Seeds sense temperature, nutrient levels and light conditions to inform decision making on the timing of germination. Limited light availability for photoblastic species results in irregular germination timing and losses of population germination percentage. Seed industries are therefore looking for interventions to mitigate this risk. A growing area of research is water treated with gas plasma (GPAW), in which the formed solution is a complex consisting of reactive oxygen and nitrogen species. Gas plasma technology is widely used for sterilisation and is an emerging technology in the food processing industry. The use of the GPAW on seeds has previously led to an increase in germination performance, often attributed to bolstered antioxidant defence mechanisms. However, there is a limited understanding of how the solution may influence the mechanisms that govern seed dormancy and whether photoreceptor-driven germination mechanisms are affected. In our work, we studied how GPAW can influence the mechanisms that govern photo-dependent dormancy, isolating the effects at low fluence response (LFR) and very low fluence response (VLFR). The two defined light intensity thresholds affect germination through different phytochrome photoreceptors, PHYB and PHYA, respectively; we found that GPAW showed a significant increase in population germination percentage under VLFR and further described how each treatment affects key physiological regulators.

Department of Biological Sciences Royal Holloway University of London Egham TW20 0EX UK

Division of Advanced Nuclear Engineering Pohang University of Science and Technology Pohang 790 784 Korea

Laboratory of Growth Regulators Institute of Experimental Botany Czech Academy of Sciences and Faculty of Science Palacký University CZ 78371 Olomouc Czech Republic

Wolfson School of Mechanical Electrical and Manufacturing Engineering Loughborough University Leicestershire LE11 3TU UK

Zobrazit více v PubMed

Finch-Savage W., Bassel G. Seed vigour and crop establishment: Extending performance beyond adaptation. J. Exp. Bot. 2016;67:567–591. doi: 10.1093/jxb/erv490. PubMed DOI

Finch-Savage W.E., Leubner-Metzger G. Seed dormancy and the control of germination. New Phytol. 2006;171:501–523. doi: 10.1111/j.1469-8137.2006.01787.x. PubMed DOI

Finch-Savage W.E., Footitt S. Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments. J. Exp. Bot. 2017;68:843–856. doi: 10.1093/jxb/erw477. PubMed DOI

Batlla D., Benech-Arnold R.L. Weed seed germination and the light environment: Implications for weed management. Weed Biol. Manag. 2014;14:77–87. doi: 10.1111/wbm.12039. DOI

Kim W.-Y., Fujiwara S., Suh S.-S., Kim J., Kim Y., Han L., David K., Putterill J., Nam H.G., Somers D.E. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature. 2007;449:356–360. doi: 10.1038/nature06132. PubMed DOI

Strasser B., Sánchez-Lamas M., Yanovsky M., Casal J., Cerdán P. Arabidopsis thaliana life without phytochromes. Proc. Natl. Acad. Sci. USA. 2010;107:4776–4781. doi: 10.1073/pnas.0910446107. PubMed DOI PMC

Legris M., Ince Y.Ç., Fankhauser C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 2019;10:5219. doi: 10.1038/s41467-019-13045-0. PubMed DOI PMC

Sullivan J.A., Deng X.W. From seed to seed: The role of photoreceptors in Arabidopsis development. Dev. Biol. 2003;260:289–297. doi: 10.1016/S0012-1606(03)00212-4. PubMed DOI

Botto J.F., Sanchez R.A., Whitelam G.C., Casal J.J. Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiol. 1996;110:439–444. doi: 10.1104/pp.110.2.439. PubMed DOI PMC

Shinomura T. Phytochrome regulation of seed germination. J Plant Res. 1997;110:151–161. doi: 10.1007/BF02506854. PubMed DOI

Borthwick H.A., Hendricks S.B., Parker M.W., Toole E.H., Toole V.K. A reversible photoreaction controlling seed germination. Proc. Natl. Acad. Sci. USA. 1952;38:662–666. doi: 10.1073/pnas.38.8.662. PubMed DOI PMC

Jiang Z., Xu G., Jing Y., Tang W., Lin R. Phytochrome B and REVEILLE1/2-mediated signalling controls seed dormancy and germination in Arabidopsis. Nat. Commun. 2016;7:12377. doi: 10.1038/ncomms12377. PubMed DOI PMC

Lee K.P., Piskurewicz U., Turečková V., Carat S., Chappuis R., Strnad M., Fankhauser C., Lopez-Molina L. Spatially and genetically distinct control of seed germination by phytochromes A and B. Genes Dev. 2012;26:1984–1996. doi: 10.1101/gad.194266.112. PubMed DOI PMC

Yan A., Chen Z. The control of seed dormancy and germination by temperature, light and nitrate. Bot. Rev. 2020;86:39–75. doi: 10.1007/s12229-020-09220-4. DOI

