Antioxidant capacity along the leaf blade of the C3-CAM facultative bromeliad Guzmania monostachia under water deficit conditions
Maria E. Abreu A , Victória Carvalho B and Helenice Mercier A C
+ Author Affiliations
- Author Affiliations
A Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil.
B Núcleo de Pesquisa em Plantas Ornamentais, Instituto de Botânica SMA/SP, 04301-902, São Paulo, SP, Brazil.
C Corresponding author. Email: hmercier@usp.br
Functional Plant Biology 45(6) 620-629 https://doi.org/10.1071/FP17162
Submitted: 6 June 2017 Accepted: 29 November 2017 Published: 15 January 2018
Abstract
Guzmania monostachia (L.) Rusby ex Mez is an epiphytic, rosette-shaped bromeliad that displays variable degrees of crassulacean acid metabolism (CAM) along the leaf under water deficit. The aim of our study was to evaluate whether the production-scavenging system of reactive oxygen species (ROS) along the leaf length of G. monostachia plants is related to the foliar gradient of CAM when irrigation is withheld. Among the leaf portions, the apex was exposed to the highest photosynthetic flux density and presented the highest relative water content, CAM activity, hydrogen peroxide and lipid peroxidation after treatment. Hence, the most intense CAM at the leaf apex may not have prevented higher oxidative burden in that region during water deficiency. However, the photosynthetic efficiency in the apex seemed unaffected by irrigation withholding or light intensity. The leaf apex also had the highest carotenoid content and increased superoxide dismutase and ascorbate peroxidase activities under treatment. Hence, G. monostachia was able to maintain ROS under tolerable levels by increasing antioxidant capacity. Our results suggest the metabolic differences within the same leaf under water deficit may derive from the gradient of light incidence, which emphasises the physiological plasticity this bromeliad applies to adapt to the adverse conditions of the canopy.
Additional keywords: antioxidant enzymes, crassulacean acid metabolism, foliar light gradient, reactive oxygen species, water deficit.
References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=187985f9d8c4a6274567637eb1db143eCAS |
Balen B, Tkalec M, Pevalek-kozlina DPB, Krsnik-Rasol M, Pavokovic D, Pevalek-Kozlina B, Pavoković D (2009) Growth conditions in in vitro culture can induce oxidative stress in Mammillaria gracilis tissues. Plant Growth Regulation 28, 36–45.
| Growth conditions in in vitro culture can induce oxidative stress in Mammillaria gracilis tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2qtrc%3D&md5=115c44fadd52580266f7022c2aab5455CAS |
Bhattacharjee S (2010) Sites of generation and physicochemical basis of formation of reactive oxygen species in plant cell. ‘Reactive oxygen species and antioxidants in higher plants’. (Ed. S Dutta Gupta) pp. 1–30. (Science Publishers: Enfield, NH, USA)
Bilgin DD (2010) ROS, oxidative stress and engineering resistance in higher plants. ‘Reactive oxygen species and antioxidants in higher plants’. (Ed. S Dutta Gupta) pp. 205–228. (Science Publishers: Enfield, NH, USA)
Borland AM, Maxwell K, Griffiths H (2000) Ecophysiology of plants with crassulacean acid metabolism. ‘Photosynthesis: physiology and metabolism’. (Eds R C Legood, T D Sharkey, S von Caemmerer) pp. 583–605. (Springer: Dordrecht, The Netherlands)
Borland AM, Elliott S, Patterson S, Taybi T, Cushman J, Pater B, Barnes J (2006) Are the metabolic components of crassulacean acid metabolism up-regulated in response to an increase in oxidative burden? Journal of Experimental Botany 57, 319–328.
| Are the metabolic components of crassulacean acid metabolism up-regulated in response to an increase in oxidative burden?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKguw%3D%3D&md5=bed04edd9fdec7e81d829ee7e8cae8baCAS |
Carvalho V, Abreu ME, Mercier H, Nievola CC (2017) Adjustments in CAM and enzymatic scavenging of H2O2 in juvenile plants of the epiphytic bromeliad Guzmania monostachia as affected by drought and rewatering. Plant Physiology and Biochemistry 113, 32–39.
