Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 11, Issue 6

Photophysiological and transcriptomic response to the broad-spectrum herbicides atrazine and glyphosate in a photosynthetic picoeukaryote Open Access

This article is part of the Microbial Genomics of Eukaryotes collection

Graphical Abstract

 Graphical abstract 

Summary of . SENEW3 photophysiology and transcriptomic changes in response to atrazine and glyphosate. Created using biorender.com.

 

 

Abstract

To feed the growing global population, intensive agriculture relies on herbicides to maximize productivity, but these come with broad-reaching environmental impacts, particularly deleterious effects on ecosystems through water run-off systems. Picoeukaryotes, with minimal genomes, can be employed to model the modes of action of herbicides on off-target species in the environment. sp. SENEW3 (. SENEW3) is a poikilohaline green alga and serves as a useful model picoeukaryote due to its small genome and robust growth characteristics. Here, we examined the growth, photophysiological and transcriptomic responses of . SENEW3 to sublethal concentrations of two common herbicides: atrazine and glyphosate. Atrazine treatment resulted in significant (<0.0001) reductions in mean photosynthetic maximum yield (/) of 46% and an increase in fluorescence minimum () of 83%, while glyphosate treatment resulted in a significant (<0.0001) 30% mean reduction in fluorescence maximum (). Atrazine treatment resulted in significant transcriptomic changes (<0.01, 1.5 log2 fold change ratio), with increased transcription of 18 genes largely involved in gene expression and ribosomal subunits, carotenoid biosynthesis, carbon fixation and reduced transcription of 27 genes largely related to DNA replication and cell cycle. Treatment with glyphosate resulted in increased transcript abundance of 45 genes, most notably those related to energy generation and redox, and chloroplastic non-photochemical quenching and reduced transcription of 188 genes, largely involved in and protein synthesis. Both herbicides resulted in a reduced abundance of transcripts for a nitrogen assimilation cluster. These results highlight the potential for commonly used herbicides to have adverse effects on coastal primary producers and demonstrate the value of . SENEW3 as a robust model for evaluating the impacts of horticultural compounds and agricultural practices on this ecologically important group of organisms.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): atrazine , glyphosate , photophysiology , Picochlorum sp. , SENEW3 and transcriptomics
Funding
This study was supported by the:
  • Macquarie University
    • Principal Award Recipient: PatrickA. da Roza
© 2025 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001402
2025-06-25
2026-03-06

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/6/mgen001402.html?itemId=/content/journal/mgen/10.1099/mgen.0.001402&mimeType=html&fmt=ahah

