Carbon allocation, nodulation, and biological nitrogen fixation of black locust (Robinia pseudoacacia L.) under soil water limitation

Authors

  • Dario Mantovani Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Via Nursina 2, 06049 - Spoleto
  • Maik Veste Brandenburg University of Technology Cottbus-Senftenberg, Chair of Soil Protection and Recultivation, Konrad-Wachsmann-Allee 6, 03046 Cottbus, Germany
  • Katja Boldt-Burisch Brandenburg University of Technology Cottbus-Senftenberg, Chair of Soil Protection and Recultivation, Konrad-Wachsmann-Allee 6, 03046 Cottbus, Germany
  • Simone Fritsch Brandenburg University of Technology Cottbus-Senftenberg, Chair of Soil Protection and Recultivation, Konrad-Wachsmann-Allee 6, 03046 Cottbus, Germany
  • Laurie Anne Koning University of Rostock, Crop Health, Satower Straße 48, 18059 Rostock, Germany
  • Dirk Freese Brandenburg University of Technology Cottbus-Senftenberg, Chair of Soil Protection and Recultivation, Konrad-Wachsmann-Allee 6, 03046 Cottbus, Germany

DOI:

https://doi.org/10.15287/afr.2015.420

Keywords:

Rhizobium, water use efficiency, carbon, nitrogen, natural 15Nabundance, drought stress

Abstract

The pioneer tree black locust (Robinia pseudoacacia L.) is a drought-resistant tree and, in symbiosis with Rhizobium, able to fix dinitrogen from the atmosphere. It is, therefore, an interesting species for marginal lands where soil amelioration is sought in addition to economic gain. However, the interaction between soil water availability, carbon allocation and nitrogen fixation is important for a successful establishment of trees on marginal lands and has not yet been investigated for black locust. Twoyear-old trees were grown under various soil water conditions and drought cycles. The stable isotopic composition of C (δ 13C) and N (δ 15N) of the leaves was used to identify i) the effective drought condition of the treatments and ii) the portion N accrued from the atmosphere by the biological nitrogen fixation. Drought-stressed plants significantly reduced their total aboveground biomass production, which was linearly linked to tree transpiration. The shoot:root ratio values changed from 2.2 for the drought-stressed to 4.3 for the well-watered plants. Our investigation shows that drought stress increases the nodule biomass of black locust in order to maintain biological nitrogen fixation and to counteract the lower soil nitrogen availability. The biological nitrogen fixation of drought-stressed trees could be maintained at relatively higher values compared to the well-watered trees. The average leaf nitrogen content varied between 2.8% and 3.0% and was not influenced by the drought stress. Carbon fixation, carbon allocation, and biological nitrogen fixation are to some extent balanced at low irrigation and allow Robinia to cope with long-term water constraints. The combination of black locust’s ecophysiological and morphological plasticity make it interesting as a biomass source for bioenergy and timber production, even in nutrient-limited and drought-affected areas of Europe.

