Climate and Competitive Status Modulate the Variation in Secondary Metabolites More in Leaves Than in Fine Roots of Betula pendula
Open accessAbstract
Plant secondary metabolites have many important functions; they also determine the productivity and resilience of trees under climate change. The effects of environmental factors on secondary metabolites are much better understood in above-ground than in below-ground part of the tree. Competition is a crucial biotic stress factor, but little is known about the interaction effect of climate and competition on the secondary chemistry of trees. Moreover, competition effect is usually overlooked when analyzing the sources of variation in the secondary chemistry. Our aim was to clarify the effects of competitive status, within-crown light environment, and climate on the secondary chemistry of silver birch (Betula pendula Roth). We sampled leaves (from upper and lower crown) and fine roots from competitively dominant and suppressed B. pendula trees in plantations along a latitudinal gradient (56–67° N) in Fennoscandia, with mean annual temperature (MAT) range: −1 to 8°C. Secondary metabolites in leaves (SM L) and fine roots (SM FR) were determined with an HPLC-qTOF mass spectrometer. We found that SM L content increased significantly with MAT. The effect of competitive stress on SM L strengthened in colder climates (MAT<4°C). Competition and shade initiated a few similar responses in SM L. SM FR varied less with MAT. Suppressed trees allocated relatively more resources to SM L in warmer climates and to SM FR in colder ones. Our study revealed that the content and profile of secondary metabolites (mostly phenolic defense compounds and growth regulators) in leaves of B. pendula varied with climate and reflected the trees’ defense requirements against herbivory, exposure to irradiance, and competitive status (resource supply). The metabolic profile of fine roots reflected, besides defense requirements, also different below-ground competition strategies in warmer and colder climates. An increase in carbon assimilation to secondary compounds can be expected at northern latitudes due to climate change.
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The concentration of these metabolites can vary significantly due to environmental factors such as climate, soil type, and stressors specific to the region.
“However, the concentration of these metabolites can vary significantly due to environmental factors such as climate, soil type, and stressors specific to the region, underscoring the need for localized phytochemical studies [12].”
From Comparative Analysis of Infusions and Ethanolic Extracts of Annona muricata Leaves from Colima, Mexico: Phytochemical Profile and Antioxidant Activity (2024) · cites this paper as [12]
The Discussion (page unavailable) reports significant variation in birch secondary-metabolite profiles with mean annual temperature and competition, and states that soil type can affect tree secondary chemistry. The Introduction links metabolite content to plant stress. However, the study’s soils were relatively uniform, so it did not demonstrate an effect of soil type or identify stressors specific to a region. (LLM, conf=0.84)
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Cites
The Dilemma of Plants: To Grow or Defend
Herms, D. A., & Mattson, W. J. (1992) · The Quarterly Review of Biology · doi:10.1086/417659 · Cited by 4,287 · see citing works
NITROGEN LIMITATION OF NET PRIMARY PRODUCTIVITY IN TERRESTRIAL ECOSYSTEMS IS GLOBALLY DISTRIBUTED
LeBauer, D. S., & Treseder, K. K. (2008) · Ecology · doi:10.1890/06-2057.1 · Cited by 2,751 · see citing works
Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory
Bryant, J. P., Chapin, F. S., & Klein, D. R. (1983) · Oikos · doi:10.2307/3544308 · Cited by 2,502 · see citing works
Flavonoids as antioxidants in plants: Location and functional significance
Agati, G., Azzarello, E., Pollastri, S., & Tattini, M. (2012) · Plant Science · doi:10.1016/j.plantsci.2012.07.014 · Cited by 2,146 · see citing works
A leaf-height-seed (LHS) plant ecology strategy scheme
Westoby, M. (1998) · Plant and Soil · doi:10.1023/a:1004327224729 · Cited by 1,925 · cited 1× · see citing works
“High SLA indicates high light capture by leaf tissue mass, whereas low SLA reflects mass allocation that increases longevity, robustness, and defense (Westoby, 1998).”
