Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway

Considerable interest exists in improving the efficiency of photosynthesis and photorespiration to increase crop yields that will address growing world food needs. The current study investigated whether a novel synthetic photorespiratory pathway demonstrated to reduce photorespiratory metabolic ener...

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Main Authors: Laura Dougherty, Bret Cooper, James Bunce, Bryan Vinyard, John Stommel
Format: Article
Language:English
Published: American Society for Horticultural Science (ASHS) 2025-01-01
Series:Journal of the American Society for Horticultural Science
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Online Access:https://journals.ashs.org/jashs/view/journals/jashs/150/1/article-p34.xml
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author Laura Dougherty
Bret Cooper
James Bunce
Bryan Vinyard
John Stommel
author_facet Laura Dougherty
Bret Cooper
James Bunce
Bryan Vinyard
John Stommel
author_sort Laura Dougherty
collection DOAJ
description Considerable interest exists in improving the efficiency of photosynthesis and photorespiration to increase crop yields that will address growing world food needs. The current study investigated whether a novel synthetic photorespiratory pathway demonstrated to reduce photorespiratory metabolic energy demands and increase plant vegetative biomass in model species could boost tomato crop yield, notably yield of marketable fruit. The tomato cultivar Moneymaker was transformed with a synthetic photorespiration pathway construct containing a Cucurbita maxima malate synthase (MS) gene and a Chlamydomonas reinhardtii glycolate dehydrogenase (CrGDH) gene targeted to the chloroplast, with a plastid glycolate-glycerate translocator 1 (PLGG1) hairpin interference construct targeting the native photorespiratory pathway. Plants of seven T2 generation lines from independent transformation events expressed the MS and CrGDH transgenes, while having at least 3-fold reduction of native PLGG1 expression relative to non-transformed Moneymaker. Plants from transformed lines were larger and exhibited up to 63% increased biomass in comparison with the Moneymaker control. The number of fruit was similarly greater (1.4- to 4.2-fold) in modified plants; however, average individual fruit weights were significantly less for all but one line. Among transformed lines, larger fruited lines had the lowest biomass, while the smaller fruited lines had the highest biomass. Values for VCmax and Jmax derived from CO2 assimilation curves were statistically similar or lower in transformants relative to the control. Metabolic profiles obtained from high-performance liquid chromatography mass spectrometry (HPLC-MS) analysis revealed increases in forms of inactivated auxin. Principal component analysis of metabolite profiles separated transformants into two groups distinguished by total biomass and fruit size. Observed increases in plant biomass in transformed lines suggests that energy savings were realized from reduced photorespiration but were directed toward vegetative growth. Further studies to balance vegetative vs. reproductive biomass and exploit higher fruit counts observed in transformants may be beneficial for enhanced fruit yield.
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publisher American Society for Horticultural Science (ASHS)
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spelling doaj-art-41c9c326fb6a486098d99892bbc5f1d72025-01-27T16:25:39ZengAmerican Society for Horticultural Science (ASHS)Journal of the American Society for Horticultural Science2327-97882025-01-011501https://doi.org/10.21273/JASHS05448-24Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration PathwayLaura Dougherty0Bret Cooper1James Bunce2Bryan Vinyard3John Stommel4US Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Genetic Improvement for Fruits & Vegetables LaboratoryUS Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Soybean Genomics and Improvement LaboratoryUS Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Adaptive Cropping Systems LaboratoryUS Department of Agriculture, Agricultural Research Service, Northeast Area Statistics GroupUS Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Genetic Improvement for Fruits & Vegetables LaboratoryConsiderable interest exists in improving the efficiency of photosynthesis and photorespiration to increase crop yields that will address growing world food needs. The current study investigated whether a novel synthetic photorespiratory pathway demonstrated to reduce photorespiratory metabolic energy demands and increase plant vegetative biomass in model species could boost tomato crop yield, notably yield of marketable fruit. The tomato cultivar Moneymaker was transformed with a synthetic photorespiration pathway construct containing a Cucurbita maxima malate synthase (MS) gene and a Chlamydomonas reinhardtii glycolate dehydrogenase (CrGDH) gene targeted to the chloroplast, with a plastid glycolate-glycerate translocator 1 (PLGG1) hairpin interference construct targeting the native photorespiratory pathway. Plants of seven T2 generation lines from independent transformation events expressed the MS and CrGDH transgenes, while having at least 3-fold reduction of native PLGG1 expression relative to non-transformed Moneymaker. Plants from transformed lines were larger and exhibited up to 63% increased biomass in comparison with the Moneymaker control. The number of fruit was similarly greater (1.4- to 4.2-fold) in modified plants; however, average individual fruit weights were significantly less for all but one line. Among transformed lines, larger fruited lines had the lowest biomass, while the smaller fruited lines had the highest biomass. Values for VCmax and Jmax derived from CO2 assimilation curves were statistically similar or lower in transformants relative to the control. Metabolic profiles obtained from high-performance liquid chromatography mass spectrometry (HPLC-MS) analysis revealed increases in forms of inactivated auxin. Principal component analysis of metabolite profiles separated transformants into two groups distinguished by total biomass and fruit size. Observed increases in plant biomass in transformed lines suggests that energy savings were realized from reduced photorespiration but were directed toward vegetative growth. Further studies to balance vegetative vs. reproductive biomass and exploit higher fruit counts observed in transformants may be beneficial for enhanced fruit yield.https://journals.ashs.org/jashs/view/journals/jashs/150/1/article-p34.xmlcrop yieldmetabolic efficiencymetabolite profilephotosynthetic efficiencytomatotransgenes
spellingShingle Laura Dougherty
Bret Cooper
James Bunce
Bryan Vinyard
John Stommel
Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
Journal of the American Society for Horticultural Science
crop yield
metabolic efficiency
metabolite profile
photosynthetic efficiency
tomato
transgenes
title Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
title_full Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
title_fullStr Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
title_full_unstemmed Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
title_short Biomass and Yield in Solanum lycopersicum Expressing a Synthetic Photorespiration Pathway
title_sort biomass and yield in solanum lycopersicum expressing a synthetic photorespiration pathway
topic crop yield
metabolic efficiency
metabolite profile
photosynthetic efficiency
tomato
transgenes
url https://journals.ashs.org/jashs/view/journals/jashs/150/1/article-p34.xml
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AT jamesbunce biomassandyieldinsolanumlycopersicumexpressingasyntheticphotorespirationpathway
AT bryanvinyard biomassandyieldinsolanumlycopersicumexpressingasyntheticphotorespirationpathway
AT johnstommel biomassandyieldinsolanumlycopersicumexpressingasyntheticphotorespirationpathway