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Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap

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Abstract

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We found mistletoe accumulates nutrient elements in its structure as a trap and causes a severe drought stress in the Scots pine in dry summer seasons.

Abstract

The mistletoe [Viscum album ssp. austriacum (Wiesbaur) Vollm.] is a hemiparasitic plant, and its infestation is known to play an important role on the mortality of Scots pines (Pinus sylvestris L.), but there is little knowledge about its action mechanism. This study, therefore, tried to gain a better understanding of the destructive effect of the mistletoe on the growth and water uptake mechanism of the Scots pine. Identical needles from neighboring plants (healthy and infested) were harvested in the middle of each month (from April to October 2013) and used as research material. Infestation success of the mistletoe was investigated by evaluating the contents of the endogenous nutrient elements such as potassium, phosphorus, calcium, sulfur, magnesium, iron, copper, zinc, manganese, boron, nickel, and sodium in both mistletoe leaves and the needles of healthy and infested Scots pine. Its effects were also evaluated by determining the content of water, chlorophyll, and dry matter, and the length of the newly formed needles of the healthy and infested trees. Mistletoe infestation led to a decrease in the availability of water and mineral nutrients, and caused a powerful inhibition on the growth parameters such as chlorophyll, dry matter, and the length of needles by accumulating the essential nutrient minerals in its structure. The findings of this study indicate that the mistletoe accumulates the nutrient elements in its structure as a trap and causes a severe drought stress in the Scots pine in dry summer seasons, thereby playing a potent role in the increasing mortality rate in the Scots pine.

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References

  • Ache P, Bauer H, Kollist H, Al-Rasheid KAS, Lautner S, Hartung W, Hedrich R (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant J 62:1072–1082

    CAS  PubMed  Google Scholar 

  • Allen CD, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Gonzales P, Hogg T, Rigling A, Breshears D et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684

    Article  Google Scholar 

  • Baquedano FJ, Castillo FJ (2006) Comparative ecophysiological effects of drought on seedlings of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera and Quercus ilex. Trees Struct Funct 20:689–700

    Article  Google Scholar 

  • Bell T, Adams M (2011) Attack on all fronts: functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiol 31:3–15

    Article  CAS  PubMed  Google Scholar 

  • Bigler C, Braker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9:330–343

    Article  Google Scholar 

  • Bolin J, Tennacoon K, Maass E (2010) Mineral nutrition and heterotrophy in the water conservative holoparasite Hydnora Thunb. Flora 205:802–810

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Buckley TN, Mott KA, Farquhar GD (2003) A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ 26:1767–1785

    Article  CAS  Google Scholar 

  • Catal Y, Carus S (2011) Effect of pine mistletoe on radial growth of Crimean pine (Pinus nigra) in Turkey. J Environ Biol 32:263–270

    PubMed  Google Scholar 

  • Cech TL, Perny B (2000) Kiefernsterben in Tirol. Forstschutz Aktuell Wien 22:12–15

    Google Scholar 

  • Dobbertin M, Rigling A (2006) Pine mistletoe (Viscum album ssp. austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. For Pathol 36:309–322

    Google Scholar 

  • Dobbertin M, Hilker N, Rebetez M, Zimmermann NE, Wohlgemoth T, Rigling A (2005) The upward shift in altitude of pine mistletoe (Viscum album ssp. austriacum) in Switzerland the result of climate warming? Int J Biometeorol 50:40–47

    Article  PubMed  Google Scholar 

  • Eilmann B, Weber P, Rigling A, Eckstein D (2006) Growth reactions of Pinus sylvestris L. and Quercus pubescens Willd. to drought years at a xeric site in Valais, Switzerland. Dendrochronologia 23:121–132

    Article  Google Scholar 

  • Erbilgin N, Raffa KF (2002) Association of declining red pine stands with reduced populations of bark beetle predators, seasonal increases in root colonizing insects, and incidence of root pathogens. For Ecol Manag 164:221–236

    Article  Google Scholar 

  • Escher P, Peuke AD, Bannister P, Fink S, Hartung W, Jiang F, Rennenberg H (2008) Transpiration, CO2 assimilation, WUE, and stomatal aperture in leaves of Viscum album (L.): effect of abscisic acid (ABA) in the xylem sap of its host (Populus euamericana). Plant Physiol Biochem 46:64–70

    Article  CAS  PubMed  Google Scholar 

  • Ewers BE, Mackay DS, Samanta S (2007) Interannual consistency in canopy stomatal conductance control of leaf water potential across seven tree species. Tree Physiol 27:11–24

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Medrano H (2002) Energy dissipation in C3 plants under drought. Funct Plant Biol 29:1209–1215

    Article  CAS  Google Scholar 

  • Gao D, Gao Q, Xu H-Y, Ma F, Zhao C-M, Liu J-Q (2009) Physiological responses to gradual drought stress in the diploid hybrid Pinus densata and its two parental species. Trees Struct Funct 23:717–728