BackgroundSecondary metabolites in plant defence mechanisms
BENNETT, R. N., & WALLSGROVE, R. M. (1994) · New Phytologist · doi:10.1111/j.1469-8137.1994.tb02968.x · Cited by 1,654 · see citing works
Significance of flavonoids in plant resistance: a review
Treutter, D. (2006) · Environmental Chemistry Letters · doi:10.1007/s10311-006-0068-8 · Cited by 1,260 · see citing works
How much does climate change threaten European forest tree species distributions?
Dyderski, M. K., Paź‐Dyderska, S., Frelich, L. E., & Jagodziński, A. M. (2017) · Global Change Biology · doi:10.1111/gcb.13925 · Cited by 935 · see citing works
Adaptive Patterns in Alkaloid Physiology
McKey, D. (1974) · The American Naturalist · doi:10.1086/282909 · Cited by 750 · see citing works
Coomes, D. A., & Grubb, P. J. (2000) · Ecological Monographs · doi:10.1890/0012-9615(2000)070[0171:iorcif]2.0.co;2 · Cited by 706 · see citing works
Comita, L. S., Queenborough, S. A., Murphy, S. J., Eck, J. L., Xu, K., Krishnadas, M., Beckman, N. G., & Zhu, Y. (2014) · Journal of Ecology · doi:10.1111/1365-2745.12232 · Cited by 663 · see citing works
Jasmonate action in plant growth and development
Huang, H., Liu, B., Liu, L., & Song, S. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erw495 · Cited by 653 · see citing works
The global distribution of diet breadth in insect herbivores
Forister, M. L., Novotný, V., Panorska, A. K., Baje, L., Basset, Y., Butterill, P. T., Čížek, L., Coley, P. D., Dem, F., Diniz, I. R., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423042112 · Cited by 644 · see citing works
Poorter, H., Niinemets, Ü., Ntagkas, N., Siebenkäs, A., Mäenpää, M., Matsubara, S., & Pons, T. L. (2019) · New Phytologist · doi:10.1111/nph.15754 · Cited by 606 · see citing works
Koricheva, J., Larsson, S., Haukioja, E., Keinänen, M., & Keinänen, M. (1998) · Oikos · doi:10.2307/3546833 · Cited by 568 · see citing works
Rethinking the role of many plant phenolics – protection from photodamage not herbivores?
Close, D. C., & McArthur, C. (2002) · Oikos · doi:10.1034/j.1600-0706.2002.990117.x · Cited by 506 · see citing works
The carbon–nutrient balance hypothesis: its rise and fall
Hamilton, J. G., Zangerl, A. R., DeLucia, E. H., & Berenbaum, M. R. (2001) · Ecology Letters · doi:10.1046/j.1461-0248.2001.00192.x · Cited by 480 · see citing works
Yuan, Z. Y., & Chen, H. Y. H. (2010) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2010.483579 · Cited by 448 · see citing works
Root exudate metabolomes change under drought and show limited capacity for recovery
Gargallo‐Garriga, A., Preece, C., Sardans, J., Oravec, M., Urban, O., & Peñuelas, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-30150-0 · Cited by 407 · see citing works
Assessing the evidence for latitudinal gradients in plant defence and herbivory
Moles, A. T., Bonser, S. P., Poore, A. G. B., Wallis, I. R., & Foley, W. J. (2010) · Functional Ecology · doi:10.1111/j.1365-2435.2010.01814.x · Cited by 388 · see citing works
Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in northern Europe
