Abstract
Key message
Eucalypt seedlings differently modulate root morphology in response to phosphorus availability, with changes in the length or density of root hairs being more common that changes in root length.
Abstract
Phosphorus (P) is an essential nutrient for plant growth and development and thus can restrict biomass accumulation when it is at low levels in the soil. Eucalypts cover large areas of planted forests in the world, including regions with naturally low P availability. This study was conducted to evaluate the morphological changes in the roots of seedlings of five eucalypt species: Eucalyptus acmenoides, E. globulus, E. grandis, E. tereticornis and Corymbia maculata in response to low P concentration. Seedlings were grown in pots with vermiculite and received a nutrient solution of low (25 μM), and sufficient concentration (500 μM) of P. Root hair length and density were evaluated in secondary root segments, and the production of plant biomass and P concentration in the shoots were determined. The species modulated root morphology differently in response to P limitation. E. tereticornis showed the lowest plasticity of these morphological traits in response to P concentration. The total root length increased in some species, but changes in the length and/or density of root hairs were the commonest response to low P concentration. P concentrations in the shoots and biomass production were not related to increase of root length or root hair density and length.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Data are available on reasonable request to the corresponding author.
References
Bahar NHA, Gauthier PPG, O’Sullivan OS, Brereton T, Evans JR, Atkin OK (2018) Phosphorus deficiency alters scaling relationships between leaf gas exchange and associated traits in a wide range of contrasting Eucalyptus species. Funct Plant Biol 45(8):813–826. https://doi.org/10.1071/FP17134
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236(2):243–250. https://doi.org/10.1023/A:1012791706800
Binkley D, Vitousek P (2000) Soil nutrient availability. In: Pearcy RW, Ehleringer J, Mooney HA, Rundel PW (eds) Plant physiological ecology field methods and instrumentation. Chapman & Hall, London, pp 75–96. https://doi.org/10.1007/978-94-010-9013-1
Brown LK, George TS, Dupuy LX, White PJ (2013) A conceptual model of root hair ideotypes for future agricultural environments: what combination of traits should be targeted to cope with limited P availability? Ann Bot-London 112(2):317–330. https://doi.org/10.1093/aob/mcs231
Bulgarelli RG, Silva FMO, Bichara S, Andrade SAL, Mazzafera P (2019) Eucalypts and low phosphorus availability: between responsiveness and efficiency. Plant Soil 445(1–2):349–368. https://doi.org/10.1007/s11104-019-04316-2
Cao X, Chen C, Zhang D, Shu B, Xiao J, Xia R (2013) Influence of nutrient deficiency on root architecture and root hair morphology of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings under sand culture. Sci Hortic 162:100–105. https://doi.org/10.1016/j.scienta.2013.07.034
Del-Saz NF, Romero-Munar A, Cawthray GR, Palma F, Aroca R, Baraza E, Florez-Sarasa I, Lambers H, Ribas-Carbó M (2018) Phosphorus concentration coordinates a respiratory bypass, synthesis and exudation of citrate, and the expression of high-affinity phosphorus transporters in Solanum lycopersicum. Plant Cell Environ 41(4):865–875. https://doi.org/10.1111/pce.13155
Dias LPR, Gatiboni LC, Brunetto G, Arruda B, Costa MM (2017) Distribuição e morfologia do sistema radicular de Eucalyptus dunnii em resposta à aplicação de fósforo. Rev Cienc Agrovet 16(3):203–213. https://doi.org/10.5965/223811711632017203
Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147(1):33–42. https://doi.org/10.1046/j.1469-8137.2000.00686.x
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cienc Agrotec 35(6):1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Flores T, Alvares CA, Souza V, Stape JL (2016) Eucalyptus no Brasil: zoneamento climático e guia para identificação. Piracicaba, IPEF, p. 488
