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Elements and ectomycorrhizal symbiosis affecting the growth of Japanese larch seedlings regenerated on slopes of an active volcano in northern Japan

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The growth of Japanese larch seedlings is regulated by the presence of nutrients as well as ectomycorrhizal symbiosis.

Abstract

The mountain slope of an active volcano is a severe environment for the regeneration of larch (Larix kaempferi Sarg. hereafter larch) seedlings. To determine parameters affecting the growth of larch seedlings, we analyzed stoichiometry of elements in the soils and plant organs, ectomycorrhizal (ECM) colonization, and photosynthetic abilities. These parameters were compared with two different elevations. From nutrient analysis of plant organs from larch seedlings grown on the slope of a volcano, potassium (K) was insufficient compared with the seedlings grown in other habitats. Symbiosis with ECM fungi enabled the uptake of nutrients, especially phosphorous (P) and nitrogen (N). The main factor affecting the differences in relative height growth rate (RHGr) of larch was attributed to ECM colonization. There was a positive relationship between ECM colonization and concentrations of P or N in needles. Larch seedlings with high rates of ECM colonization showed high concentrations of P and N, and had high photosynthetic rates. At lower elevation sites, concentrations of N and K in needles were low with high density of individuals. Moreover, larch showed a high accumulation of aluminum (Al) and iron (Fe) even though the amount of these elements in the soil was small. These seedlings exhibited a suppressed photosynthetic rate and RHGr. Symbiosis with ECM fungi could suppress the excessive uptake of Al and Fe.

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References

  • Adamski JM, Peters JA, Danieloski R, Bacarin MA (2011) Excess iron-induced changes in the photosynthetic characteristics of sweet potato. J Plant Physiol 168:2056–2062

    Article  CAS  PubMed  Google Scholar 

  • Adikari Y, Kikuchi S, Makinow T, Araya T (2007) Naturally revegetated forest governed by mudflow induced sediment heterogeneity. New For 33:53–65

    Article  Google Scholar 

  • Akasaka M, Tsuyuzaki S (2005) Tree seedling performance in microhabitats along an elevational gradient on Mount Koma, Japan. J Veg Sci 16:647–654

    Article  Google Scholar 

  • Akasaka M, Tsuyuzaki S (2009) Comparisons of recruitment, survival, and growth in invasive and native saplings on a volcano. Plant Ecol 202:235–245

    Article  Google Scholar 

  • Akasaka M, Tsuyuzaki S, Hase A (2007) Annual growth of invasive Larix kaempferi seedlings with reference to microhabitat and ectomycorrhizal colonization on a volcano. J Plant Res 120:329–336

    Article  PubMed  Google Scholar 

  • Bae KS, Barton LL (1989) Alkaline phosphatase and other hydrolyases produced by Cenococcum graniforme, an ectomycorrhizal fungus. Appl Environ Microbiol 55:2511–2516

    PubMed Central  CAS  PubMed  Google Scholar 

  • Baillon F, Dalschaert X, Grassi S, Geiss F (1988) Spruce photosynthesis: possibility of early damage diagnosis due to exposure to magnesium or potassium deficiency. Trees 2:173–179

    Article  Google Scholar 

  • Barron-Gafford GA, Will RE, Burkes EC, Shiver B, Teskey RO (2003) Nutrients concentrations and contents, and their relation to stem growth, of intensively managed Pinus taeda and Pinus elliottii stands of different planting densities. Forest Sci 49:291–300

    Google Scholar 

  • Bautista AT, Inoue K (1993) Significance of loess addition in relation to andic soil properties of volcanic ash soils. Soil Sci Plant Nutr 39:517–527

    Article  CAS  Google Scholar 

  • Bourioug M, Alaoui-Sossé L, Laffray X, Raouf N, Benbrahim M, Badot PM, Alaoui-Sossé B (2014) Evaluation of sewage sludge effects on soil properties, plant growth, mineral nutrition state, and heavy metal distribution in European larch seedlings (Larix decidua). Arab J Sci Eng 39:5325–5335

    Article  CAS  Google Scholar 

  • Bown HE, Watt MS, Clinton PW, Mason EG, Richardson B (2007) Partitioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. Tree Physiol 27:335–344

    Article  CAS  PubMed  Google Scholar 

  • Braatne JH, Bliss LC (1999) Comparative physiological ecology of lupines colonizing early successional habitats on mount St. Helens. Ecology 80:891–907

