Guntur V. Subbarao, Masahiro Kishii, Adrian Bozal-Leorri, Ivan Ortiz-Monasterio, Xiang Gao, Maria Itria Ibba, Hannes Karwat, M. B. Gonzalez-Moro, Carmen Gonzalez-Murua, Tadashi Yoshihashi, Satoshi Tobita, Victor Kommerell, Hans-Joachim Braun, and Masa Iwanaga

PNAS August 31, 2021 118 (35) e2106595118

Figure: Total nitrogen uptake (based on aboveground dry matter that includes grain) in wheat BNI isogenic lines (MUNAL control and BNI-MUNAL) under various nitrogen fertilizer applications in the field.

Significance

Globally, wheat farming is a major source of nitrogen pollution. Rapid generation of soil nitrates cause nitrogen leakage and damage ecosystems and human health. Here, we show the 3Ns^bS chromosome arm in wild grass (Leymus racemosus) that controls root nitrification inhibitor production can be transferred into elite wheat cultivars, without disrupting the elite agronomic features. Biological nitrification inhibition (BNI)–enabled wheats can improve soil ammonium levels by slowing down its oxidation and generate significant synergistic benefits from assimilating dual nitrogen forms and improving adaptation to low N systems. Deploying BNI-enabled wheat on a significant proportion of current global wheat area (ca. 225 M ha) could be a powerful nature-based solution for reducing N fertilizer use and nitrogen losses while maintaining productivity.

Abstract

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#3Ns^b” (Lr#n), which can be transferred to wheat as T3BL.3Ns^bS (denoted Lr#n-SA), where 3BS arm of chromosome 3B of wheat was replaced by 3Ns^bS of L. racemosus. We successfully introduced T3BL.3Ns^bS 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.3Ns^bS 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.

See: https://www.pnas.org/content/118/35/e2106595118

Figure 4: Two- to fivefold higher BNI activity is released from BNI-MUNAL (i.e., MUNAL carrying T3BL.3Ns^bS) compared to MUNAL control (BNI isogenic lines) during a 6-d monitoring period using various root exudate trap solutions (SI Appendix, Study 5b). 1) RE-NH₄-1 (1.8 L aerated solutions of 0.5 mM NH₄Cl + 200 μM CaCl₂ for 24 h—first day collection); 2) RE-nutr-NH₄-1 (1.8 L aerated solutions of one-quarter strength nutrient solution with 0.5 mM NH₄Cl for 24 h—second day collection); 3) RE-water-1 (1.8 L aerated solutions of 200 μM CaCl₂ for 24 h—third day collection); 4) RE-NH₄-2 (1.8 L aerated solutions of 1.0 mM NH₄Cl + 200 μM CaCl₂ for 24 h—fourth day collection); 5) RE-nutr-NH₄-2 (1.8 L aerated solutions of one-quarter strength nutrient solution with 1.0 mM NH₄Cl for 24 h—fifth day collection); and 6) RE-water-2 (1.8 L aerated solutions of 200 μM CaCl₂ for 24 h—sixth day collection). Values are means ± SE from four replications.