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Combined effects of irrigation amount and nitrogen load on growth and needle biochemical traits of Cryptomeria japonica seedlings

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Growth of C. japonica under highly irrigated and N-loaded soil is noticeable because of N-induced increase of needle mass and alleviation of high irrigation-induced reduction in photosynthesis.

Abstract

To clarify the combined effects of change in precipitation amount and increasing nitrogen load on Japanese forest trees, 2-year-old seedlings of Cryptomeria japonica were treated with combinations of four irrigation levels (80, 100, 120, or 140% of annual precipitation) and three nitrogen loads (15, 50, or 100 kg ha−1 year−1). The 100% of annual precipitation corresponded to 1520 mm year−1 which was the average annual precipitation in the habitats of C. japonica in Japan. High irrigation amount significantly enhanced the whole-plant dry mass of the seedlings. The N load significantly enhanced the extent of high irrigation-induced increase in needle dry mass. As a result, the irrigation-induced increase in the whole-plant dry mass was greater in the treatment with the highest N. However, increase in needle dry mass induced by high irrigation enhanced plant water consumption and caused dehydration and oxidative damage in needles, thus resulting in reduced net photosynthetic rate. The high irrigation-induced reduction in net photosynthetic rate was alleviated by N load. This alleviation was not caused by N load-induced changes in antioxidative capacity but by a N load-induced increase in ribulose 1,5-bisphosphate carboxylase/oxygenase activity. These results indicate that an increase in the whole-plant dry mass of C. japonica seedlings grown in highly irrigated and N-loaded soil was attributed to N load-induced enhancement of high irrigation-induced increase in needle dry mass and alleviation of high irrigation-induced reduction in net photosynthetic rate.

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References

  • Aikawa M, Ohara T, Hiraki T, Oishi O, Tsuji A, Yamagami M, Murano K, Mukai H (2010) Significant geographic gradients in particulate sulfate over Japan determined from multiple-site measurements and a chemical transport model: impacts of transboundary pollution from the Asian continent. Atmos Environ 44:381–391

    Article  CAS  Google Scholar 

  • Akimoto H (2003) Global air quality and pollution. Science 302:1716–1719

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM, Park YI, Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol Plant 100:214–223

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Phys 50:601–639

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll Fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681

    Article  CAS  Google Scholar 

  • Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384

    Article  CAS  PubMed  Google Scholar 

  • Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Qualls RG, Blank RR (2005) Effect of soil flooding on photosynthesis, carbohydrate partitioning and nutrient uptake in the invasive exotic Lepidium latifolium. Aquat Bot 82:250–268

    Article  CAS  Google Scholar 

  • Cornic G, Briantais JM (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183:178–184

    Article  CAS  PubMed  Google Scholar 

  • Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species. Production, scavenging and signaling. Plant Signal Behav 3:156–165

    Article  PubMed  PubMed Central  Google Scholar 

  • Damour G, Vandame M, Urban L (2009) Long-term drought results in a reversible decline in photosynthetic capacity in mango leaves, not just a decrease in stomatal conductance. Tree Physiol 29:675–684

    Article  CAS  PubMed  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • Egea G, Verhoef A, Vidale PL (2011) Towards an improved and more flexible representation of water stress in coupled photosynthesis–stomatal conductance models. Agric Forest Meteorol 151:1370–1384

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Nagi JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  PubMed  Google Scholar 

  • Endo T, Yagoh H, Sato K, Matsuda K, Hayashi K, Noguchi I, Sawada K (2011) Regional characteristics of dry deposition of sulfur and nitrogen compounds at EANET sites in Japan from 2003 to 2008. Atmos Environ 45:1259–1267

    Article  CAS  Google Scholar 

  • Flückiger W, Braun S (1998) Nitrogen deposition in Swiss forests and its possible relevance for leaf nutrient status, parasite attacks and soil acidification. Environ Pollut 102:69–76

    Article  Google Scholar 

  • Forest Agency of Japan (2012). http://www.rinya.maff.go.jp/j/keikaku/genkyou/h24/4.html. Accessed 15 July 2016

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  CAS  PubMed  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DJ, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JL, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  CAS  Google Scholar 

  • Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93

    Article  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849

    Article  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Yang Y, Wang G, Yang L, Sun X (2010) Ecophysiological responses of Abies fabri seedlings to drought stress and nitrogen supply. Physiol Plant 139:335–347

    CAS  PubMed  Google Scholar 

  • Heath RL, Packer L (1965) Effect of light on lipid peroxidation in chloroplasts. Biochem Bioph Res Commun 19:716–720

