Skip to main content
Log in

He–Ne Laser Enhances Seed Germination and Salt Acclimation in Salvia officinalis Seedlings in a Manner Dependent on Phytochrome and H2O2

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

In the current study the role of H2O2 in He–Ne laser-induced effects on seed germination and post-germinative performance of Salvia officinalis seedlings was assessed under both non-stress and saline conditions. Salinity had adverse impacts on seed germination and root length and decreased seed germination tolerance index. Seed priming with H2O2 and He–Ne laser impacted the seed germination and vigoration in a dose-dependent manner. The optimal effects were gathered by energy dose of 6 J/cm2 laser and concentration of 5 mM H2O2. These pre-treatments enhanced seed germination due to increasing contents of total soluble and reducing sugars and the amylase activity in seeds and improved seedling performance under saline and non-saline conditions. Furthermore, Phy B transcripts were upregulated, salt-accrued oxidative stress was mitigated, and the activities of POD and CAT increased in seedlings primed with H2O2 and laser. Interestingly, applying diphenyleneiodonium (DPI as an inhibitor of NADPH oxidase activity) and N, N-dimethyl thiourea (DMTU as a H2O2 scavenger) arrested the upregulation of phy B gene and abolished stimulatory impact of laser priming on the aforementioned attributes under both non-stress and saline conditions. These novel findings suggest that H2O2 as a downstream signal modulates the impacts of He–Ne laser on seed germination, seedling performance and salt acclimation in sage seedlings, and likely phy B also is involved in these responses.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abu-Elsaoud AM, Tuleukhanov ST (2013) Can He-Ne laser induce changes in oxidative stress and antioxidant activities of wheat cultivars from Kazakhstan and Egypt. J Ecol Health Environ 1(1):39–50

    Google Scholar 

  • Amooaghaie R (2011) The effect of hydro and osmopriming on alfalfa seed germination and antioxidant defenses under salt stress. Afr J Biotechnol 10(33):6269–6275

    Google Scholar 

  • Amooaghaie R, Ahmadi F (2017) Triangular interplay between ROS, ABA and GA in dormancy alleviation of Bunium persicum seeds by cold stratification. Russ J Plant Physiol 64(4):588–599

    Article  Google Scholar 

  • Amooaghaie R, Nikzad K (2013) The role of nitric oxide in priming-induced low-temperature tolerance in two genotypes of tomato. Seed Sci Res 23(2):123–131

    Article  Google Scholar 

  • Amooaghaie R, Tabatabaie F (2017) Osmopriming-induced salt tolerance during seed germination of alfalfa most likely mediates through H2O2 signaling and upregulation of heme oxygenase. Protoplasma 254(4):1791–1803

    Article  Google Scholar 

  • Amooaghaie R, Nikzad K, Shareghi B (2010) The effect of priming on emergence and biochemical changes of tomato seeds under suboptimal temperatures. Seed Sci Technol 38(2):508–512

    Article  Google Scholar 

  • Bailly C, EL-maarouf-bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. Comptes Rendus Biologies 331(10):806–814

    Article  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signaling. J Exp Bot 65(5):1229–1240. https://doi.org/10.1093/jxb/ert375

    Article  Google Scholar 

  • Chen K, Arora R (2013) Priming memory invokes seed stress-tolerance. Environ Exp Bot 94:33–45

    Article  Google Scholar 

  • Cheng H, Zhang Q, Guo D (2013) Genes that respond to H2O2 are also evoked under light in Arabidopsis. Mol Plant 6(1):226–228

    Article  Google Scholar 

  • Cheng H, Liang Q, Chen X, Zang Y, Qiao F, Gao D (2019) Hydrogen peroxide facilitates Arabidopsis seedling establishment by interacting with light signalling pathway in the dark. Plant Cell Environ 42(4):1302–1317

