Skip to main content

Inducing Hypoxic Stress Responses by Herbicides That Inhibit Amino Acid Biosynthesis

  • Chapter
  • First Online:
Low-Oxygen Stress in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 21))

Abstract

Nowadays, there are two main types of herbicides that inhibit amino acid biosynthesis: glyphosate, which inhibits aromatic amino acid synthesis via specific inhibition of 5-enolpyruvyl-shikimate-3-phosphate synthase (EPSPS), and inhibitors of branched-chain amino acid synthesis that act via specific inhibition of acetolactate synthase (ALS). Both types of inhibitors share different aspects of their mode of action, such as the induction of fermentation. Although this physiological effect resembles the hypoxic stress response, it was detected under aerobic conditions and it was not related to a change in respiratory rates or to a decrease in the energy charge. Fermentative induction has also been detected after treatment with other compounds inhibiting amino acid biosynthesis, such as glufosinate or ketol-acid reductoisomerase inhibitors suggesting that it can be considered as part of a general plant response to the stress conditions caused by this kind of herbicide treatment. Fermentation seems to be part of the impaired carbon metabolism detected in these treated plants that prevent the optimal utilization of available carbohydrates and energy.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

ADH:

Alcohol dehydrogenase

AEC:

Adenylate energy charge

ALS:

Acetolactate synthase

CPCA:

1,1-Cyclopropanedicarboxylic acid

EPSPS:

5-Enolpyruvyl-shikimate-3-phosphate synthase

KARI:

Ketol-acid reductoisomerase

PDC:

Pyruvate decarboxylase

RC:

Redox charge

References

  • Bailey-Serres J, Chang R (2005) Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann Bot 96:507–518

    Article  CAS  PubMed  Google Scholar 

  • Cobb AH, Reade JPH (2010) Herbicides and plant physiology. Wiley-Blackwell, Oxford, UK

    Book  Google Scholar 

  • Das M, Reichman JR, Haberer G, Welzl G, Aceituno FF, Mader MT, Watrud LS, Pfleeger TG, Gutiérrez RA, Schäffner AR, Olszyk DM (2010) A composite transcriptional signature differentiates responses towards closely related herbicides in Arabidopsis thaliana and Brassica napus. Plant Mol Biol 72:545–556

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dayan FE, Duke SO, Grossmann K (2010) Herbicides as probes in plant biology. Weed Sci 58:340–350

    Article  CAS  Google Scholar 

  • Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis adh gene. Plant Physiol 105:1075–1087

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duke SO (1990) Overview of herbicide mechanisms of action. Environ Health Perspect 87:263–271

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gaston S, Zabalza A, González EM, Arrese-Igor C, Aparicio-Tejo PM, Royuela M (2002) Imazethapyr, an inhibitor of the branched-chain amino acid biosynthesis, induces aerobic fermentation in pea plants. Physiol Plant 114:524–532

    Article  CAS  PubMed  Google Scholar 

  • Gaston S, Ribas-Carbo M, Busquets S, Berry JA, Zabalza A, Royuela M (2003) Changes in mitochondrial electron partitioning in response to herbicides inhibiting branched-chain amino acid biosynthesis in soybean. Plant Physiol 133:1351–1359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gerwick BC, Mireless LC, Eilers RJ (1993) Rapid diagnosis of ALS/AHAS-resistant weeds. Weed Technol 7:519–524

    CAS  Google Scholar 

  • Gruys KJ, Sikorski JA (1999) Inhibitors of tryptophan, phenylalanine, and tyrosine biosynthesis as herbicides. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York

    Google Scholar 

  • Kürsteiner O, Dupuis I, Kuhlemeier C (2003) The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol 132:968–978

    Article  PubMed Central  PubMed  Google Scholar 

  • Leason M, Cunliffe D, Parkin D, Lea PJ, Miflin BJ (1982) Inhibition of pea leaf glutamine synthetase by methionine sulphoximine, phosphinothricin and other glutamate analogues. Phytochemistry 21:855–857

    Article  CAS  Google Scholar 

  • Millar AH, Wiskich JT, Whelan J, Day DA (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett 329:259–262

    Article  CAS  PubMed  Google Scholar 

  • Orcaray L, Igal M, Marino D, Zabalza A, Royuela M (2010) The possible role of quinate in the mode of action of glyphosate and acetolactate synthase inhibitors. Pest Manag Sci 66:262–269

