JOURNAL BROWSE
Search
Advanced SearchSearch Tips
Emerging Roles of RNA-Binding Proteins in Plant Growth, Development, and Stress Responses
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
  • Journal title : Molecules and Cells
  • Volume 39, Issue 3,  2016, pp.179-185
  • Publisher : Korea Society for Molecular and Cellular Biology
  • DOI : 10.14348/molcells.2016.2359
 Title & Authors
Emerging Roles of RNA-Binding Proteins in Plant Growth, Development, and Stress Responses
Lee, Kwanuk; Kang, Hunseung;
  PDF(new window)
 Abstract
Posttranscriptional regulation of RNA metabolism, including RNA processing, intron splicing, editing, RNA export, and decay, is increasingly regarded as an essential step for fine-tuning the regulation of gene expression in eukaryotes. RNA-binding proteins (RBPs) are central regulatory factors controlling posttranscriptional RNA metabolism during plant growth, development, and stress responses. Although functional roles of diverse RBPs in living organisms have been determined during the last decades, our understanding of the functional roles of RBPs in plants is lagging far behind our understanding of those in other organisms, including animals, bacteria, and viruses. However, recent functional analysis of multiple RBP family members involved in plant RNA metabolism and elucidation of the mechanistic roles of RBPs shed light on the cellular roles of diverse RBPs in growth, development, and stress responses of plants. In this review, we will discuss recent studies demonstrating the emerging roles of multiple RBP family members that play essential roles in RNA metabolism during plant growth, development, and stress responses.
 Keywords
plant development;RNA-binding protein;RNA chaperone;RNA metabolism;stress response;
 Language
English
 Cited by
1.
Abiotic stresses affect differently the intron splicing and expression of chloroplast genes in coffee plants ( Coffea arabica ) and rice ( Oryza sativa ), Journal of Plant Physiology, 2016, 201, 85  crossref(new windwow)
2.
Three zinc-finger RNA-binding proteins in cabbage (Brassica rapa) play diverse roles in seed germination and plant growth under normal and abiotic stress conditions, Physiologia Plantarum, 2017, 159, 1, 93  crossref(new windwow)
3.
RNA structure, binding, and coordination in Arabidopsis, Wiley Interdisciplinary Reviews: RNA, 2017, 8, 5, e1426  crossref(new windwow)
4.
Plant RNA Interactome Capture: Revealing the Plant RBPome, Trends in Plant Science, 2017, 22, 6, 449  crossref(new windwow)
5.
Chloroplast- or Mitochondria-Targeted DEAD-Box RNA Helicases Play Essential Roles in Organellar RNA Metabolism and Abiotic Stress Responses, Frontiers in Plant Science, 2017, 8  crossref(new windwow)
6.
Comparative Transcriptome Analysis Reveals Adaptive Evolution of Notopterygium incisum and Notopterygium franchetii, Two High-Alpine Herbal Species Endemic to China, Molecules, 2017, 22, 7, 1158  crossref(new windwow)
 References
1.
Alba, M.M., and Pages, M. (1998). Plant proteins containing the RNA-recognition motif. Trends Plant Sci. 3, 15-21.

2.
Aliprandi, P., Sizun, C., Perez, J., Mareuil, F., Caputo, S., Leroy, J.- L., Odaert, B., Laalami, S., Uzan, M., and Bontems, F. (2008). S1 ribosomal protein functions in translation initiation and ribonuclease RegB activation are mediated by similar RNAprotein interactions: an NMR and SAXS analysis. J. Biol. Chem. 283, 13289-13301. crossref(new window)

3.
Arthur, D.C., Ghetu, A.F., Gubbins, M.J., Edwards, R.A., Frost, L.S., and Glover, J.M. (2003). FinO is an RNA chaperone that facilitates sense-antisense RNA interactions. EMBO J. 22, 6346-6355. crossref(new window)

4.
Asakura, Y., and Barkan, A. (2006). Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol. 142, 1656-1663. crossref(new window)

5.
Asakura, Y., and Barkan, A. (2007). A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts. Plant Cell 19, 3864-3875. crossref(new window)

6.
Asakura, Y., Bayraktar, O.A., and Barkan, A. (2008). Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14, 2319-2332. crossref(new window)

7.
Asakura, Y., Galarneau, E., Watkins, K.P., Barkan, A., and van Wijk, K.J. (2012). Chloroplast RH3 DEAD Box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome riogenesis. Plant Physiol. 159, 961-974. crossref(new window)

8.
Barkan, A., and Small, I. (2014). Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65, 415-442. crossref(new window)

9.
Barkan, A., Klipcan, L., Ostersetzer, O., Kawamura, T., Asakura, Y., and Watkins, K.P. (2007). The CRM domain: an RNA binding module derived from an ancient ribosome-associated protein. RNA 13, 55-64.

