Mechanisms of copper stress alleviation in Citrus trees after metal uptake by leaves or roots
Tóm tắt
Nutritional disorders caused by copper (Cu) have affected citrus orchards. Since Cu is foliar sprayed as a pesticide to control citrus diseases, this metal accumulates in the soil. Thereby, we evaluated the effects of Cu leaf absorption after spray of different metal sources, as well as roots absorption on growth, nutritional status, and oxidative stress of young sweet orange trees. Two experiments were carried out under greenhouse conditions. The first experiment was set up with varying Cu levels to the soil (nil Cu, 0.5, 2.0, 4.0 and 8.0 g of Cu per plant as CuSO4.5H2O), whereas the second experiment with Cu application via foliar sprays (0.5 and 2.0 g of Cu per plant) and comparing two metal sources (CuSO4.5H2O or Cu(OH)2). Copper was mainly accumulated in roots with soil supply, but an increase of oxidative stress levels was observed in leaves. On the other hand, Cu concentrations were higher in leaves that received foliar sprays, mainly as Cu(OH)2. However, when sulfate was foliar sprayed, plants exhibited more symptoms of injuries in the canopy with decreased chlorophyll contents and increased hydrogen peroxide and lipid peroxidation levels. Copper toxicity was characterized by sap leakage from the trunk and twigs, which is the first report of this specific Cu excess symptom in woody trees. Despite plants with 8.0 g of Cu soil-applied exhibiting the sap leakage, growth of new plant parts was more vigorous with lower oxidative stress levels and injuries compared to those with 4.0 g of Cu soil-applied (without sap leakage). With the highest level of Cu applied via foliar as sulfate, Cu was eliminated by plant roots, increasing the rhizospheric soil metal levels. Despite citrus likely exhibiting different mechanisms to reduce the damages caused by metal toxicity, such as responsive enzymatic antioxidant system, metal accumulation in the roots, and metal exclusion by roots, excess Cu resulted in damages on plant growth and metabolism when the metal was taken up either by roots or leaves.
Tài liệu tham khảo
Alva AK, Chen EQ (1995) Effects of external copper concentrations on uptake of trace elements by citrus seedlings. Soil Sci 159:59–64
Alexieva V, Sergiev I, Mapelli E, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and trees markers in pea and wheat. Plant Cell Environ 24:1337–1344
Andrade SAL, Gratão PL, Azevedo RA, Silveira APD, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207
Andrés-Bordería A, Andrés F, Garcia-Molina A, Perea-García A, Domingo C, Puig S, Peãrrubia L (2017) Copper ectopic expression of the Arabidopsis transport protein COPT1 alter iron homeostasis in rice (Oryza sativa L.) Plant Mol Biol. https://doi.org/10.1007/s11103-017-0622-8
Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air ozone fumigation, in leaves and roots of wild-type and catalase-deficient mutant of barley. Physiol Plant 104:280–292
Bakshi S, He ZL, Harris WG (2013) Particulate copper in soils and surface runoff from contaminated sandy soils under citrus production. Environ Sci Pollut Res 20:8801–8812
Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100
Bataglia OC, Furlani AMC, Teixeira JPF, Furlani PR, Gallo JR (1983) Métodos de análise química de plantas. IAC, Campinas
Beauchamp CH, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Behlau F, Belasque Junior J, Graham JH, Leite Junior RP (2010) Effect of frequency of copper applications on control of citrus canker and yield of young bearing sweet orange trees. Crop Prot 29:300–305
Behlau F, Scandelai LH, Silva Junior GJ, Lanza FE (2017) Soluble and insoluble copper formulations and metallic copper rate for control of citrus canker on sweet orange trees. Crop Prot 94:185–191
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principles of protein dye-binding. Anal Biochem 72:248–254
Bradl HB (2004) Adsorption of heavy metal ions on soils and soils constituents. J Colloid Interface Sci 27:1–18
Bulgarelli RG, Araujo P, Tezotto T, Mazzafera P, Andrade SAL (2016) Expression of metallothionein genes in coffee leaves in response to the absence or excess of cu and Zn. Theor Exp Plant Physiol 28:371–383
Deinlein U, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Krämer U, Clemens S (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24:708–723
Del Rio LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837
Fan J, He Z, Ma LQ, Stoffella PJ (2011) Accumulation and availability of copper in citrus grove soils as affected by fungicide application. J Soils Sediments 11:639–648
Fontes MPF, Gomes PC (2003) Simultaneous competitive adsorption of heavy metals by the mineral matrix of tropical soils. Appl Geochem 18:795–804
