Tropospheric ozone, one of the most phytotoxic air pollutants, may specially impose in long-lived forest trees substantial reduction in productivity and biomass. European beech saplings grown in lysimeter around areas were used to monitor proteomic changes upon elevated ozone concentrations following four vegetation periods of exposure. A proteome study based on highly sensitive two-dimensional fluorescence difference gel electrophoresis (2-D DIGE) was performed to identify protein changes in European beech, the most important deciduous tree in Central Europe. Main emphasis was on identifying differentially expressed proteins after long-time period of ozone exposure under natural conditions rather than short-term responses or reactions under controlled conditions. Our results clearly demonstrate a response of European beech saplings to long-term ozone fumigation at the protein level. We indicate changes in the protein abundance of 142 protein spots; among them 59 were increased and 83 decreased following three years of elevated ozone exposure. As the first step, 40 proteins were identified by a homology driven mass spectrometric approach. Some of the identified proteins have been previously described in the context of short-term ozone responses in plants, indicating, at least for certain cellular functions, the congruence of plant reactions following short- and long-term ozone exposure. Under elevated ozone exposure, abundance of proteins related to the Calvin cycle and photosynthetic electron transport chain were decreased whereas the abundance of proteins regarding the carbon metabolism/catabolism were increased.
Keywords
, , , ,
Citation
Kerner R, Winkler JB, Dupuy JW, Jürgensen M, Lindermayr C, Ernst D, Müller-Starck G (2011). Changes in the proteome of juvenile European beech following three years exposure to free-air elevated ozone. iForest 4: 69-76. - doi: 10.3832/ifor0570-004
Paper history
Received: Sep 13, 2010
Accepted: Jan 17, 2011
First online: Apr 05, 2011
Publication Date: Apr 05, 2011
Publication Time: 2.60 months
© SISEF - The Italian Society of Silviculture and Forest Ecology 2011
Open Access
This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
Breakdown by View Type
(Waiting for server response...)
Article Usage
Total Article Views: 58697
(from publication date up to now)
Breakdown by View Type
HTML Page Views: 49133
Abstract Page Views: 2754
PDF Downloads: 5160
Citation/Reference Downloads: 72
XML Downloads: 1578
Web Metrics
Days since publication: 4937
Overall contacts: 58697
Avg. contacts per week: 83.22
Article Citations
Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)
Total number of cites (since 2011): 12
Average cites per year: 0.92
Publication Metrics
by Dimensions ©
Articles citing this article
List of the papers citing this article based on CrossRef Cited-by.
(1)
Agrawal GK, Rakwal R, Yonekura M, Kubo A, Saji H (2002)Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (
Oryza sativa L.) seedlings. Proteomics 2: 947-959.
CrossRef |
Gscholar
(2)
Ahsan N, Nanjo Y, Sawada H, Kohno Y, Komatsu S (2010)Ozone stress-induced proteomic changes in leaf total soluble and chloroplast proteins of soybean reveal that carbon allocation is involved in adaptation in the early developmental stage. Proteomics 10: 2605-2619.
CrossRef |
Gscholar
(3)
Bahl A, Loitsch SM, Kahl G (1993)Air pollution and plant gene expression. Plant responses to the environment. P. M. Gresshoff. Knoxville, Tennessee, USA, pp. 184.
Gscholar
(4)
Benjamini Y, Hochberg Y (2000)On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics 25: 60-83.
CrossRef |
Gscholar
(5)
Blumenröther MC, Löw M, Matyssek R, Oβwald W (2007)Flux-based response of sucrose and starch in leaves of adult beech trees (
Fagus sylvatica L.) under chronic free-air O
3 fumigation. Plant Biology 9: 207-214.
CrossRef |
Gscholar
(6)
Bohler S, Bagard, Mouhssin Oufir M, Planchon S, Hoffmann L, Jean-François YJ, Dizengremel HP, Renaut J (2007)A DIGE analysis of developing poplar leaves subjected to ozone reveals major changes in carbon metabolism. Proteomics 7: 1584-1599.
CrossRef |
Gscholar
(7)
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004)Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
CrossRef |
Gscholar
(8)
Cho K, Shibato J, Agrawal GK, Jung Y-H, Kubo A, Jwa N-S, Tamogami S, Satoh K, Kikuchi S, Higashi T, Kimura S, Saji H, Tanaka Y, Iwahashi H, Masuo Y, Rakwal R (2008)Integrated transcriptomics, proteomics, and metabolomics analyses to survey ozone responses in the leaves of rice seedling. Journal of Proteome Research 7: 2980-2998.
