Amino acids are a nitrogen source for sugarcane
Kerry Vinall A , Susanne Schmidt A , Richard Brackin A , Prakash Lakshmanan B and Nicole Robinson A C
+ Author Affiliations
- Author Affiliations
A School of Agriculture and Food Science, The University of Queensland, Brisbane, Qld 4072, Australia.
B BSES Ltd, 50 Meiers Road, Indooroopilly, Qld 4068, Australia.
C Corresponding author. Email: nicole.robinson@uq.edu.au
Functional Plant Biology 39(6) 503-511 https://doi.org/10.1071/FP12042
Submitted: 7 February 2012 Accepted: 16 April 2012 Published: 15 May 2012
Abstract
Organic forms of nitrogen (ON) represent potential N sources for crops and an alternative to inorganic N (IN, ammonium nitrate). Sugarcane soils receive organic harvest residues (~40–100 kg ON ha–1), but it is unknown whether ON is a direct N source for crops. We investigated whether sugarcane can use organic monomers in the form of amino acids and whether the use of amino acids as a N source results in distinct metabolic or morphological change when compared with use of inorganic N (IN). Plantlets cultivated in sterile culture and young plants grown in non-sterile soil culture were supplied with IN, ON (five amino acids present in sugarcane soils), or combined IN and ON. All treatments resulted in similar biomass and N content indicating that sugarcane has a well developed capacity to use ON and confirms findings in other species. ON-supplied plants in axenic culture had increased total branch root length per unit primary root axis which has not been reported previously. In both experimental systems, ON supplied plants had increased asparagine concentrations suggesting altered N metabolism. Root of ON-supplied soil-grown plants had significantly reduced nitrate concentrations. We interpret the shift from nitrate to asparagine as indicative of N form use other than or in addition to nitrate by sugarcane. N metabolite profiling could advance knowledge of crop N sources and this will aid in development of N efficient cropping systems with a reduced N pollution footprint.
Additional keywords: ammonium, nitrate, organic N, sugarcane production, sustainable.
References
Adamczyk B, Godlewski M, Zimny J, Zimny A (2008) Wheat (Triticum aestivum) seedlings secrete proteases from the roots and, after protein addition, grow well on medium without inorganic nitrogen. Plant Biology 10, 718–724.| Wheat (Triticum aestivum) seedlings secrete proteases from the roots and, after protein addition, grow well on medium without inorganic nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslajsbg%3D&md5=15304f10a2405ffa780193cf3f136e39CAS |
Bardgett R, Streeter T, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84, 1277–1287.
| Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands.Crossref | GoogleScholarGoogle Scholar |
Basanta MV, Dourado-Neto D, Reichardt K, Bacchi OOS, Oliveira JCM, Trivelin PCO, Timm LC, Tominaga TT, Correchel V, Cássaro FAM, Pires LF, de Macedo JR (2003) Management effects on nitrogen recovery in a sugarcane crop grown in Brazil. Geoderma 116, 235–248.
| Management effects on nitrogen recovery in a sugarcane crop grown in Brazil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltF2isbw%3D&md5=51b517770d256d0a4c148b8e00c62d76CAS |
Biggs IM (2003) An investigation of sugarcane nitrogen physiology: sources, uptake, and metabolism. PhD thesis, University of Queensland.
Bollard EG (1966) A comparative study of the ability of organic nitrogenous compounds to serve as sole sources of nitrogen for the growth of plants. Plant and Soil 25, 153–166.
| A comparative study of the ability of organic nitrogenous compounds to serve as sole sources of nitrogen for the growth of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXhvFCl&md5=392bf2752ca78c420e9f6dbe17044720CAS |
Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. Journal of Plant Physiology 159, 567–584.
| NH4 + toxicity in higher plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVCrtbc%3D&md5=d4570194bea534ec8f781104f0ad6abeCAS |
Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T (2011) Patterns of plant biomass partitioning depend on nitrogen source. PLoS ONE 6, e19211
| Patterns of plant biomass partitioning depend on nitrogen source.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVanu7w%3D&md5=899fc879424bd1d93fc574ad17ad22b2CAS |
Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153.
| Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhtVWisb4%3D&md5=4b1bc6c53d947c916d3bfa1160965376CAS |
Dluzniewska P, Gessler A, Kopriva S, Strnad M, Novak O, Dietrich H, Rennenberg H (2006) Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 – uptake rates in poplar. Plant, Cell & Environment 29, 1284–1297.
| Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 – uptake rates in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVGjsrw%3D&md5=7a1152ddc2c4416cc70f8cfbe96e2551CAS |
Erisman JW, Sutton MA, Galloway J, Klimont Z, Winiwarter W (2008) How a century of ammonia synthesis changed the world. Nature Geoscience 1, 636–639.
