Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota
Allen Van Deynze, Pablo Zamora, Pierre-Marc Delaux, Cristobal Heitmann, Dhileepkumar Jayaraman, Shanmugam Rajasekar, Danielle Graham, Junko Maeda, Donald Gibson, Kevin D. Schwartz, Alison M. Berry, Srijak Bhatnagar, Guillaume Jospin, Aaron Darling, Richard Jeannotte, Javier Lopez, Bart C. Weimer, Jonathan A. Eisen, Howard-Yana Shapiro, Jean-Michel Ané, Alan B. Bennett
Plants are associated with a complex microbiota that contributes to
nutrient acquisition, plant growth, and plant defense. Nitrogen-fixing
microbial associations are efficient and well characterized in legumes
but are limited in cereals, including maize. We studied an indigenous
landrace of maize grown in nitrogen-depleted soils in the Sierra Mixe
region of Oaxaca, Mexico. This landrace is characterized by the
extensive development of aerial roots that secrete a carbohydrate-rich
mucilage. Analysis of the mucilage microbiota indicated that it was
enriched in taxa for which many known species are diazotrophic, was
enriched for homologs of genes encoding nitrogenase subunits, and
harbored active nitrogenase activity as assessed by acetylene reduction
and 15N2 incorporation assays. Field experiments in Sierra Mixe using 15N natural abundance or 15N-enrichment
assessments over 5 years indicated that atmospheric nitrogen fixation
contributed 29%–82% of the nitrogen nutrition of Sierra Mixe maize.
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The aerial roots of Sierra Mixe maize secrete large quantities of
mucilage between 3 and 6 months after planting. The mucilage is
carbohydrate rich, with the composition dominated by arabinose, fucose,
and galactose.
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