Effects of CO2 application and endophytic bacterial inoculation on morphological properties, photosynthetic characteristics and cadmium uptake of two ecotypes of Sedum alfredii Hance

Abstract

Plant uptake of cadmium (Cd) is affected by soil and environmental conditions. In this study, hydroponic experiments were conducted to investigate the effects of elevated CO2 coupled with inoculated endophytic bacteria M002 on morphological properties, gas exchange, photosynthetic pigments, chlorophyll fluorescence, and Cd uptake of S. alfredii. The results showed that bio-fortification processes (elevated CO2 and/or inoculated with endophytic bacteria) significantly (p < 0.05) promoted growth patterns, improved photosynthetic characteristics and increased Cd tolerance of both ecotypes of S. alfredii, as compared to normal conditions. Net photosynthetic rate (Pn) in intact leaves of hyperaccumulating ecotype (HE) and non-hyperaccumulating ecotype (NHE) were increased by 73.93 and 32.90%, respectively at the low Cd (2 μM), 84.41 and 57.65%, respectively at the high Cd level (10 μM). Superposition treatment increased Cd concentration in shoots and roots of HE, by 50.87 and 82.12%, respectively at the low Cd and 46.75 and 88.92%, respectively at the high Cd level. Besides, superposition treatment declined Cd transfer factor of NHE, by 0.85% at non-Cd rate, 17.22% at the low Cd and 22.26% at the high Cd level. These results indicate that elevated CO2 coupled with endophytic bacterial inoculation may effectively improve phytoremediation efficiency of Cd-contaminated soils by hyperaccumulator, and alleviate Cd toxicity to non-hyperaccumulator ecotype of Sedum alfredii.

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References

  1. Afzal M, Khan QM, Sessitsch A (2014) Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117:232–242

    Article  CAS  Google Scholar 

  2. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  CAS  Google Scholar 

  3. Ashraf S, Afzal M, Rehman K, Naveed M, Zahir ZA (2018) Plant-endophyte synergism in constructed wetlands enhances the remediation of tannery effluent. Water Sci Techn 77:1262–1270

    Article  CAS  Google Scholar 

  4. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  Google Scholar 

  5. Barton CVM, Duursma RA, Medlyn BE, Ellsworth DS, Eamus D, Tissue DT, Adams MA, Conroy J, Crous KY, Liberloo M (2012) Effects of elevated atmospheric [CO2] on instantaneous transpiration efficiency at leaf and canopy scales in Eucalyptus saligna. Glob Change Biol 18:585–595

    Article  Google Scholar 

  6. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

  7. Bernacchi CJ, Morgan PB, Ort DR, Long SP (2005) The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434–446

    Article  CAS  Google Scholar 

  8. Cao L, Bala G, Caldeira K, Nemani R, Ban-Weiss G (2009) Climate response to physiological forcing of carbon dioxide simulated by the coupled community atmosphere model (CAM3.1) and community land model (CLM3.0). Geophys Res Lett 36:L10402

    Article  Google Scholar 

  9. Chen B, Shen JG, Zhang XC, Pan FS, Yang XE, Feng Y (2014a) The Endophytic bacterium, Sphingomonas SaMR12, improves the potential for zinc phytoremediation by its host, Sedum alfredii. PLoS One 9:e106826

    Article  CAS  Google Scholar 

  10. Chen B, Zhang YB, Rafiq MT, Khan KY, Pan FS, Yang XE, Feng Y (2014b) Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: effects on plant growth and root exudates. Chemosphere 117:367–373

    Article  CAS  Google Scholar 

  11. Croonenborghs S, Ceusters J, Londers E, De Proft MP (2009) Effects of elevated CO2 on growth and morphological characteristics of ornamental bromeliads. Sci Hortic 121:192–198

    Article  CAS  Google Scholar 

  12. Donohue RJ, Roderick ML, McVicar TR, Yang YT (2017) A simple hypothesis of how leaf and canopy-level transpiration and assimilation respond to elevated CO2 reveals distinct response patterns between disturbed and undisturbed vegetation. J Geophys Res-Biogeo 122:168–184

    Article  CAS  Google Scholar 

  13. Drennan PM, Nobel PS (2000) Responses of CAM species to increasing atmospheric CO2 concentrations. Plant Cell Environ 23:767–781

    Article  CAS  Google Scholar 

  14. Ehsan M, Lara Viveros FM, Hernández VE, Barakat MA, Ortega AR, Maza AV, Monter JV (2015) Zinc and cadmium accumulation by Lupinus uncinatus Schldl. grown in nutrient solution. Int J Environ Sci Technol 12:307–316

    Article  CAS  Google Scholar 

  15. Guo BH, Dai SX, Wang RG, Guo JK, Ding YZ, Xu YM (2015) Combined effects of elevated CO2 and Cd-contaminated soil on the growth, gas exchange, antioxidant defense, and Cd accumulation of poplars and willows. Environ Exp Bot 115:1–10

    Article  CAS  Google Scholar 

  16. Haldimann P, Strasser RJ (1999) Effects of anaerobiosis as probed by the polyphasic chlorophyll a fluorescence rise kinetic in pea (Pisum sativum L.). Photosynth Res 62:67–83

    Article  CAS  Google Scholar 

  17. Hamid Y, Tang L, Yaseen M, Hussain B, Zehra A, Aziz MZ, He ZL, Yang XE (2019) Comparative efficacy of organic and inorganic amendments for cadmium and lead immobilization in contaminated soil under rice - wheat cropping system. Chemosphere 214:259–268

    Article  CAS  Google Scholar 

  18. Houshmandfar A, Fitzgerald GJ, Tausz M (2015) Elevated CO2 decreases both transpiration flow and concentrations of Ca and Mg in the xylem sap of wheat. J Plant Physiol 174:157–160

    Article  CAS  Google Scholar 

  19. Hussain Z, Arslan M, Malik MH, Mohsin M, Iqbal S, Afzal M (2018) Integrated perspectives on the use of bacterial endophytes in horizontal flow constructed wetlands for the treatment of liquid textile effluent: phytoremediation advances in the field. J Environ Manag 224:387–395

    Article  CAS  Google Scholar 

  20. IPCC (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York

    Google Scholar 

  21. Jaffrin A, Bentounes N, Joan AM, Makhlouf S (2003) Landfill biogas for heating greenhouses and providing carbon dioxide supplement for plant growth. Biosyst Eng 86:113–123

    Article  Google Scholar 

  22. Jia Y, Tang SR, Wang RG, Ju XH, Ding YZ, Tu SX, Smith DL (2010) Effects of elevated CO2 on growth, photosynthesis, elemental composition, antioxidant level, and phytochelatin concentration in Lolium mutiforum and Lolium perenne under cd stress. J Hazard Mater 180:384–394

    Article  CAS  Google Scholar 

  23. Jing YX, Yan JL, He HD, Yang DJ, Xiao L, Zhong T, Yuan M, Cai XD, Li SB (2014) Characterization of bacteria in the rhizosphere soils of Polygonum pubescens and their potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Int J Phytoremed 16:321–333

    Article  CAS  Google Scholar 

  24. Khan MU, Sessitsch A, Harris M, Fatima K, Imran A, Arslan M, Shabir G, Khan QM, Afzal M (2015) Cr-resistant rhizo- and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils. Front Plant Sci 5:755

    Article  Google Scholar 

  25. Kolbas A, Kidd P, Guinberteau J, Jaunatre R, Herzig R, Mench M (2015) Endophytic bacteria take the challenge to improve cu phytoextraction by sunflower. Environ Sci Pollut Res 22:5370–5382

    Article  CAS  Google Scholar 

  26. Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304:35–44

    Article  CAS  Google Scholar 

  27. Küpper H, Parameswaran A, Leitenmaier B, Trtilek M, Setlik I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674

    Article  Google Scholar 

  28. Li TQ, Di ZZ, Han X, Yang XE (2012) Elevated CO2 improves root growth and cadmium accumulation in the hyperaccumulator Sedum alfredii. Plant Soil 354:325–334

    Article  CAS  Google Scholar 

  29. Li TQ, Tao Q, Han X, Yang XE (2013) Effects of elevated CO2 on rhizosphere characteristics of Cd/Zn hyperaccumulator Sedum alfredii. Sci Total Environ 454:510–516

    Article  CAS  Google Scholar 

  30. Li TQ, Tao Q, Di ZZ, Lu F, Yang XE (2015) Effect of elevated CO2 concentration on photosynthetic characteristics of hyperaccumulator Sedum alfredii under cadmium stress. J Integr Plant Biol 57:653–660

    Article  CAS  Google Scholar 

  31. Liu L, Hu L, Tang J, Li Y, Zhang Q, Chen X (2012) Food safety assessment of planting patterns of four vegetable-type crops grown in soil contaminated by electronic waste activities. J Environ Manag 93:22–30

    Article  CAS  Google Scholar 

  32. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    Article  CAS  Google Scholar 

  33. Long XX, Chen XM, Chen YG, Woon-Chung WJ, Wei ZB, Wu QT (2011) Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World J Microbiol Biotechnol 27:1197–1207

    Article  CAS  Google Scholar 

  34. Luo S, Chen L, Chen J, Xiao X, Xu T, Wan Y, Rao C, Liu C, Liu Y, Lai C, Zeng G (2011) Analysis and characterization of cultivable heavy metal resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138

    Article  CAS  Google Scholar 

  35. Pan FS, Meng Q, Luo S, Shen J, Chen B, Khan KY, Japenga J, Ma XX, Yang XE, Feng Y (2017) Enhanced Cd extraction of oilseed rape (Brassica napus) by plant growth-promoting bacteria isolated from cd hyperaccumulator Sedum alfredii Hance. Int J Phytoremed 19:281–289

