Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses

Climate-smart and sustainable crops are needed for the future. Engineering crops for tolerance of both abiotic and biotic stress is one approach. The accumulation of trehalose, controlled through <i>trehalose-6-phosphate synthase</i> (<i>TPS</i>) or <i>OtsA</i> an...

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Main Authors: Britany Lauren Morgan, Tayebeh Kakeshpour, Alessandro Occhialini, Gabriella King, Megan Sichterman, Stacee A. Harbison, Stephen B. Rigoulot, Holly Brabazon, Charles Neal Stewart, Scott C. Lenaghan
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/12/19/3394
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author Britany Lauren Morgan
Tayebeh Kakeshpour
Alessandro Occhialini
Gabriella King
Megan Sichterman
Stacee A. Harbison
Stephen B. Rigoulot
Holly Brabazon
Charles Neal Stewart
Scott C. Lenaghan
author_facet Britany Lauren Morgan
Tayebeh Kakeshpour
Alessandro Occhialini
Gabriella King
Megan Sichterman
Stacee A. Harbison
Stephen B. Rigoulot
Holly Brabazon
Charles Neal Stewart
Scott C. Lenaghan
author_sort Britany Lauren Morgan
collection DOAJ
description Climate-smart and sustainable crops are needed for the future. Engineering crops for tolerance of both abiotic and biotic stress is one approach. The accumulation of trehalose, controlled through <i>trehalose-6-phosphate synthase</i> (<i>TPS</i>) or <i>OtsA</i> and <i>trehalose-6-phosphate phosphatase</i> (<i>TPP</i>) or <i>OtsB</i> genes in microbes, is known to provide protection for many microbial and fungal species against abiotic stress. The effect of trehalose accumulation in plant species is less understood. Here, we studied the heterologous expression of <i>Escherichia coli OtsB</i> in potato (<i>Solanum tuberosum</i> var. ‘Desiree’) with regards to stress tolerance. The performance of transgenic lines was assessed in both growth chambers and greenhouse mesocosms. Overexpressing potato <i>OtsB</i> lines significantly increased resilience to heat, photoperiod, herbivory, and competition when compared with wildtype plants. Most strikingly, when subjected to high temperatures, transgenic lines exhibited a significantly lower reduction in tuber yield ranging from 40% to 77%, while wildtype plants experienced a 95% decrease in tuber yield. When exposed to competitors in a selected <i>StSP3D::OtsB</i> line, tuber yield was 1.6 times higher than wildtype. Furthermore, transgenic lines performed significantly better under low-nutrient regimes: under competition, yield increased by 1.5-fold. Together, these results demonstrate that increased trehalose has the potential to create more resistant and stable crop plants.
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spelling doaj.art-9f0fb37d51634dd4a199b95bcdc865422023-11-19T14:53:47ZengMDPI AGPlants2223-77472023-09-011219339410.3390/plants12193394Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic StressesBritany Lauren Morgan0Tayebeh Kakeshpour1Alessandro Occhialini2Gabriella King3Megan Sichterman4Stacee A. Harbison5Stephen B. Rigoulot6Holly Brabazon7Charles Neal Stewart8Scott C. Lenaghan9Center for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USADepartment of Plant Sciences, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USADepartment of Plant Sciences, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USACenter for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USAClimate-smart and sustainable crops are needed for the future. Engineering crops for tolerance of both abiotic and biotic stress is one approach. The accumulation of trehalose, controlled through <i>trehalose-6-phosphate synthase</i> (<i>TPS</i>) or <i>OtsA</i> and <i>trehalose-6-phosphate phosphatase</i> (<i>TPP</i>) or <i>OtsB</i> genes in microbes, is known to provide protection for many microbial and fungal species against abiotic stress. The effect of trehalose accumulation in plant species is less understood. Here, we studied the heterologous expression of <i>Escherichia coli OtsB</i> in potato (<i>Solanum tuberosum</i> var. ‘Desiree’) with regards to stress tolerance. The performance of transgenic lines was assessed in both growth chambers and greenhouse mesocosms. Overexpressing potato <i>OtsB</i> lines significantly increased resilience to heat, photoperiod, herbivory, and competition when compared with wildtype plants. Most strikingly, when subjected to high temperatures, transgenic lines exhibited a significantly lower reduction in tuber yield ranging from 40% to 77%, while wildtype plants experienced a 95% decrease in tuber yield. When exposed to competitors in a selected <i>StSP3D::OtsB</i> line, tuber yield was 1.6 times higher than wildtype. Furthermore, transgenic lines performed significantly better under low-nutrient regimes: under competition, yield increased by 1.5-fold. Together, these results demonstrate that increased trehalose has the potential to create more resistant and stable crop plants.https://www.mdpi.com/2223-7747/12/19/3394sustainable agriculture<i>Solanum tuberosum</i> var. ‘Desiree’ (potato)<i>trehalose-6-phosphate phosphatase</i> (<i>OtsB</i>)biotic stressabiotic stresscompetition
spellingShingle Britany Lauren Morgan
Tayebeh Kakeshpour
Alessandro Occhialini
Gabriella King
Megan Sichterman
Stacee A. Harbison
Stephen B. Rigoulot
Holly Brabazon
Charles Neal Stewart
Scott C. Lenaghan
Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
Plants
sustainable agriculture
<i>Solanum tuberosum</i> var. ‘Desiree’ (potato)
<i>trehalose-6-phosphate phosphatase</i> (<i>OtsB</i>)
biotic stress
abiotic stress
competition
title Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
title_full Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
title_fullStr Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
title_full_unstemmed Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
title_short Heterologous Expression of <i>OtsB</i> Increases Tuber Yield and Phenotypic Stability in Potato under Both Abiotic and Biotic Stresses
title_sort heterologous expression of i otsb i increases tuber yield and phenotypic stability in potato under both abiotic and biotic stresses
topic sustainable agriculture
<i>Solanum tuberosum</i> var. ‘Desiree’ (potato)
<i>trehalose-6-phosphate phosphatase</i> (<i>OtsB</i>)
biotic stress
abiotic stress
competition
url https://www.mdpi.com/2223-7747/12/19/3394
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