RNA editing affects the potential protein kinase phosphorylation sites in mitochondrial proteins --Konstantinov, YM, Arziev, AS It is well known that both transcriptional and post-transcriptional events play important roles in governing the expression of the maize mitochondrial genes (Finnegan, Brown, Plant Cell 2:71-83, 1990). RNA editing in plant mitochondria involves post-transcriptional conversion of hundreds of different cytidine residues to uridine, or uridine-like, residues. Moreover, few uridine to cytidine transitions have been detected (Cattaneo, Annu. Rev. Genet. 25:71-88, 1991). From 668 editing sites in plant mitochondria transcripts studied so far, it appears that 60% of the edited codons correspond to Ser and Pro codons (Araya, Bégu, Litvak, Physiol. Plant. 91:543-550, 1994). We propose that part of these changes of Ser codons under RNA editing may lead to the damage of some protein kinase phosphorylation sites in mitochondrial proteins. Mitochondrial proteins are potential targets for the catalytic action of at least three types of protein kinases: protein kinase C, casein kinase II and tyrosine kinase. Therefore the change of protein kinase phosphorylation sites may also be the result of substitution of some other amino acids in the pattern of phosphorylation sites under transcript editing. If partially edited transcripts are translated, such an alteration of the phosphorylation state of definite mitochondrial proteins may be a part of a special physiological regulation mechanism.

The aim of this work was to check the hypothesis that the editing events in primary transcripts may influence the protein kinase phosphorylation pattern of genomically deduced proteins through alteration of protein kinase phosphorylation sites. For that purpose, we studied the presumed protein kinase phosphorylation site patterns in the genomically encoded proteins, and proteins translated from an edited mRNA.

Amino acid sequences of mitochondrially encoded polypeptides (ATP6, COX2, NAD4L, NAD3, NAD9), before and after editing of the appropriate mRNAs, are taken from the EMBL Nucleotide Sequence Database (the nucleotide sequence data under the accession numbers M16223, Z11843, V00712, J01425, X52865, AB015175, X52200, AF279446, AF279447, AB020062) (http://www.ebi.ac.uk/). The analysis of protein kinase phosphorylation patterns in mitochondrial proteins was performed using the PROSCAN (PROSITE SCAN) program (http://npsa-pbil.ibcp.fr/).

The sequence comparison of Zea mays and other plant species' mitochondrially encoded polypeptides, before and after editing of the appropriate mRNAs, reveals a significant number of amino acid replacements leading to alteration of presumed protein kinase phosphorylation sites (Table). Thus, in maize, RNA editing damages one protein kinase C phosphorylation site in the mitochondrial ATPase complex subunit 6 gene transcript of the C male-sterile cytoplasm (Kumar and Levings, Curr. Genet. 23:154-9, 1993), and one phosphorylation site for tyrosine kinase in subunit II of cytochrome c oxidase. A similar situation was revealed for Beta vulgaris ATPase subunit 6 transcript editing, with alteration of the protein kinase C phosphorylation site. RNA editing of subunit 3 NADH dehydrogenase transcript in Oenothera berteriana decreases the number of phosphorylation sites for casein kinase II from 5 to 3, and damages the site for protein kinase C. The alteration of protein kinase C phosphorylation site number was also shown for ATPase subunit 6 in Sorghum bicolor. Therefore one consequence of RNA editing in plant mitochondria is to change protein kinase phosphorylation site patterns in mitochondrial enzyme subunits.
 
 

Table. The alteration of potential protein kinase phosphorylation sites in mitochondrial proteins through RNA editing
 
Species Protein  Protein kinase
Number of phosphorylation sites per molecule 
Sites and their location
Zea mays ATP6 Protein kinase C 
2
69TKK
       
213SVK 
    Casein kinase II
3
25SPLD 
       
83SLVE
       
247TGLE
  ATP6* Protein kinase C
1
207TKK
    Casein kinase II
3
163SPLD
       
221SLVE
       
385TGLE
  COX2 Protein kinase C
2
119TIK 
       
243TLK
    Casein kinase II
4
81TTIE 
       
138SSDE 
       
183TPAD 
       
243TLKD
    Tyrosine kinase
1
129RSYEYSDY 
  COX2* Protein kinase C 
2
119TIK
       
243TLK
    Casein kinase II
4
81TTIE 
       
138SSDE 
       
183TPAD 
       
243TLKD
    Tyrosine kinase
0
-
         
Beta vulgaris ATP6 Protein kinase C
2
32TKK 
       
176SVK
    Casein kinase II
2
46SLVE
       
210TGLE
  ATP6* Protein kinase C
1
32TKK
    Casein kinase II
2
46SLVE
       
210TGLE 
  NAD4L Protein kinase C
2
2SIK
       
83TFR
    Casein kinase II
1
52SSDD 
  NAD4L* Protein kinase C 
2
2SIK
       
83TFR
    Casein kinase II
1
52SSDD 
         
Oenothera berteriana NAD3 Protein kinase C 
1
115SDR
    Casein kinase II
5
34TYPE
       
40SAYE
       
54SRFD 
       
106SLYE
       
115SDRE
    Tyrosine kinase
1
53RSRFDIRFY 
  NAD3* Protein kinase C
0
-
    Casein kinase II
3
34TYPE
       
40SAYE
       
54SRFD 
    Tyrosine kinase
1
53RSRFDIRFY 
         
Sorghum bicolor ATP6 Protein kinase C
4
26TRR
       
61TGR 
       
172TKK 
       
316SVK
    Casein kinase II
4
7SLTD
       
128SPLD
       
186SLVE
       
350TGLE 
  ATP6* Protein kinase C 
3
26TRR
       
61TGR 
       
172TKK 
    Casein kinase II
4 
7SLTD
       
128SPLD
       
186SLVE
       
350TGLE 
         
Lupinus luteus NAD9 Protein kinase C 
2
66SRK 
       
79STR
    Casein kinase II
4
33TNTD
       
90TSAD
       
91SADE
       
182SPWE
    Tyrosine kinase
2
69RRFEVVY
       
68KRRFEVVY
  NAD9* Protein kinase C 
2
66SRK
       
79STR 
    Casein kinase II
4
33TNTD
       
90TSAD
       
91SADE
       
182SPWE
    Tyrosine kinase
2
69RRFEVVY
       
68KRRFEVVY
Protein abbreviations without asterisks correspond to sequence-deduced protein. An asterisk designates protein translated from an edited mRNA.

We suggest also that the change in potential protein kinase phosphorylation site numbers in mitochondrial proteins under RNA editing is a remnant of some evolutionary mechanism to alterate or modify the functional activity of proteins in plant mitochondria.
 
 
 
 

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