Skip to main content
Genetics logoLink to Genetics
. 2003 Jan;163(1):311–319. doi: 10.1093/genetics/163.1.311

Unexpected complexity of poly(A)-binding protein gene families in flowering plants: three conserved lineages that are at least 200 million years old and possible auto- and cross-regulation.

Dmitry A Belostotsky 1
PMCID: PMC1462424  PMID: 12586718

Abstract

Eukaryotic poly(A)-binding protein (PABP) is a ubiquitous, essential factor involved in mRNA biogenesis, translation, and turnover. Most eukaryotes examined have only one or a few PABPs. In contrast, eight expressed PABP genes are present in Arabidopsis thaliana. These genes fall into three distinct classes, based on highly concordant results of (i) phylogenetic analysis of the amino acid sequences of the encoded proteins, (ii) analysis of the intron number and placement, and (iii) surveys of gene expression patterns. Representatives of each of the three classes also exist in the rice genome, suggesting that the diversification of the plant PABP genes has occurred prior to the split of monocots and dicots >or=200 MYA. Experiments with the recombinant PAB3 protein suggest the possibility of a negative feedback regulation, as well as of cross-regulation between the Arabidopsis PABPs that belong to different classes but are simultaneously expressed in the same cell type. Such a high complexity of the plant PABPs might enable a very fine regulation of organismal growth and development at the post-transcriptional level, compared with PABPs of other eukaryotes.