Hynynen, J., Niemistö, P., Viherä‐Aarnio, A., Brunner, A., Hein, S., & Velling, P. (2009) · Forestry An International Journal of Forest Research · doi:10.1093/forestry/cpp035 · Cited by 387 · see citing works
Surplus Carbon Drives Allocation and Plant–Soil Interactions
Prescott, C. E., Grayston, S. J., Helmisaari, H., Kaštovská, E., Körner, C., Lambers, H., Meier, I. C., Millard, P., & Ostonen, I. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.08.007 · Cited by 366 · see citing works
Bergh, J., Linder, S., Lundmark, T., & Elfving, B. (1999) · Forest Ecology and Management · doi:10.1016/s0378-1127(98)00509-x · Cited by 338 · see citing works
Induced resistance to pests and pathogens in trees
Eyles, A., Bonello, P., Ganley, R. J., & Mohammed, C. L. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.03127.x · Cited by 319 · see citing works
Finér, L., Ohashi, M., Noguchi, K., & Hirano, Y. (2011) · Forest Ecology and Management · doi:10.1016/j.foreco.2011.08.042 · Cited by 317 · see citing works
Forrester, D. I. (2019) · Forest Ecology and Management · doi:10.1016/j.foreco.2019.05.053 · Cited by 316 · see citing works
Are Flavonoids Effective Antioxidants in Plants? Twenty Years of Our Investigation
Agati, G., Brunetti, C., Fini, A., Gori, A., Guidi, L., Landi, M., Sebastiani, F., & Tattini, M. (2020) · Antioxidants · doi:10.3390/antiox9111098 · Cited by 290 · see citing works
De novo biosynthesis of defense root exudates in response to Fusarium attack in barley
Lanoue, A., Burlat, V., Henkes, G. J., Koch, I., Schurr, U., & Röse, U. S. R. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.03066.x · Cited by 260 · see citing works
Jucker, T., Bouriaud, O., Avăcăriței, D., Constantin, I., Duduman, G., Valladares, F., & Coomes, D. A. (2014) · Journal of Ecology · doi:10.1111/1365-2745.12276 · Cited by 247 · see citing works
Molecular mechanisms of plant competition: neighbour detection and response strategies
Pierik, R., Mommer, L., & Voesenek, L. A. C. J. (2012) · Functional Ecology · doi:10.1111/1365-2435.12010 · Cited by 216 · see citing works
Witzell, J., & Martín, J. A. M. (2008) · Canadian Journal of Forest Research · doi:10.1139/x08-112 · Cited by 210 · see citing works
Weih, M., & Karlsson, P. S. (2001) · New Phytologist · doi:10.1046/j.1469-8137.2001.00078.x · Cited by 199 · see citing works
Grass roots chemistry: meta -Tyrosine, an herbicidal nonprotein amino acid
Bertin, C., Weston, L. A., Huang, T., Jander, G., Owens, T. G., Meinwald, J., & Schroeder, F. C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707198104 · Cited by 197 · see citing works
Meier, I. C., Tückmantel, T., Heitkötter, J., Müller, K., Preußer, S., Wrobel, T. J., Kandeler, E., Marschner, B., & Leuschner, C. (2019) · New Phytologist · doi:10.1111/nph.16389 · Cited by 170 · see citing works
Keinänen, M., Julkunen‐Tiitto, R., Mutikäinen, P., Walls, M., Ovaska, J., & Vapaavuori, E. (1999) · Ecology · doi:10.1890/0012-9658(1999)080[1970:toipmo]2.0.co;2 · Cited by 163 · see citing works
