Abstract
Pyruvate orthophosphate dikinase (PPDK) catalyzes the conversion of pyruvate to phosphoenolpyruvate, and its activity is essential to maintain photosynthetic CO2 assimilation in C4 plants. Thus, it has been described as a promising target for the development of selective herbicides for C4 weeds. We evaluated whether bromoacetic acid, a known PPDK inhibitor of Clostridium symbiosum, can also inhibit the PPDK of a C4 plant, maize, in in vitro experiments. We also evaluated the effects of foliar application of 0.5–10 mM bromoacetic acid on the leaf pyruvate content and gas exchange of maize plants. Bromoacetic acid reduced maize PPDK activity in vitro in a dose-dependent manner; the degree of inhibition ranged from 13.6 to 73.6% with 0.5–10 mM bromoacetic acid. The foliar application of bromoacetic acid increased the leaf pyruvate content, suggesting that this compound may also inhibit PPDK activity in vivo. As a consequence, impairments to the gas exchange parameters of maize plants were noted, with a marked reduction in the photosynthetic rate and an increase in the intercellular CO2 concentration. Despite the abrupt decrease in stomatal conductance and transpiration, the plants showed large dehydration and reduction of leaf fresh weight after 48 h of application to bromoacetic acid. Our data allow us to affirm that bromoacetic acid has a potent herbicidal effect on a C4 plant, maize; the most likely mechanism of action is the inhibition of PPDK.
This is a preview of subscription content, log in via an institution to check access.
References
Balabanova DA, Paunov M, Goltsev V et al (2016) Photosynthetic performance of the imidazolinone resistant sunflower exposed to single and combined treatment by the herbicide Imazamox and an amino acid extract. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01559
Bergmeyer H-U, Bernt E, Hess B (1965) Lactic dehydrogenase. Bergmeyer H-UBT-M of EA, 3rd edn. Academic Press, London, pp 736–743
Buchanan BB, Gruissem W, Jones RL (2015) Biochemistry and molecular biology of plants, 2nd edn. Wiley-Blackwell, Chichester
Chastain CJ, Failing CJ, Manandhar L et al (2011) Functional evolution of C4 pyruvate, orthophosphate dikinase. J Exp Bot 62:3083–3091
Chen YB, Lu TC, Wang HX et al (2014) Posttranslational modification of maize chloroplast pyruvate orthophosphate dikinase reveals the precise regulatory mechanism of its enzymatic activity. Plant Physiol 165:534–549
Colturato CP, Constantin RP, Maeda AS et al (2012) Metabolic effects of silibinin in the rat liver. Chem Biol Interact 195:119–132. https://doi.org/10.1016/j.cbi.2011.11.006
Dayan FE, Duke SO (2020) Discovery for new herbicide sites of action by quantification of plant primary metabolite and enzyme pools. Engineering. https://doi.org/10.1016/j.eng.2020.03.004
Doyle JR, Burnell JN, Haines DS et al (2005) A rapid screening method to detect specific inhibitors of pyruvate orthophosphate dikinase as leads for C4 plant-selective herbicides. J Biomol Screen 10:67–75
Duke SO (2011) Why have no new herbicide modes of action appeared in recent years? Pest Manag Sci 68:505–512. https://doi.org/10.1002/ps.2333
Ermakova M, Danila FR, Furbank RT, von Caemmerer S (2020) On the road to C4 rice: advances and perspectives. Plant J 101:940–950
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Gordon AR, Richardson TL, Pinckney JL (2015) Ecotoxicology of bromoacetic acid on estuarine phytoplankton. Environ Pollut 206:369–375. https://doi.org/10.1016/j.envpol.2015.07.014
Haines DS, Burnell JN, Doyle JR et al (2005) Translation of in vitro inhibition by marine natural products of the C4 acid cycle enzyme pyruvate Pi dikinase to in vivo C4 plant tissue death. J Agric Food Chem 53:3856–3862
Heap I (2020) The international survey of herbicide resistant weeds
Ling F, Su Q, Jiang H et al (2020) Effects of strigolactone on photosynthetic and physiological characteristics in salt-stressed rice seedlings. Sci Rep 10:6183
