chrysin, were significantly reduced compared with the +Rhiz-positive control. (B) Pentachlorophenol treatment significantly reduced plant yield, both when plants were inoculated with S. melioti or left uninoculated, as compared with the +Rhiz-positive control. At all time points measured, plant yield of both pentachlorophenol treatment groups was statistically equivalent to the −Rhiz-negative control group, which was not inoculated with S. melioti. Plant yields of pentachlorophenol treatment groups and −Rhiz-negative control group were significantly less than +Rhiz-positive control at all time points measured. Treatment groups pictured are (from left to right) alfalfa inoculated with S. melioti and treated with pentachlorophenol, alfalfa that were not inoculated with S. melioti but were treated with pentachlorophenol, alfalfa inoculated with S. melioti and not treated with any chemicals (+Rhiz-positive control), and alfalfa that were not inoculated with S. melioti and not treated with any chemicals (−Rhiz-negative control). All plant biomass values are presented in Table 1.
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Fig. 3.Model of pesticide inhibition of symbiotic recruitment resulting in reduced harvest yields. Pesticides and environmental chemicals delay recruitment of S. melioti to host plants by 4–6 weeks after treatment. Alfalfa is harvested approximately every 30 days, which yields an average of three harvests per growing season (45). The environmental chemicals methyl parathion, DDT, bisphenol A, and pentachlorophenol inhibited symbiotic recruitment and delayed nodulation, resulting in suboptimal N fixation and reduced plant yields for 4–6 weeks after treatment. The resulting reduction in number of plants and/or prolonged time until plant yield maxima is reached may prolong time until harvest, resulting in fewer total harvests per season; a 4- to 6-week delay would result in an estimated loss of one harvest per season and a one-third reduction in overall alfalfa crop yield. The solid line indicates alfalfa treated with noninhibitory pesticides and/or not exposed to inhibitory environmental chemicals. The dashed red line indicates alfalfa treated with pesticides and/or exposed to inhibitory environmental chemicals that disrupt or delay symbiotic recruitment (i.e., methyl parathion, DDT, bisphenol A, pentachlorophenol, etc.).
Footnotes
- ‖To whom correspondence should be addressed. E-mail: john.mclachlan{at}tulane.edu
- © 2007 by The National Academy of Sciences of the USA