Contrasting patterns of biomass allocation in dominant and suppressed loblolly pine
Naidu, S. L., DeLucia, E. H., & Thomas, R. B. (1998) · Canadian Journal of Forest Research · doi:10.1139/x98-083 · Cited by 160 · see citing works
Dubois, H., Verkasalo, E., & Claessens, H. (2020) · Forests · doi:10.3390/f11030336 · Cited by 154 · see citing works
Donaldson, J. R., Kruger, E. L., & Lindroth, R. L. (2005) · New Phytologist · doi:10.1111/j.1469-8137.2005.01613.x · Cited by 146 · see citing works
A light-dependent molecular link between competition cues and defence responses in plants
Fernández-Milmanda, G. L., Crocco, C. D., Reichelt, M., Mazza, C. A. D. S., Köllner, T. G., Zhang, T., Cargnel, M. D., Lichy, M. Z., Fiorucci, A.-S., Fankhauser, C., et al. (2020) · Nature Plants · doi:10.1038/s41477-020-0604-8 · Cited by 142 · see citing works
Reich, P. B., Oleksyn, J., & Tjoelker, M. G. (1996) · Functional Ecology · doi:10.2307/2390512 · Cited by 141 · see citing works
Künstler, G., Albert, C. H., Courbaud, B., Lavergne, S., Thuiller, W., Vieilledent, G., Zimmermann, N. E., & Coomes, D. A. (2010) · Journal of Ecology · doi:10.1111/j.1365-2745.2010.01751.x · Cited by 139 · see citing works
Соколова, Т. А. (2020) · Eurasian Soil Science · doi:10.1134/s1064229320050154 · Cited by 136 · see citing works
Changes in Leaf Trichomes and Epicuticular Flavonoids during Leaf Development in Three Birch Taxa
Valkama, E. (2004) · Annals of Botany · doi:10.1093/aob/mch131 · Cited by 135 · see citing works
Proximity signal and shade avoidance differences between early and late successional trees
Gilbert, I., Jarvis, P. G., & Smith, H. (2001) · Nature · doi:10.1038/35081062 · Cited by 134 · see citing works
Zwetsloot, M. J., Muñoz-Ucros, J., Wickings, K. G., Wilhelm, R. C., Sparks, J. P., Buckley, D. H., & Bauerle, T. L. (2020) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2020.107797 · Cited by 129 · see citing works
Latitudinal variation in plant chemical defences drives latitudinal patterns of leaf herbivory
Moreira, X., Castagneyrol, B., Abdala‐Roberts, L., y Terán, J. C. B. M., Timmermans, B. G. H., Bruun, H. H., Covelo, F., Glauser, G., Rasmann, S., & Tack, A. J. M. (2017) · Ecography · doi:10.1111/ecog.03326 · Cited by 125 · see citing works
Root:shoot ratios across China’s forests: Forest type and climatic effects
Luo, Y., Wang, X., Zhang, X., Booth, T. H., & Lü, F. (2012) · Forest Ecology and Management · doi:10.1016/j.foreco.2012.01.005 · Cited by 113 · see citing works
Genomics of Secondary Metabolism inPopulus: Interactions with Biotic and Abiotic Environments
Chen, F., Liu, C., Tschaplinski, T. J., & Zhao, N. (2009) · Critical Reviews in Plant Sciences · doi:10.1080/07352680903241279 · Cited by 113 · see citing works
Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling
Barchet, G. L. H., Dauwe, R., Guy, R. D., Schroeder, W. R., Soolanayakanahally, R. Y., Campbell, M. M., & Mansfield, S. D. (2013) · Tree Physiology · doi:10.1093/treephys/tpt080 · Cited by 103 · see citing works
Can the growth–differentiation balance hypothesis be tested rigorously?
