Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise

Water limitation represents the main environmental constraint affecting crop yield worldwide. Photosynthesis is a primary drought target, resulting in over-reduction of the photosynthetic electron transport chain and increased production of reactive oxygen species in plastids. Manipulation of chloro...

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Main Authors: Juan J. Pierella Karlusich, Rocío C. Arce, Fahimeh Shahinnia, Sophia Sonnewald, Uwe Sonnewald, Matias D. Zurbriggen, Mohammad-Reza Hajirezaei, Néstor Carrillo
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/21/19/7199
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spelling doaj-169b56b28f0d4e97b531b84e3ff920f22020-11-25T03:28:26ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-09-01217199719910.3390/ijms21197199Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox PoiseJuan J. Pierella Karlusich0Rocío C. Arce1Fahimeh Shahinnia2Sophia Sonnewald3Uwe Sonnewald4Matias D. Zurbriggen5Mohammad-Reza Hajirezaei6Néstor Carrillo7Instituto de Biología Molecular y Celular de Rosario (IBR-UNR/CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Rosario 2000, ArgentinaInstituto de Biología Molecular y Celular de Rosario (IBR-UNR/CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Rosario 2000, ArgentinaLeibniz Institute of Plant Genetics and Crop Plant Research, OT Gatersleben, Corrensstrasse, D-06466 Stadt Seeland, GermanyDivision of Biochemistry, Department of Biology, Friedrich-Alexander-University Erlangen-Nurenberg, 91058 Erlangen, GermanyDivision of Biochemistry, Department of Biology, Friedrich-Alexander-University Erlangen-Nurenberg, 91058 Erlangen, GermanyInstitute of Synthetic Biology and CEPLAS, University of Düsseldorf, Universitätsstr, 1 40225 Düsseldorf, GermanyLeibniz Institute of Plant Genetics and Crop Plant Research, OT Gatersleben, Corrensstrasse, D-06466 Stadt Seeland, GermanyInstituto de Biología Molecular y Celular de Rosario (IBR-UNR/CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Rosario 2000, ArgentinaWater limitation represents the main environmental constraint affecting crop yield worldwide. Photosynthesis is a primary drought target, resulting in over-reduction of the photosynthetic electron transport chain and increased production of reactive oxygen species in plastids. Manipulation of chloroplast electron distribution by introducing alternative electron transport sinks has been shown to increase plant tolerance to multiple environmental challenges including hydric stress, suggesting that a similar strategy could be used to improve drought tolerance in crops. We show herein that the expression of the cyanobacterial electron shuttle flavodoxin in potato chloroplasts protected photosynthetic activities even at a pre-symptomatic stage of drought. Transcriptional and metabolic profiling revealed an attenuated response to the adverse condition in flavodoxin-expressing plants, correlating with their increased stress tolerance. Interestingly, 5–6% of leaf-expressed genes were affected by flavodoxin in the absence of drought, representing pathways modulated by chloroplast redox status during normal growth. About 300 of these genes potentially contribute to stress acclimation as their modulation by flavodoxin proceeds in the same direction as their drought response in wild-type plants. Tuber yield losses under chronic water limitation were mitigated in flavodoxin-expressing plants, indicating that the flavoprotein has the potential to improve major agronomic traits in potato.https://www.mdpi.com/1422-0067/21/19/7199droughtstress responsesphotosynthesischloroplast redox statusflavodoxintranscriptomics
collection DOAJ
language English
format Article
sources DOAJ
author Juan J. Pierella Karlusich
Rocío C. Arce
Fahimeh Shahinnia
Sophia Sonnewald
Uwe Sonnewald
Matias D. Zurbriggen
Mohammad-Reza Hajirezaei
Néstor Carrillo
spellingShingle Juan J. Pierella Karlusich
Rocío C. Arce
Fahimeh Shahinnia
Sophia Sonnewald
Uwe Sonnewald
Matias D. Zurbriggen
Mohammad-Reza Hajirezaei
Néstor Carrillo
Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
International Journal of Molecular Sciences
drought
stress responses
photosynthesis
chloroplast redox status
flavodoxin
transcriptomics
author_facet Juan J. Pierella Karlusich
Rocío C. Arce
Fahimeh Shahinnia
Sophia Sonnewald
Uwe Sonnewald
Matias D. Zurbriggen
Mohammad-Reza Hajirezaei
Néstor Carrillo
author_sort Juan J. Pierella Karlusich
title Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
title_short Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
title_full Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
title_fullStr Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
title_full_unstemmed Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise
title_sort transcriptional and metabolic profiling of potato plants expressing a plastid-targeted electron shuttle reveal modulation of genes associated to drought tolerance by chloroplast redox poise
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-09-01
description Water limitation represents the main environmental constraint affecting crop yield worldwide. Photosynthesis is a primary drought target, resulting in over-reduction of the photosynthetic electron transport chain and increased production of reactive oxygen species in plastids. Manipulation of chloroplast electron distribution by introducing alternative electron transport sinks has been shown to increase plant tolerance to multiple environmental challenges including hydric stress, suggesting that a similar strategy could be used to improve drought tolerance in crops. We show herein that the expression of the cyanobacterial electron shuttle flavodoxin in potato chloroplasts protected photosynthetic activities even at a pre-symptomatic stage of drought. Transcriptional and metabolic profiling revealed an attenuated response to the adverse condition in flavodoxin-expressing plants, correlating with their increased stress tolerance. Interestingly, 5–6% of leaf-expressed genes were affected by flavodoxin in the absence of drought, representing pathways modulated by chloroplast redox status during normal growth. About 300 of these genes potentially contribute to stress acclimation as their modulation by flavodoxin proceeds in the same direction as their drought response in wild-type plants. Tuber yield losses under chronic water limitation were mitigated in flavodoxin-expressing plants, indicating that the flavoprotein has the potential to improve major agronomic traits in potato.
topic drought
stress responses
photosynthesis
chloroplast redox status
flavodoxin
transcriptomics
url https://www.mdpi.com/1422-0067/21/19/7199
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