Ploidy level of citrus rootstocks affects the carbon and nitrogen metabolism in the leaves of Chromium-stressed Kinnow mandarin plants

ATSDR (Agency for Toxic Substances and Disease Registry), 1998 Ali, 2015, Alleviation of chromium toxicity by glycine-betaine is related to elevated antioxidant enzymes and suppressed chromium uptake and antioxidative stress in wheat (Triticum aestivum L.), Environ. Sci. Pollut. Res., 22, 10669, 10.1007/s11356-015-4193-4 Allario, 2013, Tetraploid rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production, Plant Cell Environ., 36, 856, 10.1111/pce.12021 Alloway, 2013, 97 Ansari, 2013, An-overview on invertase in sugarcane, Bioinformation, 9, 464, 10.6026/97320630009464 Arabzadeh, 2012, The effect of drought stress on soluble carbohydrates (sugars) in two species of Haloxylon persicum and Haloxylon aphyllum, Asian J. Plant Sci., 11, 44, 10.3923/ajps.2012.44.51 Balal, 2017, Kinnow mandarin plants grafted on tetraploid rootstocks are more tolerant to Cr-toxicity than those grafted on its diploids one, Environ. Exp. Bot., 140, 8, 10.1016/j.envexpbot.2017.05.011 Bird, 1974, Intracellular site of sucrose synthesis in leaves, Phytochemistry, 13, 59, 10.1016/S0031-9422(00)91267-6 Bittsanszky, 2015, Overcoming ammonium toxicity, Plant Sci., 231, 184, 10.1016/j.plantsci.2014.12.005 Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 Buysse, 1993, An improved colorimetric method to quantify sugar content of plant tissue, J. Exp. Bot., 44, 1627, 10.1093/jxb/44.10.1627 Cataldo, 1975, Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid, Commun. Soil Sci. Anal., 6, 71, 10.1080/00103627509366547 Da-Costa, 2016, Effect of chromium oxide (III) nanoparticles on the production of reactive oxygen species and photosystem II activity in the green alga Chlamydomonas reinhardtii, Sci. Total Environ., 565, 951, 10.1016/j.scitotenv.2016.01.028 Das, 2017, Metabolomic profiling of soybeans (Glycine max L.) reveals the importance of sugar and nitrogen metabolism under drought and heat stress, Plants, 6, 1, 10.3390/plants6020021 Dias, 2013, Cadmium toxicity affects photosynthesis and plant growth at different levels, Acta Physiol. Plant., 35, 1281, 10.1007/s11738-012-1167-8 Fiasconaro, 2012, Effects of nitrogen source and water availability on stem carbohydrates and cellulosic bioethanol traits of alfalfa plants, Plant Sci., 192, 16, 10.1016/j.plantsci.2012.04.007 Froelicher, 2008, Characterization of microsatellite markers in mandarin orange (Citrus reticulata Blanco), Mol. Ecol. Res., 8, 119, 10.1111/j.1471-8286.2007.01893.x Giagnonia, 2016, Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency, Appl. Soil Ecol., 98, 30, 10.1016/j.apsoil.2015.09.004 Gill, 2015, Chromium-induced physio-chemical and ultra structural changes in four cultivars of Brassica napus L, Chemosphere, 120, 154, 10.1016/j.chemosphere.2014.06.029 Gupta, 2005, Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants, J. Biosci., 30, 761, 10.1007/BF02703574 Gupta, 2014, MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives, Plant Mol. Biol., 84, 1, 10.1007/s11103-013-0120-6 Habran, 2016, Roostocks/scion/nitrogen interactions affect secondary metabolism in the grape berry, Front. Plant Sci., 7, 1134, 10.3389/fpls.2016.01134 Hamid, 2012, Chromium stress in Brassica juncea L. cv. ‘Pusa Jai Kissan’ under hydroponic culture, Afr. J. Biotechnol., 90, 15658 Jasso-Chávez, 2010, Toxic effects of Cr(VI) and Cr(III) on energy metabolism of heterotrophic Euglena gracilis, Aquatic toxicol., 100, 329, 10.1016/j.aquatox.2010.08.006 Jones, 1977, Enzymic assay of 107 to 1014 moles of sucrose in plant tissues, Plant Physiol., 60, 379, 10.1104/pp.60.3.379 Jun, 2009, Effects