Whole-plant mineral partitioning during the reproductive development of rice (Oryza sativa L.)

Raul A. Sperotto, Marta W. Vasconcelos, Michael A. Grusak, Janette P. Fett


Minimal information exists on whole-plant dynamics of mineral flow. Understanding these phenomena in a model plant such as rice could help in the development of nutritionally enhanced cultivars. A whole-plant mineral accumulation study was performed in rice (cv. Kitaake), using sequential harvests during reproductive development panicle exertion, grain filling, and full maturity stages in order to characterize mineral accumulation in roots, non-flag leaves, flag leaves, stems/sheaths, and panicles. Partition quotient analysis showed that Fe, Zn, Cu and Ni are preferentially accumulated in roots; Mn and Mg are accumulated in leaves; Mo, Ca, and S in roots and leaves; and K in roots, leaves and stems/sheaths. Correlation analysis indicated that changes in the concentrations of mineral pairs Fe-Mn, K-S, Fe-Ni, Cu-Mg, Mn-Ni, S-Mo, Mn-Ca, and Mn-Mg throughout the reproductive development of rice were positively correlated in all four of the above ground organs evaluated, with Fe-Mn and K-S being positively correlated also in roots, which suggest that root-to-shoot transfer is not driven simply by concentrations in roots. These analyses will serve as a starting point for a more detailed examination of mineral transport and accumulation in rice plants.


elemental analysis; mineral flow; correlation analysis; panicle exertion; grain filling; full maturity.

Full Text:



Abou-khalifa AAB, Misra AN, Salem AEAKM, 2008. Effect of leaf cutting on physiological traits and yield of two rice cultivars. Afr J Plant Sci 2: 147-150.

Andreeva IV, Govorina VV, Yagodin BA, Dosimova OT, 2000. Dynamics of nickel accumulation and distribution in oat plants. Agrokhimiya 4: 68-71.

Baxter I, Hermans C, Lahner B, Yakubova E, Tikhonova M, Verbruggen N, Chao DY, Salt DE, 2012. Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana. PLoS ONE 7: e35121. https://doi.org/10.1371/journal.pone.0035121

Bengtsson B, Jensen P, 1983. Uptake and distribution of calcium, magnesium and potassium in cucumber of different age. Physiol Plant 57: 428-434. https://doi.org/10.1111/j.1399-3054.1983.tb02764.x

Bittner F, 2014. Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5: 28. https://doi.org/10.3389/fpls.2014.00028

Briat JF, Rouached H, Tissot N, Gaymard F, Dubos C, 2015. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front Plant Sci 6: 290. https://doi.org/10.3389/fpls.2015.00290

Chaignon V, Bedin F, Hinsinger P, 2002a. Copper bioavailability and rhizosphere pH changes as affected by nitrogen supply for tomato and oilseed rape cropped on an acidic and calcareous soil. Plant Soil 243: 219-228. https://doi.org/10.1023/A:1019942924985

Chaignon V, DiMalta D, Hinsinger P, 2002b. Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil. New Phytol 154: 121-130. https://doi.org/10.1046/j.1469-8137.2002.00349.x

Clarkson DT, 1984. Calcium transport between tissues and its distribution in the plant. Plant Cell Environ 7: 449-456. https://doi.org/10.1111/j.1365-3040.1984.tb01435.x

Colangelo EP, Guerinot ML, 2006. Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9: 322-330. https://doi.org/10.1016/j.pbi.2006.03.015

Counce PA, Keisling TC, Mitchell AJ, 2000. A uniform, objective and adaptative system for expressing rice development. Crop Sci 40: 436-443. https://doi.org/10.2135/cropsci2000.402436x

Curie C, Briat JF, 2003. Iron transport and signaling in plants. Annu Rev Plant Biol 54: 183-206. https://doi.org/10.1146/annurev.arplant.54.031902.135018

Distelfeld A, Cakmak I, Peleg Z, Ozturk L, Yazici AM, Budak H, Saranga Y, Fahima T, 2007. Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiol Plant 129: 635-643. https://doi.org/10.1111/j.1399-3054.2006.00841.x