Marchiosi R, de Souza BG, Böhm PAF et al (2016) Photosynthetic response of soybean to l-DOPA and aqueous extracts of velvet bean. Plant Growth Regul 80:171–182. https://doi.org/10.1007/s10725-016-0154-2
Maroco JP, Ku MSB, Lea PJ et al (1998) Oxygen requirement and inhibition of C4 photosynthesis: an analysis of C4 plants deficient in the C3 and C4 cycles. Plant Physiol 116:823–832
May RM (1981) The world’s worst weeds. Nature 290:85–86
Medina S, Vicente R, Nieto-Taladriz MT et al (2019) The plant-transpiration response to vapor pressure deficit (VPD) in durum wheat is associated with differential yield performance and specific expression of genes involved in primary metabolism and water transport. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01994
Minges A, Groth G (2017) Small-molecule inhibition of pyruvate phosphate dikinase targeting the nucleotide binding site. PLoS ONE. https://doi.org/10.1371/journal.pone.0181139
Motti CA, Bourne DG, Burnell JN et al (2007) Screening marine fungi for inhibitors of the C4 plant enzyme pyruvate phosphate dikinase: unguinol as a potential novel herbicide candidate. Appl Environ Microbiol 73:1921–1927
Muellner MG, Attene-ramos MS, Hudson ME et al (2010) Human cell toxicogenomic analysis of bromoacetic acid: a regulated drinking water disinfection by-product. Environ Mol Mutagen 51:205–214. https://doi.org/10.1002/em.20530
Nguyen GTT, Erlenkamp G, Jäck O et al (2016) Chalcone-based selective inhibitors of a C4 plant key enzyme as novel potential herbicides. Sci Rep. https://doi.org/10.1038/srep27333
Parizotto AV, Marchiosi R, Bubna GA et al (2017) Benzoxazolin-2-(3H)-one reduces photosynthetic activity and chlorophyll fluorescence in soybean. Photosynthetica 55:386–390. https://doi.org/10.1007/s11099-016-0656-1
Parvez S, Frost K, Sundararajan M (2017) Evaluation of drinking water disinfectant byproducts compliance data as an indirect measure for short-term exposure in humans. Int J Environ Res Public Health 14:548. https://doi.org/10.3390/ijerph14050548
Pribil M, Leister D (2017) Photosynthesis. Encyclopedia of applied plant sciences. Elsevier, Amsterdam, pp 90–95
Sage RF, Zhu XG (2011) Exploiting the engine of C4 photosynthesis. J Exp Bot 62:2989–3000
Tremmel DC, Patterson DT (1993) Responses of soybean and five weeds to CO2 enrichment under two temperature regimes. Can J Plant Sci 73:1249–1260
Vadez V, Kholova J, Medina S et al (2014) Transpiration efficiency: new insights into an old story. J Exp Bot 65:6141–6153
von Caemmerer S, Furbank RT (2016) Strategies for improving C4 photosynthesis. Curr Opin Plant Biol 31:125–134
Westhoff P, Gowik U (2004) Evolution of C4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Ann Bot 93:13–23
Wu C, Dunaway-Mariano D, Mariano PS (2013) Design, synthesis, and evaluation of inhibitors of pyruvate phosphate dikinase. J Org Chem 78:1910–1922
Yip DY (2003) Developing a better understanding of the relationship between transpiration and water uptake in plants. J Sci Educ Technol 12:13–19
Yoshida H, Wood HG (1978) Crystalline pyruvate, phosphate dikinase from Bacteroides symbiosus. Modification of essential histidyl residues and bromopyruvate inactivation. J Biol Chem 253:7650–7655
Zhou YH, Yu JQ (2006) Allelochemicals and photosynthesis. Allelopathy: a physiological Process with ecological implications. Springer, Berlin, pp 127–139
Acknowledgements
RM and OFF are research fellows of National Council for Scientific and Technological Development (CNPq). RPC was the recipient of a CNPq fellowship. This work was funding by grants from Fundação de Apoio ao Desenvolvimento Científico e Tecnológico do Paraná (Fundação Araucária; Grant no. 002/2017).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by R. Marchiosi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Constantin, R.P., de Melo, G.S.R., Martarello, D.C.I. et al. Bromoacetic acid inhibits pyruvate orthophosphate dikinase and reduces photosynthetic activity in maize. Acta Physiol Plant 43, 54 (2021). https://doi.org/10.1007/s11738-021-03222-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-021-03222-4