References

  1. Evenson RE, Gollin D. Assessing the impact of the green revolution, 1960 to 2000. Science 2003; 300:758–762 [View Article] [PubMed]
     [Google Scholar]
  2. FAOSTAT Database collection of the food and agriculture organization of the united nations. Food and Agriculture Organization of the United Nations. Pesticides Use; 2021a
  3. FAOSTAT Database collection of the food and agriculture organization of the united nations. Food and Agriculture Organization of the United Nations. Pesticides Trade; 2021b
  4. De A, Bose R, Kumar A, Mozumdar S. Worldwide pesticide use. In Targeted Delivery of Pesticides Using Biodegradable Polymeric Nanoparticles New Delhi: Springer India; 2014 pp 5–6
     [Google Scholar]
  5. Maggi F, Tang FHM, la Cecilia D, McBratney A. PEST-CHEMGRIDS, global gridded maps of the top 20 crop-specific pesticide application rates from 2015 to 2025. Sci Data 2019; 6:170 [View Article] [PubMed]
     [Google Scholar]
  6. Maino JL, Thia J, Hoffmann AA, Umina PA. Estimating rates of pesticide usage from trends in herbicide, insecticide, and fungicide product registrations. Crop Prot 2023; 163:106125 [View Article]
     [Google Scholar]
  7. Sharma A, Kumar V, Shahzad B, Tanveer M, Sidhu GPS et al. Worldwide pesticide usage and its impacts on ecosystem. SN Appl Sci 2019; 1: [View Article]
     [Google Scholar]
  8. Walsh MJ, Powles SB. Management strategies for herbicide-resistant weed populations in Australian dryland crop production systems. Weed Technol 2007; 21:332–338 [View Article]
     [Google Scholar]
  9. Boutsalis P, Gill GS, Preston C. Incidence of herbicide resistance in rigid ryegrass (Lolium rigidum) across southeastern Australia. Weed technol 2012; 26:391–398 [View Article]
     [Google Scholar]
  10. Owen MJ, Martinez NJ, Powles SB. Multiple herbicide-resistant wild radish (Raphanus raphanistrum) populations dominate Western Australian cropping fields. Crop Pasture Sci 2015; 66:1079 [View Article]
     [Google Scholar]
  11. Bajwa AA, Walsh M, Chauhan BS. Weed management using crop competition in Australia. Crop Prot 2017; 95:8–13 [View Article]
     [Google Scholar]
  12. Gomes MP, Smedbol E, Chalifour A, Hénault-Ethier L, Labrecque M et al. Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview. J Exp Bot 2014; 65:4691–4703 [View Article] [PubMed]
     [Google Scholar]
  13. Cheng M, Zeng G, Huang D, Lai C, Xu P et al. Degradation of atrazine by a novel Fenton-like process and assessment the influence on the treated soil. J Hazard Mater 2016; 312:184–191 [View Article] [PubMed]
     [Google Scholar]
  14. Kumar V, Upadhyay N, Singh S, Singh J, Kaur P. Thin-layer chromatography: comparative estimation of soil’s atrazine. Curr World Environ 2013; 8:469–472 [View Article]
     [Google Scholar]
  15. Rutherford AW, Krieger-Liszkay A. Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 2001; 26:648–653 [View Article] [PubMed]
     [Google Scholar]
  16. Siehl DL, Roe R. Inhibitors of EPSP synthase, glutamine synthetase and histidine synthesis. Crit Rev Toxicol 1997; 1:37–68
     [Google Scholar]
  17. Tohge T, Watanabe M, Hoefgen R, Fernie AR. Shikimate and phenylalanine biosynthesis in the green lineage. Front Plant Sci 2013; 4:62 [View Article] [PubMed]
     [Google Scholar]
  18. Fedtke C, Duke S. Herbicides. In Plant Toxicology, 4th ed 2005 pp 247–330
     [Google Scholar]
  19. Anton FA, Ariz M, Alia M. Ecotoxic effects of four herbicides (glyphosate, alachlor, chlortoluron and isoproturon) on the algae Chlorella pyrenoidosa Chick. Sci Total Environ 1993; 134:845–851 [View Article]
     [Google Scholar]
  20. Fairchild JF, Ruessler DS, Carlson AR. Comparative sensitivity of five species of macrophytes and six species of algae to atrazine, metribuzin, alachlor, and metolachlor. Environ Toxicol Chem 1998; 17:1830–1834 [View Article]
     [Google Scholar]
  21. Tsui MTK, Chu LM. Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 2003; 52:1189–1197 [View Article] [PubMed]
     [Google Scholar]
  22. Esperanza M, Seoane M, Rioboo C, Herrero C, Cid Á. Chlamydomonas reinhardtii cells adjust the metabolism to maintain viability in response to atrazine stress. Aquat Toxicol 2015; 165:64–72 [View Article] [PubMed]
     [Google Scholar]
  23. Esperanza M, Seoane M, Rioboo C, Herrero C, Cid Á. Early alterations on photosynthesis-related parameters in Chlamydomonas reinhardtii cells exposed to atrazine: a multiple approach study. Sci Total Environ 2016; 554–555:237–245 [View Article] [PubMed]
