The source of nitrogen (NH4+ or NO3–) affects the concentration of oxalate in the shoots and the growth of Atriplex nummularia (oldman saltbush)
Hussein Al Daini A B , Hayley C. Norman C D , Paul Young C and Edward G. Barrett-Lennard B D E FA School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
C CSIRO Animal, Food and Health Sciences and Sustainable Agriculture Flagship, Private Bag 5, Wembley, WA 6913, Australia.
D Centre for Ecohydrology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
E Department of Agriculture and Food of WA, South Perth, WA 6151, Australia.
F Corresponding author. Email: egbarrettlennard@agric.wa.gov.au
Functional Plant Biology 40(10) 1057-1064 https://doi.org/10.1071/FP13060
Submitted: 19 March 2013 Accepted: 27 April 2013 Published: 3 June 2013
Abstract
Atriplex nummularia Lindl. (oldman saltbush) is a halophytic shrub used widely as a forage for ruminant production in saline farming systems. However, it can contain high concentrations of oxalate in the leaves, which may cause calcium deficiency in grazing animals. We hypothesised that supplying NH4+ instead of NO3– to a clone of this species would decrease oxalate concentrations in the shoots, and also decrease plant growth. Oxalate concentrations were measured in plants in the field, and a glasshouse experiment was conducted in which plants were grown with 10 mM NO3– or NH4+, with 50, 200 or 500 mM NaCl. The field survey showed effects of site (P < 0.001), with average oxalate concentrations in shoots varying between 2.4 and 6.4% dry mass (DM). In the glasshouse, oxalate concentrations and plant growth were both affected by N-source and salinity (P < 0.001). Averaged across salinities, plants grown with NH4+ for 24 days had only 43% of the shoot DM but 25% of the oxalate concentration of plants grown with NO3–. We discuss the effects of N-source on oxalate concentrations, the implications of this for halophyte growth, and the opportunity to select halophytes with lower oxalate and higher nutritive value for livestock.
Additional keywords: growth analysis, halophytes, nitrogen nutrition, nitrogen uptake, osmotic adjustment, salt tolerance.
References
Abu-Zanat MM, Al-Hassanat FM, Alawi M, Ruyle GB (2003) Oxalate and tannins assessment in Atriplex halimus L. and A. nummularia L. Journal of Range Management 56, 370–374.| Oxalate and tannins assessment in Atriplex halimus L. and A. nummularia L.Crossref | GoogleScholarGoogle Scholar |
Albert R, Popp M (1977) Chemical composition of halophytes from Neusiedler Lake region in Austria. Oecologia 27, 157–170.
| Chemical composition of halophytes from Neusiedler Lake region in Austria.Crossref | GoogleScholarGoogle Scholar |
Aslam M, Huffaker RC (1982) In vivo nitrate reduction in roots and shoots of barley (Hordeum vulgare L.) seedlings in light and darkness. Plant Physiology 70, 1009–1013.
| In vivo nitrate reduction in roots and shoots of barley (Hordeum vulgare L.) seedlings in light and darkness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlvFGrtb0%3D&md5=5fcb0cfa75f2aea5d75d46c6156eb024CAS | 16662604PubMed |
Aslam Z, Jeschke WD, Barrett-Lennard EG, Greenway H, Setter TL, Watkin E (1986) Effects of external NaCl on the growth of Atriplex amnicola and the ion relations and carbohydrate status of the leaves. Plant, Cell & Environment 9, 571–580.
Bazihizina N, Barrett-Lennard EG, Colmer TD (2012) Plant responses to heterogeneous salinity: shoot growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root-zone. Journal of Experimental Botany 63, 6347–6358.
| Plant responses to heterogeneous salinity: shoot growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root-zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslakt77I&md5=666acba7387be80af43c988bd0a3c4c7CAS | 23125356PubMed |
Ben Salem H, Norman HC, Nefzaoui A, Mayberry DE, Pearce KL, Revell DK, Morand-Fehr P (2010) Potential use of oldman saltbush (Atriplex nummularia Lindl.) in sheep and goat feeding. Small Ruminant Research 91, 13–28.
