Manganese toxicity and UV-B radiation differentially influence the physiology and biochemistry of highbush blueberry (Vaccinium corymbosum) cultivars
Yesenia Rojas-Lillo A B , Miren Alberdi B C , Patricio Acevedo D E , Claudio Inostroza-Blancheteau B F , Zed Rengel G , Maria de la Luz Mora B C and Marjorie Reyes-Díaz B C H
+ Author Affiliations
- Author Affiliations
A Programa de Doctorado y Magíster en Recursos de Ciencias Naturales, Universidad de La Frontera, PO Box 54-D, Temuco, Chile.
B Center of Plant–Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, PO Box 54-D, Temuco, Chile.
C Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería Ciencias y Administración, Universidad de La Frontera, PO Box 54-D, Temuco, Chile.
D Departamento de Ciencias Físicas, Facultad de Ingeniería, Ciencias y Administración, Universidad de La Frontera, PO Box 54-D, Temuco, Chile.
E Center for Optics and Photonics, Universidad de Concepción, PO Box 4016, Concepción, Chile.
F Núcleo de Investigación en Producción Alimentaria, Facultad de Recursos Naturales, Escuela de Agronomía, Universidad Católica de Temuco, PO Box 56-D, Temuco, Chile.
G Soil Science and Plant Nutrition, School of Earth and Environment, The University of Western Australia, Crawley, WA 6009, Australia.
H Corresponding author. Email: marjorie.reyes@ufrontera.cl
Functional Plant Biology 41(2) 156-167 https://doi.org/10.1071/FP12393
Submitted: 27 December 2012 Accepted: 15 July 2013 Published: 30 September 2013
Abstract
Manganese (Mn2+) toxicity or UV-B radiation and their individual effects on plants have been documented previously. However, no study about the combined effect of these stresses is available. We evaluated the individual and combined effects of excess Mn2+ and UV-B radiation on physiological and biochemical parameters in two highbush blueberry (Vaccinium corymbosum L.) cultivars differing in resistance to Mn toxicity (Brigitta (resistant) and Bluegold (sensitive)). Plants grown in Hoagland nutrient solution were subjected to the following treatments: 2 µM MnCl2 (control), 500 µM MnCl2 (toxic Mn2+), UV-B radiation (a daily dose of 94.4 kJ m–2), and the combined treatment (toxic Mn2+ + UV-B) for 30 days. In both cultivars, the Mn2+ + UV-B treatment caused a more negative effect on net photosynthesis (Pn), stomatal conductance (gs), the photochemical parameters of PSII and the chl a/b ratio than the treatments with toxic Mn2+ or UV-B alone. However, Brigitta showed also a better acclimation response in Pn and gs than Bluegold at the end of the experiment. The Mn2+ + UV-B treatment inhibited growth, enhanced radical scavenging activity and superoxide dismutase activity, and increased the concentration of total UV-absorbing compounds, phenols and anthocyanins, mainly in Bluegold. In conclusion, Mn-resistant Brigitta showed a better acclimation response and greater resistance to the combined stress of Mn2+ toxicity and UV-B exposure than the Mn-sensitive Bluegold. An increased concentration of photoprotective compounds and enhanced resistance to oxidative stress in Brigitta could underpin increased resistance to the combined stress.
Additional keywords: antioxidants; phenols, photosynthesis, photochemical efficiency of PSII; photosynthetic pigments, stomatal conductance.
References
Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54, 41–49.| Photoprotective strategies of overwintering evergreens.Crossref | GoogleScholarGoogle Scholar |
Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytologist 186, 786–793.
| Multiple functional roles of flavonoids in photoprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWhtLc%3D&md5=77ac74ff74530ccd55b27ab5a0089de5CAS | 20569414PubMed |
Agrawal SB, Mishra S (2009) Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L. Ecotoxicology and Environmental Safety 72, 610–618.
| Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaqur%2FE&md5=ffbd8a4276df5a6692a5100733f4de7bCAS | 18061671PubMed |
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
| Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSlsL4%3D&md5=03ee994bf3de3fd6d70534d6ed7a688fCAS | 11997379PubMed |
Arya SK, Roy BK (2011) Manganese induced changes in growth, chlorophyll content and antioxidants activity in seedlings of broad bean (Vicia faba L.). Journal of Environmental Biology 32, 707–711.
