Advertisement

Plant and Soil

, Volume 431, Issue 1–2, pp 71–87 | Cite as

Natural variation of CsSTOP1 in tea plant ( Camellia sinensis ) related to aluminum tolerance

  • Hua ZhaoEmail author
  • Wei Huang
  • Yange Zhang
  • Ziwei Zhang
  • Yong Li
  • Che Tang
  • Jie Huang
  • Dejiang Ni
Regular Article
  • 392 Downloads

Abstract

The tea plant (Camellia sinensis (L.) O. Kuntze) is indigenous to China, where its wild ancestors are broadly distributed in Southwest China. As an aluminum (Al) accumulator, tea plant is very tolerant to Al and accumulates Al at high levelin the leaves. Here an Al tolerant transcription factor of CsSTOP1 was characterized and assumed to regulate multiple genes critical for Al tolerance. The transcriptional regulations by STOP1-like proteins were conserved and conferred the ability to survive in acid soil. Furthermore, a 9-bp deletion was found in five varieties of assamica subspecies and CsSTOP1Mkdy-OE Arabidopsis lines showed more tolerant to Al than CsSTOP1JM1-OE lines, which might be the natural selection of the genetic variation for the tea plant’s adaptation to acidic soil. Given the CsSTOP1Mkdy allele more tolerant to Al and tea plant gradually spreading from the original center of Southwest China, this present study suggests that CsSTOP1 is labelled as an ‘adaptive’ trait that increases tea plant fitness in a particular environmental context of rhizotoxicity Al toxicity in acid soil. The qPCR result suggests the 9-bp deletion is not responsible for transcriptional activity while this deletion may affect the transcriptional regulation level.

Keywords

Adaptation Acid soil Aluminum tolerance CsSTOP1 Natural variation Tea plant 

Notes

Acknowledgements

This work was jointly supported by National Natural Science Foundation of China (31470406), the Fundamental Research Funds for the Central Universities (2662015BQ011 and 2662018JC046).

Author Contributions

H Zhao and DJ Ni funded project and designed the study. H Zhao conducted data analysis and wrote the manuscript. YG Zhang, W Huang, Y Li, ZW Zhang & J Huang carried out the in planta transformation, phenotype identification and subcellular localization. C Tang assessed the Al concentration.

Supplementary material

11104_2018_3746_MOESM1_ESM.pptx (874 kb)
ESM 1 The Arabidopsis (WT) growth in response to a gradient Al levels (a) and the comparison between WT and stop1 mutant exposed to sensititive Al level of 6 μM (b). (PPTX 874 kb)
11104_2018_3746_MOESM2_ESM.docx (25 kb)
Table S1 (DOCX 24 kb)
11104_2018_3746_MOESM3_ESM.xlsx (45 kb)
Table S2 Haplotype analysis of the CsSTOP1 gene region based on amino acid sequence from 50 tea plant accessions. The conserved zinc finger domain for the 50 tea plant accessions. (XLSX 44 kb)
11104_2018_3746_MOESM4_ESM.xlsx (34 kb)
Table S3 (XLSX 34 kb)

