The Mitochondrion-Targeted PENTATRICOPEPTIDE REPEAT78 Protein Is Required for nad5 Mature mRNA Stability and Seed Development in Maize

被引:50
作者
Zhang, Ya-Feng [2 ]
Suzuki, Masaharu [3 ]
Sun, Feng [1 ]
Tan, Bao-Cai [1 ]
机构
[1] Shandong Univ, Sch Life Sci, Minist Educ, Key Lab Plant Cell Engn & Germplasm Innovat, Jinan 250100, Shandong, Peoples R China
[2] South China Agr Univ, Coll Agr, Guangdong Prov Key Lab Plant Mol Breeding, Guangzhou 510642, Guangdong, Peoples R China
[3] Univ Florida, Plant Mol & Cellular Biol Program, Gainesville, FL 32611 USA
基金
中国国家自然科学基金;
关键词
PPR; nad5; mitochondrial RNA stability; complex I; seed development; maize; PLANT MITOCHONDRIAL; PPR PROTEIN; TRANSCRIPT; END; MECHANISM; SEQUENCE; BINDING; TERMINI; GENES; STABILIZATION;
D O I
10.1016/j.molp.2017.09.009
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Pentatricopepetide repeat (PPR) proteins are a large family of RNA-binding proteins involved in RNA metabolism in plant organelles. Although many PPR proteins have been functionally studied, few of them are identified with a function in mitochondrial RNA stability. By using a reverse genetic approach, we characterized the role of the mitochondrion-targeted PPR78 protein in nad5 mature mRNA stability and maize (Zea mays) seed development. Loss of PPR78 function leads to a dramatic reduction in the steady-state level of mitochondrial nad5 mature mRNA, blocks the assembly of complex I in the electron transport chain, and causes an arrest in embryogenesis and endosperm development. Characterization of a second strong allele confirms the function of PPR78 in nad5 mRNA accumulation and maize seed development. The generation of mature nad5 requires the assembly of three distinct precursor RNAs via trans-splicing reactions, and the accumulation of nad5T1 precursor is reduced in the ppr78 mutants. However, it is the instability of mature nad5 rather than nad5T1 causing loss of the full-length nad5 transcript, and degradation of nad5 losing both translation start and stop codons is enriched in the mutant. Our data imply the assembly of mature nad5 mRNA precedes the protection of PPR78.
引用
收藏
页码:1321 / 1333
页数:13
相关论文
共 41 条
[1]  
[Anonymous], 2013, Abstr Appl Anal, DOI [DOI 10.1155/2013/157140, DOI 10.4225/08/58B5BAAD4FCC2]
[2]   Structure of a PLS-class Pentatricopeptide Repeat Protein Provides Insights into Mechanism of RNA Recognition [J].
Ban, Ting ;
Ke, Jiyuan ;
Chen, Runze ;
Gu, Xin ;
Tan, M. H. Eileen ;
Zhou, X. Edward ;
Kang, Yanyong ;
Melcher, Karsten ;
Zhu, Jian-Kang ;
Xu, H. Eric .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2013, 288 (44) :31540-31548
[3]   Pentatricopeptide Repeat Proteins in Plants [J].
Barkan, Alice ;
Small, Ian .
ANNUAL REVIEW OF PLANT BIOLOGY, VOL 65, 2014, 65 :415-+
[4]   A Combinatorial Amino Acid Code for RNA Recognition by Pentatricopeptide Repeat Proteins [J].
Barkan, Alice ;
Rojas, Margarita ;
Fujii, Sota ;
Yap, Aaron ;
Chong, Yee Seng ;
Bond, Charles S. ;
Small, Ian .
PLOS GENETICS, 2012, 8 (08)
[5]   P-class pentatricopeptide repeat proteins are required for efficient 5′ end formation of plant mitochondrial transcripts [J].
Binder, Stefan ;
Stoll, Katrin ;
Stoll, Birgit .
RNA BIOLOGY, 2013, 10 (09) :1511-1519
[6]   Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants [J].
Cheng, Shifeng ;
Gutmann, Bernard ;
Zhong, Xiao ;
Ye, Yongtao ;
Fisher, Mark F. ;
Bai, Fengqi ;
Castleden, Ian ;
Song, Yue ;
Song, Bo ;
Huang, Jiaying ;
Liu, Xin ;
Xu, Xun ;
Lim, Boon L. ;
Bond, Charles S. ;
Yiu, Siu-Ming ;
Small, Ian .
PLANT JOURNAL, 2016, 85 (04) :532-547
[7]   Sequence and comparative analysis of the maize NB mitochondrial genome [J].
Clifton, SW ;
Minx, P ;
Fauron, CMR ;
Gibson, M ;
Allen, JO ;
Sun, H ;
Thompson, M ;
Barbazuk, WB ;
Kanuganti, S ;
Tayloe, C ;
Meyer, L ;
Wilson, RK ;
Newton, KJ .
PLANT PHYSIOLOGY, 2004, 136 (03) :3486-3503
[8]   Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles [J].
Delannoy, E. ;
Stanley, W. A. ;
Bond, C. S. ;
Small, I. D. .
BIOCHEMICAL SOCIETY TRANSACTIONS, 2007, 35 :1643-1647
[9]   The Pentatricopeptide Repeat Proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 Are Involved in the Splicing of the Multipartite nad5 Transcript Encoding a Subunit of Mitochondrial Complex I [J].
des Francs-Small, Catherine Colas ;
de Longevialle, Andeol Falcon ;
Li, Yunhai ;
Lowe, Elizabeth ;
Tanz, Sandra K. ;
Smith, Caroline ;
Bevan, Michael W. ;
Small, Ian .
PLANT PHYSIOLOGY, 2014, 165 (04) :1409-1416
[10]   Mapping of mitochondrial mRNA termini in Arabidopsis thaliana:: t-elements contribute to 5′ and 3′ end formation [J].
Forner, Joachim ;
Weber, Bärbel ;
Thuss, Sabine ;
Wildum, Steffen ;
Binder, Stefan .
NUCLEIC ACIDS RESEARCH, 2007, 35 (11) :3676-3692