    Article  CAS  PubMed  Google Scholar 

  • Orcaray L, Igal M, Zabalza A, Royuela M (2011) Role of exogenously supplied ferulic and p-coumaric acids in mimicking the mode of action of acetolactate synthase inhibiting herbicides. J Agric Food Chem 59:10162–10168

    Article  CAS  PubMed  Google Scholar 

  • Orcaray L, Zulet A, Zabalza A, Royuela M (2012) Impairment of carbon metabolism induced by the herbicide glyphosate. J Plant Physiol 169:27–33

    Article  CAS  PubMed  Google Scholar 

  • Rhodes D, Hogan AL, Deal L, Jamieson GC, Haworth P (1987) Amino-acid metabolism of Lemna minor L. 2. Responses to chlorsulfuron. Plant Physiol 84:775–780

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schmid J, Amrhein N (1999) The shikimate pathway. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York

    Google Scholar 

  • Schulz A, Sponemann P, Kocher H, Wegenmayer F (1988) The herbicidally active experimental compound Hoe 704 is a potent inhibitor of the enzyme acetolactate reductoisomerase. FEBS Lett 238:375–378

    Article  CAS  PubMed  Google Scholar 

  • Shaner DL, Reider ML (1986) Physiological responses of corn (Zea mays) to Ac 243,997 in combination with valine, leucine, and isoleucine. Pestic Biochem Physiol 25:248–257

    Article  CAS  Google Scholar 

  • Singh BK (1999) Biosynthesis of valine, leucine and isoleucine. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York

    Google Scholar 

  • Steinrücken HC, Amrhein N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Commun 94:1207–1212

    Article  PubMed  Google Scholar 

  • Tadege M, Dupuis I, Kuhlemeier C (1999) Ethanolic fermentation: new functions for an old pathway. Trends Plant Sci 4:320–325

    Article  PubMed  Google Scholar 

  • Tan S, Evans R, Singh B (2006) Herbicidal inhibitors of amino acid biosynthesis and herbicide-tolerant crops. Amino Acids 30:195–204

    Article  CAS  PubMed  Google Scholar 

  • Vanlerbergue GC, Day DA, Wiskich JT, Vanlerbergue AE, McIntosh L (1995) Alternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol 109:353–361

    Google Scholar 

  • Wang CY (2001) Effect of glyphosate on aromatic amino acid metabolism in purple nutsedge (Cyperus rotundus). Weed Technol 15:628–635

    Article  CAS  Google Scholar 

  • Wittenbach VA, Abell LM (1999) Inhibition of valine, leucine and isoleucine biosynthesis. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York

    Google Scholar 

  • Zabalza A, Orcaray L, Gastón S, Royuela M (2004) Carbohydrate accumulation in leaves of plants treated with the herbicide chlorsulfuron or imazethapyr is due to a decrease in sink strength. J Agric Food Chem 52:7601–7606

    Article  CAS  PubMed  Google Scholar 

  • Zabalza A, González EM, Arrese-Igor C, Royuela M (2005) Fermentative metabolism is induced by inhibiting different enzymes of the branched-chain amino acid biosynthesis pathway in pea plants. J Agric Food Chem 53:7486–7493

    Article  CAS  PubMed  Google Scholar 

  • Zabalza A, Gaston S, Ribas-Carbó M, Orcaray L, Igal M, Royuela M (2006) Nitrogen assimilation studies using 15N in soybean plants treated with imazethapyr, an inhibitor of branched-chain amino acid biosynthesis. J Agric Food Chem 54:8818–8823

    Article  CAS  PubMed  Google Scholar 

  • Zabalza A, van Dongen JT, Froehlich A, Oliver S, Faix B, Kapuganti JG, Schmalzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zabalza A, Orcaray L, Igal M, Schauer N, Fernie AR, Geigenberger P, van Dongen JT, Royuela M (2011) Unraveling the role of fermentation in the mode of action of acetolactate synthase inhibitors by metabolic profiling. J Plant Physiol 168:1568–1575

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Patzoldt WL, Shealy RT, Vodkin LO, Clough SJ, Tranel PJ (2008) Transcriptome response to glyphosate in sensitive and resistant soybean. J Agric Food Chem 56:6355–6363

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Zabalza .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Zabalza, A., Royuela, M. (2014). Inducing Hypoxic Stress Responses by Herbicides That Inhibit Amino Acid Biosynthesis. In: van Dongen, J., Licausi, F. (eds) Low-Oxygen Stress in Plants. Plant Cell Monographs, vol 21. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1254-0_20

Download citation

Publish with us

Policies and ethics