Browse > Article
http://dx.doi.org/10.14348/molcells.2016.2359

Emerging Roles of RNA-Binding Proteins in Plant Growth, Development, and Stress Responses  

Lee, Kwanuk (Department of Plant Biotechnology, College of Agriculture and Life Sciences, Chonnam National University)
Kang, Hunseung (Department of Plant Biotechnology, College of Agriculture and Life Sciences, Chonnam National University)
Publication Information
Molecules and Cells / v.39, no.3, 2016 , pp. 179-185 More about this Journal
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;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 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.   DOI
3 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.   DOI
4 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.   DOI
5 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.   DOI
6 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.   DOI
7 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   DOI
8 Saha, D., Prasad, A.M., and Srinivasan, R. (2007). Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521-534.   DOI
9 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.   DOI
10 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.   DOI
11 Schmitz-Linneweber, C., and Small, I. (2008). Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670.   DOI
12 Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., Vichas, A., and Barkan, A. (2006). A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18, 2650-2663.   DOI
13 Simpson, G.G., and Filipowicz, W. (1996). Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol. Biol. 32, 1-41   DOI
14 Small, I.D., and Peeters, N. (2000). The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 45-47.   DOI
15 Stern, D.B., Goldschmidt-Clermont, M. and Hanson, M.R. (2010). Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 61, 125-155.   DOI
16 Tan, J., Tan, Z., Wu, F., Sheng, P., Heng, Y., Wang, X., Ren, Y., Wang, J., Guo, X., and Zhang, X. (2014). A novel chloroplastlocalized pentatricopeptide repeat protein involved in splicing affects chloroplast development and abiotic stress response in rice. Mol. Plant 7, 1329-1349.   DOI
17 Yin, P., Li, Q., Yan, C., Liu, Y., Liu, J., Yu, F., Wang, Z., Long, J., He, J., and Wang, H.-W. (2013). Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504, 168-171.   DOI
18 Tripurani, S.K., Nakaminami, K., Thompson, K.B., Crowell, S.V., Guy, C.L., and Karlson, D.T. (2011). Spatial and temporal expression of cold-responsive DEAD-box RNA helicases reveals their functional roles during embryogenesis in Arabidopsis thaliana. Plant Mol. Biol. Rep. 29, 761-768.   DOI
19 Woodson, S.A. (2010). Taming free energy landscapes with RNA chaperones. RNA Biol. 7, 677-686.   DOI
20 Xu, T., Gu, L., Choi, M.J., Kim, R.J., Suh, M.C., and Kang, H. (2014). Comparative functional analysis of wheat (Triticum aestivum). zinc finger-containing glycine-rich RNA-binding proteins in response to abiotic stresses. PLoS One 9, e96877.   DOI
21 Zmudjak, M., Colas des Francs-Small, C., Keren, I., Shaya, F., Belausov, E., Small, I., and Ostersetzer-Biran, O. (2013). mCSF1, a nucleus-encoded CRM protein required for the processing of many mitochondrial introns, is involved in the biogenesis of respiratory complexes I and IV in Arabidopsis. New Phytol. 199, 379-394.   DOI
22 Zsigmond, L., Rigo, G., Szarka, A., Szekely, G., Otvos, K., Darula, Z., Medzihradszky, K.F., Koncz, C., Koncz, Z., and Szabados, L. (2008). Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol. 146, 1721-1737.   DOI
23 Zsigmond, L., Szepesi, A., Tari, I., Rigo, G., Kiraly, A., and Szabados, L. (2012). Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci. 182, 87-93.   DOI
24 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.   DOI
25 Alba, M.M., and Pages, M. (1998). Plant proteins containing the RNA-recognition motif. Trends Plant Sci. 3, 15-21.
26 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.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 Barkan, A., and Small, I. (2014). Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65, 415-442.   DOI
32 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.
33 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.
34 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.   DOI
35 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.   DOI
36 del Campo, E.M. (2009). Post-transcriptional control of chloroplast gene expression. Gene Regul. Syst. Biol. 3, 31.
37 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.   DOI
38 Chaikam, V., and Karlson, D. (2008). Functional characterization of two cold shock domain proteins from Oryza sativa. Plant Cell Environ. 31, 995-1006.   DOI
39 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.   DOI
40 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.   DOI
41 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.   DOI
42 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.   DOI
43 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.   DOI
44 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.   DOI
45 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.   DOI
46 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.   DOI
47 Filipovska, A., and Rackham, O. (2012). Modular recognition of nucleic acids by PUF, TALE and PPR proteins. Mol. Biosyst. 8, 699-708.   DOI
48 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.   DOI
49 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.   DOI
50 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.   DOI
51 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.   DOI
52 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.   DOI
53 Graumann, P.L., and Marahiel, M.A. (1998). A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23, 286-290.   DOI
54 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.   DOI
55 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.   DOI
56 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.   DOI
57 Hammani, K., and Giege, P. (2014). RNA metabolism in plant mitochondria. Trends Plant Sci. 19, 380-389.   DOI
58 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.   DOI
59 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.   DOI
60 Herschlag, D. (1995). RNA chaperones and the RNA folding problem. J. Biol. Chem. 270, 20871-20874.   DOI
61 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.   DOI
62 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.   DOI
63 Jankowsky, E. (2011). RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36, 19-29.   DOI
64 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.   DOI
65 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.   DOI
66 Kang, H., Park, S.J., and Kwak, K.J. (2013). Plant RNA chaperones in stress response. Trends Plant Sci. 18, 100-106.   DOI
67 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.   DOI
68 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.   DOI
69 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.   DOI
70 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.   DOI
71 Karlson, D., and Imai, R. (2003). Conservation of the cold shock domain protein family in plants. Plant Physiol. 131, 12-15.   DOI
72 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.   DOI
73 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.   DOI
74 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.   DOI
75 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.   DOI
76 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.   DOI
77 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.
78 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.   DOI
79 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.   DOI
80 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.   DOI
81 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.   DOI
82 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.   DOI
83 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.
84 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.   DOI
85 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.   DOI
86 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.   DOI
87 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.   DOI
88 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.   DOI
89 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.   DOI
90 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.   DOI
91 Lightowlers, R., and Chrzanowska-Lightowlers, Z. (2008). PPR (pentatricopeptide repeat) proteins in mammals: important aids to mitochondrial gene expression. Biochem. J. 416, e5-e6.   DOI
92 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.   DOI
93 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.   DOI
94 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.   DOI
95 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.   DOI
96 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.   DOI
97 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.   DOI
98 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.   DOI
99 Lorkovic, Z.J. (2009). Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci.14, 229-236.   DOI
100 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.   DOI
101 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.   DOI
102 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.   DOI
103 Martin, S.L. (2010). Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1. RNA Biol. 7, 706-711.   DOI
104 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.   DOI
105 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.   DOI
106 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.   DOI
107 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.   DOI
108 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.   DOI
109 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.   DOI
110 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.   DOI
111 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.   DOI