A nuclear-located RNA Helicase 13 is essential for chloroplast development in Arabidopsis thaliana.

Chloroplast is a semi-autonomous organelle with a double membrane structure, and its structural stability is the prerequisite for its correct function. Chloroplast development is regulated by known nuclear-encoded chloroplast proteins or proteins encoded within the chloroplast itself. However, the mechanism of chloroplast development is involved in other organelles remains largely unknown. Here, we report that a nuclear-located DEAD-box RNA helicase 13 (RH13) is essential for chloroplast development in Arabidopsis thaliana. RH13 is widely expressed in tissues and localized to the nucleolus. Homozygous rh13 mutant shows abnormal chloroplast structure and leaf morphogenesis. Proteomic analysis shows that the expression levels of photosynthesis related proteins in chloroplasts are reduced due to loss of RH13. Furthermore, RNA-sequencing and proteomics data reveals that the expression levels of these chloroplast-related genes are decreased which undergo alternative splicing events in rh13 mutant. Taken together, we propose that nucleolus-located RH13 is critical for chloroplast development in Arabidopsis.

[1]  Xiuren Zhang,et al.  Functions and mechanisms of RNA helicases in plants. , 2022, Journal of experimental botany.

[2]  Amit Kumar Sharma,et al.  Curvature thylakoid 1 proteins modulate prolamellar body morphology and promote organized thylakoid biogenesis in Arabidopsis thaliana , 2021, Proceedings of the National Academy of Sciences.

[3]  N. Rouhier,et al.  Novel insights into the diversity of the sulfurtransferase family in photosynthetic organisms with emphasis on oak. , 2020, The New phytologist.

[4]  M. Suorsa,et al.  Arabidopsis PsbP-like protein 1 Facilitates the Assembly of the Photosystem II Supercomplexes and Optimizes Plant Fitness under Fluctuating Light. , 2020, Plant & cell physiology.

[5]  A. Grover,et al.  Cpn60β4 protein regulates growth and developmental cycling and has bearing on flowering time in Arabidopsis thaliana plants. , 2019, Plant science : an international journal of experimental plant biology.

[6]  D. Gallie,et al.  Chloroplast-localized iron superoxide dismutases FSD2 and FSD3 are functionally distinct in Arabidopsis , 2019, PloS one.

[7]  A. Murphy,et al.  The Arabidopsis ATP-BINDING CASSETTE Transporter ABCB21 Regulates Auxin Levels in Cotyledons, the Root Pericycle, and Leaves , 2019, Front. Plant Sci..

[8]  J. Rochaix,et al.  Nucleus-Encoded Protein BFA1 Promotes Efficient Assembly of the Chloroplast ATP Synthase Coupling Factor 1 , 2018, Plant Cell.

[9]  Jian Wang,et al.  SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data , 2017, GigaScience.

[10]  T. Kleine,et al.  The DEAD-box RNA Helicase RH50 Is a 23S-4.5S rRNA Maturation Factor that Functionally Overlaps with the Plastid Signaling Factor GUN11[OPEN] , 2017, Plant Physiology.

[11]  Yifan Wang,et al.  Growing Slowly 1 locus encodes a PLS-type PPR protein required for RNA editing and plant development in Arabidopsis , 2016, Journal of experimental botany.

[12]  J. Zhao,et al.  Ribosomal protein L18aB is required for both male gametophyte function and embryo development in Arabidopsis , 2016, Scientific Reports.

[13]  Shan Lu,et al.  The DnaJ-Like Zinc Finger Domain Protein PSA2 Affects Light Acclimation and Chloroplast Development in Arabidopsis thaliana , 2016, Front. Plant Sci..

[14]  M. Dassanayake,et al.  The Cytoplasmic Carbonic Anhydrases βCA2 and βCA4 Are Required for Optimal Plant Growth at Low CO21[OPEN] , 2016, Plant Physiology.

[15]  J. Fogelqvist,et al.  Loss and retention of resistance genes in five species of the Brassicaceae family , 2014, BMC Plant Biology.

[16]  D. R. Scholes,et al.  Overcompensation in Response to Herbivory in Arabidopsis thaliana: The Role of Glucose-6-Phosphate Dehydrogenase and the Oxidative Pentose-Phosphate Pathway , 2013, Genetics.

[17]  Y. Asakura,et al.  Chloroplast RH3 DEAD Box RNA Helicases in Maize and Arabidopsis Function in Splicing of Specific Group II Introns and Affect Chloroplast Ribosome Biogenesis1[W][OA] , 2012, Plant Physiology.

