Skip to main content
SpringerLink
Log in

Stress, Mutators, Mutations and Stress Resistance

  • Chapter
  • First Online:
Abiotic Stress Adaptation in Plants

Summary

Organisms need genetic mechanisms to rapidly adapt to changing, stressful environments. Having a high mutation frequency would have a drag on a population due to the deleterious nature of mutations, but having a sub-population with high mutation rate due to the presence of mutator genes seems to be nature’s solution. Far more is known about mutator genes in bacteria than in higher organisms. Mutator effects can be genetic, through mutations in genes that affect genome stability or it can be epigenetic through up- or down-regulation of these genes. The mutator genes can be genes with partially lost function, which deal with DNA replication or repair, or with detoxification of DNA-damaging cellular components. Transposons, which are sensitive to environmental stress, can also act as mutators in plants. Mutators can be constitutive or stress-induced. Most evidence for mutator-assisted evolution of stress resistance in plants is circumstantial, except for the evolution of atrazine herbicide resistance due to a nuclearly-inherited plastome mutator, which was repeated experimentally. An important feature of the mutator effect is that it is transient and is followed by reversion to the stable wild type, and can be counter-selected following outcrossing with the wild type. Similarly, “remembered” epigenetic stress-induced mutator effects were shown to last for a few generations. In summary, mutator genes could be playing an important role in the evolution of resistance to stress in plants, as it does in other systems, but to an extent that is yet unclear.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Abbreviations

HPPD:

hydroxyl phenyl-pyruvate-dioxygenase

MULE:

Mu-like elements

SLAM:

stress lifestyle-assisted mutations

References

  • Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackensie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous toi MutS. Proc Natl Acad Sci USA 100:5968-5973

    Article  PubMed  CAS  Google Scholar 

  • Arntzen CJ, Duesing JH (1983) Chloroplast-encoded herbicide resistance. In: Ahmand F, Downey K, Schultz J, Voellmy RW (eds) Advances in gene technology. Academic Press, New York, pp 273-299

    Google Scholar 

  • Boe L, Danielsen M, Knudsen S, Petersen JB, Maymann J, Jensen PR (2000) The frequency of mutators in populations of Escherichia coli. Mutat Res 448:47-55

    Article  PubMed  CAS  Google Scholar 

  • Boyko A, Filkowski J, Kovalchuk I (2005) Homologous recombination in plants is temperature- and day-length dependent. Mutat Res - Fundam Mol Mech Mutagen 572:73-83

    Article  CAS  Google Scholar 

  • Bray CM, West CE (2005) DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity. New Phytol 168:511-528

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603-608

    Article  CAS  Google Scholar 

  • Byrne M, Taylor WC (1996) Analysis of mutator-induced mutations in the iojap gene of maize. Mol Gen Genet 252:216-220

    PubMed  CAS  Google Scholar 

  • Crow JF (1957) Genetics of insect resistance to chemicals. Ann Rev Entomol 2:227-246

    Article  CAS  Google Scholar 

  • Cunliffe K (2005) The ryegrass complex. In: Gressel J (ed) Crop ferality and volunteerism. CRC Press, Boca Raton, FL, pp 236-242

    Google Scholar 

  • Diao XM, Freeling M, Lisch D (2006) Horizontal transfer of a plant transposon. PLoS Biol 4:119-128

    Article  CAS  Google Scholar 

  • Dominguez O, Ruiz JF, de Lera TL, Garcia-Diaz M, Gonzalez MA, Kirchhoff T, Martinez AC, Bernad A, Blanco L (2000) DNA polymerase mu (Pol mu), homologous to TdT, could act as a DNA mutator in eukaryotic cells. EMBO J 19:1731-1742

    Article  PubMed  CAS  Google Scholar 

  • Ducruet JM, Gasquez J (1978) Observation of whole leaf fluorescence and demonstration of chloroplastic resistance to atrazine in Chenopodium album L. and Poa annua L. Chemosphere 8:695-699

    Google Scholar 

  • Duesing JH (1983) Genetic analysis of herbicide resistance. Proc North Central Weed Control Conf 38:143-147

    Google Scholar 

  • Fernandes J, Dong QF, Schneider B, Morrow DJ, Nan GL, Brendel V, Walbot V (2004) Genome-wide mutagenesis of Zea mays L. using RescueMu transposons. Genome Biol 5(10):R82

