Белковая интерференция как механизм регуляции экспрессии генов растений


https://doi.org/10.18699/VJ18.419

Полный текст:


Аннотация

Транскрипционные факторы (ТФ) играют центральную роль в регуляционных процессах, связанных с развитием растений и их ответом на внешние воздействия. Работа ТФ регулируется на каждой стадии из активности. Как правило, ТФ состоят из трех доменов, необходимых для ДНК-связывания, димеризации и транскрипционной регуляции. Альтернативный сплайсинг позволяет получить множество белков с различным составом доменов. Недавние исследования показали, что в результате альтернативного сплайсинга некоторых генов, кодирующих ТФ, образуются малые пептиды (малые интерферирующие пептиды/белки, siPEP/ siPROT), у которых отсутствует один или несколько доменов и которые негативно регулируют целевой ТФ благодаря механизму белковой интерференции (белковая/пептидная интерференция, PEPi/PROTi). Было показано наличие альтернативной формы для транскрипционного фактора ССА1 Arabidopsis thaliana, которая участвует в регуляции ответа на холодовой стресс. Для белка PtFLC обнаружена одна из изоформ, которая образуется в результате альтернативного сплайсинга и действует как негативный репрессор, связываясь с полноразмерным ТФ PtFLC и тем самым регулируя некоторые стадии развития растения Poncirus trifoliata. Для A. thaliana обнаружен ген FLM, образующий изоформу FLM-б, которая работает как доминантный негативный регулятор и стимулирует процесс формирования цветка благодаря образованию гетеродимера с транскрипционным фактором SVP. Малые интерферирующие пептиды и белки могут быть активными участниками регуляции экспрессии генов, например, при стрессовых воздействиях или на разных стадиях развития растения. Более того, небольшие интерферирующие пептиды и белки могут быть использованы в качестве инструмента для фундаментальных исследований функции генов, а также в прикладных исследованиях, например, для временного или постоянного выключения гена. Данный обзор посвящен последним исследованиям, связанным с малыми интерферирующими пептидами и их ролью в ответе на различные стрессовые факторы, а также возможным путям получения малых интерферирующих пептидов.


Об авторах

А. О. Вячеславова
Институт общей генетики им. Н.И. Вавилова, Российская академия наук
Россия

Москва



И. А. Абдеева
Институт общей генетики им. Н.И. Вавилова, Российская академия наук
Россия

Москва



Э. С. Пирузян
Институт общей генетики им. Н.И. Вавилова, Российская академия наук
Россия

Москва



С. А. Брускин
Институт общей генетики им. Н.И. Вавилова, Российская академия наук
Россия

Москва



Список литературы

1. Alabadi D., Oyama T., Yanovsky M.J., Harmon F.G., Mas P., Kay S.A. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science. 2001;293(5531):880-883. DOI 10.1126/science.1061320.

2. Arana M.V., Marin-de la Rosa N., Maloof J.N., Blazquez M.A., Ala-badi D. Circadian oscillation of gibberellin signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108(22):9292-9297. DOI 10.1073/ pnas.1101050108.

3. Balasubramanian S., Sureshkumar S., Lempe J., Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2006;2(7):e106. DOI 10.1371/journal.pgen. 0020106.

4. Bauer D., Viczian A., Kircher S., Nobis T., Nitschke R., Kunkel T., Panigrahi K.C., Adam E., Fejes E., Schafer E., Nagy F. Constitutive Photomorphogenesis 1 and multiple photoreceptors control degradation of Phytochrome Interacting Factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell. 2004;16(6): 1433-1445. DOI 10.1105/tpc.021568.

5. Bhattacharjee A., Ghosh S.K., Neogi K., Aich A., Willard B., Kinter M., Sen S.K., Ghosh D., Ghosh S. Deposition of stearate-oleate rich seed fat in Mangifera indica is mediated by a FatA type acyl-ACP thioesterase. Phytochemistry. 2011;72(2-3):166-177. DOI 10.1016/j. phytochem.2010.11.004.

6. Capovilla G., Schmid M., Pose D. Control of flowering by ambient temperature. J. Exp. Bot. 2015;66(1):59-69. DOI 10.1093/jxb/eru416.

7. Chen L., Bush S.J., Tovar-Corona J.M., Castillo-Morales A., Urru-tia A.O. Correcting for differential transcript coverage reveals a strong relationship between alternative splicing and organism complexity. Mol. Biol. Evol. 2014;31(6):1402-1413. DOI 10.1093/molbev/msu083.

8. Dong M.A., Farre E.M., Thomashow M.F. CIRCADIAN CLOCK ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108(17):7241-7246. DOI 10.1073/pnas.1103741108.

9. Duek P.D., Fankhauser C. HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signaling. Plant J. 2003;34(6):827-836.