References

Aranjuelo I., Tcherkez G., Molero G., Francoise G., Avice J.C., Nogués S., 2013. Concerted changes in N and C primary metabolism in alfalfa (Medicago sativa) under water restriction. Journal of Experimental Botany 64: 1–17. AranjueloI., Arrese-Igor C., Molero G., 2014. Nodule performance within a changing environmental context. Journal of Plant Physiology 171: 1076-1090. Batzli J.M., Graves W.R., van Berkum P., 1992. Diversity among Rhizobia effective with Robinia pseudoacacia L. Applied and Environmental Microbiology 58(7): 2137-2143. Bloom A.J., Chapin F.S., Mooney, H.A., 1985. Resource limitation in plants-an economic analogy. Annual Review of Ecology and Systematics 16: 363-392. Böhm C., Quinkenstein A., Freese D., 2011. Yield prediction of young black locust (Robinia pseudoacacia L.) plantations for woody biomass production using allometric relations. Annals ofForestResearch 54 (2): 215–227. Boddey R.M., Peoples M.B., Palmer B., Dart P.J., 2000. Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutrient Cycling in Agroecosystems 57: 235-270. Bréda N., Badeau, V., 2008.Foresttree responses to extreme drought and some biotic events : towards a selection according to hazard tolerance? Comptes Rendus Geoscience 340 (9-10): 651-662. Boring L.R., Swank W.T., 1984. The role of black locust (Robinia pseudoacacia L.) in forest succession. Journal of Ecology 72: 749-766. CairnsM.A., Brown S., Helmer E.H., Baumgardner G.A., 1997. Root biomass allocation in the world's upland forests. Oecologia, 111(1): 1-11. Cheng X., Zhao Z., Guo M., Wang D., Yuan Z.,2007. Amodel for vertical distribution of fine roots in Robinia pseudoacacia plantations on the Loess Plateau. Frontiers of Forestry inChina2 (3): 291-297. Cierjacks A., Kowarik I., Joshi J., Hempel S., Ristow M., von der Lippe M., Weber E., 2013. Biological Flora of theBritish Isles: Robinia pseudoacacia. Journal of Ecology 101 (6): 1623-1640. Cramer M.D., Van Cauter A., Bond W.J., 2010. Growth of N2-fixing African savanna Acacia species is constrained by below-ground competition with grass. Journal of Ecology 98: 156-167. Delucia E.H., Schlesinger W.H.,BillingsW.D., 1988. Water relations and maintenance of Sierra conifers on hydrothermally altered rock. Ecology 69: 303-311. Dilly O., Nii-Annang S., Schrautzer J., Breuer V., Pfeiffer E.-M., Gerwin W., Schaaf W., Freese D., Veste M. Hüttl, R.F., 2010. Ecosystem manipulation and restoration on the basis of long-term conceptions. In: Müller F., Baessler C., Schubert H., Klotz S. (eds.), Long-Term Ecological Research Between Theory and Application, Springer Science+Business Media, Amsterdam, pp. 411-428. Enescu C. M., Dănescu A., 2013. Black locust (Robinia pseudoacacia L.) - an invasive neophyte in the conventional land reclamation flora inRomania. Bulletin of theTransilvaniaUniversityofBrasov, Series II - Forestry, Wood Industry, Agricultural Food Engineering 6: 23-30. Erice G., Sanz-Sáez A., Aroca R., Ruíz-Lozano J.M., Avice J.-C., Irigoyen J.J., Sanchez-Diaz M., Aranjuelo I., 2014. Photosynthetic down-regulation in N2-fixing alfalfa under elevated CO2 alters rubisco content and decreases nodule metabolism via nitrogenase and tricarboxylic acid cycle. Acta Physiologiae Plantarum 36: 2607-2617. Farquhar G.D., O'Leary M.H.,BerryJ.A., 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Functional Plant Biology 9(2): 121-137. Ferrari A.E., Wall L.G., 2007. Nodulation and growth of black locust (Robinia pseudoacacia L.) on a de-surfaced soil inoculated with a local Rhizobium isolate. Biology and Fertility of Soils 43(4): 471-477. Gálvez L., González E.M., Arrese-Igor C., 2005. Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J.Exp. Bot.56: 2551- 2561. Gao X.F., Wang J.X., Zhang B., Ma H.F., Zhong N., 2010. Effects of drought stress on dry matter partitioning of young Robinia pseudoacacia at its different growth stages. Chinese Journal of Ecology 29: 1103-1108. Grünewald H., Böhm C., Quinkenstein A., Grundmann P., Eberts J., von Wühlisch G., 2009. Robinia pseudoacacia L.: a lesser known tree species for biomass production. BioEnergy Research 2(3): 123-133. Gray S.B., Strellner R.S., Puthuval K.K., Ng C., Shulman R.E., Siebers M.H., Rogers A., Leakey, A.D.B., 2013. Minirhizotron imaging reveals that nodulation of field-grown soybean is enhanced by free-air CO2 enrichment only when combined with drought stress. Functional Plant Biology 40 (2): 137-147 Hoagland, D.R., Arnon D.I., 1950. The water-culture method for growing plants without soil.CaliforniaAgricultural Experiment Station, Circular 347,UniversityofCalifornia, pp. 1-32. Johnsen K.H., Bongarten B.C., 1991. Allometry of acetylene reduction and nodule growth of Robinia pseudoacacia families subjected to varied root zone nitrate concentrations. Tree Physiology 9: 50-522. Johnsen KH, Bongarten B.C., 1992. Relationships between nitrogen fixation and growth in Robinia pseudoacacia L. seedlings: A functional growth analysis approach using 15N. Physiologia Plantarum 85 (1): 77-84. Kanzler M., Böhm C., Freese D., 2015. Impact of P fertilisation on the growth performance of black locust (Robinia pseudoacacia L.) in a lignite post-mining area inGermany. Annals ofForestResearch 58 (1): 1-16. Khan B., Ablimit A., Mahmood R., Qasim M., 2010. Robinia pseudoacacia leaves improve soil physical and chemical properties. Journal of Arid Land 2(4): 266-271. Kirda C.S.K.A., Danso S.K.A., Zapata F. 1989. Temporal water stress effects on nodulation, nitrogen accumulation and growth of soybean. Plant and Soil 120 (1): 49-55. DOI: 10. 1007/BF02370289 Kriebitzsch W.-U., Veste M., 2012. Bedeutung trockener Sommer für die Photosynthese und Transpiration von verschiedenen Herkünften der Rotbuche (Fagus sylvatica L.) [Importance of dry summer for photo- synthesis and transpiration of different provenances of beech (Fagus sylvatica L.)]. Landbauforschung 62(4): 193-209. Küppers M., 1992. Changes in resource-use efficiency in different woody growth forms during secondary forest succession inCentral Europe. In: Teller A., Mathy P., Jeffers J.N.R., (eds.). Responses of Forest Ecosystems to Environmental Changes, Springer,Heidelberg, pp 628-630 Ladrera R., Marino D., Larrainzar E., González E.M., Arrese-Igor C., 2007. Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiology 145 (2): 539-546. Lambers H., Chapin III F.S., Pons T.L., 2008. Plant physiological ecology. Springer-Verlag, NewYork. 605 pp. Landgraf D., Wedig S., Klose S., 2005. Medium- and short term available organic matter, microbial biomass, and enzyme activities in soils under Pinus sylvestris L. and Robinia pseudoacacia L. in a sandy soil in NE Saxony, Germany. Journal of Plant Nutrition and Soil Science 168(2): 193-201. Larcher, W., 2003. Physiological plant ecology. Springer,Heidelberg,,New York, 514 pp. Leuschner C., Backes K., Hertel D., Schipka F., Schmitt U., Terborg O., Runge M., 2001. Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years.ForestEcology and Management 149: 33-46. Li P., Zhao Z., Li Z., Xue S., 2011. Root distributions and drought resistance of plantation tree species on the Weibei Loess Plateau inChina. African Journal of Agricultural Research 21: 4989-4997. Linderson M.L., Iritz Z., Lindroth A., 2007. The effect of water availability on stand-level productivity, transpiration, water use efficiency and radiation use efficiency of field-grown willow clones. Biomass and Bioenergy 31(7): 460-468. Lindroth A., Cienciala E., 1996. Water use efficiency of short-rotation Salix viminalis at leaf, tree and stand scales. Tree Physiology 16 (1-2): 257-262. López M., Lluch C., 2008. Nitrogen fixation is synchronized with carbon metabolism in Lotus japonicus and Medicago truncatula nodules under salt stress. Journal of Plant Interactions 3 (3): 137-144. Lopez M.L., Mizota C., Nobori Y., Sasaki T., Yamanaka T., 2014. Temporal changes in nitrogen acquisition of Japanese black pine (Pinus thunbergii) associated with black locust (Robinia pseudoacacia). Journal of Forestry Research 