| Adjustments in CAM and enzymatic scavenging of H2O2 in juvenile plants of the epiphytic bromeliad Guzmania monostachia as affected by drought and rewatering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXitFentrw%3D&md5=2991019f42951d878e9e3405ee02b686CAS |
Castillo FJ (1996) Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery. Oecologia 107, 469–477.
| Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznsFyqug%3D%3D&md5=7822a1f40186470ad06a17e20a5b0f16CAS |
Cela J, Arrom L, Munné SB (2009) Diurnal changes in photosystem II photochemistry, photoprotective compounds and stress-related phytohormones in the CAM plant, Aptenia cordifolia. Plant Science 177, 404–410.
| Diurnal changes in photosystem II photochemistry, photoprotective compounds and stress-related phytohormones in the CAM plant, Aptenia cordifolia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKktr7O&md5=ad9712c7ef33852cc447fb2e257aab65CAS |
Cushman J, Borland A (2002) Induction of crassulacean acid metabolism by water limitation. Plant, Cell & Environment 25, 295–310.
| Induction of crassulacean acid metabolism by water limitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakuro%3D&md5=f94d6326bae3dd11531953ede5d0a372CAS |
De Gara L, Locato V, Dipierro S, Pinto MC (2010) Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respiratory Physiology & Neurobiology 173, S13–S19.
| Redox homeostasis in plants. The challenge of living with endogenous oxygen production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVOis70%3D&md5=1c0758cc8ad4fcd36204b74d59026b0aCAS |
Delaplace P, Fauconnier ML, Jardin P (2010) Antioxidants involvement in the ageing of non-green organs: the potato tuber as a model. ‘Reactive oxygen species and antioxidants in higher plants’. (Ed. S Dutta Gupta) pp. 205–228. (Science Publishers: Enfield, NH, USA)
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
| Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSgs70%3D&md5=d7973de9177e493fc72042664098df39CAS |
Freschi L, Mercier H (2012) Connecting environmental stimuli and crassulacean acid metabolism expression: phytohormones and other signaling molecules. ‘Progress in botany. Vol. 73’. (Eds U Lüttge, W Beyschlag, B Büdel, D Francis) pp. 231–255. (Springer: Berlin)
Freschi L, Rodrigues MA, Tiné MAS, Mercier H (2010a) Correlation between citric acid and nitrate metabolisms during CAM cycle in the atmospheric bromeliad Tillandsia pohliana. Journal of Plant Physiology 167, 1577–1583.
| Correlation between citric acid and nitrate metabolisms during CAM cycle in the atmospheric bromeliad Tillandsia pohliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2itL%2FE&md5=06376236fbac7d9d19de59d474d66091CAS |
Freschi L, Takahashi CA, Cambui CA, Semprebom TR, Cruz AB, Mioto PT, Versieux L de M, Calvente A, Latansio-Aidar SR, Aidar MPM, Mercier H (2010b) Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage. Journal of Plant Physiology 167, 526–533.
| Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1Krsro%3D&md5=0560bb4e684b226d259f15ddd33b63edCAS |
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
| Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKnu7fF&md5=7b82092aa9a1ff517035845aa906e844CAS |
González-Salvatierra C, Andrade LJ, Escalante-Erosa F, García-Sosa K, Peña-Rodríguez ML (2010) Antioxidant content in two CAM bromeliad species as a response to seasonal light changes in a tropical dry deciduous forest. Journal of Plant Physiology 167, 792–799.
| Antioxidant content in two CAM bromeliad species as a response to seasonal light changes in a tropical dry deciduous forest.Crossref | GoogleScholarGoogle Scholar |
Grams TEE, Haag-Kerwer A, Olivares E, Ball E, Arndt S, Popp M, Medina E, Lüttge U (1997) Comparative measurements of chlorophyll a fluorescence, acid accumulation and gas exchange in exposed and shaded plants of Clusia minor L. and Clusia multiflora H.B.K. in the field. Trees 11, 240–247.
