Skip to main content

Advertisement

Log in

Modulation of structural carbohydrates, phenol compounds and lignin content in Eucalyptus urophylla cuttings grown under boron, copper and zinc induced-deficiency

  • Published:
New Forests Aims and scope Submit manuscript

Abstract

Micronutrients participate in various plant metabolic pathways, including the synthesis of carbohydrates, lignin, and phenols, which are necessary for plant growth and defense against pests and pathogens. In this study, we evaluated the effects of nutrient solutions deplete in B, Cu, or Zn on the nutrition, growth, and production of biochemical compounds in Eucalyptus urophylla cuttings. The experiment was carried out in a greenhouse for 90 days, with clonal cuttings of E. urophylla at four months of age. The treatments evaluated were complete fertilization (CF) and individual omissions of B, Cu, and Zn in the nutrient solution. The omission of Cu and Zn increased the concentration of carbohydrates in the leaves by 10% and reduced the rate of CO2 assimilation (A) by more than 30%. Cu omission decreased the lignification process compared to complete fertilization. Flavonoid production in plants with complete fertilization was 45–75% higher than that in plants maintained under B, Cu, or Zn deficiencies. Collectively, these results suggest that micronutrient deficiencies may reduce plant productivity as well as plant resistance to pests and pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • ABRAF (2010) Anuário estatístico da ABRAF 2010 ano base 2009/ ABRAF. – Brasília, p 140

  • Alvares CA, Sentelhas PC, Mattos EM, Miranda AC, Moraes WB, Silva PHM, Furtado EL, Stape JL (2017) Climatic favorability zones for Eucalyptus rust in Brazil. Forest Pathol 47:1–17

    Article  Google Scholar 

  • Battie-Laclau P, Laclau JP, Beri C, Mietton L, Muniz MRA, Arenque BC, Piccolo MC, Jordan-Meille L, Bouilet JP, Nouvellon V (2014) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ 37:70–81

    Article  CAS  PubMed  Google Scholar 

  • Blount JW, Dixon RA, Paiva NL (1992) Stress responses in alfalfa (Medicago sativa L.) XVI. Antifungal activity of medicarpin and its biosynthetic precursors; implications for the genetic manipulation of stress metabolites. Physiol Mol Plant Pathol 41:333–349

    Article  CAS  Google Scholar 

  • Bonello P, Blodgett JT (2003) Pinus nigraSphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol Mol Plant Physiol 63:249–261

    Article  Google Scholar 

  • Chormova D, Fry SC (2016) Boron bridging of rhamnogalacturonan-II is promoted in vitro by cationic chaperones, including polyhistidine and wall glycoproteins. New Phytol 209:241–251

    Article  CAS  PubMed  Google Scholar 

  • Chow PS, Landhausser SMA (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136

    Article  CAS  PubMed  Google Scholar 

  • Dalcorso G, Manara A, Piasentina S, Furinia A (2014) Nutrient metal elements in plants. Metallomics 6(10):1770–1788

    Article  CAS  PubMed  Google Scholar 

  • Dell B, Huang L (1997) Physiological responses of plants to low boron. Plant Soil 193:85–101

    Article  Google Scholar 

  • Dell B, Malajczuk N (1994) Boron deficiency in eucalypt plantations in China. Can J Res 24(12):2409–2416

    Article  Google Scholar 

  • Dell B, Robinson JM (1993) Symptoms of mineral nutrient deficiencies and the nutrient concentration ranges in seedlings of Eucalyptus maculata Hook. Plant Soil 155–156:255–261

    Article  Google Scholar 

  • Dell B, Xu D (1995) Diagnosis of zinc deficiency in seedlings of a tropical eucalypt (Eucalyptus urophylla S.T. Blake). Plant Soil 176:329–332

    Article  CAS  Google Scholar 

  • Dell B, Xu D, Rogers C, Huang L (2003) Micronutrient disorders in eucalypt plantations: causes, symptoms, identification, impact and management. In: Wei R, Xu D (eds) Eucalyptus plantations: research, management and development. World Scientific Publising, London, pp 241–252