| Potential use of oldman saltbush (Atriplex nummularia Lindl.) in sheep and goat feeding.Crossref | GoogleScholarGoogle Scholar |
Burritt EA, Provenza FD (2000) Role of toxins in intake of varied diets by sheep. Journal of Chemical Ecology 26, 1991–2005.
| Role of toxins in intake of varied diets by sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVyhtbY%3D&md5=70e08f24d6f47e55325c3945f3e3474aCAS |
Davis AM (1981) The oxalate, tannin, crude fiber and crude protein composition of young plants of some Atriplex species. Journal of Range Management 34, 329–331.
| The oxalate, tannin, crude fiber and crude protein composition of young plants of some Atriplex species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt12gur4%3D&md5=1f0a5b75889cf8fe4940b344275c2529CAS |
Ewing K, Earle C, Piccinin B, Kershaw KA (1989) Vegetation patterns in James Bay coastal marshes. II. Physiological adaptation to salt-induced water stress in three halophytic graminoids. Canadian Journal of Botany 67, 521–528.
| Vegetation patterns in James Bay coastal marshes. II. Physiological adaptation to salt-induced water stress in three halophytic graminoids.Crossref | GoogleScholarGoogle Scholar |
Fancote CR, Norman HC, Williams IH, Masters DG (2009) Cattle performed as well as sheep when grazing a river saltbush (Atriplex amnicola)-based pasture. Animal Production Science 49, 998–1006.
| Cattle performed as well as sheep when grazing a river saltbush (Atriplex amnicola)-based pasture.Crossref | GoogleScholarGoogle Scholar |
Finlayson JS (1969) ‘Basic biochemical calculations: related procedures and principles.’ (Addison-Wesley Publishing Company: Reading, MA, USA
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=06dcabcbf1411c34a35d7aed78f04afbCAS | 18565144PubMed |
Hungerford TG (1990) ‘Diseases of livestock.’ (9th edn.) (McGraw-Hill: Sydney)
Ilarslan H, Palmer RG, Imsande J, Horner HT (1997) Quantitative determination of calcium oxalate and oxalate in developing seeds of soybean (Leguminosae). American Journal of Botany 84, 1042–1046.
| Quantitative determination of calcium oxalate and oxalate in developing seeds of soybean (Leguminosae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFejur0%3D&md5=5837a40abf5ca12fa7da4720a5ff6195CAS | 21708659PubMed |
James L, Butcher J (1972) Halogeton poisoning of sheep: effect of high level oxalate intake. Journal of Animal Science 35, 1233–1238.
Ji XM, Peng XX (2005) Oxalate accumulation as regulated by nitrogen forms and its relationship to photosynthesis in rice (Oryza sativa L.). Journal of Integrative Plant Biology 47, 831–838.
| Oxalate accumulation as regulated by nitrogen forms and its relationship to photosynthesis in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt12jsQ%3D%3D&md5=d8b70d9ac2b39bab7576ccd1edaa13ebCAS |
Joy KW (1964) Accumulation of oxalate in tissues of sugar-beet, and the effect of nitrogen supply. Annals of Botany 28, 689–701.
Kirkby EA, Knight AH (1977) Influence of the level of nitrate nutrition on ion uptake and assimilation, organic acid accumulation, and cation-anion balance in whole tomato plants. Plant Physiology 60, 349–353.
| Influence of the level of nitrate nutrition on ion uptake and assimilation, organic acid accumulation, and cation-anion balance in whole tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlvF2qt74%3D&md5=0b0f335cc8a5dbc3a4d60232395e5b0cCAS | 16660091PubMed |
Kirkby EA, Mengel K (1967) Ionic balance in different tissues of the tomato plant in relation to nitrate, urea, or ammonium nutrition. Plant Physiology 42, 6–14.
| Ionic balance in different tissues of the tomato plant in relation to nitrate, urea, or ammonium nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXnsFeksw%3D%3D&md5=c5b0d34685d32751604e8dacddce9886CAS | 16656486PubMed |
Malcolm CV (1964) An agronomic study of Kochia brevifolia. Journal of the Australian Institute of Agricultural Science 30, 272
Malcolm CV, Clarke AJ, D’Antuono MF, Swaan TC (1988) Effects of plant spacing and soil conditions on the growth of five Atriplex species. Agriculture, Ecosystems & Environment 21, 265–279.
