Skip to main content
Log in

Apoplastic reactive oxygen species mediated escape growth of root during illumination in Vigna radiata (L.) Wilczek seedlings

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Besides gravity, roots are also guided by light to grow deep into the soil and sensitivity of roots to light is evidently due to presence of photoreceptors like phototropins. Such light-induced root growth (light-escape growth) presumably involves reactive oxygen species (ROS). Present study explores the possibility of ROS action in this event during early seedling growth of Vigna radiata based on pharmacological evidences. Germinated (20 h) seeds were incubated in dark or light in presence of general ROS scavenger (propyl gallate), specific scavengers of \({\text{O}}_{2}^{ \cdot \; - }\) (copper chloride; CuCl2), H2O2 [dimethylthiourea (DMTU) and potassium iodide (KI)] and ˙OH (sodium benzoate) and ROS-producing enzyme inhibitors [zinc chloride (ZnCl2), inhibitor of NADPH oxidase (NOX); diethyldithiocarbamate (DEDTC), inhibitor of superoxide dismutase (SOD) and salicylhydroxamic acid (SHAM), inhibitor of peroxidase]. Light-induced root growth of 3-day seedlings diminished significantly in case of all the treatments suggesting for a positive role of ROS in light-escape growth. This is supported by elevated level of apoplastic ROS in light grown roots as evident from ROS-specific staining [nitroblue tetrazolium chloride (NBT) for \({\text{O}}_{2}^{ \cdot \; - }\) and 3,3,5,5-tetramethylbenzidine (TMB) for H2O2] and spectrophotometric estimation of apoplastic ROS production (\({\text{O}}_{2}^{ \cdot \; - }\) and H2O2). In addition, higher activity of membrane bound NOX (producing \({\text{O}}_{2}^{ \cdot \; - }\)) and apoplastic class III peroxidase (Prx, producing ˙OH) in light grown roots further corroborates the view that apoplastic ROS (initiated with NOX-generated \({\text{O}}_{2}^{ \cdot \; - }\), which is converted, either spontaneously or by the activity of SOD, to H2O2 and further metabolized by Prx to ˙OH that participates in cell wall relaxation required for growth) is instrumental in light-escape growth of roots.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Airianah OB, Vreeburg RAM, Fry SC (2016) Pectic polysaccharides are attacked by hydroxyl radicals in ripening fruit: evidence from a fluorescent fingerprinting method. Ann Bot 117:441–455. https://doi.org/10.1093/aob/mcv192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Burbach C, Markus K, Zhang Y, Schlicht M, Baluška F (2012) Photophobic behavior of maize roots. Plant Signal Behav 7:874–878

    Article  CAS  Google Scholar 

  • Carter C, Healy R, O’Tool NM, Saqlan Naqvi SM, Ren G, Park S, Beattie GA, Horner HT, Thornburg RW (2007) Tobacco nectarines express a novel NADPH oxidase implicated in the defense of floral reproductive tissues against microorganisms. Plant Physiol 143:389–399. https://doi.org/10.1104/pp.106.089326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Causin HF, Roqueiro G, Petrillo E, Lainez V, Pena LB, Marchetti CF, Gallego SM, Maldonado SI (2012) The control of root growth by reactive oxygen species in Salix nigra Marsh. seedlings. Plant Sci 183:197–205. https://doi.org/10.1016/j.plantsci.2011.08.012

    Article  CAS  PubMed  Google Scholar 

  • Černý M, Habánová H, Berka M, Luklová M, Brzobohatý B (2018) Hydrogen peroxide: its role in plant biology and crosstalk with signalling networks. Int J Mol Sci 19(2812):1–30. https://doi.org/10.3390/ijms19092812

    Article  CAS  Google Scholar 

  • Das S, Kar RK (2017) Reactive oxygen species-mediated promotion of root growth under mild water stress during early seedling stage of Vigna radiata (L.) Wilczek. J Plant Growth Regul 36:338–347

    Article  CAS  Google Scholar 

  • Fick GN, Qualset CO (1975) Genetic control of endosperm amylase activity and gibberellic acid responses in standard-height and short-statured wheats. Proc Natl Acad Sci USA 72:892–895

    Article  CAS  Google Scholar 

  • Foyer C (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot 154:134–142. https://doi.org/10.1016/j.envexpbot.2018.05.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frahry G, Schopfer P (2001) NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:175–183

    Article  CAS  Google Scholar 

  • Galen C, Rabenold JJ, Liscum E (2007a) Light-sensing in roots. Plant Signal Behav 2:106–108