Stamp, N. E. (2004) · Oikos · doi:10.1111/j.0030-1299.2004.12039.x · Cited by 99 · see citing works
Henriksson, J., Haukioja, E., Ossipov, V. I., Ossipova, S., Sillanpää, S., Kapari, L., & Pihlaja, K. (2003) · Oikos · doi:10.1034/j.1600-0706.2003.12306.x · Cited by 92 · see citing works
Hartikainen, K., Riikonen, J., Nerg, A., Kivimäenpää, M., Ahonen, V. H., Tervahauta, A. I., Kärenlampi, S. O., Mäenpää, M., Rousi, M., Kontunen‐Soppela, S., et al. (2012) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2012.04.014 · Cited by 85 · see citing works
Self-citationStone and gravel contents of arable soils influence estimates of C and N stocks
Rytter, R.-M. (2012) · CATENA · doi:10.1016/j.catena.2012.02.015 · Cited by 84 · see citing works
Assessing the latitudinal gradient in herbivory
Lim, J. Y., Fine, P. V. A., & Mittelbach, G. G. (2015) · Global Ecology and Biogeography · doi:10.1111/geb.12336 · Cited by 81 · see citing works
Competitive status influences tree‐growth responses to elevated CO2 and O3 in aggrading aspen stands
McDonald, E. P., Kruger, E. L., Riemenschneider, D. E., & Isebrands, J. G. (2002) · Functional Ecology · doi:10.1046/j.1365-2435.2002.00683.x · Cited by 81 · see citing works
The latitudinal herbivory‐defence hypothesis takes a detour on the map
Johnson, M. T. J., & Rasmann, S. (2011) · New Phytologist · doi:10.1111/j.1469-8137.2011.03816.x · Cited by 78 · see citing works
High herbivore pressure favors constitutive over induced defense
Bixenmann, R. J., Coley, P. D., Weinhold, A., & Kursar, T. A. (2016) · Ecology and Evolution · doi:10.1002/ece3.2208 · Cited by 78 · see citing works
Nitrogen limitation and microbial diversity at the treeline
Thébault, A., Clément, J., Ibanez, S., Roy, J., Geremia, R. A., Pérez, C. A., Buttler, A., Estienne, Y., & Lavorel, S. (2014) · Oikos · doi:10.1111/j.1600-0706.2013.00860.x · Cited by 77 · see citing works
Environmental drivers interactively affect individual tree growth across temperate European forests
Maes, S. L., Perring, M. P., Vanhellemont, M., Depauw, L., den Bulcke, J. V., Brūmelis, G., Brunet, J., Decocq, G., den Ouden, J., Härdtle, W., et al. (2018) · Global Change Biology · doi:10.1111/gcb.14493 · Cited by 77 · see citing works
Needle nutrients in geographically diverse Pinus sylvestris L. populations
Oleksyn, J., Reich, P. B., Żytkowiak, R., Karolewski, P., & Tjoelker, M. G. (2002) · Annals of Forest Science · doi:10.1051/forest:2001001 · Cited by 69 · see citing works
Chemical defense in birch. Platyphylloside: A phenol fromBetula pendula inhibiting digestibility
Sunnerheim, K., Palo, R. T., Theander, O., & Knutsson, P.-G. (1988) · Journal of Chemical Ecology · doi:10.1007/bf01013906 · Cited by 63 · see citing works
Anti‐herbivore defences and insect herbivory: Interactive effects of drought and tree neighbours
Castagneyrol, B., Jactel, H., & Moreira, X. (2018) · Journal of Ecology · doi:10.1111/1365-2745.12956 · Cited by 62 · see citing works
Adams, J. M., Rehill, B. J., Zhang, Y., & Gower, J. (2008) · Ecological Research · doi:10.1007/s11284-008-0541-x · Cited by 60 · see citing works
Berendse, F., & Möller, F. (2008) · Plant Ecology · doi:10.1007/s11258-008-9485-z · Cited by 57 · see citing works
Mäenpää, M., Riikonen, J., Kontunen‐Soppela, S., Rousi, M., & Oksanen, E. J. (2011) · Tree Physiology · doi:10.1093/treephys/tpr075 · Cited by 51 · see citing works
Self-citationSmith, E. A., Collette, S. B., Boynton, T. A., Lillrose, T., Stevens, M. R., Bekker, M. F., Eggett, D. L., & Clair, S. B. S. (2011) · Tree Physiology · doi:10.1093/treephys/tpq100 · Cited by 49 · see citing works
Massad, T. J., Trumbore, S. E., Ganbat, G., Reichelt, M., Unsicker, S. B., Boeckler, G. A., Gleixner, G., Gershenzon, J., & Ruehlow, S. (2014) · New Phytologist · doi:10.1111/nph.12811 · Cited by 41 · see citing works
Högberg, P., Wellbrock, N., Högberg, M. N., Mikaelsson, H., & Stendahl, J. (2021) · Forest Ecology and Management · doi:10.1016/j.foreco.2020.118899 · Cited by 40 · see citing works
Does competition stress decrease allelopathic potential?
