Plant and Soil

, Volume 437, Issue 1–2, pp 313–326 | Cite as

Aluminum-accumulating Vochysiaceae species growing on a calcareous soil in Brazil

  • Matheus Armelin Nogueira
  • Anna C. G. Bressan
  • Marcelo H. O. Pinheiro
  • Gustavo HabermannEmail author
Regular Article



Cerrado woody species are divided into a small group of aluminum (Al)-accumulating species and the rest of the woody species. Both groups grow well on acidic and Al-rich soils. We found a Cerrado remnant growing on a calcareous soil with high calcium (Ca) and low Al saturations (m%). We checked whether Al deposition differs between leaf veins and leaf blade, and predicted that plants grown on the acidic soil store more Al than those grown on the calcareous soil.


Adult plants of Qualea grandiflora and Q. parviflora, two Al-accumulators, were found in this area, and we compared leaf Ca and Al concentrations with those of the same species growing on a dystrophic Cerrado soil.


Leaf Ca concentration reflected differences between the soil types, and Ca was more accumulated in leaf veins. However, Al accumulation was independent of m%, and it was more deposited in the leaf blade of both species, which was confirmed by hystochemical reactions and X-ray spectra in SEM analysis (EDS).


The leaf tissue to which Al is preferentially allocated in the leaf blade could not be distinguished. Granules in epidermal cells exhibiting high Al EDS peaks suggest an important allocation for this metal.


Al Calcium Leaf blade Qualea sp SEM analysis X-ray spectra 



MA Nogueira acknowledges the Coordination for the Improvement of Higher Education Personnel (Capes) for a MSc. scholarship. ACG Bressan acknowledges the São Paulo Research Foundation (Fapesp Grant# 2014/14386-0) for a PhD scholarship, and G. Habermann acknowledges the Brazilian National Council for Scientific and Technological Development (CNPq) for a productivity fellowship (Grant# 309149/2017-7).

Authors’ contribution

ACGB, MAN and GH conceived and designed the experiments. ACGB, MAN and MHOP performed the experiments. ACGB, MAN and GH analyzed the data. ACGB, MAN, MHOP and GH wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11104_2019_3978_Fig8_ESM.png (146.7 mb)
Fig. S1

Location map of the study area of cerrado sensu stricto remnants growing on a calcareous soil in the municipality of Ituiutaba, Minas Gerais state (A, C) and on an acidic soil in the municipality of Mogi Guaçu, São Paulo state (B, E), southeastern Brazil, in South America (D) (PNG 150174 kb)

11104_2019_3978_MOESM1_ESM.tif (138.2 mb)
High Resolution Image (TIF 141507 kb)
11104_2019_3978_MOESM2_ESM.docx (15 kb)
ESM 1 (DOCX 14 kb)


