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Characterization of biomass sorghum for copper phytoremediation: photosynthetic response and possibility as a bioenergy feedstock from contaminated land

  • Letícia Rigonato Lima
  • Higor Ferreira Silva
  • Alcindo Souza Brignoni
  • Fabiano Guimarães Silva
  • Liliane Santos Camargos
  • Lucas Anjos SouzaEmail author
Research Article

Abstract

In order to decrease the concentration of toxic metals in contaminated lands, phytoextraction can be suitable considering the use of plant species with high potential for biomass production, such as biomass sorghum (Sorghum bicolor L.). We assessed a biomass sorghum (BRS716) potential as a copper phytoextractor as well as the physiological stability under this stressful condition. A completely randomized experimental design was used for a greenhouse experiment in which sorghum plants were submitted to a range of Cu2+ concentrations: 2.3, 10.9, 19.6, 30.5, 37.6 and 55.6 mg dm−3. The plant growth was not affected by increasing Cu2+ concentrations, suggesting that this species is tolerant to copper. There was a decrease in photosynthetic rate according to the increase in Cu2+ concentration, but not at a level that could disturb plant metabolism and eventual death. The values obtained for transfer index ranged from 0.62 to 0.11 which evidenced the restriction of Cu2+ transport to the aerial parts. The more Cu2+ available in soil, the smaller the amount of Cu2+ transported to aerial parts of sorghum. So, our results show that biomass sorghum has potential to be used for Cu2+ phytoextraction in concentration of up to 20 mg dm−3. Also, in heavily Cu2+ polluted sites, it can be used to produce biomass for bioenergy purpose, promoting a low rate of Cu2+ extraction.

Keywords

Bioenergy Environmental protection Toxic metals Plant production Clean technology Photosynthesis 