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
| Production and scavenging of reactive oxygen species in chloroplasts and their functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksbY%3D&md5=0a8de50ebf385debd1de530b72d61f2bCAS | 16760493PubMed |
Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R (2010) Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterol. Plant, Cell & Environment 33, 1–10.
| Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlOqsL0%3D&md5=0bc8829bfca78ebf64b63e7cce33447bCAS |
Bilger W, Johnsen T, Schreiber U (2001) UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. Journal of Experimental Botany 52, 2007–2014.
| UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1Wkt70%3D&md5=e672d999b27391c20b30d7d53e123f5fCAS | 11559736PubMed |
Blokhina O, Virolainen E, Fagestedt KV (2003) Antioxidants, oxidative damage, and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
| Antioxidants, oxidative damage, and oxygen deprivation stress: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCksbw%3D&md5=7eb817ec347d1442f49f210c3a527914CAS | 12509339PubMed |
Boojar MM, Goodarzi F (2007) The copper tolerance strategies and the role of antioxidative enzymes in three plant species grown on copper mine. Chemosphere 67, 2138–2147.
| The copper tolerance strategies and the role of antioxidative enzymes in three plant species grown on copper mine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVGjtLo%3D&md5=58f2fe2e7fd84641ef9e0c67f10de297CAS | 17316756PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS | 942051PubMed |
Burchard P, Bilger W, Weissenböck G (2000) Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant, Cell & Environment 23, 1373–1380.
| Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlyktQ%3D%3D&md5=59d70614657b3df09bf259d75af98abfCAS |
Cadwell MM, Flint SD (1997) Uses of biological spectral weighting functions and the need of scaling for the ozone reduction problem. Plant Ecology 128, 66–76.
| Uses of biological spectral weighting functions and the need of scaling for the ozone reduction problem.Crossref | GoogleScholarGoogle Scholar |
Chen LS, Qi YP, Liu XH (2005) Effects of aluminum on light energy utilization and photoprotective systems in citrus leaves. Annals of Botany 96, 35–41.
| Effects of aluminum on light energy utilization and photoprotective systems in citrus leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnsVejt7w%3D&md5=0c99c9450dffdbd63f1d11d33d287339CAS | 15829508PubMed |
Chinnici F, Bendini A, Gaiani A, Riponi C (2004) Radical scavenging activities of peels and pulps from cv. Golden delicious apples as related to their phenolic composition. Journal of Agricultural and Food Chemistry 52, 4684–4689.
| Radical scavenging activities of peels and pulps from cv. Golden delicious apples as related to their phenolic composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlCmsL0%3D&md5=ff84896ecc754f32af647269d817ec59CAS | 15264900PubMed |
Day TA (1993) Relating UV-B radiation screening effectiveness of foliage to absorbing-compound concentration and anatomical characteristics in a diverse group of plants. Oecologia 95, 542–550.
| Relating UV-B radiation screening effectiveness of foliage to absorbing-compound concentration and anatomical characteristics in a diverse group of plants.Crossref | GoogleScholarGoogle Scholar |
De los Ríos P, Acevedo P (2010) Effects of natural ultraviolet radiation exposure in inland water ecosystems of Chilean Patagonia. In ‘Photobiology: principles, applications and effects’. (Eds L. N. Collignon and C. B. Normand) pp. 195–207. (Nova Science Publishers: Hauppauge, NY)
De los Ríos P, Hauenstein E, Acevedo P, Jaque X (2007) Littoral crustaceans in mountain lakes of Huerquehue National Park (38°S, Araucania Region, Chile). Crustaceana 80, 401–410.
