Biological nitrification inhibition by weeds: wild radish, brome grass, wild oats and annual ryegrass decrease nitrification rates in their rhizospheres
Cathryn A. O’ Sullivan A B , Kelley Whisson A , Karen Treble A , Margaret M. Roper A , Shayne F. Micin A and Philip R. Ward AA CSIRO Agriculture, Private Bag 5, Wembley, WA 6913, Australia.
B Corresponding author. Email: cathryn.osullivan@csiro.au
Crop and Pasture Science 68(8) 798-804 https://doi.org/10.1071/CP17243
Submitted: 11 July 2017 Accepted: 4 September 2017 Published: 6 October 2017
Abstract
This study investigated the ability of several plant species commonly occurring as weeds in Australian cropping systems to produce root exudates that inhibit nitrification via biological nitrification inhibition (BNI). Seedlings of wild radish (Raphanus raphanistrum), great brome grass (Bromus diandrus), wild oats (Avena fatua), annual ryegrass (Lolium rigidum) and Brachiaria humidicola (BNI-positive control) were grown in hydroponics, and the impact of their root exudates on NO3– production by Nitrosomonas europaea was measured in a pure-culture assay. A pot study (soil-based assay) was then conducted to confirm the ability of the weeds to inhibit nitrification in whole soils. All of the tested weeds slowed NO3– production by N. europaea in the pure-culture assay and significantly inhibited potential nitrification rates in soil-based assays. Root exudates produced by wild radish were the most inhibitory, slowing NO3– production by the pure culture of N. europaea by 53 ± 6.1% and completely inhibiting nitrification in the soil-based assay. The other weed species all had BNI capacities comparable to that of B. humidicola and significantly higher than that previously reported for wheat cv. Janz. This study demonstrates that several commonly occurring weed species have BNI capacity. By altering the N cycle, and retaining NH4+ in the soils in which they grow, these weeds may gain a competitive advantage over species (including crops) that prefer NO3–. Increasing our understanding of how weeds compete with crops for N may open avenues for novel weed-management strategies.
Additional keywords: ammonium, nitrification, nitrification inhibitors, weed ecology.
References
Bending GD, Lincoln SD (2000) Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. Soil Biology & Biochemistry 32, 1261–1269.| Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslyhs70%3D&md5=e84e6078f4ba2f8c41f3944e482e8181CAS |
Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytologist 127, 617–633.
| Secondary metabolites in plant defence mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFOisrg%3D&md5=2dcba85916d2ed889b0c26434ed24875CAS |
Blank RR, Morgan T (2012) Mineral N in a crested wheatgrass stand: Implications for suppression of cheatgrass. Rangeland Ecology and Management 65, 101–104.
| Mineral N in a crested wheatgrass stand: Implications for suppression of cheatgrass.Crossref | GoogleScholarGoogle Scholar |
Boutsalis P, Gill GS, Preston C (2012) Incidence of herbicide resistance in rigid ryegrass (Lolium rigidum) across Southeastern Australia. Weed Technology 26, 391–398.
| Incidence of herbicide resistance in rigid ryegrass (Lolium rigidum) across Southeastern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlOnur3L&md5=76cc8628ac7ae84dd43a3b80adf41840CAS |
Brown PD, Morra MJ (2009) Brassicaceae tissues as inhibitors of nitrification in soil. Journal of Agricultural and Food Chemistry 57, 7706–7711.
| Brassicaceae tissues as inhibitors of nitrification in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFakt7Y%3D&md5=bfa61132342017c18441ec23142504e4CAS |
Dietz MS, Machill S, Hoffmann HC, Schmidtke K (2013) Inhibitory effects of Plantago lanceolata L. on soil N mineralization. Plant and Soil 368, 445–458.
| Inhibitory effects of Plantago lanceolata L. on soil N mineralization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Gntr0%3D&md5=b9e245e498fbc504beba958b8153adbfCAS |
Evans RD, Rimer RL, Sperry L, Belnap J (2001) Exotic plant invasion alters N dynamics in an arid grassland. Ecological Applications 11, 1301–1310.
| Exotic plant invasion alters N dynamics in an arid grassland.Crossref | GoogleScholarGoogle Scholar |
Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Advances in Microbial Ecology 1, 134–214.