References

  1. Andrade LRM, Barros LMG, Echevarria GF et al (2011) Al-hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Environ Exp Bot 70:37–42CrossRefGoogle Scholar
  2. Balasaravanan T, Pius PK, Raj Kumar R et al (2003) Genetic diversity among South Indian tea germplasm (Camellia sinensis, C. assamica and C.assamica spp. lasiocalyx) using AFLP markers. Plant Sci 165:365–372CrossRefGoogle Scholar
  3. Chen L, Yamaguchi S (2005) RAPD markers for discriminating tea germplasms on the inter-specific level in China. Plant Breed 124:404–409CrossRefGoogle Scholar
  4. Chen L, Zhou ZX (2005) Variations of main quality components of tea genetic resources [Camellia sinensis (L.) O. Kuntze] preserved in the China National Germplasm Tea Repository. Plant Foods Hum Nutr 60:31–35CrossRefPubMedGoogle Scholar
  5. Chen L, Yu FL, Tong QQ (2000) Discussions on phylogenetic classification and evolution of sect Thea. J Tea Sci 20:89–94Google Scholar
  6. Chen ZC, Yamaji N, Motoyama R (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633CrossRefPubMedPubMedCentralGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  8. Comadran J, Kilian B, Russell J et al (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44:1388–1392CrossRefPubMedGoogle Scholar
  9. Cuenca G, Herrera R, Medina E (1990) Aluminium tolerance in trees of a tropical cloud forest. Plant Soil 125:169–175CrossRefGoogle Scholar
  10. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321CrossRefPubMedPubMedCentralGoogle Scholar
  11. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262CrossRefPubMedGoogle Scholar
  12. Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348CrossRefPubMedGoogle Scholar
  13. Fan W, Lou HQ, Gong YL et al (2015) Characterization of an inducible C2H2 -type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol 208:456–468CrossRefPubMedGoogle Scholar
  14. Fan W, Lou HQ, Yang JL et al (2016) The roles of STOP1-like transcription factors in aluminum and proton tolerance. Plant Signal Behav e1131371:11Google Scholar
  15. Fumagalli M, Sironi M, Pozzoli U et al (2011) Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressurethrough human evolution. PLoS Genet e1002355:7Google Scholar
  16. Furukawa J, Yamaji N, Wang H et al (2007) An aluminum activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091CrossRefPubMedGoogle Scholar
  17. Grevenstuk T, Romano A (2013) Aluminium speciation and internal detoxification mechanisms in plants: where do we stand? Metallomics 5:1584–1594CrossRefPubMedGoogle Scholar
  18. Grotz N, Fox T, Connolly E et al (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci 95:7220–7224CrossRefPubMedGoogle Scholar
  19. Hajiboland R, Barceló J, Poschenrieder C et al (2013) Amelioration of iron toxicity: A mechanism for aluminum-induced growth stimulation in tea plants. J Inorg Biochem 128:183–187CrossRefPubMedGoogle Scholar
  20. Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197CrossRefPubMedPubMedCentralGoogle Scholar
  21. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667CrossRefPubMedPubMedCentralGoogle Scholar
  22. Huang CF, Yamaji N, Ma JF (2010) Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiol 153:1669–1677CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance. Bot Rev 68:235–269CrossRefGoogle Scholar
  24. Klug BL, Horst WJ (2010) Oxalate exudation into the root-tip water free space confers protection from aluminum toxicity and allows aluminum accumulation in the symplast in buckwheat (Fagopyrum esculentum). New Phytol 187:380–391CrossRefPubMedGoogle Scholar
  25. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Biol 46:237–260CrossRefGoogle Scholar
  26. Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493CrossRefPubMedGoogle Scholar
  27. Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  28. Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J 41:353–363CrossRefPubMedGoogle Scholar
  29. Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–1458CrossRefPubMedGoogle Scholar
  30. Li JY, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci 111:6503–6508CrossRefPubMedGoogle Scholar
  31. Li Y, Huang J, Song X, Zhang Z, Jiang Y, Zhu Y, Zhao H, Ni D (2017a) An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant. Planta 246:91–103CrossRefPubMedGoogle Scholar
  32. Li YB, Iqbal M, Zhang QQ, Spelt C, Bliek M, Hakvoort HWJ, Quattrocchio FM, Koes R, Schat H (2017b) Two Silene vulgaris copper transporters residing in different cellular compartments confer copper hypertolerance by distinct mechanisms when expressed in Arabidopsis thaliana. New Phytol 215:1102–1114CrossRefPubMedGoogle Scholar
  33. Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399CrossRefPubMedGoogle Scholar
  34. Lu SJ, Zhao XH, Hu YL et al (2017) Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield. Nat Genet 49:773–779CrossRefPubMedGoogle Scholar
  35. Ma JF, Ryan PR, Delhaize E (2001) Aluminum resistance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278CrossRefPubMedGoogle Scholar
