Does age matter under winter photoinhibitory conditions? A case study in stems and leaves of European mistletoe (Viscum album)
Fátima Míguez A B , Beatriz Fernández-Marín A , Antonio Hernández A , José Maria Becerril A and José Ignacio García-Plazaola AA Department of Plant Biology and Ecology, University of Basque country (UPV/EHU) Apdo 644, 48080 Bilbao, Spain.
B Corresponding author. Email: fatimamiguezcano@gmail.com
Functional Plant Biology 42(2) 175-185 https://doi.org/10.1071/FP14083
Submitted: 27 March 2014 Accepted: 3 August 2014 Published: 12 September 2014
Abstract
European mistletoe (Viscum album L.) is a hemiparasitic plant with perennial leaves and photosynthetic stems easily discernible according to their age. These properties make V. album the perfect species to (i) compare the mechanisms of seasonal acclimation of photosynthetic stems with those of leaves, and (ii) evaluate the influence of ageing in the efficiency of photosynthetic tissues. To achieve these general objectives, photosynthetic pigments, maximal photochemical efficiency of PSII (Fv/Fm), recovery kinetics and key thylakoidal proteins were analysed during winter and spring in leaves and at different age stems. During winter, some woody species are able to maintain photosynthetic activity, but at lower rates than during spring. In the case of V. album, photosynthetic relevance of green stems appears equal to leaves in terms of total area. Besides, mistletoe stems are able to maintain higher Fv/Fm and lower level of antioxidants than leaves, especially during winter season. The recovery from winter photoinhibition is also faster in stems than in leaves. Thylakoidal protein composition (mainly high levels of D1) also supports the idea of stems as main photosynthetic organs in V. album during winter. Further, in winter, the level of photoinhibition of V. album stems decreased concomitantly with ageing. This work highlights the importance of stem photosynthesis in plant carbon balance and demonstrates that ageing does not necessarily imply a loss of vitality in stems.
Additional keywords: ageing, Fv/Fm, pigments, thylakoidal proteins, tocopherols, V-cycle, winter photoinhibition.
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 |
Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora 198, 81–97.
| Non-foliar photosynthesis – a strategy of additional carbon acquisition.Crossref | GoogleScholarGoogle Scholar |
Aschan G, Wittmann C, Pfanz H (2001) Age-dependent bark photosynthesis of aspen twigs. Trees 15, 431–437.
| Age-dependent bark photosynthesis of aspen twigs.Crossref | GoogleScholarGoogle Scholar |
Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends in Plant Science 5, 349–353.
| Age-related changes in photosynthesis of woody plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvhtFCktA%3D%3D&md5=4a4bfbf2a382505977e6481b466b8a39CAS | 10908880PubMed |
Day ME, Greenwood MS, Díaz-Sala C (2002) Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiology 22, 507–513.
| Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zgsVeiuw%3D%3D&md5=6fea66b06ffa2d1d58578fa2eed6d373CAS | 12045024PubMed |
Dobbertin M, Hilker N, Rebetez M, Zimmermann NE, Wohlgemuth T, Rigling A (2005) The upward shift in altitude of pine mistletoe (Viscum album ssp. austriacum) in Switzerland – the result of climate warming? International Journal of Biometeorology 50, 40–47.
| The upward shift in altitude of pine mistletoe (Viscum album ssp. austriacum) in Switzerland – the result of climate warming?Crossref | GoogleScholarGoogle Scholar | 15875222PubMed |
Escher P, Eiblmeier M, Hetzger I, Rennenberg H (2004) Spatial and seasonal variation in amino compounds in the xylem sap of a mistletoe (Viscum album) and its hosts (Populus spp and Abies alba). Tree Physiology 24, 639–650.
| Spatial and seasonal variation in amino compounds in the xylem sap of a mistletoe (Viscum album) and its hosts (Populus spp and Abies alba).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlylurc%3D&md5=ad93c57ba64e811fafe7d1b10d4cb248CAS | 15059764PubMed |
Falk S, Maxwell DP, Laudenbach DE, Huner NPA (1996) Photosynthetic adjustment to temperature. In ‘Photosynthesis and environment’. (Ed. NR Baker) pp. 367–385. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Filippou M, Fasseas C, Karabournioti G (2007) Photosynthetic characteristics of olive tree (Olea europaea) bark. Tree Physiology 27, 977–984.
| Photosynthetic characteristics of olive tree (Olea europaea) bark.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslGgtrY%3D&md5=368b7414367e9283ff43665d74cddf6aCAS | 17403650PubMed |
Fineran H (1995) Green tissue within the haustorium of the dwarf mistletoe Korthalsella (Viscaceae). An ultrastructural comparison between chloroplasts of sucker and aerial stem tissues. Protoplasma 189, 216–228.