     [Google Scholar]
  24. Harris EH. The Chlamydomonas Sourcebook: Introduction to Chlamydomonas and Its Laboratory Use: Volume 1 Academic press; 2009 [View Article]
     [Google Scholar]
  25. Yang H, Han F, Wang Y, Yang W, Tu W. Strategies to study dark growth deficient or slower mutants in Chlamydomonas reinhardtii. In Yin R, Li L, Zuo K. eds Plant Photomorphogenesis: Methods and Protocols New York, NY: Springer US; 2021 pp 125–140
     [Google Scholar]
  26. Wang S, Lambert W, Giang S, Goericke R, Palenik B. Microalgal assemblages in a poikilohaline pond. J Phycol 2014; 50:303–309 [View Article] [PubMed]
     [Google Scholar]
  27. Foflonker F, Price DC, Qiu H, Palenik B, Wang S et al. Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions. Environ Microbiol 2015; 17:412–426 [View Article] [PubMed]
     [Google Scholar]
  28. Foflonker F, Ananyev G, Qiu H, Morrison A, Palenik B et al. The unexpected extremophile: tolerance to fluctuating salinity in the green alga Picochlorum. Algal Res 2016; 16:465–472 [View Article]
     [Google Scholar]
  29. Foflonker F, Mollegard D, Ong M, Yoon HS, Bhattacharya D. Genomic analysis of Picochlorum species reveals how microalgae may adapt to variable environments. Mol Biol Evol 2018; 35:2702–2711 [View Article] [PubMed]
     [Google Scholar]
  30. Krasovec M, Vancaester E, Rombauts S, Bucchini F, Yau S et al. Genome analyses of the microalga Picochlorum provide insights into the evolution of thermotolerance in the green lineage. Genome Biol Evol 2018; 10:2347–2365 [View Article] [PubMed]
     [Google Scholar]
  31. Dahlin LR, Gerritsen AT, Henard CA, Van Wychen S, Linger JG et al. Development of a high-productivity, halophilic, thermotolerant microalga Picochlorum renovo. Commun Biol 2019; 2:388 [View Article] [PubMed]
     [Google Scholar]
  32. Guillard RR, Ryther JH. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 1962; 8:229–239 [View Article] [PubMed]
     [Google Scholar]
  33. Guillard RRL. Culture of phytoplankton for feeding marine invertebrates. In Smith WL, Chanley MH. eds Culture of Marine Invertebrate Animals: Proceedings — 1st Conference on Culture of Marine Invertebrate Animals Greenport Boston, MA: Springer US; 1975 pp 29–60 [View Article]
     [Google Scholar]
  34. Keller MD, Selvin RC, Claus W, Guillard RRL. Media for the culture of oceanic ultraphytoplankton. J Phycol 1987; 23:633–638
     [Google Scholar]
  35. Sanchez F, Geffroy S, Norest M, Yau S, Moreau H et al. Simplified transformation of Ostreococcus tauri using polyethylene glycol. Genes 2019; 10:399 [View Article] [PubMed]
     [Google Scholar]
  36. Baker NR. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 2008; 59:89–113 [View Article] [PubMed]
     [Google Scholar]
  37. da Roza PA, Muller H, Sullivan GJ, Walker RSK, Goold HD et al. Chromosome-scale assembly of the streamlined picoeukaryote Picochlorum sp. SENEW3 genome reveals Rabl-like chromatin structure and potential for C4 photosynthesis. Microb Genom 2024; 10:001223 [View Article] [PubMed]
     [Google Scholar]
  38. Wagner GP, Kin K, Lynch VJ. Measurement of mrna abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 2012; 131:281–285 [View Article] [PubMed]
     [Google Scholar]
  39. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:550 [View Article] [PubMed]
     [Google Scholar]
  40. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  41. Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S et al. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res 2021; 49:D344–D354 [View Article]
     [Google Scholar]
  42. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
     [Google Scholar]
  43. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article]
     [Google Scholar]
  44. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
     [Google Scholar]
  45. Hemschemeier A, Casero D, Liu B, Benning C, Pellegrini M et al. Copper response regulator1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 2013; 25:3186–3211 [View Article] [PubMed]
     [Google Scholar]
  46. Singh S, Kumar V, Chauhan A, Datta S, Wani AB et al. Toxicity, degradation and analysis of the herbicide atrazine. Environ Chem Lett 2018; 16:211–237 [View Article]
     [Google Scholar]
  47. Gomes MP, Le Manac’h SG, Maccario S, Labrecque M, Lucotte M et al. Differential effects of glyphosate and aminomethylphosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plants. Pestic Biochem Physiol 2016; 130:65–70 [View Article] [PubMed]