Dirk L.M.A., Kumar S., Majee M., Downie A.B. PHYTOCHROME INTERACTING FACTOR1 interactions leading to the completion or prolongation of seed germination. Plant Signal. Behav. 2018;13:e1525999. doi: 10.1080/15592324.2018.1525999. PubMed DOI PMC

Footitt S., Douterelo-Soler I., Clay H., Finch-Savage W.E. Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc. Natl. Acad. Sci. USA. 2011;108:20236–20241. doi: 10.1073/pnas.1116325108. PubMed DOI PMC

Barros-Galvão T., Dave A., Gilday A.D., Harvey D., Vaistij F.E., Graham I.A. ABA INSENSITIVE4 promotes rather than represses PHYA-dependent seed germination in Arabidopsis thaliana. New Phytol. 2020;226:953–956. doi: 10.1111/nph.16363. PubMed DOI PMC

Arana M.V., Burgin M.J., de Miguel L.C., Sánchez R.A. The very-low-fluence and high-irradiance responses of the phytochromes have antagonistic effects on germination, mannan-degrading activities, and DfGA3ox transcript levels in Datura ferox seeds. J. Exp. Bot. 2007;58:3997–4004. doi: 10.1093/jxb/erm256. PubMed DOI

Steinbrecher T., Leubner-Metzger G. The biomechanics of seed germination. J. Exp. Bot. 2017;68:765–783. doi: 10.1093/jxb/erw428. PubMed DOI

Ogawa M., Hanada A., Yamauchi Y., Kuwahara A., Kamiya Y., Yamaguchi S. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell. 2003;15:1591–1604. doi: 10.1105/tpc.011650. PubMed DOI PMC

Bourke P., Ziuzina D., Boehm D., Cullen P., Keener K. The potential of cold plasma for safe and sustainable food production. Trends Biotechnol. 2018;36:615–626. doi: 10.1016/j.tibtech.2017.11.001. PubMed DOI

Weltmann K.-D., Kolb J.F., Holub M., Uhrlandt D., Šimek M., Ostrikov K., Hamaguchi S., Cvelbar U., Černák M., Locke B., et al. The future for plasma science and technology. Plasma Process. Polym. 2019;16:1800118. doi: 10.1002/ppap.201800118. DOI

Araújo S.d.S., Paparella S., Dondi D., Bentivoglio A., Carbonera D., Balestrazzi A. Physical Methods for Seed Invigoration: Advantages and Challenges in Seed Technology. Front. Plant Sci. 2016;7:646. doi: 10.3389/fpls.2016.00646. PubMed DOI PMC

Pedrini S., Merritt D.J., Stevens J., Dixon K. Seed Coating: Science or Marketing Spin? Trends Plant Sci. 2017;22:106–116. doi: 10.1016/j.tplants.2016.11.002. PubMed DOI

Sharma K.K., Singh U.S., Sharma P., Kumar A., Sharma L. Seed treatments for sustainable agriculture—A review. J. Appl. Nat. Sci. 2015;7:521–539. doi: 10.31018/jans.v7i1.641. DOI

Lukes P., Dolezalova E., Sisrova I., Clupek M. Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: Evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H2O2and HNO2. Plasma Sources Sci. Technol. 2014;23:015019. doi: 10.1088/0963-0252/23/1/015019. DOI

Montazersadgh F., Wright A., Ren J., Shaw A., Neretti G., Bandulasena H., Iza F. Influence of the On-time on the Ozone Production in Pulsed Dielectric Barrier Discharges. Plasma. 2019;2:39–50. doi: 10.3390/plasma2010005. DOI

Bradu C., Kutasi K., Magureanu M., Puač N., Živković S. Reactive nitrogen species in plasma-activated water: Generation, chemistry and application in agriculture. J. Phys. D Appl. Phys. 2020;53:223001. doi: 10.1088/1361-6463/ab795a. DOI

Shaw A., Shama G., Iza F. Emerging applications of low temperature gas plasmas in the food industry. Biointerphases. 2015;10:029402. doi: 10.1116/1.4914029. PubMed DOI

Adamovich I., Baalrud S.D., Bogaerts A., Bruggeman P.J., Cappelli M., Colombo V., Czarnetzki U., Ebert U., Eden J.G., Favia P., et al. The 2017 Plasma Roadmap: Low temperature plasma science and technology. J. Phys. D Appl. Phys. 2017;50:323001. doi: 10.1088/1361-6463/aa76f5. DOI

Grainge G., Nakabayashi K., Steinbrecher T., Kennedy S., Ren J., Iza F., Leubner-Metzger G. Molecular mechanisms of seed dormancy release by gas plasma-activated water technology. J. Exp. Bot. 2022 doi: 10.1093/jxb/erac150. PubMed DOI PMC

