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Exogenous ethylene enhanced the cadmium resistance and changed the alkaloid biosynthesis in Catharanthus roseus seedlings

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Abstract

Cadmium (Cd) is not an essential nutrition element to plants and high concentration of Cd in the environment causes severe damage to plants. It is reported that the gas phytohormone ethylene plays important roles in plant responses to Cd stress. However, whether plant secondary metabolism is involved in this process remains to be investigated. Here, the regulations of exogenous ethylene on internal Cd accumulation and terpenoid indole alkaloids (TIAs) biosynthesis in the medicinal plant Catharanthus roseus (L.) G. Don (C. roseus) under Cd stress condition were explored. Our results showed that Cd treatment inhibited biomass accumulation, increased Cd accumulation and H2O2 and malondialdehyde (MDA) productions. Simultaneously, Cd treatment enhanced yields of vindoline, catharanthine and vinblastine, as well as the gene expressions of TIAs pathway enzymes at transcriptional level. Exogenous ethylene application significantly reduced the Cd content in whole plants and the H2O2 and MDA productions in roots and leaves, indicating that Cd stress in C. roseus was effectively alleviated by the ethylene application. It was interesting to find that exogenous ethylene promoted the Cd transport from roots to leaves and the value of Cd TF (transfer factor) was increased from 0.41 to 0.53. In leaves, the transcriptional expression of metallothionein (MT) was up-regulated by exogenous ethylene application, together with the increase of Cd accumulation. Additionally, exogenous ethylene reduced the TIAs productions, with an exception of catharanthine in leaves. The transcriptional expressions of alkaloid transporters, triose phosphate translocator (MDR) and multidrug resistance (TPT) were also up-regulated in leaves by exogenous ethylene, in accordance with the change of catharanthine biosynthesis. All of our results showed that exogenous ethylene could elevate the Cd resistance of C. roseus and effectively influence TIAs biosynthesis in C. roseus. Regulations of ethylene on the transcriptional expressions of MT, pathway enzymes and alkaloid transporters might be involved in this process.

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References

  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol 90(1):109–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arraes FBM, Beneventi MA, Lisei de Sa ME, Paixao JF, Albuquerque EV, Marin SR, Purgatto E, Nepomuceno AL, Grossi-de-Sa MF (2015) Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance. BMC Plant Biol 15(1):213–233

    Article  PubMed  PubMed Central  Google Scholar 

  • Arteca RN, Arteca JM (2007) Heavy-metal-induced ethylene production in Arabidopsis thaliana. J Plant Physiol 164(11):1480–1488

    Article  CAS  PubMed  Google Scholar 

  • Asgher M, Khan NA, Khan MI, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  PubMed  Google Scholar 

  • Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252(2):399–413

    Article  CAS  PubMed  Google Scholar 

  • Bahieldin A, Atef A, Edris S, Gadalla NO, Ali HM, Hassan SM, Al-Kordy MA, Ramadan AM, Makki RM, Al-Hajar ASM, El-Domyati FM (2016) Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC Plant Biol 16(1):216–225

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao F, Chen F, Sun H, Zhang G, Chen ZH, Wu F (2014) Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genom 15(1):611–625

    Article  Google Scholar 

  • Carrio-Segui A, Garcia-Molina A, Sanz A, Penarrubia L (2015) Defective copper transport in the copt5 mutant affects cadmium tolerance. Plant Cell Physiol 56(3):442–454

    Article  CAS  PubMed  Google Scholar 

  • Chmielowska-Bąk J, Lefèvre I, Lutts S, Deckert J (2013) Short term signaling responses in roots of young soybean seedlings exposed to cadmium stress. J Plant Physiol 170(18):1585–1594

    Article  PubMed  Google Scholar 

  • Costa MM, Hilliou F, Duarte P, Pereira LG, Almeida I, Leech M, Memelink J, Barcelo AR, Sottomayor M (2008) Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiol 146(2):403–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50(10):1268–1280

    Article  CAS  PubMed  Google Scholar 

  • De Carolis E, De Luca V (1993) Purification, characterization, and kinetic analysis of a 2-oxoglutarate-dependent dioxygenase involved in vindoline biosynthesis from Catharanthus roseus. J Biol Chem 268(8):5504–5511

    PubMed  Google Scholar 

  • Ferguson LR, Zhu ST, Harris PJ (2005) Antioxidant and antigenotoxic effects of plant cell wall hydroxycinnamic acids in cultured HT-29 cells. Mol Nutr Food Res 49(6):585–593

    Article  CAS  PubMed  Google Scholar 

  • Ferreres F, Figueiredo R, Bettencourt S, Carqueijeiro I, Oliveira J, Gil-Izquierdo A, Pereira DM, Valentão P, Andrade PB, Duarte P, Barceló AR, Sottomayor M (2011) Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: an H2O2 affair? J Exp Bot 62(8):2841–2854

    Article  CAS  PubMed  Google Scholar 

  • Filipič M (2012) Mechanisms of cadmium induced genomic instability. Mut Res/Fund Mol M 733(1–2):69–77

    Article  Google Scholar 

  • Guo XR, Chang BW, Zu YG, Tang ZH (2014) The impacts of increased nitrate supply on Catharanthus roseus growth and alkaloid accumulations under ultraviolet-B stress. J Plant Interact 9(1):640–646

    Article  Google Scholar 

  • Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette ML, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88(11):1751–1765

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:37. https://doi.org/10.1155/2012/872875

    Google Scholar 

  • Keunen E, Schellingen K, Vangronsveld J, Cuypers A (2016) Ethylene and metal stress: small molecule, big impact. Front Plant 7(192):23–41

    Google Scholar 

  • Khan NA, Khan MIR (2014) The ethylene: from senescence hormone to key player in plant metabolism. J Plant Biochem Physiol 2:2. https://doi.org/10.4172/2329-9029.1000e124

    Article  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173(3):9–18

    Article  CAS  PubMed  Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Mobin M, Anjum NA, Khan NA (2016) Modulation and significance of nitrogen and sulfur metabolism in cadmium challenged plants. Plant Growth Regul 78(1):1–11

    Article  CAS  Google Scholar 

  • Kim DI, Pedersen H, Chin CK (1991) Cultivation of Thalictrum rugosum cell suspension in an improved airlift bioreactor: stimulatory effect of carbon dioxide and ethylene on alkaloid production. Biotechnol Bioeng 38(4):331–339

    Article  CAS  PubMed  Google Scholar 

  • Kumar SP, Varman PAM, Kumari BDR (2011) Cadmium stress response in Catharanthus roseus leaves through proteomic approach. In: Paper presented at the international conference on biology, environment and chemistry, Singapore

  • Lv Y, Deng X, Quan L, Xia Y, Shen Z (2013) Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana. Plant Soil 367(1–2):507–519

    Article  CAS  Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35(3):524–533

    Article  CAS  PubMed  Google Scholar 

  • Monteiro C, Santos C, Pinho S, Oliveira H, Pedrosa T, Dias MC (2012) Cadmium-induced cyto- and genotoxicity are organ-dependent in lettuce. Chem Res Toxicol 25(7):1423–1434

    Article  CAS  PubMed  Google Scholar 

  • Pan YJ, Liu J, Guo XR, Zu YG, Tang ZH (2015) Gene transcript profiles of the TIA biosynthetic pathway in response to ethylene and copper reveal their interactive role in modulating TIA biosynthesis in Catharanthus roseus. Protoplasma 252(3):813–824

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Gupta K, Mukherjee AK (2007) Impact of cadmium and lead on Catharanthus roseus—a phytoremediation study. J Environ Biol 28(3):655–662

    CAS  PubMed  Google Scholar 

  • Papon N, Bremer J, Vansiri A, Andreu F, Rideau M, Creche J (2005) Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells. Planta Med 71(6):572–574

    Article  CAS  PubMed  Google Scholar 

  • Per TS, Khan NA, Masood A, Fatma M (2016) Methyl jasmonate alleviates cadmium-induced photosynthetic damages through increased S-assimilation and glutathione production in mustard. Front Plant Sci 7(468):1933–1946

