Biological nitrification inhibition in maize—isolation and identification of hydrophobic inhibitors from root exudates

Abstract

To control agronomic N losses and reduce environmental pollution, biological nitrification inhibition (BNI) is a promising strategy. BNI is an ecological phenomenon by which certain plants release bioactive compounds that can suppress nitrifying soil microbes. Herein, we report on two hydrophobic BNI compounds released from maize root exudation (1 and 2), together with two BNI compounds inside maize roots (3 and 4). On the basis of a bioassay-guided fractionation method using a recombinant nitrifying bacterium Nitrosomonas europaea, 2,7-dimethoxy-1,4-naphthoquinone (1, ED50 = 2 μM) was identified for the first time from dichloromethane (DCM) wash concentrate of maize root surface and named “zeanone.” The benzoxazinoid 2-hydroxy-4,7-dimethoxy-2H-1,4-benzoxazin-3(4H)-one (HDMBOA, 2, ED50 = 13 μM) was isolated from DCM extract of maize roots, and two analogs of compound 2, 2-hydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (HMBOA, 3, ED50 = 91 μM) and HDMBOA-β-glucoside (4, ED50 = 94 μM), were isolated from methanol extract of maize roots. Their chemical structures (1–4) were determined by extensive spectroscopic methods. The contributions of these four isolated BNI compounds (1–4) to the hydrophobic BNI activity in maize roots were 19%, 20%, 2%, and 4%, respectively. A possible biosynthetic pathway for zeanone (1) is proposed. These results provide insights into the strength of hydrophobic BNI activity released from maize root systems, the chemical identities of the isolated BNIs, and their relative contribution to the BNI activity from maize root systems.

Effects of frequency and amount of stover mulching on soil nitrogen and the microbial functional guilds of the endosphere and rhizosphere

“…Nitrification and anaerobic nitrate oxidation are two microbial biochemical reactions that cause major N losses in fertilised soil ( Otaka et al, 2021 ). Mobile NO 3 − produced by nitrification may leach out of the agricultural fields, polluting groundwater and affecting human health ( Riuett et al, 2008 ; Ward et al, 2018 ).…”

“…Moreover, the anaerobic nitrate-oxidising microbes reduce NO 3 − to N 2 O or NO, two pollution and greenhouse gases that are 300 times more potent than CO 2 , which are then released from soil into the air ( Lubbers et al, 2013 ; Hu et al, 2020 ). Therefore, agricultural management should be focused on inhibiting microbial nitrification and anaerobic nitrate oxidation driven by roots ( Otaka et al, 2021 ). Conversely, nitrogen-fixing bacteria can convert N in the atmosphere into ammonia, which is conducive to crops ( Batista and Dixon, 2019 ).…”

“…Root endophytic microorganisms, as part of the root system, usually play the role of producers and have a different function from that of soil microorganisms. Nitrifying bacteria in roots always supply available NO 3 − to plants and other microorganisms, whereas those in soil mainly cause N losses ( Batista and Dixon, 2019 ; Otaka et al, 2021 ). Aerobic nitrite-oxidising bacteria in roots can help plants to obtain the essential Fe, but the same bacteria in soil can reduce NO 3 − to N 2 O, thereby causing loss of N ( Gu et al, 2020 ; Xue et al, 2020 ).…”

“…Frontiers in Microbiology frontiersin.org into the air (Lubbers et al, 2013;Hu et al, 2020). Therefore, agricultural management should be focused on inhibiting microbial nitrification and anaerobic nitrate oxidation driven by roots (Otaka et al, 2021). Conversely, nitrogen-fixing bacteria can convert N in the atmosphere into ammonia, which is conducive to crops (Batista and Dixon, 2019).…”

Rice genotypes significantly affect nitrification inhibition activity in the rhizosphere

“…Thus, there is a need to develop plant-derived biological nitri cation inhibitor (BNI). Up to now, seven BNIs in plant root exudates have been isolated and identi ed, namely brachialactone in brachiaria humidicola (Subbarao et al 2009), sorgoleno, sakuranetin and MHPP in sorghum (Subbarao et al 2012), 1,9-decanediol in rice (Oryza sativa L.) (Sun et al 2016) and zeanone and HDMBOA in maize (Otaka et al 2021). To the best of our knowledge, most of the current studies on nitri cation inhibition by plant BNI have been conducted under hydroponics, and only a few studies have focused on differences in nitri cation inhibition by plant genotypes in soil environments.…”