    Chapter  Google Scholar 

  • Dell B, Hardy G, Burgess T (2008) Health and nutrition of plantation eucalypts in Asia. Southern Forests JForest Sci 70(2):131–138

    Article  Google Scholar 

  • dos Santos EF, S, Zanchim B J, Campos A G, Garrone, R F, Lavres, J, (2013) Photosynthesis rate, chlorophyll content and initial development of physic nut without micronutrient fertilization. R Bras Ci Solo 37:1334–1342

    Article  Google Scholar 

  • du Toit B, Smith CW, Little KM, Boreham G, Pallett RN (2010) Intensive, site-specific silviculture: Manipulating resource availability at establishment for improved stand productivity. A review of South African research. Forest Ecol Manag 259(9):1836–1845

    Article  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric methods for determination of sugars related substances. Anal Chem 28(3):350–356

    Article  CAS  Google Scholar 

  • Elmer WH, Datnoff LE (2014) Mineral nutrition and suppression of plant disease. In: van Alfen N (ed) Encyclopedia of agriculture and food systems, 4 edn. Elsevier, San Diego, pp 231–244

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2, Sunderland Mass: Sinauer, p 400

  • Ferraz A, Mendonça R, Silva FT (2000) Organosolv delignification of white- and brown-rotted Eucalyptus grandis hardwood. J Chem Technol Biotechnol 75:18–24

    Article  CAS  Google Scholar 

  • Gonçalves JLM, Alvares CA, Higa RA, Silva LD, Alfenas AC, Stahl J, Ferraz SFB, Paula Lima W, Brancalion PHS, Hubner A, Bouillet JPD, Laclau JP, Nouvellon Y, Epron D (2013) Integrating genetic and silvicultural strategies to minimize abiotic and biotic constraints in Brazilian eucalypt plantations. For Ecol Manage 301:6–27

    Article  Google Scholar 

  • Graham RD (1980) The distribution of copper and soluble carbohydrates in wheat plants grown at high and low levels of copper supply. Zeitschrift Für Pflanzenernährung Und Bodenkunde 143(2):161–169

    Article  CAS  Google Scholar 

  • Hagen-Thorn A, Stjernquist I (2005) Micronutrient levels in some temperate European tree species: a comparative field study. Trees 19:572–579

    Article  CAS  Google Scholar 

  • Hajiboland R, Amirazad F (2010) Growth, photosynthesis and antioxidant defense system in Zn-deficient red cabbage plants. Plant, Soil Environ 56:209–217

    Article  CAS  Google Scholar 

  • Huber D, Römheld V, Weinmann M (2012) Relationship between nutrition, plant diseases and pests. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, San Diego, pp 283–298

    Chapter  Google Scholar 

  • IBA Relatório IBA (2017) [s.l: s.n.]. Disponível em:. https://iba.org/images/shared/Biblioteca/IBA_RelatorioAnual2017.pdf. Accessed 27 July 2020

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain pehnolics. J Agric Food Chem 33(2):213–217

    Article  CAS  Google Scholar 

  • Kastori R, Plesnicar M, Pankovic D, Sakac Z (1995) Photosynthesis, chlorophyll flu- orescence and soluble carbohydrates in sunflower leaves as affected by boron deficiency. J Plant Nutr 18:1751–1763

    Article  CAS  Google Scholar 

  • Kim T, Wetzstein HY (2003) Cytological and ultrastructural evaluations of zinc deficiency in leaves. J Am Soc Hortic Sci 128:171–175

    Article  CAS  Google Scholar 

  • Kulbat K (2016) The role of phenolic compounds in plant resistance. Biotechnol Food Sci 80(2):97–108

    Google Scholar 

  • Lehto T, Ruuhola T, Dell B (2010) Boron in forest trees and forest ecosystems. For Ecol Manage 260:2053–2069

    Article  Google Scholar 

  • Li JW, Richter DD, Mendoza A, Heine P (2008) Four-decade responses of soil trace elements to an aggrading old-field forest: B, Mn, Zn, Cu, and Fe. Ecology 89:2911–2923

