Significance of intracellular and secreted acid phosphatase enzyme activities, and zinc and calcium interactions, on phosphorus efficiency in wheat, sunflower, chickpea, and lentil cultivars
Aydin Gunes A B and Ali Inal AA Faculty of Agriculture, Department of Soil Science and Plant Nutrition, Ankara University, 06110 Ankara, Turkey.
B Corresponding author. Email: agunes@agri.ankara.edu.tr
Australian Journal of Agricultural Research 59(4) 339-347 https://doi.org/10.1071/AR07195
Submitted: 17 May 2007 Accepted: 17 December 2007 Published: 8 April 2008
Abstract
Phosphorus efficiency (PE), and its relationship with intracellular (APase) and secreted (S-APase) acid phosphatases, anthocyanin accumulation, and calcium and zinc nutrition, were compared among 8 cultivars of each of wheat, sunflower, chickpea, and lentil grown under greenhouse conditions with low and high rates of P supply in a P-deficient calcareous soil. Except for the chickpea cultivars, deficiency of P resulted in significant decreases in shoot dry weight of all the crop cultivars and led to significant decreases in root dry weight in wheat and sunflower, significant increases in root dry weight in chickpea, and no significant difference in root dry weight in lentil. PE differed greatly among species and their cultivars. On average, shoot P concentration in cultivars of wheat, sunflower, chickpea, and lentil increased by 44%, 54%, 47%, and 8%, respectively, with P supply, and the increases in P concentration differed greatly among cultivars of all species. Intracellular leaf APase activity of wheat and lentil cultivars was slightly decreased by P supply, while it was unchanged in sunflower and chickpea cultivars. However, root-secreted acid phosphatase (S-APase) activity was significantly reduced by P supply in wheat, sunflower, and chickpea cultivars. Under low-P conditions, S-APase activities of all species except sunflower were negatively correlated with PE. Phosphorus deficiency increased the anthocyanin concentration of the cultivars of wheat and sunflower, whereas it was usually decreased in cultivars of the P-efficient species chickpea and lentil. In general, concentration of Ca was found to be lower, but Zn concentration was higher, in P-efficient cultivars than in P-inefficient cultivars. The results demonstrated that PE of the cultivars clearly depends on their ability to take up P and Zn, and on secretion of acid phosphatases from their roots under P deficiency. The results also suggest that characteristics of Zn and Ca nutrition should be taken into consideration when screening cultivars of crop species for their P efficiency.
Additional keywords: anthocyanin, P-efficiency, phosphatases.
Acknowledgments
We are grateful to TUBITAK (The Scientific and Technological Research Council of Turkey) for supporting the project (Project no: 104 O 426). Thanks to Dr David J. Pilbeam, University of Leeds, UK, for help with the manuscript.
Besford RT
(1979) Phosphorus nutrition and acid phosphatase activity in leaves of seven plant species. Journal of the Science of Food and Agriculture 30, 282–285.
Cakmak I
(2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant and Soil 247, 3–24.
| Crossref | GoogleScholarGoogle Scholar |
Elliot GC, Läuchli A
(1986) Evaluation of an acid phosphatase assay for detection of phosphorus deficiency in leaves of maize (Zea mays L.). Journal of Plant Nutrition 9, 1469–1477.
Gahoonia TS,
Ali O,
Sarker A,
Rahman MM, Erskine W
(2005) Root traits, nutrient uptake, multi-location grain yield and benefit-cost ratio of two lentil (Lens culinaris, Medikus) varieties. Plant and Soil 272, 153–161.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE
(2004) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant and Soil 262, 55–62.
| Crossref | GoogleScholarGoogle Scholar |
Gaume A,
Machler F,
Leon CD,
Narro L, Frossard E
(2001) Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant and Soil 228, 253–264.
| Crossref | GoogleScholarGoogle Scholar |
Gill MA,
Kanwal S,
Aziz T, Rahmatullah I
(2004) Differences in phosphorus–zinc interaction among sunflower (Helianthus annuus L.), Brassica (Brassica napus L.) and maize (Zea mays L.). Pakistan Journal of Agricultural Science 41, 29–34.
