The effects of diversified phosphorus nutrition on the growth of oat (Avena sativa L.) and acid phosphatase activity

Ewa Żebrowska, Kamila Zujko, Anna Kuleszewicz, Iwona Ciereszko

Abstract


We studied the effect of differential phosphorus (P) supply on the development of oat seedlings (Avena sativa L. ‘Arab’) as well as localization and activity of acid phosphatases in tissues and root exudates. Plants were grown for 1–3 weeks on nutrient media with inorganic phosphate (+P, control), reduced Pi (0.1 P), phytic acid (PA) as organic P source, and without P addition (−P), in standard conditions or in a split-root culture system. Phosphate starvation reduced shoot growth but increased root elongation and root/shoot ratio, whereas 0.1 P and PA oat plants had similar growth parameters to +P plants. The growth on −P medium significantly decreased Pi content in all tissues, but only a slight Pi decrease was observed in plants grown on 0.1 P and PA media or various split-root system conditions. Pi starvation led to an increase in acid phosphatase (APase) activity in root exudates when compared to +P, 0.1 P, and PA plant samples. APase activity was especially intensive in root cross sections in rhizodermis and around/in vascular tissues of −P plants. For plants grown on 0.1 P medium and on phytic acid, APase activity did not change when compared to the control. Three major isoforms of APases were detected in plant tissues (similar in all studied conditions, with a higher activity of one isoform under Pi deficit). Generally, lowered Pi content (0.1 P) was not stressful to oat plants for up to 3 weeks of culture. Oat plants grew equally well on nutrient media with Pi and on media with phytate, although phytate was considered not available for other plants. The oat plants activated mainly extracellular APases, but also intracellular enzymes, rather via nonlocal signals, to acquire Pi from external/internal sources under Pi deficiency.

Keywords


APase localization; extracellular acid phosphatase; phytate; Pi deficit; root exudates; split root

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References


Hammond JP, Broadley MR, White PJ. Genetic responses to phosphorus deficiency. Ann Bot. 2004;94:323–332. https://doi.org/10.1093/aob/mch156

Rychter AM, Rao IM. Role of phosphorus in photosynthetic carbon metabolism. In: Pessarakli M, editor. Handbook of photosynthesis. 2nd ed. New York, NY: Marcel Dekker Inc.; 2005. p. 123–148. https://doi.org/10.1201/9781420027877.ch7

Fang ZY, Shao C, Meng YJ, Wu P, Chen M. Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci. 2009;176:170–180. https://doi.org/10.1016/j.plantsci.2008.09.007

Polit JT, Ciereszko I. Sucrose synthase activity and carbohydrates content in relation to phosphorylation status of Vicia faba root meristems during reactivation from sugar depletion. J Plant Physiol. 2012;169:1597–1606. https://doi.org/10.1016/j.jplph.2012.04.017

Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 2003;157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x

Schachtman DP, Reid RJ, Ayling SM. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 1998;116:447–453. https://doi.org/10.1104/pp.116.2.447

Rouached H, Arpat AB, Poirier Y. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant. 2010;3:288–299. https://doi.org/10.1093/mp/ssp120

Wang X, Shen J, Liao H. Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci. 2010;179:302–306. https://doi.org/10.1016/j.plantsci.2010.06.007

Ciereszko I, Szczygła A, Żebrowska E. Phosphate deficiency affects acid phosphatases activity and growth of two wheat varieties. J Plant Nutr. 2011;34:815–829. https://doi.org/10.1080/01904167.2011.544351

Ciereszko I, Żebrowska E, Ruminowicz M. Acid phosphatases and growth of barley (Hordeum vulgare L.) cultivars under diverse phosphorus nutrition. Acta Physiol Plant. 2011;33:2355–2368. https://doi.org/10.1007/s11738-011-0776-y

Negi M, Sanagala R, Rai V, Jain A. Deciphering phosphate deficiency-mediated temporal effects on different root traits in rice grown in a modified hydroponic system. Front Plant Sci. 2016;7:550. https://doi.org/10.3389/fpls.2016.00550

Péret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L. Root architecture responses: in search of phosphate. Plant Physiol. 2014;166:1713–1723. https://doi.org/10.1104/pp.114.244541

