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Low soil phosphorus availability has limited effects on wood traits in young plants of five eucalypt species

Published online by Cambridge University Press:  27 May 2024

Franklin Magnum de Oliveira Silva
Affiliation:
Department of Plant Biology, Institute of Biology, State University of Campinas, Campinas, Brazil
Helena Augusto Gioppato
Affiliation:
Department of Plant Biology, Institute of Biology, State University of Campinas, Campinas, Brazil
Alexandre Augusto Borghi
Affiliation:
Department of Plant Biology, Institute of Biology, State University of Campinas, Campinas, Brazil
Sara Adrián López Andrade
Affiliation:
Department of Plant Biology, Institute of Biology, State University of Campinas, Campinas, Brazil
Paulo Mazzafera*
Affiliation:
Department of Plant Biology, Institute of Biology, State University of Campinas, Campinas, Brazil
*
Corresponding author: Paulo Mazzafera; Email: pmazza@unicamp.br

Summary

Plant-derived products rely heavily on the availability of phosphorus (P) in the soil. With reserves of P-rocks being limited, there is a growing demand to enhance the efficiency of P utilization by crops. Eucalypts, an important economic crop in many countries, is a source of timber, coal, essence oils, and cellulose. After identifying low P tolerant and susceptible species in a previous study, we explored the various physiological and biochemical responses of these same species to low P availability. The aim was to expand our understanding of how different P-nutrition responses might impact eucalypt wood production and traits related to its quality. Our results indicate that low soil P minimally affects physiological wood parameters in the young trees of Eucalyptus acmenoides, Corymbia maculata, E. grandis, E. globulus, and E. tereticornis. Decreases in cellulose contents and increases in lignin content and syringyl and guaiacyl (S/G) ratios were observed under low P and only in E. acmenoides plants. Wood density remained unaffected in all species. Additionally, bark, stem, and root P concentrations increased under sufficient P conditions in E. globulus, E. grandis, and E. tereticornis. These findings suggest that these plant parts may act as reserve pools of this nutrient.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Baker, A., Ceasar, S.A., Palmer, A.J., Paterson, J.B., Qi, W., Muench, S.P. and Baldwin, S.A. (2015) Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. Journal of Experimental Botany 66(12), 35233540. https://doi.org/10.1093/jxb/erv210 CrossRefGoogle ScholarPubMed
Bhering, L.L. (2017) Rbio: A tool for biometric and statistical analysis using the R platform. Crop Breeding and Applied Biotechnology 17, 187190.CrossRefGoogle Scholar
Börcsök, Z. and Pásztory, Z. (2021) The role of lignin in wood working processes using elevated temperatures: an abbreviated literature survey. European Journal of Wood and Wood Products 79, 511526.CrossRefGoogle Scholar
Bulgarelli, R.G., de Oliveira Silva, F.M., Bichara, S., Andrade, S.A.L. and Mazzafera, P. (2019) Eucalypts and low phosphorus availability: between responsiveness and efficiency. Plant and Soil 445, 349368.CrossRefGoogle Scholar
Carnus, J.-M., Parrotta, J., Brockerhoff, E., Arbez, M., Jactel, H., Kremer, A., Lamb, D., O’Hara, K. and Walters, B. (2006) Planted forests and biodiversity. Journal of Forestry 104, 6577.CrossRefGoogle Scholar