Griffiths H, Maxwell K (1999) In memory of CS Pittendrigh: does exposure in forest canopies relate to photoprotective strategies in epiphytic bromeliads? Functional Ecology 13, 15–23.
| In memory of CS Pittendrigh: does exposure in forest canopies relate to photoprotective strategies in epiphytic bromeliads?Crossref | GoogleScholarGoogle Scholar |
Habibi G, Hajiboland R (2011) Comparison of water stress and UV radiation effects on induction of CAM and antioxidative defense in the succulent Rosularia elymaitica (Crassulaceae). Acta Biologica Cracoviensia. Series; Botanica 53, 15–24.
| Comparison of water stress and UV radiation effects on induction of CAM and antioxidative defense in the succulent Rosularia elymaitica (Crassulaceae).Crossref | GoogleScholarGoogle Scholar |
Habibi G, Hajiboland R (2012) Comparison of photosynthesis and antioxidative protection in Sedum album and Sedum stoloniferum (Crassulaceae) under water stress. Photosynthetica 50, 508–518.
| Comparison of photosynthesis and antioxidative protection in Sedum album and Sedum stoloniferum (Crassulaceae) under water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFSgtL3P&md5=ed28bb84a5a2b7a30c218058f3b146b0CAS |
Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. ‘Plant stress tolerance: methods and protocols’. (Ed. R Sunkar) pp. 291–297. (Humana Press: New York)
Jiang Y, Watkins E (2010) Antioxidative responses and candidate gene expression in Prairie Junegrass under drought stress. Journal of the American Society for Horticultural Science 135, 303–309.
Jiang ZY, Woollard ACS, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26, 853–856.
| Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XjtVKm&md5=d9d685216c49bcb2fd28841d8196f7eeCAS |
Junglee S, Urban L, Sallanon H, Lopez-lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. American Journal of Analytical Chemistry 5, 730–736.
| Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFKnsb3E&md5=5c2ed52f717beb09c3d554429b8d97d9CAS |
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annual Review of Plant Biology 60, 239–260.
| Sensing and responding to excess light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGls7k%3D&md5=5cdc8fec4565bed205d14d6879517af0CAS |
Luo YL, Su ZL, Cui XL, Lan QY (2015) Water loss prevention plays a greater role than ROS scavenging in dehydration tolerance of Kalanchoe tubiflora epiphyllous buds. Israel Journal of Plant Sciences 62, 153–159.
| Water loss prevention plays a greater role than ROS scavenging in dehydration tolerance of Kalanchoe tubiflora epiphyllous buds.Crossref | GoogleScholarGoogle Scholar |
Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. Journal of Experimental Botany 53, 2131–2142.
| CO2-concentrating: consequences in crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Annals of Botany 93, 629–652.
| Ecophysiology of crassulacean acid metabolism (CAM).Crossref | GoogleScholarGoogle Scholar |
Males J (2017) Adaptive variation in vein placement underpins diversity in a major neotropical plant radiation. Oecologia 185, 375–386.
| Adaptive variation in vein placement underpins diversity in a major neotropical plant radiation.Crossref | GoogleScholarGoogle Scholar |
Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant & Cell Physiology 51, 190–200.
| Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1Kjurg%3D&md5=915cdd45c1c0298e88fe10338353524eCAS |
Mattos LM, Moretti CL (2015) Oxidative stress in plants under drought conditions and the role of different enzymes. Enzyme Engineering 5, 1–6.