Drossopoulos B, Kouchaji GG, Bouranis DL, 1996. Seasonal dynamics of mineral nutrients and carbohydrates by walnut tree leaves. J Plant Nutr 19: 493-516. https://doi.org/10.1080/01904169609365138

Duan M, Sun SSM, 2005. Profiling the expression of genes controlling rice grain quality. Plant Mol Biol 59: 165-178. https://doi.org/10.1007/s11103-004-7507-3

Dwivedi S, Tripathi RD, Srivastava S, Mishra S, Shukla MK, Tiwari KK, Singh R, Rai UN, 2007. Growth performance and biochemical responses of three rice (Oryza sativa L.) cultivars grown in fly-ash amended soil. Chemosphere 67: 140-151. https://doi.org/10.1016/j.chemosphere.2006.09.012

Ghandilyan A, Vreugdenhil D, Aarts MGM, 2006. Progress in the genetic understanding of plant iron and zinc nutrition. Physiol Plant 126: 407-417. https://doi.org/10.1111/j.1399-3054.2006.00646.x

Glass ADM, 1983. Regulation of ion transport. Annu Rev Plant Physiol 34: 311-326. https://doi.org/10.1146/annurev.pp.34.060183.001523

Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K, 2015. Magnesium stress signaling in plant: just a beginning. Plant Signal Behav 10 (3): e992287. https://doi.org/10.4161/15592324.2014.992287

Gupta UC, Lipsett J, 1981. Molybdenum in soils, plants, and animals. Adv Agron 34: 73-115. https://doi.org/10.1016/S0065-2113(08)60885-8

Haneklaus S, Bloem E, Schung E, de Kok LJ, Stulen I, 2007. Sulfur. In: Handbook of plant nutrition; Barker AV, Pilbeam DJ (eds.). pp. 183-238. CRC Press, Taylor & Francis Group, Boca Raton, FL, USA.

Hochmal AK, Schulze S, Trompelt K, Hippler M, 2015. Calcium-dependent regulation of photosynthesis. Biochim Biophys Acta 1847: 993-1003. https://doi.org/10.1016/j.bbabio.2015.02.010

Huang XY, Salt DE, 2016. Plant ionomics: from elemental profiling to environmental adaptation. Mol Plant 9: 787-797. https://doi.org/10.1016/j.molp.2016.05.003

Humpries JM, Stangoulis JCR, Graham RD, 2007. Manganese. In: Handbook of plant nutrition; Barker AV, Pilbeam DJ (eds.). pp. 351-374. CRC Press, Taylor & Francis Group, Boca Raton, FL, USA.

Impa SM, Morete MJ, Ismail AM, Schulin R, Johnson-Beebout SE, 2013. Zn uptake, translocation, and grain Zn loading in rice (Oryza sativa L.) genotypes selected for Zn deficiency tolerance and high grain Zn. J Exp Bot 64: 2739-2751. https://doi.org/10.1093/jxb/ert118

Kirkby EA, Pilbeam DJ, 1984. Calcium as a plant nutrient. Plant Cell Environ 7: 397-405. https://doi.org/10.1111/j.1365-3040.1984.tb01429.x

Kobayashi NI, Tanoi K, 2015. Critical issues in the study of magnesium transport systems and magnesium deficiency symptoms in plants. Int J Mol Sci 16: 23076-23093. https://doi.org/10.3390/ijms160923076

Kopriva S, Calderwood A, Weckopp SC, Koprivova A, 2015. Plant sulfur and Big Data. Plant Sci 241: 1-10. https://doi.org/10.1016/j.plantsci.2015.09.014

Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith AC, 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379: 635-638. https://doi.org/10.1038/379635a0

Kumar J, Sen Gupta D, Kumar S, Gupta S, Singh NP, 2016. Current knowledge on genetic biofortification in lentil. J Agric Food Chem 64: 6383-6396. https://doi.org/10.1021/acs.jafc.6b02171

Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G, 2004. Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430: 803-806. https://doi.org/10.1038/nature02681

Lobréaux S, Briat JF, 1991. Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J 274: 601-606. https://doi.org/10.1042/bj2740601