| Littoral crustaceans in mountain lakes of Huerquehue National Park (38°S, Araucania Region, Chile).Crossref | GoogleScholarGoogle Scholar |
Dehariya P, Kataria S, Pandey GP, Guruprasad KN (2011) Assessment of impact of solar UV components on growth and antioxidant enzyme activity in cotton plant. Physiology and Molecular Biology of Plants 17, 223–229.
| Assessment of impact of solar UV components on growth and antioxidant enzyme activity in cotton plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Kjs7nP&md5=340034444a92b5f4e9f50f7eab68e787CAS | 23573013PubMed |
Donahue JL, Okpodu CM, Cramer CL, Grabau EA, Aslcher RG (1997) Responses of antioxidant to paraquat in pea leaves (relationships to resistance). Plant Physiology 113, 249–247.
| Responses of antioxidant to paraquat in pea leaves (relationships to resistance).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlOmtQ%3D%3D&md5=c428369f120836112185c97d3fad26ddCAS | 12223604PubMed |
Doncheva S, Poschenrieder C, Stoyanova Z, Georgieva K, Velichkova M, Barceló J (2009) Silicon amelioration of manganese toxicity in Mn-sensitive and Mn tolerant maize varieties. Environmental and Experimental Botany 65, 189–197.
| Silicon amelioration of manganese toxicity in Mn-sensitive and Mn tolerant maize varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKqsbY%3D&md5=3d38b77c81dbb3642ac700f9ada299b8CAS |
Ducic T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Brazilian Journal of Plant Physiology 17, 103–112.
| Transport and detoxification of manganese and copper in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWrsLs%3D&md5=cb999defd36bca846987fbac7be62f6eCAS |
El-Jaoual T, Cox C (1998) Manganese toxicity in plants. Journal of Plant Nutrition 21, 353–386.
| Manganese toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlWltrg%3D&md5=b4d83f312d5bd27dbb9e6c7bad5ae0c4CAS |
Farrar JF, Jones DL (2000) The control of carbon acquisition by root. New Phytologist 147, 43–53.
| The control of carbon acquisition by root.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1ylt7o%3D&md5=cfac1527cb23f5754886059372a89b47CAS |
Feng JP, Shi QH, Wang XF (2009) Effects of exogenous silicon on photosynthetic capacity and antioxidant enzyme activities in chloroplast of cucumber seedlings under excess manganese. Agricultural Sciences in China 8, 40–50.
| Effects of exogenous silicon on photosynthetic capacity and antioxidant enzyme activities in chloroplast of cucumber seedlings under excess manganese.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvVyms7w%3D&md5=13ab9533094a0cd77f447a19940ceda9CAS |
Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signaling & Behavior 6, 709–711.
| Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlOhs78%3D&md5=589b4110b3dc0e57a10bbf46b7785579CAS |
Fracheboud Y, Leipner J (2003) The application of chlorophyll fluorescence to study light, temperature, and drought stress. In ‘Practical applications of chlorophyll fluorescence in plant biology’. (Eds JR DeEll, PMA Toivonen) pp. 125–150. (Kluwer Academic Publishers: Dordrecht)
Gangwar S, Singh VP, Maurya JN (2011) Response of Pisum sativum L. to exogenous indol acetic acid application under manganese toxicity. Bulletin of Environmental Contamination and Toxicology 86, 605–609.
| Response of Pisum sativum L. to exogenous indol acetic acid application under manganese toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvVeruro%3D&md5=9b9335da7dc8ea804508f5ff966c1451CAS | 21516457PubMed |
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
| The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=c7e023b607e8d6002006223a88c3674dCAS |
Goh C-H, Schreiber U, Hedrich R (1999) New approach of monitoring changes in chlorophyll a fluorescence of single guard cells and protoplasts in response to physiological stimuli. Plant, Cell & Environment 22, 1057–1070.
