PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway

详细信息    查看全文

• 作者：Lorena A Siena (1)
  Juan Pablo A Ortiz (1) (2)
  Olivier Leblanc (3)
  Silvina Pessino (1)
  
  1. Laboratorio de Biolog铆a Molecular ; Facultad de Ciencias Agrarias ; Universidad Nacional de Rosario ; Parque Villarino ; (S2125ZAA) Zavalla ; Santa Fe ; Argentina
  2. Instituto de Bot谩nica del Nordeste -IBONE- (UNNE-CONICET) ; Facultad de Ciencias Agrarias ; Universidad Nacional del Nordeste ; Sargento Cabral 2131 ; 3400 ; Corrientes ; Argentina
  3. Institut de Recherche pour le D茅veloppement ; ERL 5300 IRD/CNRS ; UMR 232 IRD/Universit茅 de Montpellier 2 ; 911 Avenue Agropolis ; Montpellier ; France
  
• 关键词：Apomixis ; Apospory ; Gene expression ; PIMT ; RNA processing ; Trimethylguanosine synthase
• 刊名：BMC Plant Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：2,055 KB
• 参考文献：1. Nogler, GA Gametophytic Apomixis. In: Johri, BM eds. (1984) Embryology of Angiosperms. Springer, Berlin, pp. 475-518 CrossRef
  2. Crane, CF Classification of Apomictic Mechanisms. In: Savidan, Y, Carman, JG, Dresselhaus, T eds. (2001) The Flowering of Apomixis: From Mechanisms to Genetic Engineering. CIMMYT, IRD, European Commission DG VI (FAIR), Mexico City, pp. 24-43
  3. Ozias-Akins, P (2006) Apomixis: developmental characteristics and genetics. Crit Rev Plant Sci 25: pp. 199-214 CrossRef
  4. Linnaeus, C (1758) Systema Naturae. Holmi忙, Impensis direct. Laurentii Salvii (Salvius publ.), Stockholm
  5. Ortiz, JPA, Quarin, CL, Pessino, SC, Acu帽a, C, Mart铆nez, EJ, Espinoza, F, Hojsgaard, DH, Sartor, ME, Caceres, ME, Pupilli, F (2013) Harnessing apomictic reproduction in grasses: what we have learned from Paspalum. Ann Bot London 112: pp. 767-787 CrossRef
  6. Quarin, CL (1992) The nature of apomixis and its origin in Panicoid grasses. Apomixis Newsletter 5: pp. 8-15
  7. Mart铆nez, EJ, Urbani, MH, Quarin, CL, Ortiz, JPA (2001) Inheritance of apospory in bahiagrass, Paspalum notatum. Hereditas 135: pp. 19-25 CrossRef
  8. Quarin, CL, Espinoza, F, Mart铆nez, EJ, Pessino, SC, Bovo, OA (2001) A rise of ploidy level induces the expression of apomixis in Paspalum notatum. Sex Plant Reprod 13: pp. 243-249 CrossRef
  9. Quarin, CL, Urbani, MH, Blount, AR, Martinez, EJ, Hack, CM, Burton, GW, Quesenberry, KH (2003) Registration of Q4188 and Q4205, sexual tetraploid germplasm lines of Bahiagrass. Crop Sci 43: pp. 745-746 CrossRef
  10. Mart铆nez, EJ, Hopp, HE, Stein, J, Ortiz, JPA, Quarin, CL (2003) Genetic characterization of apospory in tetraploid Paspalum notatum based on the identification of linked molecular markers. Mol Breed 12: pp. 312-327 CrossRef
  11. Pupilli, F, Mart铆nez, EJ, Busti, A, Calderini, O, Quarin, CL, Arcioni, S (2004) Comparative mapping reveals partial conservation of synteny at the apomixis locus in Paspalum spp. Mol Genet Genom 270: pp. 539-548 CrossRef
  12. Stein, J, Quarin, CL, Mart铆nez, EJ, Pessino, SC, Ortiz, JPA (2004) Tetraploid races of Paspalum notatum show polysomic inheritance and preferential chromosome pairing around the apospory-controlling locus. Theor Appl Genet 109: pp. 186-191 CrossRef
  13. Stein, J, Pessino, SC, Mart铆nez, EJ, Rodr铆guez, MP, Siena, LA, Quarin, CL, Ortiz, JPA (2007) A genetic map of tetraploid Paspalum notatum Fl眉gge (bahiagrass) based on single-dose molecular markers. Mol Breed 20: pp. 153-166 CrossRef
