Skip to main content

Aluminum-Dependent Root Growth Inhibition as Mediated by DNA-Damage Responses

  • Chapter
Aluminum Stress Adaptation in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 24))

Abstract

Aluminum (Al) toxicity is a global agricultural problem that reduces crop yields primarily due to root growth inhibition. Several advances in our knowledge of Al resistance mechanisms have recently been made through studies of Al exclusion, yet due to the complicated nature of studying internalized Al, it has proven difficult to determine the biochemical basis of Al toxicity and tolerance. Recent studies show that Al triggers a DNA-damage response mediated by the cell cycle checkpoint ATAXIA TELANGIECTASIA MUTATED AND RAD3-RELATED (ATR). This is an active process that forces terminal differentiation of the root meristem and is at least in part the cause of stoppage of root growth following chronic exposure to Al. Interestingly, unlike well-studied stressors like IR or gamma (γ) radiation, Al is a real world genotoxic stress that represents a novel system for analysis of DNA damage in biological systems under environmentally relevant conditions. Understanding DNA-damage response and repair pathways following Al treatment in plant systems can offer more effective and safer agricultural practices but also begs to serve as a beacon of caution about Al as a genotoxic stress in other organisms since the cell cycle checkpoint machinery that has been attributed to Al responses is universally found in eukaryotes.

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

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Achary VM, Parinandi NL, Panda BB (2013) Calcium channel blockers protect against aluminium-induced DNA damage and block adaptive response to genotoxic stress in plant cells. Mutat Res 751(2):130–138

    Article  CAS  PubMed  Google Scholar 

  • Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, Kondou Y, Kaminuma E, Kawashima M, Toyoda T, Matsui M, Kurihara D, Matsunaga S, Umeda M (2011) Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci U S A 108:10004–10009

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aklilu BB, Soderquist RS, Culligan KM (2013) Genetic analysis of the Replication Protein A large subunit family in Arabidopsis reveals unique and overlapping roles in DNA repair, meiosis and DNA replication. Nucleic Acids Res 42:1–15

    Google Scholar 

  • Andersson M (1988) Toxicity and tolerance of aluminum in vascular plants: a literature review. Water Air Soil Pollut 39:439–462

    CAS  Google Scholar 

  • Barceló J, Poschenrieder C (2002) Fast root growth responses root exudates and internal detoxification as clues to the mechanisms of aluminum toxicity and resistance: a review. Environ Exper Bot 48:75–92

    Article  Google Scholar 

  • Biedermann S, Hellmann H (2010) The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J 62:404–415

    Article  CAS  PubMed  Google Scholar 

  • Chandran D, Sharopova N, Ivashuta S, Gantt JS, Vandenbosch KA, Samac DA (2008) Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta 228:151–166

    Article  CAS  PubMed  Google Scholar 

  • Cortez D, Guntuku S, Qin J, Elledge SJ (2001) ATR and ATRIP: partners in checkpoint signaling. Science 294:867–870

    Article  Google Scholar 

  • Culligan KM, Britt AB (2008) Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. Plant J 4:629–638

    Article  Google Scholar 

  • Culligan KM, Robertson CE, Foreman J, Doerner P, Britt AB (2006) ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J 48:947–961

    Article  CAS  PubMed  Google Scholar 

  • De Boni U, Scott JW, Crapper DR (1974) Intracellular aluminum binding; a histochemical study. Histochemistry 40:31–37

    Article  PubMed  Google Scholar 

  • Degenhardt J, Larsen PB, Howell SH, Kochian LV (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiol 117:19–27

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702

    PubMed Central  CAS  PubMed  Google Scholar 

  • Edwards RJ, Bently NJ, Carr AM (1999) A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint protein. Nat Cell Biol 1:393–398

    Article  CAS  PubMed  Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127:918–927

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • FitzPatrick EA (1986) An introduction to soil science. Longman Scientific and Technical, Essex, 255 pp

    Google Scholar 

  • Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–566

    Article  CAS  Google Scholar 

  • Gabrielson KM, Cancel JD, Morua LF, Larsen PB (2006) Identification of dominant mutations that confer increased aluminium tolerance through mutagenesis of the Al-sensitive Arabidopsis mutant, als3-1. J Exp Bot 57:943–951

    Article  CAS  PubMed  Google Scholar 

  • Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci U S A 103:9738–9743

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M (1999) Does aluminum inhibit root growth of maize through interaction with the cell wall, plasma membrane, cytoskeleton continuum? Plant Soil 192:23–30