Carstensen, A., Herdean, A., Schmidt, S.B., Sharma, A., Spetea, C., Pribil, M. and Husted, S. (2018) The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiology 177, 271284.CrossRefGoogle ScholarPubMed
Cesarino, I., Araújo, P., Domingues, A.P. Jr. and Mazzafera, P. (2012) An overview of lignin metabolism and its effect on biomass recalcitrance. Revista Brasileira de Botânica 35, 303311.Google Scholar
Chen, L., Auh, C., Chen, F., Cheng, X., Aljoe, H., Dixon, R.A. and Wang, Z. (2002) Lignin deposition and associated changes in anatomy, enzyme activity, gene expression, and ruminal degradability in stems of tall fescue at different developmental stages. Journal of Agriculture and Food Chemistry 50, 55585565.CrossRefGoogle ScholarPubMed
Crous, K.Y., Ósvaldsson, A. and Ellsworth, D.S. (2015) Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant and Soil 391, 293305.CrossRefGoogle Scholar
de Andrade, S.A.L., de Oliveira, V.H. and Mazzafera, P. (2024) Metabolomics of nutrient-deprived forest trees. In Antonio, C. (ed.), Monitoring Forest Damage with Mass Spectrometry-Based Metabolomics Methods. New York, NY: Wiley, pp. 235265.CrossRefGoogle Scholar
de Moraes Gonçalves, J.L., Stape, J.L., Laclau, J-P., Smethurst, P. and Gava, J.L. (2004) Silvicultural effects on the productivity and wood quality of eucalypt plantations. Forest Ecology and Management 193, 4561.CrossRefGoogle Scholar
de Oliveira Silva, F.M., Bulgarelli, R.G., Mubeen, U., Caldana, C., Andrade, S.A.L. and Mazzafera, P. (2022) Low phosphorus induces differential metabolic responses in eucalyptus species improving nutrient use efficiency. Frontiers in Plant Science 13, 989827.CrossRefGoogle Scholar
Fukushima, R.S., Kerley, M.S., Ramos, M.H., Porter, J.H. and Kallenbach, R.L. (2015) Comparison of acetyl bromide lignin with acid detergent lignin and Klason lignin and correlation with in vitro forage degradability. Animal Feed Science and Technology 201, 2537.CrossRefGoogle Scholar
González-Vila, F.J., Almendros, G., del Rio, J.C., Martıín, F., Gutiérrez, A. and Romero, J. (1999) Ease of delignification assessment of wood from different Eucalyptus species by pyrolysis (TMAH)-GC/MS and CP/MAS 13 C-NMR spectrometry. Journal of Analytical Applied Pyrolysis 49, 295305.CrossRefGoogle Scholar
Hacke, U.G., Sperry, J.S. and Pittermann, J. (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic and Applied Ecology 1, 3141.CrossRefGoogle Scholar
Hawkesford, M., Horst, W., Kichey, T., Lambers, H., Schjoerring, J., Møller, I.S. and White, P. (2012) Functions of macronutrients. In Marschner, P. (ed.), Marschner’s Mineral Nutrition of Higher Plants. Amsterdam, Netherlands: Elsevier/Academic Press, pp. 135189.CrossRefGoogle Scholar
Horikawa, Y. (2022) Structural diversity of natural cellulose and related applications using delignified wood. Journal of Wood Science 68, 54.CrossRefGoogle Scholar
IUSS Working Group WRB (2015) World Reference Base for Soil Resources 2014, Update 2015. International Soil Classification System for Naming Soils and Creating Legends for Soil Maps. World Soil Resources Reports No. 106, Rome: FAO.Google Scholar
Jucker, T., Sanchez, A.C., Lindsell, J.A., Allen, H.D., Amable, G.S. and Coomes, D.A. (2016) Drivers of aboveground wood production in a lowland tropical forest of West Africa: teasing apart the roles of tree density, tree diversity, soil phosphorus, and historical logging. Ecology and Evolution 6, 40044017.CrossRefGoogle Scholar