    Google Scholar 

  • Friedberg EC, Gerlach VL (1999) Novel DNA polymerases offer clues to the molecular basis of mutagenesis. Cell 98:413-416

    Article  PubMed  CAS  Google Scholar 

  • Funchain P, Yeung A, Stewart JL, Lin R, Slupska MM, Miller JH (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154:959-970

    PubMed  CAS  Google Scholar 

  • Gardner SN, Gressel J, Mangel M (1998) A revolving dose strategy to delay the evolution of both quantitative vs. major monogene resistances to pesticides and drugs. Intl J Pest Manag 44:161-180

    Article  CAS  Google Scholar 

  • Gressel J (2002) Molecular biology of weed control. Taylor & Francis, London

    Google Scholar 

  • Gressel J, Segel LA (1978) The paucity of genetic adaptive resistance of plants to herbicides: possible biological reasons and implications. J Theor Biol 75:349-371

    Article  PubMed  CAS  Google Scholar 

  • Gressel J, Segel LA (1982) Interrelating factors controlling the rate of appearance of resistance: The outlook for the future. In: Le Baron H, Gressel J (eds) Herbicide resistance in plants. Wiley, New York, pp 325-347

    Google Scholar 

  • GuhaMajumdar M, Baldwin S, Sears BB (2004) Chloroplast mutations induced by 9-aminoacridine hydrochloride are independent of the plastome mutator in Oenothera. Theor Appl Genet 108:543-549

    Article  PubMed  CAS  Google Scholar 

  • Hagemann R (1971) Struktur und funktion der genetischen information in den PlastidenI. Die Bedentung fon Pladtiden mutanten unddoe genetische nomenklatur extranucleauer mutationen. Biol Zentralblatt 90:409-418

    CAS  Google Scholar 

  • Harfe BD, Jinks-Robertson S (2000) Mismatch repair proteins and mitotic genome stability. Mutat Res 451:151-167

    Article  PubMed  CAS  Google Scholar 

  • Heap IM (1988) Resistance to herbicides in annual ryegrass (Lolium rigidum). Ph.D. Thesis, University Waite Agriculture Institute, Adelaide

    Google Scholar 

  • Heap IM (2008) International survey of herbicide-resistant weeds. http://www.weedscience.org

    Google Scholar 

  • Hoffman PD, Leonard JM, Lindberg GE, Bollmann SR, Hays JB (2004) Rapid accumulation of mutations during seed-to-seed propagation of mismatch-repair-defective Arabidopsis. Genes Dev 18:2676-2685

    Article  PubMed  CAS  Google Scholar 

  • Horst JP, Wu TH, Marinus MG (1999) Escherichia coli mutator genes. Trends Microbiol 7:29-36

    Article  PubMed  CAS  Google Scholar 

  • Hughes A (1999) Adaptive evolution of genes and genomes. Oxford University Press, Oxford

    Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102-106

    Article  PubMed  CAS  Google Scholar 

  • Kovalchuk I, Kovalchuk O, Hohn B (2000) Genome-wide variation of the somatic mutation frequency in transgenic plants. EMBO J 19:4431-4438

    Article  PubMed  CAS  Google Scholar 

  • Kovalchuk I, Kovalchuk O, Hohn B (2001) Biomonitoring the genotoxicity of environmental factors with transgenic plants. Trends Plant Sci 6:306-310

    Article  PubMed  CAS  Google Scholar 

  • LeClerc JE, Li B, Payne WL, Cebula TA (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274:1208-1211

    Article  PubMed  CAS  Google Scholar 

  • LeClerc JE, Paynes WL, Kupchella E, Cebula TA (1998) Detection of mutator subpopulations in Salmonella typhimurium LT2 by reversion of his alleles. Mutat Res 400:89-97

    Article  PubMed  CAS  Google Scholar 

  • Lederberg J, Lederberg E (1952) Replicate plating and indirect selection of bacterial mutants. J Bact 63:399-406

    PubMed  CAS  Google Scholar 

  • Lee TC, Tanaka N, Lamb PW, Gilmer TM, Barrett JC (1988) Induction of gene amplification by arsenic. Science 241:79-81

    Article  PubMed  CAS  Google Scholar 

  • Letouze A, Gasquez J (2003) Ebhanced activity of several herbicide-degrading enzymes: a suggested mechanism responsible for multiple resistance in blackgrass (Alopecurus myosuroides Huds.). Agronomie 23:601-608