    Article  CAS  Google Scholar 

  36. Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex steudel. Plant Physiol 133:829–837

    Article  CAS  Google Scholar 

  37. Redondo-Gómez S, Mateos-Naranjo E, Andrades-Moreno L (2010) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. J Hazard Mater 184:299–307

    Article  CAS  Google Scholar 

  38. Rehman K, Imran A, Amin I, Afzal M (2018) Inoculation with bacteria in floating treatment wetlands positively modulates the phytoremediation of oil field wastewater. J Hazard Mater 349:242–251

    Article  CAS  Google Scholar 

  39. Singh SK, Reddy VR, Fleisher DH, Timlin DJ (2017) Relationship between photosynthetic pigments and chlorophyll fluorescence in soybean under varying phosphorus nutrition at ambient and elevated CO2. Photosynthetica 55:421–433

    Article  CAS  Google Scholar 

  40. Solti A, Gaspar L, Meszaros I, Szigeti Z, Levai L, Sarvari E (2008) Impact of iron supply on the kinetics of recovery of photosynthesis in Cd-stressed poplar (Populus glauca). Ann Bot 102:771–782

    Article  CAS  Google Scholar 

  41. Song NN, Ma YB, Zhao YJ, Tang SR (2015) Elevated ambient carbon dioxide and Trichoderma inoculum could enhance cadmium uptake of Lolium perenne explained by changes of soil pH, cadmium availability and microbial biomass. Appl Soil Ecol 85:56–64

    Article  Google Scholar 

  42. Tang L, Luo WJ, Tian SK, He ZL, Stoffella PJ, Yang XE (2016) Genotypic differences in cadmium and nitrate co-accumulation among the Chinese cabbage genotypes under field conditions. Sci Hortic 201:92–100

    Article  CAS  Google Scholar 

  43. Tang L, Luo WJ, Chen WK, He ZL, Gurajala HK, Hamid Y, Deng MH, Yang XE (2017) Field crops (Ipomoea aquatica Forsk. and Brassica chinensis L.) for phytoremediation of cadmium and nitrate co-contaminated soils via rotation with Sedum alfredii Hance. Environ Sci Pollut Res 24:19293–19305

    Article  CAS  Google Scholar 

  44. Tang L, Luo WJ, He ZL, Gurajala HK, Hamid Y, Khan KY, Yang XE (2018) Variations in cadmium and nitrate co-accumulation among water spinach genotypes and implications for screening safe genotypes for human consumption. J Zhejiang Univ-Sci B (Biomed & Biotechnol) 19:147–158

    Article  CAS  Google Scholar 

  45. Tao Q, Hou DD, Yang XE, Li TQ (2016) Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant Soil 398:139–152

    Article  CAS  Google Scholar 

  46. Wu HB, Tang SR, Zhang XM, Guo JK, Song ZG, Tian SA, Smith DL (2009) Using elevated CO2 to increase the biomass of a Sorghum vulgare × Sorghum vulgare var. sudanense hybrid and Trifolium pratense L. and to trigger hyperaccumulation of cesium. J Hazard Mater 170:861–870

    Article  CAS  Google Scholar 

  47. Xia C, Li NN, Zhang XX, Feng Y, Christensen MJ, Nan ZB (2016) An Epichloe endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol 22:26–34

    Article  Google Scholar 

  48. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  49. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189

    Article  CAS  Google Scholar 

  50. Zheng JM, Wang HY, Li ZQ, Tang SR, Chen ZY (2008) Using elevated carbon dioxide to enhance copper accumulation in Pteridium revolutum, a copper-tolerant plant, under experimental conditions. Int J Phytoremed 10:161–172

    Article  CAS  Google Scholar 

  51. Zhou WB, Qiu BS (2005) Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745

    Article  CAS  Google Scholar 

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Funding

This study was financially supported by the Key Projects from Ministry of Science and Technology of China (#2016YFD0800805), Zhejiang Provincial Science and Technology Bureau (#2015C02011-3; #2015C03020-2), Fundamental Research Funds for the Central Universities, and the Funding from Ministry of Education Key Laboratory of Environmental Remediation and Ecosystem Health.

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Correspondence to Xiaoe Yang.

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Responsible editor: Yi-ping Chen

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Tang, L., Hamid, Y., Gurajala, H.K. et al. Effects of CO2 application and endophytic bacterial inoculation on morphological properties, photosynthetic characteristics and cadmium uptake of two ecotypes of Sedum alfredii Hance. Environ Sci Pollut Res 26, 1809–1820 (2019). https://doi.org/10.1007/s11356-018-3680-9

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Keywords

  • Cadmium uptake
  • Elevated CO2
  • Endophyte
  • Photosynthesis
  • Sedum alfredii