Skip to main content
SpringerLink
Log in

Trace concentrations of imazethapyr (IM) affect floral organs development and reproduction in Arabidopsis thaliana: IM-induced inhibition of key genes regulating anther and pollen biosynthesis

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Understanding how herbicides affect plant reproduction and growth is critical to develop herbicide toxicity model and refine herbicide risk assessment. Although our knowledge of herbicides toxicity mechanisms at the physiological and molecular level in plant vegetative phase has increased substantially in the last decades, few studies have addressed the herbicide toxicity problematic on plant reproduction. Here, we determined the long-term (4–8 weeks) effect of a chiral herbicide, imazethapyr (IM), which has been increasingly used in plant crops, on floral organ development and reproduction in the model plant Arabidopsis thaliana. More specifically, we followed the effect of two IM enantiomers (R- and S-IM) on floral organ structure, seed production, pollen viability and the transcription of key genes involved in anther and pollen development. The results showed that IM strongly inhibited the transcripts of genes regulating A. thaliana tapetum development (DYT1: DYSFUNCTIONAL TAPETUM 1), tapetal differentiation and function (TDF1: TAPETAL DEVELOPMENT AND FUNCTION1), and pollen wall formation and developments (AMS: ABORTED MICROSPORES, MYB103: MYB DOMAIN PROTEIN 103, MS1: MALE STERILITY 1, MS2: MALE STERILITY 2). Since DYT1 positively regulates 33 genes involved in cell-wall modification (such as, TDF1, AMS, MYB103, MS1, MS2) that can catalyze the breakdown of polysaccharides to facilitate anther dehiscence, the consistent decrease in the transcription of these genes after IM exposure should hamper anther opening as observed under scanning electron microscopy. The toxicity of IM on anther opening further lead to a decrease in pollen production and pollen viability. Furthermore, long-term IM exposure increased the number of apurinic/apyrimidinic sites (AP sites) in the DNA of A. thaliana and also altered the DNA of A. thaliana offspring grown in IM-free soils. Toxicity of IM on floral organs development and reproduction was generally higher in the presence of the R-IM enantiomer than of the S-IM enantiomer. This study unraveled several IM toxicity targets and mechanisms at the molecular and structural level linked to the toxicity of IM trace concentrations on A. thaliana reproduction.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aarts MG, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira A (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12:615–623

    Article  CAS  Google Scholar 

  • Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Baucom RS, Mauricio R, Chang SM (2008) Glyphosate induces transient male sterility in Ipomoea purpurea. Botany 86:587–594

    Article  CAS  Google Scholar 

  • Boatman ND, Parry HR, Bishop JD, Cuthbertson AGS (2007) Impacts of agricultural change for farmland biodiversity. In: Hester R, Harrison RM (eds) Biodiversity under threat. The Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Boutin C, Standberg B, Carpenter D, Mathiassen SK, Thomas PJ (2014) Herbicide impact on non-target plant reproduction: what are the toxicological and ecological implications? Environ Poll 185:295–306

    Article  CAS  Google Scholar 

  • Carpenter C, Boutin C (2010) Sublethal effects of the herbicide glufosinate ammonium on crops and wild plants: short-term effects compared to vegetative recovery and plant reproduction. Ecotoxicology 19:1322–1336

    Article  CAS  Google Scholar 

  • Curran WC, Liebl RA, Simmons FW (1992) Effects of tillage and application method on clomazone, imazaquin and imazethapyr persistence. Weed Sci 40:482–489

    CAS  Google Scholar 

  • Dalton RL, Boutin C (2010) Comparison of the effects of glyphosate and atrazine herbicides on nontarget plants grown singly and in microcosms. Environ Toxicol Chem 29:2304–2315

    Article  CAS  Google Scholar 

  • Demura T, Ye ZH (2010) Regulation of plant biomass production. Curr Opin Plant Biol 13:299–304

    Article  Google Scholar 

  • Feng B, Lu D, Ma X, Peng Y, Sun Y, Ning G, Ma H (2012) Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J 72:612–624

    Article  CAS  Google Scholar 

  • Fletcher SJ, Pfleeger TG, Hillman CR (1993) Potential environmental risks associated with the new sulfonylurea herbicides. Environ Sci Technol 27:2250–2252

