Large-scale phylogenomic analysis suggests three ancient superclades of the WUSCHEL-RELATED HOMEOBOX transcription factor family in plants
Autoři:
Cheng-Chiang Wu aff001; Fay-Wei Li aff002; Elena M. Kramer aff001
Působiště autorů:
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America
aff001; Boyce Thompson Institute, Ithaca, New York, United States of America
aff002; Section of Plant Biology, Cornell University, Ithaca, New York, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223521
Souhrn
The adaptation of plants to land required multiple morphological innovations. Among these include a variety of lateral organs that are initiated from apical meristems, in which the mantainance of undifferentiated stem cells is regulated by the homeodomain WUSCHEL-RELATED (WOX) transcription factors. Expansion of the WOX gene family has been associated with whole genome duplication (WGD) events and postulated to have been pivotal to the evolution of morphological complexity in land plants. Previous studies have classified the WOX gene family into three superclades (e.g., the ancient clade, the intermediate clade, and the modern clade). In order to improve our understanding of the evolution of the WOX gene family, we surveyed the WOX gene sequences from 38 genomes and 440 transcriptomes spanning the Viridiplantae and Rhodophyta. The WOX phylogeny inferred from 1039 WOX proteins drawn from 267 species with improved support along the backbone of the phylogeny suggests that the plant-specific WOX family contains three ancient superclades, which we term Type 1 (T1WOX, the WOX10/13/14 clade), Type 2 (T2WOX, the WOX8/9 and WOX11/12 clades), and Type 3 (T3WOX, the WUS, WOX1/6, WOX2, WOX3, WOX4 and WOX5/7 clades). Divergence of the T1WOX and T2WOX superclades may predate the diversification of vascular plants. Synteny analysis suggests contribution of WGD to expansion of the WOX family. Promoter analysis finds that the capacity of the WOX genes to be regulated by the auxin and cytokinin signaling pathways may be deeply conserved in the Viridiplantae. This study improves our phylogenetic context for elucidating functional evolution of the WOX gene family, which has likely contributed to the morphological complexity of land plants.
Klíčová slova:
Arabidopsis thaliana – Flowering plants – Paleogenetics – Phylogenetics – Plant genomics – Sequence alignment – Sequence motif analysis – Ferns
Zdroje
1. Graham LE, Cook ME, Busse JS. The origin of plants: Body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA. 2000;97(9):4535–4540. doi: 10.1073/pnas.97.9.4535 10781058
2. Langdale JA. Evolution of developmental mechanisms in plants. Current Opinion in Genetics & Development. 2008;18(4):368–373.
3. Soltis PS, Soltis DE. Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion in Plant Biology. 2016;30:159–165. doi: 10.1016/j.pbi.2016.03.015 27064530
4. Jill Harrison C. Development and genetics in the evolution of land plant body plans. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017;372(1713):20150490. doi: 10.1098/rstb.2015.0490 27994131
5. Sussex IM, Kerk NM. The evolution of plant architecture. Current Opinion in Plant Biology. 2001;4:33–37. 11163165
6. Gehring W, Muller M, Affolter M, Percival-Smith A, Billeter M, Qian Y, et al. The structure of the homeodomain and its functional implications. Trends in Genetics. 1990;6:323–329. doi: 10.1016/0168-9525(90)90253-3 1980756
7. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004;131(3):657–668. doi: 10.1242/dev.00963 14711878
8. Laux T, Mayer KFX, Berger J, Juergens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122:87–96. 8565856
9. Mayer K, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998;95(6):805–815. doi: 10.1016/s0092-8674(00)81703-1 9865698
10. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 2000;299:617–619.
