In vivo functional analysis of a nuclear restorer PPR protein View Full Text


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Article Info

DATE

2014-11-18

AUTHORS

Xike Qin, Richard Warguchuk, Nadège Arnal, Lydiane Gaborieau, Hakim Mireau, Gregory G Brown

ABSTRACT

BackgroundNuclear restorers of cytoplasmic male fertility (CMS) act to suppress the male sterile phenotype by down-regulating the expression of novel CMS-specifying mitochondrial genes. One such restorer gene is Rfo, which restores fertility to the radish Ogura or ogu CMS. Rfo, like most characterized restorers, encodes a pentatricopeptide repeat (PPR) protein, a family of eukaryotic proteins characterized by tandem repeats of a 35 amino acid motif. While over 400 PPR genes are found in characterized plant genomes and the importance of this gene family in organelle gene expression is widely recognized, few detailed in vivo assessments of primary structure-function relationships in this protein family have been conducted.ResultsIn contrast to earlier studies, which identified 16 or 17 PPR domains in the Rfo protein, we now find, using a more recently developed predictive tool, that Rfo has 18 repeat domains with the additional domain N-terminal to the others. Comparison of transcript sequences from pooled rfo/rfo plants with pooled Rfo/Rfo plants of a mapping population led to the identification of a non-restoring rfo allele with a 12 bp deletion in the fourth domain. Introduction into ogu CMS plants of a genetic construct in which this deletion had been introduced into Rfo led to a partial loss in the capacity to produce viable pollen, as assessed by vital staining, pollen germination and the capacity for seed production following pollination of CMS plants. The degree of viable pollen production among different transgenic plants roughly correlated with the copy number of the introduced gene and with the reduction of the levels of the ORF138 CMS-associated protein. All other constructs tested, including one in which only the C-terminal PPR repeat was deleted and another in which this repeat was replaced by the corresponding domain of the related, non-restoring gene, PPR-A, failed to result in any measure of fertility restoration.ConclusionsThe identification of the additional PPR domain in Rfo indicates that the protein, apart from its N-terminal mitochondrial targeting presequence, consists almost entirely of PPR repeats. The newly identified rfo allele carries the same 4 amino acid deletion as that found in the neighboring, related, non-restoring PPR gene, PPR-A. Introduction of this four amino acid deletion into a central domain the Rfo protein, however, only partially reduces its restoration capacity, even though this alteration might be expected to alter the spacing between the adjoining repeats. All other tested alterations, generated by deleting specific PPR repeats or exchanging repeats with corresponding domains of PPR-A, led to a complete loss of restorer function. Overall we demonstrate that introduction of targeted alterations of Rfo into ogu CMS plants provides a sensitive in vivo readout for analysis of the relationship between primary structure and biological function in this important family of plant proteins. More... »

PAGES

313

References to SciGraph publications

  • 2007-05-23. Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection in BMC GENOMICS
  • 2010-02-24. Sequence analysis of two alleles reveals that intra-and intergenic recombination played a role in the evolution of the radish fertility restorer (Rfo) in BMC PLANT BIOLOGY
  • 2013-10-27. Structural basis for the modular recognition of single-stranded RNA by PPR proteins in NATURE
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  • 1998-07. Characterisation of the radish introgression carrying the Rfo restorer gene for the Ogu-INRA cytoplasmic male sterility in rapeseed (Brassica napus L.) in THEORETICAL AND APPLIED GENETICS
  • 2009-02-08. The Ogura sterility-inducing protein forms a large complex without interfering with the oxidative phosphorylation components in rapeseed mitochondria in PLANT MOLECULAR BIOLOGY
  • 1994-09. Ogura cytoplasmic male-sterility (CMS)-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica cybrids in MOLECULAR GENETICS AND GENOMICS
  • 1999-07. The restorer Rfo gene acts post-translationally on the stability of the ORF138 Ogura CMS-associated protein in reproductive tissues of rapeseed cybrids in PLANT MOLECULAR BIOLOGY
  • 1994-11. Organ-specific reduction in the abundance of a mitochondrial protein accompanies fertility restoration in cytoplasmic male-sterile radish in PLANT MOLECULAR BIOLOGY
  • 1983-08. Intergeneric cytoplasmic hybridization in cruciferae by protoplast fusion in MOLECULAR GENETICS AND GENOMICS
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    http://scigraph.springernature.com/pub.10.1186/s12870-014-0313-4