    Article  Google Scholar 

  • Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhiza. FEMS Microbiol Rev 22:21–44

    Article  CAS  PubMed  Google Scholar 

  • Chen LS, Qi YP, Smith BR, Liu XH (2005) Aluminum-induced decrease in CO2 assimilation in citrus seedlings is unaccompanied by decreased activities of key enzyme involved in CO2 assimilation. Tree Physiol 25:317–324

    Article  CAS  PubMed  Google Scholar 

  • Donan Agricultural Experiment Station (2013) Annual report of Donan Agricultural Experiment Station in 2012. Hokkaido Research Organization, Agriculture Research Department, Sapporo (in Japanese)

  • Douhan GW, Rizzo DM (2005) Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytol 166:263–271

    Article  CAS  PubMed  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Finlay RD (1989) Functional aspects of phosphorus uptake and carbon translocation in incompatible ectomycorrhizal association between Pinus sylvestris and Suillus grevillei and Boletinus cavipes. New Phytol 112:185–192

    Article  CAS  Google Scholar 

  • Genetet I, Martin F, Stewart GR (1984) Nitrogen assimilation in mycorrhizas. Plant Physiol 76:395–399

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Geological survey of Japan (2013) Hokkaido-Komagatake volcano. https://gbank.gsj.jp/volcano/Act_Vol/hokkaidokomagatake/text/eng/exp05-1e.html

  • Hakodate district forest office (1967) The history of Hakodate district forest office. Japan Forestry Foundation, Tokyo (in Japanese)

    Google Scholar 

  • Haruki M, Tsuyuzaki S (2001) Woody plant establishment during the early stages of volcanic succession on Mount Usu, northern Japan. Ecol Res 16:451–457

    Article  Google Scholar 

  • Hodge A, Alexander IJ, Gooday GW (1995) Chitinolytic enzymes of pathogenic and ectomycorrhizal fungi. Mycol Res 99:935–941

    Article  CAS  Google Scholar 

  • Horikawa Y (1972) Atlas of the Japanese flora, an introduction to plant sociology of East Asia. Gakken, Tokyo

    Google Scholar 

  • Igarashi T, Yajima T, Matsuda K, Natsume S, Takikawa S (1987) Natural regeneration in the Japanese larch plantation. Res Bull Hokkaido Univ For 44:1019–1040 (in Japanese and English summary)

    Google Scholar 

  • Imaya A, Inagaki Y, Tanaka N, Ohta S (2007) Free oxides and short-range ordered mineral properties of brown forest soils developed from different parent materials in the submontane zone of the Kanto and Chubu districts, Japan. Soil Sci Plant Nutr 53:621–653

    Article  CAS  Google Scholar 

  • Ishikawa T, Saijoh Y, Bratawinata AA (1978) Some site factors in a natural forest of Larix leptolepis Gordon (Japanese larch) on mount Ontake, central Japan. Res Bull Fac Agric Gifu Univ 41:251–260

    Google Scholar 

  • Ishimaru K, Tokuchi N, Osawa N, Kawamura K, Takeda H (2005) Behavior of four broad-leaved tree species used to revegetate eroded granite hill slopes. J Forest Res 10:27–34

    Article  Google Scholar 

  • Japan Meteorological Agency (2006) Monthly report of climate, Oshima branch, Hokkaido. http://www.data.jma.go.jp/obd/stats/etrn/index.php

  • Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116

    Article  CAS  Google Scholar 

  • Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871

    Article  CAS  PubMed  Google Scholar 

  • Kayama M, Yamanaka T (2014) Growth characteristics of ectomycorrhizal seedlings of Quercus glauca, Quercus salicina, and Castanopsis cuspidata planted on acidic soil. Trees 28:569–583

    Article  CAS  Google Scholar 

  • Kayama M, Kitaoka S, Wang W, Choi DS, Koike T (2007) Needle longevity, photosynthetic rate and nitrogen concentration of eight spruce taxa planted in northern Japan. Tree Physiol 27:1585–1593

    Article  CAS  PubMed  Google Scholar 

  • Kayama M, Makoto K, Nomura M, Satoh F, Koike T (2009) Dynamics of elements in larch seedlings (Larix Kaempferi) regenerated on serpentine soil in northern Japan. Landsc Ecol Eng 5:125–135

    Article  Google Scholar 

  • Kayama M, Satoh F, Koike T (2011) Photosynthetic rate, needle longevity, and nutrient contents in Picea glehnii growing on strongly acidic volcanic ash soil in northern Japan. Photosynthetica 49:239–245