Maxwell K, Griffiths H, Young AJ (1994) Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle. Functional Ecology 8, 746–754.
| Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle.Crossref | GoogleScholarGoogle Scholar |
Maxwell K, Griffiths H, Borland AM, Young AJ, Broadmeadow MSJ, Fordham MC (1995) Short-term photosynthetic responses of the C3-CAM epiphyte Guzmania monostachia var. monostachia to tropical seasonal transitions under field conditions. Australian Journal of Plant Physiology 22, 771–781.
| Short-term photosynthetic responses of the C3-CAM epiphyte Guzmania monostachia var. monostachia to tropical seasonal transitions under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpt12hs78%3D&md5=a68865989870577a4df2d51ce39429aeCAS |
Maxwell K, Marrison JL, Leech RM, Griffiths H, Horton P (1999) Chloroplast acclimation in leaves of Guzmania monostachia in response to high light. Plant Physiology 121, 89–96.
| Chloroplast acclimation in leaves of Guzmania monostachia in response to high light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGlsLo%3D&md5=a2c74c51a65dbd0df76f333be717eac2CAS |
Minocha R, Martinez G, Lyons B, Long S (2009) Development of a standardized methodology for quantifying total chlorophyll and carotenoids from foliage of hardwood and conifer tree species. Canadian Journal of Forest Research 39, 849–861.
| Development of a standardized methodology for quantifying total chlorophyll and carotenoids from foliage of hardwood and conifer tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlSrsLo%3D&md5=b1d56e084e461ab1cd11a519a54e2913CAS |
Mioto PT, Mercier H (2013) Abscisic acid and nitric oxide signaling in two different portions of detached leaves of Guzmania monostachia with CAM up-regulated by drought. Journal of Plant Physiology 170, 996–1002.
| Abscisic acid and nitric oxide signaling in two different portions of detached leaves of Guzmania monostachia with CAM up-regulated by drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFOhtrs%3D&md5=50b90cd5bdfc7627138d6dd1e81062a9CAS |
Miszalski Z, Niewiadomska E, Ślesak I, Lüttge U, Kluge M, Ratajczak R (2001) The effect of irradiance on carboxylating/decarboxylating enzymes and fumarase activities in Mesembryanthemum crystallinum L. exposed to salinity stress. Plant Biology 3, 17–23.
| The effect of irradiance on carboxylating/decarboxylating enzymes and fumarase activities in Mesembryanthemum crystallinum L. exposed to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFOlsrs%3D&md5=0b414a83cf724a340efe9d308585107fCAS |
Niewiadomska E, Borland AM (2008) Crassulacean acid metabolism: a cause or consequence of oxidative stress in planta? ‘Progress in botany. Vol. 69’. (Eds U Lüttge, W Beyschlag, J Murata) pp. 247–266. (Springer: Berlin)
Niewiadomska E, Miszalski Z, Ślesak I, Ratajczak R (1999) Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves. Free Radical Research 31, 251–256.
| Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves.Crossref | GoogleScholarGoogle Scholar |
North GB, Lynch FH, Maharaj FD, Phillips CA, Woodside WT (2013) Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water. Frontiers in Plant Science 4, 78
| Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water.Crossref | GoogleScholarGoogle Scholar |
Oelze ML, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A, Maurino VG, Dietz KJ (2012) Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals. Journal of Experimental Botany 63, 1297–1313.
| Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Olt7s%3D&md5=991443d696b68c9c3470f746c28a2e90CAS |
Popp M, Janett HP, Lüttge U, Medina E (2003) Metabolite gradients and carbohydrate translocation in rosette leaves of CAM and C3 bromeliads. New Phytologist 157, 649–656.
| Metabolite gradients and carbohydrate translocation in rosette leaves of CAM and C3 bromeliads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisF2nsr8%3D&md5=e6f07471b03ac2ac07437e0c23ca050cCAS |
Rodrigues MA, Hamachi L, Mioto PT, Purgatto E, Mercier H (2016) Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia. Plant Physiology and Biochemistry 108, 400–411.
| Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtl2murbL&md5=ccdb7468ea3f160eec67378f72a7add6CAS |
Schmitt AK, Lee HSJ, Lüttge U (1988) The response of the C3-CAM tree, Clusia rosea, to light and water stress. Journal of Experimental Botany 39, 1581–1590.
| The response of the C3-CAM tree, Clusia rosea, to light and water stress.Crossref | GoogleScholarGoogle Scholar |
Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regulation 46, 209–221.
| Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKit77M&md5=dbe68c0bfd8c267c0ab8f981cdd85406CAS |
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Le Journal de Botanique 2012, 1–26.
