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NAC transcription factors from Aegilops markgrafii reduce cadmium concentration in transgenic wheat

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Abstract

Background and aims

Cadmium (Cd) is one of the heavy metal elements that are most harmful to human health, and the transmission of Cd through the food chain is a global issue. Aegilops markgrafii is a wild relative of the cultivated wheat that is tolerant of high levels of Cd. The objective of this study is to investigate the NAC transcription factors (TFs) involved in Cd tolerance in Ae. markgrafii and to verify their function in transgenic wheat.

Methods

We cloned NAC TFs from Ae. markgrafii plants exposed to excessive Cd treatment. The expression profiles of NAC TFs in root and shoot tissues were examined using qRT-PCR. Transgenic wheat was obtained via Agrobacterium-mediated transformation. Finally, we examined Cd concentrations in transgenic wheat under excess Cd treatment.

Results

We identified three NAC TFs and classified them into four subfamilies. Sequence alignments showed that the NAC TFs had conserved N-terminal domains but varied C-terminal domains. Expression profiles of NAC TFs showed about 150-fold up-regulation in the transcription of AemNAC2 and AemNAC3 under excess Cd treatment. Overexpression of AemNAC2 in the wheat cultivar ‘Bobwhite’ led to reduce Cd concentration in the root, shoot and grains.

Conclusions

AemNAC2 is an important TF that contributes to Cd tolerance in wheat.

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References

  1. Abuhammad WA, Mamidi S, Kumar A, Pireseyedi S, Manthey FA, Kianian SF, Alamri MS, Mergoum M, Elias EM (2016) Identification and validation of a major cadmium accumulation locus and closely associated SNP markers in North Dakota durum wheat cultivars. Mol Breed 35:112

  2. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

  3. Cai HL, Xie PF, Zeng WA, Zhai ZG, Zhou W, Tang Z (2019) Root-specific expression of rice OsHMA3 reduces shoot cadmium accumulation in transgenic tobacco. Mol Breed 39:49

  4. Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228

  5. Codex Alimentarius Commission (2015) General standard for contaminants and toxins in food and feed. CODEX Standards 193–1995, amended in: 2015

  6. Deng FL, Yu M, Martinoia E, Song WY (2019a) Ideal cereals with lower arsenic and cadmium by accurately enhancing vacuolar sequestration capacity. Front Genet. https://doi.org/10.3389/fgene.2c019.00322

  7. Deng RY, Zhao HX, Xiao YH, Huang YJ, Yao PF, Lei YL, Li CL, Chen H, Wu Q (2019b) Cloning, characterization, and expression analysis of eight stress-related NAC genes in tartary buckwheat. Crop Sci 59:266–279

  8. Du XY, Wang HN, He JF, Zhu B, Guo J, Hou WQ, Weng QB, Zhang XC (2018) Identification of nicotianamine synthase genes in Triticum monococcum and their expression under different Fe and Zn concentrations. Gene 672:1–7

  9. Grant C, Flaten D, Tenuta M, Malhi S, Akinremi W (2013) The effect of rate and Cd concentration of repeated phosphate fertilizer applications on seed Cd concentration varies with crop type and environment. Plant Soil 372:221–233

  10. Guttieri MJ, Baenziger PS, Frels K, Carver B, Arnall B, Wang SC, Akhunov E, Waters BM (2015) Prospects for selecting wheat with increased zinc and decreased cadmium concentration in grain. Crop Sci 55:1712–1728

  11. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313

  12. Hou WQ, Feng W, Yu GH, Du XY, Ren MJ (2017) Cloning and functional analysis of a novel x-type high-molecular-weight glutenin subunit with altered cysteine residues from Aegilops umbellulata. Crop Pasture Sci 68:409–414

  13. Hu HH, Dai MQ, Yao JL, Xiao BZ, Li X, Zhang QF, Xiong LZ (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci U S A 103:12987–12992

  14. Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

  15. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Phytol 153:185–197

  16. Ji L, Hu RB, Jiang JX, Qi G, Yang XW, Zhu M, Fu CX, Zhou GK, Yi ZL (2014) Molecular cloning and expression analysis of 13 NAC transcription factors in Miscanthus lutarioriparius. Plant Cell Rep 33:2077–2092

  17. Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635

  18. Kubo K, Watanabe Y, Oyanagi A, Kaneko S, Chono M, Matsunaka H, Seki M, Fujita M (2008) Cadmium concentration in grains of Japanese wheat cultivars genotypic difference and relationship with agronomic characteristics. Plant Prod Sci 11:243–249

  19. Liu CX, Guttieri MJ, Waters BM, Eskridge KM, Easterly A, Baenziger PS (2018) Cadmium concentration in terminal tissues as tools to select low-cadmium wheat. Plant Soil 430:127–138

  20. Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress responsive genes in Arabidopsis. Plant Mol Biol 63:289–305

  21. Mao XG, Zhang HY, Qian XY, Li A, Zhao GY, Jing RL (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

  22. Mao XG, Chen SS, Li A, Zhai CC, Jing RL (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One 9:e84359

  23. Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

  24. Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945

  25. Oomen RJFJ, Wu J, Lelièvre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MGM, Thomine S (2008) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Physiol 181:637–650

