Effect of phosphate solubilising bacteria (Enterobacter cloacae) on phosphorus uptake efficiency in sugarcane (Saccharum officinarum L.)
Saeed Safirzadeh
A B , Mostafa Chorom A and Naeimeh Enayatizamir A
+ Author Affiliations
- Author Affiliations
A Agriculture Faculty, Shahid Chamran University of Ahvaz, Iran.
B Corresponding author. Email: s_safirzade@yahoo.com
Soil Research 57(4) 333-341 https://doi.org/10.1071/SR18128
Submitted: 13 May 2018 Accepted: 19 March 2019 Published: 28 May 2019
Abstract
Phosphorus (P) is an essential nutrient in sustainable production of sugarcane. Due to low labile P in soil under sugarcane cultivation, evaluation of the efficiency of P uptake and the application of phosphate solubilising bacteria (PSB) play important roles in management of P fertiliser. To investigate the effect of using PSB on P uptake in sugarcane (variety CP57–614), a pot experiment was conducted with three replications in greenhouse conditions. The treatments were a combination of three P rates (0 (P0), 50 and 100% (~40 mg kg−1) as triple superphosphate, and two PSB strains (Enterobacter cloacae R13 (R13) and R33 (R33)) which were applied independently and simultaneously. Morphological characteristics of sugarcane and some biochemical parameters were evaluated in the rhizosphere at three harvesting times: 60, 95 and 140 days after planting (DAP). Whereas in low available P (P0), bacterial strain R33 improved P uptake along with sugarcane ageing, P uptake was diminished in non-inoculated treatment over time. Activity of PSBs in the rhizosphere (especially strain R33) prevented the sharp fall of P influx after 95 DAP in low available P condition. Indeed, activity of R33 in the rhizosphere decreased the dependence of P uptake on root development via improving P uptake. Therefore, influx was the main mechanism of P uptake in sugarcane. Sugarcane inoculated by PSBs acquired 76 and 81% of total P uptake from non-Olsen-P fraction in P0R13 and P0R33 respectively at 95 DAP. However, this amount was lower (70.4%) in P0R0. Furthermore, strain R33 improved P uptake efficiency in sugarcane by changing root morphology (e.g. specific root length and root length) and reducing soil limitations (e.g. enhancement of P compound solubility and P influx).
Additional keywords: non-Olsen-phosphorus, phosphorus influx, phosphatase, phosphate solubilising bacteria, rhizosphere, sugarcane.
References
Albuquerque AWD, Sa LDA, Rodrigues WAR, Moura AB, Oliveira-Filho MDS (2016) Growth and yield of sugarcane as a function of phosphorus doses and forms of application. Revista Brasileira de Engenharia Agrícola e Ambiental 20, 29–35.| Growth and yield of sugarcane as a function of phosphorus doses and forms of application.Crossref | GoogleScholarGoogle Scholar |
Asmar F, Singh T, Gahoonia T, Nielsen NE (1995) Barley genotypes differ in activity of soluble extracellular phosphatase and depletion of organic phosphorus in the rhizosphere soil. Plant and Soil 172, 117–122.
| Barley genotypes differ in activity of soluble extracellular phosphatase and depletion of organic phosphorus in the rhizosphere soil.Crossref | GoogleScholarGoogle Scholar |
Barraclough PB, Tinker PB (1981) The determination of ionic diffusion coefficient in field soils. I. Diffusion coefficient in sieved soils in relation to water content and bulk density. European Journal of Soil Science 32, 225–236.
| The determination of ionic diffusion coefficient in field soils. I. Diffusion coefficient in sieved soils in relation to water content and bulk density.Crossref | GoogleScholarGoogle Scholar |
Bhadoria PBS, Singh S, Claassen N (2001) Phosphorus efficiency of wheat, maize and groundnut grown in low phosphorus-supplying soil. Plant Nutrition 92, 530–531.
