Abstract
The release of chemical compounds from plant roots that suppress soil nitrification is termed biological nitrification inhibition (BNI). Determining the environmental factors that control the synthesis and release of BNI-compounds from Brachiaria humidicola (Rendle) Schweick, a tropical pasture grass that thrives on acid soils, is the focus of this investigation. Because the BNI trait is related to the N status of the plant, we investigated the possibility that the expression of this trait would be related to the forms of N found in the root environment. Plants were grown with two sources of N, NH +4 or NO −3 for 60 days and the release of BNI-compounds monitored. Only plants grown with NH +4 released BNI-compounds from roots. The presence of NH +4 and possibly the secondary effect of its uptake (i.e., acidic pH) in the root environment significantly enhanced the release of BNI-compounds. Both the NH +4 and NO −3 grown plants responded to the stimulus from NH +4 in the root environment. BNI-compounds found in root tissue and their release were nearly three times greater in NH +4 grown than from NO −3 grown plants. The BNI-compounds released from roots composed of at least three active components—Type-I (stable to pH changes from 3.0 to 10), Type-II (temporarily loses its inhibitory effect at a pH higher than a threshold pH of 4.5 and the inhibitory effect is reestablished when the root exudate pH is adjusted to <4.5) and Type-III (inhibitory effect is irreversibly lost if the pH of the root exudate reaches 10.0 or above). A major portion of BNI-compounds released in the presence of NH +4 is of Type-I. In the absence of NH +4 , mostly Type-II and Type-III BNI-compounds were released. The BNI-compounds inhibited the function of Nitrosomonas europaea through the blocking of both ammonia monooxygenase and hydroxylamino oxidoreductase pathways. These results indicate that the release of BNI-compounds from B. humidicola roots is a regulated function and that presence of NH +4 in the root environment is necessary for the sustained synthesis and release of BNI.
This is a preview of subscription content, access via your institution.
References
Belser LW, Schmidt EL (1981) Inhibiting effect of nitrapyrin on three genera of ammonia oxidizing nitrifiers. Appl Environ Microbiol 41:819–821
Dijkshoorn W (1973) Organic acids, and their role in ion uptake. In: Butler GW, Bailey RW (eds) Chemistry and biochemistry of herbage. Academic, London, pp 163–188
Giles J (2005) Nitrogen study fertilizes fears of pollution. Nature 433:791
Glass ADM (2003) Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Crit Rev Plant Sci 22:453–470
Iizumi T, Nakamura K (1997) Cloning, nucleotide sequence, and regulatory analysis of the Nitrosomonas europaea dnaK gene. Appl Environ Microbiol 63:1777–1784
Iizumi T, Mizumoto M, Nakamura K (1998) A bioluminescence assay using Nitrosomonas europaea for rapid and sensitive detection of nitrification inhibitors. Appl Environ Microbiol 64:3656–3662
Ishikawa T, Subbarao GV, Ito O, Okada K (2003) Suppression of nitrification and nitrous oxide emission by the tropical grass Brachiaria humidicola. Plant Soil 255:413–419
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529
Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11:707–726
Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L (2004) Grass population control nitrification in Savanna soils. Funct Ecol 13:762–763
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Marschner H, Haussling M, George E (1991) Ammonium and nitrate uptake rates and rhizosphere-pH in non-mycorrhizal roots of Norway spruce (Picea abies (L.) Karst.). Trees 5:14–21
McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29:1–9
Miles JW, do Valle WCB, Rao IM, Euclides VPB (2004) Brachiaria grasses. In: Sollenberger LE, Moser L, Burson B (eds) Warm-season grasses. ASA/CSSA/SSSA, Madison, pp 745–783
Norton JM, Alzerreca JJ, Suwa Y, Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch Microbiol 177:139–149
Palmgren MG, Harper JF (1999) Pumping with plant P-type ATPase. J Exp Bot 50:883–893
Prasad R, Power JF (1995) Nitrification inhibitors for agriculture, health, and the environment. Adv Agron 54:233–281
Rao IM, Zeigler RS, Vera RR, Sarkarung S (1993) Selection and breeding for acid-soil tolerance in crops: upland rice and tropical forages as case studies. Bioscience 43:454–465
Rao IM, Kerridge PC, Macedo M (1996) Adaptation to low fertility acid soils and nutritional requirements of Brachiaria. In: Miles JW, Maass BL, do Valle CB (eds) The biology, agronomy and improvement of Brachiaria. CIAT, Cali, Colombia, pp 53–71
Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363
Raven JA (1986) Biochemical disposal of excess H+ in growing plants. New Phytol 104:175–206
Rice CW, Pancholy SK (1972) Inhibition of nitrification by climax ecosystem. Am J Bot 59:1033–1040
Robinson JB (1963) Nitrification in a New Zealand grassland soil. Plant Soil 14:173–183
Salsac L, Haillou S, Morot-Gaudry J, Lesaint C (1987) Nitrate and ammonium nutrition in plants. Plant Physiol Biochem 25:805–812
Subbarao GV, Ito O, Sahrawat KL, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006a) Scope and strategies for regulation of nitrification in agricultural systems—challenges and opportunities. Crit Rev Plant Sci 25:303–335
Subbarao GV, Ishikawa T, Ito O, Nakahara K, Wang HY, Berry WL (2006b) A bioluminescence assay to detect nitrification inhibitors released from plant roots—a case study with Brachiaria humidicola. Plant Soil. http://www.springerlink.com/content/r435654g2r514044
Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell 11:677–689
Takaki H, Ikeda M, Yamada Y, Harada T (1968) Occurrence of glucosamine in higher plants. Soil Sci Plant Nutr (Japan) 14:56–61
Vannelli T, Hooper AB (1992) Oxidation of nitrapyrin to 6-chloropicolinic acid by the ammonia-oxidizing bacterium Nitrosomonas europaea. Appl Environ Microbiol 58:2321–2325
Woldendorp JW, Laanbroek HJ (1989) Activity of nitrifiers in relation to nitrogen nutrition of plants in natural ecosystems. Plant Soil 115:217–228
Yan F, Feuerle R, Schaffer S, Fortmeier H, Schubert S (1998) Adaptation of active proton pumping and plasmalemma ATPase activity of corn roots to low root medium pH. Plant Physiol 117:311–319
Acknowledgements
We are grateful to Dr Taro Iizumi (Kurita Water Industries Limited, Wakamtya, Japan) who has kindly provided us with the luminescent recombinant N. europaea strain for this research. We acknowledge the participation and help from our colleagues at CIAT (Cali, Colombia) during this study have also provided the seed material used for various experiments described in this manuscript. We are thankful to Dr Yiyong Zhu (Nanjing Agricultural University, Nanjing, China) for many thoughtful suggestions and inputs during the interpretation of the data. Also, we are grateful to Dr K.L. Sahrawat (ICRISAT, India), who has gone through our manuscript critically and offered many suggestions to improve the clarity of our presentation and interpretation of the data.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Subbarao, G.V., Wang, H.Y., Ito, O. et al. NH +4 triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant Soil 290, 245–257 (2007). https://doi.org/10.1007/s11104-006-9156-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-006-9156-6