25(3): 585−589.Mantovani D., Freese D., Veste M., Hüttl R.F., 2011. Modified wick lysimeters for critical water use efficiency evaluation and yield crop modelling. In: Conference proceedings 14th Lysimeter Conference Lysimeters in Climate Change Research and Water Resources Management", pp. 245-248 Mantovani D., Veste, M., Badorreck A., Freese D., 2013. Evaluation of fast growing tree transpiration under different soil moisture regimes using wicked lysimeters. iForest - Journal of Biogeosciences and Forestry 6: 190-200. Mantovani D., Veste M., Freese D., 2014a. Black locust (Robinia pseudoacacia L.) ecophysiological and morphological adaptations to drought and their consequence on biomass production and water use efficiency. New ZealandJournal of Forestry 44: 29. DOI: 10.1186/ s40490-014-0029-0 Mantovani D., Veste M., Freese D., 2014b. Effects of drought frequency on growth performance and transpiration of young black locust (Robinia pseudoacacia L.). International Journal of Forestry Research 2014, Article ID 821891, 1-11 pages. DOI: 10.1155/2014/ 821891 Marino D., Frendo P., Ladrera R., Zabalza A., Puppo A., Arrese-Igor C., González E.M., 2007. Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiology 143(4): 1968-1974. DOI: 10.1104/pp.107.097139 Malcolm G.M., Bush D.S., Rice S.K., 2008. Soil nitrogen conditions approach pre-invasion levels following restoration of nitrogen-fixing black locust (Robinia pseudoacacia) stands in a pine-oak ecosystem. Restoration Ecology 16 (1): 70–78. DOI: 10.1111/j.1526-100X. 2007.00263.x Matos E.S., Freese D., Böhm C., Quinkenstein A., Hüttl R.F., 2012. Organic matter dynamics in reclaimed lignite mine soils under Robinia pseudoacacia L. plantations of different ages in Germany. Communications in Soil Science and Plant Analysis 43: 745–755. DOI: 10.1080/ 00103624.2012.648354 Meier I.C., Leuschner C., 2008. Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biology 14: 2081-2095. DOI: 10.1111/j.1365-2486.2008.01634.x Mokany K., Raison R., Prokushkin A.S., 2006. Critical analysis of root:shoot ratios in terrestrial biomes. Global Change Biology 12(1): 84-96. DOI: 10.1111/j.1365-2486.2005. 001043.x Moro MJ, Domingo F, Bermudez-de-Castro, F. 1992. Acetylene reduction activity (ARA) by the shrub legume Adenocarpus decorticans Boiss. in southernSpain(Almeria). Acta Oecologia 13:325–333. Noh N.J., Son Y., Koo J., Seo K.W., Kim R.H., Lee Y.Y., Yoo K.S., 2010. Comparison of nitrogen fixation for north-and south-facing Robinia pseudoacacia stands in Central Korea. Journal of Plant Biology 53(1): 61-69. DOI: 10.1007/s12374-009-9088-9 Olesen P.O., 1971. Water displacement method: a fast and accurate method of determining the green volume of wood samples. Forest Tree Improvement Vol. 3, pp.1–23. Qiu L., Zhang X., Cheng J., Yin X., 2010. Effects of black locust (Robinia pseudoacacia L.) on soil properties in the loessial gully region of the Loess Plateau, China. Plant and Soil 332 (1-2): 207–217. DOI: 10.1007/s11104-010-0286-5 Quinkenstein A., Böhm C., Matos E., Freese D., Hüttl R.F., 2011. Assessing the carbon sequestration in short rotation coppice systems of Robinia pseudoacacia on marginal sites in NE-Germany. In: Kumar B.M., Nair P.K.R. (eds.) Advances in Agroforestry: Carbon sequestration potential of agroforestry systems - opportunities and challenges. Springer, Heidelberg, pp. 201–216. DOI: 10.1007/978-94-007-1630-8_11 Quinkenstein A., Pape D., Freese D., Schneider B.U., Hüttl RF., 2012. Biomass, carbon and nitrogen distribution in living woody plant parts of Robinia pseudoacacia L. growing on reclamation sites in the mining region of Lower Lusatia (Northeast Germany). International Journal of Forestry Research. Article ID 891798, 1–10. doi:10.1155/2012/891798. DOI: 10.1155/2012/891798 Rédei K.,CsihaI., Keserű Z., 2011. Black locust (Robinia pseudoacacia L.) short-rotation crops under marginal site conditions. Acta Silvatica et Lignaria Hungarica, 7: 125–132. Rice S.K., Westerman B., Federici R., 2004. Impacts of the exotic, nitrogen-fixing black locust (Robinia pseudoacacia) on nitrogen cycling in a pine-oak ecosystem. Ecology 174 (1): 97–107. DOI: 10.1023/b:vege.0000046049.21900.5a Russow R., Veste M., Littmann T., 2004. Using the natural 15N-abundance to assess the major nitrogen inputs into the sand dune area of the north-western NegevDesert(Israel). Isotopes in Environmental and Health Studies 40: 57-67. DOI: 10.1080/102560103100 01646554 Russow R., Veste M., Breckle S.