| New approach of monitoring changes in chlorophyll a fluorescence of single guard cells and protoplasts in response to physiological stimuli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt12gtbY%3D&md5=bbeb1db8f1c43ac0554df62581e2f9d7CAS |
González A, Steffen KL, Lynch JP (1998) Light and excess manganese: implications for oxidative stress in common bean. Plant Physiology 118, 493–504.
| Light and excess manganese: implications for oxidative stress in common bean.Crossref | GoogleScholarGoogle Scholar | 9765534PubMed |
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiology 103, 1067–1073.
| Overexpression of superoxide dismutase protects plants from oxidative stress.Crossref | GoogleScholarGoogle Scholar | 12232001PubMed |
Harborne JB (1986) Nature, distribution and function of plant flavonoids. Progress in Clinical and Biological Research 213, 14–24.
Hoagland DR, Arnon DI (1959) The water culture method for growing plants without soil. California Agricultural Experiment Station 347, 1–32.
Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Annals of Botany 90, 37–42.
| Avoiding bias in calculations of relative growth rate.Crossref | GoogleScholarGoogle Scholar | 12125771PubMed |
Horst W (1988) The physiology of Mn toxicity. In ‘Manganese in soils and plants’. (Eds MF Webb, RO Nable, RD Graham) pp. 175–188. (Kluwer Academic Publishers: Dordrecht)
Huovinen P, Gómez I, Lovengreen C (2006) A five-year study of solar ultraviolet radiation in southern Chile (39°S): potential impact on physiology of coastal marine algae? Photochemistry and Photobiology 82, 515–522.
| A five-year study of solar ultraviolet radiation in southern Chile (39°S): potential impact on physiology of coastal marine algae?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1OksLs%3D&md5=393469bb4aec942f0a2398b545c4633bCAS | 16613507PubMed |
Kataria S, Jain K, Guruprasad KN (2007) UV-B induced changes in antioxidant enzymes and their isoform in cucumber (Cucumis sativus) cotyledons. Indian Journal of Biochemistry & Biophysics 44, 31–37.
Kolb CA, Käser MA, Kopeck J, Zotz G, Riederer M, Pfündel EE (2001) Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiology 127, 863–875.
| Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1Knurk%3D&md5=604a0f85b30a3556ab1ca9e47754cf5aCAS | 11706169PubMed |
Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68, 686–694.
| Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFejtbc%3D&md5=a6d66700ef97b5c12dd04131bc2513acCAS | 17346769PubMed |
Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH, Li Y, Yang GH (2010) Effects of manganese-excess on CO2 assimilation, ribulose-1.5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biology 10, 42
| Effects of manganese-excess on CO2 assimilation, ribulose-1.5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings.Crossref | GoogleScholarGoogle Scholar | 20205939PubMed |
Lichtenthaler K, Wellburn R (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvent. Biochemical Society Transactions 11, 591–592.
| Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhslSquro%3D&md5=1c03ad7ee048de971db93affaf8051e0CAS |
Lidon FC, Barreiro MG, Ramalho JC (2004) Manganese accumulation in rice: implications for photosynthetic functioning. Journal of Plant Physiology 161, 1235–1244.
| Manganese accumulation in rice: implications for photosynthetic functioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFensg%3D%3D&md5=07f5a401ebbe54e464e0bdfd78890802CAS | 15602815PubMed |
Lynch J, Marschner P, Rengel Z (2012) Effects of internal and external factors on root growth and development. In ‘Mineral nutrition of higher plants’. (Eds P Marschner). pp. 331–346. (Academic Press: London)
Maxwell K, Johnson G (2000) Chlorophyll fluorescence. A practical guide. Journal of Experimental Botany 51, 659–668.
