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Physiological, genomic and transcriptomic comparison of two Brassica napus cultivars with contrasting cadmium tolerance

  • Shufeng Wang
  • Juanjuan Sun
  • Shengting Li
  • Kun Lu
  • Hongjun Meng
  • Zhongchun Xiao
  • Zhen Zhang
  • Jiana Li
  • Feng LuoEmail author
  • Nannan LiEmail author
Regular Article
  • 10 Downloads

Abstract

Aims

Cadmium (Cd) is the most widespread toxic heavy metal to plant growth. As the second leading oil crop, some genotypes of Brassica napus (B. napus) are potential Cd accumulators. However, the Cd translocation mechanism from root to shoot in B. napus in response to Cd toxicity remains unknown.

Methods

In the present study, a couple of B. napus genotypes with contrasting Cd uptake and root-to-shoot translocation abilities, named P78 (the high Cd accumulator, HC) and P72 (the low Cd accumulator, LC), were chosen from 39 B. napus genotypes with various Cd accumulation features.

Results

Physiological comparison of P78 and P72 reveals that P72 is more sensitive to Cd toxicity than P78. With genomic resequencing, transcriptomics and qRT-PCR assay, BnNramp2;1 and BnNramp4;2 were focused with highly upregulation in shoot of P78 under Cd treatment condition. Furthermore, BnNramp2;1 and BnNramp4;2 can successfully complement the function of tonoplast localized Cd transporter YCF1. And when BnNramp2;1 and BnNramp4;2 were transferred in Arabidopsis atnramp mutants, the transgenic plants showed better growth rate than mutants under higher Cd stress conditions.

Conclusions

The results reveals that BnNramp2;1 and BnNramp4;2 were two main Cd transporters associated with enhanced root-to-shoot translocation and accumulation of Cd in shoot of B. napus.

Keywords

Brassica napus Cd detoxification Genotypes Nramp gene family Transcriptomic analysis Yeast complementation 

Abbreviations

APX

Ascorbate peroxidase

AsA

Ascorbic acid

BCF

Biological enrichment factor

B.napus

Brassica napus

Ca

Calcium

CAT

Catalase

Cd

Cadmium

Ci

Intercellular CO2 concentration

Cu

Copper

DEGs

Differentially expressed genes

Fe

iron

GO

Gene ontology

GR

Glutathione reductase

Gs

Stomatal conductance

GSH

Glutataione

HC

High Cd accumulator

LC

Low Cd accumulator

MDA

Malondialdehyde

MDHAR

Monodehydroascorbate reductase

Mg

Magnesium

Mn

Manganese

Pn

Variation of net CO2 assimilation

POD

Peroxidase

R

Root

S

Shoot

SOD

Superoxide dismutase

TF

Translocation factor

Tr

Transpiration

Zn

Zinc

Notes

Acknowledgements

This work was supported by National Key R & D Program of China (2018YFD0800600, 2018YFD0200903), National Natural Science Foundation of China (31870587; 31400063; 31500038) and Fundamental Research Funds for the Central Universities (XDJK2017B030; SWU116021; XDJK2018C095; SWU118114; SWU115018), Research Funds of Scientific Platform and Base Construction (cstc2014pt-sy0017), and The Recruitment Program for Foreign Experts (No. WQ20125500073).

Authors’ contributions

SW and NL designed and conceived the study and drafted the manuscript. SW, JS, KL and SL performed experiments and data analysis. NL, SW, KL, HM, ZX, JL, FL and SL coordinated the research and helped to finalize the manuscript. All authors have read and approved the final manuscript.

