Transcriptome landscape of Rafflesia cantleyi floral buds reveals insights into the roles of transcription factors and phytohormones in flower development
Autoři:
Safoora Amini aff001; Khadijah Rosli aff001; Mohd-Faizal Abu-Bakar aff003; Halimah Alias aff003; Mohd-Noor Mat-Isa aff003; Mohd-Afiq-Aizat Juhari aff004; Jumaat Haji-Adam aff004; Hoe-Han Goh aff005; Kiew-Lian Wan aff001
Působiště autorů:
School of Biosciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, UKM Bangi, Selangor, Malaysia
aff001; Centre for Biotechnology and Functional Food, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, UKM Bangi, Selangor, Malaysia
aff002; Malaysia Genome Institute, Jalan Bangi, Kajang, Selangor, Malaysia
aff003; School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, UKM Bangi, Selangor, Malaysia
aff004; Institute of Systems Biology, Universiti Kebangsaan Malaysia, UKM Bangi, Selangor, Malaysia
aff005
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226338
Souhrn
Rafflesia possesses unique biological features and known primarily for producing the world’s largest and existing as a single flower. However, to date, little is known about key regulators participating in Rafflesia flower development. In order to further understand the molecular mechanism that regulates Rafflesia cantleyi flower development, RNA-seq data from three developmental stages of floral bud, representing the floral organ primordia initiation, floral organ differentiation, and floral bud outgrowth, were analysed. A total of 89,890 transcripts were assembled of which up to 35% could be annotated based on homology search. Advanced transcriptome analysis using K-mean clustering on the differentially expressed genes (DEGs) was able to identify 12 expression clusters that reflect major trends and key transitional states, which correlate to specific developmental stages. Through this, comparative gene expression analysis of different floral bud stages identified various transcription factors related to flower development. The members of WRKY, NAC, bHLH, and MYB families are the most represented among the DEGs, suggesting their important function in flower development. Furthermore, pathway enrichment analysis also revealed DEGs that are involved in various phytohormone signal transduction events such as auxin and auxin transport, cytokinin and gibberellin biosynthesis. Results of this study imply that transcription factors and phytohormone signalling pathways play major role in Rafflesia floral bud development. This study provides an invaluable resource for molecular studies of the flower development process in Rafflesia and other plant species.
Klíčová slova:
Gene expression – Transcription factors – Transcriptome analysis – Arabidopsis thaliana – Auxins – Buds – Regulator genes – Floral development
Zdroje
1. Adam JH, Mohamed R, Juhari MAA, Ariff NNFN, Wan KL. Rafflesia sharifah-hapsahiae (Rafflesiaceae), a new species from Peninsular Malaysia. Turkish Journal of Botany. 2013;37: 1038–1044.
2. Adam JH, Juhari MAA, Mohamed R, Wahan NAA, Arshad S, Kamruzaman MP, et al. Rafflesia tuanku halimii n. (Rafflesiaceae), a new species from peninsular Malaysia. Sains Malaysiana. 2016;45: 1589–1595.
3. Nais J, Rafflesia of the World, Sabah Parks Trustees, Kota Kinabalu 2001.
4. Davis CC, Endress PK, Baum DA. The evolution of floral gigantism. Current Opinion in Plant Biology. 2008;11: 49–57. doi: 10.1016/j.pbi.2007.11.003 18207449
5. Meijer W. Rafflesiaceae. Flora Malesiana. 1997;13: 1–42.
6. Srikanth A, Schmid M. Regulation of flowering time: all roads lead to Rome. Cellular and Molecular Life Sciences. 2011;68: 2013–2037. doi: 10.1007/s00018-011-0673-y 21611891
7. Komeda Y. Genetic regulation of time to flower in Arabidopsis thaliana. Annual Review of Plant Biology. 2004;55: 521–535. doi: 10.1146/annurev.arplant.55.031903.141644 15377230
8. Causier B, Schwarz-Sommer Z, Davies B. Floral organ identity: 20 years of ABCs. Seminars in Cell & Developmental Biology. 2010;21: 73–79.
