Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota

Abstract

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.

A plant perspective on nitrogen cycling in the rhizosphere

“…In boreal forests, this N 2 fixation by cyanobacteria living in symbiosis with mosses can account to up to 50% of total biological N input (DeLuca, Zackrisson, Nilsson, & Sellstedt, ; Santi et al, ; Warshan et al, ). In N‐depleted soils in Mexico, recent work has shown that the mucilage of aerial roots of an indigenous landrace of maize enriched in diazotrophs (Van Deynze et al, ) (Figure ). This mucilage, rich in arabinose, fucose and galactose, can support N 2 ‐fixing activity by the diazotrophs.…”

Sticky mucilages and exudates of plants: putative microenvironmental design elements with biotechnological value

“…The AGP nanoparticles are highly uniform and evenly spread over the attachment area (Lenaghan & Zhang, 2012). Whether Extrafloral nectars secreted by stems, leaves or aerial roots to provide protection and nutrition Many land plant species secrete mucilage through their stems as extrafloral nectar (Deynze et al, 2018;Pierce, 2019). Whether Extrafloral nectars secreted by stems, leaves or aerial roots to provide protection and nutrition Many land plant species secrete mucilage through their stems as extrafloral nectar (Deynze et al, 2018;Pierce, 2019).…”

“…The firm attachment is further supported by cellulose microfibrildependent shape changes of adventitious root hairs at the attachment interface (Melzer et al, 2010), accentuating the possibility that structural and chemical features have been finetuned together to form an attachment organ that meets the special needs of climbing plants. Despite their name, extrafloral nectars are not involved in attracting pollinators but rather entice invertebrates such as ants or wasps to protect the plants from herbivorous predators (Gaume & Forterre, 2007;Llhan et al, 2007) or to supplement their diet with nitrogen by trapping insects or cultivating microbial symbionts (Adlassnig et al, 2010;Deynze et al, 2018). Despite their name, extrafloral nectars are not involved in attracting pollinators but rather entice invertebrates such as ants or wasps to protect the plants from herbivorous predators (Gaume & Forterre, 2007;Llhan et al, 2007) or to supplement their diet with nitrogen by trapping insects or cultivating microbial symbionts (Adlassnig et al, 2010;Deynze et al, 2018).…”

“…To meet these demands, plants have developed a range of strategies, including morphological adaptations, long-distance communication via volatiles or synthesis of protective metabolites. Other types of exudates are produced by leaves or by stems and have become known as extrafloral nectars (Deynze et al, 2018;Pierce, 2019). Mucilage, defined by Sasse et al (2018) as a matrix of high-molecular-weight compounds, is secreted as a viscoelastic gel that is often polysacchariderich.…”

“…Mucilage, defined by Sasse et al (2018) as a matrix of high-molecular-weight compounds, is secreted as a viscoelastic gel that is often polysacchariderich. These functions range from attracting beneficial microbiota (Haichar et al, 2014) and insects (Deynze et al, 2018), modifying soils for enhanced nutrient and water uptake or surface anchorage for climbing (Bowling & Vaughn, 2008) to attachment to hosts before their infection (Vaughn, 2002). Depending on the plant species, exudates and mucilages can be secreted by almost any plant organ, and seemingly from all clades of the angiosperms , and in a few cases multiple exudate types with different origins have been described for the same species or genus (e.g.…”