Keith, H., Raison, R.J. and Jacobsen, K.L. (1997) Allocation of carbon in a mature eucalypt forest and some effects of soil phosphorus availability. Plant and Soil 196, 8199.CrossRefGoogle Scholar
Lambers, H. (2023) Nutrient-use efficiency. In Rengel, Z., Cakmak, I., White, P.J. (eds.), Marschner’s Mineral Nutrition of Plants. London: Elsevier, pp. 651664.CrossRefGoogle Scholar
Lambers, H. and Plaxton, W.C. (2015) Phosphorus: back to the roots. Annual Plant Reviews 48, 322.Google Scholar
Lambers, H., Shane, M.W., Cramer, M.D., Pearse, S.J. and Veneklaas, E.J. (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693713.CrossRefGoogle ScholarPubMed
Liu, Q., Luo, L. and Zheng, L. (2018) Lignins: biosynthesis and biological functions in plants. International Journal of Molecular Science 19, 335.CrossRefGoogle ScholarPubMed
Lourenço, A., Gominho, J., Marques, A.V. and Pereira, H. (2013) Variation of lignin monomeric composition during kraft pulping of Eucalyptus globulus heartwood and sapwood. Journal of Wood Chemistry and Technology 33, 118.CrossRefGoogle Scholar
Luo, X., Li, Z., Xiao, S., Ye, Z., Nie, X., Zhang, X., Kong, J. and Zhu, L. (2021) Phosphate deficiency enhances cotton resistance to Verticillium dahliae through activating jasmonic acid biosynthesis and phenylpropanoid pathway. Plant Science 302, 110724.CrossRefGoogle ScholarPubMed
Mahood, S.A. and Cable, D.E. (1922) The chemistry of wood. Journal of Industrial and Engineering Chemistry 14, 933934.CrossRefGoogle Scholar
Mclaughlin, M., Alston, A. and Martin, J. (1988) Phosphorus cycling in wheat pasture rotations. I. The source of phosphorus taken up by wheat. Soil Research 26, 323.CrossRefGoogle Scholar
Mokochinski, J.B., Bataglion, G.A., Kiyota, E., de Souza, L.M., Mazzafera, P. and Sawaya, A.C.H.F. (2015) A simple protocol to determine lignin S/G ratio in plants by UHPLC-MS. Analytical and Bioanalytical Chemistry 407, 72217227.CrossRefGoogle ScholarPubMed
Mulligan, D.R. (1988) Phosphorus concentrations and chemical fractions in Eucalyptus seedlings grown for a prolonged period under nutrient-deficient conditions. New Phytologist 110, 479486.CrossRefGoogle Scholar
Netzer, F., Herschbach, C., Oikawa, A., Okazaki, Y., Dubbert, D., Saito, K. and Rennenberg, H. (2018) Seasonal alterations in organic phosphorus metabolism drive the phosphorus economy of annual growth in F. sylvatica Trees on P-Impoverished Soil. Frontiers in Plant Science 9, 723. https://doi.org/10.3389/fpls.2018.00723 CrossRefGoogle ScholarPubMed
Ogden, M., Hoefgen, R., Roessner, U., Persson, S. and Khan, G. (2018) Feeding the walls: how does nutrient availability regulate cell wall composition? International Journal of Molecular Science 19, 2691.CrossRefGoogle ScholarPubMed
Pavinato, P.S., Cherubin, M.R., Soltangheisi, A., Rocha, G.C., Chadwick, D.R. and Jones, D.L. (2020) Revealing soil legacy phosphorus to promote sustainable agriculture in Brazil. Scientific Reports 10, 15615.CrossRefGoogle ScholarPubMed
Raymond, C.A. and Muneri, A. (2000) Effect of fertilizer on wood properties of Eucalyptus globulus . Canadian Journal of Forest Research 30, 136144.CrossRefGoogle Scholar
Rocha, J.H.T., de Moraes Gonçalves, J.L., de Vicente Ferraz, A., Poiati, D.A., Arthur Junior, J.C. and Hubner, A. (2019) Growth dynamics and productivity of an Eucalyptus grandis plantation under omission of N, P, K Ca and Mg over two crop rotation. Forest Ecology Management 447, 158168.CrossRefGoogle Scholar