    Article  CAS  Google Scholar 

  • Fletcher JS, Pfeeger TG, Ratsch HC, Hayes R (1996) Potential impact of low levels of chlorosulfuron and other herbicides on growth and yield of nontarget plants. Environ Toxicol Chem 15:1189–1196

    Article  CAS  Google Scholar 

  • Gavrilescu M (2005) Fate of pesticides in the environment and its bioremediation. Eng Life Sci 5:497–525

    Article  CAS  Google Scholar 

  • Gealy DR, Boerboom CM, Ogg AG Jr (1995) Growth and yield of pea (Pisum sativum L) and lentil (Lens culinaris L) sprayed with low rates of sulfonylurea and phenoxy herbicide. Weed Sci 43:640–647

    CAS  Google Scholar 

  • Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129

    Article  CAS  Google Scholar 

  • Jettner RJ, Walker SR, Churchett JD, Blameye FC, Adkins SW, Bell K (1999) Plant sensitivity to atrazine and chlorsulfuron residues in a soil-free system. Weed Res 39:287–295

    Article  CAS  Google Scholar 

  • Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermo sensory activation of flowering. Nature 484:242–245

    Article  CAS  Google Scholar 

  • Lambrev P, Ivanov S, Goltsev V (2003) Effect of prolonged action of sub-herbicide concentration of atrazine on the photosynthetic function of pea plants. Comp Rend Acad Bulg Sci 56:59–62

    CAS  Google Scholar 

  • Lansac AR, Sullivan CY, Johnson E, Lee KW (1994) Viability and germination of the pollen of sorghum [Sorghum bicolor (L.) Moench]. Ann Bot 74:27–33

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Mills JA, Witt WW (1989) Efficacy, phytotoxicity, and persistence of imazaquin, imazethapyr, and clomazone in non-till double crop soybeans (Glycine max). Weed Sci 37:353–359

    CAS  Google Scholar 

  • Ó’Maoiléidigh DS, Graciet E, Wellmer F (2013) Gene networks controlling Arabidopsis thaliana flower development. New Phytol 201:16–30

    Article  Google Scholar 

  • Olofsdotter M, Watson A, Piggin C (1998) Weeds: a looming problem in modern rice production. In: Dowling NG, Greenfield SM, Fisher KS (eds) Sustainability of rice in the global food system. Davis, California, pp 165–173

    Google Scholar 

  • Pimentel D (1995) Amounts of pesticides reaching target pests: environmental impacts and ethics. J Agr Environ Ethic 8:17–29

    Article  Google Scholar 

  • Pline WA, Viator R, Wilcut JW, Edmisten KL, Thomas J, Wells R (2002) Reproductive abnormalities in glyphosate-resistant cotton caused by lower CP4-EPSPS levels in the male reproductive tissue. Weed Sci 50:438–447

    Article  CAS  Google Scholar 

  • Qian HF, Hu HJ, Ma J, Mao Y, Zhang A, Liu WP, Fu Z (2009) Enantioselective phytotoxicity of the herbicide imazethapyr in rice. Chemosphere 76:885–892

    Article  CAS  Google Scholar 

  • Qian HF, Lu T, Peng X, Han X, Fu Z, Liu W (2011a) Enantioselective phytotoxicity of the herbicide imazethapyr on the response of the antioxidant system and starch metabolism in Arabidopsis thaliana. PLoS ONE 6:e19451

    Article  CAS  Google Scholar 

  • Qian HF, Wang R, Hu H, Lu T, Chen X, Ye H, Liu W, Fu Z (2011b) Enantioselective phytotoxicity of the herbicide imazethapyr and its effect on rice physiology and gene transcription. Environ Sci Technol 45:7036–7043

    Article  CAS  Google Scholar 

  • Qian HF, Han X, Zhang Q, Sun Z, Sun L, Fu Z (2013) Imazethapyr enantioselectively affects chlorophyll synthesis and photosynthesis in Arabidopsis thaliana. J Agric Food Chem 61:1172–1178

    Article  CAS  Google Scholar 

  • Qian HF, Han X, Peng X, Lu T, Liu W, Fu Z (2014) The circadian clock gene regulatory module enantioselectively mediates Imazethapyr-induced early flowering in Arabidopsis thaliana. J Plant Physiol 171:92–98

