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

Karlusich, Juan J. Pierella; Arce, Rocío C.; Shahinnia, Fahimeh; Sonnewald, Sophia; Sonnewald, Uwe; Zurbriggen, Matias D.; Hajirezaei, Mohammad-Reza; Carrillo, Néstor

doi:10.3390/ijms21197199

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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

Juan J. Pierella Karlusich

^1,†,‡

^1,†

³,

^4,*,

Mohammad-Reza Hajirezaei

^2,* and

Néstor Carrillo

^1,*

Instituto de Biología Molecular y Celular de Rosario (IBR-UNR/CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Rosario 2000, Argentina

Leibniz Institute of Plant Genetics and Crop Plant Research, OT Gatersleben, Corrensstrasse, D-06466 Stadt Seeland, Germany

Division of Biochemistry, Department of Biology, Friedrich-Alexander-University Erlangen-Nurenberg, 91058 Erlangen, Germany

⁴

Institute of Synthetic Biology and CEPLAS, University of Düsseldorf, Universitätsstr, 1 40225 Düsseldorf, Germany

Authors to whom correspondence should be addressed.

^†

These authors have contributed equally to this work.

^‡

Present address: Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l’Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France.

Int. J. Mol. Sci. 2020, 21(19), 7199; https://doi.org/10.3390/ijms21197199

Received: 25 August 2020 / Revised: 25 September 2020 / Accepted: 28 September 2020 / Published: 29 September 2020

(This article belongs to the Special Issue Drought Stress Tolerance in Plants)

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Abstract

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. View Full-Text

Keywords: drought; stress responses; photosynthesis; chloroplast redox status; flavodoxin; transcriptomics; metabolomics; potato; tuber yield

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MDPI and ACS Style

Karlusich, J.J.P.; Arce, R.C.; Shahinnia, F.; Sonnewald, S.; Sonnewald, U.; Zurbriggen, M.D.; Hajirezaei, M.-R.; Carrillo, N. 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. Int. J. Mol. Sci. 2020, 21, 7199. https://doi.org/10.3390/ijms21197199

AMA Style

Karlusich JJP, Arce RC, Shahinnia F, Sonnewald S, Sonnewald U, Zurbriggen MD, Hajirezaei M-R, Carrillo N. 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. 2020; 21(19):7199. https://doi.org/10.3390/ijms21197199

Chicago/Turabian Style

Karlusich, Juan J.P., Rocío C. Arce, Fahimeh Shahinnia, Sophia Sonnewald, Uwe Sonnewald, Matias D. Zurbriggen, Mohammad-Reza Hajirezaei, and Néstor Carrillo. 2020. "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 21, no. 19: 7199. https://doi.org/10.3390/ijms21197199

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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

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