    Article  CAS  Google Scholar 

  • Giuggiola A, Bugmann H, Zingg A, Dobbertin M, Rigling A (2013) Reduction of stand density increases drought resistance in xeric Scots pine forests. For Eco. Manag 310:827–835

    Article  Google Scholar 

  • Glatzel G (1983) Mineral nutrition and water relations of hemiparasitic mistletoes: a question of partitioning. Experiments with Loranthus europaeus on Quercus petrea and Quercus robur. Oecologia 56:193–201

    Article  Google Scholar 

  • Glatzel G (1996) Ecophysiology of Amyema mackayense, a mistletoe on a salt excreting mangrove host. Adv Parasit Plant Res 36:293–302

    Google Scholar 

  • Glatzel G, Geils BW (2009) Mistletoe ecophysiology: host-parasite interactions. Botany 87:10–15

    Article  CAS  Google Scholar 

  • Gullo MAL, Glatzel G, Devkota M, Raimondo F, Trifilo P, Richter H (2012) Mistletoes and mutant albino shoots on woody plants as mineral nutrient traps. Ann Bot Lond 109:1101–1109

    Article  Google Scholar 

  • Hibberd JM, Jeschke WD (2001) Solute flux into parasitic plants. J Exp Bot 52:2043–2049

    Article  CAS  PubMed  Google Scholar 

  • Hosseini SM, Kartoolinejad D, Mirnia SK, Tabibzadeh Z, Akbarinia M, Shayanmehr F (2007) The effects of Viscum Album L. on foliar weight and nutrients content of host trees in Caspian forests (Iran). Pol J Ecol 55:579–583

    CAS  Google Scholar 

  • Karunaichamy K, Paliwal K, Arp P (1999) Biomass and nutrient dynamics of mistletoe (Dendrophthoe falcata) and neem (Azadirachta indica) seedlings. Curr Sci Bangalore 76:840–843

    Google Scholar 

  • Kaya C, Ashraf M, Sonmez O (2015) Promotive effect of exogenously applied thiourea on key physiological parameters and oxidative defense mechanism in salt-stressed Zea mays L. plants. Turk J Bot 39:786–795

    Article  Google Scholar 

  • Kuijt J (1977) Haustoria of phanerogamic parasites. Ann Rev Phytopathol 15:91–118

    Article  Google Scholar 

  • Kuijt J, Toth R (1976) Ultrastructure of angiosperm haustoria-a review. Ann Bot Lond 40:1121–1130

    Google Scholar 

  • Lamont B, Southall K (1982) Distribution of mineral nutrients between the mistletoe Amyema preissii, and its host, Acacia acuminata. Ann Bot Lond 49:721–725

    Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Wrolstad RE (Ed.), Current protocols in food analytical chemistry. John Wiley and Sons, New York, pp F4.3.1–F4.3.8

  • Lüttge U, Haridasan M, Fernandes GW, de Mattos EA, Trimborn P, Franco AC, Caldas LS, Ziegler H (1998) Photosynthesis in mistletoes in relation to their hosts at various sites in tropical Brazil. Trees Struct Funct 12:167–174

    Article  Google Scholar 

  • Mathiasen RL, Nickrent DL, Shaw DC, Watson DM (2008) Mistletoes: pathology, systematics, ecology, and management. Plant Dis 92:988–1006

    Article  Google Scholar 

  • Mutlu S, Atici O, Esim N (2010) Bioherbicidal effects of essential oils of Nepeta meyeri Benth. on weed spp. Allelopath J 26:291–300

    Google Scholar 

  • Mutlu S, Atici O, Esim N, Mete E (2011) Essential oils of catmint (Nepeta meyeri Benth.) induce oxidative stress in early seedlings of various weed species. Acta Physiol Plant 33:943–951

    Article  CAS  Google Scholar 

  • Mutlu S, Atici O, Gulen Y (2013) Cement dust pollution induces toxicity or deficiency of some essential elements in wild plants growing around a cement factory. Toxicol Ind Health 29:474–480

    Article  PubMed  Google Scholar 

  • Olson AR, Kuijt J (1985) Sieve elements in the morphologically reduced mistletoe, Viscum minimum Harvey (Viscaceae). Am J Bot 72:1220–1224

    Article  Google Scholar 

  • Osma E, Ilhan V, Yalcin IE (2014) Heavy metals accumulation causes toxicological effects in aquatic Typha domingensis Pers. Braz J Bot 37:461–467

    Article  Google Scholar 

  • Press M, Smith S, Stewart G (1991) Carbon acquisition and assimilation in parasitic plants. Func Ecol 5:278–283