    Article  CAS  Google Scholar 

  • Ratsch HC, Johndro DJ, McFarlane JC (1986) Growth inhibition and morphological effects of several chemicals in Arabidopsis thaliana (L.) Heynh. Environ Toxicol Chem 5:55–60

    CAS  Google Scholar 

  • Satake A, Kawagoe T, Saburi Y, Chiba Y, Sakurai G, Kudoh H (2013) Forecasting flowering phenology under climate warming by modeling the regulatory dynamics of flowering-time genes. Nat Commun 4:2303

    Article  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, pp 227–247

    Google Scholar 

  • Strandberg B, Mathiassen SK, Bruus M, Kjær C, Damgaard C, Andersen HV, Bossi R, Løfstrøm P, Larsen SE, Bak J, Kudsk P (2012) Effects of herbicides on non-target plants: how do effects in standard plant test relate to effects in natural habitats? Pesticide Research No 137, Danish Ministry of the Environment, EPA, p 114. http://www2.mst.dk/udgiv/publications/2012/06/978-87-92779-53-3.pdf

  • Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H (2013) Flower Development under Drought Stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 25:3785–3807

    Article  CAS  Google Scholar 

  • Thomas WE, Pline-Srnie WA, Thomas JF, Edmisten KL, Wells R, Wileut JW (2004) Glyphosate negatively affects pollen viability but not pollination and seed set in glyphosate-resistant corn. Weed Sci 52:725–734

    Article  CAS  Google Scholar 

  • Thorstensen T, Grini PE, Mercy IS, Alm V, Erdal S, Aasland R, Aalen RB (2008) The Arabidopsis SET-domain protein ASHR3 is involved in stamen development and interacts with the bHLH transcription factor ABORTED MICROSPORES (AMS). Plant Mol Biol 66:47–59

    Article  CAS  Google Scholar 

  • Wang XL, Takai T, Kamijo S, Gunawan H, Ogawa H, Okumura K (2009) NADPH oxidase activity in allergenic pollen grains of different plant species. Biochem Bioph Res Co 387:430–434

    Article  CAS  Google Scholar 

  • Yasuor H, Abu-Abied M, Belausov E, Madmony A, Sadot E, Riov J, Rubin B (2006) Glyphosate-induced anther indehiscence in cotton is partially temperature dependent and involves cytoskeleton and secondary wall modifications and auxin accumulation. Plant Physiol 141:1306–1315

    Article  CAS  Google Scholar 

  • York AC, Wilcut JW, Swann CW, Jordan DL, Walls R Jr (1995) Efficacy of imazethapyr in peanut (Arachis hypogaea) as affected by time of application. Weed Sci 43:107–116

    CAS  Google Scholar 

  • Zabaloy MC, Zanini GP, Bianchinotti V, Gomez MA, Garland JL (2011) Herbicides in the soil environment: linkage between bioavailability and microbial ecology. In: Soloneski S, Larramendy ML (eds) Inherbicides, theoryand applications. Croatia, Intech, pp 161–192

    Google Scholar 

  • Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encodinga putative bHLH transcription factor. Development 133:3085–3095

    Article  CAS  Google Scholar 

  • Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in Tapetal Development and Function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277

    Article  CAS  Google Scholar 

  • Zhu J, Lou Y, Xu X, Yang ZN (2011) A genetic pathway for tapetum development and function in Arabidopsis. J Integr Plant Biol 53:892–900

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Natural Science Foundation of China (21277127, 21277125), and Zhejiang Provincial Natural Science Foundation of China (LR14B070001).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Haifeng Qian, Chongchong Sun & Xiaocui Bai

  2. College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Haifeng Qian, Yali Li, Jun Xie & Zhengwei Fu

  3. Quebec-Ocean and Takuvik Joint International Research Unit, Université Laval, Quebec, Canada

    Michel Lavoie

Authors
  1. Haifeng Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yali Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chongchong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michel Lavoie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaocui Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhengwei Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhengwei Fu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qian, H., Li, Y., Sun, C. et al. Trace concentrations of imazethapyr (IM) affect floral organs development and reproduction in Arabidopsis thaliana: IM-induced inhibition of key genes regulating anther and pollen biosynthesis. Ecotoxicology 24, 163–171 (2015). https://doi.org/10.1007/s10646-014-1369-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1369-5

Keywords

Search

Navigation