Active nitrifiers and rapid nitrification are major contributing factors to nitrogen losses in global wheat production. Suppressing nitrifier activity is an effective strategy to limit N losses from agriculture. Production and release of nitrification inhibitors from plant roots is termed “biological nitrification inhibition” (BNI). Here, we report the discovery of a chromosome region that controls BNI production in “wheat grass” Leymus racemosus (Lam.) Tzvelev, located on the short arm of the “Lr#3Nsb” (Lr#n), which can be transferred to wheat as T3BL.3NsbS (denoted Lr#n-SA), where 3BS arm of chromosome 3B of wheat was replaced by 3NsbS of L. racemosus. We successfully introduced T3BL.3NsbS into the wheat cultivar “Chinese Spring” (CS-Lr#n-SA, referred to as “BNI-CS”), which resulted in the doubling of its BNI capacity. T3BL.3NsbS from BNI-CS was then transferred to several elite high-yielding hexaploid wheat cultivars, leading to near doubling of BNI production in “BNI-MUNAL” and “BNI-ROELFS.” Laboratory incubation studies with root-zone soil from field-grown BNI-MUNAL confirmed BNI trait expression, evident from suppression of soil nitrifier activity, reduced nitrification potential, and N2O emissions. Changes in N metabolism included reductions in both leaf nitrate, nitrate reductase activity, and enhanced glutamine synthetase activity, indicating a shift toward ammonium nutrition. Nitrogen uptake from soil organic matter mineralization improved under low N conditions. Biomass production, grain yields, and N uptake were significantly higher in BNI-MUNAL across N treatments. Grain protein levels and breadmaking attributes were not negatively impacted. Wide use of BNI functions in wheat breeding may combat nitrification in high N input–intensive farming but also can improve adaptation to low N input marginal areas.
Background
Agriculture relies on the intensive use of synthetic nitrogen (N) fertilizers to maximize crop yields, which has led to the transformation of agricultural soils into high-nitrifying environments. Nevertheless, nitrification inhibitors (NIs) have been developed to suppress soil-nitrifier activity and decrease N losses. The NIs 3,4-dimethylpyrazole phosphate (DMPP) and 2-(3,4-dimethyl-1H-pyrazol-1-yl) succinic acid isomeric mixture (DMPSA) are able to reduce N2O emissions and maintain soil NH4+ for a longer time. Although both NIs have been proven to be effective to inhibit soil nitrification, their exact mode of action has not been confirmed. We aimed to provide novel insights to further understand the mode of action of DMP-based NIs. We evaluated the performance of DMPP and DMPSA in soil and pure cultures of nitrifying bacteria Nitrosomonas europaea.
Results
DMPSA did not inhibit nitrification in pure cultures of N. europaea. In the soil, we evidenced that DMPSA needs to be broken into DMP to achieve the inhibition of nitrification, which is mediated by a soil biological process that remains to be identified. Moreover, both DMPP and DMPSA are thought to inhibit nitrification due to their ability to chelate the Cu2+ cations that the ammonia monooxygenase enzyme (AMO) needs to carry on the first step of NH4+ oxidation. However, the efficiency of DMPP was not altered regardless the Cu2+ concentration in the medium. In addition, we also showed that DMPP targets AMO but not hydroxylamine oxidoreductase enzyme (HAO).
Conclusions
The inability of DMPSA to inhibit nitrification in pure cultures together with the high efficiency of DMPP to inhibit nitrification even in presence of toxic Cu2+ concentration in the medium, suggest that the mode of action of DMP-based NIs does not rely on their capacity as metal chelators.
Graphical Abstract
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