Gama F, Saavedra T, Diaz I, Campillo MC, Varennes A, Duarte A, Pestana M, Correia PJ (2015) Fe deficiency induction in Poncirus trifoliata rootstock growing in nutrient solution changes its performance after transplant to soil. Sci Hort 182:102–109
Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peres LEP, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816
Hippler FWR, Boaretto RM, Dovis VL, Quaggio JA, Azevedo RA, Mattos-Jr D (2018) Oxidative stress induced by Cu nutritional disorders in Citrus depends on nitrogen and calcium availability. Sci Rep 8:1641
Hippler FWR, Boaretto RM, Quaggio JA, Boaretto AE, Abreu-Junior CH, Mattos-Jr D (2015) Uptake and distribution of soil applied zinc by Citrus trees—addressing fertilizer use efficiency with 68Zn labelling. PLoS One 10:e0116903
Hippler FWR, Cipriano DO, Boaretto RM, Quaggio JA, Gaziola SA, Azevedo RA, Mattos-Jr D (2016) Citrus rootstocks regulate the enzymatic and nutritional status and antioxidant system of trees under copper stress. Environ Exp Bot 130:42–52
Hippler FWR, Reis IMS, Boaretto RM, Quaggio JA, Mattos-Jr D (2014) Características adsortivas de solos e o suprimento de zinco e manganês para os citros. Citrus Res Technol 35:73–83
Husak V (2015) Copper and copper-containing pesticides: metabolism, toxicity and oxidative stress. J Vasyl Stefanyk Precarpathian National University 2:38–50
Komárek M, Vanekb A, Chrastny V, Száková J, Kubová K, Drahotad P, BalíK J (2009) Retention of copper originating from different fungicides in contrasting soil types. J Hazard Mat 166:1395–1402
Kováčik J, Klejdus B, Hedbavny J, Štork F, Bačkor M (2009) Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant Soil 320:231–242
Kraus TE, Mckersie BD, Fletcher RA (1995) Paclobutrazol-induced tolerance of wheat leaves to paraquat may involve increased antioxidant enzyme activity. J Plant Physiol 145:570–576
López-Climent MF, Arbona V, Pérez-Clemente RM, Zandalinas I, Gómez-Cadenas A (2014) Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biol 16:79–87
Lyubenova L, Bipuah H, Belford E, Michalke B, Winkler B, Schröder P (2015) Comparative study on the impact of copper sulphate and copper nitrate on the detoxification mechanisms in Thypha latifolia. Environ Sci Pollut Res 22:657–666
Lyubenova L, Kuhn AJ, Höltkemeier A, Schröder P (2013) Root exudation pattern of Typha latifolia L. plants after copper exposure. Plant Soil 370:187–195
Martins V, Texeira A, Bassil E, Hanana M, Blumwald E, Geros H (2014) Metabolic changes of Vitis vinifera berries and leaves exposed to Bordeaux mixture. Plant Physiol Biochem 82:270–278
Mattos-Jr D, Ramos UM, Quaggio JA, Furlani PR (2010) Nitrogênio e cobre na produção de mudas de citros em diferentes porta-enxertos. Bragantia 69:135–147
Mouta ER, Soares MR, Casagrande JC (2008) Copper adsorption as a function of solution parameters of variable charge soils. J Braz Chem Soc 19:996–1009
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
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
van Raij B, Alcarde JC, Cantarella H, Quaggio JA (2001) Análise química para avaliação da fertilidade de solos tropicais. IAC, Campinas
Sereno ML, Almeida RS, Nishimura DS, Figueira A (2007) Response of sugarcane to increasing concentrations of copper and cadmium and expression of metallothionein genes. J Plant Physiol 164:1499–1515
Silva Jr GJ, Scapin MS, Silva FP, Silva ARP, Behlau F, Ramos HH (2016) Spray volume and fungicide rates for citrus black spot control based on tree canopy volume. Crop Prot 85:38–45
Smoleń S (2012) Foliar nutrition: current state of knowledge and opportunities. In: Srivastava AK (ed) Advances in Citrus nutrition. Springer, Amsterdam, pp 41–58
Sonmez S, Kaplan M, Sonmez NK, Kaya H, Uz I (2006) High level of copper application to soil and leaves reduce the growth and yield of tomato plants. Sci Agric 63:213–218
Sposito G (1982) On the Langmuir equation in the interpretation of adsorption phenomena. II. The two-surface Langmuir equation. Soil Sci Soc Am J 46:1174–1252
Syvertsen JP, Garcia-Sanchez F (2014) Multiple abiotic stresses occurring with salinity stress in citrus. Environ Exp Bot 103:128–137
Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633
Waters BM, Armbrust LC (2013) Optimal copper supply is required for normal plant iron deficiency responses. Plant Signal Behav 8:e26611
Yruela I (2013) Transition metals in plant photosynthesis. Metallomics 5:1090–1109
Zlobin IE, Kholodova VP, Rakhmankulova ZF, Kuznetsov VV (2015) Brassica napus responses to short-term excessive copper treatment with decrease of photosynthetic pigments, differential expression of heavy metal homeostasis genes including activation of gene NRAMP4 involved in photosystem II stabilization. Photosynth Res 125:141–150