| How a century of ammonia synthesis changed the world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOlur%2FM&md5=83ba34e59cae61f1bbc3cb88fe8d8033CAS |
Forde BG, Walch-Lui P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell & Environment 32, 682–693.
| Nitrate and glutamate as environmental cues for behavioural responses in plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslemsLo%3D&md5=7ed87f0f6524e0f1ab5905b8c772750dCAS |
Forsum O, Svennerstam H, Ganeteg U, Näsholm T (2008) Capacities and constraints of amino acid utilization in Arabidopsis. New Phytologist 179, 1058–1069.
Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. The Plant Cell 11, 937–947.
Glass ADM (2003) Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Critical Reviews in Plant Sciences 22, 453–470.
Glass ADM (2009) Nitrate uptake by plant roots. Botany 87, 659–667.
| Nitrate uptake by plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVaksrjE&md5=9b1ae1753b6e8565b322b51e272404c7CAS |
Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science 9, 597–605.
| Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaksLvM&md5=7744d9a9d99f669b2f9b12d4b1392114CAS |
Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296.
| An Earth-system perspective of the global nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Cqsg%3D%3D&md5=bb4aabfa39c07e855e5159534b47f798CAS |
Hartung W, Ratcliffe RG (2002) Utilization of glycine and serine as nitrogen sources in the roots of Zea mays and Chamaegigas intrepidus. Journal of Experimental Botany 53, 2305–2314.
| Utilization of glycine and serine as nitrogen sources in the roots of Zea mays and Chamaegigas intrepidus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVKhsw%3D%3D&md5=0b9c56f5761724e4cc53ab626f84d40aCAS |
Hill PW, Quilliam RS, DeLuca TH, Farrar J, Farrell M, Roberts P, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011) Acquisition and assimilation of nitrogen as peptide-bound and d-enantiomers of amino acids by wheat. PLoS ONE 6, e19220
| Acquisition and assimilation of nitrogen as peptide-bound and d-enantiomers of amino acids by wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Klu7s%3D&md5=6124ad757d50def6838af2ec631c7797CAS |
Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. The Plant Cell 18, 1931–1946.
| Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xoslyhtb8%3D&md5=755734cfc89cbe4112a16777e26b4774CAS |
Hodge A (2006) Plastic plants and patchy soils. Journal of Experimental Botany 57, 401–411.
| Plastic plants and patchy soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKgsw%3D%3D&md5=61f069ed60a5bec6e87407dc14dea9b2CAS |
Holst J, Robinson N, Brackin R, Lakshmanan P, Schmidt S (2012) Soluble inorganic and organic nitrogen in two Australian soils under sugarcane cultivation. Agriculture Ecosystems & Environment 155, 16–26.
| Soluble inorganic and organic nitrogen in two Australian soils under sugarcane cultivation.Crossref | GoogleScholarGoogle Scholar |
Jämtgård S, Näsholm T, Huss-Danell K (2007) Occurrence of amino acids in soil and their uptake in barley. Amino Acids 33, 221–231.
Jämtgård S, Näsholm T, Huss-Danell K (2008) Characteristics of amino acid uptake in barley. Plant and Soil 302, 221–231.
| Characteristics of amino acid uptake in barley.Crossref | GoogleScholarGoogle Scholar |
Jämtgård S, Näsholm T, Huss-Danell K (2010) Nitrogen compounds in soil solutions of agricultural land. Soil Biology & Biochemistry 42, 2325–2330.
| Nitrogen compounds in soil solutions of agricultural land.Crossref | GoogleScholarGoogle Scholar |
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants − an important N uptake pathway? Soil Biology & Biochemistry 37, 413–423.
| Dissolved organic nitrogen uptake by plants − an important N uptake pathway?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGgsrnI&md5=abc5be5de91f23f61ffc8d97e8de49bcCAS |
Ju X-T, Xing G-X, Chen X-P, Zhang S-L, Zhang L-J, Liu X-J, Cui Z-L, Yin B, Christie P, Zhu Z-L, Zhang F-S (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proceedings of the National Academy of Sciences of the United States of America 106, 3041–3046.
| Reducing environmental risk by improving N management in intensive Chinese agricultural systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFyqtbY%3D&md5=60d3de5d3e9e9e3cd17200dc47dd11a9CAS |
Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383.
| Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling.Crossref | GoogleScholarGoogle Scholar |
Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Grotemeyer MS, Tegeder M, Rentsch D (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology 148, 856–869.