    Article  PubMed  Google Scholar 

  • Li DD, Li YJ, Liang J, Zhao CZ, Yin HJ, Yin CY, Cheng XY, Liu Q (2014) Responses of soil micronutrient availability to experimental warming in two constrasting forest ecosystems in the Eastern Tibetan Plateau, China. Journal of Soils and Sediments 14(6), 1050–1060. Ma D, Sun D, Wang C, Ding H, Qin H, Hou J, Huang X, Xie Y, Guo T (2017) Physiological responses and yield of wheat plants in zinc-mediated alleviation of drought stress. Front Plant Sci 8:1–12

    Google Scholar 

  • Liakopoulos G, Karabourniotis G (2005) Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. Tree Physiol 25(3):307–315

    Article  CAS  PubMed  Google Scholar 

  • Mabry TJ, Markham KR, Thomas MB (1970) The Systematic Identification of the Flavonoids. Springer, New York, p 354

    Book  Google Scholar 

  • Malavolta E, Vitti GC, Oliveira SA (1997) Avaliação do estado nutricional das plantas. Princípios e aplicações. 2, POTAFOS, Piracicaba, p 319

  • Marschner H (2012) Mineral nutrition of higher plants. In: Marschner H, Marschner P (eds) Mineral nutrition of higher plants. Academic Press

  • Martín-Rejano EM, Camacho-Cristóbal JJ, Herrera-Rodríguez MB, Rexach J, Navarro-Gochicoa MT, González-Fontes A (2011) Auxin and ethylene are involved in the responses of root system architecture to low boron supply in Arabidopsis seedlings. Physiol Plant 142:170–178

    Article  PubMed  Google Scholar 

  • Masullo LS, Ferraz AV, de Gonçalves JL, M, Camargo L E A, Ávila P A de, Drago J R, Esteves O, Dias C T dos S, (2020) Relationship between forest residue management and micronutrient fertilization with eucalyptus rust severity in Eucalyptus grandis. Forest Ecol Manag 475:118443

    Article  Google Scholar 

  • Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: Structure and Function of a Borate Cross-Linked Cell Wall Pectic Polysaccharide. Annu Rev Plant Biol 55:109–139

    Article  PubMed  Google Scholar 

  • Pandey N, Sharma CP (2000) Carbonic anhydrase activity and stomata morphology associated with zinc deficiency induced changes in faba bean. Phytomorphology 50:261–265

    Google Scholar 

  • Prasad D, Singh A, Singh KP, Bist S, Tewari A, Singh UP (2010) The role of phenolic compounds in disease resistance in geranium. Arch Phytopathol Plant Protect 43(7):615–623

    Article  CAS  Google Scholar 

  • Printz B, Lutts S, Hausman JF, Sergean K (2016) Copper trafficking in plants and its implication on cell wall dynamics. Front Plant Sci 7:1–16

    Article  Google Scholar 

  • Rocha JHT, Wenzel AVA, Melo EASC et al (2019) Responses of coppiced Eucalyptus to macro- and micronutrient application. New for 50:717–731

    Article  Google Scholar 

  • Santos RM, Fortes GAC, Ferri PH, Santos CS (2011) Influence of foliar nutrients on phenol level in leaves of Eugenia uniflora. Brazilian J Pharmacogn 21:581–586

    Article  CAS  Google Scholar 

  • Sasaki H, Hirose T, Watanabe Y, Ohsugi R (1998) Carbonic anhydrase activity and CO2-transfer resistance in Zn-deficient rice leaves. Plant Physiol 118(3):929–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekimoto H, Hoshi M, Nomura T, Yokota T (1997) Zinc deficiency affects the levels of endogenous gibberellins in Zea mays L. Plant Cell Physiol 38:1087–1090

    Article  CAS  Google Scholar 

  • Sequeira CH, Barros NF, Neves JCL, Novais RF, Silva IR, Alley M (2011) Micronutrient soil-test levels and eucalyptus foliar contents. Commun Soil Sci Plant Anal 42(4):475–488

    Article  CAS  Google Scholar 

  • Seth K, Aery NC (2014) Effect of boron on the contents of chlorophyll, carotenoid, phenol and soluble leaf protein in mung Bean, Vigna radiata (L) Wilczek. Proc. Natl. Acad Sci India Sect B Biol Sci 84:713–719

