Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance

It has been challenging to simultaneously improve photosynthesis and stress tolerance in plants. Crassulacean acid metabolism (CAM) is a CO<sub>2</sub>-concentrating mechanism that facilitates plant adaptation to water-limited environments. We hypothesized that the ectopic expression of...

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Main Authors: Degao Liu, Rongbin Hu, Jin Zhang, Hao-Bo Guo, Hua Cheng, Linling Li, Anne M. Borland, Hong Qin, Jin-Gui Chen, Wellington Muchero, Gerald A. Tuskan, Xiaohan Yang
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/10/3/582
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spelling doaj-f27c6b2118744bf69c2cae7672a3739e2021-03-07T00:02:34ZengMDPI AGCells2073-44092021-03-011058258210.3390/cells10030582Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress ToleranceDegao Liu0Rongbin Hu1Jin Zhang2Hao-Bo Guo3Hua Cheng4Linling Li5Anne M. Borland6Hong Qin7Jin-Gui Chen8Wellington Muchero9Gerald A. Tuskan10Xiaohan Yang11Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USADepartment of Computer Science and Engineering, SimCenter, University of Tennessee Chattanooga, Chattanooga, TN 37403, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USADepartment of Computer Science and Engineering, SimCenter, University of Tennessee Chattanooga, Chattanooga, TN 37403, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USAIt has been challenging to simultaneously improve photosynthesis and stress tolerance in plants. Crassulacean acid metabolism (CAM) is a CO<sub>2</sub>-concentrating mechanism that facilitates plant adaptation to water-limited environments. We hypothesized that the ectopic expression of a CAM-specific phospho<i>enol</i>pyruvate carboxylase (PEPC), an enzyme that catalyzes primary CO<sub>2</sub> fixation in CAM plants, would enhance both photosynthesis and abiotic stress tolerance. To test this hypothesis, we engineered a CAM-specific <i>PEPC</i> gene (named <i>AaPEPC1</i>) from <i>Agave americana</i> into tobacco. In comparison with wild-type and empty vector controls, transgenic tobacco plants constitutively expressing <i>AaPEPC1</i> showed a higher photosynthetic rate and biomass production under normal conditions, along with significant carbon metabolism changes in malate accumulation, the carbon isotope ratio δ<sup>13</sup>C, and the expression of multiple orthologs of CAM-related genes. Furthermore, <i>AaPEPC1</i> overexpression enhanced proline biosynthesis, and improved salt and drought tolerance in the transgenic plants. Under salt and drought stress conditions, the dry weight of transgenic tobacco plants overexpressing <i>AaPEPC1</i> was increased by up to 81.8% and 37.2%, respectively, in comparison with wild-type plants. Our findings open a new door to the simultaneous improvement of photosynthesis and stress tolerance in plants.https://www.mdpi.com/2073-4409/10/3/582<i>Agave americana</i>crassulacean acid metabolismgenetic engineering<i>Nicotiana sylvestris</i>phospho<i>enol</i>pyruvate carboxylasephotosynthesis
collection DOAJ
language English
format Article
sources DOAJ
author Degao Liu
Rongbin Hu
Jin Zhang
Hao-Bo Guo
Hua Cheng
Linling Li
Anne M. Borland
Hong Qin
Jin-Gui Chen
Wellington Muchero
Gerald A. Tuskan
Xiaohan Yang
spellingShingle Degao Liu
Rongbin Hu
Jin Zhang
Hao-Bo Guo
Hua Cheng
Linling Li
Anne M. Borland
Hong Qin
Jin-Gui Chen
Wellington Muchero
Gerald A. Tuskan
Xiaohan Yang
Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
Cells
<i>Agave americana</i>
crassulacean acid metabolism
genetic engineering
<i>Nicotiana sylvestris</i>
phospho<i>enol</i>pyruvate carboxylase
photosynthesis
author_facet Degao Liu
Rongbin Hu
Jin Zhang
Hao-Bo Guo
Hua Cheng
Linling Li
Anne M. Borland
Hong Qin
Jin-Gui Chen
Wellington Muchero
Gerald A. Tuskan
Xiaohan Yang
author_sort Degao Liu
title Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
title_short Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
title_full Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
title_fullStr Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
title_full_unstemmed Overexpression of an <i>Agave</i> Phospho<i>enol</i>pyruvate Carboxylase Improves Plant Growth and Stress Tolerance
title_sort overexpression of an <i>agave</i> phospho<i>enol</i>pyruvate carboxylase improves plant growth and stress tolerance
publisher MDPI AG
series Cells
issn 2073-4409
publishDate 2021-03-01
description It has been challenging to simultaneously improve photosynthesis and stress tolerance in plants. Crassulacean acid metabolism (CAM) is a CO<sub>2</sub>-concentrating mechanism that facilitates plant adaptation to water-limited environments. We hypothesized that the ectopic expression of a CAM-specific phospho<i>enol</i>pyruvate carboxylase (PEPC), an enzyme that catalyzes primary CO<sub>2</sub> fixation in CAM plants, would enhance both photosynthesis and abiotic stress tolerance. To test this hypothesis, we engineered a CAM-specific <i>PEPC</i> gene (named <i>AaPEPC1</i>) from <i>Agave americana</i> into tobacco. In comparison with wild-type and empty vector controls, transgenic tobacco plants constitutively expressing <i>AaPEPC1</i> showed a higher photosynthetic rate and biomass production under normal conditions, along with significant carbon metabolism changes in malate accumulation, the carbon isotope ratio δ<sup>13</sup>C, and the expression of multiple orthologs of CAM-related genes. Furthermore, <i>AaPEPC1</i> overexpression enhanced proline biosynthesis, and improved salt and drought tolerance in the transgenic plants. Under salt and drought stress conditions, the dry weight of transgenic tobacco plants overexpressing <i>AaPEPC1</i> was increased by up to 81.8% and 37.2%, respectively, in comparison with wild-type plants. Our findings open a new door to the simultaneous improvement of photosynthesis and stress tolerance in plants.
topic <i>Agave americana</i>
crassulacean acid metabolism
genetic engineering
<i>Nicotiana sylvestris</i>
phospho<i>enol</i>pyruvate carboxylase
photosynthesis
url https://www.mdpi.com/2073-4409/10/3/582
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