Lotus japonicus karrikin receptors display divergent ligand-binding specificities and organ-dependent redundancy
Autoři:
Samy Carbonnel aff001; Salar Torabi aff001; Maximilian Griesmann aff001; Elias Bleek aff001; Yuhong Tang aff003; Stefan Buchka aff001; Veronica Basso aff001; Mitsuru Shindo aff004; François-Didier Boyer aff005; Trevor L. Wang aff006; Michael Udvardi aff003; Mark T. Waters aff007; Caroline Gutjahr aff001
Působiště autorů:
LMU Munich, Faculty of Biology, Genetics, Biocenter Martinsried, Martinsried, Germany
aff001; Technical University of Munich (TUM), TUM School of Life Sciences, Plant Genetics, Freising, Germany
aff002; Noble Research Institute, Ardmore, Oklahoma, United States of America
aff003; Institute for Materials Chemistry and Engineering, Kyushu University, Kasuga, Fukuoka, Japan
aff004; Université Paris-Saclay, CNRS, Institut de Chimie des Substances Naturelles, Gif-sur-Yvette, France
aff005; John Innes Centre, Norwich Research Park, Norwich, United Kingdom
aff006; School of Molecular Sciences, The University of Western Australia, Perth, Australia
aff007; Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia
aff008
Vyšlo v časopise:
Lotus japonicus karrikin receptors display divergent ligand-binding specificities and organ-dependent redundancy. PLoS Genet 16(12): e1009249. doi:10.1371/journal.pgen.1009249
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009249
Souhrn
Karrikins (KARs), smoke-derived butenolides, are perceived by the α/β-fold hydrolase KARRIKIN INSENSITIVE2 (KAI2) and thought to mimic endogenous, yet elusive plant hormones tentatively called KAI2-ligands (KLs). The sensitivity to different karrikin types as well as the number of KAI2 paralogs varies among plant species, suggesting diversification and co-evolution of ligand-receptor relationships. We found that the genomes of legumes, comprising a number of important crops with protein-rich, nutritious seed, contain two or more KAI2 copies. We uncover sub-functionalization of the two KAI2 versions in the model legume Lotus japonicus and demonstrate differences in their ability to bind the synthetic ligand GR24ent-5DS in vitro and in genetic assays with Lotus japonicus and the heterologous Arabidopsis thaliana background. These differences can be explained by the exchange of a widely conserved phenylalanine in the binding pocket of KAI2a with a tryptophan in KAI2b, which arose independently in KAI2 proteins of several unrelated angiosperms. Furthermore, two polymorphic residues in the binding pocket are conserved across a number of legumes and may contribute to ligand binding preferences. The diversification of KAI2 binding pockets suggests the occurrence of several different KLs acting in non-fire following plants, or an escape from possible antagonistic exogenous molecules. Unexpectedly, L. japonicus responds to diverse synthetic KAI2-ligands in an organ-specific manner. Hypocotyl growth responds to KAR1, KAR2 and rac-GR24, while root system development responds only to KAR1. This differential responsiveness cannot be explained by receptor-ligand preferences alone, because LjKAI2a is sufficient for karrikin responses in the hypocotyl, while LjKAI2a and LjKAI2b operate redundantly in roots. Instead, it likely reflects differences between plant organs in their ability to transport or metabolise the synthetic KLs. Our findings provide new insights into the evolution and diversity of butenolide ligand-receptor relationships, and open novel research avenues into their ecological significance and the mechanisms controlling developmental responses to divergent KLs.