  14. Podio, M, Rodriguez, MP, Felitti, S, Stein, J, Martinez, E, Siena, LA, Quarin, CL, Pessino, SC, Ortiz, JPA (2012) Sequence characterization, in silico mapping and cytosine methylation analysis of markers linked to apospory in Paspalum notatum. Genet Mol Biol 35: pp. 827-837 CrossRef
  15. Podio, M, Siena, LA, Hojsgaard, D, Stein, J, Quarin, CL, Ortiz, JPA (2012) Evaluation of meiotic abnormalities and pollen viability in aposporous and sexual tetraploid Paspalum notatum (Poaceae). Plant System Evol 298: pp. 1625-1633 CrossRef
  16. Jia, G, Fu, Y, He, C (2012) Reversible RNA adenosine methylation in biological regulation. Trends Genet 29: pp. 108-115 CrossRef
  17. Zhong, S, Li, H, Bodi, Z, Button, J, Vespa, L, Herzog, M, Fray, RG (2008) MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell 20: pp. 1278-1288 CrossRef
  18. Burd, CG, Dreyfuss, G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265: pp. 615-621 CrossRef
  19. Lorkovic, ZJ, Barta, A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNAbinding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30: pp. 623-635 CrossRef
  20. Buckner, B, Swaggart, KA, Wong, CC, Smith, HA, Aurnad, KM, Scanlon, MJ, Schnable, PS, Janic-Buckner, D (2008) Expression and nucleotide diversity of the maize RIK gene. J Hered 99: pp. 407-416 CrossRef
  21. Rodrigues, JC, Cabral, GB, Dusi, DMA, Mello, LV, Rinden, D, Carneiro, VTC (2003) Identification of differentially expressed cDNA sequences in ovaries of sexual and apomictic plants of Brachiaria brizantha. Plant Mol Biol 53: pp. 745-757 CrossRef
  22. Albertini, E, Marconi, G, Barcaccia, G, Raggi, L, Falcinelli, M (2004) Isolation of candidate genes for apomixis in Poa pratensis. Plant Mol Biol 56: pp. 879-894 CrossRef
  23. Laspina, NV, Vega, T, Martelotto, L, Stein, J, Podio, M, Ortiz, JP, Echenique, V, Quarin, C, Pessino, SC (2008) Gene expression analysis at the onset of aposporous apomixis in immature inflorecences of Paspalum notatum. Plant Mol Biol 67: pp. 615-628 CrossRef
  24. Yamada-Akiyama, H, Akiyama, Y, Ebina, M, Xu, Q, Tsuruta, S, Yazaki, J, Kishimoto, N, Kikuchi, S, Takahara, M, Takamizo, T, Sugita, S, Nakagawa, H (2009) Analysis of expressed sequence tags in apomictic Guinea grass (Panicum maximum). J Plant Physiol 166: pp. 750-761 CrossRef
  25. Sharbel, TF, Voigt, ML, Corral, JM, Galla, G, Kumlehn, J, Klukas, C, Schreiber, F, Vogel, H, Rotter, B (2010) Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. Plant Cell 22: pp. 655-671 CrossRef
  26. Polegri, L, Calderini, O, Arcioni, S, Pupilli, F (2010) Specific expression of apomixis-linked alleles revealed by comparative transcriptomic analysis of sexual and apomictic Paspalum simplex Morong flowers. J Exp Bot 61: pp. 1869-1883 CrossRef
  27. Okada, T, Hu, Y, Tucker, MR, Taylor, JM, Johnson, SD, Spriggs, A, Tsuchiya, T, Oelkers, K, Rodrigues, JCM, Koltunow, AMG (2013) Enlarging cells initiating apomixis in Hieracium praealtum transition to an embryo sac program prior to entering mitosis. Plant Physiol 163: pp. 216-231 CrossRef
  28. Pessino, SC, Espinoza, F, Mart铆nez, EJ, Ortiz, JPA, Valle, EM, Quarin, CL (2001) Isolation of cDNA clones differentially expressed in flowers of apomictic and sexual Paspalum notatum. Hereditas 134: pp. 35-42 CrossRef
  29. Colau, G, Thiry, M, Leduc, V, Bordonn茅, R, Lafontaine, DLJ (2004) The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol 24: pp. 7976-7986 CrossRef