    Google Scholar 

  • Macia MD, Blanquer D, Togores B, Sauleda J, Perez JL, Oliver A (2005) Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrobial Agents Chemo 49:3382-3386

    Article  CAS  Google Scholar 

  • Maliszewska-Tkaczyk M, Jonczyk P, Bialoskorska M, Schaaper RM, Fijalkowska IJ (2000) SOS mutator activity: unequal mutagenesis on leading and lagging strands. Proc Natl Acad Sci USA 97:12678-12683

    Article  PubMed  CAS  Google Scholar 

  • Matic I, Radman M, Taddei F, Picard B, Doit C, Bingen E, Denamur E, Elion J (1997) Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277:1833-1834

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harbor Symp Quant Biol 16:13-47

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792-801

    Article  PubMed  CAS  Google Scholar 

  • Means JC, Plewa MJ, Gentile JM (1988) Assessment of the mutagenicity of fractions from s-triazine-treated Zea mays. Mutat Res 197:325-336

    Article  PubMed  CAS  Google Scholar 

  • Metzgar D, Wills C (2000) Evidence for the adaptive evolution of mutation rates. Cell 101:581-584

    Article  PubMed  CAS  Google Scholar 

  • Modrich P, Lahue R (1996) Mismatch repair in replication fidelity, genetic recombination and cancer biology. Ann Rev Bioch 65:101-133

    Article  CAS  Google Scholar 

  • Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046-1049

    Article  PubMed  CAS  Google Scholar 

  • Mourad G, White J (1992) The isolation of apparently homoplastic mutants induced by a nuclear recessive gene in Arabidopsis thaliana. Theor Appl Genet 84:906-914

    Article  Google Scholar 

  • Neve P, Powles S (2005) High survival frequencies at low herbicide use rates in populations of Lolium rigidum result in rapid evolution of herbicide resistance. Heredity 95:485-492

    Article  PubMed  CAS  Google Scholar 

  • Oettmeier W (1999) Herbicide resistance and supersensitivity in photosystem II. Cell Mol Life Sci 55:1255-1277

    Article  PubMed  CAS  Google Scholar 

  • Ottaviano E, Sari Gorla M, Mulcahy DL (1990) Pollen selection: efficiency and monitoring. Prog Clin Biol Res 344:575-588

    PubMed  CAS  Google Scholar 

  • Otto SP, Michalakis Y (1998) The evolution of recombination in changing environments. Trends Evol Environ 13:145-151

    Article  CAS  Google Scholar 

  • Owen MJ, Walsh MJ, Llewellyn RS, Powles SB (2007) Widespread occurrence of multiple herbicide resistance in Western Australian annual ryegrass (Lolium rigidum) populations. Aust J Agric Res 58:711-718

    Article  CAS  Google Scholar 

  • Peck JR, Waxman D (2000) Mutation and sex in a competitive world. Nature 406:399-404

    Article  PubMed  CAS  Google Scholar 

  • Pedersen S, Simonsen V, Loeschke V (1987) Overlap of gametophytic and sporophytic gene expression in barley. Theor Appl Genet 75:200-206

    Article  Google Scholar 

  • Plewa MJ (1985) Mutation testing with maize. Basic Life Sci 34:323-328

    PubMed  CAS  Google Scholar 

  • Preston C (2003) Inheritance and linkage of metabolism-based herbicide cross-resistance in rigid ryegrass (Lolium rigidum). Weed Sci 51:4-12

    Article  CAS  Google Scholar 

  • Radman M (1999) Enzymes of evolutionary change. Nature 401:866-867

    Article  PubMed  CAS  Google Scholar 

  • Ray TB (1982) The mode of action of chlorsulfuron: a new herbicide for cereals. Pestic Biochem Physiol 17:10-17

    Article  CAS  Google Scholar 

  • Redei GP (1973) Extra-chromosomal mutability determined by a nuclear gene locus in Arabidopsis. Mutat Res 18:149-162

    Article  Google Scholar 

  • Redei GP, Plurad SB (1973) Hereditary structural alterations of plastids induced by a nuclear mutator gene in Arabidopsis. Protoplasma 77:361-380

    Article  Google Scholar 

  • Richter J, Powles SB (1993) Pollen expression of herbicide target resistance genes in annual ryegrass (Lolium rigidum). Plant Physiol 102:1037-1041

    PubMed  CAS  Google Scholar 

  • Rios RD, Saione H, Robredo C, Acevedo A, Colombo N, Prina AR (2003) Isolation and molecular characterization of atrazine tolerant barley mutants. Theor Appl Genet 106:696-702