Supplementary material

11104_2019_4083_MOESM1_ESM.docx (5.1 mb)
ESM 1 (DOCX 5260 kb)

References

  1. Anjum NA, Ahmad I, Rodrigues SM, Henriques B, Cruz N, Coelho C, Pacheco M, Duarte AC, Pereira E (2013) Eriophorum angustifolium and Lolium perenne metabolic adaptations to metals- and metalloids-induced anomalies in the vicinity of a chemical industrial complex. Environ Sci Pollut Res Int 20(1):568–581CrossRefGoogle Scholar
  2. Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422(2):217–228CrossRefGoogle Scholar
  3. Chen L, Wan H, Qian J, Guo J, Sun C, Wen J, Yi B, Ma C, Tu J, Song L, Fu T, Shen J (2018) Genome-wide association study of cadmium accumulation at the seedling stage in rapeseed (Brassica napus L.). Front Plant Sci 9:375CrossRefGoogle Scholar
  4. Choppala G, Saifullah BN, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33(5):374–391CrossRefGoogle Scholar
  5. Curie C, Alonso JM, Jean ML, Ecker JR, Briat J-F (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755CrossRefGoogle Scholar
  6. D'Alessandro A, Taamalli M, Gevi F, Timperio AM, Zolla L, Ghnaya T (2013) Cadmium stress responses in Brassica juncea: hints from proteomics and metabolomics. J Proteome Res 12(11):4979–4997CrossRefGoogle Scholar
  7. Fan W, Liu C, Cao B, Qin M, Long D, Xiang Z, Zhao A (2018) Genome-wide identification and characterization of four gene families putatively involved in cadmium uptake, translocation and sequestration in mulberry. Front Plant Sci 9:879CrossRefGoogle Scholar
  8. Feng J, Jia W, Lv S, Bao H, Miao F, Zhang X, Wang J, Li J, Li D, Zhu C, Li S, Li Y (2018) Comparative transcriptome combined with morpho-physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes. Plant Biotechnol J 16(2):558–571CrossRefGoogle Scholar
  9. Gao H, Xie W, Yang C, Xu J, Li J, Wang H, Chen X, Huang CF (2018) NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol 217(1):179–193CrossRefGoogle Scholar
  10. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930CrossRefGoogle Scholar
  11. Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B-ATPase, functions as a cd/Pb transporter in yeast. FEBS Lett 561(1–3):22–28CrossRefGoogle Scholar
  12. Gupta DK, Pena LB, Romero-Puertas MC, Hernandez A, Inouhe M, Sandalio LM (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ 40(4):509–526CrossRefGoogle Scholar
  13. Hua Y, Zhou T, Ding G, Yang Q, Shi L, Xu F (2016) Physiological, genomic and transcriptional diversity in responses to boron deficiency in rapeseed genotypes. J Exp Bot 67(19):5769–5784CrossRefGoogle Scholar
  14. Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2012) Characterizing the role of rice NRAMP5 in manganese, Iron and cadmium transport. Sci Rep 2(1)Google Scholar
  15. 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
  16. Lanquar V, Lelièvre F, Barbier-Brygoo H, Thomine S (2004) Regulation and function of AtNRAMP4 metal transporter protein. Soil Sci Plant Nutr 50(7):1141–1150CrossRefGoogle Scholar
  17. Lanquar V, Leliévre F, Bolte S, Hamés C, Alcon C, Neumann D, Vansuyt G. 2005. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4. EMBO J 24: 4041–4051, 2005Google Scholar
  18. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12(323)Google Scholar
  19. Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc Natl Acad Sci 94(1):42–47CrossRefGoogle Scholar
  20. Li N, Xiao H, Sun J, Wang S, Wang J, Chang P, Zhou X, Lei B, Lu K, Luo F, Shi X, Li J (2018) Genome-wide analysis and expression profiling of the HMA gene family in Brassica napus under cd stress. Plant Soil 426(1–2):365–381CrossRefGoogle Scholar
  21. Lu G, Casaretto JA, Ying S, Mahmood K, Liu F, Bi YM, Rothstein SJ (2017) Overexpression of OsGATA12 regulates chlorophyll content, delays plant senescence and improves rice yield under high density planting. Plant Mol Biol 94(1–2):215–227CrossRefGoogle Scholar