    Article  Google Scholar 

  • Christou A, Manganaris GA, Fotopoulos V (2014) Systemic mitigation of salt stress by hydrogen peroxide and sodium nitroprusside in strawberry plants via transcriptional regulation of enzymatic and non-enzymatic antioxidants. Environ Exp Bot 107:46–54

    Article  Google Scholar 

  • Costilla-Hermosillo MG, Ortiz-Morales M, Loza-Cornejo S, Frausto-Reyes, Metwally SA (2019) Laser biostimulation for improving seeds germinative capacity and seedlings growth of Prosopis laevigata and Jacaranda mimosifolia. Maderay Bosques 25(2):e2521665. https://doi.org/10.21829/myb.2019.2521665

  • Devireddy AR, Liscum E, Mittler R (2020) Phytochrome B is required for systemic stomatal responses and reactive oxygen species signaling during light stress. Plant Physiol 184:1563–1572

  • Drozd D, Szajner H, Jezierski A (1999) Electron paramagnetic resonance [EPR] investigations of laser induced free radicals in spring wheat grains. Int Agrophys 13(3):343–346

  • Ellouzi H, Oueslati S, Hessini K, Rabhi M, Abdelly C (2021) Seed-priming with H2O2 alleviates subsequent salt stress by preventing ROS production and amplifying antioxidant defense in cauliflower seeds and seedlings. Sci Hortic 288:110360

    Article  Google Scholar 

  • Gao LM, Li YF, Han R (2015) He-Ne laser preillumination improves the resistance of tall fescue (Festuca arundinacea Schreb) seedlings to high saline conditions. Protoplasma 252:1135–1148

    Article  Google Scholar 

  • Gao L, Li Y, Shen Z, Han R (2018) Responses of He-Ne laser on agronomic traits and the crosstalk between UVR8 signaling and phytochrome B signaling pathway in Arabidopsis thaliana subjected to supplementary ultraviolet-B (UV-B) stress. Protoplasma 255:761–771

    Article  Google Scholar 

  • Hashemi M, Armaki MA (2015) Impact of salinity stress on seed germination characteristics of two medicinal species Salvia verticillata and Salvia limbata. Biological Forum Satya Prakashan 7(1):1409–1413

  • Hernández A, Dominguez P, Cruz O, Ivanov R, Carballo C, Zepeda B (2010) Laser in Agriculture. Int Agrophys 24:407–422

    Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    Article  Google Scholar 

  • Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46

    Article  Google Scholar 

  • Ishibashi Y, Kasa S, Sakamoto M, Aoki K, Kai K, Yuasa T, Hanada A, Yamaguchi S, Iwaya-Inoue M (2015) A role for reactive oxygen species produced by NADPH oxidases in the embryo and aleurone cells in barley seed germination. PLoS ONE 10:e0143173

    Article  Google Scholar 

  • Jamil Y, Perveen R, Ashraf M, Ali Q, Lqbal M, Ahmad MR (2013) He–Ne laser-induced changes in germination, thermodynamic parameters, internal energy, enzyme activities and physiological attributes of wheat during germination and early growth. Laser Phys Lett 10:045606

    Article  Google Scholar 

  • Jiang XW, Zhang CR, Wang WH, Xu GH, Zhang HY (2020) Seed priming improves seed germination and seedling growth of Isatis indigotica Fort. under salt stress. HortScience 55:647–650

    Article  Google Scholar 

  • Johnson R, Puthur JT (2021) Seed priming as a cost effective technique for developing plants with cross tolerance to salinity stress. J Plant Biochem Physiol 162:247–257

    Article  Google Scholar 

  • Junior CAS, D’amico-Damião V, Carvalho RF (2021) Phytochrome type B family: The abiotic stress responses signaller in plants. Ann Appl Biol 178:135–148

    Article  Google Scholar 

  • Khamis G, Hassan M, Morsy M, Ebrahim MA, Abd-Elsalam RM, Badawy SAE, Azouz AA, Gala M (2020) Innovative application of helium-neon laser: enhancing the germination of Adansonia digitata and evaluating the hepatoprotective activities in mice. Environ Sci Pollut Res 27:26520–26531