| Effects of plant spacing and soil conditions on the growth of five Atriplex species.Crossref | GoogleScholarGoogle Scholar |
Masters D, Rintoul A, Dynes R, Pearce K, Norman H (2005) Feed intake and production in sheep fed diets high in sodium and potassium. Australian Journal of Agricultural Research 56, 427–434.
| Feed intake and production in sheep fed diets high in sodium and potassium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1ert7Y%3D&md5=644b3d5209908bfe9554781eb226e227CAS |
Masters DG, Benes S, Norman HC (2007) Biosaline agriculture for forage and livestock production. Agriculture, Ecosystems & Environment 119, 234–248.
| Biosaline agriculture for forage and livestock production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslGitg%3D%3D&md5=83f4c49017110a67764a3a09bef5d9f4CAS |
Mayberry D, Masters DG, Vercoe P (2010) Mineral metabolism of sheep fed saltbush or a formulated high-salt diet. Small Ruminant Research 91, 81–86.
| Mineral metabolism of sheep fed saltbush or a formulated high-salt diet.Crossref | GoogleScholarGoogle Scholar |
McDonald P, Edwards RA, Greenhalgh JFD, Morgan CA (2002) ‘Animal nutrition.’ (6th edn.) (Pearson Education Ltd: Essex, UK)
McQuaker NR, Brown DF, Klucker PD (1979) Digestion of environmental materials for analysis by inductively coupled plasma-atomic emission spectrometry. Analytical Chemistry 51, 1082–1084.
| Digestion of environmental materials for analysis by inductively coupled plasma-atomic emission spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXitFCls74%3D&md5=d8210b1922cbb5807ee647ea4a7f5112CAS |
Norman HC, Wilmot MG, Thomas D, Barrett-Lennard EG, Masters DG (2010) Sheep production, plant growth and nutritive value of a saltbush-based pasture system subject to rotational grazing or set stocking. Small Ruminant Research 91, 103–109.
| Sheep production, plant growth and nutritive value of a saltbush-based pasture system subject to rotational grazing or set stocking.Crossref | GoogleScholarGoogle Scholar |
Norman HC, Masters DG, Barrett-Lennard EG (2013) Halophytes as forages in saline landscapes: interactions between plant genotype and environment change their feeding value to ruminants. Environmental and Experimental Botany
Richardson SG, McKell CM (1981) Growth response of two saltbush species to nitrate, ammonium, and urea nitrogen added to processed oil shale. Journal of Range Management 34, 424–425.
| Growth response of two saltbush species to nitrate, ammonium, and urea nitrogen added to processed oil shale.Crossref | GoogleScholarGoogle Scholar |
Storey R, Wyn Jones RG (1979) Responses of Atriplex spongiosa and Suaeda monoica to salinity. Plant Physiology 63, 156–162.
| Responses of Atriplex spongiosa and Suaeda monoica to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtlGisrc%3D&md5=45dd40e250b39a395e35ef96a26ab7bbCAS | 16660671PubMed |
Weston RL (1964) Nitrogen nutrition in Atriplex hastata L. Plant and Soil 20, 251–259.
| Nitrogen nutrition in Atriplex hastata L.Crossref | GoogleScholarGoogle Scholar |
Wilson AD (1966) The value of Atriplex (saltbush) and Kochia (bluebush) species as food for sheep. Australian Journal of Agricultural Research 17, 147–153.
| The value of Atriplex (saltbush) and Kochia (bluebush) species as food for sheep.Crossref | GoogleScholarGoogle Scholar |
Zall DM, Fisher D, Garner MQ (1956) Photometric determination of chlorides in water. Analytical Chemistry 28, 1665–1668.
| Photometric determination of chlorides in water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2sXhsVelsw%3D%3D&md5=5ab15d72a707db6aebb84fe220814792CAS |
Zhang Y, Lin X, Zhang Y, Zheng SJ, Du S (2005) Effects of nitrogen levels and nitrate/ammonium ratios on oxalate concentrations of different forms in edible parts of spinach. Journal of Plant Nutrition 28, 2011–2025.
| Effects of nitrogen levels and nitrate/ammonium ratios on oxalate concentrations of different forms in edible parts of spinach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1emsLzF&md5=dda6fecab0908299275663784c23a690CAS |