Klíčová slova:
Arabidopsis thaliana – Flowering plants – Hypocotyl – Legumes – Plant genomics – Rice – Seed germination – Tryptophan
Zdroje
1. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD. A compound from smoke that promotes seed germination. Science. 2004;305(5686):977. doi: 10.1126/science.1099944 15247439
2. Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, et al. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 2009;149(2):863–73. doi: 10.1104/pp.108.131516 19074625
3. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, et al. F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2011;108(21):8897–902. doi: 10.1073/pnas.1100987108 21555559
4. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, et al. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 2012;139(7):1285–95. doi: 10.1242/dev.074567 22357928
5. Guo Y, Zheng Z, La Clair JJ, Chory J, Noel JP. Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. Proc Natl Acad Sci U S A. 2013;110(20):8284–9. doi: 10.1073/pnas.1306265110 23613584
6. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, et al. Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells. 2013;18(2):147–60. Epub 2013/01/11. doi: 10.1111/gtc.12025 23301669
7. Zheng J, Hong K, Zeng L, Wang L, Kang S, Qu M, et al. Karrikin signaling acts parallel to and additively with strigolactone signaling to regulate rice mesocotyl elongation in darkness. Plant Cell. 2020. Epub 2020/07/16. doi: 10.1105/tpc.20.00123 32665307
8. Khosla A, Morffy N, Li Q, Faure L, Chang SH, Yao J, et al. Structure-function analysis of SMAX1 reveals domains that mediate its karrikin-induced proteolysis and interaction with the receptor KAI2. Plant Cell. 2020;32(8):2639–59. Epub 2020/05/22. doi: 10.1105/tpc.19.00752 32434855
9. Toh S, Holbrook-Smith D, Stokes ME, Tsuchiya Y, McCourt P. Detection of parasitic plant suicide germination compounds using a high-Throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem & Biol. 2014;21(9):1253. doi: 10.1016/j.chembiol.2014.07.005 25126711
10. Hrdlička J, Gucký T, Novák O, Kulkarni M, Gupta S, van Staden J, et al. Quantification of karrikins in smoke water using ultra-high performance liquid chromatography–tandem mass spectrometry. Plant Methods. 2019;15(1):81. doi: 10.1186/s13007-019-0467-z 31372177
11. Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol. 2012;63:107–30. Epub 2012/03/13. doi: 10.1146/annurev-arplant-042811-105545 22404467
12. Conn CE, Nelson DC. Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front Plant Sci. 2016;6:1219. Epub 2016/01/19. doi: 10.3389/fpls.2015.01219 26779242
13. Li W, Nguyen KH, Chu HD, Ha CV, Watanabe Y, Osakabe Y, et al. The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana. PLoS Genet. 2017;13(11):e1007076. Epub 2017/11/14. doi: 10.1371/journal.pgen.1007076 29131815
14. Swarbreck SM, Guerringue Y, Matthus E, Jamieson FJC, Davies JM. Impairment in karrikin but not strigolactone sensing enhances root skewing in Arabidopsis thaliana. Plant J. 2019;(98):607–21. Epub 2019/01/20. doi: 10.1111/tpj.14233 30659713
15. Villaecija Aguilar JA, Hamon-Josse M, Carbonnel S, kretschmar A, Schmid C, Dawid C, et al. SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signaling in Arabidopsis. PLoS Genet. 2019;15(8):1–27. doi: 10.1371/journal.pgen.1008327 31465451
16. Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG, Summers W, et al. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science. 2015;350(6267):1521–4. doi: 10.1126/science.aac9715 26680197
17. Choi J, Lee T, Cho J, Servante EK, Pucker B, Summers W, et al. The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice. Nat Commun. 2020;11(1):2114. Epub 2020/05/02. doi: 10.1038/s41467-020-16021-1 32355217
18. Sun YK, Flematti GR, Smith SM, Waters MT. Reporter gene-facilitated detection of compounds in Arabidopsis leaf extracts that activate the karrikin signaling pathway. Front Plant Sci. 2016;7:1799. Epub 2016/12/21. doi: 10.3389/fpls.2016.01799 27994609
19. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science. 1966;154(3753):1189–90. doi: 10.1126/science.154.3753.1189 17780042
20. Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005;435(7043):824–7. doi: 10.1038/nature03608 15944706
21. Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 2006;4(7):e226. Epub 2006/06/22. doi: 10.1371/journal.pbio.0040226 16787107
22. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, et al. Strigolactone inhibition of shoot branching. Nature. 2008;455(7210):189–94. doi: 10.1038/nature07271 18690209
23. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature. 2008;455(7210):195–200. doi: 10.1038/nature07272 18690207
24. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A. 2011;108(50):20242–7. Epub 2011/11/30. doi: 10.1073/pnas.1111902108 22123958
25. Swarbreck SM, Mohammad-Sidik A, Davies JM. Common components of the strigolactone and karrikin signaling pathways suppress root branching in Arabidopsis thaliana. Plant Physiol. 2020. Epub 2020/07/22. doi: 10.1104/pp.19.00687 32690756
26. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, et al. DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 2012;22(21):2032–6. Epub 2012/09/11. doi: 10.1016/j.cub.2012.08.007 22959345
27. Waters MT, Scaffidi A, Flematti GR, Smith SM. Substrate-induced degradation of the alpha/beta-fold hydrolase KARRIKIN INSENSITIVE2 requires a functional catalytic triad but is independent of MAX2. Mol Plant. 2015;8(5):814–7. doi: 10.1016/j.molp.2014.12.020 25698586
28. Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell. 2015;27(11):3143–59. doi: 10.1105/tpc.15.00562 26546447
29. Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z, et al. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-Like SMXL repressor proteins for ubiquitination and degradation. Plant Cell. 2015;27(11):3128–42. doi: 10.1105/tpc.15.00605 26546446
30. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, et al. D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signaling. Nature. 2013;504(7480):406–10. doi: 10.1038/nature12878 24336215
31. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, et al. DWARF 53 acts as a repressor of strigolactone signaling in rice. Nature. 2013;504(7480):401–5. doi: 10.1038/nature12870 24336200
32. Bythell-Douglas R, Rothfels CJ, Stevenson DWD, Graham SW, Wong GK, Nelson DC, et al. Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues. BMC Biol. 2017;15(1):52. doi: 10.1186/s12915-017-0397-z 28662667
33. Végh A, Incze N, Fábián A, Huo H, Bradford KJ, Balázs E, et al. Comprehensive analysis of DWARF14-LIKE2 (DLK2) reveals its functional divergence from strigolactone-related paralogs. Front Plant Sci. 2017;8(1641):1–14. doi: 10.3389/fpls.2017.01641 28970845
34. Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM. A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell. 2015;27(7):1925–44. doi: 10.1105/tpc.15.00146 26175507
35. Waters MT, Gutjahr C, Bennett T, Nelson DC. Strigolactone signaling and evolution. Annu Rev Plant Biol. 2017;68:291–322. doi: 10.1146/annurev-arplant-042916-040925 28125281
36. Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, et al. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol. 2008;178(4):863–74. Epub 2008/03/19. doi: 10.1111/j.1469-8137.2008.02406.x 18346111
37. Bürger M, Mashiguchi K, Lee HJ, Nakano M, Takemoto K, Seto Y, et al. Structural basis of karrikin and non-natural strigolactone perception in Physcomitrella patens. Cell Rep. 2019;26(4):855–65. doi: 10.1016/j.celrep.2019.01.003 30673608
38. Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, et al. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science. 2015;349(6247):540–3. doi: 10.1126/science.aab1140 26228149
39. Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenko O, Lumba S, Tsuchiya Y, et al. Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science. 2015;350(6257):203–7. Epub 2015/10/10. doi: 10.1126/science.aac9476 26450211
40. Sun YK, Yao J, Scaffidi A, Melville KT, Davies SF, Bond CS, et al. Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds. Nat Commun. 2020;11(1):1264. Epub 2020/03/11. doi: 10.1038/s41467-020-14991-w 32152287
41. Wojciechowski MF, Lavin M, Sanderson MJ. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. American J Bot. 2004;91(11):1846–62. doi: 10.3732/ajb.91.11.1846 21652332
42. Shen H, Luong P, Huq E. The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 2007;145(4):1471–83. doi: 10.1104/pp.107.107227 17951458
43. Stirnberg P, Furner IJ, Ottoline Leyser HM. MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 2007;50(1):80–94. doi: 10.1111/j.1365-313X.2007.03032.x 17346265
44. Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM. Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2010;107(15):7095–100. doi: 10.1073/pnas.0911635107 20351290
45. Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, et al. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 2014;165(3):1221–32. doi: 10.1104/pp.114.240036 24808100
46. Wang L, Xu Q, Yu H, Ma H, Li X, Yang J, et al. Strigolactone and karrikin signaling pathways elicit ubiquitination and proteolysis of SMXL2 to regulate hypocotyl elongation in Arabidopsis. Plant Cell. 2020;32(7):2251–70. Epub 2020/05/03. doi: 10.1105/tpc.20.00140 32358074
47. Yao J, Mashiguchi K, Scaffidi A, Akatsu T, Melville KT, Morita R, et al. An allelic series at the KARRIKIN INSENSITIVE 2 locus of Arabidopsis thaliana decouples ligand hydrolysis and receptor degradation from downstream signaling. Plant J. 2018;96(1):75–89. Epub 2018/07/10. doi: 10.1111/tpj.14017 29982999
48. Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, et al. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci U S A. 2014;111(50):18084–9. Epub 2014/11/27. doi: 10.1073/pnas.1410801111 25425668
49. de Saint Germain A, Retailleau P, Norsikian S, Servajean V, Pelissier F, Steinmetz V, et al. Contalactone, a contaminant formed during chemical synthesis of the strigolactone reference GR24 is also a strigolactone mimic. Phytochemistry. 2019;168:112112. Epub 2019/09/10. doi: 10.1016/j.phytochem.2019.112112 31499274
50. Seto Y, Yasui R, Kameoka H, Tamiru M, Cao M, Terauchi R, et al. Strigolactone perception and deactivation by a hydrolase receptor DWARF14. Nat Commun. 2019;10(1):191. Epub 2019/01/16. doi: 10.1038/s41467-018-08124-7 30643123
51. Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA, Graham SW, et al. One thousand plant transcriptomes and the phylogenomics of green plants. Nature. 2019;574(7780):679–85. doi: 10.1038/s41586-019-1693-2 31645766
52. Malolepszy A, Mun T, Sandal N, Gupta V, Dubin M, Urbanski D, et al. The LORE1 insertion mutant resource. Plant J. 2016;88(2):306–17. doi: 10.1111/tpj.13243 27322352
53. Fukai E, Soyano T, Umehara Y, Nakayama S, Hirakawa H, Tabata S, et al. Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J. 2012;69(4):720–30. doi: 10.1111/j.1365-313X.2011.04826.x 22014259
54. Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, Yoshida S, et al. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol. 2003;131(3):866–71. doi: 10.1104/pp.102.017384 12644638
55. Beveridge CA, Ross JJ, Murfet IC. Branching in pea (action of genes Rms3 and Rms4). Plant Physiol. 1996;110(3):859–65. doi: 10.1104/pp.110.3.859 12226224
56. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J. Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 2005;46(1):79–86. doi: 10.1093/pcp/pci022 15659436
57. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, et al. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol. 2011;155(2):721–34. doi: 10.1104/pp.110.166645 21119044
58. Jiang L, Matthys C, Marquez-Garcia B, De Cuyper C, Smet L, De Keyser A, et al. Strigolactones spatially influence lateral root development through the cytokinin signaling network. J Exp Bot. 2016;67(1):379–89. doi: 10.1093/jxb/erv478 26519957
59. De Cuyper C, Fromentin J, Yocgo RE, De Keyser A, Guillotin B, Kunert K, et al. From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J Exp Bot. 2015;66(1):137–46. doi: 10.1093/jxb/eru404 25371499
60. Halouzka R, Tarkowski P, Zwanenburg B, Cavar Zeljkovic S. Stability of strigolactone analog GR24 toward nucleophiles. Pest Manag Sci. 2018;74(4):896–904. doi: 10.1002/ps.4782 29095562
61. Mayzlish-Gati E, LekKala SP, Resnick N, Wininger S, Bhattacharya C, Lemcoff JH, et al. Strigolactones are positive regulators of light-harvesting genes in tomato. J Exp Bot. 2010;61(11):3129–36. doi: 10.1093/jxb/erq138 20501744
62. Mashiguchi K, Sasaki E, Shimada Y, Nagae M, Ueno K, Nakano T, et al. Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci Biotechnol Biochem. 2009;73(11):2460–5. doi: 10.1271/bbb.90443 19897913
63. Wong MML, Vaillancourt RE, Freeman JS, Hudson CJ, Bakker FT, Cannon CH, et al. Novel insights into karyotype evolution and whole genome duplications in legumes. BioRxiv 099044; 2017.