Rivoal, A., Fernandez, C., Greff, S., Montès, N., & Vila, B. (2011) · Biochemical Systematics and Ecology · doi:10.1016/j.bse.2011.05.017 · Cited by 39 · see citing works
Lihavainen, J., Keinänen, M., Keski‐Saari, S., Kontunen‐Soppela, S., Sõber, A., & Oksanen, E. J. (2016) · Journal of Experimental Botany · doi:10.1093/jxb/erw219 · Cited by 38 · see citing works
Self-citationKnowledge for Use: Science, Higher Learning, and America's New Industrial Heartland, 1880-1915
Kargon, R. H., & Knowles, S. G. (2002) · Annals of Science · doi:10.1080/00033790010028188 · Cited by 37 · see citing works
Long‐term exposure to elevated CO2 and O3 alters aspen foliar chemistry across developmental stages
Couture, J. J., Holeski, L. M., & Lindroth, R. L. (2013) · Plant Cell & Environment · doi:10.1111/pce.12195 · Cited by 34 · see citing works
Poeydebat, C., Jactel, H., Moreira, X., Koricheva, J., Barsoum, N., Bauhus, J., Eisenhauer, N., Ferlian, O., Francisco, M., Gottschall, F., et al. (2020) · Functional Ecology · doi:10.1111/1365-2435.13700 · Cited by 34 · see citing works
Leaf Canopy Layers Affect Spectral Reflectance in Silver Birch
Deepak, M., Keski‐Saari, S., Fauch, L., Granlund, L., Oksanen, E. J., & Keinänen, M. (2019) · Remote Sensing · doi:10.3390/rs11242884 · Cited by 33 · see citing works
Self-citationSaviranta, N., Julkunen‐Tiitto, R., Oksanen, E. J., & Karjalainen, R. (2009) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.3831 · Cited by 28 · see citing works
Self-citationGenotype- and provenance-related variation in the leaf surface secondary metabolites of silver birch
Deepak, M., Lihavainen, J., Keski‐Saari, S., Kontunen‐Soppela, S., Salojärvi, J., Tenkanen, A., Heimonen, K., Oksanen, E. J., & Keinänen, M. (2018) · Canadian Journal of Forest Research · doi:10.1139/cjfr-2017-0456 · Cited by 27 · see citing works
Self-citationLaurent, L., Mårell, A., Korboulewsky, N., Saı̈d, S., & Balandier, P. (2017) · Forest Ecology and Management · doi:10.1016/j.foreco.2017.02.003 · Cited by 26 · see citing works
Heimonen, K., Valtonen, A., Kontunen‐Soppela, S., Keski‐Saari, S., Rousi, M., Oksanen, E. J., & Roininen, H. (2015) · Climatic Change · doi:10.1007/s10584-015-1392-4 · Cited by 25 · see citing works
Self-citationMaja, M. M., Kasurinen, A., Holopainen, T., Kontunen‐Soppela, S., Oksanen, E. J., & Holopainen, J. K. (2015) · Tree Physiology · doi:10.1093/treephys/tpv052 · Cited by 25 · see citing works
Self-citationLatitudinal Gradients in Induced and Constitutive Resistance against Herbivores
Anstett, D. N., Chen, W., & Johnson, M. T. J. (2016) · Journal of Chemical Ecology · doi:10.1007/s10886-016-0735-6 · Cited by 25 · see citing works
Influence of root herbivory on plant communities in heterogeneous nutrient environments
Stevens, G., & Jones, R. H. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01731.x · Cited by 20 · see citing works
Early growth of different tree species on agricultural land along a latitudinal transect in Sweden
Rytter, L., & Lutter, R. (2019) · Forestry An International Journal of Forest Research · doi:10.1093/forestry/cpz064 · Cited by 20 · see citing works