     [Google Scholar]
  48. Van Bruggen AHC, He MM, Shin K, Mai V, Jeong KC et al. Environmental and health effects of the herbicide glyphosate. Sci Total Environ 2018; 616–617:255–268 [View Article] [PubMed]
     [Google Scholar]
  49. Ma J, Wang S, Wang P, Ma L, Chen X et al. Toxicity assessment of 40 herbicides to the green alga Raphidocelis subcapitata. Ecotoxicol Environ Saf 2006; 63:456–462 [View Article] [PubMed]
     [Google Scholar]
  50. Murchie EH, Lawson T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 2013; 64:3983–3998 [View Article] [PubMed]
     [Google Scholar]
  51. Duke SO, Powles SB. Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 2008; 64:319–325 [View Article] [PubMed]
     [Google Scholar]
  52. Mesnage R, Benbrook C, Antoniou MN. Insight into the confusion over surfactant co-formulants in glyphosate-based herbicides. Food Chem Toxicol 2019; 128:137–145 [View Article] [PubMed]
     [Google Scholar]
  53. Consalvey M, Perkins RG, Paterson DM, Underwood GJC. PAM fluorescence: a beginners guide for benthic diatomists. Diatom Res 2005; 20:1–22 [View Article]
     [Google Scholar]
  54. Baxter L, Brain RA, Lissemore L, Solomon KR, Hanson ML et al. Influence of light, nutrients, and temperature on the toxicity of atrazine to the algal species Raphidocelis subcapitata: implications for the risk assessment of herbicides. Ecotoxicol Environ Saf 2016; 132:250–259 [View Article] [PubMed]
     [Google Scholar]
  55. Bradbury M, Baker NR. The kinetics of photoinhibition of the photosynthetic apparatus in pea chloroplasts. Plant Cell Environ 1986; 9:289–297 [View Article]
     [Google Scholar]
  56. Osmond CB. What is photoinhibition? Some insights from comparisons of shade and sun plants. In Baker NRB. eds Photoinhibition of Photosynthesis-from Molecular Mechanisms to the Field Oxford: BIOS Scientific Publishers; 1994 pp 1–24
     [Google Scholar]
  57. Aro EM, Virgin I, Andersson B. Inactivation, protein damage and turnover. Biochim Biophys Acta Bioenerg 1993; 1143:113–134 [View Article]
     [Google Scholar]
  58. Briantais J-M, Dacosta J, Goulas Y, Ducruet J-M, Moya I. Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, Fo: a time-resolved analysis. Photosynth Res 1996; 48:189–196 [View Article]
     [Google Scholar]
  59. Melis A. Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage ?. Trends Plant Sci 1999; 4:130–135 [View Article] [PubMed]
     [Google Scholar]
  60. Coordinators NR. Database resources of the national center for biotechnology information. Nucleic Acids Res 2018; 46:D8-d13
     [Google Scholar]
  61. Seifert GJ. Fascinating fasciclins: a surprisingly widespread family of proteins that mediate interactions between the cell exterior and the cell surface. Int J Mol Sci 2018; 19:1628 [View Article] [PubMed]
     [Google Scholar]
  62. Rezayian M, Niknam V, Ebrahimzadeh H. Oxidative damage and antioxidative system in algae. Toxicol Rep 2019; 6:1309–1313 [View Article] [PubMed]
     [Google Scholar]
  63. Gerashchenko MV, Lobanov AV, Gladyshev VN. Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc Natl Acad Sci USA 2012; 109:17394–17399 [View Article]
     [Google Scholar]
  64. Blevins WR, Tavella T, Moro SG, Blasco-Moreno B, Closa-Mosquera A et al. Extensive post-transcriptional buffering of gene expression in the response to severe oxidative stress in baker’s yeast. Sci Rep 2019; 9:11005 [View Article] [PubMed]
     [Google Scholar]
  65. Shcherbik N, Pestov DG. The impact of oxidative stress on ribosomes: from injury to regulation. Cells 2019; 8:1379 [View Article] [PubMed]
     [Google Scholar]
  66. Zhu M, Dai X. Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress. Nucleic Acids Res 2019; 47:7592–7604 [View Article] [PubMed]
     [Google Scholar]
  67. Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M et al. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci USA 2015; 112:3558–3563 [View Article] [PubMed]
     [Google Scholar]
  68. Young AJ, Lowe GM. Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 2001; 385:20–27 [View Article] [PubMed]
     [Google Scholar]
  69. Shen Y, Li J, Gu R, Yue L, Wang H et al. Carotenoid and superoxide dismutase are the most effective antioxidants participating in ROS scavenging in phenanthrene accumulated wheat leaf. Chemosphere 2018; 197:513–525 [View Article] [PubMed]
     [Google Scholar]