9. Stewart D, Graciet E, Wellmer F. Molecular and regulatory mechanisms controlling floral organ development. The FEBS Journal. 2016;283: 1823–1830. doi: 10.1111/febs.13640 26725470
10. Huijser P, Schmid M. The control of developmental phase transitions in plants. Development. 2011;138: 4117–4129. doi: 10.1242/dev.063511 21896627
11. Wee SL, Tan SB, Jürgens A. Pollinator specialization in the enigmatic Rafflesia cantleyi: A true carrion flower with species-specific and sex-biased blow fly pollinators. Phytochemistry. 2018;153: 120–128. doi: 10.1016/j.phytochem.2018.06.005 29906658
12. Ng SM, Lee XW, Mat-Isa MN, Aizat-Juhari MA, Adam JH, Mohamed R, et al. Comparative analysis of nucleus-encoded plastid-targeting proteins in Rafflesia cantleyi against photosynthetic and non-photosynthetic representatives reveals orthologous systems with potentially divergent functions. Scientific Reports. 2018;8: 17258. doi: 10.1038/s41598-018-35173-1 30467394
13. Lee XW, Mat-Isa MN, Mohd-Elias NA, Aizat-Juhari MA, Goh HH, Dear PH, et al. Perigone lobe transcriptome analysis provides insights into Rafflesia cantleyi flower development. PLoS One. 2016;11: e0167958. doi: 10.1371/journal.pone.0167958 27977777
14. Nikolov LA, Endress PK, Sugumaran M, Sasirat S, Vessabutr S, Kramer EM, et al. Developmental origins of the world’s largest flowers, Rafflesiaceae. Proceedings of the National Academy of Sciences. 2013;110: 18578–18583.
15. Amini S, Alias H, Aizat-Juhari MA, Mat-Isa MN, Adam JH, Goh HH, et al. RNA-seq data from different developmental stages of Rafflesia cantleyi floral buds. Genomics Data. 2017;14: 5–6. doi: 10.1016/j.gdata.2017.07.008 28761813
16. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404
17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology. 2011;29: 644. doi: 10.1038/nbt.1883 21572440
18. Wang Y, Pan Y, Liu Z, Zhu X, Zhai L, Xu L, et al. De novo transcriptome sequencing of radish (Raphanus sativus L.) and analysis of major genes involved in glucosinolate metabolism. BMC Genomics. 2013;14: 836. doi: 10.1186/1471-2164-14-836 24279309
19. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21: 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474
20. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, et al. WEGO: a web tool for plotting GO annotations. Nucleic Acids Research. 2006;34: W293–W297. doi: 10.1093/nar/gkl031 16845012
21. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research. 1999;27: 29–34. doi: 10.1093/nar/27.1.29 9847135
22. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Research. 2013;42: D222–D230. doi: 10.1093/nar/gkt1223 24288371
23. Consortium GO. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Research. 2004;32: D258–D261. doi: 10.1093/nar/gkh036 14681407
24. Pérez-Rodríguez P, Riano-Pachon DM, Corrêa LGG, Rensing SA, Kersten B, Mueller-Roeber B. PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Research. 2009;38: D822–D827. doi: 10.1093/nar/gkp805 19858103
25. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12: 323. doi: 10.1186/1471-2105-12-323 21816040
26. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
27. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research. 2011;39: W316–W322. doi: 10.1093/nar/gkr483 21715386
28. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6: e21800. doi: 10.1371/journal.pone.0021800 21789182
29. Doyle JJ. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin. 1987;19: 11–15.
30. Japelaghi RH, Haddad R, Garoosi GA. Rapid and efficient isolation of high quality nucleic acids from plant tissues rich in polyphenols and polysaccharides. Molecular Biotechnology. 2011;49: 129–137. doi: 10.1007/s12033-011-9384-8 21302150
31. Reid KE, Olsson N, Schlosser J, Peng F, Lund ST. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biology. 2006;6: 27. doi: 10.1186/1471-2229-6-27 17105665
32. Nikolov LA, Staedler YM, Manickam S, Schönenberger J, Endress PK, Kramer EM, et al. Floral structure and development in Rafflesiaceae with emphasis on their exceptional gynoecia. American Journal of Botany. 2014;101: 225–243. doi: 10.3732/ajb.1400009 24509798
33. Hu W, Ma H. Characterization of a novel putative zinc finger gene MIF1: involvement in multiple hormonal regulation of Arabidopsis development. The Plant Journal. 2006;45: 399–422. doi: 10.1111/j.1365-313X.2005.02626.x 16412086
34. Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences. 2012;109: 1560–1565.
