TY - JOUR

T1 - Limiting etioplast gene expression induces apical hook twisting during skotomorphogenesis of Arabidopsis seedlings

AU - Sajib, Salek Ahmed

AU - Grübler, Björn

AU - Oukacine, Cylia

AU - Delannoy, Etienne

AU - Courtois, Florence

AU - Mauve, Caroline

AU - Lurin, Claire

AU - Gakière, Bertrand

AU - Pfannschmidt, Thomas

AU - Merendino, Livia

N1 - Funding Information: This work was supported by the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS) to IPS2; grants from the Deutsche Forschungsgemeinschaft (DFG) [PF323-5-2] and the DFG research group FOR 804; the Centre National de la Recherche Scientifique [Projets Exploratoires Premier Soutien] to TP; and the French Ministry of Education and the Grenoble Alliance for Integrated Structural Cell Biology (LabEx GRAL, ANR-10-LABX-49-01) to LPCV. We thank Michael Hodges and Emmanuelle Issakidis-Bourguet from IPS2 (Orsay, France) for helpful discussions and Géraldine Bonnard (IBMP, Strasburg, France) for sharing NAD9 antisera. We thank Olivier van Aken (Lund University, Sweden) for sharing anac017 seeds, Fredy Barneche (IBENS, France) for gun1-201 and cop1-4 seeds, and Kristina Kühn (Universität Halle, Germany) for aox1a seeds. RNA sample processing and Affymetrix microarray hybridization were carried out at the genomics core facility, Center of Excellence for Fluorescent Bioanalytics (KFB, University of Regensburg, Germany). SAS was supported by a fellowship from the Ministère de l'Enseignement supérieur, de la Recherche et de l'Innovation (MESRI) of the French Government (Doctoral School of Plant Sciences [SEVE], Université Paris-Saclay) for his PhD. Funding Information: This work was supported by the LabEx Saclay Plant Sciences‐SPS (ANR‐10‐LABX‐0040‐SPS) to IPS2; grants from the Deutsche Forschungsgemeinschaft (DFG) [PF323‐5‐2] and the DFG research group FOR 804; the Centre National de la Recherche Scientifique [Projets Exploratoires Premier Soutien] to TP; and the French Ministry of Education and the Grenoble Alliance for Integrated Structural Cell Biology (LabEx GRAL, ANR‐10‐LABX‐49‐01) to LPCV. We thank Michael Hodges and Emmanuelle Issakidis‐Bourguet from IPS2 (Orsay, France) for helpful discussions and Géraldine Bonnard (IBMP, Strasburg, France) for sharing NAD9 antisera. We thank Olivier van Aken (Lund University, Sweden) for sharing seeds, Fredy Barneche (IBENS, France) for and seeds, and Kristina Kühn (Universität Halle, Germany) for seeds. RNA sample processing and Affymetrix microarray hybridization were carried out at the genomics core facility, Center of Excellence for Fluorescent Bioanalytics (KFB, University of Regensburg, Germany). SAS was supported by a fellowship from the Ministère de l'Enseignement supérieur, de la Recherche et de l'Innovation (MESRI) of the French Government (Doctoral School of Plant Sciences [SEVE], Université Paris‐Saclay) for his PhD. anac017 gun1‐201 cop1‐4 aox1a

PY - 2023/4/8

Y1 - 2023/4/8

N2 - When covered by a layer of soil, seedling development follows a dark-specific program (skotomorphogenesis). In the dark, seedlings consist of small, non-green cotyledons, a long hypocotyl, and an apical hook to protect meristematic cells. We recently highlighted the role played by mitochondria in the high energy-consuming reprogramming of Arabidopsis skotomorphogenesis. Here, the role played by plastids, another energy-supplying organelle, in skotomorphogenesis is investigated. This study was conducted in dark conditions to exclude light signals so as to better focus on those produced by plastids. It was found that limitation of plastid gene expression (PGE) induced an exaggerated apical hook bending. Inhibition of PGE was obtained at the levels of transcription and translation using the antibiotics rifampicin (RIF) and spectinomycin, respectively, as well as plastid RPOTp RNA polymerase mutants. RIF-treated seedlings also showed expression induction of marker nuclear genes for mitochondrial stress, perturbation of mitochondrial metabolism, increased ROS levels, and an augmented capacity of oxygen consumption by mitochondrial alternative oxidases (AOXs). AOXs act to prevent overreduction of the mitochondrial electron transport chain. Previously, we reported that AOX1A, the main AOX isoform, is a key component in the developmental response to mitochondrial respiration deficiency. In this work, we suggest the involvement of AOX1A in the response to PGE dysfunction and propose the importance of signaling between plastids and mitochondria. Finally, it was found that seedling architecture reprogramming in response to RIF was independent of canonical organelle retrograde pathways and the ethylene signaling pathway.

AB - When covered by a layer of soil, seedling development follows a dark-specific program (skotomorphogenesis). In the dark, seedlings consist of small, non-green cotyledons, a long hypocotyl, and an apical hook to protect meristematic cells. We recently highlighted the role played by mitochondria in the high energy-consuming reprogramming of Arabidopsis skotomorphogenesis. Here, the role played by plastids, another energy-supplying organelle, in skotomorphogenesis is investigated. This study was conducted in dark conditions to exclude light signals so as to better focus on those produced by plastids. It was found that limitation of plastid gene expression (PGE) induced an exaggerated apical hook bending. Inhibition of PGE was obtained at the levels of transcription and translation using the antibiotics rifampicin (RIF) and spectinomycin, respectively, as well as plastid RPOTp RNA polymerase mutants. RIF-treated seedlings also showed expression induction of marker nuclear genes for mitochondrial stress, perturbation of mitochondrial metabolism, increased ROS levels, and an augmented capacity of oxygen consumption by mitochondrial alternative oxidases (AOXs). AOXs act to prevent overreduction of the mitochondrial electron transport chain. Previously, we reported that AOX1A, the main AOX isoform, is a key component in the developmental response to mitochondrial respiration deficiency. In this work, we suggest the involvement of AOX1A in the response to PGE dysfunction and propose the importance of signaling between plastids and mitochondria. Finally, it was found that seedling architecture reprogramming in response to RIF was independent of canonical organelle retrograde pathways and the ethylene signaling pathway.

KW - AOX1A

KW - apical hook bending

KW - Arabidopsis thaliana

KW - gene expression

KW - mitochondria

KW - plastids

KW - reactive oxygen species

KW - rifampicin

KW - skotomorphogenesis

KW - spectinomycin

UR - http://www.scopus.com/inward/record.url?scp=85149465680&partnerID=8YFLogxK

U2 - 10.1111/tpj.16134

DO - 10.1111/tpj.16134

M3 - Article

C2 - 36748183

AN - SCOPUS:85149465680

VL - 114

SP - 293

EP - 309

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 2

ER -