Abstract
Sierra Mixe maize is a geographically remote landrace variety grown on nitrogen-deficient fields in Oaxaca, Mexico that meets its nutritional requirements without synthetic fertilizer by associating with free-living diazotrophs comprising the microbiota of its aerial root mucilage. We selected nearly 500 diazotrophic (N2-fixing) bacteria isolated from Sierra Mixe maize mucilage and sequenced their genomes. Comparative genomic analysis demonstrated that isolates represented diverse genera and composed three major diazotrophic groups based on nitrogen fixation gene content. In addition to nitrogen fixation, we examined deamination of 1-amino-1-cyclopropanecarboxylic acid, biosynthesis of indole-3-acetic acid, and phosphate solubilization as alternative mechanisms of direct plant growth promotion (PGP). Genome mining showed that isolates of all diazotrophic groups possessed marker genes for multiple mechanisms of direct plant growth promotion (PGP). Implementing in vitro assays corroborated isolate genotypes by measuring each isolate’s potential to confer the targeted PGP traits and revealed phenotypic variation among isolates based on diazotrophic group assignment. Investigating the ability of mucilage diazotrophs to confer PGP by direct inoculation of clonally propagated potato plants in planta led to the identification of 16 bio-stimulant candidates. Conducting nitrogen-stress greenhouse experiments demonstrated that potato inoculation with a synthetic community of bio-stimulant candidates, as well as with its individual components, resulted in PGP phenotypes. We further demonstrated that one diazotrophic isolate conferred PGP to a conventional maize variety under nitrogen-stress in the greenhouse. These results indicate that, while many diazotrophic isolates from Sierra Mixe maize possessed genotypes and in vitro phenotypes for targeted PGP traits, a subset of these organisms promoted the growth of potato and conventional maize, potentially through the use of multiple promotion mechanisms.
Highlights
Plants are sessile organisms that interact with bacteria in their surrounding environment to alleviate abiotic and biotic stresses
Utilizing small molecules as chemical signals secreted in root exudates, plants may acquire an associated microbiome enriched for plant growth promoting bacteria (PGPB) that exhibit an array of plant growth promotion (PGP) mechanisms [1]
Querying open reading frames of mucilage diazotroph genomes for marker genes associated with forms of direct PGP alternative to biological nitrogen fixation (BNF) revealed that members of the isolate collection possessed the genetic underpinnings to confer ACC deamination, biosynthesis of Indole-3-Acetic acid (IAA), and phosphate solubilization (S1 Table in S1 File)
Summary
Plants are sessile organisms that interact with bacteria in their surrounding environment to alleviate abiotic and biotic stresses. The Sierra Mixe landrace of maize cultivated for generations on nutrient depleted fields without synthetic fertilizer was recently reported to derive 28–82% of its nitrogen from air and harbor PGPB capable of BNF (diazotrophs) within aerial root mucilage [9]. Taxonomic analysis of the mucilage bacterial isolates revealed that isolated diazotrophs were predominantly classified to proteobacterial genera that comprise plant-associated microbiomes, exhibit endophytic lifestyles, and confer mechanisms of direct PGP independent of BNF [12]. The evidence that Sierra Mixe maize thrives under cultivation in the absence of synthetic fertilizers and the characterization of confirmed diazotrophs classified to genera known to confer an array of PGP mechanisms suggests that the mucilage-derived bacterial isolates may be a useful tool to develop novel bio-stimulants for conventional maize varieties or other crops
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