Bhadoria RS, Steingrobe B, Claassen N, Liebersbach H (2002) Phosphorus efficiency of wheat and sugar beet seedlings grown in soils with mainly calcium, or iron and aluminium phosphate. Plant and Soil 246, 41–52.
| Phosphorus efficiency of wheat and sugar beet seedlings grown in soils with mainly calcium, or iron and aluminium phosphate.Crossref | GoogleScholarGoogle Scholar |
Bouyoucos GJ (1961) Hydrometer method improved for making particle size analyses of soils. Agronomy Journal 54, 464–465.
| Hydrometer method improved for making particle size analyses of soils.Crossref | GoogleScholarGoogle Scholar |
Chotchutima S, Tudsri S, Kangvansaichol K, Sripichitt P (2016) Effects of sulfur and phosphorus application on the growth, biomass yield and fuel properties of leucaena (Leucaena leucocephala(Lam.) de Wit.) as bioenergy crop on sandy infertile soil. Agriculture and Natural Resources 50, 54–59.
Fernández LA, Zalba P, Gómez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biology and Fertility of Soils 43, 805–809.
Föhse D, Claassen N, Jungk A (1988) Phosphorus efficiency of plants: I. External and internal P requirement and P uptake efficiency of different plant species. Plant and Soil 110, 101–109.
| Phosphorus efficiency of plants: I. External and internal P requirement and P uptake efficiency of different plant species.Crossref | GoogleScholarGoogle Scholar |
Föhse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants, II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species. Plant and Soil 132, 261–272.
| Phosphorus efficiency of plants, II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE, Raza S (1994) Phosphorus depletion in the rhizosphere as influenced by soil moisture. Plant and Soil 159, 213–218.
| Phosphorus depletion in the rhizosphere as influenced by soil moisture.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Asmar F, Giese H, Gissel-Nielsen G, Nielsen NE (2000) Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments. European Journal of Agronomy 12, 281–289.
| Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments.Crossref | GoogleScholarGoogle Scholar |
Gianfreda L (2015) Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition 15, 283–306.
| Enzymes of importance to rhizosphere processes.Crossref | GoogleScholarGoogle Scholar |
Gourley CJP, Allan DL, Russelle MP (1993) Defining phosphorus efficiency in plants. Plant and Soil 155-156, 289–292.
| Defining phosphorus efficiency in plants.Crossref | GoogleScholarGoogle Scholar |
Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant and Soil 245, 83–93.
| Role of soil microorganisms in improving P nutrition of plants.Crossref | GoogleScholarGoogle Scholar |
Hamdi H (2016) Sustainability in sugarcane production: opportunities and limitations in south west of Iran. Sugar Tech 18, 642–646.
| Sustainability in sugarcane production: opportunities and limitations in south west of Iran.Crossref | GoogleScholarGoogle Scholar |
Harinathan B, Sankaralingam S, Palpperumal S, Kathiresan D, Shankar T, Prabhu D (2016) Effect of phosphate solubilizing bacteria on growth and development of pearl millet and ragi. Journal of Advances in Biology & Biotechnology 7, 1–7.
| Effect of phosphate solubilizing bacteria on growth and development of pearl millet and ragi.Crossref | GoogleScholarGoogle Scholar |
Hariprasad P, Niranjana SR (2009) Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant and Soil 316, 13–24.
| Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato.Crossref | GoogleScholarGoogle Scholar |
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60, 579–598.
| Soil beneficial bacteria and their role in plant growth promotion: a review.Crossref | GoogleScholarGoogle Scholar |
Hedley MJ, White RE, Nye PH (1982) Plant-induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings III. Changes in L value, soil phosphate fractions and phosphatase activity. New Phytologist 91, 45–56.
| Plant-induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings III. Changes in L value, soil phosphate fractions and phosphatase activity.Crossref | GoogleScholarGoogle Scholar |
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173–195.
| Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review.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.