| Chlorophyll fluorescence. A practical guide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2js74%3D&md5=bc22e4e77aa4127dd9f2794b99d9a4f9CAS | 10938857PubMed |
Mazza CA, Battista D, Zima AM, Szwarcberg-Bracchitta M, Giordano CV, Acevedo A, Scopel AL, Ballaré CL (1999) The effects of solar UV-B radiation on the growth and yield of barley are accompanied by increased DNA damage and antioxidant responses. Plant, Cell & Environment 22, 61–70.
| The effects of solar UV-B radiation on the growth and yield of barley are accompanied by increased DNA damage and antioxidant responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1yisbg%3D&md5=02bc843cc7c2a5a0c213e9b5f1a4690cCAS |
Merzlyak MN, Melo TB, Naqvi KR (2008) Effect of anthocyanins, carotenoids, and flavonols on chlorophyll fluorescence excitation spectra in apple fruit: signature analysis, assessment, modeling, and relevance to photoprotection. Journal of Experimental Botany 59, 349–359.
| Effect of anthocyanins, carotenoids, and flavonols on chlorophyll fluorescence excitation spectra in apple fruit: signature analysis, assessment, modeling, and relevance to photoprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVamt7k%3D&md5=f9e3d1398cae490ad90e053e7477846eCAS | 18256050PubMed |
Millaleo R, Reyes-Diaz M, Mora ML, Alberdi M (2009) Effect of manganese on photochemical parameters and antioxidant activity in highbush blueberry cultivars. Biological Research 42, R152
Millaleo R, Reyes-Díaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. Journal Soil Science and Plant Nutrition 10, 476–494.
| Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms.Crossref | GoogleScholarGoogle Scholar |
Millaleo R, Reyes-Díaz M, Alberdi M, Ivanov AG, Krol M, Hüner NPA (2013) Excess manganese differentially inhibit photosystem I versus II in Arabidopsis thaliana. Journal of Experimental Botany 64, 343–354.
| Excess manganese differentially inhibit photosystem I versus II in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2gsbvF&md5=26de3aacb32fb745de24081add2e5db7CAS | 23183256PubMed |
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends in Plant Science 16, 300–309.
| ROS signaling: the new wave?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVyrs7w%3D&md5=cf6bc0a79abd78bd76262c61a60530c6CAS | 21482172PubMed |
Mohammed GH, Zarco-Tejada P, Miller JR (2003) Applications of chlorophyll fluorescence in forestry and ecophysiology. In ‘Practical applications of chlorophyll fluorescence in plant biology’. (Ed JR DeEll) pp. 79–124. (Kluwer Academic Publishers: Dordrecht)
Moody SA, Coop DJS, Paul ND (1997) Effects of elevated of UV-B radition and levated CO2 on heatland communities. In ‘Plants and UV-B; responses to environmental change’. (Ed PJ Lumsden ) pp. 283–304. (Cambridge University Press, Cambridge, UK)
Mora M, Alfaro M, Williams P, Stehr W, Demanet R (2004) Effect of fertilizer input on soil acidification in relation to growth and chemical composition of a pasture and animal production. Journal Soil Science and Plant Nutrition 4, 29–40.
| Effect of fertilizer input on soil acidification in relation to growth and chemical composition of a pasture and animal production.Crossref | GoogleScholarGoogle Scholar |
Mora M, Rosas A, Ribera A, Rengel Z (2009) Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates. Plant and Soil 320, 79–89.
| Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFGjtL4%3D&md5=b72423709e2faaa94ab43393dbfdee98CAS |
Nguyen HN, Kim JH, Hyun WY, Nguyen NT, Hong S-W, Lee H (2013) TTG1-mediated flavonols biosynthesis alleviates roots growth inhibition in response to ABA. Plant Cell Reports 32, 503–514.