Foehse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74(3):359–368. https://doi.org/10.1007/BF02181353
Friesen DK, Rao IM, Thomas RJ, Oberson A, Sanz JI (1997) Phosphorus acquisition and cycling in crop and pasture systems in low fertility tropical soils. Plant Soil 196(2):289–294. https://doi.org/10.1023/A:1004226708485
Funayama-Noguchi S, Noguchi K, Terashima I (2014) Comparison of the response to phosphorus deficiency in two lupin species, Lupinus albus and L. angustifolius, with contrasting root morphology. Plant Cell Environ 38(3):399–410. https://doi.org/10.1111/pce.12390
Graciano C, Guiamét JJ, Goya JF (2005) Impact of nitrogen and phosphorus fertilization on drought responses in Eucalyptus grandis seedlings. For Ecol Manag 212(1–3):40–49. https://doi.org/10.1016/j.foreco.2005.02.057
Grattapaglia D, Kirst M (2008) Eucalyptus applied genomics: from gene sequences to breeding tools. Plant Physiol 179(4):911–929. https://doi.org/10.1111/j.1469-8137.2008.02503.x
Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163(1):161–179. https://doi.org/10.1007/s10681-015-1572-3
Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013) Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. J Exp Bot 64(12):3711–3721. https://doi.org/10.1093/jxb/ert200
Haling RE, Brown LK, Stefanski A, Kidd DR, Ryan MH, Sandral GA, George TS, Lambers H, Simpson RJ (2018) Differences in nutrient foraging among Trifolium subterraneum cultivars deliver improved P-acquisition efficiency. Plant Soil 424(1–2):539–554. https://doi.org/10.1007/s11104-017-3511-7
Hinsinger P, Gilkes RJ (1996) Mobilization of phosphate from phosphate rock and alumina-sorbed phosphate by the roots of ryegrass and clover as related to rhizosphere pH. Eur J Soil Sci 47(4):533–544. https://doi.org/10.1111/j.1365-2389.1996.tb01853.x
Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:32
Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35(2):227–239
Huang G, Hayes PE, Ryan MH, Pang J, Lambers H (2017) Peppermint trees shift their phosphorus-acquisition strategy along a strong gradient of plant-available phosphorus by increasing their transpiration at very low phosphorus availability. Oecologia 185(3):387–400. https://doi.org/10.1007/s00442-017-3961-x
Kakade D, Singh J, Wallalwar M, Janjal A, Gupta A, Raghuvanshi R, Kongbrailatpam M, Verulkar S, Banerjee S (2017) Differential response of root morphology of rice (Oryza sativa L.) genotypes under different phosphorus conditions. Int J Curr Microbiol Appl Sci 6(7):149–160. https://doi.org/10.20546/ijcmas.2017.607.018
Klamer F, Vogel F, Li X, Bremer H, Neumann G, Neuhäuser B, Hochholdinger F, Ludewig U (2019) Estimating the importance of maize root hairs in low phosphorus conditions and under drought. Ann Bot 124(6):961–968. https://doi.org/10.1093/aob/mcz011
Kramer-Walter KR, Laughlin DC (2017) Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant Soil 416:539–550. https://doi.org/10.1007/s11104-017-3234-9
Lambers H, Plaxton WC (2018) Phosphorus: back to the roots. Annu Plant Rev 48:3–22. https://doi.org/10.1002/9781119312994
Li D, Nan H, Liang J, Cheng X, Zhao C, Yin H, Yin C, Liu Q (2017) Responses of nutrient capture and fine root morphology of subalpine coniferous tree Picea asperata to nutrient heterogeneity and competition. PLoS ONE 12(11):e0187496. https://doi.org/10.1371/journal.pone.0187496
Liu CY, Zhang F, Zhang DJ, Zou YN, Shu B, Wu QS (2020) Transcriptome analysis reveals improved root hair growth in trifoliate orange seedlings by arbuscular mycorrhizal fungi. Plant Growth Regul 92:195–203. https://doi.org/10.1007/s10725-020-00630-3
Loew CAE, Schack-Kirchner H, Fink S, Lang F (2020) Fine root size and morphology of associated hyphae reflect the phosphorus nutrition strategies of european beech forests. Front Glob Change 3:1–15. https://doi.org/10.3389/ffgc.2020.00095
