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BIOLOGICAL SCIENCES / SUSTAINABILITY SCIENCE
Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants

Jennifer E. Fox^*,, Jay Gulledge, Erika Engelhaupt, Matthew E. Burow^,¶, and John A. McLachlan^,||

*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

Edited by Christopher B. Field, Carnegie Institution of Washington, Stanford, CA, and approved May 8, 2007 (received for review January 8, 2007)

Unprecedented agricultural intensification and increased crop yield will be necessary to feed the burgeoning world population, whose global food demand is projected to double in the next 50 years. Although grain production has doubled in the past four decades, largely because of the widespread use of synthetic nitrogenous fertilizers, pesticides, and irrigation promoted by the "Green Revolution," this rate of increased agricultural output is unsustainable because of declining crop yields and environmental impacts of modern agricultural practices. The last 20 years have seen diminishing returns in crop yield in response to increased application of fertilizers, which cannot be completely explained by current ecological models. A common strategy to reduce dependence on nitrogenous fertilizers is the production of leguminous crops, which fix atmospheric nitrogen via symbiosis with nitrogen-fixing rhizobia bacteria, in rotation with nonleguminous crops. Here we show previously undescribed in vivo evidence that a subset of organochlorine pesticides, agrichemicals, and environmental contaminants induces a symbiotic phenotype of inhibited or delayed recruitment of rhizobia bacteria to host plant roots, fewer root nodules produced, lower rates of nitrogenase activity, and a reduction in overall plant yield at time of harvest. The environmental consequences of synthetic chemicals compromising symbiotic nitrogen fixation are increased dependence on synthetic nitrogenous fertilizer, reduced soil fertility, and unsustainable long-term crop yields.

legume | nitrogen fixation | symbiosis | Sinorhizobium meliloti

Author contributions: J.E.F. and J.A.M. designed research; J.E.F. performed research; J.E.F. and M.E.B. contributed new reagents/analytic tools; J.E.F., J.G., E.E., M.E.B., and J.A.M. analyzed data; and J.E.F. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

^||To whom correspondence should be addressed. E-mail: john.mclachlan{at}tulane.edu

© 2007 by The National Academy of Sciences of the USA

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