Ślesak I, Karpinska B, Surówka E, Miszalski Z, Karpinski S (2003) Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L. Plant & Cell Physiology 44, 573–581.
| Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar |
Ślesak I, Libik M, Miszalski Z (2008) The foliar concentration of hydrogen peroxide during salt-induced C3-CAM transition in Mesembryanthemum crystallinum L. Plant Science 174, 221–226.
| The foliar concentration of hydrogen peroxide during salt-induced C3-CAM transition in Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar |
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences 16, 13561–13578.
| Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslymtbnE&md5=d1f3105cef15fcbbcf358e0ed9165d4bCAS |
Souza SR, Blande JD, Holopainen JK (2013) Pre-exposure to nitric oxide modulates the effect of ozone on oxidative defenses and volatile emissions in lima bean. Environmental Pollution 179, 111–119.
| Pre-exposure to nitric oxide modulates the effect of ozone on oxidative defenses and volatile emissions in lima bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXoslaisrw%3D&md5=01a99704342ba46cdcac2a7f377ff110CAS |
Spalding MH, Stumpf DK, Ku MSB, Burris RH, Edwards GE (1979) Crassulacean acid metabolism and diel variations of internal CO2 and O2 concentrations in Sedum praeltum DC. Australian Journal of Plant Physiology 6, 557–567.
| Crassulacean acid metabolism and diel variations of internal CO2 and O2 concentrations in Sedum praeltum DC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhvV2ktg%3D%3D&md5=4824a6cf0cfa11f9673c97c1a3e5d335CAS |
Storr SJ, Woolston CM, Zhang Y, Martin SG (2013) Redox environment, free radical, and oxidative DNA damage. Antioxidants & Redox Signalling 18, 2399–2408.
| Redox environment, free radical, and oxidative DNA damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFKnsLk%3D&md5=941af7624fbe38484ef5b6fd540539bfCAS |
Sunagawa H, Cushman JC, Agarie S (2010) Crassulacean acid metabolism may alleviate production of reactive oxygen species in a facultative CAM plant, the common ice plant Mesembryanthemum crystallinum L. Plant Production Science 13, 256–260.
| Crassulacean acid metabolism may alleviate production of reactive oxygen species in a facultative CAM plant, the common ice plant Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCmsrfP&md5=2e624da9cee626527a9b662da5f94a1aCAS |
Szechyńska-Hebda M, Karpinski S (2013) Light intensity-dependent retrograde signalling in higher plants. Journal of Plant Physiology 170, 1501–1516.
| Light intensity-dependent retrograde signalling in higher plants.Crossref | GoogleScholarGoogle Scholar |
Takahashi CA, Ceccantini GCT, Mercier H (2007) Differential capacity of nitrogen assimilation between apical and basal leaf portions of a tank epiphytic bromeliad. Brazilian Journal of Plant Physiology 19, 119–126.
| Differential capacity of nitrogen assimilation between apical and basal leaf portions of a tank epiphytic bromeliad.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aitrY%3D&md5=61a41ce4232fcd7440af3888e96479dbCAS |
Weng X, Zheng C-J, Xu H-X, Sun J (2007) Characteristics of photosynthesis and functions of the water-water cycle in rice (Oryza sativa) leaves in response to potassium deficiency. Physiologia Plantarum 131, 614–621.
| Characteristics of photosynthesis and functions of the water-water cycle in rice (Oryza sativa) leaves in response to potassium deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVersL7P&md5=05328c56abd8371945a9e47459bd7aefCAS |
Yadav MK, Bhatla SC (2011) Localization of lipoxygenase activity on the oil bodies and in protoplasts using a novel fluorescence imaging method. Plant Physiology and Biochemistry 49, 230–234.
| Localization of lipoxygenase activity on the oil bodies and in protoplasts using a novel fluorescence imaging method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVaruro%3D&md5=611ae6cde39854bf27c5a99629cf9284CAS |
Zwieniecki MA, Boyce CK (2014) Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings. Biological Sciences 281, 20132829
| Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology.Crossref | GoogleScholarGoogle Scholar |