  26. Peng F, Wang C, Zhu JS, Zeng J, Kang HY, Fan X, Sha LN, Zhang HQ, Zhou YH, Wang Y (2018) Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247:1395–1406

  27. Qiao K, Gong L, Tian YB, Wang H, Chai TY (2018) The metal-binding domain of wheat heavy metal ATPase 2 (TaHMA2) is involved in zinc/cadmium tolerance and translocation in Arabidopsis. Plant Cell Rep 37:1343–1352

  28. Salsman E, Kumar A, AbuHammad W, Abbasabadi AO, Dobrydina M, Chao S, Li XH, Manthey FA, Elias EM (2018) Development and validation of molecular markers for grain cadmium in durum wheat. Mol Breed 38:28

  29. Sasaki A, Yamaji Y, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

  30. Shao JF, Xia JX, Yamaji N, Shen RF, Ma JF (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of OsHMA2 promoter. J Exp Bot 69:2743–2752

  31. Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genomewide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403–423

  32. 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 62:4843–4850

  33. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183

  34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

  35. Tang L, Mao BG, Li YK, Lv QM, Zhang LP, Chen CY, He HJ, Wang WP, Zeng XF, Shao Y, Pan YL, Hu YY, Peng Y, Fu XQ, Li HQ, Xia ST, Zhao BR (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7:14438

  36. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

  37. Wan YF, Wang DW, Shewry PR, Halford NG (2002) Isolation and characterization of five novel high molecular weight subunit of glutenin genes from Triticum timopheevii and Aegilops cylindrical. Theor Appl Genet 104:828–839

  38. Wang CH, Guo WL, Ye S, Wei PC, Ow DW (2016) Reduction of Cd in rice through expression of OXS3-like gene fragments. Mol Plant 9:301–304

  39. Wang CH, Guo WL, Cai XZ, Li RY, Ow DW (2019) Engineering low-cadmium rice through stress-inducible expression of OXS3-family member genes. New Biotechnol 48:29–34

  40. Weibe K, Harris NS, Faris JD, Clarke JM, Knox RE, Taylor GJ, Pozniak CJ (2010) Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum). Theor Appl Genet 121:1047–1058

  41. Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290

  42. Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016) The HvNRAMP5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172:1899–1910

  43. Xia N, Zhang G, Sun YF, Zhu L, Xu LS, Chen XM, Liu B, Yu YT, Wang XJ, Huang LL, Kang ZS (2010) TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol 74:394–402

  44. Xiang SQ, Feng SS, Zhang YX, Tian JJ, Liang S, Chai TY (2015) The N-terminal degenerated metal-binding domain is involved in the heavy metal transport activity of TaHMA2. Plant Cell Rep 34:1615–1628

  45. Xiao H, Yin L, Xu X, Li T, Han Z (2008) The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Ann Bot 102:881–889

  46. Xue GP, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712

  47. Yang M, Zhang Y, Zhang L, Hu J, Zhang X, Lu K, Dong H, Wang D, Zhao F, Huang C, Lian X (2014) OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot 65:4849–4861

  48. Yang XW, Wang XY, Ji L, Yi ZL, Fu CX, Ran JC, Hu RB, Zhou GK (2015) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep 34:943–958

  49. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075

  50. Yue JY, Wei XJ, Wang HZ (2018) Cadmium tolerant and sensitive wheat lines: their differences in pollutant accumulation, cell damage, and autophagy. Biol Plantarum 62:379–387

  51. Zhang SJ, Zhang RZ, Song GQ, Gao J, Li W, Han XD, Chen ML, Li YL, Li GY (2018) Targeted mutagenesis using the Agrobacterium tumefaciens-mediated CRISPR-Cas9 system in common wheat. BMC Plant Biol 18:302

  52. Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. TaNAC2 confers multiple abiotic stress tolerances. Biochem Bioph Res Co 379:985–989

  53. Zhu B, Huo DA, Hong XX, Guo J, Peng T, Liu J, Huang XL, Yan HQ, Weng QB, Zhang XC, Du XY (2019) The Salvia miltiorrhiza NAC transcription factor SmNAC1 enhances zinc content in transgenic Arabidopsis. Gene 688:54–61

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Acknowledgments

This work was financed by the Natural Science Foundation of Guizhou Province (2019-1236), the National Natural Science Foundation of China (31660390), the Foundation for Breeding Programs (2017YFD0100900), and the Achievements Transformation Program for Agriculture in Guizhou Province (Qiankehe Achievement 2016-4022).

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Correspondence to Mingjian Ren or Heng Tang.

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Du, X., He, F., Zhu, B. et al. NAC transcription factors from Aegilops markgrafii reduce cadmium concentration in transgenic wheat. Plant Soil (2020). https://doi.org/10.1007/s11104-019-04419-w

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Keywords

  • Aegilops markgrafii
  • NAC transcription factor
  • Transgenic wheat
  • Cadmium tolerance