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerance acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Koike T, Yazaki K, Funada R, Maruyama Y, Mori S, Sasa K (2000) Forest health and vitality in northern Japan—a history of larch plantation. Res Note Fac Forest Univ Joensuu 92:49–60

    Google Scholar 

  • Kondo T, Tsuyuzaki S (1999) Natural regeneration patterns of the introduced larch, Larix Kaempferi (Pinaceae) on the volcanic Mount Koma, Northern Japan. Divers Distrib 5:223–233

    Article  Google Scholar 

  • Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Heidelberg

    Book  Google Scholar 

  • Leski T, Rudawska M (2012) Ectomycorrhizal fungal community of naturally regenerated European larch (Larix decidua) seedlings. Symbiosis 56:45–53

    Article  Google Scholar 

  • Leyton L (1957) The relationship between the growth and mineral composition of the foliage of Japanese larch. Plant Soil 9:31–48

    Article  CAS  Google Scholar 

  • Maeda T, Asanuma S, Tanimoto T (1978) Larix leptolepis natural forest and its succession on Mt. Asama. Jpn J Forest Environ 19:1–9 (in Japanese)

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Nakamura T (1961) Studies on nutritional diagnosis by leaf analysis of Japanese larch. J Fac Agric Shinshu Univ 2:377–419

    Google Scholar 

  • Nara K (2006) Pioneer dwarf willow may facilitate tree succession by providing late colonizers with compatible ectomycorrhizal fungi in a primary successional volcanic desert. New Phytol 171:187–198

    Article  PubMed  Google Scholar 

  • Nguyen NT, Hiep ND, Fujita K (2005) Iron enhances aluminum-induced leaf necrosis and plant growth inhibition in Eucalyptus camaldulensis. Plant Soil 277:139–152

    Article  CAS  Google Scholar 

  • Nogueira MA, Nehls U, Hampp R, Poralla K, Cardoso EJBN (2007) Mycorrhiza and soil bacteria influence extractable iron and manganese in soil and uptake by soybean. Plant Soil 298:273–284

    Article  CAS  Google Scholar 

  • Osaki M, Watanabe T, Tadano T (1997) Beneficial effect of aluminum on growth of plants adapted to low pH soils. Soil Sci Plant Nutr 43:551–563

    Article  CAS  Google Scholar 

  • Pereira EG, Oliva MA, Rosado-Souza L, Mendes GC, Colares DS, Stopato CH, Almeida AM (2013) Iron excess affects rice photosynthesis through stomatal and non-stomatal limitations. Plant Sci 201–202:81–92

    Article  PubMed  Google Scholar 

  • Pettigrew WT (2008) Potassium influences on yield and quality production for maize, wheat, soybean and cotton. Physiol Plant 133:670–681

    Article  CAS  PubMed  Google Scholar 

  • Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139

    Article  CAS  PubMed  Google Scholar 

  • Qu LY, Quoreshi AM, Iwase K, Tamai Y, Funada R, Koike T (2003) In vitro ectomycorrhiza formation on two larch species of seedlings with six different fungal species. Eurasian J Forest Res 6:65–73

    Google Scholar 

  • Qu LY, Kayama M, Akasaka M, Kitaoka S, Sasa K, Koike T (2004a) Micro-environmental analysis of the natural regeneration of larch forests in northern Japan. Eurasian J Forest Res 7:43–51

    Google Scholar 

  • Qu LY, Shinano T, Quoreshi AM, Tamai Y, Osaki M, Koike T (2004b) Allocation of 14C-carbon in two species of larch seedlings infected with ectomycorrhizal fungi. Tree Physiol 24:1369–1376

    Article  CAS  PubMed  Google Scholar 

  • Quoreshi AM, Timmer VR (1998) Exponential fertilization increases nutrient uptake and ectomycorrhizal development of black spruce seedlings. Can J Forest Res 28:674–682

    Article  Google Scholar 

  • Raaimakers D, Boot RGA, Dijkstra P, Pot S, Pons T (1995) Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia 102:120–125

    Article  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Sasaoka E, Yajima T, Shibuya M, Takahashi K, Nakamura F, Shimizu O (1999) Stand structure and regeneration process of a natural Larix kaempferi stand on Mt. Komagatake, Hokkaido. J Jpn Forest Soc 81:22–28 (in Japanese and English summary)