11. Schoof H, Lenhard M, Haecker A, Mayer KFX, Juergens G, Laux T. The stem cell polulation of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100:635–644. doi: 10.1016/s0092-8674(00)80700-x 10761929
12. Nardmann J, Reisewitz P, Werr W. Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Molecular Biology and Evolution. 2009;26:1745–1755. doi: 10.1093/molbev/msp084 19387013
13. Nardmann J, Werr W. The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Molecular Biology. 2012;78(1):123–134.
14. Somssich M, Je BI, Simon R, Jackson D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016;143(18):3238–3248. doi: 10.1242/dev.133645 27624829
15. Zhang Y, Jiao Y, Jiao H, Zhao H, Zhu Y-X. Two-step functional innovation of the stem-cell factors WUS/WOX5 during plant evolution. Molecular Biology and Evolution. 2017;34(3):640–653. doi: 10.1093/molbev/msw263 28053005
16. Lenhard M, Bohnert A, Juergens G, Laux T. Termination of stem cell maintenance in Arabidopsis floral meristems by interacitons between WUSCHEL and AGAMOUS. Cell. 2001;105:805–814. doi: 10.1016/s0092-8674(01)00390-7 11440722
17. Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, et al. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell. 2001;105:793–803. doi: 10.1016/s0092-8674(01)00384-1 11440721
18. Gross-Hardt R, Lenhard M, Laux T. WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes & Development. 2002;16(9):1129–1138.
19. Ikeda M, Mitsuda N, Ohme-Takagi M. Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. The Plant Cell. 2009;21(11):3493–3505. doi: 10.1105/tpc.109.069997 19897670
20. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M. Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. The Plant Journal. 2003;35:429–441. doi: 10.1046/j.1365-313x.2003.01816.x 12904206
21. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature. 2007;446(7137):811–814. doi: 10.1038/nature05703 17429400
22. Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W. WOX gene phylogeny in Poaceae: A comparative approach addressing leaf and embryo development. Molecular Biology and Evolution. 2007;24(11):2474–2484. doi: 10.1093/molbev/msm182 17768306
23. Zhao S, Jiang Q-T, Ma J, Zhang X-W, Zhao Q-Z, Wang X-Y, et al. Characterization and expression analysis of WOX5 genes from wheat and its relatives. Gene. 2014;537(1):63–69. doi: 10.1016/j.gene.2013.12.022 24368329
24. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell. 2004;119(1):109–120. doi: 10.1016/j.cell.2004.09.018 15454085
25. Nole-Wilson S, Tranby TL, Krizek BA. AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Molecular Biology. 2005;57(5):613–628. doi: 10.1007/s11103-005-0955-6 15988559
26. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature. 2007;449:1053–1057. doi: 10.1038/nature06206 17960244
27. Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development. 2000;127(3):595–603. 10631180
28. Sabatini S, Heidstra R, Wildwater M, Scheres B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes & Development. 2003;17(3):354–358.
29. Li C, Potuschak T, Colón-Carmona A, Gutiérrez RA, Doerner P. Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA. 2005;102(36):12978–12983. doi: 10.1073/pnas.0504039102 16123132
30. Hervé C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, et al. In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiology. 2009;149(3):1462–1477. doi: 10.1104/pp.108.126136 19091878
31. Shimotohno A, Heidstra R, Blilou I, Scheres B. Root stem cell niche organizer specification by molecular convergence of PLETHORA and SCARECROW transcription factor modules. Genes & Development. 2018;32(15–16):1085–1100.
32. Sieber P, Gheyselinck J, Gross-Hardt R, Laux T, Grossniklaus U, Schneitz K. Pattern formation during early ovule development in Arabidopsis thaliana. Developmental Biology. 2004;273(2):321–334. doi: 10.1016/j.ydbio.2004.05.037 15328016
33. Deyhle F, Sarkar A, Tucker E, Laux T. WUSCHEL regulates cell differentiation during anther development. Developmental Biology. 2007;302:154–159. doi: 10.1016/j.ydbio.2006.09.013 17027956
34. Zhang F, Tadege M. Repression of AS2 by WOX family transcription factors is required for leaf development in Medicago and Arabidopsis. Plant Signaling & Behavior. 2015;10(7):e993291.
35. Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema A, Gerats T. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. The Plant Cell. 2009;21:2269–2283. doi: 10.1105/tpc.109.065862 19717616
36. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Developmental Cell. 2008;14:867–876. doi: 10.1016/j.devcel.2008.03.008 18539115
37. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable P, Scanlon M. Tissue specificity and evolution of meristematic WOX3 function. Plant Physiology. 2009;149:841–850. doi: 10.1104/pp.108.130765 19073779
38. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ. WOX4 promotes procambial development. Plant Physiology. 2010;152(3):1346–1356. doi: 10.1104/pp.109.149641 20044450
39. Etchells JP, Provost CM, Mishra L, Turner SR. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development. 2013;140(10):2224–2234. doi: 10.1242/dev.091314 23578929
40. Zhu J, Shi H, Lee B, Damsz B, Cheng S, Stirm V, et al. An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci USA. 2004;101:9873–9878. doi: 10.1073/pnas.0403166101 15205481
41. Park S, Zheng Z, Oppenheimer D, Hauser B. The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeo domain protein that regulates ovule development. Development. 2005;132:841–849. doi: 10.1242/dev.01654 15659481
42. Kong D, Hao Y, Cui H. The WUSCHEL Related Homeobox protein WOX7 regulates the sugar response of lateral root development in Arabidopsis thaliana. Molecular Plant. 2016;9(2):261–270. doi: 10.1016/j.molp.2015.11.006 26621542
43. Ueda M, Zhang Z, Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Developmental Cell. 2011;20(2):264–270. doi: 10.1016/j.devcel.2011.01.009 21316593
44. Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, et al. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. The Plant Cell. 2014;26(3):1081–1093. doi: 10.1105/tpc.114.122887 24642937
45. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, et al. Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evolutionary Biology. 2008;8:291. doi: 10.1186/1471-2148-8-291 18950478
46. Nardmann J, Werr W. The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol Biol Evol. 2006;23:2492–2504. doi: 10.1093/molbev/msl125 16987950
47. van der Graaff E, Laux T, Rensing S. The WUS homeobox-containing (WOX) protein family. Genome Biology. 2009;10(12):248. doi: 10.1186/gb-2009-10-12-248 20067590
48. Katayama N, Koi S, Kato M. Expression of SHOOT MERISTEMLESS, WUSCHEL, and ASYMMETRIC LEAVES1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. The Plant Cell. 2010;22(7):2131–2140. doi: 10.1105/tpc.109.073189 20647344
49. Nardmann J, Werr W. Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytologist. 2013;199(4):1081–1092. doi: 10.1111/nph.12343 23721178
50. Harrison CJ, Morris JL. The origin and early evolution of vascular plant shoots and leaves. Philosophical Transactions of the Royal Society B: Biological Sciences. 2018;373(1739):20160496.
51. Chandler JW, Werr W. Histology versus phylogeny: Viewing plant embryogenesis from an evo-devo perspective. In: Grossniklaus U, editor. Current Topics in Developmental Biology. 131: Academic Press; 2019. p. 545–564. doi: 10.1016/bs.ctdb.2018.11.009 30612629
52. Hedman H, Zhu T, von Arnold S, Sohlberg J. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer Picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biology. 2013;13(1):89.
53. Lian G, Ding Z, Wang Q, Zhang D, Xu J. Origins and evolution of WUSCHEL-Related Homeobox protein family in plant kingdom. The Scientific World Journal. 2014;2014:12.
54. Segatto ALA, Thompson CE, Freitas LB. Molecular evolution analysis of WUSCHEL-related homeobox transcription factor family reveals functional divergence among clades in the homeobox region. Development Genes and Evolution. 2016;226(4):259–268. doi: 10.1007/s00427-016-0545-4 27150824
55. Alvarez JM, Bueno N, Cañas RA, Avila C, Cánovas FM, Ordás RJ. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in Pinus pinaster: New insights into the gene family evolution. Plant Physiology and Biochemistry. 2018;123:304–318. doi: 10.1016/j.plaphy.2017.12.031 29278847
56. Zeng M, Hu B, Li J, Zhang G, Ruan Y, Huang H, et al. Stem cell lineage in body layer specialization and vascular patterning of rice root and leaf. Science Bulletin. 2016;61(11):847–858.
57. Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M. Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. The Plant Cell. 2001;13(8):1959–1968. doi: 10.1105/TPC.010127 11487705
58. Paponov I, Teale W, Lang D, Paponov M, Reski R, Rensing S, et al. The evolution of nuclear auxin signalling. BMC Evoltionary Biology. 2009;9:126.