    Article  Google Scholar 

  • Khodabakhsh F, Amooaghaie R, Mostajeran A (2014) Effect of hydro-and osmo-priming on membrane deterioration, proline accumulation and H2O2 scavenging enzymes in two salt stressed chickpea cultivars. Environ Eng Manag J 13(3):619–626. https://doi.org/10.30638/eemj.2014.065

  • Konigshofer H, Tromballa HW, Loppert HG (2008) Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production Plant. Cell and Environ 31:1771–1780

    Article  Google Scholar 

  • Lariguet P, Ranocha P, De Meyer M, Barbier O, Penel C, Dunand C (2013) Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta 238:381–395

    Article  Google Scholar 

  • Legris M, Ince YC, Fankhauser C (2019) Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat Commun 10:1–15

    Article  Google Scholar 

  • Li Z, Gao Y, Zhang Y (2018) Reactive oxygen species and gibberellin acid mutual induction to regulate tobacco seed germination. Front Plant Sci 9:1279

    Article  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  Google Scholar 

  • Manickavelu A, Kambara K, Mishina K, Koba T (2007) An efficient method for purifying high quality RNA from wheat pistils. Colloids Surf B Biointerfaces 54:254–258

    Article  Google Scholar 

  • Muthusamy A, Kudwa PP, Prabhu V, Mahato KK, Babu VS, Raon MR, Gopinath PM, Satyamoorthy K (2012) Influence of Helium-Neon laser irradiation on seed germination in vitro and physico-biochemical characters in seedlings of brinjal (Solanum melongena L.) var. Mattu Gulla J Photochem Photobiol 88:1227–1235

    Article  Google Scholar 

  • Nabaei M, Amooaghaie R (2019) Interactive effect of melatonin and sodium nitroprusside on seed germination and seedling growth of Catharanthus roseusunder cadmium stress. Russ J Plant Physiol 66(1):128–139

    Article  Google Scholar 

  • Paik I, Chen F, Pham VN (2019) A phyB-PIF1-SPA1 kinase regulatory complex promotes photomorphogenesis in Arabidopsis. Nat Commun 10:1–17

    Article  Google Scholar 

  • Perveen R, Jamil Y, Ashraf M, Ali Q, Lqbal M, Ahmad MR (2011) He-Ne laser-induced improvement in biochemical, physiological, growth and yield characteristics in sunflower (Helianthus annuus L.). J Photochem Photobiol 87:1453–1463

    Article  Google Scholar 

  • Perveen R, Wang X, Jamil Y, Ali Q, Ali S, Zakaria MQ, Afzaal M, Kasana RA, Saleem MH, Fiaz S (2021) Quantitative determination of the effects of He–Ne laser irradiation on seed thermodynamics, germination attributes and metabolites of safflower (Carthamus tinctorius L.) in relation with the activities of germination enzymes. Agronomy 11:1411

    Article  Google Scholar 

  • Pirooz P, Amooaghaie R, Ahadi AM, Sharififar F, Torkzadeh-Mahani M (2021) Silicon and nitric oxide synergistically modulate the production of essential oil and rosmarinic acid in Salvia officinalis under Cu stress Protoplasma. https://doi.org/10.1007/s00709-021-01708-z

  • Podlesna A, Gladyszewska B, Podlesny J, Zgrajka W (2015) Changes in the germination process and growth of pea in effect of laser seed irradiation. Int Agrophys 29:485–492

  • Podlesny J, Stochmal A, Podleśna A, Misiak LE (2012) Effect of laser light treatment on some biochemical and physiological processes in seeds and seedlings of white lupine and faba bean. J Plant Growth Regul 67:227–233

    Article  Google Scholar 

  • Qiu Z, Li Q, Bi Z, Yue M (2012) Hydrogen peroxide acts as a signal molecule in CO2 laser pretreatment-induced osmotic tolerance in wheat seedling. Plant Soil Environ 57:403–408

