Skip to main content
Log in

Plant hormone signaling and modulation of DNA repair under stressful conditions

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

The role played by phytohormone signaling in the modulation of DNA repair gene and the resulting effects on plant adaptation to genotoxic stress are poorly investigated. Information has been gathered using the Arabidopsis ABA (abscisic acid) overly sensitive mutant abo4-1, defective in the DNA polymerase ε function that is required for DNA repair and recombination. Similarly, phytohormone-mediated regulation of the Ku genes, encoding the Ku heterodimer protein involved in DNA repair, cell cycle control and telomere homeostasis has been demonstrated, highlighting a scenario in which hormones might affect genome stability by modulating the frequency of homologous recombination, favoring plant adaptation to genotoxic stress. Within this context, the characterisation of Arabidopsis AtKu mutants allowed disclosing novel connections between DNA repair and phytohormone networks. Another intriguing aspect deals with the emerging correlation between plant defense response and the mechanisms responsible for genome stability. There is increasing evidence that systemic acquired resistance (SAR) and homologous recombination share common elements represented by proteins involved in DNA repair and chromatin remodeling. This hypothesis is supported by the finding that volatile compounds, such as methyl salicylate (MeSA) and methyl jasmonate (MeJA), participating in the plant-to-plant communication can trigger genome instability in response to genotoxic stress agents. Phytohormone-mediated control of genome stability involves also chromatin remodeling, thus expanding the range of molecular targets. The present review describes the most significant advances in this specific research field, in the attempt to provide a better comprehension of how plant hormones modulate DNA repair proteins as a function of stress.

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.

Fig. 1

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

AP:

Apurinic/apyrimidinic site

At:

Arabidopsis thaliana

BER:

Base excision repair

CRC:

Chromatin remodeling complex

DSB:

Double strand break

GA:

Gibberellic acid

HR:

Homologous recombination

HRF:

Homologous recombination frequency

JA:

Jasmonic acid

MeSA:

Methyl salicylate

MeJA:

Methyl Jasmonate

NER:

Nucleotide excision repair

NHEJ:

Nonhomologous end joining

PCD:

Programmed cell death

PR:

Pathogenesis related

ROS:

Reactive oxygen species

SA:

Salicylic acid

SAR:

Systemic acquired resistance

SRS:

Systemic recombination signal

SSB:

Single strand break

SWS:

Systemic wound signal

References

  • Achary VMM, Panda BB (2010) Aluminium-induced DNA damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates. Mutagenesis 25:201–209

    Article  Google Scholar 

  • Achary VMM, 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 Genet Toxicol Environ Mutagen 751:130–138

    Article  CAS  Google Scholar 

  • Ahmad A, Zhang Y, Cao X-F (2010) Decoding the epigenetic language of plant development. Mol Plant 3:719–728

    Article  CAS  PubMed  Google Scholar 

  • Al-Rumaih MM (2007) The radio-protective role of gibberellic acid on nucleic acid metabolism in three species of senna. J Food Agric Environ 5:359–362

    CAS  Google Scholar 

  • Balestrazzi A, Locato V, Bottone MG, De Gara L, Biggiogera M, Pellicciari C, Botti S, Di Gesù D, Donà M, Carbonera D (2010) Response to UV-C radiation in topo I-deficient carrot cells with low ascorbate levels. J Exp Bot 61:575–585

    Article  CAS  PubMed  Google Scholar 

  • Balestrazzi A, Confalonieri M, Macovei A, Carbonera D (2011) Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity. Plant Cell Rep 30:287–295

    Article  CAS  PubMed  Google Scholar 

  • Balestrazzi A, Confalonieri M, Macovei A, Carbonera D (2012) Genotoxic stress, DNA repair, and crop productivity. In: Tuteja N, Gill SS (eds) Crop improvement under adverse conditions. Springer-Verlag, Berlin (in press)

    Google Scholar 

  • Bissenbaev AK, Ishchenko AA, Taipakova SM, Saparbaev MK (2011) Presence of base excision repair enzymes in the wheat aleurone and their activation in cells undergoing programmed cell death. Plant Physiol Biochem 49:1155–1164