| Variation in phosphorus uptake efficiency by genotypes of cowpea (Vigna unguiculata) due to differences in root and root hair length and induced rhizosphere processes.Crossref | GoogleScholarGoogle Scholar |
Kuo S (1996) Phosphorus. In ‘Methods of Soil Analysis’. Part 3. (Ed. DL Sparks) pp. 869–919. (Soil Science Society of America Publishing: Madison, WI, USA)
Lal KN, Singh JN (1961) Uptake of phosphorus and its accumulation in component parts of sugarcane as affected by age, phosphorus deficiency and levels of phosphorus. Soil and Plant Food 6, 120–126.
| Uptake of phosphorus and its accumulation in component parts of sugarcane as affected by age, phosphorus deficiency and levels of phosphorus.Crossref | GoogleScholarGoogle Scholar |
Lamizadeh E, Enayatizamir N, Motamedi H (2016) Isolation and identification of plant growth-promoting rhizobacteria (PGPR) from the rhizosphere of sugarcane in saline and non-saline soil. International Journal of Current Microbiology and Applied Sciences 5, 1072–1083.
| Isolation and identification of plant growth-promoting rhizobacteria (PGPR) from the rhizosphere of sugarcane in saline and non-saline soil.Crossref | GoogleScholarGoogle Scholar |
Loeppert HL, Suarez DL (1996) Carbonate and gypsum. In ‘Methods of Soil Analysis’. Part 3. (Ed. DL Sparks) pp. 437–474. (Soil Science Society of America Publishing: Madison, WI, USA)
Mareni R, Nyathi C, Madanzi T, Masaka J, Manjeru C, Manjeru P (2013) The effect of phosphorus fertiliser application rates on root biomass characteristics of irrigated sugarcane (Saccharum officinarum L). Midlands State University Journal of Science, Agriculture and Technology 4, 108–124.
Meyer JH, Wood RA (1989) Factors affecting phosphorus nutrition and fertiliser use by sugarcane in south Africa. In ‘Proceedings of the South African Sugar Technologists’ Association’ pp. 153–158. Mount Edgecombe, South Africa.
Miller RO (1998) Determination of dry matter content of plant tissue: gravimetric moisture. In ‘Handbook of Methods for Plant Analysis’. (Ed Y. P. Kalra) pp. 51–52. (CRC Press: USA)
Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74, 562–564.
| Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization.Crossref | GoogleScholarGoogle Scholar |
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
| A modified single solution method for the determination of phosphate in natural waters.Crossref | GoogleScholarGoogle Scholar |
Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In ‘Methods of Soil Analysis’. Part 3. (Ed. DL Sparks) pp. 961–1010. (Soil Science Society of America Publishing: Madison, WI, USA)
Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant and Soil 281, 109–120.
| Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes.Crossref | GoogleScholarGoogle Scholar |
Olsen SR, Cole CV, Watanabe ES, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture Circular 939, 1–18.
Panhwar QA, Radziah O, Naher UA, Zaharah AR, Razi MI, Shamshuddin J (2013) Effect of phosphate-solubilizing bacteria and oxalic acid on phosphate uptake from different P fractions and growth improvement of aerobic rice using 32P technique. Australian Journal of Crop Science 7, 1131–1140.
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant and Soil 288, 127–139.
| Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status.Crossref | GoogleScholarGoogle Scholar |
Sharma S, Kumar V, Tripathi RB (2011) Isolation of phosphate solubilizing microorganism (PSMs) from soil. Journal of Microbiology and Biotechnology Research 1, 90–95.
Tennant D (1975) A test of a modified line intercepts method of estimating root length. Journal of Ecology 63, 995–1001.
| A test of a modified line intercepts method of estimating root length.Crossref | GoogleScholarGoogle Scholar |
Tsado PA, Lawal BA, Igwe CA, Adeboye MKA, Odofin AJ, Adekambi AA (2013) Effects of sources and levels of phosphorus on yield and quality of sugarcane in southern Guinea Savanna zone of Nigeria. Agriculture Science Developments 2, 25–27.