Self-citationZvereva, E. L., Zverev, V., & Kozlov, M. V. (2020) · Journal of Animal Ecology · doi:10.1111/1365-2656.13350 · Cited by 20 · see citing works
Tenkanen, A., Suprun, S., Oksanen, E. J., Keinänen, M., Keski‐Saari, S., & Kontunen‐Soppela, S. (2020) · Tree Physiology · doi:10.1093/treephys/tpaa148 · Cited by 20 · see citing works
Self-citationHeimonen, K., Valtonen, A., Kontunen‐Soppela, S., Keski‐Saari, S., Rousi, M., Oksanen, E. J., & Roininen, H. (2016) · Scandinavian Journal of Forest Research · doi:10.1080/02827581.2016.1195867 · Cited by 17 · see citing works
Self-citationPossen, B., Rousi, M., Keski‐Saari, S., Silfver, T., Kontunen‐Soppela, S., Oksanen, E. J., & Mikola, J. (2021) · Ecosphere · doi:10.1002/ecs2.3520 · Cited by 17 · see citing works
Self-citationTullus, A., Kupper, P., Kaasik, A., Tullus, H., Lõhmus, K., Sõber, A., & Sellin, A. (2016) · Global Change Biology · doi:10.1111/gcb.13540 · Cited by 14 · see citing works
Self-citationRosinger, C., Sandén, H., & Godbold, D. L. (2020) · Mycorrhiza · doi:10.1007/s00572-020-00939-x · Cited by 14 · see citing works
Rusalepp, L., Lutter, R., Hepner, H., Kaasik, A., & Tullus, A. (2021) · Annals of Forest Science · doi:10.1007/s13595-020-01014-3 · Cited by 12 · see citing works
Self-citationKolstad, A. L., Asplund, J., Nilsson, M., Ohlson, M., & Nybakken, L. (2016) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2016.06.013 · Cited by 7 · see citing works
Linear Programming from Fibonacci to Farkas
Biggs, N. (2020) · Annals of Science · doi:10.1080/00033790.2020.1811377 · Cited by 3 · see citing works
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Khan, N. (2025) · Plant Cell & Environment · doi:10.1111/pce.15473 · Cited by 73 · see citing works
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Chen, M., Yao, X., Cheng, H., Fan, A., Lin, R., Wang, X., Yang, Y., & Chen, G. (2023) · Forest Ecology and Management · doi:10.1016/j.foreco.2023.121239 · Cited by 49 · see citing works
Čėsnienė, I., Miškelytė, D., Novickij, V., Mildažienė, V., & Sirgedaitė‐Šėžienė, V. (2023) · Plants · doi:10.3390/plants12173048 · Cited by 17 · see citing works
Hernandez-Fuentes, G. A., Delgado-Enciso, O. G., Larios-Cedeño, E. G., Sánchez-Galindo, J. M., Ceballos-Magaña, S. G., Pineda-Urbina, K., Alcalá-Pérez, M. A., Magaña-Vergara, N. E., Delgado-Enciso, J., Díaz-Llerenas, U., et al. (2024) · Life · doi:10.3390/life14121702 · Cited by 15 · see citing works
Tenkanen, A., Keinänen, M., Oksanen, E. J., Keski‐Saari, S., & Kontunen‐Soppela, S. (2022) · Tree Physiology · doi:10.1093/treephys/tpac104 · Cited by 12 · see citing works
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Self-citationLv, J., Du, Q., Shi, S., Ma, M., Zhang, W., Ge, D., Xing, L., & Yu, N. (2024) · Molecules · doi:10.3390/molecules29050992 · Cited by 6 · see citing works
Gamal Eldin, A., Morsy, A. A., Shehata, M. M., Ibrahim, M., & Saleh, H. A. (2025) · BMC Plant Biology · doi:10.1186/s12870-025-07521-7 · Cited by 2 · see citing works
