Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress

Cadmium (Cd) accumulation in agricultural soils constitutes a serious problem for crop yields and food safety. It is known that proline (Pro) can rapidly accumulate in plant tissues in response to abiotic stress. To analyze the potential protective effect of Pro accumulation against Cd toxicity, we...

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Main Authors: Vanesa S. García de la Torre, Teodoro Coba de la Peña, M. Mercedes Lucas, José J. Pueyo
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.829069/full
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author Vanesa S. García de la Torre
Teodoro Coba de la Peña
M. Mercedes Lucas
José J. Pueyo
author_facet Vanesa S. García de la Torre
Teodoro Coba de la Peña
M. Mercedes Lucas
José J. Pueyo
author_sort Vanesa S. García de la Torre
collection DOAJ
description Cadmium (Cd) accumulation in agricultural soils constitutes a serious problem for crop yields and food safety. It is known that proline (Pro) can rapidly accumulate in plant tissues in response to abiotic stress. To analyze the potential protective effect of Pro accumulation against Cd toxicity, we compared the response to Cd stress of wild-type (WT) Medicago truncatula and a transgenic line that we had previously obtained and characterized (p18), which expressed the Δ1-pyrroline-5-carboxylate synthetase gene from Vigna aconitifolia (VaP5CS), and accumulated high Pro levels. Cadmium significantly reduced germination of WT seeds compared to p18 seeds, and seedling relative root growth, a valid indicator of metal tolerance, was significantly higher for p18 than WT seedlings. We analyzed the relative expression of genes related to Pro metabolism, phytochelatin biosynthesis. antioxidant machinery, and NADPH recycling, which are relevant mechanisms in the response to Cd stress. They presented differential expression in the seedlings of both genotypes both under control conditions and under Cd stress, suggesting that the Cd response mechanisms might be constitutively activated in the transgenic line. Pro accumulation promoted higher survival, enhanced growth performance, and minor nutrient imbalance in transgenic p18 plants compared to WT plants. These facts, together with the recorded gluthatione levels, lipid peroxidation and antioxidant enzyme activities strongly suggested that VaP5CS expression and Pro accumulation conferred enhanced Cd tolerance to M. truncatula p18 plants, which was likely mediated by changes in Pro metabolism, increased phytochelatin biosynthesis and a more efficient antioxidant response. Moreover, p18 roots accumulated significantly higher Cd amounts than WT roots, while Cd translocation to the aerial part was similar to WT plants, thus suggesting that high Pro levels increased not only Cd tolerance, but also Cd phytostabilization by rhizosequestration.
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spelling doaj.art-8b1b023d4bc444b19e0b43fb811c39632022-12-21T19:43:50ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-01-011310.3389/fpls.2022.829069829069Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium StressVanesa S. García de la Torre0Teodoro Coba de la Peña1M. Mercedes Lucas2José J. Pueyo3Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Cientiíficas (ICA-CSIC), Madrid, SpainCentro de Estudios Avanzados en Zonas Áridas (CEAZA), La Serena, ChileInstituto de Ciencias Agrarias, Consejo Superior de Investigaciones Cientiíficas (ICA-CSIC), Madrid, SpainInstituto de Ciencias Agrarias, Consejo Superior de Investigaciones Cientiíficas (ICA-CSIC), Madrid, SpainCadmium (Cd) accumulation in agricultural soils constitutes a serious problem for crop yields and food safety. It is known that proline (Pro) can rapidly accumulate in plant tissues in response to abiotic stress. To analyze the potential protective effect of Pro accumulation against Cd toxicity, we compared the response to Cd stress of wild-type (WT) Medicago truncatula and a transgenic line that we had previously obtained and characterized (p18), which expressed the Δ1-pyrroline-5-carboxylate synthetase gene from Vigna aconitifolia (VaP5CS), and accumulated high Pro levels. Cadmium significantly reduced germination of WT seeds compared to p18 seeds, and seedling relative root growth, a valid indicator of metal tolerance, was significantly higher for p18 than WT seedlings. We analyzed the relative expression of genes related to Pro metabolism, phytochelatin biosynthesis. antioxidant machinery, and NADPH recycling, which are relevant mechanisms in the response to Cd stress. They presented differential expression in the seedlings of both genotypes both under control conditions and under Cd stress, suggesting that the Cd response mechanisms might be constitutively activated in the transgenic line. Pro accumulation promoted higher survival, enhanced growth performance, and minor nutrient imbalance in transgenic p18 plants compared to WT plants. These facts, together with the recorded gluthatione levels, lipid peroxidation and antioxidant enzyme activities strongly suggested that VaP5CS expression and Pro accumulation conferred enhanced Cd tolerance to M. truncatula p18 plants, which was likely mediated by changes in Pro metabolism, increased phytochelatin biosynthesis and a more efficient antioxidant response. Moreover, p18 roots accumulated significantly higher Cd amounts than WT roots, while Cd translocation to the aerial part was similar to WT plants, thus suggesting that high Pro levels increased not only Cd tolerance, but also Cd phytostabilization by rhizosequestration.https://www.frontiersin.org/articles/10.3389/fpls.2022.829069/fullΔ1-pyrroline-5-carboxylate synthetaseP5CSprolineMedicago truncatulacadmiumphytochelatin biosynthesis
spellingShingle Vanesa S. García de la Torre
Teodoro Coba de la Peña
M. Mercedes Lucas
José J. Pueyo
Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
Frontiers in Plant Science
Δ1-pyrroline-5-carboxylate synthetase
P5CS
proline
Medicago truncatula
cadmium
phytochelatin biosynthesis
title Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
title_full Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
title_fullStr Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
title_full_unstemmed Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
title_short Transgenic Medicago truncatula Plants That Accumulate Proline Display Enhanced Tolerance to Cadmium Stress
title_sort transgenic medicago truncatula plants that accumulate proline display enhanced tolerance to cadmium stress
topic Δ1-pyrroline-5-carboxylate synthetase
P5CS
proline
Medicago truncatula
cadmium
phytochelatin biosynthesis
url https://www.frontiersin.org/articles/10.3389/fpls.2022.829069/full
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