Gopalakrishnan S, Subbarao GV, Nakahara K, Yoshihashi T, Ito O, Maeda I, Ono H, Yoshida M (2007) Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. Journal of Agricultural and Food Chemistry 55, 1385–1388.
| Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Okuw%3D%3D&md5=2ef30f5f0e42aa293c5ac0bce1fde32cCAS |
Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In ‘Methods of soil analysis Part 2: Microbiological and biochemical properties’. Soil Science Society of America Book Series. (Eds RW Weaver, JS Angle, BS Bottomley) (Soil Science Society of America: Madison, WI, USA)
Hashem A, Borger C, Michael P, Peltzer S (2011) Management of emerging weeds within Western Australian wheat belt. In ‘Proceedings 23rd Asian-Pacific Weed Science Society Conference’. Cairns, Qld. (Asian-Pacific Weed Science Society)
Hollister EB, Hu P, Wang ASM, Hons FM, Gentry TJ (2013) Differential impacts of brassicaceous and nonbrassicaceous oilseed meals on soil bacterial and fungal communities. FEMS Microbiology Ecology 83, 632–641.
| Differential impacts of brassicaceous and nonbrassicaceous oilseed meals on soil bacterial and fungal communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1Smt7Y%3D&md5=86a59f6165257f7843e67467fff6c51dCAS |
Iannucci A, Fragasso M, Platani C, Papa R (2013) Plant growth and phenolic compounds in the rhizosphere soil of wild oat (Avena fatua L.). Frontiers in Plant Science 4, art. 509
| Plant growth and phenolic compounds in the rhizosphere soil of wild oat (Avena fatua L.).Crossref | GoogleScholarGoogle Scholar |
Ishikawa T, Subbarao GV, Okada K, Nakamura T, Ito O (2004) Inhibition of nitrification in Brachiaria humidicola. Working Report 36. Japan International Research Centre for Agricultural Sciences, Tsukuba, Japan.
Jones RE, Vere DT, Alemseged Y, Medd RW (2005) Estimating the economic cost of weeds in Australian annual winter crops. Agricultural Economics 32, 253–265.
| Estimating the economic cost of weeds in Australian annual winter crops.Crossref | GoogleScholarGoogle Scholar |
Karwat H, Moreta D, Arango J, Vergara D, Pardo P, Herrera Y, Núñez J, Arevalo A, Sotelo Cabrera ME, Rao I, Rincón A, Rasche F, Cadisch G (2015) Biological nitrification inhibition (BNI) in tropical pasture and its influence on the recovery of applied N fertiliser by subsequent maize crop in the Llanos of Colombia. In ‘Management of land use systems for enhanced food security: conflicts, controversies and resolutions. Tropentag 2015’. 16–18 September 2015, Berlin. (DITSL: Witzenhausen, Germany)
Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L (2004) Grass populations control nitrification in savanna soils. Functional Ecology 18, 605–611.
| Grass populations control nitrification in savanna soils.Crossref | GoogleScholarGoogle Scholar |
Li WH, Zhang CB, Peng CL (2012) Responses of soil microbial community structure and potential mineralization processes to Solidago canadensis invasion. Soil Science 177, 433–442.
| Responses of soil microbial community structure and potential mineralization processes to Solidago canadensis invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xps1Ggurw%3D&md5=cdb3c0ab550183545f3ef16ad225e69cCAS |
Michael PJ, Owen MJ, Powles SB (2010) Herbicide-resistant weed seeds contaminate grain sown in the Western Australian grainbelt. In ‘Proceedings 17th Australasian Weeds Conference’. Christchurch, New Zealand. (Council of Australasian Weed Societies)
Moreta D,E, Arango J, Sotelo M, Vergara D, Rincon A, Ishitani M, Castro A, Miles J, Peters M, Tohme J, Subbarao GV, Rao IM (2014) Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel strategy to improve eco-efficiency of crop–livestock systems and to mitigate climate change. Tropical Grasslands—Forrajes Tropicales 2, 88–91.
| Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel strategy to improve eco-efficiency of crop–livestock systems and to mitigate climate change.Crossref | GoogleScholarGoogle Scholar |
O’Sullivan CA, Fillery IRP, Roper MM, Richards RA (2016) Identification of several wheat landraces with biological nitrification inhibition capacity. Plant and Soil 404, 61–74.
| Identification of several wheat landraces with biological nitrification inhibition capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisV2lsLw%3D&md5=b739b94a06e29481ba569508ac2da653CAS |
O’Sullivan CA, Duncan EG, Whisson K, Treble K, Ward PR, Roper MM (2017) A colourimetric microplate assay for simple, high-throughput assessment of synthetic and biological nitrification inhibitors. Plant and Soil 413, 275–287.
| A colourimetric microplate assay for simple, high-throughput assessment of synthetic and biological nitrification inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVShsr7L&md5=bf0f8d0822b8de2653c9e2a55b6c1e0bCAS |
Rossiter-Rachor NA, Setterfield SA, Douglas MM, Hutley LB, Cook GD, Schmidt S (2009) Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of N relations in Australian savanna. Ecological Applications 19, 1546–1560.
| Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of N relations in Australian savanna.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnjvVSgsA%3D%3D&md5=c8453d3195926d7864e9da9280899cb1CAS |
Sinden J, Jones R, Hester S, Odom D, Kalisch C, James R, Cacho O (2004) The economic impact of weeds in Australia. Technical Report Series 8. CRC for Australia Weed Management, Adelaide, S. Aust.
