Priming with Small Molecule-Based Biostimulants to Improve Abiotic Stress Tolerance in Arabidopsis thaliana
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000827
Research, Development and Education (OP RDE), Czech Republic
PubMed
35631712
PubMed Central
PMC9144751
DOI
10.3390/plants11101287
PII: plants11101287
Knihovny.cz E-zdroje
- Klíčová slova
- abiotic stress, biostimulant, growth, plant phenotyping,
- Publikační typ
- časopisecké články MeSH
Biostimulants became a hotspot in the fight to alleviate the consequences of abiotic stresses in crops. Due to their complex nature, it is challenging to obtain stable and reproducible final products and more challenging to define their mechanism of action. As an alternative, small molecule-based biostimulants, such as polyamines have promoted plant growth and improved stress tolerance. However, profound research about their mechanisms of action is still missing. To go further, we tested the effect of putrescine (Put) and its precursor ornithine (Orn) and degradation product 1,3-diaminopropane (DAP) at two different concentrations (0.1 and 1 mM) as a seed priming on in vitro Arabidopsis seedlings grown under optimal growth conditions, osmotic or salt stress. None of the primings affected the growth of the seedlings in optimal conditions but altered the metabolism of the plants. Under stress conditions, almost all primed plants grew better and improved their greenness. Only Orn-primed plants showed different plant responses. Interestingly, the metabolic analysis revealed the implication of the N- acetylornithine and Orn and polyamine conjugation as the leading player regulating growth and development under control and stress conditions. We corroborated polyamines as very powerful small molecule-based biostimulants to alleviate the adverse abiotic stress effects.
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Bouras E., Jarlan L., Khabba S., Er-Raki S., Dezetter A., Sghir F., Tramblay Y. Assessing the Impact of Global Climate Changes on Irrigated Wheat Yields and Water Requirements in a Semi-Arid Environment of Morocco. Sci. Rep. 2019;9:19142. doi: 10.1038/s41598-019-55251-2. PubMed DOI PMC
Tramblay Y., Koutroulis A., Samaniego L., Vicente-Serrano S.M., Volaire F., Boone A., Le Page M., Llasat M.C., Albergel C., Burak S., et al. Challenges for Drought Assessment in the Mediterranean Region under Future Climate Scenarios. Earth Sci. Rev. 2020;210:103348.
Corwin D.L. Climate Change Impacts on Soil Salinity in Agricultural Areas. Eur. J. Soil Sci. 2021;72:842–862.
Qadir M., Quillérou E., Nangia V., Murtaza G., Singh M., Thomas R.J., Drechsel P., Noble A.D. Economics of Salt-Induced Land Degradation and Restoration. Nat. Resour. Forum. 2014;38:282–295. doi: 10.1111/1477-8947.12054. DOI
FAO Land and Plant Nutrition Management Service. [(accessed on 19 April 2022)]. Available online: https://scholar.google.com/scholar_lookup?title=FAOLandandPlantNutritionManagementService&publication_year=2010&author=FAO.
Awasthi R., Kaushal N., Vadez V., Turner N.C., Berger J., Siddique K.H.M., Nayyar H. Individual and Combined Effects of Transient Drought and Heat Stress on Carbon Assimilation and Seed Filling in Chickpea. Funct. Plant Biol. 2014;41:1148–1167. PubMed
Lyon C., Saupe E.E., Smith C.J., Hill D.J., Beckerman A.P., Stringer L.C., Marchant R., McKay J., Burke A., O’Higgins P., et al. Climate Change Research and Action Must Look beyond 2100. Glob. Chang. Biol. 2022;28:349–361. doi: 10.1111/gcb.15871. PubMed DOI
Le Mouël C., Forslund A. How Can We Feed the World in 2050? A Review of the Responses from Global Scenario Studies. Eur. Rev. Agric. Econ. 2017;44:541–591. doi: 10.1093/erae/jbx006. DOI
Brodersen C.R., Roddy A.B., Wason J.W., McElrone A.J. Functional Status of Xylem Through Time. Annu. Rev. Plant Biol. 2019;70:407–433. PubMed
Ceccarelli S., Grando S., Maatougui M., Michael M., Slash M., Haghparast R., Rahmanian M., Taheri A., Al-Yassin A., Benbelkacem A., et al. Plant Breeding and Climate Changes. J. Agric. Sci. 2010;148:627–637. doi: 10.1017/S0021859610000651. DOI
Brummer E.C., Barber W.T., Collier S.M., Cox T.S., Johnson R., Murray S.C., Olsen R.T., Pratt R.C., Thro A.M. Plant Breeding for Harmony between Agriculture and the Environment. Front. Ecol. Environ. 2011;9:561–568.