Lugli LF, Andersen KM, Aragão LEOC, Cordeiro AL, Cunha HFV, Fuchslueger L, Meir P, Mercado LM, Oblitas E, Quesada CA, Rosa JS, Schaap KJ, Valverde-Barrantes O, Hartley IP (2019) Multiple phosphorus acquisition strategies adopted by fine roots in low-fertility soils in Central Amazonia. Plant Soil 450:49–63. https://doi.org/10.1007/s11104-019-03963-9
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56. https://doi.org/10.1007/s11104-004-1096-4
Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24(4):459–467. https://doi.org/10.1046/j.1365-3040.2001.00695.x
Ma Q, Chen L, Du M, Zhang Y, Zhang Y (2020) Localized and moderate phosphorus application improves plant growth and phosphorus accumulation in Rosa multiflora thunb. ex murr. via efficient root system development. Forests 11(5):570. https://doi.org/10.3390/f11050570
Ma X, Li X, Ludewig U (2021) Arbuscular mycorrhizal colonization outcompetes root hairs in maize under low phosphorus availability. Ann Bot-London 127(1):155–166. https://doi.org/10.1093/aob/mcaa159
Marschner H (2012) The mineral nutrition of higher plants. Academic Press, London, p 158
Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between root hair length and basal root growth angle for phosphorus acquisition. Plant Physiol 167(4):1430–1439. https://doi.org/10.1104/pp.15.00145
Palmer CM, Bush SM, Maloof JN (2012) Phenotypic and developmental plasticity in plants. In: eLS. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0002092.pub2
Pérez-Cruzado C, Merino A, Rodríguez-Soalleiro R (2011) A management tool for estimating bioenergy production and carbon sequestration in Eucalyptus globulus and Eucalyptus nitens grown as short rotation woody crops in north-west Spain. Biomass Bioenerg 35(7):2839–2851. https://doi.org/10.1016/j.biombioe.2011.03.020
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193(1):30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49. https://doi.org/10.1007/s11104-004-2005-6
Rongsawat T, Peltier J, Boyer J, Véry A, Sentenac H (2020) Looking for root hairs to overcome poor soils. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2020.09.001
Rossel RAV, Bui EN (2016) A new detailed map of total phosphorus stocks in Australian soil. Sci Total Environ 542:1040–1049. https://doi.org/10.1016/j.scitotenv.2015.09.119
Ruiz S, Koebernick N, Duncan S, Fletcher DM, Scotson C, Boghi A, Marin M, Bengough AG, George TS, Brown LK, Hallett PD, Roose T (2020) Significance of root hairs at the field scale—modelling root water and phosphorus uptake under different field conditions. Plant Soil 447:281–304. https://doi.org/10.1007/s11104-019-04308-2
Sandral GA, Haling RE, Ryan MH, Price A, Pitt WM, Hildebrand SM, Fuller CG, Kidd DR, Stefanksi A, Lambers H, Simpson RJ (2018) Intrinsic capacity for nutrient foraging predicts critical external phosphorus requirement of 12 pasture legumes. Crop Pasture Sci 69(2):174–182. https://doi.org/10.1071/CP17276
Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100(2):309–316. https://doi.org/10.1111/j.1365-2745.2011.01904.x
Silva IM, Schiavon NC, França AC, Franco MHR, Farneza MM (2019) Respostas de genótipos de Coffea arabica à aplicação de fósforo em substrato com ácido cítrico. Rev Cienc Agrar 62:1–7. https://doi.org/10.22491/rca.2019.2768
Tang H, Chen X, Gao Y, Hong L, Chen Y (2020) Alteration in root morphological and physiological traits of two maize cultivars in response to phosphorus deficiency. Rhizosphere 14:100201. https://doi.org/10.1016/j.rhisph.2020.100201
Thomas DS, Montagu KD, Conroy JP (2006) Leaf inorganic phosphorus as a potential indicator of phosphorus status, photosynthesis and growth of Eucalyptus grandis seedlings. For Ecol Manag 223:267–274. https://doi.org/10.1016/j.foreco.2005.11.006
Trindade RS, Araujo AP (2014) Variability of root traits in common bean genotypes at different levels of phosphorus supply and ontogenetic stages. Rev Bras Cienc Solo 38(4):1170–1180. https://doi.org/10.1590/S0100-06832014000400013
