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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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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