The exosome and trans-acting small interfering RNAs regulate cuticular wax biosynthesis during arabidopsis inflorescence stem development

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 323-336

  Lam, Patricia ^a   Zhao, Lifang ^a   Eveleigh, Nathan ^a   Yu, Yu ^b   Chen, Xuemei ^b   Kunst, Ljerka ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

ARABIDOPSIS PROTEIN; MESSENGER RNA; SMALL INTERFERING RNA; WAX;

ARABIDOPSIS; EXOSOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; INFLORESCENCE; METABOLISM; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PLANT STEM; SEQUENCE ANALYSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; EXOSOMES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; INFLORESCENCE; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PLANT STEMS; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; WAXES;

EID: 84921992534     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.252825     Document Type: Article

References (62)

1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouché N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16: 927-932
2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480
3. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221
4. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
5. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106
6. Baulcombe D (2005) RNA silencing. Trends Biochem Sci 30: 290-293
7. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102: 11928-11933
8. Berendzen K, Searle I, Ravenscroft D, Koncz C, Batschauer A, Coupland G, Somssich IE, Ulker B (2005) A rapid and versatile combined DNA/ RNA extraction protocol and its application to the analysis of a novel DNA marker set polymorphic between Arabidopsis thaliana ecotypes Col-0 and Landsberg erecta. Plant Methods 1: 4
9. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A (2010) Manipulation of FASTQ data with Galaxy. Bioinformatics 26: 1783-1785
10. Boutet S, Vazquez F, Liu J, Béclin C, Fagard M, Gratias A, Morel JB, Crété P, Chen X, Vaucheret H (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol 13: 843-848
11. Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101: 4706-4711
12. Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129: 1085-1094
13. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23: 549-554
14. Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37: 1356- 1360
15. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328: 912-916
16. Fukudome A, Kanaya A, Egami M, Nakazawa Y, Hiraguri A, Moriyama H, Fukuhara T (2011) Specific requirement of DRB4, a dsRNA-binding protein, for the in vitro dsRNA-cleaving activity of Arabidopsis Dicerlike 4. RNA 17: 750-760
17. Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and Dicer-Like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22: 481-496
18. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15: 1494-1500
19. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
20. Go YS, Kim H, Kim HJ, Suh MC (2014) Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ ERF-type transcription factor. Plant Cell 26: 1666-1680
21. Hernandez-Pinzon I, Yelina NE, Schwach F, Studholme DJ, Baulcombe D, Dalmay T (2007) SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J 50: 140-148
22. Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, Murai Y, Koiwa H, Seki M, Shinozaki K, Fukuhara T (2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol Biol 57: 173-188
23. Hooker TS, Lam P, Zheng H, Kunst L (2007) A core subunit of the RNAprocessing/ degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19: 904-913
24. Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutiérrez-Nava M, Poethig SR (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973-2981
25. Jauvion V, Elmayan T, Vaucheret H (2010) The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22: 2697- 2709
26. Jetter R, Kunst L, Samuels L (2006). Composition of plant cuticular waxes. In M Riederer, C Muller, eds, Biology of the Plant Cuticle, Vol 23. Blackwell Publishing, Oxford, pp 145-181
27. Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G, Höfte H, PaulyM, Riechmann JL, Broun P (2007) The transcription factorWIN1/ SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19: 1278-1294
28. Kidner CA, Martienssen RA (2005) The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Dev Biol 280: 504-517
29. Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1994) Characterization of two cDNAs (ERD10 and ERD14) corresponding to genes that respond rapidly to dehydration stress in Arabidopsis thaliana. Plant Cell Physiol 35: 225-231
30. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151: 1918-1929
31. Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R, Watanabe Y (2009) SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/ RDR6-bodies. FEBS Lett 583: 1261-1266
32. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42: 51-80
33. Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12: 721-727
34. Lam P, Zhao L, McFarlane HE, Aiga M, Lam V, Hooker TS, Kunst L (2012) RDR1 and SGS3, components of RNA-mediated gene silencing, are required for the regulation of cuticular wax biosynthesis in developing inflorescence stems of Arabidopsis. Plant Physiol 159: 1385-1395
35. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, et al (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40: D1202-D1210
36. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
37. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 39-end uridylation activity in Arabidopsis. Curr Biol 15: 1501-1507
38. McCarthyDJ, Chen Y, SmythGK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40: 4288-4297
39. Nakazawa Y, Hiraguri A, Moriyama H, Fukuhara T (2007) The dsRNAbinding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol Biol 63: 777-785
40. Nogueira FT, Chitwood DH, Madi S, Ohtsu K, Schnable PS, Scanlon MJ, Timmermans MC (2009) Regulation of small RNA accumulation in the maize shoot apex. PLoS Genet 5: e1000320
41. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18: 2368- 2379
42. Péret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, et al (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24: 2874-2885
43. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45
44. Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13: 236-246
45. Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, Huard C, Blée E, Mongrand S, Domergue F, Roby D (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20: 752-767
46. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140
47. Schwab R, Maizel A, Ruiz-Ferrer V, Garcia D, Bayer M, Crespi M, Voinnet O, Martienssen RA (2009) Endogenous tasiRNAs mediate noncell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS ONE 4: e5980
48. Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138-1152
49. Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, Métraux JP, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721-738
50. Somerville CR, Ogren WL (1982) Isolation of photorespiratory mutants of Arabidopsis. In M Edelman, RB Hallick, N-H Chua, eds, Methods in Chloroplast Molecular Biology. Elsevier, New York, pp 129-139
51. Suh MC, Samuels AL, Jetter R, Kunst L, Pollard M, Ohlrogge J, Beisson F (2005) Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol 139: 1649-1665
52. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crété P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16: 69-79
53. von Wettstein-Knowles P (July 16, 2012) Plant waxes. In eLS. John Wiley & Sons, Chichester, UK, doi: 10.1002/9780470015902.a0001919.pub2 (July 2014)
54. Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102: 9703-9708
55. Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102: 12984- 12989
56. Xie Z, Qi X (2008) Diverse small RNA-directed silencing pathways in plants. Biochim Biophys Acta 1779: 720-724
57. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19: 2164- 2175
58. Yu B, Bi L, Zhai J, Agarwal M, Li S, Wu Q, Ding SW, Meyers BC, Vaucheret H, Chen X (2010) siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res 38: 5844-5850
59. Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307: 932-935
60. Yu D, Fan B, MacFarlane SA, Chen Z (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant Microbe Interact 16: 206-216
61. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689-707
62. Zhang Z, Schwartz S, Wagner L, Miller W (2000). A greedy algorithm for aligning DNA sequences. J Comput Biol 7: 203-214