  36. Magalhaes JV, Liu J, Guimaraes CT (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161CrossRefPubMedGoogle Scholar
  37. Maron LG, Pineros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao C et al (2010) Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61:728–740CrossRefPubMedGoogle Scholar
  38. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ et al (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci 110:5241–5246CrossRefPubMedGoogle Scholar
  39. Matsumoto H, Hirasawa E, Morimura S, Takahashi E (1976) Localization of aluminium in tea leaves. Plant Cell Physiol 17:627–631CrossRefGoogle Scholar
  40. Ming TL (1992) A revision of Camellia sect. Thea. Acta Bot Yunnanica 14:115–132Google Scholar
  41. Morita A, Horie H, Fujii Y, Takatsu S, Wtanabe N, Yagia A, Yokotaa H (2004) Chemical forms of aluminum in xylem sap of tea plants (Camellia sinensis L.). Phytochemistry 65:2775–2780CrossRefPubMedGoogle Scholar
  42. Morita A, Yanagisawa O, Maeda S, Takatsu S, Ikka T (2011) Tea plant (Camellia sinensis L.) roots secrete oxalic acid and caffeine into medium containing aluminum. Soil Sci Plant Nutr 57:796–802CrossRefGoogle Scholar
  43. Ohyama Y, Ito H, Kobayashi Y, Ikka T, Morita A, Kobayashi M, Imaizumi R, Aoki T, Komatsu K, Sakata Y, Iuchi S, Koyama H (2013) Characterization of AtSTOP1 orthologous genes in tobacco and other plant species. Plant Physiol 162:1937–1946CrossRefPubMedPubMedCentralGoogle Scholar
  44. Osaki M, Watababe T, Tadano T (1997) Beneficial effect of aluminum on growth of plants adapted to low pH soils. Soil Sci Plant Nutr 43:551–563CrossRefGoogle Scholar
  45. Ryan PR, Delhaize E (2010) The convergent evolution of aluminium resistance in plants exploits a convenient currency. Funct Plant Biol 37:275–284CrossRefGoogle Scholar
  46. Ryan PR, DiTomaso JM, Kochian LV (1993) Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446CrossRefGoogle Scholar
  47. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and highsalinity stress conditions. Plant Physiol 136:2734–2746Google Scholar
  49. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, Sakurai N, Fujita M, Shinozaki K, Shibata D, Kobayashi M, Koyama H (2009) STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281–294CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone in maize. Plant Physiol 116:155–163CrossRefPubMedCentralGoogle Scholar
  51. Takanashi K, Shitan N, Yazaki K (2014) The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnology 31:417–430CrossRefGoogle Scholar
  52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  53. Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15CrossRefGoogle Scholar
  54. Watanabe T, Osaki M (2002) Mechanisms of adaptation to high aluminum condition in native plant species growing in acid soils: A review. Commun Soil Sci Plant Anal 33:1247–1260CrossRefGoogle Scholar
  55. Watanabe T, Misawa S, Hiradate S, Osaki M (2008) Characterization of root mucilage from Melastoma malabathricum, with emphasis on its roles inaluminum accumulation. New Phytol 178:581–589CrossRefPubMedGoogle Scholar
  56. Wolfe SA, Nekludova L, Pabo CO (2000) DNA recognition by Cys(2)His(2) zinc finger proteins. Annu Rev Biophys Biomol Struct 29:183–212Google Scholar
  57. Xia J, Yamaji N, Kasai T (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci 107:18381–18385Google Scholar
  58. Xia JX, Yamaji N, Ma JF (2013) A plasma membrane-localized small peptide is involved in Al tolerance in rice. Plant J 76:345–355PubMedGoogle Scholar
  59. Xu Q, Wang Y, Ding Z, Song L, Li Y, Ma D, Wang Y, Shen J, Jia S, Sun H, Zhang H (2016) Aluminum induced metabolic responses in two tea cultivars. Plant Physiol Biochem 101:162–172CrossRefPubMedGoogle Scholar
  60. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21:3339–3349CrossRefPubMedPubMedCentralGoogle Scholar
  61. Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37: 296–303Google Scholar
  62. Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 69:1061–1069CrossRefGoogle Scholar
  63. Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF (2016) Functional Analysis of a MATE Gene OsFRDL2 Revealed its Involvement in Al-Induced Secretion of Citrate, but a Lower Contribution to Al Tolerance in Rice. Plant Cell Physiol 57:976–985CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Hua Zhao
    • 1
    • 2
    Email author
  • Wei Huang
    • 1
    • 2
  • Yange Zhang
    • 1
    • 2
  • Ziwei Zhang
    • 1
    • 2
  • Yong Li
    • 1
    • 2
  • Che Tang
    • 3
  • Jie Huang
    • 1
    • 2
  • Dejiang Ni
    • 1
    • 2
  1. 1.Key Laboratory of Horticultural Plant Biology of Ministry of EducationHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.College of Horticulture & Forestry SciencesHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  3. 3.Hubei Province Agricultural Products Quality Safety Testing CenterWuhanPeople’s Republic of China

Personalised recommendations