    Article  Google Scholar 

  • Galen C, Rabenold JJ, Liscum E (2007b) Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytol 173:91–99

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:81–96

    Article  Google Scholar 

  • Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220

    Article  CAS  Google Scholar 

  • Gelderen KV, Kang C, Pierik R (2018) Light signaling, root development, and plasticity. Plant Physiol 176:1049–1060

    Article  Google Scholar 

  • Georgiou C, Tairis N, Sotiropoulou A (2000) Hydroxyl radical scavengers inhibit lateral-type sclerotial differentiation and growth in phytopathogenic fungi. Mycologia 92(5):825–834. https://doi.org/10.2307/3761577

    Article  CAS  Google Scholar 

  • Hejl AM, Koster KL (2004) Juglone disrupts root plasma membrane H+-ATPase activity and impairs water uptake, root respiration and growth in soybean (Glycine max) and corn (Zea mays). J Chem Ecol 30:453–471

    Article  CAS  Google Scholar 

  • Kar RK (2011) Plant responses to water stress, role of reactive oxygen species. Plant Signal Behav 6:1741–1745

    Article  CAS  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123

    Article  CAS  Google Scholar 

  • Lushchak V, Semchyshyn H, Lushchak O, Mandryk S (2006) Diethyldithiocarbamate inhibits in vivo Cu, Zn-superoxide dismutase and perturbs free radical processes in the yeast Saccharomyces cerevisiae cells. Biochem Biophys Res Comm 338:1739–1744. https://doi.org/10.1016/j.bbrc.2005.10.147

    Article  CAS  Google Scholar 

  • Majumdar A, Kar RK (2016) Integrated role of ROS and Ca2+ in blue light-induced chloroplast avoidance movement in leaves of Hydrilla verticillata (L.f) Royle. Protoplasma 253:1529–1539. https://doi.org/10.1007/s00709-015-0911-5

    Article  CAS  PubMed  Google Scholar 

  • Majumdar A, Kar RK (2018) Congruence between PM H+-ATPase and NADPH oxidase during root growth: a necessary probability. Protoplasma 255:1129–1137. https://doi.org/10.1007/s00709-018-1217-1

    Article  CAS  PubMed  Google Scholar 

  • Majumdar A, Kar RK (2019) Orchestration of Cu-Zn SOD and class III peroxidase with upstream interplay between NADPH oxidase and PM H+-ATPase mediates root growth in Vigna radiata (L.) Wilczek. J Plant Physiol 232:248–256. https://doi.org/10.1016/j.jplph.2018.11.001

    Article  CAS  PubMed  Google Scholar 

  • Majumdar A, Kar RK (2020) Chloroplast avoidance movement: a novel paradigm of ROS signalling. Photosynth Res 144:109–121. https://doi.org/10.1007/s11120-020-00736-9

    Article  CAS  PubMed  Google Scholar 

  • Mandoli DF, Briggs WR (1982) Optical properties of etiolated plant tissues. Proc Natl Acad Sci USA 79:2902–2906

    Article  CAS  Google Scholar 

  • Minibayeva F, Kolesnikov O, Chasov A, Beckett R, Luthje S, Vylegzhanina N, Buck F, Bottger M (2009) Wound-induced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species. Plant Cell Environ 32(5):497–508

    Article  CAS  Google Scholar 

  • Misra PA, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Article  CAS  Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19. https://doi.org/10.1016/j.tplants.2016.08.002

    Article  CAS  PubMed  Google Scholar 

  • Mo M, Yokawa K, Wan Y, Baluska F (2015) How and why do root apices sense light under the soil surface? Frontiers Plant Sci. https://doi.org/10.3389/fpls.2015.00775

    Article  Google Scholar 

  • Moothoo-Padayachie A, Varghese B, Pammenter NW, GovenderSershen P (2016) Germination associated ROS production and glutathione redox capacity in two recalcitrant-seeded species differing in seed longevity. Botany 94(12):1103–1114. https://doi.org/10.1139/cjb-2016-0130

    Article  CAS  Google Scholar 

  • Neel JK (1948) A limnological investigation of the Psammon in Douglas Lake, Michigan, with especial reference to shoal and shore line dynamics. Trans Am Micr Soc 67:1–53

    Article  Google Scholar 

  • Paddock T, Lima D, Mason ME, Apel K, Armstrong GA (2012) Arabidopsis light-dependent protochlorophyllide oxidoreductase A (PORA) is essential for normal plant growth and development. Plant Mol Biol 78:447–460