Notes

Acknowledgements

The authors acknowledge: Dr. Rafael Augusto Costa Parrella to kindly give biomass sorghum BRS-716 seeds; FAPESP for the following Grant (2015/09567-9); IF Goiano, FEIS-UNESP, FAPEG, CNPq and CAPES for general fundings to institutions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Andreazza R, Bortolon L, Pieniz S, Giacometti M, Roehrs DD, Lambais MR, Camargo FO (2011) Potential phytoextraction and phytostabilization of perennial peanut on copper-contaminated vineyard soils and copper mining waste. Biol Trace Elem Res 143:1729–1739CrossRefGoogle Scholar
  2. Antoniadis V, Golia EE, Shaheen SM, Rinklebe J (2017) Bioavailability and health risk assessment of potentially toxic elements in Thriasio Plain, near Athens, Greece. Environ Geochem Health 39:319–330CrossRefGoogle Scholar
  3. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190CrossRefGoogle Scholar
  4. Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Parque J, Makino T, Kirkham MB, ScheckeL K (2014) Remediation of heavy metal(loid)s contaminated soils—to mobilize or to immobilize? J Hazard Mater 266:141–166CrossRefGoogle Scholar
  5. Bonfranceschi AB, Flocco CG, Donati ER (2009) Study of the heavy metal phytoextraction capacity of two forage species growing in an hydroponic environment. J Hazard Mater 165:366–371CrossRefGoogle Scholar
  6. Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In: Maschner P (ed) Marschner’s mineral nutrition of higher plants, 4th ed. Academic PressGoogle Scholar
  7. Carvalho MEA, Piotto FA, Nogueira ML, Gomes-junior FG, Maria H, Pescarin C, Pizzaia D, Azevedo RA (2018) Cadmium exposure triggers genotype-dependent changes in seed vigor and germination of tomato offspring. Protoplasma 255:989–999CrossRefGoogle Scholar
  8. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97:13430–13435CrossRefGoogle Scholar
  9. Evangelou MWH, Conesa HM, Robinson BH, Schulin R (2012) Biomass production on trace element-contaminated land: a review. Environ Eng Sci 29:823–839CrossRefGoogle Scholar
  10. Evangelou MWH, Papazoglou EG, Robinson BH, Schulin R (2015) Phytomanagement: phytoremediation and the production of biomass for economic revenue on contaminated land. In: Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (eds) Phytoremediation: management of environmental contaminants. Springer, Switzerland, pp 115–132Google Scholar
  11. Fässler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58CrossRefGoogle Scholar
  12. Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cien Agrotec 35:1039–1042CrossRefGoogle Scholar
  13. Gomez-Sagasti MT, Epelde L, Alkorta I, Garbisu C (2016) Reflections on soil contamination research from a biologist point of view. Appl Soil Ecol 105:207–210CrossRefGoogle Scholar
  14. González-Mendoza D, Espadas y Gil F, Escoboza-Garcia F, Santamaría JM, Zapata-Perez O (2013) Copper stress on photosynthesis of black mangle (Avicennia germinans). An Acad Bras Cienc 85:665–670CrossRefGoogle Scholar
  15. Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochim Biophys Acta Mol Cell Res 1763:595–608CrossRefGoogle Scholar
  16. Jia W, Lv S, Feng J, Li J, Li Y, Li S (2016) Morphophysiological characteristic analysis demonstrated the potential of sweet sorghum (Sorghum bicolor (L.) Moench) in the phytoremediation of cadmium-contaminated soils. Environ Sci Pollut Res 23:18823–18831CrossRefGoogle Scholar
  17. Jia W, Miao F, Lv S, Feng J, Zhou S, Zhang X, Wang D, Li S, Li Y (2017) Identification for the capability of Cd-tolerance, accumulation and translocation of 96 sorghum genotypes. Ecotoxicol Environ Saf 145:391–397CrossRefGoogle Scholar
  18. Kabata-Pendias A (2004) Soil-plant transfer of trace elements—an environmental issue. Geoderma 122:143–149CrossRefGoogle Scholar
  19. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefGoogle Scholar
  20. Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272CrossRefGoogle Scholar
  21. Li C, Xiao B, Wang QH, Yao SH, Wu JY (2014) Phytoremediation of Zn- and Cr-contaminated soil using two promising energy grasses. Water Air Soil Pollut 225:2027–2039CrossRefGoogle Scholar
  22. Li Y, Wang Q, Wang L, He LY, Sheng XF (2016) Increased growth and root Cu accumulation of Sorghum sudanense by endophytic Enterobacter sp. K3-2: implications for Sorghum sudanense biomass production and phytostabilization. Ecotoxicol Environ Saf 124:163–168CrossRefGoogle Scholar
  23. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  24. Liu X, Shen Y, Lou L, Ding C, Cai Q (2009) Copper tolerance of the biomass crops elephant grass (Pennisetum purpureum Schumach), vetiver grass (Vetiveria zizanioides) and the upland reed (Phragmites australis) in soil culture. Biotechnol Adv 27:633–640CrossRefGoogle Scholar
  25. Mehr MR, Keshavarzi B, Moore F, Sharifi R, Lahijanzadeh A, Kermani M (2017) Distribution, source identification and health risk assessment of soil heavy metals in urban areas of Isfahan province, Iran. J Afr Earth Sci 132:16–26CrossRefGoogle Scholar