Loneragan JF, 1988. Distribution and movement of manganese in plants. In: Manganese in soils and plants; Graham RD, Hannam RJ, Uren NC (eds.). pp. 113-121. Kluwer Acad Publ, Dordrecht. https://doi.org/10.1007/978-94-009-2817-6_9

Luan M, Tang RJ, Tang Y, Tian W, Hou C, Zhao F, Lan W, Luan S, 2016. Transport and homeostasis of potassium and phosphate: limiting factors for sustainable crop production. J Exp Bot: erw444. https://doi.org/10.1093/jxb/erw444.

Marschner H, 1995. Mineral nutrition of higher plants, 2nd edn. Academic Press, London.

Martre P, Porter JR, Jamieson PD, Triböi E, 2003. Modeling grain nitrogen accumulation and protein composition to understand the sink/source regulation of nitrogen remobilization for wheat. Plant Physiol 133: 1959-1967. https://doi.org/10.1104/pp.103.030585

Mengel K, Secer M, Koch K, 1981. Potassium effect on protein formation and amino acid turnover in developing wheat grain. Agron J 73: 74-78. https://doi.org/10.2134/agronj1981.00021962007300010018x

Obata H, Kawamura S, Senoo K, Tanaka A, 1999. Changes in the level of protein and activity of Cu/Zn-superoxide dismutase in zinc deficient rice plant, Oryza sativa L. Soil Sci Plant Nutr 45: 891-896. https://doi.org/10.1080/00380768.1999.10414338

Ouzounidou G, Ilias I, Tranopoulou H, Karatglis S, 1998. Amelioration of copper toxicity by iron on spinach physiology. J Plant Nutr 21: 2089-2101. https://doi.org/10.1080/01904169809365546

Ozturk L, Yazici MA, Yucel C, Torun A, Cekic C, Bagci A, Ozkan H, Braun HJ, Sayers Z, Cakmak I, 2006. Concentration and localization of zinc during seed development and germination in wheat. Physiol Plant 128: 144-152. https://doi.org/10.1111/j.1399-3054.2006.00737.x

Palmgren MG, Clemens D, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D, 2008. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13: 464-473. https://doi.org/10.1016/j.tplants.2008.06.005

Parida BK, Chhibba IM, Nayyar VK, 2003. Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci Hort 98: 113-119. https://doi.org/10.1016/S0304-4238(02)00208-X

Pearson JN, Rengel Z, 1994. Distribution and remobilization of Zn and Mn during grain development in wheat. J Exp Bot 45: 1829-1835. https://doi.org/10.1093/jxb/45.12.1829

Pederson GA, Brink GE, Fairbrother TE, 2002. Nutrient uptake in plant parts of sixteen forages fertilized with poultry litter: Nitrogen, phosphorus, potassium, copper, and zinc. Agron J 94: 895-904. https://doi.org/10.2134/agronj2002.8950

Polacco JC, Mazzafera P, Tezotto T, 2013. Opinion - Nickel and urease in plants: still many knowledge gaps. Plant Sci 199-200: 79-90. https://doi.org/10.1016/j.plantsci.2012.10.010

Puig S, Andrés-Colás N, García-Molina A, Peñarrubia L, 2007. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ 30: 271-290. https://doi.org/10.1111/j.1365-3040.2007.01642.x

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

Ramani S, Kannan S, 1987. Manganese absorption and transport in rice. Physiol Plant 33: 133-137. https://doi.org/10.1111/j.1399-3054.1975.tb03780.x

Ricachenevsky FK, Menguer PK, Sperotto RA, Fett JP, 2015. Got to hide your Zn away: molecular control of Zn accumulation and biotechnological applications. Plant Sci 236: 1-17. https://doi.org/10.1016/j.plantsci.2015.03.009

Römheld V, Nikolic M, 2007. Iron. In: Handbook of plant nutrition; Barker AV, Pilbeam DJ (eds.). pp. 329-350. CRC Press, Taylor & Francis Group, Boca Raton, FL, USA.