CrossRef |
Gscholar
(9)
Coleman MD, Isebrands JG, Dickson RE, Karnosky DF (1995)Photosynthetic productivity of aspen clones varying in sensitivity to tropospheric ozone. Tree Physiology 15: 585-592.
CrossRef |
Gscholar
(10)
Damerval C, De Vienne D, Zivy M, Thiellement H (1986)Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7: 52-54.
CrossRef |
Gscholar
(11)
Dizengremel P (2001)Effects of ozone on the carbon metabolism of forest trees. Plant Physiology and Biochemistry 39: 729-742.
CrossRef |
Gscholar
(12)
Dizengremel P, Thiec DL, Hasenfratz-Sauder M-P, Vaultier MN, Bagard M, Jolivet Y (2009)Metabolic-dependent changes in plant cell redox power after ozone exposure. Plant Biology 11: 35-42.
CrossRef |
Gscholar
(13)
Feng Y, Komatsu S, Furukawa T, Koshiba T, Kohno Y (2008)Proteome analysis of proteins responsive to ambient and elevated ozone in rice seedlings. Agriculture, Ecosystems & Environment 125: 255-265.
CrossRef |
Gscholar
(14)
Fleischman F, Winkler JB, Oßwald W (2009)Effects of ozone and
Phytophthora citricola on non-structural carbohydrates of European beech (
Fagus sylvatica) saplings. Plant Soil 323: 75-84.
CrossRef |
Gscholar
(15)
He XY, Fu SL, Chen W, Zhao TH, Xu S, Tuba Z (2007)Changes in effects of ozone exposure on growth, photosynthesis, and respiration of
Ginkgo biloba in Shenyang urban area. Photosynthetica 45: 555-561.
CrossRef |
Gscholar
(16)
Heukeshoven J, Dernick R (1988)Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9: 28-32.
CrossRef |
Gscholar
(17)
Hough AM, Derwent RG (1990)Changes in the global concentration of tropospheric ozone due to human activities. Nature 344: 645-648.
CrossRef |
Gscholar
(18)
Jorrín-Novo JV, Maldonado AM, Echevarría-Zomeño S, Valledor L, Castillejo MA, Curto M, Valero J, Sghaier B, Donoso G, Redondo I (2009)Plant proteomics update (2007-2008): Second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge. Journal of Proteomics 72: 285-314.
CrossRef |
Gscholar
(19)
Kontunen-Soppela S, Riikonen J, Ruhanen H, Brosché M, Somervuo P, Peltonen P, Kangasjärvi J, Auvinen P, Paulin L, Keinänen M, Oksanen E, Vapaavuori E (2010)Differential gene expression in senescing leaves of two silver birch genotypes in response to elevated CO
2 and tropospheric ozone. Plant, Cell and Environment 33: 1016-1028.
CrossRef |
Gscholar
(20)
Kronfuß G, Polle A, Tausz M, Havranek WM, Wieser G (1998)Effects of ozone and mild drought stress on gas exchange, antioxidants and chloroplast pigments in current-year needles of young Norway spruce [
Picea abies (L.) Karst.]. Trees 12: 482-489.
CrossRef |
Gscholar
(21)
Lawson T, Oxborough K, Morison JIL, Baker NR (2002)Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO
2, and humidity. Plant Physiology 128: 52-62.
CrossRef |
Gscholar
(22)
Liu X, Kozovits AR, Grams TEE, Blaschke H, Rennenberg H, Matyssek R (2004)Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech. Tree Physiology 24: 1045-1055.
CrossRef |
Gscholar
(23)
Luethy-Krause B, Pfenninger I, Landolt W (1990)Effects of ozone on organic acids in needles of Norway spruce and Scots pine. Trees 4: 198-204.
CrossRef |
Gscholar
(24)
Marenco A, Gouget H, Nédélec P, Pagés JP, Karcher F (1994)Evidence of a long-term increase in tropospheric ozone from Pic du Midi data series: consequences: positive radiative forcing. Journal of Geophysical Research 99: 16617-16632.
CrossRef |
Gscholar
(25)
Matyssek R, Keller T, Koike T (1993)Branch growth and leaf gas exchange of
Populus tremula exposed to low ozone concentrations throughout two growing seasons. Environmental Pollution 79: 1-7.