| AtPTR1 and AtPTR5 transport dipeptides in planta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GmtLvN&md5=fdf2f0f8990a4ecdac284349099c5bd7CAS |
Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. The Plant Journal 16, 345–353.
| Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsVOqsQ%3D%3D&md5=f6322692f84767443cc502231bf2d3beCAS |
Lea PJ, Sodek L, Parry MAJ, Shewry R, Halford NG (2007) Asparagine in plants. The Annals of Applied Biology 150, 1–26.
| Asparagine in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtF2isbk%3D&md5=ac484609258f991dbe81a49100e7f632CAS |
Liao M, Palta J, Fillery I (2006) Root characteristics of vigorous wheat improve early nitrogen uptake. Australian Journal of Agricultural Research 57, 1097–1107.
| Root characteristics of vigorous wheat improve early nitrogen uptake.Crossref | GoogleScholarGoogle Scholar |
Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128, 305–316.
| The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar |
Meier EA, Thorburn PJ, Wegener MK, Basford KE (2006) The availability of nitrogen from sugarcane trash on contrasting soils in the wet tropics of north Queensland. Nutrient Cycling in Agroecosystems 75, 101–114.
| The availability of nitrogen from sugarcane trash on contrasting soils in the wet tropics of north Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot12jsb8%3D&md5=6001d0b183481b0429779bb45cdd4278CAS |
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62–71.
| A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFemsrs%3D&md5=d86c2804574e39b7ac063511503ccf89CAS |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=653cbff4216b152d155a6572062308d2CAS |
Näsholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal forests. Physiologia Plantarum 111, 419–426.
| Plant acquisition of organic nitrogen in boreal forests.Crossref | GoogleScholarGoogle Scholar |
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182, 31–48.
| Uptake of organic nitrogen by plants.Crossref | GoogleScholarGoogle Scholar |
Ng Kee Kwong KF, Deville J, Cavalot PC, Riviere V (1987) Value of cane trash in nitrogen nutrition of sugarcane. Plant and Soil 102, 79–83.
| Value of cane trash in nitrogen nutrition of sugarcane.Crossref | GoogleScholarGoogle Scholar |
Okazaki K, Oka N, Shinano T, Osaki M, Takebe M (2008) Differences in the metabolite profiles of spinach (Spinacia oleracea L.) leaf in different concentrations of nitrate in the culture solution. Plant & Cell Physiology 49, 170–177.
| Differences in the metabolite profiles of spinach (Spinacia oleracea L.) leaf in different concentrations of nitrate in the culture solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVWlur8%3D&md5=b788bb717e123a4d6de743cc1b738f2fCAS |
Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biology & Biochemistry 33, 651–657.
| Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1aksLo%3D&md5=9c79c57f5a3e695878d1d4e6bd6d7237CAS |
Parish DH (1965) The amino-acids of sugar cane. I. The amino-acids of cane-juice and the effect of nitrogenous fertilisation on the levels of these substances. Journal of the Science of Food and Agriculture 16, 240–242.
| The amino-acids of sugar cane. I. The amino-acids of cane-juice and the effect of nitrogenous fertilisation on the levels of these substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXksFyjtrw%3D&md5=dded8760274e42e07bef10ed84500950CAS |
Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. Proceedings of the National Academy of Sciences of the United States of America 105, 4524–4529.
| Plants can use protein as a nitrogen source without assistance from other organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1Wku7g%3D&md5=a9d1a8ae45ce85c42dd2224d0948ab13CAS |
Paungfoo-Lonhienne C, Schenk PM, Lonhienne TGA, Brackin R, Meier S, Rentsch D, Schmidt S (2009) Nitrogen affects cluster root formation and expression of putative peptide transporters. Journal of Experimental Botany 60, 2665–2676.
| Nitrogen affects cluster root formation and expression of putative peptide transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlGit7w%3D&md5=90d11d7a96e31c90634bb472adb0e64bCAS |
Persson J, Gardestrom P, Näsholm T (2006) Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris. Journal of Experimental Botany 57, 2651–2659.
| Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xotl2mtL4%3D&md5=98ed75544b83f31a8f7d9f96afbe36f1CAS |
Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Letters 581, 2281–2289.
| Transporters for uptake and allocation of organic nitrogen compounds in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aiu7g%3D&md5=20995b23ed153f66ce61aba9beeee25fCAS |
Robertson FA, Thorburn PJ (2000) Trash management - consequences for soil carbon and nitrogen. Proceedings of the Australian Society of Sugar Cane Technologists 22, 225–229.
