Abstract
Background
The highly diversified flora in the Brazilian Cerrado (savanna) region is attributed to several factors, including the high concentrations of metals in soils, especially Al in widespread Ferralsols and Ni in soils derived from ultramafic rocks. We hypothesized that adaptation mechanisms are responsible for the genetic diversity of the following native plant species that are found in the abovementioned environments: Euploca salicoides (ES), Justicia lanstyakii (JL), and Oxalis hirsutissima (OH).
Objectives
We aimed to analyse the main edaphic factors that differentiate ultramafic from Al-rich environments, and act as drivers of the evolution of physiological mechanisms underlying plant adaptation to these harsh environments.
Methods
We analysed the chemical attributes of four ultramafic soils (SAP5, SAP7, SAP9, LAT) and an Al-rich soil (CAM), and the elemental composition and DNA of the three species growing in both environments. ES was used as a model species to analyse changes in the levels of non-structural carbohydrates (NSCs) and Ni localization in plant leaves.
Results
The soil types presented significant differences in available nutrients and heavy metals. The DNA sampled from the same species from ultramafic sites was genetically closer, but different from that in the Al-rich sites. In ultramafic soils, ES accessions had high levels of NSCs and Ni accumulated in trichomes.
Conclusions
The genetic diversity observed in plants growing in both areas is probably related to plant adaptation to the contrasting edaphic conditions of these environments. The raffinose production and Ni allocation to trichomes are mechanisms employed by ES to overcome metal toxification in ultramafic environments.
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References
Alencar A, Shimbo JZ, Lenti F, Marques CB, Zimbres B, Rosa M, Arruda V, Castro I, Ribeiro JPFM, Varela V, Alencar I, Piontekowski V, Ribeiro V, Bustamante MMC, Sano EE, Barroso M (2020) Mapping three decades of changes in the Brazilian Savanna native vegetation using Landsat Data processed in the Google Earth Engine. Plataform Remote Sens 12:1–23. https://doi.org/10.3390/rs12060924
Andrade LRM, Barros LMG, Echevarria GF, Amaral LIV, Cotta MG, Rossato DR, Haridasan M, Franco AC (2011) Al-hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Environ Exper Bot 70:37–42. https://doi.org/10.1016/j.envexpbot.2010.05.013
Andrade LRM, Aquino FG, Reis FB Jr, Pachêco BS, Echevarria G (2015) Potencial de uso de espécies vegetais nativas dos complexos ultramáficos. Barro Alto (GO) nos processos de recuperação de áreas alteradas pela extração de Ni, de fitoextração e fitomineração de metais. Proceedins of the XXXV Congresso Brasileiro de Ciência do Solo: O solo e suas múltiplas funções. SBCS, Natal, RN, Brazil
Anglo A (2011) Anglo American inaugura oficialmente Unidade Barro Alto. https://brasil.angloamerican.com/pt-pt/imprensa/noticias/year2011/18-12-2011. Accessed 18 Dec 2021
Aquino FG, Viana RM, Miranda ZJG, Andrade LRM (2011) Floristic composition in the ultramafic soils in Central Brazil. Proceedings of the 7th International Conference on Serpentine Ecology, Coimbra, Portugal
Aziz H, Sabir M, Ahmad HR, Aziz T, Khalid MZ-u-R, Hakeem R, Ozturk M (2014) Alleviating effect of calcium on nickel toxicity in rice. CLEAN - Soil Air Water. https://doi.org/10.1002/clen.201400085
Baker DE, Amacher MC (1982) Nickel, Copper, Zinc, and Cadmium. In: Dinauer RC (ed) Methods of soil analysis - Part 2: Chemical and microbiological properties. 2nd edn. SSSA, Madison
Bothe H, Słomkab A (2017) Divergent biology of facultative heavy metal plants. J Plant Physiol 219:17. https://doi.org/10.1016/j.jplph.2017.08.014
Brown PH, Welch RM, Cary EE (1987) Nickel: A micronutrient essential for higher plants. Plant Physiol 85:801–803
Burak DL, Fontes MPF, Santos NT, Monteiro LVS, Martins EdS, Becquer T (2010) Geochemistry and spatial distribution of heavy metals in Oxisols in a mineralized region of the Brazilian Central Plateau. Geoderma 160(2):131–142. https://doi.org/10.1016/j.geoderma.2010.08.007
Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of hyperaccumulation. Planta 239:267–275. https://doi.org/10.1007/s00425-013-1983-0
