PPR gene family

From Purdue Genomics Database Facility

Existence of a huge gene family encoding pentatricopeptide repeat (PPR) proteins in Selaginella

Mamoru Sugita and Mitsuru Hattori sugita@gene.nagoya-u.ac.jp

The pentatricopeptide repeat (PPR) proteins are characterized by tandem repeats of a degenerate 35 amino acid motif, and are found in animals, fungi, algae and plants (1, 2). In particular, a large gene family encoding PPR proteins exists in plants, from the moss Physcomitrella patens (100 genes) to flowering plants (rice and Arabidopsis, over 450 genes) (3), but not in green alga Chlamydomonas reinhardtii (4). The majority of plant PPR proteins is predicted to be located in the mitochondria or in plastids (2). PPR proteins have been shown to play important roles in a wide range of physiological and developmental functions, namely respiration, photosynthesis, and embryogenesis (5). Several PPR proteins have been shown to be involved in posttranscriptional processes in plant organelles and are thought to be sequence-specific RNA binding proteins (5). Nucleus-localized PPR proteins are also found in Arabidopsis (6).

The expansion of the PPR family probably occurred at an evolutionary transition of early land plants from aquatic ancestors. The second large expansion may have occurred following the divergence of mosses and the lineage leading to vascular plants (3). We speculate that the large expansion of the PPR family that followed may have occurred after the divergence of non-vascular and vascular plants. Therefore, we surveyed the PPR genes in Selaginella genome sequences.

We found 1718 sequences encoding PPR motif(s) in the Selaginella genome sequences of two divergent haplotypes. This could be overestimated because many single PPR genes are probably predicted as two different genes by gene models. Therefore, the Selaginella PPR genes can be estimated to be 600 to 800 for a haplotype. A hundred forty-four sequences encode a C-terminal DYW motif containing PPR protein. Ninety and 87 PPR proteins with DYW motif are found in rice and Arabidopsis, respectively (3), and they are proposed to play a role in RNA editing within organelles (7). The number of DYW motif-containing PPR proteins is strictly correlated with the number of RNA editing sites (7). In Arabidopsis and rice, over 400 RNA editing sites are found in mitochondria (9, 10), while several editing sites are found in plastids and mitochondria in P. patens (11, 12). In contrast, neither RNA editing sites nor DYW type PPR proteins are found in Chlamydomonas. From these observations, a high frequency of RNA editing is predicted to occur in Selaginella plastids (8). In conclusion, our survey strongly suggests that the dramatic expansion of the PPR family occurred after the divergence of non-vascular and vascular plants. The increasing number of PPR genes may be correlated with the evolution of land plants towards increasing complexity and stature.

The number of PPR genes has recently been estimated to be 600 in grape (Vitis vinifera) and poplar (Populus trichocarpa) (13).

References

1. Small, I. D. and Peeters, N. (2000) The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.

2. Lurin, C., Andres, C., Aubourg, et al. (19 co-authors) (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103.

3. O’Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M. and Small, I. (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25, 1120-1128.

4. Merchant, S. S. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250.

5. Saha, D., Prasad, A. M. and Srinivasan, R. (2007) Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521-534.

6. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K. J. and Oelmuller, R. (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18, 176-197.

7. Salone, V., Rudinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V. and Lurin, C. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett., 581, 4132-4138.

8. Tsuji, S., Ueda, K., Nishiyama, T., Hasebe, M., Yoshikawa, S., Konagaya, A., Nishiuchi, T. and Yamaguchi, K. (2007) The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses. J. Plant Res. 120, 281-290.

9. Giegé, P. and Brennicke, A. (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl. Acad. Sci. USA. 96, 15324-15329.

10. Notsu, Y., Masood, S., Nishikawa, T., Kubo, N., Akiduki, G., Nakazono, M., Hirai, A. and Kadowaki, K. (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol. Genet. Genomics 268, 434-445.

11. Miyata, Y. and Sugita, M. (2004) Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J. Plant Physiol. 161, 113-115.

12. Terasawa, K., Odahara, M., Kabeya, Y., Kikugawa, T., Sekine, Y., Fujiwara, M. and Sato, N. (2007) The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol. Biol. Evol. 24, 699-709.

13. Schmitz-Linneweber, C. and Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. in press. doi:10.1016/j.tplants.2008.10.001

Table of PPR gene numbers

	Rice	Arabidopsis	Selaginella	Physcomitrella	Chlamydomonas
PPR protein genes	477	450	1718	103	12
DYW-containing PPR protein genes	90	87	144	10	0

See Full list of 1718 PPR proteins in Selaginella

See Full list of DYW-containing PPR proteins in Selaginella