    Article  CAS  Google Scholar 

  • Padmanabhan MS, Dinesh-Kumar SP (2010) All hands on deck—the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity. Mol Plant Microbe Interact 23(11):1368–1380. https://doi.org/10.1094/MPMI-05-10-0113

    Article  CAS  PubMed  Google Scholar 

  • Perkins EJ (1963) Penetration of light into littoral soils. J Ecol 51:687–692

    Article  Google Scholar 

  • Podgorska A, Burian M, Szal B (2017) Extra-cellular but extra-ordinarily important for cell: apoplastic reactive oxygen species metabolism. Front Plant Sci 8:1353

    Article  Google Scholar 

  • Qin L, Walk TC, Han P, Chen L, Zhang S, Li Y, Hu X, Xie L, Yang Y, Liu J, Lu X, Yu C, Tian J, Shaff JE, Kochian LV, Liao X, Liao H (2019) Adaptation of roots to nitrogen deficiency revealed by 3D quantification and proteomic analysis. Plant Physiol 179:329–347

    Article  CAS  Google Scholar 

  • Rodrigues ML, Pacheco CA, Chaves MM (1995) Soil-plant relations, root distribution and biomass partitioning in Lupinus albus L. under drought conditions. J Exp Bot 46:947–956

    Article  CAS  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Article  CAS  Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28(6):679–688

    Article  CAS  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    Article  CAS  Google Scholar 

  • Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjärvi J (2012) ROS-talk – how the apoplast, the chloroplast, and the nucleus get the message through. Front Plant Sci 3:1–9. https://doi.org/10.3389/fpls.2012.00292

    Article  CAS  Google Scholar 

  • Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351

    Article  CAS  Google Scholar 

  • Silva-Navas J, Moreno-Risueno MA, Manzano C, Téllez-Robledo B, Navarro-NeilaS CV, Pollmann S, Gallego FJ, del Pozoa JC (2016) Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition. Plant Cell 28:1372–1387. https://doi.org/10.1105/tpc.15.00857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh KL, Chaudhuri A, Kar RK (2015) Role of peroxidase activity and Ca2+ in axis growth during seed germination. Planta 242:997–1007

    Article  CAS  Google Scholar 

  • Singh KL, Mukherjee A, Kar RK (2017) Early axis growth during seed germination is gravitropic and mediated by ROS and calcium. J Plant Physiol 216:181–187

    Article  CAS  Google Scholar 

  • Singh KL, Chaudhuri A, Kar RK (2014) Superoxide and its metabolism during germination and axis growth of Vigna radiata (L.) Wilczek seeds. Plant Signal Behav 9(8):e29278

    Article  Google Scholar 

  • Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol 29:57–63. https://doi.org/10.1016/j.pbi.2015.09.008

    Article  CAS  PubMed  Google Scholar 

  • Wada M, Kong S-G (2018) Actin-mediated movement of chloroplasts. J Cell Sci 131:1–8. https://doi.org/10.1242/jcs.210310

    Article  CAS  Google Scholar 

  • Woolley JT, Stoller EW (1978) Light penetration and light-induced seed germination in soil. Plant Physiol 61:597–600

    Article  CAS  Google Scholar 

  • Yokawa K, Baluska F (2016) The TOR complex: an emergency switch for root behavior. Plant Cell Physiol 57:14–18

    Article  CAS  Google Scholar 

  • Yokawa K, Kagenishi T, Kawano T, Mancuso S, Baluska F (2011) Illumination of Arabidopsis roots induces immediate burst of ROS production. Plant Signal Behav 6:1460–1464

    Article  CAS  Google Scholar 

  • Zhang J, Kirkham MB (1996) Lipid peroxidation in sorghum and sunflower seedlings as affected by ascorbic acid, benzoic acid, and propyl gallate. J Plant Physiol 149:489–493

    Article  CAS  Google Scholar 

Download references

Acknowledgements

One of the authors (AM) gratefully recognizes financial support for the present investigation from University Grants Commission (UGC), New Delhi, India as BSR Fellowship [vide letter F. No. 25-1/2014-15(BSR)/220/2009/(BSR)]. The authors also acknowledge the Departmental research facilities created under UGC-SAP and DST-FIST programs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rup Kumar Kar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by V. P. Singh.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 3845 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dey, T., Das, S., Majumdar, A. et al. Apoplastic reactive oxygen species mediated escape growth of root during illumination in Vigna radiata (L.) Wilczek seedlings. Acta Physiol Plant 43, 145 (2021). https://doi.org/10.1007/s11738-021-03313-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-021-03313-2

Keywords

Navigation