    PubMed  CAS  Google Scholar 

  • Rosenberg SM, Thulin C, Harris RS (1998) Transient and heritable mutators in adaptive evolution in the lab and in nature. Genetics 148:1559-1566

    PubMed  CAS  Google Scholar 

  • Sakamoto W, Kondo H, Murata M, Motoyoshi F (1996) Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8:1377-1390

    PubMed  CAS  Google Scholar 

  • Sandhu AP, Abdelnoor RV, Mackensie SA (2007) Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants. Proc Natl Acad Sci USA 104:1766-1770

    Article  PubMed  CAS  Google Scholar 

  • Schönfeld M, Yaacoby T, Ben-Yehuda A, Rubin B, Hirschberg J (1987) Triazine resistance in Phalaris paradoxa physiological and molecular analyses. Z Naturforsch 42c:779-782

    Google Scholar 

  • Smith BT, Walker GC (1998) Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics 148:1599-1610

    PubMed  CAS  Google Scholar 

  • Stambuk S, Radman M (1998) Mechanism and control of interspecies recombination in Escherichia coli. I. Mismatch repair, methylation, recombination and replication functions. Genetics 150:533-542

    PubMed  CAS  Google Scholar 

  • Swoboda P, Gal S, Hohn B, Puchta H (1994) Intrachromosomal homologous recombination in whole plants. EMBO J 13:484-489

    PubMed  CAS  Google Scholar 

  • Taddei F, Radman M, Maynard-Smit J, Toupance B, Gouyon PH, Godelle B (1997) Role of mutator alleles in adaptive evolution. Nature 387:700-702

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Zamir D, Rick CM (1981) Evidence for overlap of sporophytic and gametophytic gene expression in Lycopersicon esculentum. Science 213:453-455

    Article  PubMed  CAS  Google Scholar 

  • Tardif FJ, Powles SB (1994) Herbicide multiple-resistance in a Lolium rigidum biotype is endowed by multiple mechanisms: isolation of a subset with resistant acetyl-CoA carboxylase. Physiol Plant 91:488-494

    Article  CAS  Google Scholar 

  • Tenaillon O, Toupance B, le Nagard H, Taddei F, Godelle B (1999) Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152:485-493

    PubMed  CAS  Google Scholar 

  • Travis JMJ, Travis ER (2002) Mutator dynamics in fluctuating environments. Proc R S London B Biol Sci 269:591-597

    Article  CAS  Google Scholar 

  • Warwick SI, Stewart CN Jr (2005) Crops come from wild plants: how domestication, transgenes and linkage together shape ferality. In: Gressel J (ed) Crop ferality and volunteerism. CRC Press, Boca Raton, FL

    Google Scholar 

  • Young LW, Cross RH, Byun-McKay SA, Wilen RW, Bonham-Smith PC (2005) A high- and low-temperature inducible Arabidopsis thaliana HSP101 promoter located in a non-autonomous mutator-like element. Genome 48:547-555

    Article  PubMed  CAS  Google Scholar 

  • Zahrt TC, Maloy S (1997) Barriers to recombination between closely related bacteria: MutS and RecBCD inhibit recombination between Salmonella typhimurium and Salmonella typhi. Proc Natl Acad Sci USA 94:9786-9791

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

A.A.L thanks the Gilbert de Botton Professorship of Plant Sciences.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, Weizmann Institute of Science, Rehovot, 76100, Israel

    Jonathan Gressel & Avraham A. Levy

Authors
  1. Jonathan Gressel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Avraham A. Levy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan Gressel .

Editor information

Editors and Affiliations

  1. School of Life Science, Jawaharlal Nehru University, New Mehrauli Road, New Delhi, 110067, India

    Ashwani Pareek

  2. School of Life Science, Jawaharlal Nehru University, New Mehrauli Road, New Delhi, 110067, India

    S.K. Sopory

  3. Dept. Plant Biology, University of Illinois, W. Gregory Drive 1201, Urbana, 61801, U.S.A.

    Hans J. Bohnert

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Gressel, J., Levy, A.A. (2009). Stress, Mutators, Mutations and Stress Resistance. In: Pareek, A., Sopory, S., Bohnert, H. (eds) Abiotic Stress Adaptation in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3112-9_21

Download citation

Publish with us

Policies and ethics

Search

Navigation