  70. Tamoi M, Nagaoka M, Miyagawa Y, Shigeoka S. Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol 2006; 47:380–390 [View Article] [PubMed]
     [Google Scholar]
  71. Uematsu K, Suzuki N, Iwamae T, Inui M, Yukawa H. Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. J Exp Bot 2012; 63:3001–3009 [View Article] [PubMed]
     [Google Scholar]
  72. Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP et al. Over-expressing the C(3) photosynthesis cycle enzyme sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO(2) fumigation (FACE). BMC Plant Biol 2011; 11:123 [View Article] [PubMed]
     [Google Scholar]
  73. Miyagawa Y, Tamoi M, Shigeoka S. Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol 2001; 19:965–969 [View Article] [PubMed]
     [Google Scholar]
  74. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA et al. Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 2005; 138:451–460 [View Article] [PubMed]
     [Google Scholar]
  75. Feng L, Wang K, Li Y, Tan Y, Kong J et al. Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 2007; 26:1635–1646 [View Article] [PubMed]
     [Google Scholar]
  76. Ogren WL. Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 1984; 35:415–442 [View Article]
     [Google Scholar]
  77. Tolbert NE. The C2 oxidative photosynthetic carbon cycle. Annu Rev Plant Physiol 1997; 48:1–25 [View Article] [PubMed]
     [Google Scholar]
  78. Foyer CH, Bloom AJ, Queval G, Noctor G. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 2009; 60:455–484 [View Article] [PubMed]
     [Google Scholar]
  79. Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I et al. Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J Exp Bot 2012; 63:1445–1459 [View Article] [PubMed]
     [Google Scholar]
  80. Guan XQ, Zhao SJ, Li DQ, Shu HR. Photoprotective function of photorespiration in several grapevine cultivars under drought stress. Photosynt 2004; 42:31–36 [View Article]
     [Google Scholar]
  81. Abogadallah GM. Differential regulation of photorespiratory gene expression by moderate and severe salt and drought stress in relation to oxidative stress. Plant Sci 2011; 180:540–547 [View Article] [PubMed]
     [Google Scholar]
  82. Zhou Y, Guo D, Li J, Cheng J, Zhou H et al. Coordinated regulation of anthocyanin biosynthesis through photorespiration and temperature in peach (Prunus persica f. atropurpurea). Tree Genet Genomes 2013; 9:265–278 [View Article]
     [Google Scholar]
  83. León-Vaz A, Romero LC, Gotor C, León R, Vigara J. Effect of cadmium in the microalga Chlorella sorokiniana: a proteomic study. Ecotoxicol Environ Saf 2021; 207:111301 [View Article] [PubMed]
     [Google Scholar]
  84. Bolhàr-Nordenkampf HR. The possible mode of herbicidal action of atrazine basing on the gas exchange and the mode of plant damage after treatment. Zeitschrift für Naturforschung C 1979; 34:923–925 [View Article]
     [Google Scholar]
  85. Busch FA. Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism. Plant J 2020; 101:919–939 [View Article] [PubMed]
     [Google Scholar]
  86. Esperanza M, Houde M, Seoane M, Cid Á, Rioboo C. Does a short-term exposure to atrazine provoke cellular senescence in Chlamydomonas reinhardtii?. Aquat Toxicol 2017; 189:184–193 [View Article] [PubMed]
     [Google Scholar]
  87. Marino D, Dunand C, Puppo A, Pauly N. A burst of plant NADPH oxidases. Trends Plant Sci 2012; 17:9–15 [View Article] [PubMed]
     [Google Scholar]
  88. Otulak-Kozieł K, Kozieł E, Valverde RA. The respiratory burst oxidase homolog d (RbohD) cell and tissue distribution in potato-potato virus y (PVY(NTN)) hypersensitive and susceptible reactions. Int J Mol Sci 2019; 20:2741 [View Article] [PubMed]
     [Google Scholar]
  89. Zhu J, Patzoldt WL, Shealy RT, Vodkin LO, Clough SJ et al. Transcriptome response to glyphosate in sensitive and resistant soybean. J Agric Food Chem 2008; 56:6355–6363 [View Article] [PubMed]
     [Google Scholar]
  90. Dumont S, Rivoal J. Consequences of oxidative stress on plant glycolytic and respiratory metabolism. Front Plant Sci 2019; 10: [View Article]
     [Google Scholar]
  91. Hancock JT, Henson D, Nyirenda M, Desikan R, Harrison J et al. Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. Plant Physiol Biochem 2005; 43:828–835 [View Article] [PubMed]
     [Google Scholar]
  92. Morigasaki S, Shimada K, Ikner A, Yanagida M, Shiozaki K. Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. Mol Cell 2008; 30:108–113 [View Article] [PubMed]
     [Google Scholar]