| TTG1-mediated flavonols biosynthesis alleviates roots growth inhibition in response to ABA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktVOnsb4%3D&md5=1a8dda537b6e8df1331f84ad0c771713CAS | 23306631PubMed |
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role of the xanthophylls cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
| Arabidopsis mutants define a central role of the xanthophylls cycle in the regulation of photosynthetic energy conversion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFejt7w%3D&md5=8a344e0e8a70426b45438ce57ca6d986CAS | 9668132PubMed |
Pinto M, Lizana C, Pastenes C, Riquelme A, Berti M (2000) Effect of the ultraviolet-B radiation on growth and photosynthesis of seven varieties of wheat (Triticum aestivum l.). Revista Chilena de Historia Natural (Valparaiso, Chile) 73, 55–66.
| Effect of the ultraviolet-B radiation on growth and photosynthesis of seven varieties of wheat (Triticum aestivum l.).Crossref | GoogleScholarGoogle Scholar |
Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta 1787, 1151–1160.
| Production of reactive oxygen species by photosystem II.Crossref | GoogleScholarGoogle Scholar | 19463778PubMed |
Ravindran KC, Indrajith A, Pratheesh PV, Sanjiviraja K, Balakrishnan V (2010) Effect of ultraviolet-B radiation on biochemical and antioxidant defense system in Indigofera tinctoria L. seedlings. International Journal of Engineering Science and Technology 2, 226–232.
| Effect of ultraviolet-B radiation on biochemical and antioxidant defense system in Indigofera tinctoria L. seedlings.Crossref | GoogleScholarGoogle Scholar |
Reyes-Díaz M, Alberdi M, Mora ML (2009) Short-term aluminum stress differentially affects the photochemical efficiency of photosystem II in highbush blueberry genotypes. Journal of the American Society for Horticultural Science 134, 14–21.
Reyes-Díaz M, Inostroza-Blancheteau C, Millaleo R, Cruces E, Wulff-Zottele C, Alberdi M, Mora ML (2010) Long-term aluminium exposure effects on physiological and biochemical features of highbush blueberry cultivars. Journal of the American Society for Horticultural Science 135, 1–11.
Rosas A, Rengel Z, Mora ML (2007) Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover. Journal of Plant Nutrition 30, 253–270.
| Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFCgtL8%3D&md5=887ab4dec7e5ca8a79a9bd632cbd368eCAS |
Rufty T, Miner S, Raper T (1979) Temperature effects on growth and Mn tolerance in tobacco. Agronomy Journal 71, 638–643.
| Temperature effects on growth and Mn tolerance in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltlGju7o%3D&md5=58e7f41d97adee6cd68489ff849e8f15CAS |
Ruhland CT, Day TA (1996) Changes in UV-B radiation screening effectiveness with leaf age in Rhododendron maximum. Plant, Cell & Environment 19, 740–746.
| Changes in UV-B radiation screening effectiveness with leaf age in Rhododendron maximum.Crossref | GoogleScholarGoogle Scholar |
Sadzawka A, Grez R, Mora ML, Saavedra N, Carrasco MA, Flores H, Rojas C (2004) ‘Métodos de análisis de tejidos vegetales.’ (Comisión de Normalización y Acreditación, Sociedad Chilena de la Ciencia del Suelo: Santiago)
Sadzawka A, Grez R, Carrasco M, Mora ML (2007) ‘Métodos de análisis de tejidos vegetales.’ (Comisión de Normalización y Acreditación, Sociedad Chilena de la Ciencia del Suelo: Santiago)
Selvakumar V (2008) Ultraviolet-B radiation (280–315 nm) invoked antioxidant defense systems in Vigna unguiculata (L.) Walp and Crotalaria juncea L. Photosynthetica 46, 98–106.
| Ultraviolet-B radiation (280–315 nm) invoked antioxidant defense systems in Vigna unguiculata (L.) Walp and Crotalaria juncea L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlWgtb4%3D&md5=45367a26838542a760d4888052177fe8CAS |
Shen X, Li X, Li Z, Li J, Duan L, Eneji AE (2010) Growth, physiological attributes and antioxidant enzyme activities in soybean seedlings treated with or without silicon under UV-B radiation stress. Journal Agronomy & Crop Science 196, 431–439.