Chang AC, Granato TC, Page AL (1992) A methodology for establishing phytotoxicity criteria for chromium, copper, nickel, and zinc in agricultural land application of municipal sewage sludges. J Environ Qual 21:521–534. https://doi.org/10.2134/jeq1992.00472425002100040001x
Costa G, Spitz E (1997) Influence of cadmium on soluble carbohydrates, free amino acids, protein content of in vitro cultured Lupinus albus Plant Sci 128:131–140. https://doi.org/10.1016/S0168-9452(97)00148-9
Cruz CD (2013) GENES - a software package for analysis in experimental statistics and quantitative genetics. Acta Sci Agron 35:271–276. https://doi.org/10.4025/actasciagron.v35i3.21251
Doria-Filho U (1999) Introdução à bioestatística - Para simples mortais, 17th edn. Elsevier, São Paulo
Drzewiecka K, Mleczek M, Gąsecka M, Magdziak Z, Budka A, Chadzinikolau T, Kaczmarek Z, Goliński P (2017) Copper and nickel co-treatment alters metal uptake and stress parameters of Salix purpurea × viminalis J Plant Physiol 216:125–134. https://doi.org/10.1016/j.jplph.2017.04.020
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Echevarria G (2018) Genesis and behavior of ultramafic soils and consequences for nickel biogeochemistry. In: Van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel J-L (eds) Agromining: farming for metals: extracting unconventional resources using plants, 2nd edn. Springer International Publishing, Cham
Embrapa – Empresa Brasileira de Pesquisa Agropecuária (1999) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Solos, Rio de Janeiro
Faleiro FG, Faleiro ASG, Cordeiro MCR, Karia CT (2003) Metodologia para operacionalizar a extração de DNA de espécies nativas do cerrado. In: Embrapa Cerrados (ed), Planaltina
Filgueiras TS (2002) Herbaceous plant communities. In: Oliveira PS, Marquis TJ (eds) The Cerrados of Brazil - Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, pp 121–139
Flora do Brasil (2020) Jardim Botânico do Rio de Janeiro. Disponível em: http://floradobrasil.jbrj.gov.br/. Acesso em: 12 Jan 2022
Freitas FG, Gomes IA, Ferreira RC, Antonello LL (1978) Levantamento de reconhecimento dos solos do Distrito Federal. In: Embrapa -SNLCS (ed) Boletim de Pesquisa no. 53. Embrapa-SNLCS, Rio de Janeiro
Gann G, Lamb D (2006) Ecological restoration: A mean of conserving biodiversity and sustaining livelihoods (version 1.1). Society for Ecological Restoration International, Tucson
Garnier J, Quantin C, Martins ES, Becquer T (2006) Solid speciation and availability of chromium in ultramafic soils from Niquelândia, Brazil. J Geochem Explor (88):206–209
Gomes JBV, Curi N, Motta PEF, Ker JC, Marques JJGSM, Schulze DG (2004) Análise de componentes principais de atributos físicos, químicos e mineralógicos de solos do bioma Cerrado. Rev Bras Ciênc Solo 28:137–153. https://doi.org/10.1590/S0100-06832004000100014
Goodland RJ, Pollard R (1973) The Brazilian Cerrado vegetation: a fertility gradient. J Ecol 61:219–224
Goolsby EW, Mason CM (2016) Response: Commentary: Toward a more physiologically and evolutionarily relevant definition of metal hyperaccumulation in plants. Front Plant Sci 6:1–4. https://doi.org/10.3389/fpls.2015.01252
Hair-Jr JF, Black WC, Babin BJ, Anderson RE, Tatham RL (2009) Análise Multivariada de Dados (Multivariate Data Analysis), 6th edn. Bookman, Porto Alegre
Hartmann H, Trumbore S (2016) Understanding the roles of non-structural carbohydrates in forest trees – from what we can measure to what we want to know. [Review] New Phytol 211:386–403. https://doi.org/10.1111/nph.13955
Haridasan M (1982) Aluminum accumulation by some Cerrado native species of central Brazil. Plant Soil 65:265–273
Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot Rev 68:235–269
Jha AB, Dubey RS (2004) Carbohydrate metabolism in growing rice seedlings under arsenic toxicity. J Plant Physiol 161:867–872. https://doi.org/10.1016/j.jplph.2004.01.004
Kabata-Pendias A, Mukherjee AB (2007) Trace elements of Group 10 (Previously part of Group VIII). In: Kabata-Pendias A, Mukherjee AB (eds) Trace elements from soil to human. Springer, New York
Khan AA, McNeilly T, Collins JC (2000) Accumulation of amino acids, proline, and carbohydrates in response to aluminum and manganese stress in maize. J Plant Nutr 23(9):1303–1314. https://doi.org/10.1080/01904160009382101
Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508. https://doi.org/10.1111/j.1469-185X.2008.00051