Wanke M, Ciereszko I, Podbielkowska M, Rychter AM. Response to phosphate deficiency in bean (Phaseolus vulgaris L.) roots. Respiratory metabolism, sugar localization and changes in ultrastructure of bean root cells. Ann Bot. 1998;82:809–819. https://doi.org/10.1006/anbo.1998.0760

Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, et al. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J. 2010;64:775–789. https://doi.org/10.1111/j.1365-313X.2010.04375.x

Hoehenwarter W, Mönchgesang S, Neumann S, Majovsky P, Abel S, Müller J. Comparative expression profiling reveals a role of the root apoplast in local phosphate response. BMC Plant Biol. 2016;16:106. https://doi.org/10.1186/s12870-016-0790-8

Ziegler J, Schmidt S, Chutia R, Müller J, Böttcher C, Strehmel N, et al. Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J Exp Bot. 2016;67:1421–1432. https://doi.org/10.1093/jxb/erv539

Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ. Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil. 2006;281:109–120. https://doi.org/10.1007/s11104-005-3936-2

Raghothama KG, Karthikeyan AS. Phosphate acquisition. Plant Soil. 2005;274:37–49. https://doi.org/10.1007/s11104-004-2005-6

Nguyen TT, Marschner P. Soil respiration, microbial biomass and nutrient availability in soil after addition of residues with adjusted N and P concentrations. Pedosphere. 2017;27:76–85. https://doi.org/10.1016/S1002-0160(17)60297-2

Rausch C, Bucher M. Molecular mechanisms of phosphate transport in plants. Planta. 2002;216:23–37. https://doi.org/10.1007/s00425-002-0921-3

Wasaki J, Yamamura T, Shinano T, Osaki M. Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant Soil. 2003;248:129–136. https://doi.org/10.1023/A:1022332320384

Ciereszko I, Kleczkowski LA. Expression of several genes involved in sucrose/starch metabolism as affected by different strategies to induce phosphate deficiency in Arabidopsis. Acta Physiol Plant. 2005;27:147–155. https://doi.org/10.1007/s11738-005-0018-2

Maleszewski S, Ciereszko I, Skowrońska A, Mieczejko E, Kozłowska-Szerenos B. Changes induced by low oxygen concentration in photosynthetic and respiratory CO2 exchange in phosphate-deficient bean leaves. Biol Plant. 2004;48:401–405. https://doi.org/10.1023/B:BIOP.0000041093.46102.0d

Zhang Y, Wang X, Lu S, Liu D. A major root-associated acid phosphatase in Arabidopsis, AtPAP10, is regulated by both local and systemic signals under phosphate starvation. J Exp Bot. 2014;65:6577–6588. https://doi.org/10.1093/jxb/eru377

Gerke J. Phytate (inositol hexakisphosphate) in soil and phosphate acquisition from inositol phosphates by higher plants. A review. Plants. 2015;4:253–266. https://doi.org/10.3390/plants4020253

Richardson AE, Hocking PJ, Simpson RJ, George TS. Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci. 2009;60:124–143. https://doi.org/10.1071/CP07125

Torri SI, Correa RS, Renella G. Biosolid application to agricultural land – a contribution to global phosphorus recycle: a review. Pedosphere. 2017;27:1–16. https://doi.org/10.1016/S1002-0160(15)60106-0

George TS, Gregory PJ, Hocking PJ, Richardson AE. Variation in root associated phosphatase activities in wheat contributes to the utilization of organic P substrates in-vitro, but does not explain differences in the P-nutrition when grown in soils. Environ Exp Bot. 2008;64:239–249. https://doi.org/10.1016/j.envexpbot.2008.05.002

Żebrowska E, Ciereszko I. Acid phosphatases role in plant cells phosphate homeostasis. Adv Cell Biol. 2009;36:583–599.

Duff SM, Sarath G, Plaxton WC. The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant. 1994;90:791–800. https://doi.org/10.1111/j.1399-3054.1994.tb02539.x

Tran HT, Hurley BA, Plaxton WC. Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci. 2010;179:14–27. https://doi.org/10.1016/j.plantsci.2010.04.005

Coello P. Purification and characterization of secreted acid phosphatase in phosphorus-deficient Arabidopsis thaliana. Physiol Plant. 2002;116:293–298. https://doi.org/10.1034/j.1399-3054.2002.1160303.x

Lu L, Qiu W, Gao W, Tyerman SD, Shou H, Wang C. OsPAP10c, a novel secreted acid phosphatase in rice, plays an important role in the utilization of external organic phosphorus. Plant Cell Environ. 2016.39:2247–2259. https://doi.org/10.1111/pce.12794