Schaart J.G., van de Wiel C.C.M., Lotz L.A.P., Smulders M.J.M. Opportunities for Products of New Plant Breeding Techniques. Trends Plant Sci. 2016;21:438–449. doi: 10.1016/j.tplants.2015.11.006. PubMed DOI
Du Jardin P. Plant Biostimulants: Definition, Concept, Main Categories and Regulation. Sci. Hortic. 2015;196:3–14. doi: 10.1016/j.scienta.2015.09.021. DOI
Xu L., Geelen D. Developing Biostimulants from Agro-Food and Industrial by-Products. Front. Plant Sci. 2018;871:1567. PubMed PMC
Lee J.K., Patel S.K.S., Sung B.H., Kalia V.C. Biomolecules from Municipal and Food Industry Wastes: An Overview. Bioresour. Technol. 2020;298:122346. PubMed
Yakhin O.I., Lubyanov A.A., Yakhin I.A., Brown P.H. Biostimulants in Plant Science: A Global Perspective. Front. Plant Sci. 2017;7:2049. doi: 10.3389/fpls.2016.02049. PubMed DOI PMC
Diego N., Spíchal L. The Chemical Biology of Plant Biostimulants. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2020. Use of Plant Metabolites to Mitigate Stress Effects in Crops; pp. 261–300.
Patel S.K.S., Kalia V.C. Advancements in the Nanobiotechnological Applications. Indian J. Microbiol. 2021;61:401–403. doi: 10.1007/s12088-021-00979-7. PubMed DOI PMC
Kalia V.C., Gong C., Patel S.K.S., Lee J.K. Regulation of Plant Mineral Nutrition by Signal Molecules. Microorganisms. 2021;9:774. PubMed PMC
Beckers G.J., Conrath U. Priming for Stress Resistance: From the Lab to the Field. Curr. Opin. Plant Biol. 2007;10:425–431. doi: 10.1016/j.pbi.2007.06.002. PubMed DOI
Majumdar R., Minocha R., Minocha S.C. Amino Acids in Higher Plants. Northern Research Station; Osfordshire, UK: 2015. Ornithine: At the Crossroads of Multiple Paths to Amino Acids and Polyamines; pp. 156–176.
Hussein H.A.A., Mekki B.B., El-Sadek M.E.A., El Lateef E.E. Effect of L-Ornithine Application on Improving Drought Tolerance in Sugar Beet Plants. Heliyon. 2019;5:e02631. doi: 10.1016/j.heliyon.2019.e02631. PubMed DOI PMC
Gupta K., Dey A., Gupta B. Plant Polyamines in Abiotic Stress Responses. Acta Physiol. Plant. 2013;35:2015–2036.
Podlešáková K., Ugena L., Spíchal L., Doležal K., De Diego N. Phytohormones and Polyamines Regulate Plant Stress Responses by Altering GABA Pathway. New Biotechnol. 2019;48:53–65. doi: 10.1016/j.nbt.2018.07.003. PubMed DOI
Alcázar R., Bueno M., Tiburcio A.F. Polyamines: Small Amines with Large Effects on Plant Abiotic Stress Tolerance. Cells. 2020;9:2373. doi: 10.3390/cells9112373. PubMed DOI PMC
Smith T.A. The Di- and Poly-Amine Oxidases of Higher Plants. Biochem. Soc. Trans. 1985;13:319–322. doi: 10.1042/bst0130319. PubMed DOI
Jammes F., Leonhardt N., Tran D., Bousserouel H., Véry A.A., Renou J.P., Vavasseur A., Kwak J.M., Sentenac H., Bouteau F., et al. Acetylated 1,3-Diaminopropane Antagonizes Abscisic Acid-Mediated Stomatal Closing in Arabidopsis. Plant J. 2014;79:322–333. doi: 10.1111/tpj.12564. PubMed DOI
De Diego N., Fürst T., Humplík J.F., Ugena L., Podlešáková K., Spíchal L. An Automated Method for High-Throughput Screening of Arabidopsis Rosette Growth in Multi-Well Plates and Its Validation in Stress Conditions. Front. Plant Sci. 2017;8:1702. doi: 10.3389/fpls.2017.01702. PubMed DOI PMC
Sorrentino M., De Diego N., Ugena L., Spíchal L., Lucini L., Miras-Moreno B., Zhang L., Rouphael Y., Colla G., Panzarová K. Seed Priming with Protein Hydrolysates Improves Arabidopsis Growth and Stress Tolerance to Abiotic Stresses. Front. Plant Sci. 2021;12:626301. doi: 10.3389/fpls.2021.626301. PubMed DOI PMC
Nagabhushan Arun M., Shankara Hebbar S., Bhanuprakash, Senthivel T., Kumar Nair A., Padmavathi G., Pandey P., Singh A. Plant Stress Physiology—Perspectives in Agriculture. IntechOpen; London, UK: 2022. Seed Priming: The Way Forward to Mitigate Abiotic Stress in Crops.