    Article  CAS  PubMed  Google Scholar 

  • Boyko A, Kovalchuck I (2011) Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective. Mol Plant 4:1014–1023

    Article  CAS  PubMed  Google Scholar 

  • Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I et al (2007) Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability). Nucleic Acids Res 35:1714–1725

    Article  CAS  PubMed  Google Scholar 

  • Bundock P, van Attikum H, Hoykaas P (2002) Increased telomere length and hypersensitivity to DNA damaging agents in an Arabidopsis KU70 mutant. Nucleic Acids Res 30:3395–3400

    Article  CAS  PubMed  Google Scholar 

  • Dominguez F, Moreno J, Cejudo FJ (2004) A gibberellin-induced nuclease is localised in the nucleus of wheat aleurone cells undergoing programmed cell death. J Biol Chem 279:11530–11536

    Article  CAS  PubMed  Google Scholar 

  • Dong L, Wen J, Pier E, Zhang X, Zhang B, Dong F, Ziegler N, Mysz M, Armenta R, Cui R (2013) Melanocyte-stimulating hormone directly enhances UV-induced DNA repair in keratinocytes by a Xeroderma Pigmentosum group A-dependent mechanisms. Cancer Res 70:3547–3556

    Article  Google Scholar 

  • Downs JA, Jackson SP (2004) A means to a DNA end: the many roles of Ku. Nat Rev Mol Cell Biol 5:367–378

    Article  CAS  PubMed  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Durrant WE, Wang S, Dong X (2007) Arabidopsis SNI1 and RAD51D regulated both gene transcription and DNA recombination during the defense response. Proc Natl Acad Sci USA 104:4223–4227

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716

    Article  CAS  PubMed  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  CAS  PubMed  Google Scholar 

  • Filkenstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45

    Google Scholar 

  • Filkowski J, Kovalchuk O, Kovalchuk I (2004) Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant J 38:60–69

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Marusaka Y et al (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gallego ME, Jalut N, White CI (2003) Telomerase dependence of telomere lengthening in Ku80 mutant Arabidopsis. Plant Cell 15:782–789

    Article  CAS  PubMed  Google Scholar 

  • Gichner T, Menke M, Strareva DA, Schubert I (2000) Maleic hydrazide induces genotoxic effects but no DNA damage detectable by the comet assay to tobacco and field beans. Mutagenesis 15:385–389

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Haffner MC, De Marzo AM, Meeker AK, Nelson WG, Yegnasubramanian S (2011) Transcription-induced DNA double strand breaks: both oncogenic force and potential therapeutic target? Clin Cancer Res 17:3858–3864

    Article  CAS  PubMed  Google Scholar 

  • Halazonetis TD, Gorgoulis VG, Bartek J (2008) An oncogene-induced DNA damage model for cancer development. Science 319:1352–1355

    Article  CAS  PubMed  Google Scholar 

  • Han P, Li Q, Zhu YX (2008) Mutation of Arabidopsis BARD1 causes meristem defects by failing to confine WUSCHEL expression to the organizing center. Plant Cell 20:1482–1493

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Silva Bruno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472

    Article  CAS  PubMed  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • Hu Y (2009) BRCA1, hormone, and tissue-specific tumor suppression. Int J Biol Sci 5:20–27

    Article  CAS  PubMed  Google Scholar 

  • Jenik PD, Jurkuta RE, Barton MK (2005) Interactions between the cell cycle and embryonic patterning in Arabidopsis uncovered by a mutation in DNA polymerase epsilon. Plant Cell 17:3362–3377

    Article  CAS  PubMed  Google Scholar 

  • Jensen RB, Carreira A, Kowalczykowski SC (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467:678–683

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kathiria P, Sidees C, Golubov A, Kalischuk M, Kawchuk LM et al (2010) Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol 153:1859–1870

    Article  CAS  PubMed  Google Scholar 

  • Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144:336–346

    Article  CAS  PubMed  Google Scholar 

  • Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J et al (2003) Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:760–762

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    Article  CAS  PubMed  Google Scholar 

  • Li H, Luan S (2011) The cyclophilin AtCYP71 interacts with CAF-1 and LHP1 and functions in multiple chromatin remodeling processes. Mol Plant 4:748–758