-W., Littmann T., Böhme, F. 2008. Nitrogen input pathways into the sand dunes: biological fixation and atmospheric nitrogen deposition. In: Breckle, S.-W, Yair, A., Veste, M. (eds.), Arid Dune Ecosystems. Ecological Studies 200, Springer, BerlinHeidelbergNew York, pp. 319-336. DOI: 10.1007/978-3-540-75498-5_22 Serraj R., Sinclair T.R., Purcell L.C., 1999. Symbiotic N2 fixation response to drought. Journal of Experimental Botany 50(331):143-155. DOI: 10.1093/jxb/50.331.143 Serraj R, Sinclair TR. 1996. Inhibition of nitrogenase activity and nodule oxygen permeability by water deficit. Journal of Experimental Botany 47, 1067–1073. DOI: 10.1093/jxb/47.8.1067 Schulze E.D., Gebauer G., Ziegler H., Lange O.L., 1991. Estimates of nitrogen fixation by trees on an aridity gradient in Namibia. Oecologia 88(3): 451-455. DOI: 10.1007/ BF00317592 Sukopp H., 2004. Human-caused impact on preserved vegetation. Landscape and Urban Planing 68 (4): 347-355. DOI: 10.1016/S0169-2046(03)00152-X Talbi C., Sánchez C., Hidalgo-Garcia A., González E.M., Arrese-Igor C., Girard L., Bedmar E.J., Delgado, J. 2012. Enhanced expression of Rhizobium etli cbb3 oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. Journal of Experimental Botany 63,: 5035-5043. DOI: 10.1093/jxb/ers101 Veste M., Böhm C., Quinkenstein A., Freese D., 2013. Biologische Stickstoff-Fixierung der Robinie [Biological nitrogen fixation of back locust]. AFZ-Der Wald 2/2013: 40-42. Veste M., Kriebitzsch W.U., 2013. Einfluss von Trockenstress auf Photosynthese, Transpiration und Wachstum junger Robinien (Robinia pseudoacacia L.) [Influence of drought stress on photosynthesis, transpiration, and growth of juvenile black locust (Robinia pseudoacacia L.)]. Forstarchiv 84:35-42. Vlachodimos K., Papatheodorou E.M., Diamantopoulos J., Monokrousos N., 2013. Assessment of Robinia pseudoacacia cultivations as a restoration strategy for reclaimed mine spoil heaps. Environ. Monit. Assess. 185: 6921-6932. DOI: 10.1007/s10661-013-3075-9 Wang X., Fang J., Zhu B., 2008. Forest biomass and root–shoot allocation in northeast China. ForestEcology and Management 255(12): 4007-4020. DOI: 10.1016/j.foreco.2008.03.055 Walter J., Nagy L., Hein R., Rascher U., Beierkuhnlein C., Willnerd E., Jentsch A., 2011. Do plants remember drought? Hints towards a drought-memory in grasses. Environmental and Experimental Botany 71 (1): 34-40. DOI: 10.1016/j.envexpbot.2010.10.020 Wurzburger N., Miniat C.F., 2013. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174: 1117-1126. DOI: 10.1007/s00442-013-2851-0 Xu F., Guo W., Wang R., Xu W., Du N., Wang Y. 2009. Leaf movement and photosynthetic plasticity of black locust (Robinia pseudoacacia L.) alleviate stress under different light and water conditions. Acta Physiologiae Plantarum, 31(3): 553-563. DOI: 10.1007/s11738-008-0265-0 Yin C., Wang X., Duan B., Luo J., Li C., 2005. Early growth, dry matter allocation and water use efficiency of two sympatric Populus species as affected by water stress. Environmental and Experimental Botany 53: 315-322. DOI: 10.1016/j.envexpbot.2004.04.007 Zahran H.H., 1999. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiology and Molecular Biology Reviews 63(4): 968-989. Zeleznik J.D., Skousen J.G., 1996. Land reclamation: survival of three tree species on old reclaimed surface mines in Ohio. Journal of Environmental Quality 25:1429-1435. DOI: 10.2134/jeq1996.00472425002500060037x

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2015-07-27

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