Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights

In addition to be used as a plant protection agent, copper (Cu) is also an essential micronutrient for plant growth and development. The bioavailability of Cu in agricultural systems can be limited due to its specific physical–chemical characteristics, leading to imbalances in plant production. To a...

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Main Authors: Youssef Rouphael, Petronia Carillo, Michele Ciriello, Luigi Formisano, Christophe El-Nakhel, Paola Ganugi, Andrea Fiorini, Begoña Miras Moreno, Leilei Zhang, Mariateresa Cardarelli, Luigi Lucini, Giuseppe Colla
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1235686/full
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author Youssef Rouphael
Petronia Carillo
Michele Ciriello
Luigi Formisano
Christophe El-Nakhel
Paola Ganugi
Paola Ganugi
Andrea Fiorini
Begoña Miras Moreno
Leilei Zhang
Mariateresa Cardarelli
Luigi Lucini
Luigi Lucini
Giuseppe Colla
author_facet Youssef Rouphael
Petronia Carillo
Michele Ciriello
Luigi Formisano
Christophe El-Nakhel
Paola Ganugi
Paola Ganugi
Andrea Fiorini
Begoña Miras Moreno
Leilei Zhang
Mariateresa Cardarelli
Luigi Lucini
Luigi Lucini
Giuseppe Colla
author_sort Youssef Rouphael
collection DOAJ
description In addition to be used as a plant protection agent, copper (Cu) is also an essential micronutrient for plant growth and development. The bioavailability of Cu in agricultural systems can be limited due to its specific physical–chemical characteristics, leading to imbalances in plant production. To address this issue, an experimental trial was conducted on Genovese basil (Ocimum basilicum L.) in protected conditions to comparatively evaluate the effects of a vegetable protein hydrolysate (VPH), free Cu and Cu complexed with peptides and amino acids of vegetal origin (Cu and Cu-VPH, respectively), and a combination of VPH and Cu-VPH (VPH+Cu-VPH). The study showed that the combined application of VPH+Cu-VPH led to a significant average increase of 16.3% in fresh yield compared to the untreated Control and Cu treatment. This finding was supported by an improved photosynthetic performance in ACO2 (+29%) and Fv/Fm (+7%). Furthermore, mineral analysis using ICP OES demonstrated that Cu and Cu-VPH treatments determined, on average, a 15.1-, 16.9-, and 1.9-fold increase in Cu in plant tissues compared to control, VPH, and VPH+Cu-VPH treatments, respectively. However, the VPH+Cu-VPH treatment induced the highest contents of the other analyzed ions, except for P. In particular, Mg, Mn, Ca, and Fe, which take part in the constitution of chlorophylls, water splitting system, and photosynthetic electron transport chain, increased by 23%, 21%, 25%, and 32% compared to respective controls. Indeed, this improved the photosynthetic efficiency and the carboxylation capacity of the plants, and consequently, the physiological and productive performance of Genovese basil, compared to all other treatments and control. Consistently, the untargeted metabolomics also pointed out a distinctive modulation of phytochemical signatures as a function of the treatment. An accumulation of alkaloids, terpenoids, and phenylpropanoids was observed following Cu treatment, suggesting an oxidative imbalance upon metal exposure. In contrast, a mitigation of oxidative stress was highlighted in Cu-VPH and VPH+Cu-VPH, where the treatments reduced stress-related metabolites. Overall, these results highlight an interaction between Cu and VPH, hence paving the way towards the combined use of Cu and biostimulants to optimize agronomic interventions.
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spelling doaj.art-1fbf90590a0445c0a467104707778c262023-08-24T21:39:11ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.12356861235686Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insightsYoussef Rouphael0Petronia Carillo1Michele Ciriello2Luigi Formisano3Christophe El-Nakhel4Paola Ganugi5Paola Ganugi6Andrea Fiorini7Begoña Miras Moreno8Leilei Zhang9Mariateresa Cardarelli10Luigi Lucini11Luigi Lucini12Giuseppe Colla13Department of Agricultural Sciences, University of Naples Federico II, Portici, ItalyDepartment of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania “Luigi Vanvitelli”, Caserta, ItalyDepartment of Agricultural Sciences, University of Naples Federico II, Portici, ItalyDepartment of Agricultural Sciences, University of Naples Federico II, Portici, ItalyDepartment of Agricultural Sciences, University of Naples Federico II, Portici, ItalyDepartment for Sustainable Food Process, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment of Sustainable Crop Production, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment of Sustainable Crop Production, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment for Sustainable Food Process, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment for Sustainable Food Process, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment of Agriculture and Forest Sciences, University of Tuscia, Viterbo, ItalyDepartment of Sustainable Crop Production, Università Cattolica del Sacro Cuore, Piacenza, ItalyCRAST Research Centre, Università Cattolica del Sacro Cuore, Piacenza, ItalyDepartment of Agriculture and Forest Sciences, University of Tuscia, Viterbo, ItalyIn addition to be used as a plant protection agent, copper (Cu) is also an essential micronutrient for plant growth and development. The bioavailability of Cu in agricultural systems can be limited due to its specific physical–chemical characteristics, leading to imbalances in plant production. To address this issue, an experimental trial was conducted on Genovese basil (Ocimum basilicum L.) in protected conditions to comparatively evaluate the effects of a vegetable protein hydrolysate (VPH), free Cu and Cu complexed with peptides and amino acids of vegetal origin (Cu and Cu-VPH, respectively), and a combination of VPH and Cu-VPH (VPH+Cu-VPH). The study showed that the combined application of VPH+Cu-VPH led to a significant average increase of 16.3% in fresh yield compared to the untreated Control and Cu treatment. This finding was supported by an improved photosynthetic performance in ACO2 (+29%) and Fv/Fm (+7%). Furthermore, mineral analysis using ICP OES demonstrated that Cu and Cu-VPH treatments determined, on average, a 15.1-, 16.9-, and 1.9-fold increase in Cu in plant tissues compared to control, VPH, and VPH+Cu-VPH treatments, respectively. However, the VPH+Cu-VPH treatment induced the highest contents of the other analyzed ions, except for P. In particular, Mg, Mn, Ca, and Fe, which take part in the constitution of chlorophylls, water splitting system, and photosynthetic electron transport chain, increased by 23%, 21%, 25%, and 32% compared to respective controls. Indeed, this improved the photosynthetic efficiency and the carboxylation capacity of the plants, and consequently, the physiological and productive performance of Genovese basil, compared to all other treatments and control. Consistently, the untargeted metabolomics also pointed out a distinctive modulation of phytochemical signatures as a function of the treatment. An accumulation of alkaloids, terpenoids, and phenylpropanoids was observed following Cu treatment, suggesting an oxidative imbalance upon metal exposure. In contrast, a mitigation of oxidative stress was highlighted in Cu-VPH and VPH+Cu-VPH, where the treatments reduced stress-related metabolites. Overall, these results highlight an interaction between Cu and VPH, hence paving the way towards the combined use of Cu and biostimulants to optimize agronomic interventions.https://www.frontiersin.org/articles/10.3389/fpls.2023.1235686/fullvegetal protein hydrolysatessustainable agricultureprimary metabolismoxidative stressmetabolomicsphotosynthetic performance
spellingShingle Youssef Rouphael
Petronia Carillo
Michele Ciriello
Luigi Formisano
Christophe El-Nakhel
Paola Ganugi
Paola Ganugi
Andrea Fiorini
Begoña Miras Moreno
Leilei Zhang
Mariateresa Cardarelli
Luigi Lucini
Luigi Lucini
Giuseppe Colla
Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
Frontiers in Plant Science
vegetal protein hydrolysates
sustainable agriculture
primary metabolism
oxidative stress
metabolomics
photosynthetic performance
title Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
title_full Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
title_fullStr Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
title_full_unstemmed Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
title_short Copper boosts the biostimulant activity of a vegetal-derived protein hydrolysate in basil: morpho-physiological and metabolomics insights
title_sort copper boosts the biostimulant activity of a vegetal derived protein hydrolysate in basil morpho physiological and metabolomics insights
topic vegetal protein hydrolysates
sustainable agriculture
primary metabolism
oxidative stress
metabolomics
photosynthetic performance
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1235686/full
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