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, trough a screen for suppressors of npr1-1. Cell 98:329–339

    Article  CAS  PubMed  Google Scholar 

  • Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128:707–719

    Article  CAS  PubMed  Google Scholar 

  • Liu PF, Chang WC, Wang YK, Munisamy SB, Hsu SH et al (2008a) Differential regulation of Ku gene expression in etiolated mungbean hypocotyls by auxins. Biochem Biophys Acta 1769:443–454

    Google Scholar 

  • Liu PF, Wang YK, Chang WC, Chang HY, Pan RL (2008b) Regulation of Arabidopsis thaliana Ku genes at different developmental stages under heat stress. Biochim Biophys Acta 1779:402–407

    Article  CAS  PubMed  Google Scholar 

  • Liu ZQ, Gao J, Dong AW, Shen WH (2009) A truncated Arabidopsis NUCLEOSOME ASSEMBLY PROTEIN 1, AtNAP1;3T, alters plant growth responses to abscisic acid and salt in the Atnap1;3-2 mutant. Mol Plant 2:688–699

    Google Scholar 

  • Lumba S, Cutler S, McCourt P (2010) Plant nuclear hormone receptors: a role for small molecules in protein–protein interactions. Annu Rev Cell Dev Biol 26:445–469

    Article  CAS  PubMed  Google Scholar 

  • Machaiah JP, Vakie UK, Sreenivasan A (1976) The effects of gamma irradiation on biosynthesis of gibberellins in germinating wheat. Environ J Exp Bot 16:131–140

    Article  CAS  Google Scholar 

  • Macovei A, Balestrazzi A, Confalonieri M, Carbonera D (2010) The Tdp1 (Tyrosyl-DNA phosphodiesterase) gene family in barrel medic (Medicago truncatula Gaertn.): bioinformatic investigation and expression profiles in response to copper- and PEG-mediated stress. Planta 232:393–407

    Article  CAS  PubMed  Google Scholar 

  • Macovei A, Balestrazzi A, Confalonieri M, Buttafava A, Carbonera D (2011) The TFIIS and TFIIS-like genes from Medicago truncatula are involved in oxidative stress response. Gene 470:20–30

    Article  CAS  PubMed  Google Scholar 

  • March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio FJ et al (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53:475–487

    Article  CAS  PubMed  Google Scholar 

  • Merkel P, Khoury N, Bertolotto C, Perfetti C (2003) Insulin and glucose regulate the expression of the DNA repair enzyme XPD. Mol Cell Endocrinol 201:75–85

    Article  CAS  PubMed  Google Scholar 

  • Mostoslavsky R (2008) DNA repair, insulin signaling and sirtuins: at the crossroad between cancer and aging. Front Biosci 13:6966–6990

    Article  CAS  PubMed  Google Scholar 

  • Murfett J, Wang XJ, Hagen G, Guilfoyle TJ (2001) Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13:1047–1061

    CAS  PubMed  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 23:13839–13844

    Article  Google Scholar 

  • Panda BB, Panda KK (2002) Genotoxicity and mutagenicity of heavy metals in plants. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal tolerance in plants. Kluwer, Amsterdam, pp 395–414

    Google Scholar 

  • Patra J, Sahoo MK, Panda BB (2005) Salicylic acid triggers genotoxic adaptation to methyl mercuric chloride and ethyl methane sulfonate, but not to maleic hydrazide in root meristem cells of Allium cepa L. Mutat Res 581:173–180

    Article  CAS  PubMed  Google Scholar 

  • Perruc E, Knoshita NI, Lopez-Molina L (2007) The role of chromatin-remodeling factor PKL in balancing osmotic stress responses during Arabidopsis seed germination. Plant J 52:927–936

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Develop Biol 28:489–521

    Article  CAS  Google Scholar 

  • Pospiech H, Syvaoja JE (2003) DNA polymerase ε-more than a polymerase. Sci World J 3:87–104

    Article  CAS  Google Scholar 

  • Puizina J, Siroky J, Mokros P, Schweizer D, Riha K (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–1978