Kierczak J, Pietranik A, Pędziwiatr A (2021) Ultramafic geoecosystems as a natural source of Ni, Cr, and Co to the environment: A review. Sci Tot Environ 755:1–18. https://doi.org/10.1016/j.scitotenv.2020.142620
Kinraide TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118:513–520. https://doi.org/10.1104/pp.118.2.513
Kruckeberg AR (2002) Geology and plant life: The effects of landforms and rock types on plants. University of Washington Press, Seattle
Lima TM (2010) Síntese geológica e prospecção geoquímica da área Barro Alto, Goiás, vol 30. Metais do Grupo da Platina e Associados. CPRM, Goiânia
Lopez S, Benizri E, Erskine PD, Cazes Y, Morel JL, Lee G, Permana E, Echevarria G, van der Ent A (2019) Biogeochemistry of the flora of Weda Bay, Halmahera Island (Indonesia) focusing on nickel hyperaccumulation. J Geochem Explor 202:113–127
Marques JJ, Schulze DG, Curi N, Mertzman SA (2004) Trace element geochemistry in Brazilian Cerrado soils. Geoderma 121:31–43
Martins ES, Becquer T, Brossard M (2010) Síntese de dados geoquímicos da região do Planalto Central – 1. Ocorrência de rochas ultramáficas na região de Cerrado contínuo e sua importância ecológica. In: LRM Andrade (ed) 2o. Workshop do Projeto 02.07.01.007.00.00: “Relações entre metais do solo e a biodiversidade no Cerrado: ferramentas para a conservação ambiental e a recuperação de áreas degradadas", Embrapa Cerrados, Planaltina
McKay JK, Christian CE, Harrison S, Rice KJ (2005) “How local is local?” - A review of practical and conceptual issues in the genetics of restoration. Rest Ecol 13:432–440. https://doi.org/10.1111/j.1526-100X.2005.00058.x
McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale Environ Sci Technol 39:2210–2218
Mendonça RC, Felfili JM, Walter BMT, Silva-Júnior MC, Rezende AV, Filgueiras TS, Nogueira PE, Fagg CW (2008) Flora vascular do Cerrado: checklist com 12.356 espécies. In: Sano SM, Almeida SPd, Ribeiro JF (eds) Cerrado: ecologia e flora, vol 2, 1st edn. Embrapa Cerrados/Embrapa Informação Tecnológica, pp 423–442
Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Calcium. In: Mengel K, Kirkby EA, Kosegarten H, Appel T (eds) Principles of Plant Nutrition. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-1009-2_11
Moreira MLO, Moreton LC, Araújo VA, Lacerda Filho JV, Costa HF (2008) Geologia do estado de Goiás e Distrito Federal: Texto explicativo do mapa geológico de Goiás e Distrito Federal. Programa Geologia do Brasil, Escala 1:500.000. CPRM, Goiânia, GO
Myers N, Mittermeier R, Mittermeier C, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Nat Ac Sci USA 76:5269–5273. https://doi.org/10.1073/pnas.76.10.5269
O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014) Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat - Clim Change 4:710–714. https://doi.org/10.1038/NCLIMATE2281
Oliveira AP, Dusi DMA, Walter BMT, Gomes ACMM, Noronha SE, Braga MB, Coelho CM, Barros LMG (2019) Avaliação de espécies do Cerrado quanto à tolerância ao alumínio. Embrapa Recursos Genéticos e Biotecnologia, Brasilia
Paul ALD, Harris HH, Erskine PD, Przybyłowicz W, Mesjasz-Przybyłowicz J, Echevarria G, van der Ent A (2020) Synchrotron µXRF imaging of live seedlings of Berkheya coddii and Odontarrhena muralis during germination and seedling growth. Plant Soil 453:487–501
Pereira MdF, Valva FD, Coelho ASG, Aguiar AV, Zucchi MI (2004) Estrutura genética de populações de espécies arbóreas nativas do cerrado encontradas em terrenos serpentínicos. Pesq Agropec Trop 34:75–82
Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217– 218:8–17. https://doi.org/10.1016/j.plantsci.2013.11.011
Psaras GK, Manetas Y (2001) Nickel localization in seeds of the metal hyperaccumulator Thlaspi pindicum Hasusskn. Ann Bot 88:513–516. https://doi.org/10.1006/anbo.2001.1470
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 24 Aug 2021
Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado vegetation and threats to its biodiversity. Ann Bot 80:223–230. https://doi.org/10.1006/anbo.1997.0469
Reeves RD, Aloupi M, Daftsis EI, Stratis JA, Mastoras P, Dimitrakopoulos PG (2022) Biogeochemical aspects of the serpentines of Rhodes (Greece) and Cyprus. Plant Soil 472:491–508. https://doi.org/10.1007/s11104-021-05265-5
Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293:107–119. https://doi.org/10.1007/s11104-007-9192-x