Gunes A,
Inal A,
Alpaslan M, Cakmak I
(2006) Genotypic variation in phosphorus efficiency between wheat cultivars grown under greenhouse and field conditions. Soil Science and Plant Nutrition 52, 470–478.
| Crossref | GoogleScholarGoogle Scholar |
Holford ICR
(1997) Soil phosphorus: its measurement and its uptake by plants. Australian Journal of Soil Research 35, 227–239.
| Crossref | GoogleScholarGoogle Scholar |
Johnson JF,
Allan DL,
Vance CP, Weiblen G
(1996) Root carbon dioxide fixation by phosphorus deficient Lupinus albus: contribution to organic acid exudation by proteoid roots. Plant Physiology 112, 19–30.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Juszczuk IM,
Wiktorowska A,
Malusa E, Rychter AM
(2004) Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.). Plant and Soil 267, 41–49.
| Crossref | GoogleScholarGoogle Scholar |
Krasilnikoff G,
Gahoonia T, Nielsen NE
(2003) Variation in phosphorus uptake efficiency by genotypes of cowpea (Vigna unguiculata) due to differences in root and root hair length and induced rhizosphere processes. Plant and Soil 251, 83–91.
| Crossref | GoogleScholarGoogle Scholar |
Li SM,
Li L,
Zhang FS, Tang C
(2004) Acid phosphatase role in chickpea/maize intercropping. Annals of Botany 94, 297–303.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu Y,
Mi G,
Chen F,
Zhang J, Zhang F
(2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Science 167, 217–223.
| Crossref | GoogleScholarGoogle Scholar |
Marschner H
(1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Research 56, 203–207.
| Crossref | GoogleScholarGoogle Scholar |
Osborne LD, Rengel Z
(2002) Screening cereals for genotypic variation in efficiency of phosphorus uptake and utilization. Australian Journal of Agricultural Research 53, 295–303.
| Crossref | GoogleScholarGoogle Scholar |
Ozturk L,
Eker S,
Torun B, Cakmak I
(2005) Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil. Plant and Soil 269, 69–80.
| Crossref | GoogleScholarGoogle Scholar |
Raghothama KG, Karthikeyan AS
(2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Crossref | GoogleScholarGoogle Scholar |
Reay FP,
Fletcher RH, Thomas VJG
(1998) Chlorophylls, carotenoids and anthocyanin concentrations in the skin of ‘Gala’ apples during maturation and the influence of foliar applications of nitrogen and magnesium. Journal of the Science of Food and Agriculture 76, 63–71.
| Crossref | GoogleScholarGoogle Scholar |
Römer W, Schenk H
(1998) Influence of genotype on phosphate uptake and utilization efficiencies in spring barley. European Journal of Agronomy 8, 215–224.
| Crossref | GoogleScholarGoogle Scholar |
Ruiz JM,
Belakbir A, Romero L
(1996) Foliar level of phosphorus and its bioindicators in cucumis melo grafted plants. A possible effect of rootstock. Journal of Plant Physiology 149, 400–404.
Schachtman DP,
Reid RJ, Ayling SM
(1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shenoy VV, Kalagudi GM
(2005) Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnology Advances 23, 501–513.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tadano T,
Ozawa K,
Sakai H,
Osaki M, Matsui H
(1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus deficient conditions and some properties of the enzyme secreted by lupin roots. Plant and Soil 155–156, 95–98.
| Crossref | GoogleScholarGoogle Scholar |
Takahashi A,
Takeda K, Ohnishi T
(1991) Light-induced anthocyanin reduces the extent of damage to DNA in UV-irradiated Centaurea cyanus cells in culture. Plant & Cell Physiology 32, 541–547.
Trull MC,
Guiltinan M,
Lynch J, Deikman J
(1997) The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant, Cell & Environment 20, 85–92.
| Crossref | GoogleScholarGoogle Scholar |
Wang QR,
Li JY,
Li ZS, Christie P
(2005) Screening Chinese wheat germplasm for phosphorus efficiency in calcareous soils. Journal of Plant Nutrition 28, 489–505.
| Crossref | GoogleScholarGoogle Scholar |
Wasaki J,
Yamamura T,
Shinano T, Osaki M
(2003) Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant and Soil 248, 129–136.
| Crossref | GoogleScholarGoogle Scholar |
Yun SJ, Kaeppler SM
(2001) Induction of maize acid phosphatase activities under phosphorus starvation. Plant and Soil 237, 109–115.
| Crossref | GoogleScholarGoogle Scholar |
Zhu YG,
Smith SE, Smith FA
(2001) Zinc (Zn)-phosphorus (P) interactions in two cultivars of spring wheat (Triticum aestivum L.) differing in P uptake efficiency. Annals of Botany 88, 941–945.
| Crossref | GoogleScholarGoogle Scholar |
Zohlen A, Tyler G
(2004) Soluble inorganic tissue phosphorus and calcicole-calcifuge behavior of plants. Annals of Botany 94, 427–432.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