of chromium on seed germination, root elongation and coleoptile growth in six pulses, Int. J. Environ. Sci. Tech., 6, 571, 10.1007/BF03326097 Karve, 2012, Arabidopsis hexokinase-like1 and hexokinase1 form a critical node in mediating plant glucose and ethylene responses, Plant Physiol., 158, 1965, 10.1104/pp.112.195636 Khan, 2001, Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent polluted soil, Environ. Int., 26, 417, 10.1016/S0160-4120(01)00022-8 Krasensky, 2012, Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks, J. Exp. Bot., 63, 1593, 10.1093/jxb/err460 Kumar, 2008, Nitrogen metabolism as affected by hexavalent chromium in sorghum (Sorghum bicolor L.), Environ. Exp. Bot., 64, 135, 10.1016/j.envexpbot.2008.02.005 Kumari, 2015, Grafting triggers differential responses between scion and rootstock, PLoS One, 10, 1, 10.1371/journal.pone.0124438 Lillo, 1984, Diurnal variations of nitrite reductase, glutamine synthetase, glutamate synthase, alanine amino transferase and aspartate amino transferase in barley leaves, Physiol. Plant, 61, 214, 10.1111/j.1399-3054.1984.tb05899.x Linero, 2015, Accumulation and translocation of essential and nonessential elements by tomato plants (Solanum lycopersicum) cultivated in open-air plots under organic or conventional farming techniques, J. Agric. Food Chem., 63, 9461, 10.1021/acs.jafc.5b03878 Lowell, 1989, Sucrose-metabolizing enzymes in transport tissues and adjacent sink structures in developing citrus fruit, Plant Physiol., 90, 1394, 10.1104/pp.90.4.1394 Lukina, 2016, Evaluating trivalent chromium toxicity on wild terrestrial and wetland plants, Chemosphere, 162, 355, 10.1016/j.chemosphere.2016.07.055 Luro, 2008, Transferability of the EST-SSRs developed on Nules clementine (Citrus clementina Hort ex Tan) to other citrus species and their effectiveness for genetic mapping, BMC Genomics, 9, 1, 10.1186/1471-2164-9-287 Ma, 2016, Beneficial role of bacterial endophytes in heavy metal phytoremediation, J. Environ. Manag., 174, 14, 10.1016/j.jenvman.2016.02.047 Miflin, 2002, The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops, J. Exp. Bot., 53, 979, 10.1093/jexbot/53.370.979 Molins-Legua, 2006, Aguide for selecting the most appropriate method for ammonium determination in water analysis, Trends Anal. Chem., 20, 282, 10.1016/j.trac.2005.12.002 Mustafa, 2016, Toxicity of heavy metals and metal-containing nanoparticles on plants, Biochem. Biophys. Acta, 8, 932 Nichols, 2000, Selected physiological responses of Salvinia minima to different chromium concentrations, Aquat. Bot., 11, 313, 10.1016/S0304-3770(00)00128-5 Oliveira, 2012, Chromium as an environmental pollutant: insights on induced plant toxicity, J. Bot., 3, 1 Pawlisz, 1997, Canadian water quality guidelines for chromium, Environ. Toxic. Water, 12, 185, 10.1002/(SICI)1098-2256(1997)12:2<123::AID-TOX4>3.0.CO;2-A Penella, 2016, Salt-tolerant rootstock increases yield of pepper under salinity through maintenance of photosynthetic performance and sinks strength, J. Plant Physiol., 193, 1, 10.1016/j.jplph.2016.02.007 Prado, 2010, Seasonal variability of physiological and biochemical aspects of chromium accumulation in outdoor-grown Salvinia minima, Chemosphere, 81, 584, 10.1016/j.chemosphere.2010.08.033 Raju, 1999, Operationally determined speciation of chromium in tannery sludges, Chem. Speciat. Bioavailab., 11, 67, 10.3184/095422999782775717 Ramarao, 1983, A simple in vivo method for the determination of nitrite reductase activity in rice roots, Zentrum Pflanzen Physiol., 109, 81, 10.1016/S0044-328X(83)80175-5 Reale, 2016, Cyto-histological and morpho-physiological responses of common duckweed (Lemna minor L.) to chromium, Chemosphere, 