  26. Merchant S, Dreyfuss BW (1998) Posttranslational assembly of photosynthetic metalloproteins. Annu Rev Plant Physiol Plant Mol Biol 49:25–51CrossRefGoogle Scholar
  27. Nogueira TAR, Abreu-Junior CH, Alleoni LRF, He Z, Soares MR, Santos Vieira C, Lessa LGF, Capra GF (2018) Background concentrations and quality reference values for some potentially toxic elements in soils of São Paulo State, Brazil. J Environ Manag 221:10–19CrossRefGoogle Scholar
  28. Palma P, Ledo L, Alvarenga P (2015) Assessment of trace element pollution and its environmental risk to freshwater sediments influenced by anthropogenic contributions: the case study of Alqueva reservoir (Guadiana Basin). CATENA 128:174–184CrossRefGoogle Scholar
  29. Panda P, Sahoo L, Panda SK (2015) Heavy metal and metalloid stress in plants: the genomics perspective. In: Chakraborty U, Chakraborty B (eds) Abiotic stresses in crop plants. CABIGoogle Scholar
  30. Peñarrubia L, Romero P, Carrió-Seguí A, Andrés-Bordería A, Moreno J, Sanz A (2015) Temporal aspects of copper homeostasis and its crosstalk with hormones. Front Plant Sci 6:1–18CrossRefGoogle Scholar
  31. Rabêlo FHS, Borgo L, Lavres J (2018) The use of forage grasses for the phytoremediation of heavy metals: plant tolerance mechanisms, classifications, and new prospects. In: Matichenkov V (ed) Phytoremediation: methods, management and assessment. Nova Science Publishers, New York, pp 59–102Google Scholar
  32. Rahman MM, Azirun SM, Boyce AN (2013) Enhanced accumulation of copper and lead in Amaranth (Amaranthus paniculatus), Indian Mustard (Brassica juncea) and Sunflower (Helianthus annuus). PLoS ONE 8:e62941CrossRefGoogle Scholar
  33. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefGoogle Scholar
  34. Rodrigues Castro FM, Bruzi AT, Rodrigues Nunes JA, Costa Parrella RA, Romeiro Lombardi GM, Brant Albuquerque CJ, Lopes M (2015) Agronomic and energetic potential of biomass sorghum genotypes. Am J Plant Sci 6:1862–1873CrossRefGoogle Scholar
  35. Sauerbeck DR (1991) Plant element and soil properties governing uptake and availability of heavy metals derived from sewage sludge. Water Air Soil Pollut 57:227–237CrossRefGoogle Scholar
  36. Sharma P, Sirhindi G, Singh AK, Kaur H, Mushtaq R (2017) Consequences of copper treatment on pigeon pea photosynthesis, osmolytes and antioxidants defense. Physiol Mol Biol Plants 23:809–816CrossRefGoogle Scholar
  37. Sipos G, Solti A, Checo V, Vashegyi I, Tóth B, Cseh E, Fodor F (2013) Heavy metal accumulation and tolerance of energy grass (Elymus elongates subsp. Ponticus cv. Szarvasi -1) grown in hydroponic culture. Plant Physiol Biochem 68:96–103CrossRefGoogle Scholar
  38. Soudek P, Petrová Š, Vaňková R, Song J, Vaněk T (2014) Accumulation of heavy metals using Sorghum sp. Chemosphere 104:15–24CrossRefGoogle Scholar
  39. Souza LA, Monteiro CC, Carvalho RF, Gratão PL, Azevedo RA (2017) Dealing with abiotic stresses: an integrative view of how phytohormones control abiotic stress-induced oxidative stress. Theor Exp Plant Physiol 29:109–127CrossRefGoogle Scholar
  40. Souza LA, Camargos LS, Carvalho MEA (2018) Toxic metal phytoremediation using high biomass non-hyperaccumulator crops: new possibilities for bioenergy resources. In: Matichenkov V (ed) Phytoremediation: methods, management and assessment. Nova Science Publishers, New York, pp 1–26Google Scholar
  41. Stankovic S, Kalaba P, Stankovic AR (2014) Biota as toxic metal indicators. Environ Chem Lett 12:63–84CrossRefGoogle Scholar
  42. Subramani T, Florence HR, Kavitha M (2014) Climate change energy and decentralized solid waste management. Int J Eng Res Appl 4:205–216Google Scholar
  43. Thyberg KL, Tonjes DJ (2016) Drivers of food waste and their implications for sustainable policy development. Resour Conserv Recycl 106:110–123CrossRefGoogle Scholar
  44. Tian YL, Zhang HY, Guo C, Wei XF (2015) Morphological responses, biomass yield, and bioenergy potential of sweet sorghum cultivated in cadmium-contaminated soil for biofuel. Int J Green Energy 12:577–584CrossRefGoogle Scholar
  45. Toler HD, Morton JB, Cumming JR (2005) Growth and metal accumulation of mycorrhizal sorghum exposed to elevated copper and zinc. Water Air Soil Pollut 164:155–172CrossRefGoogle Scholar
  46. Vernay P, Gauthier-Moussard C, Hitmi A (2007) Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere 68:1563–1575CrossRefGoogle Scholar
  47. Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2019

Authors and Affiliations

  1. 1.Instituto Federal de EducaçãoCiência e Tecnologia Goiano – Campus Rio VerdeRio VerdeBrazil
  2. 2.Faculdade de Engenharia, Departamento de Biologia e Zootecnia, Laboratório de Fisiologia do Metabolismo VegetalUniversidade Estadual Paulista (UNESP)Ilha SolteiraBrazil
  3. 3.Instituto Federal de EducaçãoCiência e Tecnologia Goiano – Campus Rio Verde – Polo de Inovação em Bioenergia e GrãosRio VerdeBrazil

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