    Google Scholar 

  • Sasaoka E, Yoshida M, Yajima T, Shibuya M, Takahashi K (2000) Soil moisture and xylem water potential of tree saplings on Mt. Komagatake. Hokkaido. Res Bull Hokkaido Univ Forest 57:105–112 (in Japanese and English summary)

    CAS  Google Scholar 

  • Siqueira-Silva AI, Silva LC, Azevedo AA, Oliva MA (2012) Iron plaque formation and morphoanatomy of roots from species of restinga subjected to excess iron. Ecotoxicol Environ Saf 78:265–275

    Article  CAS  PubMed  Google Scholar 

  • Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnson CT, Sumner ME (1996) Methods of soil analysis, part 3. Soil Science Society of America Inc., Madison

    Google Scholar 

  • Sugimoto S (1966) Considering about larch forests. North Forestry Society, Sapporo (in Japanese)

    Google Scholar 

  • Takada J, Takamatsu T, Satake K, Sase H (1994) Data on elemental concentration in land plants by neutron activation analysis (No. I). National Institute for Environmental Studies, Tsukuba (in Japanese)

    Google Scholar 

  • Tam PCF (1995) Heavy metal tolerance by ectomycorrhizal fungi and metal amelioration by Pisolithus tinctorius. Mycorrhiza 5:181–187

    Article  CAS  Google Scholar 

  • Tanaka A, Yamamura Y, Nakano T (2008) Effects of forest-floor avalanche disturbance on the structure and dynamics of a subalpine forest near the forest limit on Mt. Fuji. Ecol Res 23:71–81

    Article  Google Scholar 

  • Thompson GW, Medve RJ (1984) Effects of aluminum and manganese on the growth of ectomycorrhizal fungi. Appl Environ Microbiol 48:556–560

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tsuda K (1963) Study on the quantitative variation of the growth and nutrient absorption in each seedling-age by todo fir, Japanese larch, and akaezo spruce seedlings. Bull FFPRI 214:1–76

    Google Scholar 

  • Usami H, Tamai Y, Yajima T, Miyamoto T (2007) Regeneration and ectomycorrhiza formation of Larix kaempferi at Mt. Komagatake, Hokkaido. Proc Jpn Forest Soc Cong 118:C31 (in Japanese)

  • van Reeuwijk LP (1993) Procedures for soil analysis. International soil reference and information centre, Wagningen

    Google Scholar 

  • van Schöll L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303:35–47

    Article  Google Scholar 

  • Yang G, Cha JY, Shibuya M, Yajima T, Takahashi K (1998) The occurrence and diversity of ectomycorrhizas of Larix kaempferi seedlings on a volcanic mountain in Japan. Mycol Res 102:1503–1508

    Article  Google Scholar 

  • Yang LT, Jiang HX, Tang N, Chen LS (2011) Mechanisms of aluminum-tolerance in two species of citrus: secretion of organic acid anion and immobilization of aluminum by phosphorus in roots. Plant Sci 180:521–530

    Article  CAS  PubMed  Google Scholar 

  • Yoshii Y (1932) Revegetation of Volcano Komagatake after great eruption in 1929. Bot Mag 46:208–215

    Article  Google Scholar 

  • Zhang HH, Tang M, Yang Y (2011) The response of ectomycorrhizal (ECM) fungi under water stress induced by polyethylene glycol (PEG) 6000. Afr J Microbiol Res 5:365–373

    CAS  Google Scholar 

  • Zhang L, Wang MX, Li H, Yuan JG, Penfold C (2014) Mobilization of inorganic phosphorus from soils by ectomycorrhizal fungi. Pedosphere 24:683–689

    Article  Google Scholar 

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Acknowledgments

We thank Prof. Y. Maruyama for his valuable comments on this study. We are grateful to the technical staff of Oshima Forest Management Office, Hokkaido Regional Forest Office, and Mori Town Office. Thanks are also due to Dr. Y. Kitahashi and Dr. N. Eguchi for measurements at Mt. Komagatake and Prof. H. Shibata for ICP analyses. Thanks are also due to Dr. Jamie Mosel of Oregon State University, USA for improving English.

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Correspondence to Masazumi Kayama.

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This study was not supported by funds from an organization. We declare that our research has no conflict of interest.

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Communicated by P. Courty.

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Kayama, M., Qu, L. & Koike, T. Elements and ectomycorrhizal symbiosis affecting the growth of Japanese larch seedlings regenerated on slopes of an active volcano in northern Japan. Trees 29, 1567–1579 (2015). https://doi.org/10.1007/s00468-015-1238-8

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