10.
Brown, G.G., Colas des Francs-Small, C., and Ostersetzer-Biran, O. (2014). Group II intron splicing factors in plant mitochondria. Front. Plant Sci. 5, 35.

11.
Bycroft, M., Hubbard, T.J., Proctor, M., Freund, S.M., and Murzin, A.G. (1997). The solution structure of the S1 RNA binding domain: A member of an ancient nucleic acid–binding fold. Cell 88, 235-242. crossref(new window)

12.
del Campo, E.M. (2009). Post-transcriptional control of chloroplast gene expression. Gene Regul. Syst. Biol. 3, 31.

13.
Castiglioni, P., Warner, D., Bensen, R.J., Anstrom, D.C., Harrison, J., Stoecker, M., Abad, M., Kumar, G., Salvador, S., D'Ordine, R., et al. (2008). Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol. 147, 446-455. crossref(new window)

14.
Chaikam, V., and Karlson, D. (2008). Functional characterization of two cold shock domain proteins from Oryza sativa. Plant Cell Environ. 31, 995-1006. crossref(new window)

15.
Chaulk, S., Smith Frieday, M.N., Arthur, D.C., Culham, D.E., Edwards, R.A., Soo, P., Frost, L.S., Keates, R.A., Glover, J.M., and Wood, J.M. (2011). ProQ is an RNA chaperone that controls ProP levels in Escherichia coli. Biochemistry 50, 3095-3106. crossref(new window)

16.
Chambers, J.R., and Bender, K.S. (2011). The RNA chaperone Hfq is important for growth and stress tolerance in Francisella novicida. PLoS One 6, e19797. crossref(new window)

17.
Chateigner-Boutin, A.L., des Francs-Small, C.C., Delannoy, E., Kahlau, S., Tanz, S.K., de Longevialle, A.F., Fujii, S., and Small, I. (2011). OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1. Plant J. 65, 532-542. crossref(new window)

18.
Chekanova, J.A., Dutko, J.A., Mian, I.S., and Belostotsky, D.A. (2002). Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′$\rightarrow$ 5′ exonuclease containing S1 and KH RNAbinding domains. Nucleic Acids Res. 30, 695-700. crossref(new window)

19.
Chi, W., He, B., Mao, J., Li, Q., Ma, J., Ji, D., Zou, M., and Zhang, L. (2012). The function of RH22, a DEAD RNA helicase, in the biogenesis of the 50S ribosomal subunits of Arabidopsis chloroplasts. Plant Physiol. 158, 693-707. crossref(new window)

20.
Choi, M.J., Park, Y.R., Park, S.J., and Kang, H. (2015). Stressresponsive expression patterns and functional characterization of cold shock domain proteins in cabbage (Brassica rapa) under abiotic stress conditions. Plant Physiol. Biochem. 96, 132-140. crossref(new window)

21.
Cottage, A., Mott, E.K., Kempster, J.A., and Gray, J.C. (2010). The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J. Exp. Bot. 61, 3773-3786. crossref(new window)

22.
Delvillani, F., Papiani, G., Deho, G., and Briani, F. (2011). S1 ribosomal protein and the interplay between translation and mRNA decay. Nucleic Acids Res. 39, 7702-7715. crossref(new window)

23.
des Francs-Small, C.C., de Longevialle, A.F., Li, Y., Lowe, E., Tanz, S.K., Smith, C., Bevan, M.W., and Small, I. (2014). The pentatricopeptide repeat proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 are involved in the splicing of the multipartite nad5 transcript encoding a subunit of mitochondrial Complex I. Plant Physiol. 165, 1409-1416. crossref(new window)

24.
Filipovska, A., and Rackham, O. (2012). Modular recognition of nucleic acids by PUF, TALE and PPR proteins. Mol. Biosyst. 8, 699-708. crossref(new window)