  30. Franke, J, Gehlen, J, Ehrenhofer-Murray, AE (2008) Hypermethylation of yeast telomerase RNA by the snRNA and snoRNA methyltransferase Tgs1. J Cell Sci 121: pp. 3553-3560 CrossRef
  31. Qiu, ZR, Shuman, S, Schwer, B (2011) An essential role for trimethylguanosine RNA caps in Saccharomyces cerevisiae meiosis and their requirement for splicing of SAE3 and PCH2 meiotic pre-mRNAs. Nucleic Acids Res 39: pp. 5633-5646 CrossRef
  32. Espinoza, F, Daurelio, LD, Pessino, SC, Quarin, CL, Valle, EM (2006) Genetic characterization of Paspalum notatum accessions by AFLP markers. Plant Syst Evol 258: pp. 147-159 CrossRef
  33. Viswakarma, N, Jia, Y, Bai, L, Vluggens, A, Borensztajn, J, Xu, J, Reddy, JK (2010) Coactivators in PPAR-regulated gene expression. PPAR Res.
  34. Zhu, Y, Qi, C, Cao, WQ, Yeldandi, AV, Rao, MS, Reddy, JK (2001) Cloning and characterization of PIMT, a protein with a methyltransferase domain, which interacts with and enhances nuclear receptor coactivator PRIP function. Proc Natl Acad Sci U S A 98: pp. 10380-10385 CrossRef
  35. Mouaikel, J, Verheggen, C, Bertrand, E, Tazi, J, Bordonn茅, R (2002) Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol Cell 9: pp. 891-901 CrossRef
  36. Misra, P, Qi, C, Yu, S, Shah, SH, Cao, WQ, Sambasiva Rao, M, Thimmapaya, B, Zhu, Y, Reddy, JK (2002) Interaction of PIMT with transcriptional coactivators CBP, p300, and PBP differential role in transcriptional regulation. J Biol Chem 277: pp. 20011-20019 CrossRef
  37. Kornberg, RD (2007) The molecular basis of eukaryotic transcription. Proc Natl Acad Sci U S A 104: pp. 12955-12961 CrossRef
  38. Kapadia, B, Viswakarma, N, Parsa, KVL, Kain, V, Behera, S, Suraj, SK, Babu, PP, Kar, A, Panda, S, Zhu, Y, Jia, Y, Thimmapaya, B, Reddy, JK, Misra, P (2013) ERK2-mediated phosphorylation of transcriptional coactivator binding protein PIMT/NcoA6IP at Ser298 augments hepatic gluconeogenesis. PLoS One 8: pp. e83787 CrossRef
  39. En眉nl眉, I, P谩pai, G, Cserp谩n, I, Udvardy, A, Jeang, K, Borors, I (2003) Different isoforms of PRIP-interacting protein with methyltransferase domain/trimethylguanosine synthase localizes to the cytoplasm and nucleus. Biochem Biophys Res Commun 309: pp. 44-51 CrossRef
  40. Jia, Y, Viswakarma, N, Crawford, SE, Sarkar, J, Sambasiva Rao, M, Karpus, WJ, Kanwar, YS, Zhu, YJ, Reddy, JK (2012) Early embryonic lethality of mice with disrupted transcription cofactor PIMT/NCOA6IP/Tgs1 gene. Mech Dev 129: pp. 193-207 CrossRef
  41. Komonyi, O, P谩pai, G, En眉nl眉, I, Muratoglu, S, Pankotai, T, Kopitova, D, Mar贸y, P, Udvardy, A, Boros, I (2005) DTL, the Drosophila homolog of PIMT/Tgs1 nuclear receptor coactivator-interacting protein/RNA methyltransferase, has an essential role in development. J Biol Chem 280: pp. 12397-12404 CrossRef
  42. Grimanelli, D (2012) Epigenetic regulation of reproductive development and the emergence of apomixis in angiosperms. Curr Opin Plant Biol 15: pp. 57-62 CrossRef
  43. Garcia-Aguilar, M, Michaud, C, Leblanc, O, Grimanelli, D (2010) Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22: pp. 3249-3267 CrossRef
  44. Singh, M, Goel, S, Meeley, RB, Dantec, C, Parrinello, H, Michaud, C, Leblanc, O, Grimanelli, D (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23: pp. 443-458 CrossRef
  45. Mancini, M, Woitovich, N, Permingeat, H, Podio, M, Siena, LA, Ortiz, JPA, Pessino, SC, Felitti, SA (2014) Development of a modified transformation platform for apomixis candidate genes research in Paspalum notatum (bahiagrass). In Vitro Cell Dev Biol Plant.