    Article  Google Scholar 

  • Rodrigues MHBS, Da Silva JN, Alves EU, Bruno RDLA (2021) Hydrogen peroxide as a mitigation of salt stress on the germination of Myracroduon urundeuva (Allemão). Engl Seeds Scientia Forestalis 49(130):e3557

    Google Scholar 

  • Sarreta Y, De Castro Neto JC (2021) Effects of 660 nm laser irradiation of soybean seeds on germination, emergence and seedling growth. Acta Agroph 28:5–18

    Article  Google Scholar 

  • Shafique H, Jamil Y, UlHaq Z, Mujahib T, Ullah Khan A, Lqbal M, Abbas M (2017) Low power continuous wave-laser seed irradiation effect on Moringa oleifera germination, seedling growth and biochemical attributes. J Photochem Photobiol B 170:314–323

    Article  Google Scholar 

  • Somogyi M (1952) Estimation of sugars by colorimetric method. J Biol Chem 200:245

    Google Scholar 

  • Srivastava AK, Suresh Kumar J, Suprasanna P (2021) Seed ‘primeomics’: plants memorize their germination under stress. Biol Rev. https://doi.org/10.1111/brv.12722

    Article  Google Scholar 

  • Swathy PS, Kiran KR, Joshi MB, Mahato KK, Muthusamy A (2021) He–Ne laser accelerates seed germination by modulating growth hormones and reprogramming metabolism in brinjal. Sci Rep 11:1–16

    Article  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth B, Remm M, Rozen S (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115–e115

    Article  Google Scholar 

  • Vafadar F, Amooaghaie R, Ehsanzadeh P, Ghanati F, Sajedi RH (2020) Crosstalk between melatonin and Ca2+/CaM evokes systemic salt tolerance in Dracocephalum kotschyi. J Plant Physiol 252:153237

    Article  Google Scholar 

  • Valivand M, Amooaghaie R, Ahadi A (2019) Interplay between hydrogen sulfide and calcium/calmodulin enhances systemic acquired acclimation and antioxidative defense against nickel toxicity in zucchini. Environ Exp Bot 158:40–50. https://doi.org/10.1016/j.envexpbot.2018.11.006

    Article  Google Scholar 

  • Valivand M, Amooaghaie R, Ahadi A (2019) Seed priming with H2S and Ca2+ trigger signal memory that induces cross-adaptation against nickel stress in zucchini seedlings. J Plant Biochem Physiol 143:286–298

    Article  Google Scholar 

  • Wojtyla L, Lechowska K, Kubala S, Garnczarska M (2016) Different modes of hydrogen peroxide action during seed germination. Front Plant Sci 7:66

    Article  Google Scholar 

  • Xie YJ, Xu S, Han B, Wu MZ, Yuan X, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292

    Article  Google Scholar 

  • Yaldiz G, Camlica M (2021) Selenium and salt interactions in sage (Salvia officinalis L.): Growth and yield, chemical content, ion uptake. Ind Crops Prod 171:113855

    Article  Google Scholar 

  • Zhang Y, Chen B, Xu Z, Shi Z, Chen S, Huang X, Chen J, Wang X (2014) Involvement of reactive oxygen species in endosperm cap weakening and embryo elongation growth during lettuce seed germination. J Exp Bot 65:3189–3200

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by Plant Science Department of Shahrekord University, Iran. The authors are very grateful to Dr. Mohammad Moradi and Mr Mohsen Zamani for providing laser equipment and helping in laser irradiation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rayhaneh Amooaghaie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Peter Nick.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mardani Korrani, F., Amooaghaie, R. & Ahadi, A. He–Ne Laser Enhances Seed Germination and Salt Acclimation in Salvia officinalis Seedlings in a Manner Dependent on Phytochrome and H2O2. Protoplasma 260, 103–116 (2023). https://doi.org/10.1007/s00709-022-01762-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-022-01762-1

Keywords

Navigation