Siqueira JO, Nair MG, Hammerschmidt R, Safir GR (1991) Significance of phenolic compounds in plant soil microbial systems. Critical Reviews in Plant Sciences 10, 63–121.
| Significance of phenolic compounds in plant soil microbial systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmtVehsrk%3D&md5=08bc7228ccb0b75040ca75d74e05b280CAS |
Snyder AJ, Johnson-Maynard JL, Morra MJ (2010) N mineralization in soil incubated with N-15-labeled Brassicaceae seed meals. Applied Soil Ecology 46, 73–80.
| N mineralization in soil incubated with N-15-labeled Brassicaceae seed meals.Crossref | GoogleScholarGoogle Scholar |
Subbarao GV, Ishikawa T, Nakahara K, Ito O, Rondon M, Rao IM, Lascano C (2006) Characterization of biological nitrification inhibition (BNI) capacity in Brachiaria humidicola. Working Report 51. Japan International Research Centre for Agricultural Sciences, Tsukuba, Japan.
Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, Lascano C, Berry WL (2007) Biological nitrification inhibition (BNI) – is it a widespread phenomenon? Plant and Soil 294, 5–18.
| Biological nitrification inhibition (BNI) – is it a widespread phenomenon?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaqsr8%3D&md5=be8b9c217e58d663587018dde50753aeCAS |
Subbarao GV, Nakahara K, Ishikawa T, Yoshihashi T, Ito O, Ono H, Ohnishi-Kameyama M, Yoshida M, Kawano N, Berry WL (2008) Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as inhibitors of nitrification. Plant and Soil 313, 89–99.
| Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as inhibitors of nitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyjsLbP&md5=b22d5e3576da799eea4774a896ad8bc6CAS |
Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of the National Academy of Sciences of the United States of America 106, 17302–17307.
| Evidence for biological nitrification inhibition in Brachiaria pastures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WktrjE&md5=950eab97cb1f25c49237c7a9aabb2688CAS |
Tanaka JP, Nardi P, Wissuwa M (2010) Nitrification inhibition activity, a novel trait in root exudates of rice. Annals of Botany Plants 2010, plq014
Teyker RH, Hoelzer HD, Liebl RA (1991) Maize and pigweed response to N supply and form. Plant and Soil 135, 287–292.
| Maize and pigweed response to N supply and form.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltlGjsLY%3D&md5=40d998711ac8a74ee62c46f5c52152f7CAS |
Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites. International Journal of Plant Sciences 164, S93–S102.
| The evolution of function in plant secondary metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt12is74%3D&md5=f0673d20721cea56015c43eb19e68addCAS |
Ward BB, Courtney KJ, Langenheim JH (1997) Inhibition of Nitrosomonas europaea by monoterpenes from coastal redwood (Sequoia sempervirens) in whole-cell studies. Journal of Chemical Ecology 23, 2583–2598.
| Inhibition of Nitrosomonas europaea by monoterpenes from coastal redwood (Sequoia sempervirens) in whole-cell studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnslGktb4%3D&md5=74a683b3ead515eb0739d5e6f23a1b69CAS |
Wheatley R, Ritz K, Griffiths B (1990) Microbial biomass and mineral N transformations in soil planted with barley, ryegrass, pea or turnip. Plant and Soil 127, 157–167.
| Microbial biomass and mineral N transformations in soil planted with barley, ryegrass, pea or turnip.Crossref | GoogleScholarGoogle Scholar |
White CS (1994) Monoterpenes—their effects on ecosystem nutrient cycling. Journal of Chemical Ecology 20, 1381–1406.
| Monoterpenes—their effects on ecosystem nutrient cycling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksFKntrs%3D&md5=eafc049b0377fd9c3b7784ff26f18718CAS |
Zakir H, Subbarao GV, Pearse SJ, Gopalakrishnan S, Ito O, Ishikawa T, Kawano N, Nakahara K, Yoshihashi T, Ono H, Yoshida M (2008) Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl) propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor). New Phytologist 180, 442–451.
| Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl) propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlKru73P&md5=0b0b051a19a76a3c774553a78088ab85CAS |