Ugena L., Hýlová A., Podlešáková K., Humplík J.F., Doležal K., De Diego N., Spíchal L. Characterization of Biostimulant Mode of Action Using Novel Multi-Trait High-Throughput Screening of Arabidopsis Germination and Rosette Growth. Front. Plant Sci. 2018;9:1327. doi: 10.3389/fpls.2018.01327. PubMed DOI PMC
García-García A.L., García-Machado F.J., Borges A.A., Morales-Sierra S., Boto A., Jiménez-Arias D. Pure Organic Active Compounds Against Abiotic Stress: A Biostimulant Overview. Front. Plant Sci. 2020;11:1839. PubMed PMC
Rhaman M.S., Imran S., Rauf F., Khatun M., Baskin C.C., Murata Y., Hasanuzzaman M. Seed Priming with Phytohormones: An Effective Approach for the Mitigation of Abiotic Stress. Plants. 2021;10:37. doi: 10.3390/plants10010037. PubMed DOI PMC
Westman S.M., Kloth K.J., Hanson J., Ohlsson A.B., Albrectsen B.R. Defence Priming in Arabidopsis—A Meta-Analysis. Sci. Rep. 2019;9:13309. doi: 10.1038/s41598-019-49811-9. PubMed DOI PMC
Bryksová M., Hybenová A., Hernándiz A.E., Novák O., Pěnčík A., Spíchal L., De Diego N., Doležal K. Hormopriming to Mitigate Abiotic Stress Effects: A Case Study of N9-Substituted Cytokinin Derivatives with a Fluorinated Carbohydrate Moiety. Front. Plant Sci. 2020;11:1941. doi: 10.3389/fpls.2020.599228. PubMed DOI PMC
Nisler J., Kopečný D., Pěkná Z., Končitíková R., Koprna R., Murvanidze N., Werbrouck S.P.O., Havlíček L., De Diego N., Kopečná M., et al. Diphenylurea-Derived Cytokinin Oxidase/Dehydrogenase Inhibitors for Biotechnology and Agriculture. J. Exp. Bot. 2021;72:355–370. doi: 10.1093/jxb/eraa437. PubMed DOI
Duarte-Sierra A., Tiznado-Hernández M.E., Jha D.K., Janmeja N., Arul J. Abiotic Stress Hormesis: An Approach to Maintain Quality, Extend Storability, and Enhance Phytochemicals on Fresh Produce during Postharvest. Compr. Rev. Food Sci. Food Saf. 2020;19:3659–3682. doi: 10.1111/1541-4337.12628. PubMed DOI
De Diego N., Sampedro M.C., Barrio R.J., Saiz-Fernández I., Moncaleán P., Lacuesta M. Solute Accumulation and Elastic Modulus Changes in Six Radiata Pine Breeds Exposed to Drought. Tree Physiol. 2013;33:69–80. doi: 10.1093/treephys/tps125. PubMed DOI
Marchetti C.F., Ugena L., Humplík J.F., Polák M., Ćavar Zeljković S., Podlešáková K., Fürst T., De Diego N., Spíchal L. A Novel Image-Based Screening Method to Study Water-Deficit Response and Recovery of Barley Populations Using Canopy Dynamics Phenotyping and Simple Metabolite Profiling. Front. Plant Sci. 2019;10:1252. doi: 10.3389/fpls.2019.01252. PubMed DOI PMC
Adio A.M., Casteel C.L., de Vos M., Kim J.H., Joshi V., Li B., Juéry C., Daron J., Kliebenstein D.J., Jandera G. Biosynthesis and Defensive Function of Nδ-Acetylornithine, a Jasmonate-Induced Arabidopsis Metabolite. Plant Cell. 2011;23:3303–3318. doi: 10.1105/tpc.111.088989. PubMed DOI PMC
Lou Y.R., Ahmed S., Yan J., Adio A.M., Powell H.M., Morris P.F., Jander G. Arabidopsis ADC1 Functions as an Nδ-Acetylornithine Decarboxylase. J. Integr. Plant Biol. 2020;62:601–613. doi: 10.1111/jipb.12821. PubMed DOI
Abdelhakim L.O.A., Mendanha T., Palma C.F.F., Vrobel O., Štefelová N., Ćavar Zeljković S., Tarkowski P., De Diego N., Wollenweber B., Rosenqvist E., et al. Elevated CO2 Improves the Physiology but Not the Final Yield in Spring Wheat Genotypes Subjected to Heat and Drought Stress During Anthesis. Front. Plant Sci. 2022;13:379. doi: 10.3389/fpls.2022.824476. PubMed DOI PMC