    DOI

    http://dx.doi.org/10.1186/s12870-014-0313-4

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    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/25403785


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        "description": "BackgroundNuclear restorers of cytoplasmic male fertility (CMS) act to suppress the male sterile phenotype by down-regulating the expression of novel CMS-specifying mitochondrial genes. One such restorer gene is Rfo, which restores fertility to the radish Ogura or ogu CMS. Rfo, like most characterized restorers, encodes a pentatricopeptide repeat (PPR) protein, a family of eukaryotic proteins characterized by tandem repeats of a 35 amino acid motif. While over 400 PPR genes are found in characterized plant genomes and the importance of this gene family in organelle gene expression is widely recognized, few detailed in vivo assessments of primary structure-function relationships in this protein family have been conducted.ResultsIn contrast to earlier studies, which identified 16 or 17 PPR domains in the Rfo protein, we now find, using a more recently developed predictive tool, that Rfo has 18 repeat domains with the additional domain N-terminal to the others. Comparison of transcript sequences from pooled rfo/rfo plants with pooled Rfo/Rfo plants of a mapping population led to the identification of a non-restoring rfo allele with a 12 bp deletion in the fourth domain. Introduction into ogu CMS plants of a genetic construct in which this deletion had been introduced into Rfo led to a partial loss in the capacity to produce viable pollen, as assessed by vital staining, pollen germination and the capacity for seed production following pollination of CMS plants. The degree of viable pollen production among different transgenic plants roughly correlated with the copy number of the introduced gene and with the reduction of the levels of the ORF138 CMS-associated protein. All other constructs tested, including one in which only the C-terminal PPR repeat was deleted and another in which this repeat was replaced by the corresponding domain of the related, non-restoring gene, PPR-A, failed to result in any measure of fertility restoration.ConclusionsThe identification of the additional PPR domain in Rfo indicates that the protein, apart from its N-terminal mitochondrial targeting presequence, consists almost entirely of PPR repeats. The newly identified rfo allele carries the same 4 amino acid deletion as that found in the neighboring, related, non-restoring PPR gene, PPR-A. Introduction of this four amino acid deletion into a central domain the Rfo protein, however, only partially reduces its restoration capacity, even though this alteration might be expected to alter the spacing between the adjoining repeats. All other tested alterations, generated by deleting specific PPR repeats or exchanging repeats with corresponding domains of PPR-A, led to a complete loss of restorer function. Overall we demonstrate that introduction of targeted alterations of Rfo into ogu CMS plants provides a sensitive in vivo readout for analysis of the relationship between primary structure and biological function in this important family of plant proteins.", 
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    33 schema:description BackgroundNuclear restorers of cytoplasmic male fertility (CMS) act to suppress the male sterile phenotype by down-regulating the expression of novel CMS-specifying mitochondrial genes. One such restorer gene is Rfo, which restores fertility to the radish Ogura or ogu CMS. Rfo, like most characterized restorers, encodes a pentatricopeptide repeat (PPR) protein, a family of eukaryotic proteins characterized by tandem repeats of a 35 amino acid motif. While over 400 PPR genes are found in characterized plant genomes and the importance of this gene family in organelle gene expression is widely recognized, few detailed in vivo assessments of primary structure-function relationships in this protein family have been conducted.ResultsIn contrast to earlier studies, which identified 16 or 17 PPR domains in the Rfo protein, we now find, using a more recently developed predictive tool, that Rfo has 18 repeat domains with the additional domain N-terminal to the others. Comparison of transcript sequences from pooled rfo/rfo plants with pooled Rfo/Rfo plants of a mapping population led to the identification