145, 98, 10.1016/j.chemosphere.2015.11.047 Rodriguez, 2011, Cr (VI) induces DNA damage, cell cycle arrest and polyploidization: a flow cytometric and comet assay study in Pisum sativum, Chem. Res. Toxicol., 24, 1040, 10.1021/tx2001465 Rufty, 1983, Changes in starch formation and activities of sucrose phosphate synthase and cytoplasmic fructose-1, 6-bisphosphatase in response to source-sink alterations, Plant Physiol., 72, 474, 10.1104/pp.72.2.474 Ruiz, 2016, Tetraploidy enhances boron-excess tolerance in carrizo citrange (Citrus sinensis L. Osb. × Poncirus trifoliata L. Raf.), Front. Plant Sci., 7, 701, 10.3389/fpls.2016.00701 Saleh, 2008, Tetraploid citrus rootstocks are more tolerant to salt stress than diploid, C. R. Biologies, 331, 703, 10.1016/j.crvi.2008.06.007 Sangwan, 2014, Effect of Chromium(VI) toxicity on enzymes of nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.), Enzyme Res., 2014, 784036, 10.1155/2014/784036 Sevcikova, 2017, Carbohydrates and gibberellins relationship in potato tuberization, J. Plant Physiol., 214, 53, 10.1016/j.jplph.2017.04.003 Shanker, 2009, Chromium interactions in plants: current status and future strategies, Metallomics, 1, 375, 10.1039/b904571f Singh, 1983, Regulation of glutamate dehydrogenase activity by amino acids in maize seedlings, Physiol. Plant., 57, 549, 10.1111/j.1399-3054.1983.tb02784.x Singh, 1986, Increase in glutamate synthase (NADH) activity in maize seedlings in response to nitrate and ammonium nitrogen, Physiol. Plant., 66, 413, 10.1111/j.1399-3054.1986.tb05944.x Singh, 2013, Chromium toxicity and tolerance in plants, Environ. Chem. Lett., 11, 229, 10.1007/s10311-013-0407-5 Singh, 2016, Nitrogen modifies NaCl toxicity in eggplant seedlings: assessment of chlorophyll a fluorescence, antioxidative response and proline metabolism, Biocatal. Agric. Biotechnol., 7, 76, 10.1016/j.bcab.2016.05.007 Skopelitis, 2006, Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine, Plant Cell, 18, 2767, 10.1105/tpc.105.038323 Snell, 1949, 804 Sym, 1984, Optimization of the in vivo assay conditions for nitrate reductase in barley (Hordeum vulgare L. cv. irgri), J. Food Sci. Agric., 35, 725, 10.1002/jsfa.2740350703 Taibi, 2016, Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L, South Afr. J. Bot., 105, 306, 10.1016/j.sajb.2016.03.011 Tan, 2015, Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement, BMC Plant Biol., 15, 89, 10.1186/s12870-015-0450-4 Tan, 2017, Metabolic adaptation following genome doubling in citrus doubled diploids revealed by non-targeted metabolomics, Metabolomics, 13, 143, 10.1007/s11306-017-1276-x Tian, 2015, Quantitative assessment of atmospheric emissions of toxic heavy metals from anthropogenic sources in China: historical trend spatial distribution, uncertainties, and control policies, J. Atmos. Chem. Phys., 15, 10127, 10.5194/acp-15-10127-2015 Tiwari, 2009, Chromium (VI) induced phytotoxicity and oxidative stress in pea (Pisum sativum L.): biochemical changes and translocation of essential nutrients, J. Environ. Biol., 30, 389 Vega, 2016, Hexokinase-2 is an intracellular glucose sensor of yeast cells that maintains the structure and activity of Mig1 repressor complex, J. Biol. Chem., 291, 7267, 10.1074/jbc.M115.711408 Viti, 2014, Molecular mechanisms of Cr(VI) resistance in bacteria and fungi Carlo, FEMS Microbiol. Rev., 38, 633, 10.1111/1574-6976.12051 Vollenweider, 2006, Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.) Part II Microlocalization and cellular effects of cadmium, Environ. Exp. Bot., 58, 25, 10.1016/j.envexpbot.2005.06.012 Zrenner, 1995, Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.), Plant J., 7, 97, 10.1046/j.1365-313X.1995.07010097.x