25.
Floris, M., Mahgoub, H., Lanet, E., Robaglia, C., and Menand, B. (2009). Post-transcriptional Regulation of Gene Expression in Plants during Abiotic Stress. Int. J. Mol. Sci. 10, 3168-3185. crossref(new window)

26.
Fusaro, A.F., Bocca, S.N., Ramos, R.L.B., Barroco, R.M., Magioli, C., Jorge, V.C., Coutinho, T.C., Rangel-Lima, C.M., De Rycke, R., and Inze, D. (2007). AtGRP2, a cold-induced nucleocytoplasmic RNA-binding protein, has a role in flower and seed development. Planta 225, 1339-1351. crossref(new window)

27.
Gong, Z., Lee, H., Xiong, L., Jagendorf, A., Stevenson, B., and Zhu, J.-K. (2002). RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc. Natl. Acad. Sci. USA 99, 11507-11512. crossref(new window)

28.
Gong, Z., Dong, C.-H., Lee, H., Zhu, J., Xiong, L., Gong, D., Stevenson, B., and Zhu, J.-K. (2005). A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17, 256-267. crossref(new window)

29.
Gong, X.D., Su, Q.Q., Lin, D.Z., Jiang, Q., Xu, J.L., Zhang, J.H., Teng, S., and Dong, Y.J. (2014). The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress. J. Integr. Plant Biol. 56, 400-410. crossref(new window)

30.
Graumann, P.L., and Marahiel, M.A. (1998). A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23, 286-290. crossref(new window)

31.
Gu, L., Xu, T., Lee, K., Lee, K.H., and Kang, H. (2014). A chloroplast-localized DEAD-box RNA helicaseAtRH3 is essential for intron splicing and plays an important role in the growth and stress response in Arabidopsis thaliana. Plant Physiol. Biochem. 82, 309-318. crossref(new window)

32.
Gu, L., Jung, H.J., Kim, B.M., Xu, T., Lee, K., Kim, Y.O., and Kang, H. (2015). A chloroplast-localized S1 domain-containing protein SRRP1 plays a role in Arabidopsis seedling growth in the presence of ABA. J. Plant. Physiol. 189, 34-41. crossref(new window)

33.
Guan, Q., Wu, J., Zhang, Y., Jiang, C., Liu, R., Chai, C., and Zhu, J. (2013). A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25, 342-356. crossref(new window)

34.
Hammani, K., and Giege, P. (2014). RNA metabolism in plant mitochondria. Trends Plant Sci. 19, 380-389. crossref(new window)

35.
Han, J.H., Lee, K., Lee, K.H., Jung, S., Jeon, Y., Pai, H.S., and Kang, H. (2015). A nuclear-encoded chloroplast-targeted S1 RNA-binding domain protein affects chloroplast rRNA processing and is crucial for the normal growth of Arabidopsis thaliana. Plant J. 83, 277-289. crossref(new window)

36.
Herschlag, D. (1995). RNA chaperones and the RNA folding problem. J. Biol. Chem. 270, 20871-20874. crossref(new window)

37.
Huang, H.-R., Rowe, C.E., Mohr, S., Jiang, Y., Lambowitz, A.M., and Perlman, P.S. (2005). The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc. Natl. Acad. Sci. USA 102, 163-168. crossref(new window)

38.
Huang, C.-K., Huang, L.-F., Huang, J.-J., Wu, S.-J., Yeh, C.-H., and Lu, C.-A. (2010). A DEAD-box protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol. 51, 694-706. crossref(new window)

39.
Ivanyi-Nagy, R., Davidovic, L., Khandjian, E., and Darlix, J.-L. (2005). Disordered RNA chaperone proteins: from functions to disease. Cell. Mol. Life Sci. 62, 1409-1417. crossref(new window)

40.
Jankowsky, E. (2011). RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36, 19-29. crossref(new window)

41.
Jeon, Y., Jung, H.J., Kang, H., Park, Y.I., Lee, S.H., and Pai, H.S. (2012). S1 domain-containing STF modulates plastid transcription and chloroplast biogenesis in Nicotiana benthamiana. New Phytol. 193, 349-363. crossref(new window)