of a non-restoring rfo allele with a 12 bp deletion in the fourth domain. Introduction into ogu CMS plants of a genetic construct in which this deletion had been introduced into Rfo led to a partial loss in the capacity to produce viable pollen, as assessed by vital staining, pollen germination and the capacity for seed production following pollination of CMS plants. The degree of viable pollen production among different transgenic plants roughly correlated with the copy number of the introduced gene and with the reduction of the levels of the ORF138 CMS-associated protein. All other constructs tested, including one in which only the C-terminal PPR repeat was deleted and another in which this repeat was replaced by the corresponding domain of the related, non-restoring gene, PPR-A, failed to result in any measure of fertility restoration.ConclusionsThe identification of the additional PPR domain in Rfo indicates that the protein, apart from its N-terminal mitochondrial targeting presequence, consists almost entirely of PPR repeats. The newly identified rfo allele carries the same 4 amino acid deletion as that found in the neighboring, related, non-restoring PPR gene, PPR-A. Introduction of this four amino acid deletion into a central domain the Rfo protein, however, only partially reduces its restoration capacity, even though this alteration might be expected to alter the spacing between the adjoining repeats. All other tested alterations, generated by deleting specific PPR repeats or exchanging repeats with corresponding domains of PPR-A, led to a complete loss of restorer function. Overall we demonstrate that introduction of targeted alterations of Rfo into ogu CMS plants provides a sensitive in vivo readout for analysis of the relationship between primary structure and biological function in this important family of plant proteins.
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    40 schema:keywords CMS
    41 CMS plants
    42 ConclusionsThe identification
    43 N-terminal
    44 Ogura
    45 PPR
    46 PPR domains
    47 PPR genes
    48 PPR proteins
    49 PPR repeats
    50 RFOs
    51 ResultsIn contrast
    52 acid deletion
    53 acid motif
    54 acts
    55 alleles
    56 alterations
    57 amino acid deletion
    58 amino acid motifs
    59 analysis
    60 assessment
    61 biological functions
    62 bp deletion
    63 capacity
    64 central domain
    65 comparison
    66 complete loss
    67 constructs
    68 contrast
    69 copy number
    70 corresponding domain
    71 degree
    72 deletion
    73 different transgenic plants
    74 domain
    75 domain N-terminal
    76 earlier studies
    77 eukaryotic proteins
    78 expression
    79 family
    80 fertility
    81 fertility restoration
    82 fourth domain
    83 function
    84 functional analysis
    85 gene expression
    86 gene family
    87 genes
    88 genetic constructs
    89 genome
    90 germination
    91 identification
    92 importance
    93 important family
    94 introduction
    95 levels
    96 loss
    97 male-sterile phenotype
    98 mapping population
    99 measures
    100 mitochondrial genes
    101 motif
    102 neighboring
    103 novel CMS
    104 number
    105 ogu CMS
    106 organelle gene expression
    107 partial loss
    108 pentatricopeptide repeat protein
    109 phenotype
    110 plant genomes
    111 plant proteins
    112 plants
    113 pollen
    114 pollen germination
    115 pollen production
    116 pollination
    117 population
    118 predictive tool
    119 presequence
    120 primary structure
    121 production
    122 protein
    123 protein family
    124 readout
    125 reduction
    126 relationship
    127 repeat domain
    128 repeat proteins
    129 repeats
    130 restoration
    131 restoration capacity
    132 restorer
    133 restorer gene
    134 seed production
    135 sensitive
    136 sequence
    137 spacing
    138 staining
    139 sterile phenotype
    140 structure
    141 structure-function relationships
    142 study
    143 tandem repeats
    144 tool
    145 transcript sequences
    146 transgenic plants
    147 viable pollen
    148 viable pollen production
    149 vital staining
    150 vivo assessment
    151 vivo functional analysis
    152 vivo readout
    153 schema:name In vivo functional analysis of a nuclear restorer PPR protein
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