10. Feng S., Martinez C., Gusmaroli G., Wang Y., Zhou J., Wang F., Chen L., Yu L., Iglesias-Pedraz J.M., Kircher S., Schafer E., Fu X., Fan L.M., Deng X.W. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature. 2008;451(7177):475-479. DOI 10.1038/nature06448.

11. Filipowicz W., Jaskiewicz L., Kolb F.A., Pillai R.S. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr. Opin. Struct. Biol. 2005;15(3):331-341. DOI 10.1016/j.sbi.2005.05.006.

12. Gu X., Le C., Wang Y., Li Z., Jiang D., Wang Y., He Y. Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat. Com-mun. 2013;4:1947. DOI 10.1038/ncomms2947.

13. Harmer S.L. The circadian system in higher plants. Annu. Rev. Plant. Biol. 2009;60:357-377. DOI 10.1146/annurev.arplant.043008.092054.

14. Hill K. Post-translational modifications of hormone-responsive transcription factors: the next level of regulation. J. Exp. Bot. 2015; 66(16):4933-4945. DOI 10.1093/jxb/erv273.

15. Hong S.Y., Kim O.K., Kim S.G., Yang M.S., Park C.M. Nuclear import and DNA binding of the ZHD5 transcription factor is modulated by a competitive peptide inhibitor in Arabidopsis. J. Biol. Chem. 2011;286(2):1659-1668. DOI 10.1074/jbc.M110.167692.

16. Hong S.Y., Seo P.J., Ryu J.Y., Cho S.H., Woo J.C., Park C.M. A competitive peptide inhibitor KIDARI negatively regulates HFR1 by forming nonfunctional heterodimers in Arabidopsis photomorphogenesis. Mol. Cells. 2013;35(1):25-31. DOI 10.1007/s10059-013-2159-2.

17. Hoppe T., Rape M., Jentsch S. Membrane-bound transcription factors: regulated release by RIP or RUP. Curr. Opin. Cell Biol. 2001; 13(3):344-348.

18. Horvath D.P., Anderson J.V., Chao W.S., Foley M.E. Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci. 2003; 8(11):534-540. DOI 10.1016/j.tplants.2003.09.013.

19. Hu W., Feng B., Ma H. Ectopic expression of the Arabidopsis MINI ZINC FINGER1 and MIF3 genes induces shoot meristems on leaf margins. Plant Mol. Biol. 2011;76(1-2):57-68. DOI 10.1007/s11103-011-9768-y.

20. Hu W., Ma H. Characterization of a novel putative zinc finger gene MIF1: involvement in multiple hormonal regulation of Arabidopsis development. Plant J. 2006;45(3):399-422. DOI 10.1111/j.1365-313X.2005.02626.x.

21. Huang W., Perez-Garda P., Pokhilko A., Millar A.J., Antoshechkin I., Riechmann J.L., Mas P. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science. 2012;336(6077):75-79. DOI 10.1126/science.1219075.

22. Huq E., Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002;21(10):2441-2450. DOI 10.1093/emboj/21.10.2441.

23. Hyun Y., Lee I. KIDARI, encoding a non-DNA binding bHLH protein, represses light signal transduction in Arabidopsis thaliana. Plant Mol. Biol. 2006;61(1-2):283-296. DOI 10.1007/s11103-006-0010-2.

24. Ingvardsen C., Veierskov B. Ubiquitin- and proteasome-dependent proteolysis in plants. Physiol. Plant. 2001;112(4):451-459.

25. Johanson U., West J., Lister C., Michaels S., Amasino R., Dean C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science. 2000;290(5490): 344-347.

26. Kebrom T.H., Burson B.L., Finlayson S.A. Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol. 2006;140(3): 1109-1117. DOI 10.1104/pp.105.074856.

27. Kim S.G., Lee A.K., Yoon H.K., Park C.M. A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J. 2008;55(1):77-88. DOI 10.1111/j.1365-313X.2008.03493.x.

28. Kim S.Y., Kim S.G., Kim Y.S., Seo P.J., Bae M., Yoon H.K., Park C.M. Exploring membrane-associated NAC transcription factors in Ara-bidopsis: implications for membrane biology in genome regulation. Nuceic Acids Res. 2007;35(1):203-213. DOI 10.1093/nar/ gkl1068.

29. Kim Y.S., Kim S.G., Lee M., Lee I., Park H.Y., Seo P.J., Jung J.H., Kwon E.J., Suh S.W., Paek K.H., Park C.M. HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabi-dopsis shoot apical meristem development. Plant Cell. 2008;20(4): 920-933. DOI 10.1105/tpc.107.057448.

30. Kim Y.S., Kim S.G., Park J.E., Park H.Y., Lim M.H., Chua N.H., Park C.M. A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell. 2006;18(11):3132-3144. DOI 10.1105/tpc.106.043018.