42.
Jiang, S.-C., Mei, C., Liang, S., Yu, Y.-T., Lu, K., Wu, Z., Wang, X.- F., and Zhang, D.-P. (2015). Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses. Plant Mol. Biol. 88, 369-385. crossref(new window)

43.
Jung, H.J., and Kang, H. (2014). The Arabidopsis U11/U12-65K is an indispensable component of minor spliceosome and plays a crucial role in U12 intron splicing and plant development. Plant J. 78, 799-810. crossref(new window)

44.
Jung, H.J., Park, S.J., and Kang, H.S., (2013). Regulation of RNA metabolism in plant development and stress responses. J. Plant Biol. 56, 123-129. crossref(new window)

45.
Kanai, M., Hayashi, M., Kondo, M., and Nishimura, M. (2013). The plastidic DEAD-box RNA helicase 22, HS3, is essential for plastid functions both in seed development and in seedling growth. Plant Cell Physiol. 54, 1431-1440. crossref(new window)

46.
Kang, H., Park, S.J., and Kwak, K.J. (2013). Plant RNA chaperones in stress response. Trends Plant Sci. 18, 100-106. crossref(new window)

47.
Kant, P., Kant, S., Gordon, M., Shaked, R., and Barak, S. (2007). STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol. 145, 814-830. crossref(new window)

48.
Karlson, D., and Imai, R. (2003). Conservation of the cold shock domain protein family in plants. Plant Physiol. 131, 12-15. crossref(new window)

49.
Karlson, D., Nakaminami, K., Toyomasu, T., and Imai, R. (2002). A cold-regulated nucleic acid-binding protein of winter wheat shares a domain with bacterial cold shock proteins. J. Biol. Chem. 277, 35248-35256. crossref(new window)

50.
Keren, I., Klipcan, L., Bezawork-Geleta, A., Kolton, M., Shaya, F., and Ostersetzer-Biran, O. (2008). Characterization of the molecular basis of group II intron RNA recognition by CRS1- CRM domains. J. Biol. Chem. 283, 23333-23342. crossref(new window)

51.
Kim, Y.O., and Kang, H. (2006). The role of a zinc finger-containing glycine-rich RNA-binding protein during the cold adaptation process in Arabidopsis thaliana. Plant Cell Physiol. 47, 793-798. crossref(new window)

52.
Kim, Y.O., Kim, J.S., and Kang, H. (2005). Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J. 42, 890-900. crossref(new window)

53.
Kim, J.S., Park, S.J., Kwak, K.J., Kim, Y.O., Kim, J.Y., Song, J., Jang, B., Jung, C.H., and Kang, H. (2007a). Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res. 35, 506-516.

54.
Kim, J.Y., Park, S.J., Jang, B., Jung, C.H., Ahn, S.J., Goh, C.H., Cho, K., Han, O., and Kang, H. (2007b). Functional characterization of a glycine‐rich RNA‐binding protein 2 in Arabidopsis thaliana under abiotic stress conditions. Plant J. 50, 439-451. crossref(new window)

55.
Kim, J.S., Jung, H.J., Lee, H.J., Kim, K., Goh, C.H., Woo, Y., Oh, S.H., Han, Y.S., and Kang, H. (2008a). Glycine‐rich RNA‐binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J. 55, 455-466. crossref(new window)

56.
Kim, J.S., Kim, K.A., Oh, T.R., Park, C.M., and Kang, H. (2008b). Functional Characterization of DEAD-Box RNA Helicases in Arabidopsis thaliana under Abiotic Stress Conditions. Plant Cell Physiol. 49, 1563-1571. crossref(new window)

57.
Kim, M.-H., Sasaki, K. and Imai, R. (2009). Cold shock domain protein 3 regulates freezing tolerance in Arabidopsis thaliana. J. Biol. Chem. 284, 23454-23460. crossref(new window)

58.
Kim, J.Y., Kim, W.Y., Kwak, K.J., Oh, S.H., Han, Y.S., and Kang, H. (2010a). Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J. Exp. Bot. 61, 2317-2325. crossref(new window)

59.
Kim, J.Y., Kim, W.Y., Kwak, K.J., Oh, S.H., Han, Y.S., and Kang, H. (2010b). Zinc finger-containing glycine-rich RNA-binding protein in Oryza sativa has an RNA chaperone activity under cold stress conditions. Plant Cell Environ. 33, 759-768.

