Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)

Abstract Background Raising global temperatures limit crop productivity and new strategies are needed to improve the resilience of thermosensitive crops such as potato (Solanum tuberosum L.). Biostimulants are emerging as potential crop protection products against environmental stress, however their...

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Main Authors: Dasuni P. Jayaweera, Charlene Dambire, Dimitra Angelopoulou, Sergi Munné-Bosch, Ranjan Swarup, Rumiana V. Ray
Format: Article
Language:English
Published: SpringerOpen 2024-01-01
Series:Chemical and Biological Technologies in Agriculture
Subjects:
Online Access:https://doi.org/10.1186/s40538-023-00531-3
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author Dasuni P. Jayaweera
Charlene Dambire
Dimitra Angelopoulou
Sergi Munné-Bosch
Ranjan Swarup
Rumiana V. Ray
author_facet Dasuni P. Jayaweera
Charlene Dambire
Dimitra Angelopoulou
Sergi Munné-Bosch
Ranjan Swarup
Rumiana V. Ray
author_sort Dasuni P. Jayaweera
collection DOAJ
description Abstract Background Raising global temperatures limit crop productivity and new strategies are needed to improve the resilience of thermosensitive crops such as potato (Solanum tuberosum L.). Biostimulants are emerging as potential crop protection products against environmental stress, however their mechanism of action remains largely unknown, hindering their wider adoption. We used comprehensive physiological, molecular, and mass spectrometry approaches to develop understanding of the mechanism of plant thermotolerance exerted by the biostimulant, Quantis™, under heat stress. Using orthologues gene mutations in Arabidopsis thaliana we report heat-defence genes, modified by Quantis™, which were also investigated for potential overlapping functions in biotic stress defence to Sclerotinia sclerotiorum and Rhizoctonia solani. Results Quantis™ enhanced PSII photochemical efficiency and decreased thermal dissipation of potato grown under heat stress. These effects were associated with upregulation of genes with antioxidant function, including PR10, flavonoid 3′‐hydroxylase and β-glucosidases, and modulation of abscisic acid (ABA) and cytokinin (CK) activity in leaves by Quantis™. The biostimulant modulated the expression of the heat-defence genes, PEN1, PR4 or MEE59, with functions in leaf photoprotection and root thermal protection, but with no overlapping function in biotic stress defence. Protective root growth under heat stress, following the biostimulant application, was correlated with enhanced CK signalling in roots. Increased endogenous concentrations of ABA and CK in potato leaves and significant upregulation of StFKF1 were consistent with tuberisation promoting effects. Quantis™ application resulted in 4% tuber weight increase and 40% larger tuber size thus mitigating negative effects of heat stress on tuber growth. Conclusions Quantis™ application prior to heat stress effectively primed heat tolerance responses and alleviated temperature stress of S. tuberosum L. and A. thaliana by modulating the expression and function of PR4 and MEE59 and by regulating CK activity above and below ground, indicating that the mechanism of action of the biostimulant is conserved, and will be effective in many plant species. Thus, a biostimulant application targeting the most susceptible crop developmental stages to heat disorders can be effectively integrated within future agronomy practices to mitigate losses in other thermosensitive crops. Graphical Abstract
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spelling doaj.art-4a836fc4c1264bd291940a968f888dc92024-01-14T12:14:50ZengSpringerOpenChemical and Biological Technologies in Agriculture2196-56412024-01-0111111910.1186/s40538-023-00531-3Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)Dasuni P. Jayaweera0Charlene Dambire1Dimitra Angelopoulou2Sergi Munné-Bosch3Ranjan Swarup4Rumiana V. Ray5Division of Plant and Crop Sciences, School of Biosciences, University of NottinghamDivision of Plant and Crop Sciences, School of Biosciences, University of NottinghamDepartment of Biochemistry and Biotechnology, School of Life Sciences, University of ThessalyDepartament de Biologia Evolutiva, University of Barcelona, Ecologia i Ciències AmbientalsDivision of Plant and Crop Sciences, School of Biosciences, University of NottinghamDivision of Plant and Crop Sciences, School of Biosciences, University of NottinghamAbstract Background Raising global temperatures limit crop productivity and new strategies are needed to improve the resilience of thermosensitive crops such as potato (Solanum tuberosum L.). Biostimulants are emerging as potential crop protection products against environmental stress, however their mechanism of action remains largely unknown, hindering their wider adoption. We used comprehensive physiological, molecular, and mass spectrometry approaches to develop understanding of the mechanism of plant thermotolerance exerted by the biostimulant, Quantis™, under heat stress. Using orthologues gene mutations in Arabidopsis thaliana we report heat-defence genes, modified by Quantis™, which were also investigated for potential overlapping functions in biotic stress defence to Sclerotinia sclerotiorum and Rhizoctonia solani. Results Quantis™ enhanced PSII photochemical efficiency and decreased thermal dissipation of potato grown under heat stress. These effects were associated with upregulation of genes with antioxidant function, including PR10, flavonoid 3′‐hydroxylase and β-glucosidases, and modulation of abscisic acid (ABA) and cytokinin (CK) activity in leaves by Quantis™. The biostimulant modulated the expression of the heat-defence genes, PEN1, PR4 or MEE59, with functions in leaf photoprotection and root thermal protection, but with no overlapping function in biotic stress defence. Protective root growth under heat stress, following the biostimulant application, was correlated with enhanced CK signalling in roots. Increased endogenous concentrations of ABA and CK in potato leaves and significant upregulation of StFKF1 were consistent with tuberisation promoting effects. Quantis™ application resulted in 4% tuber weight increase and 40% larger tuber size thus mitigating negative effects of heat stress on tuber growth. Conclusions Quantis™ application prior to heat stress effectively primed heat tolerance responses and alleviated temperature stress of S. tuberosum L. and A. thaliana by modulating the expression and function of PR4 and MEE59 and by regulating CK activity above and below ground, indicating that the mechanism of action of the biostimulant is conserved, and will be effective in many plant species. Thus, a biostimulant application targeting the most susceptible crop developmental stages to heat disorders can be effectively integrated within future agronomy practices to mitigate losses in other thermosensitive crops. Graphical Abstracthttps://doi.org/10.1186/s40538-023-00531-3Solanum tuberosumBiostimulantThermotoleranceAbscisic acidCytokininsGibberellins
spellingShingle Dasuni P. Jayaweera
Charlene Dambire
Dimitra Angelopoulou
Sergi Munné-Bosch
Ranjan Swarup
Rumiana V. Ray
Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
Chemical and Biological Technologies in Agriculture
Solanum tuberosum
Biostimulant
Thermotolerance
Abscisic acid
Cytokinins
Gibberellins
title Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
title_full Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
title_fullStr Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
title_full_unstemmed Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
title_short Physiological, molecular, and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.)
title_sort physiological molecular and genetic mechanism of action of the biostimulant quantis™ for increased thermotolerance of potato solanum tuberosum l
topic Solanum tuberosum
Biostimulant
Thermotolerance
Abscisic acid
Cytokinins
Gibberellins
url https://doi.org/10.1186/s40538-023-00531-3
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