    Article  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karlik SJ, Eichhorn GL, Lewis PN, Crapper DR (1980) Interaction of aluminum species with deoxyribonucleic acid. Biochemistry 19:5991–5998

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumari M, Taylor GJ, Deyholos MK (2008) Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Mol Genet Genom 279:339–357

    Article  CAS  Google Scholar 

  • Larsen PB, Tai C-Y, Kochian LV, Howell SH (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol 110:743–751

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larsen PB, Kochian LV, Howell SH (1997) Al inhibits both shoot development and root growth in als3, an al sensitive Arabidopsis mutant. Plant Physiol 114:1207–1214

    PubMed Central  CAS  PubMed  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20:152–167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 4:383–390

    Article  Google Scholar 

  • Macdonald TL, Martin RB (1988) Aluminum ion in biological systems. Trends Biochem Sci 13:15–19

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H (1988) Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminum. Soil Sci Plant Nutr 34:499–506

    Article  CAS  Google Scholar 

  • Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminum tolerance in snapbeans: root exudation of citric acid. Plant Physiol 96:737–743

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nezames CD, Sjogren CA, Barajas JF, Larsen PB (2012a) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell 24:608–621

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nezames CD, Ochoa V, Larsen PB (2012b) Mutational loss of Arabidopsis SLOW WALKER2 results in reduced endogenous spermine concomitant with increased aluminum sensitivity. Funct Plant Biol 40:67–78

    Article  Google Scholar 

  • Preuss SB, Britt AB (2003) A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genetics 164:323–334

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reynolds MP, Ortiz-Monasterio JI, McNab A (eds) (2001) Application of physiology in wheat breeding. CIMMYT, Mexico

    Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116(1):409–418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rounds MA, Larsen PB (2008) Aluminum dependent root growth inhibition results from AtATR dependent cell cycle arrest and loss of the quiescent center in Arabidopsis. Curr Biol 18:1495–1500

    Article  CAS  PubMed  Google Scholar 

  • Rouse J, Jackson SP (2000) An essential gene involved in checkpoint control and regulation of the MEC1 signaling pathway in Saccharomyces cerevisiae. EMBO J 19:5801–5812

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saijo M (2013) The role of Cockayne syndrome group A (CSA) protein in transcription-coupled nucleotide excision repair. Mech Ageing Dev 134:196–201

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto AN, Lan VT, Puripunyavanich V, Hase Y, Yokota Y, Shikazono N, Nakagawa M, Narumi I, Tanaka A (2009) A UVB-hypersensitive mutant in Arabidopsis thaliana is defective in the DNA damage response. Plant J 60:509–517

    Article  CAS  PubMed  Google Scholar 

  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39–85

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    Article  CAS  PubMed  Google Scholar 

  • Siede W, Kow YW, Doetsch PW (2006) DNA damage recognition. Taylor & Francis, New York, NY

    Google Scholar 

  • Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123:543–552

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sweeney PR, Britt AB, Culligan KM (2009) The Arabidopsis ATRIP ortholog is required for a programmed response to replication inhibitors. Plant J 60:518–526

    Article  CAS  PubMed  Google Scholar 

  • Tyler G, Berggren D, Bergkvist B, Falkengren-Grerup U, Folkeson L, Rühling Å (1987) In: Hutchinson TC, Meema KM (eds) Effects of atmospheric pollutants on forests, wetlands and agricultural ecosystems. NATO ASI series G16. Springer, Berlin, 347 pp

    Google Scholar 

  • Wissemeir AH, Klotz F, Horst WJ (1987) Aluminum induced callose synthesis in roots of soybean (Glycine max L.). J Plant Physiol 129:487–492

    Article  Google Scholar 

  • Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. PNAS USA 107:18381–18385

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshiyama K, Conklin PA, Huefner ND, Britt AB (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. PNAS USA 106:12843–12848

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshiyama KO et al (2013a) ATM-mediated phosphorylation of SOG1. EMBO Rep 14(9):817–822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshiyama KO, Sakaguchi K, Kimura S (2013b) DNA damage response in plants: conserved and variable response compared to animals. Biology 2:1338–1356

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul B. Larsen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sjogren, C.A., Larsen, P.B. (2015). Aluminum-Dependent Root Growth Inhibition as Mediated by DNA-Damage Responses. In: Panda, S., Baluška, F. (eds) Aluminum Stress Adaptation in Plants. Signaling and Communication in Plants, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-319-19968-9_3

Download citation

Publish with us

Policies and ethics