60.
Kim, W.Y., Jung, H.J., Kwak, K.J., Kim, M.K., Oh, S.H., Han, Y.S., and Kang, H. (2010c). The Arabidopsis U12-type spliceosomal protein U11/U12-31K is involved in U12 intron splicing via RNA chaperone activity and affects plant development. Plant Cell 22, 3951-3962. crossref(new window)

61.
Kohler, D., Schmidt-Gattung, S., and Binder, S. (2010). The DEADbox protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana. Plant. Mol. Biol. 72, 459-467. crossref(new window)

62.
Koprivova, A., des Francs-Small, C.C., Calder, G., Mugford, S.T., Tanz, S., Lee, B.R., Zechmann, B., Small, I., and Kopriva, S. (2010). Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J. Biol. Chem. 285, 32192-32199. crossref(new window)

63.
Kroeger, T.S., Watkins, K.P., Friso, G., van Wijk, K.J., and Barkan, A. (2009). A plant-specific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc. Natl. Acad. Sci. USA 106, 4537-4542. crossref(new window)

64.
Kwak, K.J., Kim, Y.O., and Kang, H. (2005). Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 56, 3007-3016. crossref(new window)

65.
Kwak, K.J., Jung, H.J., Lee, K.H., Kim, Y.S., Kim, W.Y., Ahn, S.J., and Kang, H. (2012). The minor spliceosomal protein U11/U12- 31K is an RNA chaperone crucial for U12 intron splicing and the development of dicot and monocot plants. PLoS One 7, e43707. crossref(new window)

66.
Laluk, K., AbuQamar, S., and Mengiste, T. (2011). The Arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Physiol. 156, 2053-2068. crossref(new window)

67.
Lee, K., Lee, H.J., Kim, D.H., Jeon, Y., Pai, H.S., and Kang, H. (2014). A nuclear-encoded chloroplast protein harboring a single CRM domain plays an important role in the Arabidopsis growth and stress response. BMC Plant Biol. 14, 98. crossref(new window)

68.
Lightowlers, R., and Chrzanowska-Lightowlers, Z. (2008). PPR (pentatricopeptide repeat) proteins in mammals: important aids to mitochondrial gene expression. Biochem. J. 416, e5-e6. crossref(new window)

69.
Lim, M.-H., Kim, J., Kim, Y.-S., Chung, K.-S., Seo, Y.-H., Lee, I., Kim, J., Hong, C.B., Kim, H.-J., and Park, C.-M. (2004). A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16, 731-740. crossref(new window)

70.
Liu, M., Shi, D.Q., Yuan, L., Liu, J., and Yang, W.C. (2010a). SLOW WALKER3, encoding a putative DEAD‐box RNA helicase, is essential for female gametogenesis in Arabidopsis. J. Int. Plant Biol. 52, 817-828. crossref(new window)

71.
Liu, Y., He, J., Chen, Z., Ren, X., Hong, X., and Gong, Z. (2010b). ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. Plant J. 63, 749-765. crossref(new window)

72.
de Longevialle, A.F., Meyer, E.H., Andres, C., Taylor, N.L., Lurin, C., Millar, A.H., and Small, I.D. (2007). The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell 19, 3256-3265. crossref(new window)

73.
de Longevialle, A.F., Hendrickson, L., Taylor, N.L., Delannoy, E., Lurin, C., Badger, M., Millar, A.H., and Small, I. (2008). The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. Plant J. 56, 157-168. crossref(new window)

74.
de Longevialle, A.F., Small, I.D., and Lurin, C. (2010). Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol. Plant 3, 691-705. crossref(new window)

75.
Lorkovic, Z.J. (2009). Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci.14, 229-236. crossref(new window)

76.
Lorkovic, Z.J., and 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, 623-635. crossref(new window)

77.
Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., and Cobbett, C. (1997). FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737-745. crossref(new window)

78.
Mangeon, A., Junqueira, R.M., and Sachetto-Martins, G. (2010). Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal. Behav. 5, 99-104. crossref(new window)

79.
Manival, X., Ghisolfi-Nieto, L., Joseph, G., Bouvet, P., and Erard, M. (2001). RNA-binding strategies common to cold-shock domainand RNA recognition motif-containing proteins. Nucleic Acids Res. 29, 2223-2233. crossref(new window)