59. Szemenyei H, Hannon M, Long JA. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science. 2008;319(5868):1384–1386. doi: 10.1126/science.1151461 18258861
60. Zhang X, Zong J, Liu J, Yin J, Zhang D. Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. Journal of Integrative Plant Biology. 2010;52(11):1016–1026. doi: 10.1111/j.1744-7909.2010.00982.x 20977659
61. Edgar R. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004;32(5):1792–1797. doi: 10.1093/nar/gkh340 15034147
62. Liu W, Xu L. Recruitment of IC-WOX genes in root evolution. Trends in Plant Science. 2018;23(6):490–496. doi: 10.1016/j.tplants.2018.03.011 29680635
63. Su Y-H, Liu Y-B, Zhang X-S. Auxin–cytokinin interaction regulates meristem development. Molecular Plant. 2011;4(4):616–625. doi: 10.1093/mp/ssr007 21357646
64. Ulmasov T, Hagen G, Guilfoyle TJ. ARF1, a transcription factor that binds to auxin response elements. Science. 1997;276(5320):1865–1868. doi: 10.1126/science.276.5320.1865 9188533
65. Xu N, Hagen G, Guilfoyle T. Multiple auxin response modules in the soybean SAUR 15A promoter. Plant Science. 1997;126(2):193–201.
66. Tiwari SB, Hagen G, Guilfoyle T. The roles of auxin response factor domains in auxin-responsive transcription. The Plant Cell. 2003;15(2):533–543. doi: 10.1105/tpc.008417 12566590
67. Weiste C, Dröge-Laser W. The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nature Communications. 2014;5:3883. doi: 10.1038/ncomms4883 24861440
68. Bao Y, Dharmawardhana P, Arias R, Allen MB, Ma C, Strauss SH. WUS and STM-based reporter genes for studying meristem development in poplar. Plant Cell Rep. 2009;28(6):947–962. doi: 10.1007/s00299-009-0685-3 19280192
69. Zhao Y, Hu Y, Dai M, Huang L, Zhou D. The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. The Plant Cell. 2009;21:736–748. doi: 10.1105/tpc.108.061655 19258439
70. Cheng S, Huang Y, Zhu N, Zhao Y. The rice WUSCHEL-related homeobox genes are involved in reproductive organ development, hormone signaling and abiotic stress response. Gene. 2014;549(2):266–274. doi: 10.1016/j.gene.2014.08.003 25106855
71. Guan C, Wu B, Yu T, Wang Q, Krogan NT, Liu X, et al. Spatial auxin signaling controls leaf flattening in Arabidopsis. Current Biology. 2017;27(19):2940–2950. doi: 10.1016/j.cub.2017.08.042 28943086
72. Brackmann K, Qi J, Gebert M, Jouannet V, Schlamp T, Grünwald K, et al. Spatial specificity of auxin responses coordinates wood formation. Nature Communications. 2018;9(1):875. doi: 10.1038/s41467-018-03256-2 29491423
73. Sakai H, Aoyama T, Oka A. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. The Plant Journal. 2000;24(6):703–711. doi: 10.1046/j.1365-313x.2000.00909.x 11135105
74. Hosoda K, Imamura A, Katoh E, Hatta T, Tachiki M, Yamada H, et al. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response Regulators. The Plant Cell. 2002;14(9):2015–2029. doi: 10.1105/tpc.002733 12215502
75. Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A. ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant and Cell Physiology. 2007;48(2):263–277. doi: 10.1093/pcp/pcl063 17202182
76. Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, et al. Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. The Plant Cell. 2017;29(6):1357–1372. doi: 10.1105/tpc.16.00640 28576846
77. Zubo YO, Blakley IC, Yamburenko MV, Worthen JM, Street IH, Franco-Zorrilla JM, et al. Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proc Natl Acad Sci USA. 2017;114(29):E5995–E6004. doi: 10.1073/pnas.1620749114 28673986
78. Wang J, Tian C, Zhang C, Shi B, Cao X, Zhang T-Q, et al. Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. The Plant Cell. 2017;29(6):1373–1387. doi: 10.1105/tpc.16.00579 28576845
79. Xie M, Chen H, Huang L, O’Neil RC, Shokhirev MN, Ecker JR. A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. Nature Communications. 2018;9(1):1604. doi: 10.1038/s41467-018-03921-6 29686312
80. Li F-W, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M, Frangedakis E, et al. Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc Natl Acad Sci USA. 2014;111(18):6672–6677. doi: 10.1073/pnas.1319929111 24733898
81. Lyons E, Freeling M. How to usefully compare homologous plant genes and chromosomes as DNA sequences. The Plant Journal. 2008;53(4):661–673. doi: 10.1111/j.1365-313X.2007.03326.x 18269575
82. Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang HB, et al. Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiology. 2008;148(4):1772–1781. doi: 10.1104/pp.108.124867 18952863
83. Li F-W, Brouwer P, Carretero-Paulet L, Cheng S, de Vries J, Delaux P-M, et al. Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nature Plants. 2018;4(7):460–472. doi: 10.1038/s41477-018-0188-8 29967517
84. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10(1):1–9.
85. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications. 2014;5:3978. doi: 10.1038/ncomms4978 24865297
86. Mirarab S, Nguyen N, Warnow T. PASTA: Ultra-Large Multiple Sequence Alignment. In: Sharan R, editor. Research in Computational Molecular Biology: 18th Annual International Conference, RECOMB 2014, Pittsburgh, PA, USA, April 2–5, 2014, Proceedings. Cham: Springer International Publishing; 2014. p. 177–191.
87. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033 24451623
88. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27(8):1164–1165. doi: 10.1093/bioinformatics/btr088 21335321
89. Miller MA, Pfeitter W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE). 2010:1–8.
90. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings International Conference on Intelligent Systems for Molecular Biology. 1994;2:28–36.
91. Tang H, Bomhoff MD, Briones E, Zhang L, Schnable JC, Lyons E. SynFind: compiling syntenic regions across any set of genomes on demand. Genome Biology and Evolution. 2015;7(12):3286–3298. doi: 10.1093/gbe/evv219 26560340
92. Chow C-N, Zheng H-Q, Wu N-Y, Chien C-H, Huang H-D, Lee T-Y, et al. PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Research. 2016;44(D1):D1154–D1160. doi: 10.1093/nar/gkv1035 26476450
93. Ge Y, Liu J, Zeng M, He J, Qin P, Huang H, et al. Identification of WOX family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes. Frontiers in Plant Science. 2016;7:93. doi: 10.3389/fpls.2016.00093 26904063
94. Mirarab S, Nguyen N, Guo S, Wang L-S, Kim J, Warnow T. PASTA: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. Journal of Computational Biology. 2015;22(5):377–386. doi: 10.1089/cmb.2014.0156 25549288
95. Mukherjee K, Brocchieri L, Bürglin TR. A comprehensive classification and evolutionary analysis of plant homeobox genes. Molecular Biology and Evolution. 2009;26(12):2775–2794. doi: 10.1093/molbev/msp201 19734295
96. Jiao YN, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011;473(7345):97–100. doi: 10.1038/nature09916 21478875
97. Li Z, Baniaga AE, Sessa EB, Scascitelli M, Graham SW, Rieseberg LH, et al. Early genome duplications in conifers and other seed plants. Science Advances. 2015;1(10):e1501084. doi: 10.1126/sciadv.1501084 26702445
98. Barker MS. Evolutionary genomic analyses of ferns reveal that high chromosome numbers are a product of high retention and fewer rounds of polyploidy relative to angiosperms. American Fern Journal. 2009;99(2):136–141.
99. Vanneste K, Sterck L, Myburg Z, Van de Peer Y, Mizrachi E. Horsetails are ancient polyploids: evidence from Equisetum giganteum. The Plant Cell. 2015;27:1567–1578. doi: 10.1105/tpc.15.00157 26002871
100. Sessa EB, Der JP. Chapter Seven—Evolutionary Genomics of Ferns and Lycophytes. In: Stefan AR, editor. Advances in Botanical Research. 78: Academic Press; 2016. p. 215–254.
101. PPG_I. A community-derived classification for extant lycophytes and ferns. J Syst Evol. 2016;54(6):563–603.
102. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. Bmc Evolutionary Biology. 2014;14(1):1–27.
103. Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS, Soltis DE, et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society. 2016;181(1):1–20.
104. Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes & Development. 2011;25(19):2025–2030.