[18]  R. Kebeish,et al.  Constitutive and dark‐induced expression of Solanum tuberosum phosphoenolpyruvate carboxylase enhances stomatal opening and photosynthetic performance of Arabidopsis thaliana , 2012, Biotechnology and bioengineering.

[19]  Qiannan Li,et al.  The Function of RH22, a DEAD RNA Helicase, in the Biogenesis of the 50S Ribosomal Subunits of Arabidopsis Chloroplasts1[W][OA] , 2011, Plant Physiology.

[20]  Rongcheng Lin,et al.  A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. , 2011, Nature communications.

[21]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[22]  C. Hölscher,et al.  Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. , 2011, The Plant journal : for cell and molecular biology.

[23]  B. Langmead,et al.  Aligning Short Sequencing Reads with Bowtie , 2010, Current protocols in bioinformatics.

[24]  A. Yokota,et al.  A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA. , 2010, The Plant journal : for cell and molecular biology.

[25]  Hsou-min Li,et al.  Protein transport into chloroplasts. , 2010, Annual review of plant biology.

[26]  L. Ponnala,et al.  Megadalton Complexes in the Chloroplast Stroma of Arabidopsis thaliana Characterized by Size Exclusion Chromatography, Mass Spectrometry, and Hierarchical Clustering* , 2010, Molecular & Cellular Proteomics.

[27]  C. Schwarz,et al.  MRL1, a Conserved Pentatricopeptide Repeat Protein, Is Required for Stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis[C][W] , 2010, Plant Cell.

[28]  F. Kessler,et al.  Chloroplast biogenesis: diversity and regulation of the protein import apparatus. , 2009, Current opinion in cell biology.

[29]  D. Honys,et al.  AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen , 2009, Plant Molecular Biology.

[30]  K. Cline,et al.  Plastid protein import and sorting: different paths to the same compartments. , 2008, Current opinion in plant biology.

[31]  M. Ikeuchi,et al.  A Heterocomplex of Iron Superoxide Dismutases Defends Chloroplast Nucleoids against Oxidative Stress and Is Essential for Chloroplast Development in Arabidopsis[W] , 2008, The Plant Cell Online.

[32]  R. Kuras,et al.  A Novel Pathway of Cytochrome c Biogenesis Is Involved in the Assembly of the Cytochrome b6f Complex in Arabidopsis Chloroplasts* , 2008, Journal of Biological Chemistry.

[33]  M. Horowitz,et al.  AtEHDs, novel Arabidopsis EH-domain-containing proteins involved in endocytosis. , 2008, The Plant journal : for cell and molecular biology.

[34]  O. Emanuelsson,et al.  Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome , 2008, PloS one.

[35]  S. Masiero,et al.  A Complex Containing PGRL1 and PGR5 Is Involved in the Switch between Linear and Cyclic Electron Flow in Arabidopsis , 2008, Cell.

[36]  H. Cho,et al.  A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[37]  F. Sato,et al.  Distinct Functions for the Two PsbP-Like Proteins PPL1 and PPL2 in the Chloroplast Thylakoid Lumen of Arabidopsis1[W][OA] , 2007, Plant Physiology.

[38]  N. Tanner,et al.  The DEAD-box protein family of RNA helicases. , 2006, Gene.

[39]  A. Lecharny,et al.  DEAD-box RNA helicases in Arabidopsis thaliana: establishing a link between quantitative expression, gene structure and evolution of a family of genes. , 2004, Plant biotechnology journal.

[40]  R. Lin,et al.  DExD/H-box proteins and their partners: helping RNA helicases unwind. , 2003, Gene.

[41]  D. Mckay,et al.  Helicase structure and mechanism. , 2002, Current opinion in structural biology.

[42]  U. Grossniklaus,et al.  Delayed activation of the paternal genome during seed development , 2022 .

[43]  F. Wollman,et al.  The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1 , 1999, Biochimica et biophysica acta.

[44]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[45]  Enrico Schleiff,et al.  Protein import into chloroplasts , 2004, Nature Reviews Molecular Cell Biology.

[46]  N. Mitsukawa,et al.  Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. , 1995, The Plant journal : for cell and molecular biology.

[47]  S Y Rhee,et al.  Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. , 1994, Science.

[48]  K. Harter,et al.  Bimolecular fluorescence complementation (BiFC) to study protein-protein interactions in living plant cells. , 2009, Methods in molecular biology.

[49]  S. Aubourg,et al.  The DEAD box RNA helicase family in Arabidopsis thaliana. , 1999, Nucleic acids research.

[50]  D. Arnon.  COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.