How do plants cope with oxidative stress in nature? A study on the dwarf bearded iris (Iris pumila)

• Autorzy: Vuleta A. , Manitasevic Jovanovic S. , Tucic B.
• Języki publikacji: EN

Abstrakty

EN

Oxidative stress results from incongruity between the generation of toxic reactive oxygen species (ROS) and the availability of their scavengers—antioxidants. Although the short-term effects of this phenomenon are attracting much scientific attention, oxidative stress may influence an organism’s metabolism over the long (evolutionary) time scale as well. To disentangle the impact of strong light intensity from co-occurring abiotic stresses in creating adaptive responses in antioxidants and heat shock proteins (Hsps), an environment manipulation experiment was performed using a xerophyte clonal monocot, Iris pumila, native to semi-arid grasslands at the Deliblato Sands. This species is very tolerant to the combined effect of extreme abiotic stressors such as high light intensity, elevated soil surface temperatures, and scarcity of water, which commonly takes place in its natural habitats during the summer. By shading half of each selected clone, leaving the other half sun-exposed, we contrasted short-term effects of reduced daylight intensity with longterm effects of photo-oxidative stress. In both light treatments, the enzymatic activities of SOD and APX antioxidants were similar in magnitude, whereas those of CAT and POD significantly decreased in exposed compared to shaded leaves. Moreover, exposed leaves expressed a unique CAT isoform that differed biochemically from two CAT isoforms observed in shaded leaves. The content of non-enzymatic antioxidants, carotenoids (Car), remained constant with the reduction of light intensity, but their ratio to total chlorophylls (Chl) significantly decreased compared to that expressed in full sunlight. The abundance of Hsps was considerably greater in exposed than in shaded leaves, especially regarding the inducible isoforms, Hsp70 and Hsp90a, as were their proportions in relation to the constitutively expressed Hsp90b isoform. The presented results, thus, indicate that adaptive metabolic responses of I. pumila leaves to photo-oxidative stress entailed the high activity of two key enzymatic antioxidants, SOD and APX and the expression of a light-resistant CAT—to counteract the stress-mediated ROS accumulation, the increased Car to Chl ratio—to adjust the photosynthetic apparatus to the high light conditions, as well as the accelerated biosynthesis of heat shock proteins Hsp70 and Hsp90—to preserve the cellular proteostasis.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 01
• Opis fizyczny: Article: 1711 [12 p.], fig.,ref.

Twórcy

autor

Vuleta A.

• Department of Evolutionary Biology, Institute for Biological Research Sinisa Stankovic, University of Belgrade, 142 Despot Stefan Blvd., 11060 Belgrade, Serbia

autor

Manitasevic Jovanovic S.

• Department of Evolutionary Biology, Institute for Biological Research Sinisa Stankovic, University of Belgrade, 142 Despot Stefan Blvd., 11060 Belgrade, Serbia

autor

Tucic B.

• Department of Evolutionary Biology, Institute for Biological Research Sinisa Stankovic, University of Belgrade, 142 Despot Stefan Blvd., 11060 Belgrade, Serbia