Zhou L., Ye Y., Zhao Q., Du X., Zakari S., Su D., Pan G., Cheng F. Suppression of ROS generation mediated by higher InsP3 level is critical for the delay of seed germination in lpa rice. Plant Growth Regul. 2018;85:411–424. doi: 10.1007/s10725-018-0402-8. DOI

Leubner-Metzger G. Functions and regulation of ß-1,3-glucanase during seed germination, dormancy release and after-ripening. Seed Sci. Res. 2003;13:17–34. doi: 10.1079/SSR2002121. DOI

Leubner-Metzger G. Seed after-ripening and over-expression of class I ß-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta. 2002;215:959–968. doi: 10.1007/s00425-002-0837-y. PubMed DOI

Dong S., Liu Y., Zhang M., Zhang J., Wang J.H., Li Z.H. Maternal light environment interacts with genotype in regulating seed photodormancy in tobacco. Environ. Exp. Bot. 2022;194:104745. doi: 10.1016/j.envexpbot.2021.104745. DOI

Fragoso V., Oh Y., Kim S., Gase K., Baldwin I. Functional specialization of Nicotiana attenuata phytochromes in leaf development and flowering time. J. Integr. Plant Biol. 2017;59:205–224. doi: 10.1111/jipb.12516. PubMed DOI

Adam E., Szell M., Szekeres M., Schäfer E., Nagy F. The developmental and tissue-specific expression of tobacco phytochrome-A genes. Plant J. 1994;6:283–293. doi: 10.1046/j.1365-313X.1994.06030283.x. DOI

Fernández A.P., Gil P., Valkai I., Nagy F., Schäfer E. Analysis of the Function of the Photoreceptors Phytochrome B and Phytochrome D in Nicotiana plumbaginifolia and Arabidopsis thaliana. Plant Cell Physiol. 2005;46:790–796. doi: 10.1093/pcp/pci073. PubMed DOI

Oh Y., Fragoso V., Guzzonato F., Kim S., Park C., Baldwin I. Root-expressed phytochromes B1 and B2, but not PhyA and Cry2, regulate shoot growth in nature. Plant Cell Environ. 2018;41:2577–2588. doi: 10.1111/pce.13341. PubMed DOI

Casal J.J., Sanchez R.A. Phytochromes and seed germination. Seed Sci. Res. 1998;8:317–329. doi: 10.1017/S0960258500004256. DOI

Borisjuk L., Rolletschek H. The oxygen status of the developing seed. New Phytol. 2009;182:17–30. doi: 10.1111/j.1469-8137.2008.02752.x. PubMed DOI

Mérai Z., Graeber K., Wilhelmsson P., Ullrich K.K., Arshad W., Grosche C., Tarkowská D., Turečková V., Strnad M., Rensing S.A., et al. Aethionema arabicum: A novel model plant to study the light control of seed germination. J. Exp. Bot. 2019;70:3313–3328. doi: 10.1093/jxb/erz146. PubMed DOI PMC

Bolouki N., Kuan W.-H., Huang Y.-Y., Hsieh J.-H. Characterizations of a Plasma-Water System Generated by Repetitive Microsecond Pulsed Discharge with Air, Nitrogen, Oxygen, and Argon Gases Species. Appl. Sci. 2021;11:6158. doi: 10.3390/app11136158. DOI

Lee K.J.D., Dekkers B.J.W., Steinbrecher T., Walsh C.T., Bacic A., Bentsink L., Leubner-Metzger G., Knox J.P. Distinct cell wall architectures in seed endosperms in representatives of the Brassicaceae and Solanaceae. Plant Physiol. 2012;160:1551–1566. doi: 10.1104/pp.112.203661. PubMed DOI PMC

Okamoto M., Kuwahara A., Seo M., Kushiro T., Asami T., Hirai N., Kamiya Y., Koshiba T., Nambara E. CYP707A1 and CYP707A2, which encode ABA 8’-hydroxylases, are indispensable for a proper control of seed dormancy and germination in Arabidopsis. Plant Physiol. 2006;141:97–107. doi: 10.1104/pp.106.079475. PubMed DOI PMC

Leubner-Metzger G. Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways. Planta. 2001;213:758–763. doi: 10.1007/s004250100542. PubMed DOI

Zhao H., Bao Y. PIF4: Integrator of light and temperature cues in plant growth. Plant Sci. 2021;313:111086. doi: 10.1016/j.plantsci.2021.111086. PubMed DOI

Saud S., Shi Z., Xiong L., Danish S., Datta R., Ahmad I., Fahad S., Banout J. Recognizing the Basics of Phytochrome-Interacting Factors in Plants for Abiotic Stress Tolerance. Plant Stress. 2022;3:100050. doi: 10.1016/j.stress.2021.100050. DOI

Locke B.R., Lukea P., Brisset J.L. In: Plasma Chemistry and Catalysis in Gases and Liquids. Vasile I.P., Magureanu M., Petr L., editors. Wiley-VCH; Weinheim, Germany: 2012. pp. 185–241. Chapter 6.