  46. Ortiz, JP, Pessino, SC, Leblanc, O, Hayward, MD, Quarin, CL (1997) Genetic fingerprint for determining the mode of reproduction in Paspalum notatum, a subtropical apomictic forage grass. Theor Appl Genet 95: pp. 850-856 CrossRef
  47. Chenchik, A, Diachenko, L, Moqadam, F, Tarabykin, V, Lukyanov, S, Siebert, PD (1996) Full-length cDNA cloning and determination of mRNA 5鈥?and 3鈥?ends by amplification of adaptor-ligated cDNA. Biotech 21: pp. 526-534
  48. Untergasser, A, Nijveen, H, Rao, X, Bisseling, T, Geurts, R, Leunissen, JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: pp. 71-74 CrossRef
  49. Podio, M, Felitti, SA, Siena, LA, Delgado, L, Mancini, M, Seijo, G, Gonz谩lez, AM, Pessino, SC, Ortiz, JPA (2014) Characterization and expression analysis of SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes in sexual and apomictic Paspalum notatum. Plant Mol Biol 84: pp. 479-495 CrossRef
  50. Felitti, SA, Seijo, JG, Gonz谩lez, AM, Podio, M, Laspina, NV, Siena, L, Ortiz, JPA, Pessino, SC (2011) Expression of lorelei-like genes in aposporous and sexual Paspalum notatum plants. Plant Mol Biol 77: pp. 337-354 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background In flowering plants, apomixis (asexual reproduction via seeds) is widely believed to result from failure of key regulators of the sexual female reproductive pathway. In the past few years, both differential display and RNA-seq comparative approaches involving reproductive organs of sexual plants and their apomictic counterparts have yielded extensive lists of candidate genes. Nevertheless, only a limited number of these genes have been functionally characterized, with few clues consequently available for understanding the molecular control of apomixis. We have previously identified several cDNA fragments with high similarity to genes involved in RNA biology and with differential amplification between sexual and apomictic Paspalum notatum plants. Here, we report the characterization of one of these candidates, namely, N69 encoding a protein of the S-adenosyl-L-methionine-dependent methyltransferases superfamily. The purpose of this work was to extend the N69 cDNA sequence and to characterize its expression at different developmental stages in both sexual and apomictic individuals. Results Molecular characterization of the N69 cDNA revealed homology with genes encoding proteins similar to yeast and mammalian trimethylguanosine synthase/PRIP-interacting proteins. These proteins play a dual role as ERK2-controlled transcriptional coactivators and mediators of sn(o)RNA and telomerase RNA cap trimethylation, and participate in mammals and yeast development. The N69-extended sequence was consequently renamed PnTgs1-like. Expression of PnTgs1-like during reproductive development was significantly higher in floral organs of sexual genotypes compared with apomicts. This difference was not detected in vegetative tissues. In addition, expression levels in reproductive tissues of several genotypes were negatively correlated with facultative apomixis rates. Moreover, in situ hybridization observations revealed that PnTgs1-like expression is relatively higher in ovules of sexual plants throughout development, from premeiosis to maturity. Tissues where differential expression is detected include nucellar cells, the site of aposporous initials differentiation in apomictic genotypes. Conclusions Our results indicate that PnTgs1-like (formerly N69) encodes a trimethylguanosine synthase-like protein whose function in mammals and yeast is critical for development, including reproduction. Our findings also suggest a pivotal role for this candidate gene in nucellar cell fate, as its diminished expression is correlated with initiation of the apomictic pathway in plants.