  1. Alves VN, Torres JLR, Lana RMQ, Pinheiro MHO (2018) Nutrient cycling between soil and leaf litter in the Cerrado (Brazilian savanna) on eutrophic and dystrophic Neosols. Acta Bot Bras 32:169–179CrossRefGoogle Scholar
  2. Andrade LRM, Barros LMG, Echevarria GF, do Amaral LIV, Cotta MG, Rossatto DR, Haridasan M, Franco AC (2011) Al-Hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Env Exp Bot 70:37–42CrossRefGoogle Scholar
  3. Bressan ACG, Coan AI, Habermann G (2016) X-ray spectra in SEM and staining with chrome azurol S show Al deposits in leaf tissues of Al - accumulating and non-accumulating plants from the cerrado. Plant Soil 404:293–306CrossRefGoogle Scholar
  4. Chenery EM (1948) Aluminium in the plant world. Kew Bull 3:173–183CrossRefGoogle Scholar
  5. Dantas VL, Batalha MA (2011) Vegetation structure: fine scale relationships with soil in a cerrado site. Flora 206:341–346CrossRefGoogle Scholar
  6. Empresa Brasileira de Pesquisa Agropecuária (Embrapa) (1997) Manual for methods of soil analyses, 2nd edn. Embrapa, Rio de JaneiroGoogle Scholar
  7. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  8. Givnish TJ (1988) Adaptation to sun and shade: a whole plant perspective. Austr J Plant Physiol 15:63–92Google Scholar
  9. Guilherme Pereira C, Clode PL, Oliveira RS, Lambers H (2018) Eudicots from severely phosphorus-impoverished environments preferentially allocate phosphorus to their mesophyll. New Phytol 218:959–973CrossRefGoogle Scholar
  10. Habermann G, Bressan ACG (2011) Root, shoot and leaf traits of the congeneric Styrax species may explain their distribution patterns in the Cerrado sensu lato areas in Brazil. Funct Plant Biol 38:209–218CrossRefGoogle Scholar
  11. Habermann G, Bressan-Smith R (2013) Will we have enough to eat in the near future? What the Brazilian Society of Plant Physiology and the Global Plant Council have to do with it? Theor Exp Plant Physiol 25:244–250CrossRefGoogle Scholar
  12. Haridasan M (1982) Aluminium accumulation by some cerrado native species of Central Brazil. Plant Soil 65:265–273CrossRefGoogle Scholar
  13. Haridasan M (2001) Nutrient cycling as a function of landscape and biotic characteristics in the Cerrado of Central Brazil. In: McClain ME, Victoria RL, Richey JE (eds) Biogeochemistry of the Amazon basin and its role in a changing world. Oxford University Press, New York, pp 68–83Google Scholar
  14. Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Braz J Plant Physiol 20:183–195CrossRefGoogle Scholar
  15. Haridasan M, Araújo GM (1988) Aluminium-accumulating species in two forest communities in the Cerrado region of Central Brazil. For Ecol Manag 24:15–26CrossRefGoogle Scholar
  16. Haridasan M, Araújo GM (2005) Perfil nutricional de espécies lenhosas de duas florestas semidecíduas em Uberlândia, MG. Rev Bras Bot 28:295–303CrossRefGoogle Scholar
  17. Haridasan M, Paviani TI, Schiavini I (1986) Localization of aluminium in the leaves of some aluminium-accumulating species. Plant Soil 94:435–437CrossRefGoogle Scholar
  18. Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot Rev 68:235–269CrossRefGoogle Scholar
  19. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Co, New YorkGoogle Scholar
  20. Karnovsky MJ (1965) A formaldehyde- glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  21. Kissmann C, Tozzi HH, Martins S, Habermann G (2012) Germination performance of congeneric Styrax species from the Cerrado sensu lato areas and their distribution pattern in different physiognomies. Flora 207:673–681CrossRefGoogle Scholar
  22. Kukachka BF, Miller R (1980) A chemical spot-test for aluminum and its value in wood identification. IAWA Bull 3:104–109CrossRefGoogle Scholar
  23. Liu Y, Dawson W, Prati D, Haeuser E, Feng Y, van Kleunen M (2016) Does greater specific leaf area plasticity help plants to maintain a high performance when shaded? Ann Bot 118:1329–1336CrossRefGoogle Scholar
  24. Malta PG, Silva AS, Ribeiro C, Campos NV, Azevedo AA (2016) Rudgea viburnoides (Rubiaceae) overcomes the low soil fertility of the Brazilian Cerrado and hyperaccumulates aluminum in cell walls and chloroplasts. Plant Soil 408:369–384CrossRefGoogle Scholar
  25. Morita A, Horie H, Fujii Y, Takatsu S, Watanabe N, Yagi A, Yokota H (2004) Chemical forms of aluminum in xylem sap of tea plants (Camellia sinensis L.). Phytochem 65:2775–2780CrossRefGoogle Scholar
  26. Oliveira Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil. Columbia University Press, New York, pp 91–120CrossRefGoogle Scholar
  27. Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado vegetation and threats to its biodiversity. Ann Bot 80:223–230CrossRefGoogle Scholar
  28. Ratter JA, Bridgewater S, Ribeiro JF (2003) Analysis of the floristic composition of the Brazilian cerrado vegetation III: comparison of the woody vegetation of 376 areas. Edinb J Bot 60:57–109CrossRefGoogle Scholar
  29. Ribeiro JF, Walter BMT (2008) As principais fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF. Ecologia e flora. Empresa Brasileira de Pesquisa Agropecuária (Embrapa): Brasília, 1, 152–212Google Scholar
  30. Sarruge JR, Haag HP (1974) Análises Químicas em plantas. Escola Superior de Agricultura Luiz de Queiróz, PiracicabaGoogle Scholar
  31. Souza MC, Bueno PCP, Morellato LPC, Habermann G (2015) Ecological strategies of Al-accumulating and non-accumulating functional groups from the Cerrado sensu stricto. An Acad Bras Ciênc 87:813–823CrossRefGoogle Scholar
  32. Taiz L, Zeiger E, Moller IM, Murphy A (2017) Mineral nutrition. In:___. (Org.). Plant Physiology and development. Sinauer Associates, Sunderland, pp 119–142Google Scholar
  33. van Raij B, Andrade JC, Cantarella H, Quaggio JA (2001) Análise química para avaliação da fertilidade de solos tropicais. Instituto Agronômico de Campinas (IAC), CampinasGoogle Scholar
  34. Villela DM, Haridasan M (1994) Response of the ground layer community of a Cerrado vegetation in Central Brazil to liming and irrigation. Plant Soil 163:25–31CrossRefGoogle Scholar
  35. Wehr JB, Blamey FPC, Hanna JV, Kopittke PM, Kerven GL, Menzies NW (2010) Hydrolysis and speciation of Al bound to pectin andplant cell wall material and its reaction with the dye chrome azurol S. J Agric Food Chem 58:5553–5560CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biologia Vegetal, Instituto de Biociências, Departamento de BotânicaUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  2. 2.Laboratório de Botânica e Ecologia no Domínio Cerrado (LABEC)Universidade Federal de Uberlandia (UFU)ItuiutabaBrazil
  3. 3.Instituto de Biociências, Departamento de BotânicaUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil

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