Tabet, T.A. and Aziz, F.A. (2013) Cellulose microfibril angle in wood and its dynamic mechanical significance. In Van De Ven, T., Godbout, L. (eds.), Cellulose, Fundamental Aspects. London, UK: INTECH - Open Science, pp. 113142.Google Scholar
Thomas, D.S., Montagu, K.D. and Conroy, J.P. (2005) Why does phosphorus limitation increase wood density in Eucalyptus grandis seedlings? Tree Physiology 26, 3542.CrossRefGoogle Scholar
Uhde-Stone, C., Zinn, K.E., Ramirez-Yáñez, M., Li, A., Vance, C.P. and Allan, D.L. (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiology 131, 10641079.CrossRefGoogle Scholar
Vaccari, D.A. (2009) Phosphorus: a looming crisis. Scientific American 300, 5459.CrossRefGoogle ScholarPubMed
Valadares, S.V., Neves, J.C.L., Leite, H.G., de Barros, N.F., Cropper, W.P. and Gerber, S. (2020) Predicting phosphorus use efficiency and allocation in eucalypt plantations. Forest Ecology Management 460, 117859.CrossRefGoogle Scholar
van de Wiel, C.C.M., van der Linden, C.G. and Scholten, O.E. (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207, 122.CrossRefGoogle Scholar
van Raij, B., Cantarella, H., Quaggio, J.A. and Furlani, A.M.C. (1996) Recomendações de adubação e calagem para o Estado de São Paulo. Campinas: Instituto Agronômico de Campinas, pp. 285. (Boletim Técnico, 100).Google Scholar
Vanholme, R., Demedts, B., Morreel, K., Ralph, J. and Boerjan, W. (2010) Lignin biosynthesis and structure. Plant Physiology 153, 895905.CrossRefGoogle ScholarPubMed
Veneklaas, E.J., Lambers, H., Bragg, J., Finnegan, P.M., Lovelock, C.E., Plaxton, W.C., Price, C.A., Scheible, W.-R.R., Shane, M.W., White, P.J. and Raven, J.A. (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306320.CrossRefGoogle ScholarPubMed
Vicentini, R., Bottcher, A., Brito, M.D.S., dos Santos, A.B., Creste, S., Landell, M.G.D.A., Cesarino, I. and Mazzafera, P. (2015) Large-scale transcriptome analysis of two sugarcane genotypes contrasting for lignin content. PLoS One 10, e0134909.CrossRefGoogle Scholar
Warren, C.R. (2011) How does P affect photosynthesis and metabolite profiles of Eucalyptus globulus? Tree Physiology 31, 727739.CrossRefGoogle Scholar
White, P.J. and Hammond, J.P. (2008) Phosphorus nutrition of terrestrial plants. In White, P.J., Hammond, J.P. (eds.), The Ecophysiology of Plant-Phosphorus Interactions. Dordrecht, the Netherlands: Springer, pp. 5181.CrossRefGoogle Scholar
Xu, D., Dell, B., Malajczuk, N. and Gong, M. (2002) Effects of P fertilisation on productivity and nutrient accumulation in a Eucalyptus grandis × E. urophylla plantation in southern China. Forest Ecology and Management 161, 89100. https://doi.org/10.1016/S0378-1127(01)00485-6 CrossRefGoogle Scholar
Xu, X., Zhu, T., Nikonorova, N. and de Smet, I. (2019) Phosphorylation-mediated signalling in plants. Annual Plant Reviews Online 2, 909932.CrossRefGoogle Scholar
Yoo, C.G., Dumitrache, A., Muchero, W., Natzke, J., Akinosho, H., Li, M., Sykes, R.W., Brown, S.D., Davison, B., Tuskan, G.A. and Pu, Y. (2018) Significance of lignin S/G ratio in biomass recalcitrance of Populus trichocarpa variants for bioethanol production. ACS Sustain Chem Eng 6, 21622168.CrossRefGoogle Scholar
Zhang, W., Ma, W., Ji, Y., Fan, M., Oenema, O. and Zhang, F. (2008) Efficiency, economics, and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutr Cycl Agroecosyst 80, 131144.CrossRefGoogle Scholar
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