Slocum R.D. Genes, Enzymes and Regulation of Arginine Biosynthesis in Plants. Plant Physiol. Biochem. 2005;43:729–745. doi: 10.1016/j.plaphy.2005.06.007. PubMed DOI
Pál M., Szalai G., Gondor O.K., Janda T. Unfinished Story of Polyamines: Role of Conjugation, Transport and Light-Related Regulation in the Polyamine Metabolism in Plants. Plant Sci. 2021;308:110923. doi: 10.1016/j.plantsci.2021.110923. PubMed DOI
Peng H., Meyer R.S., Yang T., Whitaker B.D., Trouth F., Shangguan L., Huang J., Litt A., Little D.P., Ke H., et al. A Novel Hydroxycinnamoyl Transferase for Synthesis of Hydroxycinnamoyl Spermine Conjugates in Plants. BMC Plant Biol. 2019;19:261. doi: 10.1186/s12870-019-1846-3. PubMed DOI PMC
Bassard J.E., Ullmann P., Bernier F., Werck-Reichhart D. Phenolamides: Bridging Polyamines to the Phenolic Metabolism. Phytochemistry. 2010;71:1808–1824. doi: 10.1016/j.phytochem.2010.08.003. PubMed DOI
Dobritzsch M., Lübken T., Eschen-Lippold L., Gorzolka K., Blum E., Matern A., Marillonnet S., Böttcher C., Dräger B., Rosahl S. MATE Transporter-Dependent Export of Hydroxycinnamic Acid Amides. Plant Cell. 2015;28:583–596. doi: 10.1105/tpc.15.00706. PubMed DOI PMC
Muroi A., Ishihara A., Tanaka C., Ishizuka A., Takabayashi J., Miyoshi H., Nishioka T. Accumulation of Hydroxycinnamic Acid Amides Induced by Pathogen Infection and Identification of Agmatine Coumaroyltransferase in Arabidopsis Thaliana. Planta. 2009;230:517–527. doi: 10.1007/s00425-009-0960-0. PubMed DOI
Li J., Zhang K., Meng Y., Hu J., Ding M., Bian J., Yan M., Han J., Zhou M. Jasmonic Acid/Ethylene Signaling Coordinates Hydroxycinnamic Acid Amides Biosynthesis through ORA59 Transcription Factor. Plant J. 2018;95:444–457. doi: 10.1111/tpj.13960. PubMed DOI
Del Duca S., Dondini L., Della Mea M., Munoz De Rueda P., Serafini-Fracassini D. Factors Affecting Transglutaminase Activity Catalysing Polyamine Conjugation to Endogenous Substrates in the Entire Chloroplast. Plant Physiol. Biochem. 2000;38:429–439. doi: 10.1016/S0981-9428(00)00761-0. DOI
Poidevin L., Unal D., Belda-Palazón B., Ferrando A. Polyamines as Quality Control Metabolites Operating at the Post-Transcriptional Level. Plants. 2019;8:109. doi: 10.3390/plants8040109. PubMed DOI PMC
Gitelson A.A., Kaufman Y.J., Stark R., Rundquist D. Novel Algorithms for Remote Estimation of Vegetation Fraction. Remote Sens. Environ. 2002;80:76–87. doi: 10.1016/S0034-4257(01)00289-9. DOI
Perry E.M., Roberts D.A. Sensitivity of Narrow-Band and Broad-Band Indices for Assessing Nitrogen Availability and Water Stress in an Annual Crop. Agron. J. 2008;100:1211–1219. doi: 10.2134/agronj2007.0306. DOI
Hunt E.R., Doraiswamy P.C., McMurtrey J.E., Daughtry C.S.T., Perry E.M., Akhmedov B. A Visible Band Index for Remote Sensing Leaf Chlorophyll Content at the Canopy Scale. Int. J. Appl. Earth Obs. Geoinf. 2012;21:103–112. doi: 10.1016/j.jag.2012.07.020. DOI
Comprehensive LC-MS/MS analysis of nitrogen-related plant metabolites
Evaluation of Halophyte Biopotential as an Unused Natural Resource: The Case of Lobularia maritima
Presence and future of plant phenotyping approaches in biostimulant research and development