31. Klemm J.D., Schreiber S.L., Crabtree G.R. Dimerization as a regulatory mechanism in signal transduction. Annu. Rev. Immunol. 1998;16: 569-592. DOI 10.1146/annurev.immunol.16.1.569.

32. Lee J.H., Ryu H.S., Chung K.S., Pose D., Kim S., Schmid M., Ahn J.H. Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science. 2013;342(6158):628-632. DOI 10.1126/science.1241097.

33. Lee J.H., Yoo S.J., Park S.H., Hwang I., Lee J.S., Ahn J.H. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 2007;21(4):397-402. DOI 10.1101/gad.1518407.

34. Marquez Y., Brown J.W., Simpson C., Barta A., Kalyna M. Transcrip-tome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res. 2012;22(6):1184-1195. DOI 10.1101/gr.134106.111.

35. Mastrangelo A.M., Marone D., Laido G., De Leonardis A.M., De Vita P. Alternative splicing: enhancing ability to cope with stress via tran-scriptome plasticity. Plant Sci. 2012;185-186:40-49. DOI 10.1016/j.plantsci.2011.09.006.

36. Michaels S.D., Amasino R.M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 1999;11(5):949-956.

37. Nagel D.H., Doherty C.J., Pruneda-Paz J.L., Schmitz R.J., Ecker J.R., Kay S.A. Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2015;112(34):E4802-E4810. DOI 10.1073/pnas.1513609112.

38. Ner-Gaon H., Halachmi R., Savaldi-Goldstein S., Rubin E., Ophir R., Fluhr R. Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J. 2004;39(6):877-885. DOI 10.1111/j.1365-313X.2004.02172.x.

39. Nieto C., Lopez-Salmeron V., Daviere J.M., Prat S. ELF3-PIF4 interaction regulates plant growth independently of the evening complex. Curr. Biol. 2015;25(2):187-193. DOI 10.1016/j.cub.2014.10.070.

40. Niwa Y., Yamashino T., Mizuno T. The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol. 2009; 50(4):838-854. DOI 10.1093/pcp/pcp028.

41. Nozue K., Covington M.F., Duek P.D., Lorrain S., Fankhauser C., Har-mer S.L., Maloof J.N. Rhythmic growth explained by coincidence between internal and external cues. Nature. 2007;448(7151):358-361. DOI 10.1038/nature05946.

42. Nusinow D.A., Helfer A., Hamilton E.E., King J.J., Imaizumi T., Schultz T.F., Farre E.M., Kay S.A. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature. 2011;475(7356):398-402. DOI 10.1038/nature10182.

43. Park M.J., Seo P.J., Park C.M. CCA1 alternative splicing as a way of linking the circadian clock to temperature response in Arabidopsis. Plant Signal Behav. 2012;7(9):1194-1196. DOI 10.4161/psb.21300.

44. Pose D., Verhage L., Ott F., Yant L., Mathieu J., Angenent G.C., Im-mink R.G., Schmid M. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature. 2013;503(7476):414-417. DOI 10.1038/nature12633.

45. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell. 2005;17(1):61-76. DOI 10.1105/tpc.104.026161.

46. Puranik S., Sahu P.P., Srivastava P.S., Prasad M. NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 2012;17(6):369-381. DOI 10.1016/j.tplants.2012.02.004.

47. Rae G.M., David K.M., Wood M. The dormancy marker DRM1/ARP associated with dormancy but a broader role in planta. Dev. Biol. J. 2013:632524. DOI 10.1155/2013/632524.

48. Rae G.M., Uversky V.N., David K., Wood M. DRM1 and DRM2 expression regulation: potential role of splice variants in response to stress and environmental factors in Arabidopsis. Mol. Genet. Genomics. 2014;289(3):317-332. DOI 10.1007/s00438-013-0804-2.

49. Rangarajan N., Kulkarni P., Hannenhalli S. Evolutionarily conserved network properties of intrinsically disordered proteins. PLoS One. 2015;10(5):e0126729. DOI 10.1371/journal.pone.0126729.

50. Sainsbury S., Bernecky C., Cramer P. Structural basis of transcription initiation by RNA polymerase II. Nat. Rev. Mol. Cell. Biol. 2015; 16(3):129-143. DOI 10.1038/nrm3952.

51. Scortecci K.C., Michaels S.D., Amasino R.M. Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 2001;26(2):229-236.

52. Seo P.J., Hong S.Y., Kim S.G., Park C.M. Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci. 2011a;16(10):541-549. DOI 10.1016/j.tplants.2011.06.001.

53. Seo P.J., Kim M.J., Ryu J.Y., Jeong E.Y., Park C.M. Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers, which may regulate starch metabolism. Nat. Com-mun. 2011b;2:303. DOI 10.1038/ncomms1303.