Full Text

The Full Text of this article is available as a PDF (391.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. An Y. Q., Huang S., McDowell J. M., McKinney E. C., Meagher R. B. Conserved expression of the Arabidopsis ACT1 and ACT 3 actin subclass in organ primordia and mature pollen. Plant Cell. 1996 Jan;8(1):15–30. doi: 10.1105/tpc.8.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bag J. Feedback inhibition of poly(A)-binding protein mRNA translation. A possible mechanism of translation arrest by stalled 40 S ribosomal subunits. J Biol Chem. 2001 Oct 4;276(50):47352–47360. doi: 10.1074/jbc.M107676200. [DOI] [PubMed] [Google Scholar]
  4. Belostotsky D. A., Meagher R. B. A pollen-, ovule-, and early embryo-specific poly(A) binding protein from Arabidopsis complements essential functions in yeast. Plant Cell. 1996 Aug;8(8):1261–1275. doi: 10.1105/tpc.8.8.1261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belostotsky D. A., Meagher R. B. Differential organ-specific expression of three poly(A)-binding-protein genes from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6686–6690. doi: 10.1073/pnas.90.14.6686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bernstein P., Peltz S. W., Ross J. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol Cell Biol. 1989 Feb;9(2):659–670. doi: 10.1128/mcb.9.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. T., Johnson A. W. A cis-acting element known to block 3' mRNA degradation enhances expression of polyA-minus mRNA in wild-type yeast cells and phenocopies a ski mutant. RNA. 2001 Nov;7(11):1566–1577. [PMC free article] [PubMed] [Google Scholar]
  8. Burd C. G., Matunis E. L., Dreyfuss G. The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities. Mol Cell Biol. 1991 Jul;11(7):3419–3424. doi: 10.1128/mcb.11.7.3419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Caponigro G., Parker R. Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol Rev. 1996 Mar;60(1):233–249. doi: 10.1128/mr.60.1.233-249.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Caponigro G., Parker R. Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Dev. 1995 Oct 1;9(19):2421–2432. doi: 10.1101/gad.9.19.2421. [DOI] [PubMed] [Google Scholar]
  11. Chekanova J. A., Shaw R. J., Belostotsky D. A. Analysis of an essential requirement for the poly(A) binding protein function using cross-species complementation. Curr Biol. 2001 Aug 7;11(15):1207–1214. doi: 10.1016/s0960-9822(01)00371-2. [DOI] [PubMed] [Google Scholar]
  12. Chekanova J. A., Shaw R. J., Wills M. A., Belostotsky D. A. Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8 S rRNA processing and mRNA decay defects of the yeast ski6 mutant and is found in an exosome-sized complex in plant and yeast cells. J Biol Chem. 2000 Oct 20;275(42):33158–33166. doi: 10.1074/jbc.M005493200. [DOI] [PubMed] [Google Scholar]
  13. Clough S. J., Bent A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998 Dec;16(6):735–743. doi: 10.1046/j.1365-313x.1998.00343.x. [DOI] [PubMed] [Google Scholar]
  14. Coller J. M., Gray N. K., Wickens M. P. mRNA stabilization by poly(A) binding protein is independent of poly(A) and requires translation. Genes Dev. 1998 Oct 15;12(20):3226–3235. doi: 10.1101/gad.12.20.3226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cosson Bertrand, Couturier Anne, Chabelskaya Svetlana, Kiktev Denis, Inge-Vechtomov Sergey, Philippe Michel, Zhouravleva Galina. Poly(A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI(+)] propagation. Mol Cell Biol. 2002 May;22(10):3301–3315. doi: 10.1128/MCB.22.10.3301-3315.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Deardorff J. A., Sachs A. B. Differential effects of aromatic and charged residue substitutions in the RNA binding domains of the yeast poly(A)-binding protein. J Mol Biol. 1997 May 30;269(1):67–81. doi: 10.1006/jmbi.1997.1013. [DOI] [PubMed] [Google Scholar]
  17. Deo R. C., Bonanno J. B., Sonenberg N., Burley S. K. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell. 1999 Sep 17;98(6):835–845. doi: 10.1016/s0092-8674(00)81517-2. [DOI] [PubMed] [Google Scholar]
  18. Gallie D. R. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 1991 Nov;5(11):2108–2116. doi: 10.1101/gad.5.11.2108. [DOI] [PubMed] [Google Scholar]
  19. Gutierrez Rodrigo A., Ewing Rob M., Cherry J. Michael, Green Pamela J. Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc Natl Acad Sci U S A. 2002 Aug 7;99(17):11513–11518. doi: 10.1073/pnas.152204099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Görlach M., Burd C. G., Dreyfuss G. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp Cell Res. 1994 Apr;211(2):400–407. doi: 10.1006/excr.1994.1104. [DOI] [PubMed] [Google Scholar]
  21. Hornstein E., Git A., Braunstein I., Avni D., Meyuhas O. The expression of poly(A)-binding protein gene is translationally regulated in a growth-dependent fashion through a 5'-terminal oligopyrimidine tract motif. J Biol Chem. 1999 Jan 15;274(3):1708–1714. doi: 10.1074/jbc.274.3.1708. [DOI] [PubMed] [Google Scholar]
  22. Hoshino S., Imai M., Kobayashi T., Uchida N., Katada T. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3'-Poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J Biol Chem. 1999 Jun 11;274(24):16677–16680. doi: 10.1074/jbc.274.24.16677. [DOI] [PubMed] [Google Scholar]
