Plant Growth Regulation

, Volume 85, Issue 1, pp 101–111 | Cite as

Overexpression of a Miscanthus sacchariflorus yellow stripe-like transporter MsYSL1 enhances resistance of Arabidopsis to cadmium by mediating metal ion reallocation

  • Houming Chen
  • Cheng Zhang
  • Haipeng Guo
  • Yimin Hu
  • Yi He
  • Dean Jiang
Original paper
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Abstract

The yellow stripe-like (YSL) family of transporters mediates the uptake, translocation, and distribution of various mineral elements in vivo by transferring metal ions chelated with phytosiderophore or nicotianamine (NA). However, little is known about the roles of the YSL genes against cadmium in planta. In this study, we first cloned and characterized a vital member of the YSL gene family, MsYSL1, from the bioenergy plant Miscanthus sacchariflorus. MsYSL1 localized in the plasma membrane and was widely expressed throughout the whole seedling with the highest expression level in the stem. In addition, its expression in the root was stimulated by excess manganese (Mn), cadmium (Cd), and lead, and a shortage of iron (Fe), zinc (Zn), and copper. Functional complementation in yeast indicated that MsYSL1 showed transport activity for Fe(II)–NA and Zn–NA, but not for Cd–NA. Although they exhibited no significant differences versus the wild type under normal cultivation conditions, MsYSL1-overexpressing Arabidopsis lines displayed a higher resistance to Cd accompanied by longer root lengths, lower Cd, Zn, and Mn levels in roots, and higher Cd, Fe, and Mn translocation ratios under Cd stress. Moreover, genes related to NA synthesis, metal translocation, long-distance transport, and Cd exclusion were highly induced in transgenic lines under Cd stress. Thus, MsYSL1 may be an essential transporter for diverse metal–NAs to participate in the Cd detoxification by mediating the reallocation of other metal ions.

Keywords

Miscanthus sacchariflorus MsYSL1 Yeast complementation Cd tolerance Arabidopsis 

Abbreviations

YSL

Yellow stripe-like

PSs

Phytosiderophores

NAs

Nicotianamines

NAS

Nicotianamine synthetase

MAs

Mugineic acids

DMAs

Deoxymugineic acids

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Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31571577, 31371591) and the National Science and Technology Support Plan of China (Grant No. 2012BAC09B01).

Author contributions

CHM, GHP and JDA conceived and designed the experiments. CHM and ZC performed the experiments. CHM, HYM and HY analyzed the data. CHM, GHP and JDA wrote the paper. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

These authors have declared that no competing interests exist.

Supplementary material

10725_2018_376_MOESM1_ESM.docx (14.5 mb)
Supplementary material 1 (DOCX 14834 KB)
10725_2018_376_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 18 KB)

References

  1. Aglawe SB, Fakrudin B, Patole CB, Bhairappanavar SB, Koti RV, Krishnaraj PU (2012) Quantitative RT-PCR analysis of 20 transcription factor genes of MADS, ARF, HAP2, MBF and HB families in moisture stressed shoot and root tissues of Sorghum. Physiol Mol Biol Plants 18:287–300CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2009) OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol 70:681–692CrossRefPubMedPubMedCentralGoogle Scholar
  3. Araki R, Murata J, Murata Y (2011) A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal-phytosiderophore complexes. Plant Cell Physiol 52:1931–1940CrossRefPubMedGoogle Scholar
  4. Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 281:32395–32402CrossRefPubMedGoogle Scholar
  5. Cao FB, Cai Y, Liu L, Zhang M, He XY, Zhang GP, Wu FB (2015) Differences in photosynthesis, yield and grain cadmium accumulation as affected by exogenous cadmium and glutathione in the two rice genotypes. Plant Growth Regul 75:715–723CrossRefGoogle Scholar
  6. Chu HH, Chiecko J, Punshon T, Lanzirotti A, Lahner B, Salt DE, Walker EL (2010) Successful reproduction requires the function of Arabidopsis YELLOW STRIPE-LIKE1 and YELLOW STRIPE-LIKE3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol 154:197–210CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chung JH, Kim DS (2012) Miscanthus, as a potential bioenergy crop in east Asia. J Crop Sci Biotechnol 15:65–77CrossRefGoogle Scholar
  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  9. Conte SS, Chu HH, Chan-Rodriguez D, Punshon T, Vasques KA, Salt DE, Walker EL (2013) Arabidopsis thaliana yellow stripe1-like4 and yellow stripe1-like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Front Plant Sci 4:283CrossRefPubMedPubMedCentralGoogle Scholar
  10. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349CrossRefPubMedGoogle Scholar
  11. Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11CrossRefPubMedGoogle Scholar
  12. Das S, Sen M, Saha C, Chakraborty D, Das A, Banerjee M, Seal A (2011) Isolation and expression analysis of partial sequences of heavy metal transporters from Brassica juncea by coupling high throughput cloning with a molecular fingerprinting technique. Planta 234:139–156CrossRefPubMedGoogle Scholar
  13. DiDonato RJ Jr, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414CrossRefPubMedGoogle Scholar
  14. Divol F, Couch D, Conéjéro G, Roschzttardtz H, Mari S, Curie C (2013) The Arabidopsis yellow stripe like4 and 6 transporters control iron release from the chloroplast. Plant Cell 25:1040–1055CrossRefPubMedPubMedCentralGoogle Scholar
  15. Eren E, Arguello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P(1B)-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ezaki B, Nagao E, Yamamoto Y, Nakashima S, Enomoto T (2008) Wild plants, Andropogon virginicus L. and Miscanthus sinensis Anders, are tolerant to multiple stresses including aluminum, heavy metals and oxidative stresses. Plant Cell Rep 27:951–961CrossRefPubMedGoogle Scholar
  17. Feng SS, Tan JJ, Zhang YX, Liang S, Xiang SQ, Wang H, Chai TY (2016) Isolation and characterization of a novel cadmium-regulated yellow stripe-like transporter (SnYSL3) in Solanum nigrum. Plant Cell Rep 36:1–16Google Scholar
  18. Gendre D, Czernic P, Conéjéro G, Pianelli K, Briat JF, Lebrun M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J 49:1–15CrossRefPubMedGoogle Scholar
  19. Gietz RD, Schiestl RH (1995) Transforming yeast with DNA. Methods Mol Cell Biol 5:255–269Google Scholar
  20. Guo HP, Hong CT, Chen XM, Xu YX, Liu Y, Jiang DA, Zheng BS (2016a) Different growth and physiological responses to cadmium of the three Miscanthus species. PLoS ONE 11:e0153475CrossRefPubMedPubMedCentralGoogle Scholar
  21. Guo HP, Hong CT, Xiao MZ, Chen XM, Chen HM, Zheng BS, Jiang DA (2016b) Real-time kinetics of cadmium transport and transcriptomic analysis in low cadmium accumulator Miscanthus sacchariflorus. Planta 244:1–14CrossRefGoogle Scholar
  22. Higuchi K, Kanazawa K, Nishizawa NK, Chino M, Mori S (1994) Purification and characterization of nicotianamine synthase from Fe-deficient barley roots. Plant Soil 165:173–179CrossRefGoogle Scholar
  23. Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390CrossRefPubMedGoogle Scholar
  24. Kakei Y, Ishimaru Y, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK (2012) OsYSL16 plays a role in the allocation of iron. Plant Mol Biol 79:583–594CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kayama M (2001) Comparison of the aluminum tolerance of Miscanthus sinensis Anderss. and Miscanthus sacchariflorus Bentham in hydroculture. Int J Plant Sci 162:1025–1031CrossRefGoogle Scholar