    Article  CAS  Google Scholar 

  • Holloway T, Levy IIH, Carmichael G (2002) Transfer of reactive nitrogen in Asia: development and evaluation of a source–receptor model. Atmos Environ 36:4251–4264

    Article  CAS  Google Scholar 

  • Inada H, Kondo T, Akhtar N, Hoshino D, Yamaguchi M, Izuta T (2012) Relationship between cultivar difference in the sensitivity of net photosynthesis to ozone and reactive oxygen species scavenging system in Japanese winter wheat (Triticum aestivum). Physiol Plant 146:217–227

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate Change 2013: the Physical Science Basis. Contribution of Working group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  • Izuta T, Nakaji T (2003) Effects of high nitrogen load and ozone on forest tree species. Eurasian J For Res 6:155–170

    Google Scholar 

  • Kimura SD, Saito M, Hara H, Xu YH, Okazaki M (2009) Comparison of nitrogen dry deposition on cedar and oak leaves in the tama hills using Foliar rinsing method. Water Air Soil Pollut 202:369–377

    Article  CAS  Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294

    Article  CAS  PubMed  Google Scholar 

  • Lawlor DW, Tezara W (2009) Cause of decrease photosynthetic rate and metabolic capacity in water-deficit leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luwe M, Heber U (1995) Ozone detoxification in the apoplasm and symplasm of spinach, broad bean and beech leaves at ambient and elevated concentrations of ozone in air. Planta 197:448–455

    Article  CAS  Google Scholar 

  • Matsumoto Y, Maruyama Y, Morikawa Y, Inoue T (1992a) Some negative results of simulative acid mist and ozone treatments to Cryptomeria japonica D. Don seedlings in explanation of mature C. japonica decline in the Kanto plains in Japan. Jpn J For Environ 34:85–97 (in Japanese with English summary)

    Google Scholar 

  • Matsumoto Y, Maruyama Y, Morikawa Y (1992b) Some aspects of water relations on large Cryptomeria japonica D. Don and climatic changes in the Kanto plains in Japan in relation to forest decline. Jpn J For Environ 34:2–13 (in Japanese with English summary)

    Google Scholar 

  • Matsumoto Y, Koike N, Kawarasaki S, Uemura A, Harayama H, Ito E, Yoshinaga S, Ohnuki Y, Shichi K, Okuda S, Ishida A, Taoda H (2002) The conditions of tree and forest of the Kanto plains in 1999–2001. Jpn J For Environ 44:53–62 (in Japanese with English summary)

    Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocupren). J Biol Chem 244:6049–6065

    CAS  PubMed  Google Scholar 

  • Medrano H, Parry MAJ, Socias X, Lawlor DW (1997) Long term water stress inactivates Rubisco in subterranean clover. Ann Appl Biol 131:491–501

    Article  CAS  Google Scholar 

  • Mielke MS, De Almeida AAF, Gomes FP, Aguilar MAG, Mangabeira PAO (2003) Leaf gas exchange, chlorophyll fluorescence and growth responses of Genipa americana seedlings to soil flooding. Environ Exp Bot 50:221–231

    Article  CAS  Google Scholar 

  • Ministry of Education, Culture, Sports, Science and Technology, Japan Meteorological Agency, Ministry of the Environment (2009) Climate Change and Its Impacts in Japan. Synthesis Report on Observations, Projections, and Impact Assessments of Climate Change, pp 36–39

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Miwa M, Izuta T, Totsuka T (1993) Effects of simulated acid rain and/or ozone on the growth of Japanese cedar seedlings. J Jpn Soc Air Pollut 28:279–287 (in Japanese with English summary)

    Google Scholar 

  • Morino Y, Ohara T, Kurokawa J, Kuribayashi M, Uno I, Hara H (2011) Temporal variations of nitrogen wet deposition across Japan from 1989 to 2008. J Geophys Res 116:D06307. doi:10.1029/2010JD015205

    Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagakura J, Kaneko S, Takahashi M, Tange T (2008) Nitrogen promotes water consumption in seedlings of Cryptomeria japonica but not in Chamaecyparis obtuse. Forest Ecol Manag 255:2533–2541

    Article  Google Scholar 

  • Nakaji T, Izuta T (2017) Effects of nitrogen load on Asian trees. In: Izuta T (ed) Air pollution impacts on plants in East Asia. Springer, Japan, pp 271–280

    Chapter  Google Scholar 

  • Nakaji T, Fukami M, Dokiya Y, Izuta T (2001) Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings. Trees Struct Funct 15:453–461

    CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nashimoto M, Takahashi K (1992) Decline of Japanese cedar (Cryptomeria japonica D. Don) trees in the Kanto-Koshin and Kansai-Setouchi districts. Jpn J For Environ 32:70–78 (in Japanese with English summary)

    Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noguchi I, Yamaguchi T (2010) Nitrogen deposition from atmosphere. Chikyu Kankyo 15(2):111–120 (in Japanese)

    Google Scholar 

  • Ogawa K, Miwa M, Shimada T (2007) Effects of ozone and water stress on the growth of cedar seedlings. Man and Environment 33:60–68 (in Japanese)

    Google Scholar 

  • Ohara T, Akimoto H, Kurokawa J, Horii N, Yamaji K, Yan X, Hayasaka T (2007) An Asian emission inventory of anthropogenic emission source for the period 1980–2020. Atmos Chem Phys 7:4419–4444

    Article  CAS  Google Scholar 

  • Osório ML, Osório J, Vieira AC, Gonçalves S, Romano A (2011) Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering. Photosynthetica 49:3–12

    Article  Google Scholar 

  • Panković D, Sakač Z, Kevrešan S, Plesničar M (1999) Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism. J Exp Bot 50:127–138

    Article  Google Scholar 

  • Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312

    Article  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Bühler J, Van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850

    Article  Google Scholar 

  • Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1:430–437

    Article  CAS  Google Scholar 

  • Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis–nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiol 23:137–144

    Article  PubMed  Google Scholar 

  • Salazar-Parra C, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Morales M (2012) Climate change (elevated CO2, elevated temperature and moderate drought) triggers the antioxidant enzymes’ response of grapevine cv. Tempranillo, avoiding oxidative damage. Physiol Plant 144:99–110

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  PubMed  Google Scholar 

  • Szabó I, Bergantino E, Giacometti GM (2005) Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO reports 6:629–634

    Article  PubMed  PubMed Central  Google Scholar 

  • Tezara W, Driscoll S, Lawlor DW (2008) Partitioning of photosynthetic electron flow between CO2 assimilation and O2 reduction in sunflower plants under water deficit. Photosynthetica 46:127–134

    Article  CAS  Google Scholar 

  • Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and rubisco in loblolly pine seedlings. Plant Cell Environ 16:859–865

    Article  CAS  Google Scholar 

  • Villar-Salvador P, Peñuelas JL, Jacobs DF (2013) Nitrogen nutrition and drought hardening exert opposite effects on the stress tolerance of Pinus pinea L. seedlings. Tree Physiol 33:221–232

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Matsuo N, Yamaguchi M, Matsumura H, Kohno Y, Izuta T (2009) Risk assessment of ozone impact on the carbon absorption of Japanese representative conifers. Eur J For Res 129:421–430

    Article  Google Scholar 

  • Yamaguchi M, Watanabe M, Iwasaki M, Tabe C, Matsumura H, Kohno Y, Izuta T (2007) Growth and photosynthetic responses of Fagus crenata seedlings to O3 under different nitrogen loads. Trees-Struct Funct 21:707–718

    Article  CAS  Google Scholar 

  • Zhang LX, Li SX, Zhang H, Liang ZS (2007) Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes. J Agron Crop Sci 193:387–397

    Article  CAS  Google Scholar 

  • Zhou S, Medlyn B, Sabaté S, Sperlich D, Prentice IC (2014) Short-term water stress impacts on stomatal, mesophyll and biochemical limitations to photosynthesis differ consistently among tree species from contrasting climates. Tree Physiol 34:1035–1046

    Article  CAS  PubMed  Google Scholar 

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Acknowledgement

The authors acknowledge the members of Prof. Izuta Laboratory (Tokyo University of Agriculture and Technology) for their valuable suggestions and technical support.

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  1. Masahiro Yamaguchi

    Present address: Graduate School of Fisheries and Environmental Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki, 852-8521, Japan

Authors and Affiliations

  1. The United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Akira Motai

  2. The Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Yuichiro Terada, Ayumi Kobayashi, Daiki Saito & Hirofumi Shimada

  3. Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Masahiro Yamaguchi & Takeshi Izuta

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  1. Akira Motai
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Motai, A., Terada, Y., Kobayashi, A. et al. Combined effects of irrigation amount and nitrogen load on growth and needle biochemical traits of Cryptomeria japonica seedlings. Trees 31, 1317–1333 (2017). https://doi.org/10.1007/s00468-017-1551-5

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