Robinson N, Brackin R, Vinall K, Soper F, Holst J, Gamage H, Paungfoo-Lonhienne C, Rennenberg H, Lakshmanan P, Schmidt S (2011) Nitrate paradigm does not hold up for sugarcane. PLoS ONE 6, e19045
| Nitrate paradigm does not hold up for sugarcane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Krsrw%3D&md5=649f6c509e76f1dad93fe8da3ae1a842CAS |
Scheible W, Lauerer M, Schulze E, Caboche M, Stitt M (1997) Accumulation of nitrate in the shoot acts as a signal to regulate shoot–root allocation in tobacco. The Plant Journal 11, 671–691.
| Accumulation of nitrate in the shoot acts as a signal to regulate shoot–root allocation in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1Clurw%3D&md5=efa80d87827c75e8896461da8a9f124dCAS |
Schmidt S, Stewart G (1999) Glycine metabolism by plant roots and its occurrence in Australian plant communities. Australian Journal of Plant Physiology 26, 253–264.
| Glycine metabolism by plant roots and its occurrence in Australian plant communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlKhtLw%3D&md5=bdb1e7334ffe44d3872bb4d99cc7f86aCAS |
Schroeder BL, Wood AW, Moody PW, Bell MJ, Garside AL (2005) Nitrogen fertiliser guidelines in perspective. Proceedings of the Australian Society of Sugar Cane Technologists 27, 291–304.
Soper FM, Paungfoo-Lonhienne C, Brackin R, Rentsch D, Schmidt S, Robinson N (2011) Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth. Functional Plant Biology 38, 788–796.
| Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFyms7fF&md5=5fc6871b215fd36f55c9fd86d1ed2769CAS |
Svennerstam H, Ganeteg U, Näsholm T (2008) Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease. New Phytologist 180, 620–630.
| Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKms7rE&md5=54517798d522983cffdcb354c4431ed7CAS |
Thornton B (2001) Uptake of glycine by non-mycorrhizal Lolium perenne. Journal of Experimental Botany 52, 1315–1322.
| Uptake of glycine by non-mycorrhizal Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVCmsL4%3D&md5=72bd5c1121f3c9fb9152cb4cb05aeeb1CAS |
Thornton B (2004) Inhibition of nitrate influx by glutamine in Lolium perenne depends upon the contribution of the HATS to the total influx. Journal of Experimental Botany 55, 761–769.
| Inhibition of nitrate influx by glutamine in Lolium perenne depends upon the contribution of the HATS to the total influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFSrtb4%3D&md5=5a646532e1b5cea9a5c14c3985325809CAS |
Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant, Cell & Environment 28, 813–821.
| Uptake and assimilation of nitrogen from solutions containing multiple N sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVaku7Y%3D&md5=5ccfcb558d23a35b494066f3602eaca4CAS |
Thornton B, Osborne SM, Paterson E, Cash P (2007) A proteomic and targeted metabolomic approach to investigate change in Lolium perenne roots when challenged with glycine. Journal of Experimental Botany 58, 1581–1590.
| A proteomic and targeted metabolomic approach to investigate change in Lolium perenne roots when challenged with glycine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeju7s%3D&md5=c973aff34986e1e2c645b302ef618aebCAS |
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418, 671–677.
| Agricultural sustainability and intensive production practices.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVyltb0%3D&md5=43ead3bac311f668051a25b33db1748bCAS |
Turnbull MH, Goodall R, Stewart GR (1995) The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook. Plant, Cell & Environment 18, 1386–1394.
| The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtFSrtbw%3D&md5=7552a2d207e69659ef4dfc68bc42f823CAS |
Walch-Liu P, Liu L-H, Remans T, Tester M, Forde BG (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant & Cell Physiology 47, 1045–1057.
| Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Warren CR, Taranto MT (2010) Temporal variation in pools of amino acids, inorganic and microbial N in a temperate grassland soil. Soil Biology & Biochemistry 42, 353–359.
| Temporal variation in pools of amino acids, inorganic and microbial N in a temperate grassland soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyrsr%2FN&md5=38c36bfefb6719a60814aafbaf0d5425CAS |
Williams RR (1993) Mineral nutrition in vitro – a mechanistic approach. Australian Journal of Botany 41, 237–251.
| Mineral nutrition in vitro – a mechanistic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmt1Gisr0%3D&md5=ef387b2c947c66ce807b6ccedeba4536CAS |
Zhang HM, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.
| An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVShtA%3D%3D&md5=a94980fe97fa4a7228721a3f06ac7ea2CAS |
Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96, 6529–6534.
| Dual pathways for regulation of root branching by nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFKktbc%3D&md5=dfeb915af6b7c85731ab55ebf2c67a53CAS |