    PubMed  PubMed Central  Google Scholar 

  • Pomahačová B, Dušek J, Dušková J, Yazaki K, Roytrakul S, Verpoorte R (2009) Improved accumulation of ajmalicine and tetrahydroalstonine in Catharanthus cells expressing an ABC transporter. J Plant Physiol 166(13):1405–1412

    Article  PubMed  Google Scholar 

  • Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez M, LA Del Rio, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29(8):1532–1544

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Del Rio LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150(1):229–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schellingen K, Van Der Straeten D, Vandenbussche F, Prinsen E, Remans T, Vangronsveld J, Cuypers A (2014) Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression. BMC Plant Biol 14(1):214–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Shitan N, Kato K, Shoji T (2014) Alkaloid transporters in plants. Plant Biotechnol 31(5):453–463

    Article  CAS  Google Scholar 

  • Singh S, Eapen S, D’souza S (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62(2):233–246

    Article  CAS  PubMed  Google Scholar 

  • Srivastava NK, Srivastava AK (2010) Influence of some heavy metals on growth, alkaloid content and composition in Catharanthus roseus L. Indian J Pharm Sci 72(6):775–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11(5):887–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thao NP, Khan MIR, Thu NBA, Hoang XLT, Asgher M, Khan NA, Tran L-SP (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169(1):73–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Trinh NN, Huang TL, Chi WC, Fu SF, Chen CC, Huang HJ (2014) Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol Plant 150(2):205–224

    Article  CAS  PubMed  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29(5):950–963

    Article  CAS  PubMed  Google Scholar 

  • Wink M (1997) Special nitrogen metabolism. In: Dey PM, Harborne JB (ed) Plant biochemistry, 1st edn. Academic Press, San Diego, London, pp 439–486

    Chapter  Google Scholar 

  • Yu F, De Luca V (2013) ATP-binding cassette transporter controls leaf surface secretion of anticancer drug components in Catharanthus roseus. Proc Natl Acad Sci 110(39):15830–15835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JC, Chen N, Zhang ZM, Pan LJ, Chen MN, Wang M, Wang T, Chi XY, Yang Z, Liu FZ, Yu SL, Wan YS (2016) Peanut ethylene-responsive element binding factor (AhERF6) improves cold and salt tolerance in Arabidopsis. Acta Physiol Plant 38(7):1–10

    Google Scholar 

  • Zhao J, Zhu WH, Hu Q (2000) Enhanced ajmalicine production in Catharanthus roseus cell cultures by combined elicitor treatment: from shake-flask to 20-l airlift bioreactor. Biotechnol Lett 22(6):509–514

    Article  CAS  Google Scholar 

  • Zheng Z, Wu M (2004) Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Sci 166(2):507–514

    Article  CAS  Google Scholar 

  • Zhu J, Zhang Q, Wu R, Zhang Z (2010) HbMT2, an ethephon-induced metallothionein gene from Hevea brasiliensis responds to H2O2 stress. Plant Physiol Biochem 48(8):710–715

    Article  CAS  PubMed  Google Scholar 

  • Zhu XX, Zeng XY, Sun C, Chen SL (2014) Biosynthetic pathway of terpenoid indole alkaloids in Catharanthus roseus. Front Med-PRC 8(3):285–293

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Fundamental Research Funds for the Central Universities (2572014CA09), the Fundamental Research Funds for the Central Universities (2572015CA04), the National Natural Science Foundation of China (31400337) and Doctor Independent Innovation Foundation of Northeast Forestry University (2572015AA02). We sincerely thank Prof. Zhonghua Tang for his critical comments on this manuscript.

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Correspondence to Hongzheng Wang.

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Communicated by G. Klobus.

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Chen, Q., Wu, K., Tang, Z. et al. Exogenous ethylene enhanced the cadmium resistance and changed the alkaloid biosynthesis in Catharanthus roseus seedlings. Acta Physiol Plant 39, 267 (2017). https://doi.org/10.1007/s11738-017-2567-6

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  • DOI: https://doi.org/10.1007/s11738-017-2567-6

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