Biological nitrification inhibitor-trait enhances nitrogen uptake by suppressing nitrifier activity and improves ammonium assimilation in two elite wheat varieties

Abstract

Synthetic nitrification inhibitors (SNI) and biological nitrification inhibitors (BNI) are promising tools to limit nitrogen (N) pollution derived from agriculture. Modern wheat cultivars lack sufficient capacity to exude BNIs, but, fortunately, the chromosome region (Lr#n-SA) controlling BNI production in Leymus racemosus, a wild relative of wheat, was introduced into two elite wheat cultivars, ROELFS and MUNAL. Using BNI-isogenic-lines could become a cost-effective, farmer-friendly, and globally scalable technology that incentivizes more sustainable and environmentally friendly agronomic practices. We studied how BNI-trait improves N-uptake, and N-use, both with ammonium and nitrate fertilization, analysing representative indicators of soil nitrification inhibition, and plant metabolism. Synthesizing BNI molecules did not mean a metabolic cost since Control and BNI-isogenic-lines from ROELFS and MUNAL presented similar agronomic performance and plant development. In the soil, ROELFS-BNI and MUNAL-BNI plants decreased ammonia-oxidizing bacteria (AOB) abundance by 60% and 45% respectively, delaying ammonium oxidation without reducing the total abundance of bacteria or archaea. Interestingly, BNI-trait presented a synergistic effect with SNIs since made it also possible to decrease the AOA abundance. ROELFS-BNI and MUNAL-BNI plants showed a reduced leaf nitrate reductase (NR) activity as a consequence of lower soil NO3− formation and a higher amino acid content compared to BNI-trait lacking lines, indicating that the transfer of Lr#-SA was able to induce a higher capacity to assimilate ammonium. Moreover, the impact of the BNI-trait in wheat cultivars was also noticeable for nitrate fertilization, with improved N absorption, and therefore, reducing soil nitrate content.

Consistent prokaryotic community patterns along the radial root axis of two Zea mays L. landraces across two distinct field locations

“…Nitrification inhibition could be a trait lost in modern maize varieties bred under high nutrient supply and for use in high-input agricultural systems. For wheat ( Triticum aestivum ), it has been shown that modern varieties exude insufficient amounts of BNIs compared to wild relatives ( Subbarao et al, 2007 ) and multiple landraces ( O’Sullivan et al, 2016 ), and BNI production has been introduced into modern varieties after identification of the responsible chromosome region ( Bozal-Leorri et al, 2022 ).…”

Seed Treatment with Plant-Defense Elicitors Decreases the Abundance of Ammonia Oxidizers Associated with Winter Wheat Roots

“…Since these two plant traits reflect plant N uptake strategies (Wright and Reich, 2004;Grassein et al, 2015), our results suggest stronger competition for ammonium between wheat and root-associated ammonia oxidizers in these particular treatments, resulting in a lower genetic potential for ammonia oxidation. These observations may be explained either by high exploitative competition limiting substrate availability for ammonia oxidizers (Thion et al, 2016) or active suppression of ammonia oxidizers through the release of biological nitrification inhibitors in root exudates (Subbarao et al, 2015;Kaur-Bhambra et al, 2021;Bozal-Leorri et al, 2022), which are two possible mechanisms leading to lower nitrification activity (Subbarao et al, 2009;Cantarel et al, 2015). Competitive interference is plausible as all three elicitors are known to activate plant metabolic pathways linked to the production of BNI compounds, including phenyl propanoids, glucosinolates and benzoxazinoids (Moraes et al, 2008;Schreiner et al, 2011;Neal et al, 2012;Subbarao et al, 2013).…”

Will crops with biological nitrification inhibition capacity be favored under future atmospheric CO2?

“…Since the discovery of BNIs in the tropical grass Brachiaria humidicola and Sorghum bicolor ( Subbarao et al., 2007a ), the search for plant species displaying this trait has led to the identification of species, including cereals of high agronomical interest such as rice and maize ( Tanaka et al., 2010 ; Sun et al., 2016 ; Otaka et al., 2022 ). Wheat cultivars show weak BNI activity but, importantly, the recent development of elite wheat cultivars that harbor a chromosomal region introgressed from Leymus racemosus , a wild wheat relative with high BNI activity ( Subbarao et al., 2021 ; Bozal-Leorri et al., 2022 ), has raised further expectations regarding the potential of crops to directly control nitrification in soils.…”