105. Tian H, Wabnik K, Niu T, Li H, Yu Q, Pollmann S, et al. WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Molecular Plant. 2014;7(2):277–289. doi: 10.1093/mp/sst118 23939433
106. Han P, Li Q, Zhu Y-X. Mutation of Arabidopsis BARD1 causes eeristem defects by failing to confine WUSCHEL expression to the organizing center. The Plant Cell. 2008;20(6):1482–1493. doi: 10.1105/tpc.108.058867 18591352
107. Han P, Zhu Y-X. BARD1 may be renamed ROW1 because it functions mainly as a REPRESSOR OF WUSCHEL1. Plant Signaling & Behavior. 2009;4(1):52–54.
108. Zhang Y, Jiao Y, Liu Z, Zhu Y-X. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nature Communications. 2015;6:6003. doi: 10.1038/ncomms7003 25631790
109. Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, et al. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature. 2015;517(7534):377–380. doi: 10.1038/nature13853 25363783
110. Kramer E. A stranger in a strange land: the utility and interpretation of heterologous expression. Frontiers in Plant Science. 2015;6:734. doi: 10.3389/fpls.2015.00734 26442047
111. Magallón S, Hilu KW, Quandt D. Land plant evolutionary timeline: Gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany. 2013;100(3):556–573. doi: 10.3732/ajb.1200416 23445823
112. Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist. 2015;207(2):437–453. doi: 10.1111/nph.13264 25615647
113. Hu X, Xu L. Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiology. 2016;172(4):2363–2373. doi: 10.1104/pp.16.01067 27784768
114. Santner A, Estelle M. Recent advances and emerging trends in plant hormone signalling. Nature. 2009;459(7250):1071–1078. doi: 10.1038/nature08122 19553990
115. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA. 2009;106(38):16529–16234. doi: 10.1073/pnas.0908122106 19717465
116. Buechel S, Leibfried A, To JPC, Zhao Z, Andersen SU, Kieber JJ, et al. Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. European Journal of Cell Biology. 2010;89(2):279–284.
117. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, et al. Hormonal control of the shoot stem-cell niche. Nature. 2010;465:1089–1092. doi: 10.1038/nature09126 20577215
118. Pils B, Heyl A. Unraveling the evolution of cytokinin signaling. Plant Physiology. 2009;151(2):782–791. doi: 10.1104/pp.109.139188 19675156
119. Gruhn N, Halawa M, Snel B, Seidl MF, Heyl A. A subfamily of putative cytokinin receptors Is revealed by an analysis of the evolution of the two-component signaling system of plants. Plant Physiology. 2014;165(1):227–237. doi: 10.1104/pp.113.228080 24520157
120. Wang C, Liu Y, Li S-S, Han G-Z. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiology. 2015;167(3):872–886. doi: 10.1104/pp.114.247403 25560880
121. Mutte SK, Kato H, Rothfels C, Melkonian M, Wong GK-S, Weijers D. Origin and evolution of the nuclear auxin response system. eLife. 2018;7:e33399. doi: 10.7554/eLife.33399 29580381
122. De Smet I, Voß U, Lau S, Wilson M, Shao N, Timme RE, et al. Unraveling the evolution of auxin signaling. Plant Physiology. 2011;155(1):209–221. doi: 10.1104/pp.110.168161 21081694
123. Rensing S, Lang D, Zimmer A, Terry A, Salamov A, Shapiro H, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science. 2008;319(5859):64–69. doi: 10.1126/science.1150646 18079367
124. Ma Y, Miotk A, Sutikovic Z, Medzihradszky A, Wenzl C, Ermakova O, et al. WUSCHEL acts as a rheostat on the auxin pathway to maintain apical stem cells in Arabidopsis. bioRxiv. 2018:468421.
125. Leibfried A, To J, Busch W, Stehling S, Kehle A, Demar M, et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature. 2005;438:1172–1175. doi: 10.1038/nature04270 16372013
Článek vyšel v časopise
PLOS One
2019 Číslo 10
- Tisícileté topoly, mokří psi, stárnoucí kočky a ospalé octomilky – „jednohubky“ z výzkumu 2024/41
- Jaké jsou aktuální trendy v léčbě karcinomu slinivky?
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Menstruační krev má značný diagnostický potenciál, mimo jiné u diabetu
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
Nejčtenější v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy