Abstract
Post-anthesis effect of phosphorus (P)-deficit is less studied in plants. P-deficit analysis is rarely performed in different tissues of the plant together. The present study analyzed total-P, inorganic-P, acid phosphatases, ribonucleases, carbohydrates, and antioxidants in the roots, lower leaves, flag leaves, and spikelets at 0, 10, 20, and 30 days after anthesis and recorded yield components at harvest in rice cultivars CSR10 (low-P tolerant) and Pusa44 (low-P susceptible) under P-deprivation (P0) compared to P-application at 30 kg ha−1 (P30). Total-P was deficient in the roots and leaves of Pusa44 compared to CSR10 under P0. Acid phosphatases and ribonucleases were enhanced by roots under P0, and the increase was exceptionally high in CSR10. Hexoses, sucrose, and starch levels remained low in the vegetative tissues of Pusa44 compared to CSR10 under P0. Starch and sucrose were mobilized from vegetative tissues especially from the roots of CSR10 compared to Pusa44 under P0. Sucrose and starch levels were high in the spikelets of CSR10 compared to Pusa44 under P0. Antioxidants were high in the vegetative tissues especially in the roots of CSR10 compared to Pusa44 under P0. At harvest, unfilled grains per panicle increased and grain yield reduced in Pusa44 under P0. Results concluded that post-anthesis roots metabolic activities, in the form of acid phosphatases/ribonucleases for P-acquisition and antioxidants to counteract stress and starch/sucrose mobilization toward spikelets, may play an important role toward low-P tolerance in rice.
Similar content being viewed by others
References
Albacete A, Cantero-Navarro E, Balibrea ME, Großkinsky DK, de la Cruz GM, Martínez-Andújar C, Smigocki AC, Roitsch T, Pérez-Alfocea F (2014) Hormonal and metabolic regulation of tomato fruit sink activity and yield under salinity. J Exp Bot 65(20):6081–6095. https://doi.org/10.1093/jxb/eru347
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Meth Enzymol 8:115–118. https://doi.org/10.1016/0076-6879(66)08014-5
Banerjee A, Singh A, Roychoudhury A (2021) Fluoride toxicity variably affects overall physiology and grain development in three contrasting rice genotypes, representing a potential biohazard. Environ Sci Pollut Res Int 28(30):40220–40232. https://doi.org/10.1007/s11356-020-10604-7
Crafts-Brandner SJ (1992) Phosphorus nutrition influence on starch and sucrose accumulation, and activities of ADP-glucose pyrophosphorylase and sucrose-phosphate synthase during the grain filling period in soybean. Plant Physiol 98(3):1133–1138. https://doi.org/10.1104/pp.98.3.1133
Cuellar-Ortiz SM, De La Paz A-M, Acosta-Gallegos J, Covarrubias AA (2008) Relationship between carbohydrate partitioning and drought resistance in common bean. Plant Cell Environ 31(10):1399–1409. https://doi.org/10.1111/j.1365-3040.2008.01853.x
Dissanayaka DMSB, Maruyama H, Nishida S, Tawaraya K, Wasaki J (2017) Landrace of japonica rice, Akamai exhibits enhanced root growth and efficient leaf phosphorus remobilization in response to limited phosphorus availability. Plant Soil 414:327–338. https://doi.org/10.1007/s11104-016-3129-1
Dissanayaka DMSB, Plaxton WC, Lambers H, Siebers M, Marambe B, Wasaki J (2018) Molecular mechanisms underpinning phosphorus-use efficiency in rice. Plant Cell Environ 41:1483–1496. https://doi.org/10.1111/pce.13191
Dong S, Beckles DM (2019) Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J Plant Physiol 234–235:80–93. https://doi.org/10.1016/j.jplph.2019.01.007
Dubois M (2022) Sugar transport from sheaths to seeds: A role for the kinase SnRK1. Plant Physiol 189(3):1196–1198. https://doi.org/10.1093/plphys/kiac187
Grabau LJ, Blevins DG, Minor HC (1986) P nutrition during seed development: leaf senescence, pod retention, and seed weight of soybean. Plant Physiol 82(4):1008–1012. https://doi.org/10.1104/pp.82.4.1008
HacisalihogluG BAL, Gustin JL, Eker S, Asikli S, Heybet EH, Ozturk L, Cakmak I, Yazici A, Burkey KO, James ORF, Settles AM (2018) Quantitative trait loci associated with soybean seed weight and composition under different phosphorus levels. J Integr Plant Biol 60:232–241. https://doi.org/10.1111/jipb.12612
Han Y, Hong W, Xiong C, Lambers H, Sun Y, Xu Z, Schulze WX, Cheng L (2022a) Combining analyses of metabolite profiles and phosphorus fractions to explore high phosphorus utilization efficiency in maize. J Exp Bot 73(12):4184–4203. https://doi.org/10.1093/jxb/erac117
Han Y, White PJ, Cheng L (2022b) Mechanisms for improving phosphorus utilization efficiency in plants. Ann Bot 129(3):247–258. https://doi.org/10.1093/aob/mcab145
Hocking PJ (1994) Dry-matter production, mineral nutrient concentrations, and nutrient distribution and redistribution in irrigated spring wheat. J Plant Nutr 17(8):1289–1308. https://doi.org/10.1080/01904169409364807
Hu W, Loka DA, Fitzsimons TR, Zhou Z, Derrick M, Oosterhuis DM (2018) Potassium deficiency limits reproductive success by altering carbohydrate and protein balances in cotton (Gossypium hirsutum L.). Environ Exp Bot 145:87–94. https://doi.org/10.1016/j.envexpbot.2017.10.024
Hu Y, Liu J, Lin Y, Xu X, Xia Y, Bai J, Yu Y, Xiao F, Ding Y, Ding C, Chen L (2022) Sucrose nonfermenting-1-related protein kinase 1 regulates sheath-to-panicle transport of nonstructural carbohydrates during rice grain filling. Plant Physiol 189(3):1694–1714. https://doi.org/10.1093/plphys/kiac124
Iqbal A, Qiang D, Xiangru W, Huiping G, Hengheng Z, Xiling Z, Meizhen S (2023a) Integrative physiological, transcriptome and metabolome analysis reveals the involvement of carbon and flavonoid biosynthesis in low phosphorus tolerance in cotton. Plant Physiol Biochem 196:302–317. https://doi.org/10.1016/j.plaphy.2023.01.042
Iqbal A, Qiang D, Xiangru W, Huiping G, Hengheng Z, Xiling Z, Meizhen S (2023b) Phosphorus and carbohydrate metabolism contributes to low phosphorus tolerance in cotton. BMC Plant Biol 23(1):97. https://doi.org/10.1186/s12870-023-04100-6
Jeong K, Baten A, Waters DL, Pantoja O, Julia CC, Wissuwa M, Heuer S, Kretzschmar T, Rose TJ (2017) Phosphorus remobilization from rice flag leaves during grain filling: an RNA-seq study. Plant Biotechnol J 15(1):15–26
Jeong K, Julia CC, Waters DLE, Pantoja O, Wissuwa M, Heuer S, Liu L, Rose TJ (2017b) Remobilisation of phosphorus fractions in rice flag leaves during grain filling: Implications for photosynthesis and grain yields. PLoS ONE 12(11):e0187521. https://doi.org/10.1371/journal.pone.0187521
Jeong K, Pantoja O, Baten A, Waters D, Kretzschmar T, Wissuwa M, Julia CC, Heuer S, Rose TJ (2018) Transcriptional response of rice flag leaves to restricted external phosphorus supply during grain filling in rice cv. IR64. PLoS ONE 13(9):e0203654. https://doi.org/10.1371/journal.pone.0203654
Joel OO, Nawiri P, Musila W, Gweyi-Onyango JP (2017) Effect of phosphorus deficiency on phenolics and antioxidants content of two African nightshade varieties grown in Kenya. Int J Plant Soil Sci 15(3):111. https://doi.org/10.9734/IJPSS/2017/32424
Julia C, Wissuwa M, Kretzschmar T, Jeong K, Rose T (2016) Phosphorus uptake, partitioning and redistribution during grain filling in rice. Ann Bot 118(6):1151–1162. https://doi.org/10.1093/aob/mcw164
Kaur A, Zhawar VK, Dhillon BS (2023) Phosphorus uptake relates to vegetative growth, grain yield and grain quality in phosphorus deprived rice genotypes. Iran J Plant Physiol (accepted)
Kaur R, Zhawar VK (2021) Regulation of secondary antioxidants and carbohydrates by gamma-aminobutyric acid under salinity-alkalinity stress in rice (Oryza sativa L.). Biol Future 72(2):229–239. https://doi.org/10.1007/s42977-020-00055-z
Kawa D, Julkowska MM, Sommerfeld HM, Ter Horst A, Haring MA, Testerink C (2016) Phosphate-dependent root system architecture responses to salt stress. Plant Physiol 172(2):690–706. https://doi.org/10.1104/pp.16.00712
Kumar S, Chugh C, Seem K, Kumar S, Vinod KK, Mohapatra T (2021) Characterization of contrasting rice (Oryza sativa L.) genotypes reveals the Pi-efficient schema for phosphate starvation tolerance. BMC Plant Biol 21:1–26. https://doi.org/10.1186/s12870-021-03015-4
Kuppusamy T, Giavalisco P, Arvidsson S, Sulpice R, Stitt M, Finnegan PM, Scheible WR, Lambers H, Jost R (2014) Lipid biosynthesis and protein concentration respond uniquely to phosphate supply during leaf development in highly phosphorus-efficient Hakea prostrata. Plant Physiol 166(4):1891–911. https://doi.org/10.1104/pp.114.248930
Li L, Liu C, Lian X (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72:423–432. https://doi.org/10.1007/s11103-009-9580-0
MacNeill GJ, Mehrpouyan S, Minow MAA, Patterson JA, Tetlow IJ, Emes MJ (2017) Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation. J Exp Bot 68(16):4433–4453. https://doi.org/10.1093/jxb/erx291
Mancinelli AL (1984) Photoregulation of anthocyanin synthesis: VIII. Effect of light pretreatments. Plant Physiol 75(2):447–453. https://doi.org/10.1104/pp.75.2.447
Mehra P, Pandey BK, Giri J (2016) Comparative morphophysiological analyses and molecular profiling reveal Pi-efficient strategies of a traditional rice genotype. Front Plant Sci 6:1184. https://doi.org/10.3389/fpls.2015.01184
Meng X, Chen WW, Wang YY, Huang ZR, Ye X, Chen LS, Yang LT (2021) Effects of phosphorus deficiency on the absorption of mineral nutrients, photosynthetic system performance and antioxidant metabolism in Citrus grandis. PLoS ONE 16(2):e0246944. https://doi.org/10.1371/journal.pone.0246944
Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Aca Sci USA 102:11934–11939. https://doi.org/10.1073/pnas.0505266102
Miura K, Sato A, Ohta M, Furukawa J (2011) Increased tolerance to salt stress in the phosphate-accumulating Arabidopsis mutants siz1 and pho2. Planta 234:1191–1199. https://doi.org/10.1007/s00425-011-1476-y
Müller J, Gödde V, Niehaus K, Zörb C (2015) Metabolic adaptations of white lupin roots and shoots under phosphorus deficiency. Front Plant Sci 6:1014. https://doi.org/10.3389/fpls.2015.01014
Nie Z, Luo B, Zhang X, Wu L, Liu D, Guo J, He X, Gao D, Gao S, Gao S (2021) Combined transcriptome and proteome analysis of maize (Zea mays L.) reveals a complementary profile in response to phosphate deficiency. Curr Issues Mol Biol 43(2):1142–1155. https://doi.org/10.3390/cimb43020081
Pariasca-Tanaka J, Satoh K, Rose T, Mauleon R, Wissuwa M (2009) Stress response versus stress tolerance: a transcriptome analysis of two rice lines contrasting in tolerance to phosphorus deficiency. Rice 2:167–185. https://doi.org/10.1007/s12284-009-9032-0
Parra-Almuna L, Diaz-Cortez A, Ferrol N, de la Luz Mora M (2018) Aluminium toxicity and phosphate deficiency activates antioxidant systems and up-regulates expression of phosphate transporters gene in ryegrass (Lolium perenne L.) plants. Plant Physiol Biochem 130:445–454. https://doi.org/10.1016/j.plaphy.2018.07.031
Plaut Z, Butow BJ, Blumenthal CS, Wrigley CW (2004) Transport of dry matter into developing wheat kernels and its contribution to grain yield under post-anthesis water deficit and elevated temperature. Field Crops Res 86(2–3):185–198. https://doi.org/10.1016/j.fcr.2003.08.005
Pontigo S, Ulloa M, Godoy K, Nikolic N, Nikolic M, de la Luz Mora M, Cartes P (2018) Phosphorus efficiency modulates phenol metabolism in wheat genotypes. J Soil Sci Plant Nutr 18(3):904–920. https://doi.org/10.4067/S0718-95162018005002603
Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341. https://doi.org/10.1006/abio.1999.4019
Rao DS, Raghavendra M, Gill P, Madan S, Munjal R (2020) Studies on role of proline, hydrogen peroxide and total antioxidant activity in wheat (Triticum aestivum L.) under drought stress after anthesis. Int J Chem Stud 8:738–742. https://doi.org/10.22271/chemi.2020.v8.i6k.10856
Rapp YG, Ransbotyn V, Grafi G (2015) Senescence meets dedifferentiation. Plants (Basel) 4(3):356–368. https://doi.org/10.3390/plants4030356
Ring AS, Waniska RD, Rooney LW (1988) Phenolic compounds in different sorghum tissues during maturation. Biomass 17(1):39–49. https://doi.org/10.1016/0144-4565(88)90069-8
Rose TJ, Rengel Z, Ma Q, Bowden JW (2007) Differential accumulation patterns of phosphorus and potassium by canola cultivars compared to wheat. J Plant Nutr Soil Sci 170(3):404–411. https://doi.org/10.1002/jpln.200625163
Rose TJ, Pariasca-Tanaka J, Rose MT, Fukuta Y, Wissuwa M (2010) Genotypic variation in grain phosphorus concentration, and opportunities to improve P-use efficiency in rice. Field Crops Res 119(1):154–160. https://doi.org/10.1016/j.fcr.2010.07.004
Rose TJ, Impa SM, Rose MT, Tanaka JP, Mori A, Heuer S, Johnson-Beebout SE, Wissuwa M (2013) Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding. Ann Bot 112:331–345. https://doi.org/10.1093/aob/mcs217
Shane MW, Stigter K, Fedosejevs ET, Plaxton WC (2014) Senescence-inducible cell wall and intracellular purple acid phosphatases: implications for phosphorus remobilization in Hakea prostrata (Proteaceae) and Arabidopsis thaliana (Brassicaceae). J Exp Bot 65:6097–6106. https://doi.org/10.1093/jxb/eru348
Shi W, Muthurajan R, Rahman H, Selvam J, Peng S, Zou Y, Jagadish KSV (2013) Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol 197(3):825–837. https://doi.org/10.1111/nph.12088
Stigter KA, Plaxton WC (2015) Molecular mechanisms of phosphorus metabolism and transport during leaf senescence. Plants 4:773–98
Tanamachi K, Miyazaki M, Matsuo K, Suriyasak C, Tamada A, Matsuyama K, Iwaya-Inoue M, Ishibashi Y (2016) Differential responses to high temperature during maturation in heat-stress-tolerant cultivars of Japonica rice. Plant Prod Sci 19(2):300–308. https://doi.org/10.1080/1343943X.2016.1140007
Teng Z, Chen Y, Meng S, Duan M, Zhang J, Ye N (2023) Environmental stimuli: a major challenge during grain filling in cereals. Int J Mol Sci 24(3):2255. https://doi.org/10.3390/ijms24032255
Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214(3):943–951. https://doi.org/10.1111/nph.14491
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
Wang Y, Wang F, Lu H, Liu Y, Mao C (2021) Phosphate uptake and transport in plants: an elaborate regulatory system. Plant Cell Physiol 62(4):564–572. https://doi.org/10.1093/pcp/pcab011
Wissuwa M, Gamat G, Ismail AM (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56(417):1943–1950. https://doi.org/10.1093/jxb/eri189
Zasoski RJ, Burau RG (1977) A rapid nitric-perchloric acid digestion method for multi-element tissue analysis. Commun Soil Sci Plant Anal 8:425–436. https://doi.org/10.1080/00103627709366735
Zhang D, Liu C, Cheng H, Kan G, Cui S, Meng Q, Gai J, Yu D (2010) Quantitative trait loci associated with soybean tolerance to low phosphorus stress based on flower and pod abscission. Plant Breed 129:243–249. https://doi.org/10.1111/j.1439-0523.2009.01682.x
Zhawar VK, Kaur N, Gupta AK (2011) Phytic acid and raffinose series oligosaccharides metabolism in developing chickpea seeds. Physiol Mol Biol Plants 17(4):355–362. https://doi.org/10.1007/s12298-011-0080-8
Zhou M, Zhu S, Mo X, Guo Q, Li Y, Tian J, Liang C (2022) Proteomic analysis dissects molecular mechanisms underlying plant responses to phosphorus deficiency. Cells 11(4):651. https://doi.org/10.3390/cells11040651
Acknowledgements
The Authorss acknowledge the support given in the form of FIST (Fund for Improvement of S&T Infrastructure in Universities and Higher Educational Institutions) facilities by DST (Department of Science and Technology) during the conduction of the present work.
Author information
Authors and Affiliations
Contributions
VKZ and BSD: conceptualization. AK: conducting experiment, analysis, interpretation, and manuscript rough draft preparation. VKZ: analysis, interpretation, drafting, and critical revisions of the manuscript.
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no competing interest.
Additional information
Handling Editor: Pramod Kumar Nagar
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kaur, A., Zhawar, V.K. & Dhillon, B.S. Post-anthesis Roots Metabolic Activities Relate Low Phosphorus (P)-Tolerance in Rice (Oryza sativa L.). J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11344-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00344-024-11344-5