Reeves RD, van der Ent A, Echevarria G, Isnard S, Baker AJM (2021) Global distribution and ecology of hyperaccumulator plants. In: Van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel J-L (eds) Agromining: farming for metals: extracting unconventional resources using plants, 2nd edn. Springer International Publishing, Cham
Ribeiro JF, Walter BMT (2008) As principais fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SPd, Ribeiro JF (eds) Cerrado: ecologia e flora, vol 1, 1st edn. Embrapa Cerrados/Embrapa Informação Tecnológica, Brasília, pp 152–212
Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii New Phytol 158:279–285. https://doi.org/10.1046/j.1469-8137.2003.00743.x
Sambroock J, Fritsch EF, Maniats T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York
SAS Institute Inc (2008) SAS user’s guide: statistic: version 9.1.3., Cary, NC, USA
Seregin IV, Kozhevnikova D (2006) Physiological role of nickel and its toxic effects on higher plants. Russian J Plant Physiol 53(2):257–277
Shahzad B, Tanveer M, Rehman A, Cheema SA, Fahad S, Rehman S, Sharma A (2018) Nickel; whether toxic or essential for plants and environment - A review. Plant Physiol Biochem 132:641–651. https://doi.org/10.1016/j.plaphy.2018.10.014
Shannon JC (1968) A procedure for extraction and fractionation of carbohydrates from immature Zea mays kernels. Ind Agr Exp Sta Res Bull 842:1–8
Silva FAM, Assad ED, Evangelista BA (2008) Caracterização climática do bioma Cerrado. In: Sano SM, Almeida SPd, Ribeiro JF (eds) Cerrado: ecologia e flora, vol 1, 1st edn. Embrapa Cerrados/Embrapa Informação Tecnológica, Brasília, pp 71–88
Sneath PEA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco
Sondaterra Equipamentos Agronômicos (n.d.) Manual de Instruções - Trado Tipo Holandês Modelos: TF-10/TP, -3/TP-4/TU-5. Available at http://www.sondaterra.com/upload/banco_imagens/files/holand.pdf. Accessed 2 Jun 2022
StatSoft Inc (2007) Statistica for Windows (data analysis software system), version 7.1. StatSoft, Tulsa
van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CW, Meech JA, Mulligan DR, Erskine PD, Simonnot M-O, Vaughan J, Morel J-L, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780. https://doi.org/10.1021/es506031u
van der Ent A, Spyers K, Brueckner D, Echevarria G, Aarts MGM, Montargès-Pelletier E (2019) Spatially-resolved localization and chemical speciation of nickel and zinc in Noccaea tymphaea and Bornmuellera emarginata Metallomics 11:2052–2065
Vidal-Torrado P, Macias F, Calvo R, Carvalho SGd, Silva AC (2006) Gênese de solos derivados de rochas ultramáficas serpentinizadas no sudoeste de Minas Gerais. R Bras Ci Solo 30:523–541. https://doi.org/10.1590/S0100-06832006000300013
Acknowledgements
The authors acknowledge the staff from the Embrapa Cerrados laboratories for their assistance in conducting chemical, physical, and biological analyses. We are grateful to Anglo American do Brasil for the financial, logistical, and technical support in Barro Alto-GO. We also thank the Eliseu Alves Foundation and its staff for the administrative and technical support and the Brazilian Institute for Environment and Renewable Natural Resources (IBAMA) for the authorizations granted to perform this study (Process n° 02001.001558/2006-21). We are very thankful for the constructive comments from Thomas Adolpho Rein and from two anonymous reviewers, which greatly improved this manuscript.
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This research was partially supported by Anglo American and Embrapa.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Leide Rovênia Miranda de Andrade, Guillaume Echevarria, Jamile S. Oliveira, Cícero D. Pereira, Karina S. Souza, Emmanuelle Montargès-Pelletier, Juaci V. Malaquias, Edson E. Sano, Fabiana G. Aquino, Fábio G. Faleiro, Fábio B. Reis Junior, Zenilton G. Miranda, Lourdes Velho do Amaral†. The first draft of the manuscript was written by Leide Rovênia Miranda de Andrade and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Andrade, L.R.M., Aquino, F.G., Echevarria, G. et al. Edaphic factors as genetic selection agents and adaptation drivers of native plant species in harsh environments of the Brazilian savanna. Plant Soil 479, 301–323 (2022). https://doi.org/10.1007/s11104-022-05520-3
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DOI: https://doi.org/10.1007/s11104-022-05520-3