  23. Imataka H., Gradi A., Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 1998 Dec 15;17(24):7480–7489. doi: 10.1093/emboj/17.24.7480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kessler S. H., Sachs A. B. RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol Cell Biol. 1998 Jan;18(1):51–57. doi: 10.1128/mcb.18.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Khaleghpour K., Kahvejian A., De Crescenzo G., Roy G., Svitkin Y. V., Imataka H., O'Connor-McCourt M., Sonenberg N. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol Cell Biol. 2001 Aug;21(15):5200–5213. doi: 10.1128/MCB.21.15.5200-5213.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kühn U., Pieler T. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J Mol Biol. 1996 Feb 16;256(1):20–30. doi: 10.1006/jmbi.1996.0065. [DOI] [PubMed] [Google Scholar]
  27. Mangus D. A., Amrani N., Jacobson A. Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol Cell Biol. 1998 Dec;18(12):7383–7396. doi: 10.1128/mcb.18.12.7383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Marhoul J. F., Adams T. H. Aspergillus fabM encodes an essential product that is related to poly(A)-binding proteins and activates development when overexpressed. Genetics. 1996 Dec;144(4):1463–1470. doi: 10.1093/genetics/144.4.1463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nietfeld W., Mentzel H., Pieler T. The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J. 1990 Nov;9(11):3699–3705. doi: 10.1002/j.1460-2075.1990.tb07582.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Palanivelu R., Belostotsky D. A., Meagher R. B. Arabidopsis thaliana poly (A) binding protein 2 (PAB2) functions in yeast translational and mRNA decay processes. Plant J. 2000 May;22(3):187–198. doi: 10.1046/j.1365-313x.2000.00721.x. [DOI] [PubMed] [Google Scholar]
  31. Palanivelu R., Belostotsky D. A., Meagher R. B. Conserved expression of Arabidopsis thaliana poly (A) binding protein 2 (PAB2) in distinct vegetative and reproductive tissues. Plant J. 2000 May;22(3):199–210. doi: 10.1046/j.1365-313x.2000.00720.x. [DOI] [PubMed] [Google Scholar]
  32. Pickett F. B., Meeks-Wagner D. R. Seeing double: appreciating genetic redundancy. Plant Cell. 1995 Sep;7(9):1347–1356. doi: 10.1105/tpc.7.9.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Proweller A., Butler J. S. Ribosomal association of poly(A)-binding protein in poly(A)-deficient Saccharomyces cerevisiae. J Biol Chem. 1996 May 3;271(18):10859–10865. doi: 10.1074/jbc.271.18.10859. [DOI] [PubMed] [Google Scholar]
  34. Roy Guylaine, De Crescenzo Gregory, Khaleghpour Kianoush, Kahvejian Avak, O'Connor-McCourt Maureen, Sonenberg Nahum. Paip1 interacts with poly(A) binding protein through two independent binding motifs. Mol Cell Biol. 2002 Jun;22(11):3769–3782. doi: 10.1128/MCB.22.11.3769-3782.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sachs A. B., Bond M. W., Kornberg R. D. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell. 1986 Jun 20;45(6):827–835. doi: 10.1016/0092-8674(86)90557-x. [DOI] [PubMed] [Google Scholar]
  36. Sachs A. B., Davis R. W., Kornberg R. D. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol Cell Biol. 1987 Sep;7(9):3268–3276. doi: 10.1128/mcb.7.9.3268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sigrist S. J., Thiel P. R., Reiff D. F., Lachance P. E., Lasko P., Schuster C. M. Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature. 2000 Jun 29;405(6790):1062–1065. doi: 10.1038/35016598. [DOI] [PubMed] [Google Scholar]
  38. Tarun S. Z., Jr, Sachs A. B. A common function for mRNA 5' and 3' ends in translation initiation in yeast. Genes Dev. 1995 Dec 1;9(23):2997–3007. doi: 10.1101/gad.9.23.2997. [DOI] [PubMed] [Google Scholar]
  39. Tarun S. Z., Jr, Wells S. E., Deardorff J. A., Sachs A. B. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9046–9051. doi: 10.1073/pnas.94.17.9046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wakiyama M., Imataka H., Sonenberg N. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr Biol. 2000 Sep 21;10(18):1147–1150. doi: 10.1016/s0960-9822(00)00701-6. [DOI] [PubMed] [Google Scholar]
  41. Wells S. E., Hillner P. E., Vale R. D., Sachs A. B. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell. 1998 Jul;2(1):135–140. doi: 10.1016/s1097-2765(00)80122-7. [DOI] [PubMed] [Google Scholar]
  42. Wilusz C. J., Gao M., Jones C. L., Wilusz J., Peltz S. W. Poly(A)-binding proteins regulate both mRNA deadenylation and decapping in yeast cytoplasmic extracts. RNA. 2001 Oct;7(10):1416–1424. [PMC free article] [PubMed] [Google Scholar]
  43. Wolfe K. H., Gouy M., Yang Y. W., Sharp P. M., Li W. H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6201–6205. doi: 10.1073/pnas.86.16.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yohn C. B., Cohen A., Danon A., Mayfield S. P. A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2238–2243. doi: 10.1073/pnas.95.5.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. de Melo Neto O. P., Standart N., Martins de Sa C. Autoregulation of poly(A)-binding protein synthesis in vitro. Nucleic Acids Res. 1995 Jun 25;23(12):2198–2205. doi: 10.1093/nar/23.12.2198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. de Souza S. J., Long M., Klein R. J., Roy S., Lin S., Gilbert W. Toward a resolution of the introns early/late debate: only phase zero introns are correlated with the structure of ancient proteins. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5094–5099. doi: 10.1073/pnas.95.9.5094. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES