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Proline Exogenously Supplied or Endogenously Overproduced Induces Different Nutritional, Metabolic, and Antioxidative Responses in Transgenic Tobacco Exposed to Cadmium

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Abstract

Proline plays adaptive roles in plant tolerance to cadmium (Cd)-induced stress, but many gaps remain to be elucidated as the responses triggered by exogenously supplied proline or endogenously overproduction are not well known. Thus, we assayed the nutritional status, metabolite profiling, and antioxidative responses in wild type and transgenic tobacco (Nicotiana tabacum L.) containing the P5CSF129A gene under control of the cauliflower mosaic virus (CaMV35S) or stress inducible rd29A promoters. The plants were exposed or unexposed to Cd (0 and 50 μmol L−1 CdCl2·H2O) for 24 and 72 h. The wild type plants were also treated with or without exogenous proline (1 mmol L−1). Plants supplied with exogenous proline exhibited lower Cd translocation from roots to leaves than plants overproducing proline, avoiding oxidative damages in the leaves of these plants. Meanwhile, tobacco overproducing proline was less susceptible to Cd-induced nutritional changes than wild type plants and presented better metabolic adjustment under Cd exposure compared to plants supplied with exogenous proline. Plants overproducing proline increased the synthesis of sugars and organic acids under Cd exposure, which contributed to absence of oxidative stress, since both superoxide dismutase and catalase were not active against Cd-induced oxidative stress in these genotypes. Plants overproducing proline under the control of rd29A presented higher proline concentration in comparison to the CaMV35S promoter. With exception of rd29A plants that presented high proline and reduced glutathione (GSH) concentrations, the other plants presented an inverse correlation between proline and GSH synthesis after 72 h of Cd exposure.

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All data generated or analyzed during this study are included in this published article (and its supplementary information files).

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Funding

This research was supported by the National Council for Scientific and Technological Development—CNPq, Brazil [Grant Number #150260/2017-2]; and the Research Foundation Flanders—FWO, Belgium [Grant Number #BOF16KV06].

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Authors and Affiliations

  1. College of Agriculture Luiz de Queiroz, University of São Paulo, Piracicaba, 13418-900, Brazil

    Lucélia Borgo, Flávio Henrique Silveira Rabêlo, Thaís Regiani Cataldi, Carlos Alberto Labate & Ricardo Antunes Azevedo

  2. Center for Nuclear Energy in Agriculture, University of São Paulo, Piracicaba, 13416-000, Brazil

    Lucélia Borgo & José Lavres

  3. Centre for Environmental Sciences, Hasselt University, 3590, Diepenbeek, Belgium

    Lucélia Borgo, Flávio Henrique Silveira Rabêlo & Ann Cuypers

  4. Institute of Biosciences, São Paulo State University, Rio Claro, 13506-900, Brazil

    Ilara Gabriela Frasson Budzinski

  5. Department of Mathematics, Federal University of Technology of Paraná, Apucarana, 86812-460, Brazil

    Thiago Gentil Ramires

  6. Federal University of Technology of Paraná, Toledo, 85902-490, Brazil

    Patricia Dayane Carvalho Schaker

  7. Department of Agronomy, University of Oeste Paulista, Presidente Prudente, 19067-175, Brazil

    Alessandra Ferreira Ribas

  8. Laboratório de Genética Bioquímica de Plantas, Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”, Avenida Pádua Dias, 11, Caixa Postal 9, Piracicaba, SP, CEP 13418-900, Brazil

    Lucélia Borgo

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Contributions

LB conducted the research and wrote the manuscript. FHSR helped to write the manuscript. IGFB, TRC, and CAL performed the analyzes concerning metabolite profile. TGR performed the statistical analysis. PDCS, AFR, and JL helped to analyze the results and review the manuscript. AN and RAA concepted the study and reviewed the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lucélia Borgo.

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Borgo, L., Rabêlo, F.H.S., Budzinski, I.G.F. et al. Proline Exogenously Supplied or Endogenously Overproduced Induces Different Nutritional, Metabolic, and Antioxidative Responses in Transgenic Tobacco Exposed to Cadmium. J Plant Growth Regul 41, 2846–2868 (2022). https://doi.org/10.1007/s00344-021-10480-6

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