  93. Hildebrandt T, Knuesting J, Berndt C, Morgan B, Scheibe R. Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub?. Biol Chem 2015; 396:523–537 [View Article] [PubMed]
     [Google Scholar]
  94. Schneider M, Knuesting J, Birkholz O, Heinisch JJ, Scheibe R. Cytosolic GAPDH as a redox-dependent regulator of energy metabolism. BMC Plant Biol 2018; 18:184 [View Article] [PubMed]
     [Google Scholar]
  95. Satre M, Mattei S, Aubry L, Gaudet P, Pelosi L et al. Mitochondrial carrier family: repertoire and peculiarities of the cellular slime mould Dictyostelium discoideum. Biochimie 2007; 89:1058–1069 [View Article] [PubMed]
     [Google Scholar]
  96. Walker JE. The NADH: ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys 1992; 25:253–324 [View Article] [PubMed]
     [Google Scholar]
  97. Massengo-Tiassé RP, Cronan JE. Diversity in enoyl-acyl carrier protein reductases. Cell Mol Life Sci 2009; 66:1507–1517 [View Article] [PubMed]
     [Google Scholar]
  98. Huang J, Silva EN, Shen Z, Jiang B, Lu H. Effects of Glyphosate on Photosynthesis, Chlorophyll Fluorescence and Physicochemical Properties of Cogongrass (’Imperata Cylindrical’ L.) Southern Cross Journals; 2012
     [Google Scholar]
  99. Zobiole LHS, Kremer RJ, Oliveira RS, Constantin J. Glyphosate affects chlorophyll, nodulation and nutrient accumulation of “second generation” glyphosate-resistant soybean (Glycine max L.). Pest Biochem Physiol 2011; 99:53–60 [View Article]
     [Google Scholar]
  100. Mateos-Naranjo E, Redondo-Gómez S, Cox L, Cornejo J, Figueroa ME. Effectiveness of glyphosate and imazamox on the control of the invasive cordgrass Spartina densiflora. Ecotoxicol Environ Saf 2009; 72:1694–1700 [View Article] [PubMed]
     [Google Scholar]
  101. Chen C, Bai LH, Qiao DR, Xu H, Dong GL et al. Cloning and expression study of a putative carotene biosynthesis related (cbr) gene from the halotolerant green alga Dunaliella salina. Mol Biol Rep 2008; 35:321–327 [View Article] [PubMed]
     [Google Scholar]
  102. Tibiletti T, Auroy P, Peltier G, Caffarri S. Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol 2016; 171:2717–2730 [View Article] [PubMed]
     [Google Scholar]
  103. Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB et al. Photosystem II subunit PsbS is involved in the induction of LHCSR protein-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 2016; 291:17478–17487 [View Article] [PubMed]
     [Google Scholar]
  104. Hendrickson L, Furbank RT, Chow WS. A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosyn Res 2004; 82:73–81 [View Article]
     [Google Scholar]
  105. Kramer DM, Johnson G, Kiirats O, Edwards GE. New fluorescence parameters for the determination of Qa redox state and excitation energy fluxes. Photosyn Res 2004; 79:209–218 [View Article]
     [Google Scholar]
  106. Herrmann KM. The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 1995; 7:907–919 [View Article] [PubMed]
     [Google Scholar]
  107. Lawlor DW. Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 2002; 53:773–787 [PubMed]
     [Google Scholar]
  108. Prado R, Rioboo C, Herrero C, Cid A. The herbicide paraquat induces alterations in the elemental and biochemical composition of non-target microalgal species. Chemosphere 2009; 76:1440–1444 [View Article] [PubMed]
     [Google Scholar]
  109. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L et al. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 2010; 105:1141–1157 [View Article] [PubMed]
     [Google Scholar]
  110. Qian H, Pan X, Chen J, Zhou D, Chen Z et al. Analyses of gene expression and physiological changes in Microcystis aeruginosa reveal the phytotoxicities of three environmental pollutants. Ecotoxicology 2012; 21:847–859 [View Article] [PubMed]
     [Google Scholar]
  111. Zablotowicz RM, Reddy KN. Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean. Crop Prot 2007; 26:370–376 [View Article]
     [Google Scholar]
  112. Reddy KN, Bellaloui N, Zablotowicz RM. Glyphosate effect on shikimate, nitrate reductase activity, yield, and seed composition in corn. J Agric Food Chem 2010; 58:3646–3650 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001402
Loading
Photophysiological and transcriptomic response to the broad-spectrum herbicides atrazine and glyphosate in a photosynthetic picoeukaryote
M Gen 11, 001402 (2025); https://doi.org/10.1099/mgen.0.001402
/content/journal/mgen/10.1099/mgen.0.001402
/content/journal/mgen/10.1099/mgen.0.001402
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error