Valadares SV, César J, Leite HG, Barros NF, Cropper WP, Gerber S (2020) Predicting phosphorus use efficiency and allocation in eucalypt plantations. For Ecol Manag 460:117859. https://doi.org/10.1016/j.foreco.2019.117859
Van de Wiel CCM, Gerard WC, Olga L, Scholten E (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207(1):1–22. https://doi.org/10.1007/s10681-015-1572-3
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157(3):423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Vandamme E, Renkens M, Pypers P, Smolders E, Vanlauwe B, Merckx R (2013) Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient ferralsol. Plant Soil 369(1–2):269–282. https://doi.org/10.1007/s11104-012-1571-2
Wang XX, Li H, Chu Q, Feng G, Kuyper TW, Rengel Z (2020) Mycorrhizal impacts on root trait plasticity of six maize varieties along a phosphorus supply gradient. Plant Soil 448:71–86. https://doi.org/10.1007/s11104-019-04396-0
White PJ, Hammond JP (2008) The ecophysiology of plant–phosphorus interactions (vol. 7). Springer Science & Business Media, Dordrecht
Wu P, Ma X, Tigabu M, Huang Y, Zhou L, Cai L, Hou X, Oden PC (2014) Comparative growth, dry matter accumulation and photosynthetic rate of seven species of Eucalypt in response to phosphorus supply. J for Res 25(2):377–383. https://doi.org/10.1007/s11676-014-0465-y
Xia Z, He Y, Yu L, Miao J, Korpelainen H, Li C (2020) Root traits and rhizosphere processes reflect differential phosphorus acquisition strategies in contrasting Populus clones. For Ecol Manag 457:117750. https://doi.org/10.1016/j.foreco.2019.117750
Yan XL, Wang C, Ma X, Wu P (2019) Root morphology and seedling growth of three tree species in southern China in response to homogeneous and heterogeneous phosphorus supplies. Trees Struct Funct 33(5):1283–1297. https://doi.org/10.1007/s00468-019-01858-x
Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Change 5(5):465–469. https://doi.org/10.1038/NCLIMATE2549
Yuan HM, Blackwell M, McGrath S, George TS, Granger SH, Hawkins JMB, Dunham S, Dunham JM, Shen JB (2016) Morphological responses of wheat (Triticum aestivum L.) roots to phosphorus supply in two contrasting soils. J Agric Sci 154(1):98–108. https://doi.org/10.1017/S0021859615000702
Zhang C, Simpson RJ, Kim CM, Warthmann N, Delhaize E, Dolan L, Byrne ME, Wu Y, Ryan PR (2018) Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol 217(4):1654–1666. https://doi.org/10.1111/nph.14980
Zhou C, Jiang W, Li Y, Hou X, Liu A, Cai L (2017) Morphological plasticity and phosphorus uptake mechanisms of hybrid Eucalyptus roots under spatially heterogeneous phosphorus stress. J for Res 28(4):713–724. https://doi.org/10.1007/s11676-016-0335-x
Zhu J, Zhang C, Lynch JP (2010) The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Funct Plant Biol 37(4):313–322. https://doi.org/10.1071/FP09197
Acknowledgements
The authors thank Espaço da Escrita—Pró-Reitoria de Pesquisa—UNICAMP for the language services provided. We also would like to thank anonymous reviewer #1 for helpful comments and generous feedback.
Funding
This study was supported by the São Paulo Research Foundation (FAPESP—Grant Number 2016/25498-0). We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brazil (CNPq) and FAPESP for a MSc fellowship to SB (FAPESP Grant Number 2019/03165-7) and a research fellowship to PM (CNPq).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that there are no conflicts of interest/competing interests in this study.
Additional information
Communicated by V. De Micco.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bichara, S., Mazzafera, P. & de Andrade, S.A.L. Root morphological changes in response to low phosphorus concentration in eucalypt species. Trees 35, 1933–1943 (2021). https://doi.org/10.1007/s00468-021-02161-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-021-02161-4