Dynamics of Chloroplast Translation during Chloroplast Differentiation in Maize

被引:93
作者
Chotewutmontri, Prakitchai [1 ]
Barkan, Alice [1 ]
机构
[1] Univ Oregon, Inst Mol Biol, Eugene, OR 97403 USA
来源
PLOS GENETICS | 2016年 / 12卷 / 07期
基金
美国国家科学基金会;
关键词
RIBOSOME PROFILING REVEALS; PENTATRICOPEPTIDE REPEAT PROTEIN; PHOTOSYSTEM-II COMPONENTS; LAND PLANT CHLOROPLASTS; MESSENGER-RNA STABILITY; NUCLEUS-ENCODED FACTOR; GENE COPY NUMBER; CHLAMYDOMONAS-REINHARDTII; BUNDLE-SHEATH; LEAF DEVELOPMENT;
D O I
10.1371/journal.pgen.1006106
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
Chloroplast genomes in land plants contain approximately 100 genes, the majority of which reside in polycistronic transcription units derived from cyanobacterial operons. The expression of chloroplast genes is integrated into developmental programs underlying the differentiation of photosynthetic cells from non-photosynthetic progenitors. In C4 plants, the partitioning of photosynthesis between two cell types, bundle sheath and mesophyll, adds an additional layer of complexity. We used ribosome profiling and RNA-seq to generate a comprehensive description of chloroplast gene expression at four stages of chloroplast differentiation, as displayed along the maize seedling leaf blade. The rate of protein output of most genes increases early in development and declines once the photosynthetic apparatus is mature. The developmental dynamics of protein output fall into several patterns. Programmed changes in mRNA abundance make a strong contribution to the developmental shifts in protein output, but output is further adjusted by changes in translational efficiency. RNAs with prioritized translation early in development are largely involved in chloroplast gene expression, whereas those with prioritized translation in photosynthetic tissues are generally involved in photosynthesis. Differential gene expression in bundle sheath and mesophyll chloroplasts results primarily from differences in mRNA abundance, but differences in translational efficiency amplify mRNA-level effects in some instances. In most cases, rates of protein output approximate steady-state protein stoichiometries, implying a limited role for proteolysis in eliminating unassembled or damaged proteins under non-stress conditions. Tuned protein output results from gene-specific trade-offs between translational efficiency and mRNA abundance, both of which span a large dynamic range. Analysis of ribosome footprints at sites of RNA editing showed that the chloroplast translation machinery does not generally discriminate between edited and unedited RNAs. However, editing of ACG to AUG at the rpl2 start codon is essential for translation initiation, demonstrating that ACG does not serve as a start codon in maize chloroplasts.
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页数:28
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共 97 条
  • [31] RNA binding and RNA remodeling activities of the half-a-tetratricopeptide (HAT) protein HCF107 underlie its effects on gene expression
    Hammani, Kamel
    Cook, William B.
    Barkan, Alice
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2012, 109 (15) : 5651 - 5656
  • [32] Ribosome Profiling of Mouse Embryonic Stem Cells Reveals the Complexity and Dynamics of Mammalian Proteomes
    Ingolia, Nicholas T.
    Lareau, Liana F.
    Weissman, Jonathan S.
    [J]. CELL, 2011, 147 (04) : 789 - 802
  • [33] Photosystem II repair in plant chloroplasts - Regulation, assisting proteins and shared components with photosystem II biogenesis
    Jarvi, Sari
    Suorsa, Marjaana
    Aro, Eva-Mari
    [J]. BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS, 2015, 1847 (09): : 900 - 909
  • [34] Biogenesis and homeostasis of chloroplasts and other plastids
    Jarvis, Paul
    Lopez-Juez, Enrique
    [J]. NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2013, 14 (12) : 787 - 802
  • [35] Identification and remediation of biases in the activity of RNA ligases in small-RNA deep sequencing
    Jayaprakash, Anitha D.
    Jabado, Omar
    Brown, Brian D.
    Sachidanandam, Ravi
    [J]. NUCLEIC ACIDS RESEARCH, 2011, 39 (21) : e141
  • [36] Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis
    Juntawong, Piyada
    Girke, Thomas
    Bazin, Jermie
    Bailey-Serres, Julia
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (01) : E203 - E212
  • [37] KLAFF P, 1991, PLANT CELL, V3, P517, DOI 10.1105/tpc.3.5.517
  • [38] The Plastid Genome-Encoded Ycf4 Protein Functions as a Nonessential Assembly Factor for Photosystem I in Higher Plants
    Krech, Katharina
    Ruf, Stephanie
    Masduki, Fifi F.
    Thiele, Wolfram
    Bednarczyk, Dominika
    Albus, Christin A.
    Tiller, Nadine
    Hasse, Claudia
    Schoettler, Mark A.
    Bock, Ralph
    [J]. PLANT PHYSIOLOGY, 2012, 159 (02) : 579 - +
  • [39] DIFFERENTIAL TRANSCRIPTION OF PLASTOME-ENCODED GENES IN THE MESOPHYLL AND BUNDLE-SHEATH CHLOROPLASTS OF THE MONOCOTYLEDONOUS NADP-MALIC ENZYME-TYPE C-4 PLANTS MAIZE AND SORGHUM
    KUBICKI, A
    STEINMULLER, K
    WESTHOFF, P
    [J]. PLANT MOLECULAR BIOLOGY, 1994, 25 (04) : 669 - 679
  • [40] Langmead B, 2012, NAT METHODS, V9, P357, DOI [10.1038/NMETH.1923, 10.1038/nmeth.1923]