Ruano A, Barcelo J, Poshcenrieder C, 1987. Zinc toxicity-induced variation of mineral element composition in hydroponically grown bush bean plants. J Plant Nutr 10: 373-384. https://doi.org/10.1080/01904168709363579

Schmidt SB, Jensen PE, Husted S, 2016. Manganese deficiency in plants: the impact on Photosystem II. Trends Plant Sci 21: 622-632. https://doi.org/10.1016/j.tplants.2016.03.001

Shin R, 2014. Strategies for improving potassium use efficiency in plants. Mol Cells 37: 575-584. https://doi.org/10.14348/molcells.2014.0141

Silveira VC, Oliveira AP, Sperotto RA, Espindola LS, Amaral L, Dias JF, Cunha JB, Fett JP, 2007. Influence of iron on mineral status of two rice (Oryza sativa L.) cultivars. Braz J Plant Physiol 19: 127-139. https://doi.org/10.1590/S1677-04202007000200005

Simmons RW, Pongsakul P, Chaney RL, Saiyasitpanich D, Klinphoklap S, Nobuntou W, 2003. The relative exclusion of zinc and iron from rice grain in relation to rice grain cadmium as compared to soybean: Implications for human health. Plant Soil 257: 163-170. https://doi.org/10.1023/A:1026242811667

Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, VandenBerg PJ, Belcher AR, Warrilow GS, 1997. Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 12: 875-884. https://doi.org/10.1046/j.1365-313X.1997.12040875.x

Socha AL, Guerinot ML, 2014. Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci 5: 106. https://doi.org/10.3389/fpls.2014.00106

Sperotto RA, 2013. Zn/Fe remobilization from vegetative tissues to rice seeds: should I stay or should I go? Ask Zn/Fe supply! Front Plant Sci 4: 464. https://doi.org/10.3389/fpls.2013.00464

Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP, 2009. Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230: 985-1002. https://doi.org/10.1007/s00425-009-1000-9

Sperotto RA, Ricachenevsky FK, Stein RJ, Waldow VA, Fett JP, 2010. Iron stress in plants: dealing with deprivation and overload. Plant Stress 4: 57-69.

Sperotto RA, Ricachenevsky FK, Waldow VA, Fett JP, 2012a. Iron biofortification in rice: it's a long way to the top. Plant Sci 190: 24-39. https://doi.org/10.1016/j.plantsci.2012.03.004

Sperotto RA, Vasconcelos MW, Grusak MA, Fett JP, 2012b. Effects of different Fe supplies on mineral partitioning and remobilization during the reproductive development of rice (Oryza sativa L.). Rice 5: 27. https://doi.org/10.1186/1939-8433-5-27

Sperotto RA, Ricachenevsky FK, Waldow VA, Müller ALH, Dressler VL, Fett JP, 2013. Rice grain Fe, Mn and Zn accumulation: how important are flag leaves and seed number? Plant Soil Environ 59: 262-266.

Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K, 2000. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23: 171-182. https://doi.org/10.1046/j.1365-313x.2000.00768.x

Very AA, Sentenac H, 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54: 575-603. https://doi.org/10.1146/annurev.arplant.54.031902.134831

Waters BM, Grusak MA, 2008. Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol 177: 389-405.

Wu C, Lu L, Yang X, Feng Y, Wei Y, Hao HL, et al., 2010. Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J Agric Food Chem 58: 6767-6773. https://doi.org/10.1021/jf100017e

Yang X, Baligar VC, Martens DC, Clark R, 1996. Plant tolerance to nickel toxicity: II. Nickel effects on influx and transport of mineral nutrients in four plant species. J Plant Nutr 19: 265-279. https://doi.org/10.1080/01904169609365121

Yusuf M, Fariduddin Q, Hayat S, Ahmad A, 2011. Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86: 1-17. https://doi.org/10.1007/s00128-010-0171-1

Zeng YW, Shen SQ, Wang LX, Liu JF, Pu XY, Du J, Qiu M, 2005. Correlation of plant morphological and grain quality traits with mineral element contents in Yunnan rice. Rice Sci 12: 101-106.

DOI: 10.5424/sjar/2017152-10332