    Article  CAS  PubMed  Google Scholar 

  • Riha K, Shippen DE (2003) Ku is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis. Proc Natl Acad Sci USA 100:611–615

    Article  CAS  PubMed  Google Scholar 

  • Riha K, Watson JM, Parkey J, Shippen DE (2002) Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J 21:2819–2826

    Article  CAS  PubMed  Google Scholar 

  • Ritchie S, Swanson SJ, Gilroy S (2000) Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cellular and molecular biology. Seed Sci Res 10:193–212

    CAS  Google Scholar 

  • Roth N, Klimesch J, Dukowic-Schulze S, Pacher M, Mannuss A et al (2012) The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells. Plant J 72:781–790

    Article  CAS  PubMed  Google Scholar 

  • Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB1-SW13B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. The Plant Cell 20:2972–2988

    Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Leon-Kloosterziel KM, Korneef M, Zeevaart JA (1997) Biochemical characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol 114:161–166

    Article  CAS  PubMed  Google Scholar 

  • Shen W-H, Xu L (2009) Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana. Mol Plant 2:600–609

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Singh DP, Moore CA, Gilliland A, Carr JP (2004) Activation of multiple antiviral defence mechanisms by salicylic acid. Mol Plant Pathol 5:57–63

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, Mou Z, Tada Y, Spivev NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–872

    Article  CAS  PubMed  Google Scholar 

  • Sridha S, Wu K (2006) Identification of Arabidopsis thaliana HD2C as a novel regulator of abscisic acid response in Arabidopsis. The Plant J 46:124–133

    Article  CAS  Google Scholar 

  • Stivers JT, Jiang YL (2003) A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem Rev 103:2729–2759

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Adachi Y, Chiba K, Oguchi K, Takahashi H (2002) Identification of Ku70 and Ku80 homologues in Arabidopsis thaliana: evidence for a role in repair of double strand breaks. Plant J 29:771–781

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522

    Article  CAS  PubMed  Google Scholar 

  • Trapp O, Seeliger K, Puchta H (2011) Homolog of breast cancer genes in plants. Front Plant Sci 2:19

    Article  CAS  PubMed  Google Scholar 

  • Trewavas A (2003) Aspects of plant intelligence. Ann Bot 92:1–20

    Article  CAS  PubMed  Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164

    CAS  PubMed  Google Scholar 

  • Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage repair and DNA repair helicases. Mutat Res 681:134–149

    Article  CAS  PubMed  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–208

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Durrant WE, Song J, Spivey NW, Dong X (2010) Arabidopsis BRCA2 and RAD51 proteins are specifically involved in defense transcription during plant immune responses. Proc Natl Acad Sci USA 107:22716–22721

    Article  CAS  PubMed  Google Scholar 

  • Weber W, Daoud-El Baba M, Fussenegger M (2007) Synthetic ecosystems based on airborne inter and intra-kingdom communication. Proc Natl Acad Sci USA 104:10435–10440

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Danna CH, Zemp FJ, Titov V, Ciftci ON et al (2011) UV-C-irradiated Arabidopsis and tobacco emit volatiles that trigger genomic instability in neighboring plants. Plant Cell 23:3842–3852

    Article  CAS  PubMed  Google Scholar 

  • Yin H, Zhang X, Liu Y, Wang Y, He J et al (2009) Epigenetic regulation, somatic homologous recombination, and abscisic acid signaling are influenced by DNA polymerase ε mutation in Arabidopsis. Plant Cell 21:388–402

    Google Scholar 

  • Zharkov DO (2008) Base excision DNA repair. Cell Mol Life Sci 65:1544–1565

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu J-K, Hasegawa PM, Bohnert HJ, Shi H, Yun D-J, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105:4945–4950

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by Fondo di Ateneo per la Ricerca-University of Pavia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alma Balestrazzi.

Additional information

Communicated by P. Kumar.

A contribution to the Special Issue: Plant Hormone Signaling.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Donà, M., Macovei, A., Faè, M. et al. Plant hormone signaling and modulation of DNA repair under stressful conditions. Plant Cell Rep 32, 1043–1052 (2013). https://doi.org/10.1007/s00299-013-1410-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1410-9

Keywords

Navigation