| Growth, physiological attributes and antioxidant enzyme activities in soybean seedlings treated with or without silicon under UV-B radiation stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1emt7vK&md5=1440f88378ac1395c0abb243b466aa01CAS |
Shi Q, Bao Z, Zhu Z, He Y, Qian Q, Yu J (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66, 1551–1559.
| Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFejsro%3D&md5=551ade93b614b3fd10907038c40154e5CAS | 15963540PubMed |
Shi Q, Zhua Z, Xua M, Qian Q, Yu J (2006) Effect of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities. Environmental and Experimental Botany 58, 197–205.
| Effect of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xosl2ktb0%3D&md5=8a358e67f0383d58448f9f7c722b40bfCAS |
Slinkard K, Singleton V (2007) Total phenol analyses: automation and comparison with manual methods. American Journal of Enology and Viticulture 28, 49–55.
Surabhi G, Reddy K, Singh S (2009) Photosynthesis, fluorescence, shoot biomass and seed weight responses of three cowpea (Vigna unguiculata [L.] Walp) cultivars with contrasting sensitivity to UV-B radiation. Environmental and Experimental Botany 66, 160–171.
| Photosynthesis, fluorescence, shoot biomass and seed weight responses of three cowpea (Vigna unguiculata [L.] Walp) cultivars with contrasting sensitivity to UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFCqs78%3D&md5=0806be9448456dcc22313b403ba77d5dCAS |
Tsonev T, Velikova V, Georgieva K, Hyde PF, Jones HG (2003) Low temperature enhances photosynthetic down-regulation in French bean (Phaseolus vulgaris L.) plants. Annals of Botany 91, 343–352.
| Low temperature enhances photosynthetic down-regulation in French bean (Phaseolus vulgaris L.) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVKisrY%3D&md5=dfae4a08fcb76347b3c6c8be9477c9d1CAS | 12547687PubMed |
Vass I, Kirilovsky D, Etienne AL (1999) UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 38, 12 786–12 794.
| UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1ajt7w%3D&md5=15e1a7d4533d76bd4286e2f864b14d97CAS |
Vega-Gálvez A, Lemus-Mondaca R, Tello-Ireland C, Miranda M, Yagnam F (2009) Kinetic study of convective drying of blueberry variety O’Niel (Vaccinium corymbosum L.). Chilean Journal of Agricultural Research 69, 171–178.
| Kinetic study of convective drying of blueberry variety O’Niel (Vaccinium corymbosum L.).Crossref | GoogleScholarGoogle Scholar |
Xu C, Natarajan S, Sullivan J (2008) Impact of solar ultraviolet-B radiation on the antioxidant defense system in soybean lines differing in flavonoid contents. Environmental and Experimental Botany 63, 39–48.
| Impact of solar ultraviolet-B radiation on the antioxidant defense system in soybean lines differing in flavonoid contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVeju74%3D&md5=64deea8b2be5ab89e3887d4f5a652c8cCAS |
Yao X, Liu Q, Han C (2008) Growth and photosynthetic responses of Picea asperata seedlings to enhanced ultraviolet-B and to nitrogen supply. Brazilian Journal of Plant Physiology 20, 11–18.
| Growth and photosynthetic responses of Picea asperata seedlings to enhanced ultraviolet-B and to nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptFygu7o%3D&md5=0105619980f008562bd3ae69831693f1CAS |
Yuan L, Ming Y, Xunling W (1998) Effects of enhanced ultraviolet-B radiation on crop structure, growth and yield components of spring wheat under field conditions. Field Crops Research 57, 253–263.
| Effects of enhanced ultraviolet-B radiation on crop structure, growth and yield components of spring wheat under field conditions.Crossref | GoogleScholarGoogle Scholar |
