Skip to main content

Advertisement

Log in

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

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 70:37–42

    Google Scholar 

  • 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 165:365–372

    CAS  Google Scholar 

  • Chen L, Yamaguchi S (2005) RAPD markers for discriminating tea germplasms on the inter-specific level in China. Plant Breed 124:404–409

    CAS  Google Scholar 

  • 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 60:31–35

    CAS  PubMed  Google Scholar 

  • Chen L, Yu FL, Tong QQ (2000) Discussions on phylogenetic classification and evolution of sect Thea. J Tea Sci 20:89–94

    Google Scholar 

  • 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 159:1624–1633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • 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 44:1388–1392

    CAS  PubMed  Google Scholar 

  • Cuenca G, Herrera R, Medina E (1990) Aluminium tolerance in trees of a tropical cloud forest. Plant Soil 125:169–175

    CAS  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262

    CAS  PubMed  Google Scholar 

  • Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348

    CAS  PubMed  Google Scholar 

  • 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 208:456–468

    CAS  PubMed  Google Scholar 

  • Fan W, Lou HQ, Yang JL et al (2016) The roles of STOP1-like transcription factors in aluminum and proton tolerance. Plant Signal Behav e1131371:11

    Google Scholar 

  • 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 e1002355:7

    Google Scholar 

  • Furukawa J, Yamaji N, Wang H et al (2007) An aluminum activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    CAS  PubMed  Google Scholar 

  • Grevenstuk T, Romano A (2013) Aluminium speciation and internal detoxification mechanisms in plants: where do we stand? Metallomics 5:1584–1594

    CAS  PubMed  Google Scholar 

  • 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 95:7220–7224

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 128:183–187

    CAS  PubMed  Google Scholar 

  • 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 106:185–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 21:655–667

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 153:1669–1677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: A review of its phylogenetic significance. Bot Rev 68:235–269

    Google Scholar 

  • 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 187:380–391

    CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Biol 46:237–260

    CAS  Google Scholar 

  • 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 55:459–493

    CAS  PubMed  Google Scholar 

  • Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    CAS  Google Scholar 

  • 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 41:353–363

    CAS  PubMed  Google Scholar 

  • 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 225:1447–1458

    CAS  PubMed  Google Scholar 

  • 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 111:6503–6508

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 246:91–103

    CAS  PubMed  Google Scholar 

  • 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 215:1102–1114

    CAS  PubMed  Google Scholar 

  • 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 57:389–399

    CAS  PubMed  Google Scholar 

  • 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 49:773–779

    CAS  PubMed  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminum resistance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    CAS  PubMed  Google Scholar 

  • 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 39:1156–1161

    CAS  PubMed  Google Scholar 

  • 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 61:728–740

    CAS  PubMed  Google Scholar 

  • 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 110:5241–5246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto H, Hirasawa E, Morimura S, Takahashi E (1976) Localization of aluminium in tea leaves. Plant Cell Physiol 17:627–631

    CAS  Google Scholar 

  • Ming TL (1992) A revision of Camellia sect. Thea. Acta Bot Yunnanica 14:115–132

    Google Scholar 

  • 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 65:2775–2780

    CAS  PubMed  Google Scholar 

  • 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 57:796–802

    CAS  Google Scholar 

  • 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 162:1937–1946

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osaki M, Watababe T, Tadano T (1997) Beneficial effect of aluminum on growth of plants adapted to low pH soils. Soil Sci Plant Nutr 43:551–563

    CAS  Google Scholar 

  • Ryan PR, Delhaize E (2010) The convergent evolution of aluminium resistance in plants exploits a convenient currency. Funct Plant Biol 37:275–284

    CAS  Google Scholar 

  • 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 44:437–446

    CAS  Google Scholar 

  • 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 149:340–351

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 136:2734–2746

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 150:281–294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone in maize. Plant Physiol 116:155–163

    CAS  PubMed Central  Google Scholar 

  • Takanashi K, Shitan N, Yazaki K (2014) The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnology 31:417–430

    CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Google Scholar 

  • 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 33:1247–1260

    CAS  Google Scholar 

  • 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 178:581–589

    CAS  PubMed  Google Scholar 

  • Wolfe SA, Nekludova L, Pabo CO (2000) DNA recognition by Cys(2)His(2) zinc finger proteins. Annu Rev Biophys Biomol Struct 29:183–212

  • Xia J, Yamaji N, Kasai T (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci 107:18381–18385

    CAS  Google Scholar 

  • Xia JX, Yamaji N, Ma JF (2013) A plasma membrane-localized small peptide is involved in Al tolerance in rice. Plant J 76:345–355

    CAS  PubMed  Google Scholar 

  • 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 101:162–172

    CAS  PubMed  Google Scholar 

  • 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 21:3339–3349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2010) Isolation and characterisation of two MATE genes in rye. Funct Plant Biol 37: 296–303

    CAS  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 69:1061–1069

    Google Scholar 

  • 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 57:976–985

    CAS  PubMed  Google Scholar 

Download references

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 information

Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Hua Zhao.

Additional information

Responsible Editor: Juan Barcelo

Electronic supplementary material

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)

Table S1

(DOCX 24 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)

Table S3

(XLSX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, H., Huang, W., Zhang, Y. et al. Natural variation of CsSTOP1 in tea plant ( Camellia sinensis ) related to aluminum tolerance . Plant Soil 431, 71–87 (2018). https://doi.org/10.1007/s11104-018-3746-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3746-y

Keywords

Navigation