Skip to main content
SpringerLink
Log in

Impact of heavy metal stresses on the growth and auxin homeostasis of Arabidopsis seedlings

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

The phytohormone auxin is an essential mediator in many aspects of plant development. Its dynamic and differential distribution within the plant is regulated by a variety of environmental cues including heavy metal stimuli. In the present study, we first evaluated the toxic effects of seven heavy metals including Pb2+, Cd2+, Hg2+, Ni2+. Zn2+, Co2+ and Cu2+ in their excess on the model plant, Arabidopsis thaliana. Various morphological defects including loss in fresh weight and leaf area, decrease of the primary root length and stimulation of the lateral root density occurred to a different extent among seven heavy metals. Next, using an indicative DR5:GUS reporter line of Arabidopsis, the auxin accumulation and distribution within plant seedlings were found to be dramatically and differentially affected by these heavy metals. We further analyzed the transcriptional changes of 27 selected auxin homeostasis-related genes by qRT-PCR technique and found that upon various heavy metals, the expressions of the candidate genes were distinctly altered in shoots and roots. Our data indicated that when confronted with excessive heavy metals, plants could dynamically and differentially regulate the transcription of auxin-related genes to adjust the location and effective accumulation of auxin within the plant for better adaptation and survival under the adverse environment.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97:883–893

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Andres-Colas N, Sancenon V, Rodriguez-Navarro S, Mayo S, Thiele DJ, Ecker JR, Puig S, Penarrubia L (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236

    Article  CAS  PubMed  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332

    Article  CAS  PubMed  Google Scholar 

  • Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J et al (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798

    Article  CAS  PubMed  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci U S A 105:8790–8794

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eren E, Arguello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P(IB)-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jurgens G et al (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673

    Article  CAS  PubMed  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  CAS  PubMed  Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hillebrand H, Bartling D, Weiler EW (1998) Structural analysis of the nit2/nit1/nit3 gene cluster encoding nitrilases, enzymes catalyzing the terminal activation step in indole-acetic acid biosynthesis in Arabidopsis thaliana. Plant Mol Biol 36:89–99

    Article  CAS  PubMed  Google Scholar 

  • Jones B, Ljung K (2012) Subterranean space exploration: the development of root system architecture. Curr Opin Plant Biol 15:97–102

    Article  PubMed  Google Scholar 

  • Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H (2005) VAN3 ARF–GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132:1699–1711

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Bae H, Jeong J, Lee JY, Yang YY, Hwang I, Martinoia E, Lee Y (2003) Functional expression of a bacterial heavy metal transporter in Arabidopsis enhances resistance to and decreases uptake of heavy metals. Plant Physiol 133:589–596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  CAS  PubMed  Google Scholar 

  • Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 34:321–342

    Article  CAS  Google Scholar 

  • Maraschin Fdos S, Memelink J, Offringa R (2009) Auxin-induced, SCF(TIR1)-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59:100–109

    Article  PubMed  Google Scholar 

  • Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci U S A 108:18512–18517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, Skupa P, Chand S, Benkova E, Zazimalova E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614

    Article  CAS  PubMed  Google Scholar 

  • Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2:a001594

    Article  PubMed Central  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D et al (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pasternak T, Rudas V, Potters G, Jansen MAK (2005) Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ Exp Bot 53:299–314

    Article  Google Scholar 

  • Paulose B, Chhikara S, Coomey J, Jung HI, Vatamaniuk O, Dhankher OP (2013) A gamma-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25:4580–4595

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peto A, Lehotai N, Lozano-Juste J, Leon J, Tari I, Erdei L, Kolbert Z (2011) Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann Bot 108:449–457

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Jansen MA (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169

    Article  PubMed  Google Scholar 

  • Rose AB, Casselman AL, Last RL (1992) A phosphoribosylanthranilate transferase gene is defective in blue fluorescent Arabidopsis thaliana tryptophan mutants. Plant Physiol 100:582–592

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rosquete MR, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786

    Article  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P et al (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • Scarpella E, Barkoulas M, Tsiantis M (2010) Control of leaf and vein development by auxin. Cold Spring Harb Perspect Biol 2:a001511

    Article  PubMed Central  PubMed  Google Scholar 

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121:1179–1190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    Article  CAS  PubMed  Google Scholar 

  • Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 106:5430–5435

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Vorwerk S, Biernacki S, Hillebrand H, Janzik I, Muller A, Weiler EW, Piotrowski M (2001) Enzymatic characterization of the recombinant Arabidopsis thaliana nitrilase subfamily encoded by the NIT2/NIT1/NIT3-gene cluster. Planta 212:508–516

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Tiwari SB, Hagen G, Guilfoyle TJ (2005) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17:1979–1993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Whippo CW, Hangarter RP (2006) Phototropism: bending towards enlightenment. Plant Cell 18:1110–1119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130

    Article  CAS  PubMed  Google Scholar 

  • Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A 108:18518–18523

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu J, Yin H, Liu X, Li X (2010) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor ShuZhen Men (Nankai University, China) for kindly donating DR5:GUS Arabidopsis seeds. This study was funded by Key Projects in the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (2012BAC07B02), National Transgenic Major Project (2014ZX08004-004B) and Tianjin Research Program of Application Foundation and Advanced Technology (13JCQNJC14500).

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, Tianjin University, Weijin Road 92, Nankai District, Tianjin, 300072, China

    Rui Wang, Jiehua Wang, Lin Zhao, Shaohui Yang & Yingjin Song

Authors
  1. Rui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiehua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shaohui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yingjin Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiehua Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, R., Wang, J., Zhao, L. et al. Impact of heavy metal stresses on the growth and auxin homeostasis of Arabidopsis seedlings. Biometals 28, 123–132 (2015). https://doi.org/10.1007/s10534-014-9808-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-014-9808-6

Keywords

Search

Navigation