80.
Martin, S.L. (2010). Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1. RNA Biol. 7, 706-711. crossref(new window)

81.
Mei, C., Jiang, S.-C., Lu, Y.-F., Wu, F.-Q., Yu, Y.-T., Liang, S., Feng, X.-J., Comeras, S.P., Lu, K., and Wu, Z. (2014). Arabidopsis pentatricopeptide repeat protein SOAR1 plays a critical role in abscisic acid signalling. J. Exp. Bot. 65, 5317-5330. crossref(new window)

82.
Mihailovich, M., Militti, C., Gabaldon, T., and Gebauer, F. (2010). Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression. BioEssays 32, 109-118. crossref(new window)

83.
Mingam, A., Toffano-Nioche, C., Brunaud, V., Boudet, N., Kreis, M., and Lecharny, A. (2004). DEAD-box RNA helicases in Arabidopsis thaliana: establishing a link between quantitative expression, gene structure and evolution of a family of genes. J. Plant Biotechnol. 2, 401-415. crossref(new window)

84.
Mockler, T.C., Yu, X., Shalitin, D., Parikh, D., Michael, T.P., Liou, J., Huang, J., Smith, Z., Alonso, J.M., and Ecker, J.R. (2004). Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc. Natl. Acad. Sci. USA 101, 12759-12764. crossref(new window)

85.
Mohr, S., Stryker, J.M., and Lambowitz, A.M. (2002). A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109, 769-779. crossref(new window)

86.
Mohr, S., Matsuura, M., Perlman, P.S., and Lambowitz, A.M. (2006). A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc. Natl. Acad. Sci. U.S.A. 103, 3569-3574. crossref(new window)

87.
Nagai, K., Oubridge, C., Ito, N., Avis, J., and Evans, P. (1995). The RNP domain : a sequence- specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem. Sci. 20, 235-240. crossref(new window)

88.
Nakaminami, K., Karlson, D.T., and Imai, R. (2006). Functional conservation of cold shock domains in bacteria and higher plants. Proc. Natl. Acad. Sci. U.S.A. 103, 10122-10127. crossref(new window)

89.
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. crossref(new window)

90.
Ostersetzer, O., Cooke, A.M., Watkins, K.P., and Barkan, A. (2005). CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell 17, 241-255. crossref(new window)

91.
Ostheimer, G.J., Barkan, A., and Matthews, B.W. (2002). Crystal structure of E. coli YhbY: a representative of a novel class of RNA binding proteins. Structure 10, 1593-1601. crossref(new window)

92.
Rackham, O., and Filipovska, A. (2012). The role of mammalian PPR domain proteins in the regulation of mitochondrial gene expression. Biochim. Biophys. Acta 1819, 1008-1016. crossref(new window)

93.
Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., Mayer, O., Jantsch, M.F., Konrat, R., Blasi, U., and Schroeder, R. (2007). RNA chaperones, RNA annealers and RNA helicases. RNA Biol. 4, 118-130. crossref(new window)

94.
Ripoll, J.J., Ferrándiz, C., Martínez-Laborda, A., and Vera, A. (2006). PEPPER, a novel K-homology domain gene, regulates vegetative and gynoecium development in Arabidopsis. Dev. Biol. 289, 346-359. crossref(new window)

95.
Sachetto-Martins, G., Franco, L.O., and de Oliveira, D.E. (2000). Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim. Biophys. Acta. 1492, 1-14 crossref(new window)

96.
Saha, D., Prasad, A.M., and Srinivasan, R. (2007). Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521-534. crossref(new window)

97.
Sasaki, K., Kim, M.-H., and Imai, R. (2007). Arabidopsis COLD SHOCK DOMAIN PROTEIN2 is a RNA chaperone that is regulated by cold and developmental signals. Biochem. Biophys. Res. Commun. 364, 633-638. crossref(new window)

98.
Schein, A., Sheffy-Levin, S., Glaser, F., and Schuster, G. (2008). The RNase E/G-type endoribonuclease of higher plants is located in the chloroplast and cleaves RNA similarly to the E. coli enzyme. RNA 14, 1057-1068. crossref(new window)

99.
Schmitz-Linneweber, C., and Small, I. (2008). Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670. crossref(new window)