35. Vimolmangkang S, Han Y, Wei G, Korban SS. An apple MYB transcription factor, MdMYB3, is involved in regulation of anthocyanin biosynthesis and flower development. BMC Plant Biology. 2013;13: 176. doi: 10.1186/1471-2229-13-176 24199943
36. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thalian. Development. 2005;132: 4563–4574. doi: 10.1242/dev.02012 16176952
37. Liu X, Dinh TT, Li D, Shi B, Li Y, Cao X, et al. AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA 2 in floral meristem determinacy. The Plant Journal. 2014;80: 629–641. doi: 10.1111/tpj.12658 25187180
38. Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science. 2004;303: 2022–2025. doi: 10.1126/science.1088060 12893888
39. Davis SJ. Integrating hormones into the floral‐transition pathway of Arabidopsis thaliana. Plant, Cell & Environment. 2009;32: 1201–1210.
40. Ness RW, Siol M, Barrett SC. De novo sequence assembly and characterization of the floral transcriptome in cross-and self-fertilizing plants. BMC Genomics. 2011;12: 298. doi: 10.1186/1471-2164-12-298 21649902
41. Parchman TL, Geist KS, Grahnen JA, Benkman CW, Buerkle CA. Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics. 2010;11: 180. doi: 10.1186/1471-2164-11-180 20233449
42. Logacheva MD, Kasianov AS, Vinogradov DV, Samigullin TH, Gelfand MS, Makeev VJ, et al. De novo sequencing and characterization of floral transcriptome in two species of buckwheat (Fagopyrum). BMC Genomics. 2011;12: 30. doi: 10.1186/1471-2164-12-30 21232141
43. Davis CC, Latvis M, Nickrent DL, Wurdack KJ, Baum DA. Floral gigantism in Rafflesiaceae. Science. 2007;315: 1812–1812. doi: 10.1126/science.1135260 17218493
44. Xi Z, Bradley RK, Wurdack KJ, Wong K, Sugumaran M, Bomblies K, et al. Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics. 2012;13: 227. doi: 10.1186/1471-2164-13-227 22681756
45. Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM. Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genetics. 2006;2: e117. doi: 10.1371/journal.pgen.0020117 16789830
46. Mallory AC, Dugas DV, Bartel DP, Bartel B. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Current Biology. 2004;14: 1035–1046. doi: 10.1016/j.cub.2004.06.022 15202996
47. Larue CT, Wen J, Walker JC. A microRNA–transcription factor module regulates lateral organ size and patterning in Arabidopsis. The Plant Journal. 2009;58: 450–463. doi: 10.1111/j.1365-313X.2009.03796.x 19154203
48. Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell. 2003;15: 2730–2741. doi: 10.1105/tpc.016238 14555699
49. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. Specific effects of microRNAs on the plant transcriptome. Developmental Cell. 2005;8: 517–527. doi: 10.1016/j.devcel.2005.01.018 15809034
50. Huang YJ, Liu LL, Huang JQ, Wang ZJ, Chen FF, Zhang QX, et al. Use of transcriptome sequencing to understand the pistillate flowering in hickory (Carya cathayensis Sarg.). BMC Genomics. 2013;14: 691. doi: 10.1186/1471-2164-14-691 24106755
51. Liu K, Feng S, Pan Y, Zhong J, Chen Y, Yuan C, Li H. Transcriptome analysis and identification of genes associated with floral transition and flower development in sugar apple (Annona squamosa L.). Frontiers in Plant Science. 2016;7: 1695. doi: 10.3389/fpls.2016.01695 27881993
52. Kayal WE, Allen CC, Ju CJT, Adams E, King-Joned S, Zaharia LI, et al. Molecular events of apical bud formation in white spruce. Picea glauca. Plant, Cell & Environment. 2011;34: 480–500.
53. Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, et al. Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin–cytokinin-regulated development. Proceedings of the National Academy of Sciences. 2004;101: 8039–8044.
54. Horiguchi G, Kim GT, Tsukaya H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. The Plant Journal. 2005;43: 68–78. doi: 10.1111/j.1365-313X.2005.02429.x 15960617
55. Kim JH, Choi D, Kende H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. The Plant Journal. 2003;36: 94–104. doi: 10.1046/j.1365-313x.2003.01862.x 12974814
56. Jin H, Martin C. Multifunctionality and diversity within the plant MYB-gene family. Plant Molecular Biology. 1999;41: 577–585. doi: 10.1023/a:1006319732410 10645718
57. Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, et al. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genetics. 2009;5: e1000440. doi: 10.1371/journal.pgen.1000440 19325888
58. Gu X, Wang Y, He Y. Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biology. 2013;11: e1001649. doi: 10.1371/journal.pbio.1001649 24019760
59. Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, et al. Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. The Plant Cell. 2012;24: 1398–1419. doi: 10.1105/tpc.112.095711 22517317
60. Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, et al. FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proceedings of the National Academy of Sciences U.S.A. 2012;109: 3582–3587.
61. Hussey SG, Mizrachi E, Spokevicius AV, Bossinger G, Berger DK, Myburg AA. SND2, a NAC transcription factor gene, regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus. BMC Plant Biology. 2011;11: 173. doi: 10.1186/1471-2229-11-173 22133261
62. Sakamoto S, Mitsuda N. Reconstitution of a secondary cell wall in a secondary cell wall-deficient Arabidopsis mutant. Plant and Cell Physiology. 2014;56: 299–310. doi: 10.1093/pcp/pcu208 25535195
63. Alabadí D, Blázquez MA, Carbonell J, Ferrándiz C, Pérez-Amador MA. Instructive roles for hormones in plant development. International Journal of Developmental Biology. 2009;53: 1597. doi: 10.1387/ijdb.072423da 19247940
64. Fan Z, Li J, Li X, Wu B, Wang J, Liu Z, et al. Genome-wide transcriptome profiling provides insights into floral bud development of summer-flowering Camellia azalea. Scientific Reports. 2015;5: 9729. doi: 10.1038/srep09729 25978548
65. Wang J, Yan DW, Yuan TT, Gao X, Lu YT. A gain-of-function mutation in IAA8 alters Arabidopsis floral organ development by change of jasmonic acid level. Plant Molecular Biology. 2013;82: 71–83. doi: 10.1007/s11103-013-0039-y 23483289
66. Elias NAM, Goh HH, Isa NM, Wan KL. Identification of ARF and AUX/IAA gene families in Rafflesia cantleyi. AIP Conference Proceedings. 2016: 020017.
67. Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, et al. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biology. 7 2009: e1000090. doi: 10.1371/journal.pbio.1000090 19385720
68. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115: 591–602. doi: 10.1016/s0092-8674(03)00924-3 14651850
69. Ribeiro DM, Araújo WL, Fernie AR, Schippers JH, Mueller-Roeber B. Translatome and metabolome effects triggered by gibberellins during rosette growth in Arabidopsis. Journal of Experimental Botany. 2012;63: 2769–2786. doi: 10.1093/jxb/err463 22291129
70. Goto N, Pharis RP. Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Canadian Journal of Botany. 1999;77: 944–954.
71. Bonhomme F, Kurz B, Melzer S, Bernier G, Jacqmard A. Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. The Plant Journal. 2000;24: 103–111. doi: 10.1046/j.1365-313x.2000.00859.x 11029708
72. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development. 1996;122: 1567–1575. 8625843
73. Yamburenko MV, Kieber JJ, Schaller GE. Dynamic patterns of expression for genes regulating cytokinin metabolism and signaling during rice inflorescence development. PLoS One. 2017;12: e0176060. doi: 10.1371/journal.pone.0176060 28419168
74. Wang Y, Li L, Ye T, Lu Y, Chen X, Wu Y. The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. Journal of Experimental Botany. 2013;64: 675–684. doi: 10.1093/jxb/ers361 23307919
75. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology. 2010;61: 651–679. doi: 10.1146/annurev-arplant-042809-112122 20192755
76. Winter G, Todd CD, Trovato M, Forlani G, Funck D. Physiological implications of arginine metabolism in plants. Frontiers in Plant Science. 2015;6: 534. doi: 10.3389/fpls.2015.00534 26284079
77. Wasternack C, Forner S, Strnad M, Hause B. Jasmonates in flower and seed development. Biochimie. 2013;95: 79–85. doi: 10.1016/j.biochi.2012.06.005 22705387
78. Xiao L, Zhang L, Yang G, Zhu H, He Y. Transcriptome of protoplasts reprogrammed into stem cells in Physcomitrella patens. PLoS One. 2012;7: e35961. doi: 10.1371/journal.pone.0035961 22545152
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