54. Seo P.J., Park M.J., Lim M.H., Kim S.G., Lee M., Baldwin I.T., Park C.M. A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED! underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell. 2012;24(6):2427-2442. DOI 10.1105/tpc.m.098723.

55. Seo P.J., Park M.J., Park C.M. Alternative splicing of transcription factors in plant responses to low temperature stress: mechanisms and functions. Planta. 2013;237(6):1415-1424. DOI 10.1007/s00425-013-1882-4.

56. Shahbazian M.D., Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007;76:75-100. DOI 10.1146/annurev.biochem.76.052705.162114.

57. Sheldon C.C., Burn J.E., Perez P.P., Metzger J., Edwards J.A., Peacock W.J., Dennis E.S. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methyla-tion. Plant Cell. 1999;11(3):445-458.

58. Song J., Angel A., Howard M., Dean C. Vernalization - a cold-induced epigenetic switch. J. Cell. Sci. 2012;125(Pt.16):3723-3731. DOI 10.1242/jcs.084764.

59. Soy J., Leivar P., Gonzalez-Schain N., Sentandreu M., Prat S., Quail P.H., Monte E. Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/ dark conditions in Arabidopsis. Plant J. 2012;71(3):390-401. DOI 10.1111/j.1365-313X.2012.04992.x.

60. Soy J., Leivar P., Monte E. PIF1 promotes phytochrome-regulated growth under photoperiodic conditions in Arabidopsis together with PIF3, PIF4, and PIF5. J. Exp. Bot. 2014;65(11):2925-2936. DOI 10.1093/jxb/ert465.

61. Stafstrom J.P., Ripley B.D., Devitt M.L., Drake B. Dormancy-associated gene expression in pea axillary buds. Cloning and expression of PsDRM1 and PsDRM2. Planta. 1998;205(4):547-552. DOI 10.1007/s004250050354.

62. Sun X., Jones W.T., Harvey D., Edwards P.J., Pascal S.M., Kirk C., Considine T., Sheerin D.J., Rakonjac J., Oldfield C.J., Xue B., Dun-ker A.K., Uversky V.N. N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/gibberellic acid receptors. J. Biol. Chem. 2010;285(15):11557-11571. DOI 10.1074/jbc.M109.027011.

63. Sun X., Xue B., Jones W.T., Rikkerink E., Dunker A.K., Uversky V.N. A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol. Biol. 2011;77(3):205-223. DOI 10.1007/s11103-011-9803-z.

64. Tatematsu K., Ward S., Leyser O., Kamiya Y., Nambara E. Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol. 2005;138(2): 757-766. DOI 10.1104/pp.104.057984.

65. Uversky V.N., Dunker A.K. Understanding protein non-folding. Bio-chim. Biophys. Acta. 2010;1804(6):1231-1264. DOI 10.1016/j.bbapap.2010.01.017.

66. Vaucheret H., Beclin C., Fagard M. Post-transcriptional gene silencing in plants. J. Cell Sci. 2001;114(Pt.17):3083-3091.

67. Verhage L., Angenent G.C., Immink R.G. Research on floral timing by ambient temperature comes into blossom. Trends Plant Sci. 2014; 19(9):583-591. DOI 10.1016/j.tplants.2014.03.009.

68. Wang W., Vinocur B., Shoseyov O., Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 2004;9(5):244-252. DOI 10.1016/j.tplants. 2004.03.006.

69. Wenkel S., Emery J., Hou B.H., Evans M.M., Barton M.K. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell. 2007;19(11):3379-3390. DOI 10.1105/tpc.107.055772.

70. Wood M., Rae G.M., Wu R.M., Walton E.F., Xue B., Hellens R.P., Uversky V.N. Actinidia DRM1 - an intrinsically disordered protein whose mRNA expression is inversely correlated with spring bud-break in kiwifruit. PLoS One. 2013;8(3):e57354. DOI 10.1371/journal.pone.0057354.

71. Yamashino T., Nomoto Y., Lorrain S., Miyachi M., Ito S., Naka-michi N., Fankhauser C., Mizuno T. Verification at the protein level of the PIF4-mediated externalcoincidence model for the temperature-adaptive photoperiodic control of plant growth in Arabidopsis thaliana. Plant Signal. Behav. 2013;8(3):e23390. DOI 10.4161/psb.23390.

72. Zhang J.Z., Li Z.M., Mei L., Yao J.L., Hu C.G. PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta. 2009;229(4):847-859. DOI 10.1007/s00425-008-0885-z.

73. Zhang X.N., Wu Y., Tobias J.W., Brunk B.P., Deitzer G.F., Liu D. HFR1 is crucial for transcriptome regulation in the cryptochrome 1-medi-ated early response to blue light in Arabidopsis thaliana. PLoS One. 2008;3(10):e3563. DOI 10.1371/journal.pone.0003563.


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