    Article  CAS  Google Scholar 

  • Sharma CP (2006) Plant micronutrients. Science Publishers, Enfield, p 265

    Book  Google Scholar 

  • Shi C, Wang J, Hu R, Zhou G, O’Neill MA, Kong Y (2017) Boron-bridged RG-II and calcium are required to maintain the pectin network of the Arabidopsis seed mucilage ultrastructure. Plant Mol Biol 94(3):267–280

    Article  CAS  PubMed  Google Scholar 

  • Silveira RLVA, Higashi EN (2003) Aspectos nutricionais envolvidos na ocorrência de doenças com ênfase para o eucalipto. Circular Técnica IPEF 200:1–13

    Google Scholar 

  • Silveira RLVA, Higashi EN, Gonçalves NA, Moreira A (2005) Evaluation of the nutritional status of eucalypts: visual and foliar diagnoses and their interpretation. In: Gongalves JLM, Benedetti V (eds) Forest nutrition and fertilization. IPEF, Piracicaba/BR, pp 85–111

  • Smith AH, Gill WM, Pinkard EA, Mohammed CL (2007) Anatomical and histochemical defense responses induced in juvenile leaves of Eucalyptus globulus and Eucalyptus nitens by Mycosphaerella infection. For Pathol 37:361–373

    Article  Google Scholar 

  • Tavares GA, Bendassolli JA, Souza G, Nolasco FR (2004) Implantação de uma estação de produção de água desionizada para uso nos laboratórios do Cena / Usp empregando resinas de troca-iônica. Revista Analytica 10(7):36–42

    Google Scholar 

  • Thomas G, Andresen E, Mattusch J, Hubáček T, Küpper H (2016) Deficiency and toxicity of nanomolar copper in low irradiance - A physiological and metalloproteomic study in the aquatic plant Ceratophyllum demersum. Aquat Toxicol 177:226–236

    Article  CAS  PubMed  Google Scholar 

  • Turnbull CRA, Beadle CL, West PW, Crome RN (1994) Copper deficiency a probable cause of stem deformity in fertilised Eucalyptus nitens. Can J for Res 24(7):1434–1439

    Article  CAS  Google Scholar 

  • Wang N, Yang C, Pan Z, Liu Y, Peng S (2015) Boron deficiency in woody plants: various responses and tolerance mechanisms. Front Plant Sci 6:1–14

    Article  Google Scholar 

  • Waterman PG (1992) Roles for secondary metabolites in plants. Ciba Found Symp 171:255–269

    CAS  PubMed  Google Scholar 

  • Whitham FH, Blaydes DF, Devlin RM (1971) Experiments in plant physiology. Van Nostrand Reinhold, New York, p 254p

    Google Scholar 

  • Wimmer MA, Abreu I, Bell RW, Bienert MD, Brown PH, Dell B, Fujiwara T, Goldbach HE, Lehto T, Mock HP, von Wirén N, Bassil E, Bienert GP (2019) Boron: an essential element for vascular plants: a comment on Lewis (2019) “Boron: the essential element for vascular plants that never was.” New Phytol 1232–1237

Download references

Funding

This study received support from São Paulo Research Foundation—FAPESP (Process: 2018/07294–3), The Brazilian National Council for Scientific and Technological Development (CNPq) and Silviculture and Management Thematic Program (PTSM-IPEF).

Author information

Authors and Affiliations

Authors

Contributions

LSM, AVF and JLMG designed this research. LSM, VDD, GRM, PAA and ALF performed this research. LSM, VDD and JHTR analyzed the data. JLMG, AVF, CLA, JL and JHTR revised this draft by rewriting, discussion and commenting. All authors contributed in the same way to the preparation of all the parts of this manuscript.

Corresponding author

Correspondence to Liamara Santos Masullo.

Ethics declarations

Conflict of interest

None declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Masullo, L.S., Derisso, V.D., Manarim, G.R. et al. Modulation of structural carbohydrates, phenol compounds and lignin content in Eucalyptus urophylla cuttings grown under boron, copper and zinc induced-deficiency. New Forests 53, 337–352 (2022). https://doi.org/10.1007/s11056-021-09859-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11056-021-09859-w

Keywords

Navigation