Gibbs D.J., Md Isa N., Movahedi M., Lozano-Juste J., Mendiondo G.M., Berckhan S., Marín-de la Rosa N., Vicente Conde J., Sousa Correia C., Pearce S.P., et al. Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol. Cell. 2014;53:369–379. doi: 10.1016/j.molcel.2013.12.020. PubMed DOI PMC

Bethke P.C., Libourel I.G.L., Jones R.L. Nitric oxide reduces seed dormancy in Arabidopsis. J. Exp. Bot. 2006;57:517–526. doi: 10.1093/jxb/erj060. PubMed DOI

Liu Y., Zhang J. Rapid accumulation of NO regulates ABA catabolism and seed dormancy during imbibition in Arabidopsis. Plant Signal. Behav. 2009;4:905–907. doi: 10.4161/psb.4.9.9532. PubMed DOI PMC

Albertos P., Romero-Puertas M.C., Tatematsu K., Mateos I., Sánchez-Vicente I., Nambara E., Lorenzo O. S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat. Commun. 2015;6:8669. doi: 10.1038/ncomms9669. PubMed DOI PMC

Holman T.J., Jones P.D., Russell L., Medhurst A., Ubeda Tomas S., Talloji P., Marquez J., Schmuths H., Tung S.A., Taylor I., et al. The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2009;106:4549–4554. doi: 10.1073/pnas.0810280106. PubMed DOI PMC

Yan D., Easwaran V., Chau V., Okamoto M., Ierullo M., Kimura M., Endo A., Yano R., Pasha A., Gong Y., et al. NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat. Commun. 2016;7:13179. doi: 10.1038/ncomms13179. PubMed DOI PMC

Li Z., Gao Y., Zhang Y., Lin C., Gong D., Guan Y., Hu J. Reactive Oxygen Species and Gibberellin Acid Mutual Induction to Regulate Tobacco Seed Germination. Front. Plant Sci. 2018;9:1279. doi: 10.3389/fpls.2018.01279. PubMed DOI PMC

Müller K., Linkies A., Vreeburg R.A.M., Fry S.C., Krieger-Liszkay A., Leubner-Metzger G. In vivo cell wall loosening by hydroxyl radicals during cress (Lepidium sativum L.) seed germination and elongation growth. Plant Physiol. 2009;150:1855–1865. doi: 10.1104/pp.109.139204. PubMed DOI PMC

Wright A., Bandulasena H., Ibenegbu C., Leak D., Holmes T., Zimmerman W., Shaw A., Iza F. Dielectric barrier discharge plasma microbubble reactor for pretreatment of lignocellulosic biomass. AIChE J. 2018;64:3803–3816. doi: 10.1002/aic.16212. PubMed DOI PMC

Eisenberg G. Colorimetric Determination of Hydrogen Peroxide. Ind. Eng. Chem. Anal. Ed. 1943;15:327–328. doi: 10.1021/i560117a011. DOI

García-Robledo E., Corzo A., Papaspyrou S. A fast and direct spectrophotometric method for the sequential determination of nitrate and nitrite at low concentrations in small volumes. Mar. Chem. 2014;162:30–36. doi: 10.1016/j.marchem.2014.03.002. DOI

Graeber K., Linkies A., Wood A., Leubner-Metzger G. A guideline to family-wide comparative state-of-the-art quantitative RT-PCR analysis exemplified with a Brassicaceae cross-species seed germination case study. Plant Cell. 2011;23:2045–2063. doi: 10.1105/tpc.111.084103. PubMed DOI PMC

Sierro N., Battey J.N.D., Ouadi S., Bakaher N., Bovet L., Willig A., Goepfert S., Peitsch M.C., Ivanov N.V. The tobacco genome sequence and its comparison with those of tomato and potato. Nat. Commun. 2014;5:3833. doi: 10.1038/ncomms4833. PubMed DOI PMC

Dekkers B.J., Willems L., Bassel G.W., van Bolderen-Veldkamp R.P.M., Ligterink W., Hilhorst H.W.M., Bentsink L. Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol. 2012;53:28–37. doi: 10.1093/pcp/pcr113. PubMed DOI

Seed priming with gas plasma-activated water in Ethiopia's "orphan" crop tef (Eragrostis tef)