CrossRef |
Gscholar
(26)
Odanaka S, Bennett AB, Kanayama Y (2002)Distinct physiological roles of fructokinase isozymes revealed by gene-specific suppression of Frk1 and Frk2 expression in tomato. Plant Physiology 129: 1119-1126.
CrossRef |
Gscholar
(27)
Olbrich M, Gerstner E, Welzl G, Winkler J, Ernst D (2009)Transcript responses in leaves of ozone-treated beech saplings seasons at an outdoor free air model fumigation site over two growing seasons. Plant and Soil 323: 61-74.
CrossRef |
Gscholar
(28)
Örvar BL, McPherson J, Ellis BE (1997)Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. The Plant Journal 11: 203-212.
CrossRef |
Gscholar
(29)
Pell EJ, Schlagnhaufer CD, Arteca RN (1997)Ozone-induced oxidative stress: mechanisms of action and reaction. Physiologia Plantarum 100: 264-273.
CrossRef |
Gscholar
(30)
Pritsch K, Ernst D, Fleischmann F, Gayler S, Grams T, Göttlein A, Heller W, Koch N, Lang H, Matyssek R, Munch J, Olbrich M, Scherb H, Stich S, Winkler J, Schloter M (2008)Plant and soil system responses to ozone after 3 years in a Lysimeter study with juvenile beech (
Fagus sylvatica L.). Water, Air and Soil Pollution: Focus 8: 139-154.
CrossRef |
Gscholar
(31)
Ranieri A, Giuntini D, Ferraro F, Nali C, Baldan B, Lorenzini G, Soldatini GF (2001)Chronic ozone fumigation induces alterations in thylakoid functionality and composition in two poplar clones. Plant Physiology and Biochemistry 39: 999-1008.
CrossRef |
Gscholar
(32)
Reich PB (1983)Effects of low concentrations of O
3 on net photosynthesis, dark respiration, and chlorophyll contents in aging hybrid poplar leaves. Plant Physiology 73: 291-296.
CrossRef |
Gscholar
(33)
Roshchina VV, Roshchina VD (2003)Ozone and plant cell. Kluwer Academic Publisher, Dordrecht, The Netherlands.
Gscholar
(34)
Ryang S, Woo S, Kwon S, Kim S, Lee S, Kim K, Lee D (2009)Changes of net photosynthesis, antioxidant enzyme activities, and antioxidant contents of
Liriodendron tulipifera under elevated ozone. Photosynthetica 47: 19-25.
CrossRef |
Gscholar
(35)
Sandermann H (1996)Ozone and plant health. Annual Review of Phytopathology 34: 347-366.
CrossRef |
Gscholar
(36)
Sarkar A, Rakwal R, Agrawal SB, Shibato J, Ogawa Y, Yoshida Y, Agrawal GK, Agrawal M (2010)Investigating the impact of elevated levels of ozone on tropical wheat using integrated phenotypical, physiological, biochemical, and proteomics approaches. Journal of Proteome Research 9: 4565-4584.
CrossRef |
Gscholar
(37)
Schloter M, Winkler JB, Aneja M, Koch N, Fleischmann F, Pritsch K, Heller W, Stich S, Grams TE, Gottlein A, Matyssek R, Munch JC (2005)Short term effects of ozone on the plant-rhizosphere-bulk soil system of young beech trees. Plant Biology 7: 728-736.
CrossRef |
Gscholar
(38)
Torres NL, Cho K, Shibato J, Hirano M, Kubo A, Masuo Y, Iwahashi H, Jwa NS, Agarwal GK, Rakwal R (2007)Gel-based proteomics reveals potential novel protein markers of ozone stress in leaves of cultivated bean and maize species of Panama. Electrophoresis 28: 4369-4381.
CrossRef |
Gscholar
(39)
Valcu CM, Schlink K (2006)Efficient extraction of proteins from woody plant samples for two-dimensional electrophoresis. Proteomics 6: 4166-4175.
CrossRef |
Gscholar
(40)
Winkler J, Lang H, Graf W, Reth S, Munch J (2009)Experimental set up of field lysimeters for studying effects of elevated ozone and below-ground pathogen infection on a plant-soil-system of juvenile beech (
Fagus sylvatica L.). Plant and Soil 323: 7-19.
CrossRef |
Gscholar