Lung SC, Leung A, Kuang R, Wang Y, Leung P, Lim BL. Phytase activity in tobacco (Nicotiana tabacum) root exudates is exhibited by a purple acid phosphatase. Phytochemistry. 2008;69:365–373. https://doi.org/10.1016/j.phytochem.2007.06.036

Mc Lachlan KD. Acid phosphatase activity of intact roots and phosphorus nutrition in plants: II. Variations among wheat roots. Austr J Agric Res. 1980;31:441–448. https://doi.org/10.1071/AR9800441

Tian J, Wang C, Zhang Q, He X, Whelan J, Shou H. Overexpression of OsPAP10a, a root-associated acid phosphatase, increased extracellular organic phosphorus utilization in rice. J Integr Plant Biol. 2012;54:631–639. https://doi.org/10.1111/j.1744-7909.2012.01143.x

Butt MS, Tahir-Nadeem M, Khan MKI, Shabir R, Butt MS. Oat: unique among the cereals. Eur J Nutr. 2008;47:68–79. https://doi.org/10.1007/s00394-008-0698-7

Żebrowska E, Bujnowska E, Ciereszko I. Differential responses of oat cultivars to phosphate deprivation: plant growth and acid phosphatase activities. Acta Physiol Plant. 2012;34:1251–1260. https://doi.org/10.1007/s11738-011-0918-2

Ciereszko I, Miłosek I, Rychter AM. Assimilate distribution in bean plants (Phaseolus vulgaris L.) during phosphate limitation. Acta Soc Bot Pol. 1999;68:269–273. https://doi.org/10.5586/asbp.1999.037

Ames BN. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1966;8:115–118. https://doi.org/10.1016/0076-6879(66)08014-5

Ciereszko I, Janonis A, Kociakowska M. Growth and metabolism of cucumber in phosphate-deficient conditions. J Plant Nutr. 2002;25:1115–1127. https://doi.org/10.1081/PLN-120003943

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

Robinson D. The responses of plants to non-uniform supplies of nutrients. New Phytol. 1994;127:635–674. https://doi.org/10.1111/j.1469-8137.1994.tb02969.x

Tang H, Li X, Zu C, Zhang F, Shen J. Spatial distribution and expression of intracellular and extracellular acid phosphatases of cluster roots at different developmental stages in white lupin. J Plant Physiol. 2013;170:1243–1250. https://doi.org/10.1016/j.jplph.2013.04.015

Wasaki J, Maruyama H, Tanaka M, Yamamura T, Dateki H, Shinamo T, et al. Overexpression of LASAP2 gene for secretory acid phosphatase in white lupin improves the phosphorus uptake and growth of tobacco plants. Soil Sci Plant Nutr. 2009;55:107–113. https://doi.org/10.1111/j.1747-0765.2008.00329.x

Del Vecchio HA, Ying S, Park J, Knowles VL, Kanno S, Tanoi K, et al. The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J. 2014;80:569–581. https://doi.org/10.1111/tpj.12663

Wang Y, Krogstad T, Clarke JL, Hallama M, Øgaard AF, Eich-Greatorex S, et al. Rhizosphere organic anions play a minor role in improving crop species’ ability to take up residual phosphorus (P) in agricultural soils low in P availability. Front Plant Sci. 2016;7:1664. https://doi.org/10.3389/fpls.2016.01664

Wang YL, Almvik M, Clarke N, Eich-Greatorex S, Øgaard AF, Krogstad T, et al. Contrasting responses of root morphology and root-exuded organic acids to low phosphorus availability in three important food crops with divergent root traits. AoB Plants. 2015;7:plv097. https://doi.org/10.1093/aobpla/plv097

Żebrowska E, Milewska M, Ciereszko I. Mechanisms of oat (Avena sativa L.) acclimation to phosphate deficiency. PeerJ. 2017;5:e3989. https://doi.org/10.7717/peerj.3989

Lu K, Li JN, Zhong WR, Zhang K, Fu FY, Chai YR. Isolation, characterization and phosphate-starvation inducible expression of potential Brassica napus PURPLE ACID PHOSPHATASE 17 (BnPAP17) gene family. Bot Stud. 2008;49:199–213.




DOI: https://doi.org/10.5586/asbp.3571

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