  26. Kim S, Takahashi M, Higuchi K, Tsunoda K, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2005) Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants. Plant Cell Physiol 46:1809–1818CrossRefPubMedGoogle Scholar
  27. Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218CrossRefPubMedGoogle Scholar
  28. Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271CrossRefPubMedPubMedCentralGoogle Scholar
  29. Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424CrossRefPubMedGoogle Scholar
  30. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277:5360–5368CrossRefPubMedGoogle Scholar
  32. Lin YF, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206CrossRefPubMedGoogle Scholar
  33. Lin H, Fang CX, Li YZ, Lin WW, He JY, Lin RY, Lin WX (2016) Cadmium-stress mitigation through gene expression of rice and silicon addition. Plant Growth Regul 81:1–11Google Scholar
  34. Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T (2006) A specific transporter for iron(III)-phytosiderophore in barley roots. Plant J 46:563–572CrossRefPubMedGoogle Scholar
  35. Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136CrossRefPubMedGoogle Scholar
  36. Pottier M, Oomen R, Picco C, Giraudat J, Scholz-Starke J, Richaud P, Carpaneto A, Thomine S (2015) Identification of mutations allowing natural resistance associated macrophage proteins (NRAMP) to discriminate against cadmium. Plant J 83:625–637CrossRefPubMedGoogle Scholar
  37. Sasaki A, Yamaji N, Xia J, Ma JF (2011) OsYSL6 is involved in the detoxification of excess manganese in rice. Plant Physiol 157:1832–1840CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021CrossRefPubMedPubMedCentralGoogle Scholar
  39. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, Von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096CrossRefPubMedGoogle Scholar
  40. Schaaf G, Schikora A, Häberle J, Vert G, Ludewig U, Briat JF, Curie C, Von Wirén N (2005) A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774CrossRefPubMedGoogle Scholar
  41. Senoura T, Sakashita E, Kobayashi T, Takahashi M, Aung MS, Masuda H, Nakanishi H, Nishizawa NK (2017) The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains. Plant Mol Biol 95:375–387CrossRefPubMedGoogle Scholar
  42. Singh S, Singh A, Bashri G, Prasad SM (2016) Impact of cd stress on cellular functioning and its amelioration by phytohormones: an overview on regulatory network. Plant Growth Regul 80:253–263CrossRefGoogle Scholar
  43. Takahashi M, Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa NK, Mori S (1999) Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiol 121:947–956CrossRefPubMedPubMedCentralGoogle Scholar
  44. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312CrossRefPubMedGoogle Scholar
  45. Wang JW, Li Y, Zhang YX, Chai TY (2013) Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep 32:651–662CrossRefPubMedGoogle Scholar
  46. Waters BM, Chu HH, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wu HL, Chen CL, Du J, Liu HF, Cui Y, Zhang Y, He YJ, Wang YQ, Chu CC, Feng ZY, Li JM, Ling HQ (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800CrossRefPubMedGoogle Scholar
  48. Xu YX, Zhang SN, Guo HP, Wang SK, Xu LG, Li CY, Qian Q, Chen F, Geisler M, Qi YH, Jiang DA (2014) OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa L.). Plant J 79:106–117CrossRefPubMedGoogle Scholar
  49. Yang J, Chen JQ, Chen X, Ma G, Wang P, Fabrice MR, Zhang SL, Wu JY (2016) Phylogenetic and expression analysis of pear yellow stripe-like transporters and functional verification of PbrYSL4 in pear pollen. Plant Mol Biol Rep 34:737–747CrossRefGoogle Scholar
  50. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Routine procedures for growing rice plants in culture solution, 3rd edn. International Rice Research Institute, Los BanosGoogle Scholar
  51. Zhang J, Yang SY, Huang YJ, Zhou SB (2015) The tolerance and accumulation of Miscanthus sacchariflorus (maxim.) Benth., an energy plant species, to cadmium. Int J Phytoremediat 17:538–545CrossRefGoogle Scholar
  52. Zheng LQ, Fujii M, Yamaji N, Sasaki A, Yamane M, Sakurai I, Sato K, Ma JF (2011) Isolation and characterization of a barley yellow stripe-like gene, HvYSL5. Plant Cell Physiol 52:765–774CrossRefPubMedGoogle Scholar
  53. Zheng LQ, Yamaji N, Yokosho K, Ma JF (2012) YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell 24:3767–3782CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Houming Chen
    • 1
  • Cheng Zhang
    • 1
  • Haipeng Guo
    • 1
    • 2
  • Yimin Hu
    • 3
  • Yi He
    • 1
  • Dean Jiang
    • 1
  1. 1.College of Life SciencesZhejiang UniversityHangzhouPeople’s Republic of China
  2. 2.School of Marine SciencesNingbo UniversityNingboPeople’s Republic of China
  3. 3.College of Food Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China

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