Bibliografia

• Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
• Aiken CT, Kaake RM, Wang X, Huang L (2011) Oxidative stressmediated regulation of proteasome complex. Mol Cell Proteomics 10(R110):006924
• Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–379
• Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
• Barua D, Heckathorn SA (2006) The interactive effects of light and temperature on heat-shock protein accumulation in Solidago altissima (Asteraceae) in the field and laboratory. Am J Bot 93:102–109
• Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Ann Biochem 161:559–566
• Bradford MM (1976) A rapid and sensitive method for quantification of microgram of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
• Bukau B, Weissman J, Hoewich A (2006) Molecular chaperones and protein quality control. Cell 125:443–451
• Cohen AA, McGraw KJ (2009) No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct Ecol 23:310–320
• Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251
• Costantini D, Verhulst S (2009) Does high antioxidant capacity indicates low oxidative stress? Funct Ecol 23:506–509
• Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21
• Domonkos I, Kis M, Gombos Z, Ughy B (2013) Carotenoids, versatile components of oxygenic photosynthesis. Prog Lipid Res 52:539–561
• Engel N, Schmidt M, Lütz C, Feierabend J (2006) Molecular identification, heterologous expression and properties of lightinsensitive plant catalases. Plant Cell Environ 29:593–607
• Estavillo G, Crisp PA, Pornsiri Wong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelen J, David P, Javot H, Brearly C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in growth and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
• Feierabend J, Schaan C, Hertwig B (1992) Photoinactivation of catalase occurs under both high- and low-temperature stress conditions and accompanies photoinactivation of photosystem II. Plant Physiol 100:1554–1561
• Frank HA, Bautista JA, Josue JS, Young AJ (2000) Mechanisms of nonphotochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry (Moscow) 39:2831–2837
• Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705
• Gordon MJ, Carmody M, Albrecht V, Pogson B (2013) Systemic and local response to repeated HL stress-induced retrograde signaling in Arabidopsis. Front Plant Sci 3:303
• Grotjohann N, Janning A, Eising R (1997) In vitro photoinactivation of catalase isoforms from cotyledons of sunflower (Helianthus annuus L.). Arch Biochem Biophys 346:208–218
• Hager A (1980) The reversible, light-induced conversion of xanthophylls in the chloroplasts. In: Czygan F-C (ed) Pigments in Plants. Gustav Fischer, Germany, pp 57–79
• Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Clarendon, Oxford
• Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574–581
• Jarosz DF, Linquist S (2010) Hsp90 and environmental stress transforms the adaptive value of natural genetic variation. Science 330:1820–1824
• Ketola T, Laakso J, Kaitala V, Airaksinen S (2004) Evolution of Hsp90 expression in Tetrahymena thermophila (Protozoa, Ciliata) populations exposed to thermally variable environments. Evolution 58:741–748
• Kukavica B, Veljović-Jovanović S (2004) Senescence-related changes in the antioxidant status of ginkgo and birch leaves during autumn yellowing. Physiol Plant 122:321–327
• Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
• Manitašević S, Dunđerski J, Matić G, Tucić B (2007) Seasonal variation in heat shock proteins Hsp70 and Hsp90 expression in an exposed and a shaded habitat of Iris pumila. Plant Cell Environ 30:1–11
• Martin RE, Asner GP, Sack L (2007) Genetic variation in leaf pigment, optical and photosynthetic function among diverse phenotypes of Metrosideros polymorpha grown in a common garden. Oecologia 151:387–400
• Martiskainen J, Kananavicius R, Linnanto J, Lehtivuori H, Keranen M, Aumanen V, Tkachenko N, Korppi-Tommola J (2011) Excitation energy transfer in the LHC-II trimer: from carotenoids to chlorophylls in space and time. Photosynth Res 107:195–207
• McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J (2007) Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131:121–135
• McGraw KJ, Cohean AA, Constantini D, Horak P (2010) The ecological significance of antioxidants and oxidative stress: marriage between mechanistic and functional perspectives. Funct Ecol 24:47–949
• Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125
• Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553
• Niki E (2010) Assessment of antioxidant capacity in vitro and in vivo. Free Radic Biol Med 49:503–515
• Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
• Noctor G, Mhamdi A, Foyer CH (2014) The role of reactive metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648
• Parsell DA, Lindquist S (1993) The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496
• Pratt WB, Morishima Y, Peng HM, Osawa Y (2010) Role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp Biol Med (Maywood) 235:278–289
• Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantphylidés C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA 14:5535–5540
• SAS Institute Inc. (2011) SAS/STAT 9.3 user’s guide. SAS Institute Inc., Cary
• Seyhan F, Tijskens LMM, Evranuz O (2002) Modelling temperature and pH dependence of lipase and peroxidase activity in Turkish hazelnuts. J Food Eng 52:387–397
• Shigeoka S, Ishikawa T, Tamoi M, Miyagava Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
• Streb P, Feierabend J, Bligny R (1997a) Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant Cell Environ 20:1030–1040
• Streb P, Tel-Or E, Feierabend J (1997b) Light stress effects and antioxidative protection in two desert plants. Funct Ecol 11:416–424
• Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43
• Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182
• Takahashi S, Badger M (2010) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60
• Tang L, Kwon SY, Kim SH, Kim JS, Choi JS, Cho KY, Sung CK, Kwak SS, Lee HS (2006) Enhanced tolerance to transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and light temperature. Plant Cell Rep 25:1380–1386
• Tomanek L (2002) The heat-shock response: its variation, regulation and ecological importance in intertidal Gastropods (genus Tegula). Integr Comp Biol 42:797–807
• Tsang EW, Bowler C, Herouart D, Van Camp W, Villarroel R, Genetello C, Van Montagu M, Inze D (1991) Differential regulation of superoxide dismutase in plants to environmental stress. Plant Cell 3:783–792
• Tucić B, Milojković S, Vujčić S, Tarasjev A (1988) Clonal diversity and dispersion in Iris pumila. Acta Oecol/Oecol Plant 9:211–219
• Tucić B, Tomić V, Avramov S, Pemac D (1998) Testing the adaptive plasticity of Iris pumila leaf traits to natural light conditions using phenotypic selection analysis. Acta Oecol 19:473–481
• Tucić B, Manitašević Jovanović S, Vuleta A (2011) Does environmentally contingent variation in the level of molecular chaperones mirror a biochemical adaptation to abiotic stress? In: Shankar AK, Venkateswarlu B (eds) Abiotic stress in plants—physiological, biochemical and genetic perspectives. InTech, Rijeka, pp 323–345
• Vuleta A (2013) Evolutionary ecophysiology of stress: enzymatic and non-enzymatic role of antioxidants in natural Iris pumila L. (Iridaceae) populations. Dissertation, Faculty of Biology, University of Belgrade
• Vuleta A, Manitašević Jovanović S, Šešlija D, Tucić B (2010) Seasonal dynamics of foliar antioxidative enzymes and total anthocyanins in natural populations of Iris pumila L. J Plant Ecol UK 3: 59–69
• Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrometers of different resolution. J Plant Physiol 144:307–313
• Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806–4816
• Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305
• Yamamoto HY (1979) Biochemistry of the violaxanthin cycle. Pure Appl Chem 51:637–648
• Zhu Y, Graham JE, Ludwig M, Xiong W, Alvey RM, Shen G, Bryant DA (2010) Roles of xanthophyll carotenoids in protection against photoinhibition and oxidative stress in the cyanobacterium Synechococcus sp. Strain PCC 7002. Arch Biochem Biophys 504:86–89

Identyfikatory

DOI

10.1007/s11738-014-1711-9