  22. Luo JS, Huang J, Zeng DL, Peng JS, Zhang GB, Ma HL, Guan Y, Yi HY, Fu YL, Han B, Lin HX, Qian Q, Gong JM (2018) A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9(1):645CrossRefGoogle Scholar
  23. Martinka M, Vaculík M, Lux A (2014) Plant cell responses to cadmium and zinc. Appl Plant Cell Biol 22:209–246CrossRefGoogle Scholar
  24. Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579(3):783–791CrossRefGoogle Scholar
  25. Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189(1):190–199CrossRefGoogle Scholar
  26. Mwamba TM, Li L, Gill RA, Islam F, Nawaz A, Ali B, Farooq MA, Lwalaba JL, Zhou W (2016) Differential subcellular distribution and chemical forms of cadmium and copper in Brassica napus. Ecotoxicol Environ Saf 134P1:239–249CrossRefGoogle Scholar
  27. Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta 1763(7):609–620CrossRefGoogle Scholar
  28. Okubo M, Yamada K, Hosoyamada M, Shibasaki T, Endou H (2003) Cadmium transport by human Nramp 2 expressed in Xenopus laevis oocytes. Toxicol Appl Pharmacol 187(3):162–167CrossRefGoogle Scholar
  29. Oomen RJ, Wu J, Lelievre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MG, Thomine S (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181(3):637–650CrossRefGoogle Scholar
  30. 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(4):625–637CrossRefGoogle Scholar
  31. Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24(5):2155–2167CrossRefGoogle Scholar
  32. Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35(2):334–346CrossRefGoogle Scholar
  33. Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in cd accumulation in rice. J Exp Bot 62(14):4843–4850CrossRefGoogle Scholar
  34. Thomine S, vre FL, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecifc vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695CrossRefGoogle Scholar
  35. Vatansever R, Filiz E, Ozyigit II (2016) In silico analysis of Mn transporters (NRAMP1) in various plant species. Mol Biol Rep 43(3):151–163CrossRefGoogle Scholar
  36. 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(3):306–312CrossRefGoogle Scholar
  37. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138CrossRefGoogle Scholar
  38. Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Hu C (2015a) Xylem transport and gene expression play decisive roles in cadmium accumulation in shoots of two oilseed rape cultivars (Brassica napus). Chemosphere 119:1217–1223CrossRefGoogle Scholar
  39. Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Qu C, Chen Z, Hu C (2015b) Antioxidant enzyme systems and the ascorbate-glutathione cycle as contributing factors to cadmium accumulation and tolerance in two oilseed rape cultivars (Brassica napus L.) under moderate cadmium stress. Chemosphere 138:526–536CrossRefGoogle Scholar
  40. Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Feng Ma J (2016) The HvNramp5 transporter mediates uptake of cadmium and manganese, but not Iron. Plant Physiol 172(3):1899–1910CrossRefGoogle Scholar
  41. Zhao FJ, Huang XY (2018) Cadmium phytoremediation: call Rice CAL1. Mol Plant 11(5):640–642CrossRefGoogle Scholar
  42. Zhou H, Zeng M, Zhou X, Liao B-H, Peng P-Q, Hu M, Zhu W, Wu Y-J, Zou Z-J (2014) Heavy metal translocation and accumulation in iron plaques and plant tissues for 32 hybrid rice (Oryza sativa L.) cultivars. Plant Soil 386(1–2):317–329Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Chongqing Key Lab of Bioresource for Energy, College of Resources and EnvironmentSouthwest UniversityChongqingPeople’s Republic of China
  2. 2.Academy of Agricultural ScienceSouthwest UniversityChongqingPeople’s Republic of China
  3. 3.College of Agronomy and BiotechnologySouthwest UniversityChongqingPeople’s Republic of China

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