    Article  Google Scholar 

  • Reblin JS, Logan BA (2015) Impacts of eastern dwarf mistletoe on the stem hydraulics of red spruce and white spruce, two host species with different drought tolerances and responses to infection. Trees Struct Funct 29:475–486

    Article  Google Scholar 

  • Reid N, Yan ZG, Fittler J (1994) Impact of mistletoes (Amyema miquelii) on host (Eucalyptus blakelyi and Eucalyptus melliodora) survival and growth in temperate Australia. For Ecol Manag 70:55–65

    Article  Google Scholar 

  • Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant Cell Environ 25:1405–1414

    Article  Google Scholar 

  • Rigling A, Eilmann B, Koechli R, Dobbertin M (2010) Mistletoe-induced crown degradation in Scots pine in a xeric environment. Tree Physiol 30:845–852

    Article  PubMed  Google Scholar 

  • Sangüesa-Barreda G, Linares JC, Camarero JJ (2012) Mistletoe effects on Scots pine decline following drought events: insights from within-tree spatial patterns, growth and carbohydrates. Tree Physiol 32:585–598

    Article  PubMed  Google Scholar 

  • Sangüesa-Barreda G, Linares JC, Camarero JJ (2013) Drought and mistletoe reduce growth and water-use efficiency of Scots pine. For Ecol Manag 296:64–73

    Article  Google Scholar 

  • Shi GR, Cai QS (2009) Photosynthetic and anatomic responses of peanut leaves to zinc stress. Biol Plantarum 53:391–394

    Article  CAS  Google Scholar 

  • Strong GL, Bannister P, Burritt D (2000) Are mistletoes shade plants? CO2 assimilation and chlorophyll fluorescence of temperate mistletoes and their hosts. Ann Bot Lond 85:511–519

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc, Suderland

    Google Scholar 

  • Tennakoon KU, Pate JS (1996) Effects of parasitism by a mistletoe on the structure and functioning of branches of its host. Plant Cell Environ 19:517–528

    Article  Google Scholar 

  • Thabeet A, Vennetier M, Gadbin-Henry C, Denelle N, Roux M, Caraglio Y, Vila B (2009) Response of Pinus sylvestris L. to recent climatic events in the French Mediterranean region. Trees Struct Funct 23:843–853

    Article  Google Scholar 

  • Tsopelas P, Angelopoulos A, Economou A, Soulioti N (2004) Mistletoe (Viscum album) in the fir forest of Mount Parnis, Greece. For Ecol Manag 202:59–65

    Article  Google Scholar 

  • Ture C, Bocuk H, Asan Z (2010) Nutritional relationships between hemi-parasitic mistletoe and some of its deciduous hosts in different habitats. Biologia 65:859–867

    Article  Google Scholar 

  • Vacchiano G, Garbarino M, Mondino EB, Motta R (2012) Evidences of drought stress as a predisposing factor to Scots pine decline in Valle d’Aosta (Italy). Eur J For Res 131:989–1000

    Article  Google Scholar 

  • Weber P, Bugmann H, Fonti P, Rigling A (2008) Using a retrospective dynamic competition index to reconstruct forest succession. For Ecol Manag 254:96–106

    Article  Google Scholar 

  • Willmott CJ, Rowe CM, Mintz Y (1985) Climatology of the terrestrial seasonal water cycle. Int J Climatol 5:589–606

    Article  Google Scholar 

  • Ziegler H, Weber J, Lüttge UE (2009) Thermal dissipation probe measurements of sap flow 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 Struct Funct 23:441–450

    Article  Google Scholar 

  • Zuber D (2004) Biological flora of central Europe: Viscum album L. Flora 199:188–203

    Article  Google Scholar 

  • Zweifel R, Steppe K, Sterck FJ (2007) Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. J Exp Bot 58:2113–2131

    Article  CAS  PubMed  Google Scholar 

  • Zweifel R, Bangerter S, Rigling A, Sterck FJ (2012) Pine and mistletoes: how to live with a leak in the water flow and storage system? J Exp Bot 63:2565–2578

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Erzincan University for appropriating research funds (Project No: 12.02.05) and to the Turkish State Meteorological Service (TSMS) for providing meteorological data.

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Authors and Affiliations

  1. Department of Biology, Science and Art Faculty, Erzincan University, 24150, Erzincan, Turkey

    Salih Mutlu, Etem Osma, Veli Ilhan & Halil Ibrahim Turkoglu

  2. Department of Biology, Science Faculty, Ataturk University, 25240, Erzurum, Turkey

    Okkes Atici

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  1. Salih Mutlu
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  2. Etem Osma
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Correspondence to Salih Mutlu.

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Communicated by U. Luettge.

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Mutlu, S., Osma, E., Ilhan, V. et al. Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap. Trees 30, 815–824 (2016). https://doi.org/10.1007/s00468-015-1323-z

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  • DOI: https://doi.org/10.1007/s00468-015-1323-z

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