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Binhan, Z., Pu, R., Yuqin, M., Lin, R., Hanyu, D., Wenhao, Z., Wenqi, X., Mao, L., Chengzhi, W., Yanli, L., et al. (2026) · Frontiers in Plant Science · doi:10.3389/fpls.2026.1777794 · Cited by 2 · see citing works
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Self-citationOksanen, E. J., Silfver, T., Ghelardini, L., Pecori, F., Nieminen, K. M., Helena, R., Rousi, M., Santini, A., & Mikola, J. (2025) · Journal of Forestry Research · doi:10.1007/s11676-025-01839-6 · Cited by 2 · see citing works
Self-citationZhang, M., Zhou, C., Huang, S., Wang, H., Shi, T., Li, M., Jing, Z., & Zhang, X. (2025) · Scientific Reports · doi:10.1038/s41598-025-32876-0 · Cited by 1 · see citing works
Rosenvald, K., Lehmann, M. M., Ostonen, I., Rohula‐Okunev, G., Kupper, P., & Tullus, A. (2026) · European Journal of Forest Research · doi:10.1007/s10342-025-01862-6 · Cited by 1 · see citing works
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Wagou, B. A.-H. O., Zhao, J., Cao, G., Shen, Y., Wu, Z., Wang, D., & He, Q. (2022) · Desalination and Water Treatment · doi:10.5004/dwt.2022.28835
Oksanen, E. J., Silfver, T., Ghelardini, L., Pecori, F., Nieminen, K. M., Helena, R., Rousi, M., Alberto, S., & Juha, M. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4863066
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Felix, J. A., Stevenson, P. C., & Koricheva, J. (2025) · Ecology and Evolution · doi:10.1002/ece3.71768
Liao, Z., Liu, L., Yang, Y., Lu, N., Wu, G., Li, P., Junhua, 陈. C., Gu, J., Kreuzwieser, J., Werner, C., et al. (2026) · Forest Ecology and Management · doi:10.1016/j.foreco.2026.123731
Liu, F., Xiong, X., Wang, Y., Dai, L., Li, Z., Geng, X., Wang, J., Ren, Y., Cai, Q., & Liu, Z. (2026) · Metabolites · doi:10.3390/metabo16090615
Morais, M. C., Ferreira, H. F., Sousa, J., Cabral, J. A., & Gonçalves, B. C. (2026) · Plants · doi:10.3390/plants15203217
- Authors
- Tullus, A., Rusalepp, L., Lutter, R., Rosenvald, K., Kaasik, A., Rytter, L., Kontunen-Soppela, S., & Oksanen, E.
- Affiliations
- University of Tartu (EE)
- Estonian University of Life Sciences (EE)
- University of Eastern Finland (FI)
- Corresponding author
- Tullus, Arvo
- Venue
- Frontiers in Plant Science
- Publisher
- Frontiers Media SA
- Published
- 2021-11-25
- Volume
- 12
- Pages
- 746165-746165
- ISSN
- 1664-462X (ISSN-L)
- PMC
- PMC8655902
- OpenAlex
- W3217233975
- Cited by
- 20
- References
- 91
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 4 · 2023: 3 · 2022: 2
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Plant Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UEF eRepo (University of Eastern Finland) (submittedVersion, cc-by)
- Funders
- Estonian Research Council (PSG7, PSG600)
- Topics
- Physical Sciences › Environmental Science › Ecology › Forest Insect Ecology and Management
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Forest ecology and management
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
- Keywords
- Betula pendula, secondary metabolites, climate change, competition (biology), fine roots, leaves, growth regulators, latitudinal gradient, mean annual temperature, resource allocation, carbon allocation
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