| Green tissue within the haustorium of the dwarf mistletoe Korthalsella (Viscaceae). An ultrastructural comparison between chloroplasts of sucker and aerial stem tissues.Crossref | GoogleScholarGoogle Scholar |
Fleming AJ (2005) The control of leaf development. New Phytologist 166, 9–20.
| The control of leaf development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtlakurc%3D&md5=c50150d8effb08ba79cbf5551162a363CAS | 15760347PubMed |
García MB, Dahlgren JP, Erhlen J (2011) No evidence of senescence in a 300-year-old mountain herb. Journal of Ecology 99, 1424–1430.
| No evidence of senescence in a 300-year-old mountain herb.Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Becerril JM (1999) A rapid HPLC method to measure lipophilic antioxidans in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochemical Analysis 10, 307–313.
| A rapid HPLC method to measure lipophilic antioxidans in stressed plants: simultaneous determination of carotenoids and tocopherols.Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Becerril JM (2001) Seasonal changes in photosynthetic pigments and antioxidans in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Australian Journal of Plant Physiology 28, 225–232.
García-Plazaola JI, Hernández A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biology 30, 319–324.
| The operation of the lutein epoxide cycle correlates with energy dissipation.Crossref | GoogleScholarGoogle Scholar |
Hincha DK, Meins F, Schmitt JM (1997) β-1.3-glucanase is cryoprotective in vitro and is accumulated in leaves during cold acclimation. Plant Physiology 114, 1077–1083.
Jeffree CE, Jeffree EP (1996) Redistribution of the potential geographical ranges of mistletoe and Colorado beetle in Europe in response to the temperature component of climate change. Functional Ecology 10, 562–577.
| Redistribution of the potential geographical ranges of mistletoe and Colorado beetle in Europe in response to the temperature component of climate change.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Haridasan M, Fernandes GW, de Mattos EA, Trimborn P, Franco AC, Caldas LS, Ziegler H (1998) Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil. Trees 12, 167–174.
| Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil.Crossref | GoogleScholarGoogle Scholar |
Matsubara S, Gilmore AM, Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein expoxide in the Australian mistletoe Amyema miquelii. Australian Journal of Plant Physiology 28, 793–800.
Morales M, Oñate M, García MB, Munné-Bosch S (2013) Photo-oxidative stress markers reveal absence of physiological deterioration with ageing in Bordera pirenaica, an extraordinarily long-lived herb. Journal of Ecology 101, 555–565.
| Photo-oxidative stress markers reveal absence of physiological deterioration with ageing in Bordera pirenaica, an extraordinarily long-lived herb.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXms1Gktrg%3D&md5=d1b61007d9fe0a72dd9934105effd7d7CAS |
Munné-Bosch S, Lalueza P (2007) Age-related changes in oxidative stress markers and abscisic acid levels in a drought-tolerant shrub, Cistus clusii grown under Mediterranean field conditions. Planta 225, 1039–1049.
| Age-related changes in oxidative stress markers and abscisic acid levels in a drought-tolerant shrub, Cistus clusii grown under Mediterranean field conditions.Crossref | GoogleScholarGoogle Scholar | 17043890PubMed |
Niinemets Ü (1999) Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144, 35–47.
| Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü, Anten NPR (2009) Packing photosynthesis machinery: from leaf to canopy. In ‘Photosynthesis in silico: understanding complexity from molecules to ecosystems’. (Eds A Laisk, L Nebdal, Govindjee) pp. 363–399. (Springer-Verlag: Berlin)
Niinemets Ü, Kull O, Tenhunen JD (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell & Environment 27, 293–313.
| Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2gtr4%3D&md5=20c67ae8a29b5c7218e26e37d3bb23f6CAS |
Niinemets Ü, García-Plazaola JI, Tosens T (2012) Photosynthesis during leaf development and ageing. In ‘Terrestrial photosynthesis in a changing environment: a molecular, physiological and ecological approach’. (Eds J Flexas, F Loreto, H Medrano) pp. 353–372. (Cambridge University Press: Cambridge, UK)
North HM, De Almeida A, Boutin JP, Frey A, To A, Botran L, Sotta B, Marion-Poll A (2007) The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulations is via neoxanthin isomers. The Plant Journal 50, 810–824.
| The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulations is via neoxanthin isomers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntV2ks7c%3D&md5=9e21af3976adddd4de6501cd1fcb9899CAS | 17470058PubMed |
Osborne CP, Chaloner WG, Beerling DJ (2004) Falling atmospheric CO2 – the key to megaphyll leaf origins. In ‘The evolution of plant physiology’. (Eds AR Hemsley, I Poole) pp. 197–215. (Elsevier Academic Press: London, UK)
Osmond CB, Smith SD, Gui-Ying B, Sharkey TD (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapour exchange under controlled conditions. Oecologia 72, 542–549.
| Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapour exchange under controlled conditions.Crossref | GoogleScholarGoogle Scholar |
Ottander C, Öquist G (1991) Recovery of photosynthesis in winter-stressed Scots pine. Plant, Cell & Environment 14, 345–349.
| Recovery of photosynthesis in winter-stressed Scots pine.Crossref | GoogleScholarGoogle Scholar |
Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197, 176–183.
| Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnvVKrt7s%3D&md5=9d66868f309a1b45e4f154c0f244a119CAS |
Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften 89, 147–162.
| Ecology and ecophysiology of tree stems: corticular and wood photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1GhsL4%3D&md5=1aaa29666a4a93a8819fd7ae985a5a98CAS | 12061398PubMed |
Sáez PL, Bravo LA, Latsague MI, Toneatti MJ, Sánchez-Olate M, Ríos DG (2013) Light energy management in micropropagated plants of Castanea sativa, effects of photoinhibition. Plant Science 201–202, 12–24.
| Light energy management in micropropagated plants of Castanea sativa, effects of photoinhibition.Crossref | GoogleScholarGoogle Scholar | 23352399PubMed |
Stokes VJ, Morecroft MD, Morison JIL (2006) Boundary layer conductance for contrasting leaf shapes in a deciduous broadleaved canopy. Agricultural and Forest Meteorology 139, 40–54.
| Boundary layer conductance for contrasting leaf shapes in a deciduous broadleaved canopy.Crossref | GoogleScholarGoogle Scholar |
Strong GL, Bannister P, Burritt DD (2000) Are mistletoes shade plants? CO2 assimilation and chlorophyll fluorescence of temperate mistletoes and their hosts. Annals of Botany 85, 511–519.
| Are mistletoes shade plants? CO2 assimilation and chlorophyll fluorescence of temperate mistletoes and their hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFelsrk%3D&md5=e31bf2debff771fc3b23926c94fccab0CAS |
Strong GL, Bannister P, Burritt DD (2001) New Zealand mistletoes have equal or lower capacities for electron transport than their hosts. New Zealand Journal of Botany 39, 171–174.
| New Zealand mistletoes have equal or lower capacities for electron transport than their hosts.Crossref | GoogleScholarGoogle Scholar |
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571–599.
| Plant cold acclimation: freezing tolerance genes and regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yktrw%3D&md5=68debb4db83316712202814c0bf822cfCAS | 15012220PubMed |
Tinoco-Ojanguren C (2008) Dirunal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. Journal of Arid Environments 72, 127–140.
| Dirunal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert.Crossref | GoogleScholarGoogle Scholar |
Vaupel JW, Baudisch A, Dölling M, Roach DA, Gampe J (2004) The case for negative senescence. Theoretical Population Biology 65, 339–351.
| The case for negative senescence.Crossref | GoogleScholarGoogle Scholar | 15136009PubMed |
Verhoeven A (2014) Sustained energy dissipation in winter evergreens. New Phytologist 201, 57–65.
| Sustained energy dissipation in winter evergreens.Crossref | GoogleScholarGoogle Scholar |
Verhoeven AS, Adams WW, Demmig-Adams B (1999) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118, 277–287.
| The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress.Crossref | GoogleScholarGoogle Scholar |
Wittmann C, Pfanz H (2007) Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees. Journal of Experimental Botany 58, 4293–4306.
| Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymu74%3D&md5=afe382eac038118adc7401439fab17afCAS | 18182432PubMed |
Yamashita N, Koike N, Ishida A (2002) Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant, Cell & Environment 25, 1341–1356.
| Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status.Crossref | GoogleScholarGoogle Scholar |
Yiotis C, Psaras GK, Manetas Y (2008) Seasonal photosynthetic changes in the green-stemmed Mediterranean shrub Calicotome villosa: a comparison with leaves. Photosynthetica 46, 262–267.
| Seasonal photosynthetic changes in the green-stemmed Mediterranean shrub Calicotome villosa: a comparison with leaves.Crossref | GoogleScholarGoogle Scholar |
Ziegler H, Weber J, Lüttge UE (2009) Thermal dissipation probe measurements of sapflow in the xylem of trees documenting dynamic relations to variable transpiration given by instantaneous weather changes and the activities of a mistletoe xylem parasite. Trees 23, 441–450.
| Thermal dissipation probe measurements of sapflow in the xylem of trees documenting dynamic relations to variable transpiration given by instantaneous weather changes and the activities of a mistletoe xylem parasite.Crossref | GoogleScholarGoogle Scholar |
Zuber D (2004) Biological flora of central Europe: Viscum album L. Flora 199, 181–203.
| Biological flora of central Europe: Viscum album L.Crossref | GoogleScholarGoogle Scholar |