64. Zhao L, Zhou XE, Wu Z, Yi W, Xu Y, Li S, et al. Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell research. 2013;23(3):436–9. Epub 2013/02/05. doi: 10.1038/cr.2013.19 23381136
65. Xu Y, Miyakawa T, Nakamura H, Nakamura A, Imamura Y, Asami T, et al. Structural basis of unique ligand specificity of KAI2-like protein from parasitic weed Striga hermonthica. Scientific reports. 2016;6:31386–. doi: 10.1038/srep31386 27507097
66. Carbonnel S, Das D, Varshney K, Kolodziej MC, Villaécija-Aguilar JA, Gutjahr C. The karrikin signaling regulator SMAX1 controls Lotus japonicus root and root hair development by suppressing ethylene biosynthesis. Proc Natl Acad Sci USA. 2020:117(35):21757–21765. doi: 10.1073/pnas.2006111117 32817510
67. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, et al. Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol. 2012;160(3):1329–41. doi: 10.1104/pp.112.202358 22968830
68. Madmon O, Mazuz M, Kumari P, Dam A, Ion A, Mayzlish-Gati E, et al. Expression of MAX2 under SCARECROW promoter enhances the strigolactone/MAX2 dependent response of Arabidopsis roots to low-phosphate conditions. Planta. 2016;243(6):1419–27. Epub 2016/02/28. doi: 10.1007/s00425-016-2477-7 26919985
69. Sun X, Ni M. HYPOSENSITIVE TO LIGHT, an alpha/beta fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol Plant. 2011;4(1):116–26. doi: 10.1093/mp/ssq055 20864454
70. Urbański DF, Małolepszy A, Stougaard J, Andersen SU. Genome-wide LORE1 retrotransposon mutagenesis and high-throughput insertion detection in Lotus japonicus. Plant J. 2012;69(4):731–41. doi: 10.1111/j.1365-313X.2011.04827.x 22014280
71. Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V, Bohmer MJ, et al. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr Biol. 2016;26(8):987–98. doi: 10.1016/j.cub.2016.01.069 27020747
72. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. Epub 2018/05/04. doi: 10.1093/molbev/msy096 29722887
73. Trifinopoulos J, Nguyen L, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research. 2016;44(W1):W232–W5. doi: 10.1093/nar/gkw256 27084950
74. Singh S, Katzer K, Lambert J, Cerri M, Parniske M. CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host & Microbe. 2014;15(2):139–52. doi: 10.1016/j.chom.2014.01.011 24528861
75. Bayle V, Nussaume L, Bhat RA. Combination of novel green fluorescent protein mutant TSapphire and DsRed variant mOrange to set up a versatile in planta FRET-FLIM assay. Plant Physiol. 2008;148(1):51–60. doi: 10.1104/pp.108.117358 18621983
76. Binder A, Lambert J, Morbitzer R, Popp C, Ott T, Lahaye T, et al. A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLoS One. 2014;9(2):1–14. doi: 10.1371/journal.pone.0088218 24551083
77. Matsuo K, Shindo M. Efficient synthesis of karrikinolide via Cu(II)-catalyzed lactonization. Tetrahedron. 2011;67(5):971–5. doi: 10.1016/j.tet.2010.11.108
78. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotides array probe level data. Biostatistics. 2003;4(2):249–64. doi: 10.1093/biostatistics/4.2.249 %J Biostatistics. 12925520
79. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5(10):R80–R. Epub 2004/09/15. doi: 10.1186/gb-2004-5-10-r80 15461798
80. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy—analysis of Affymetrix GeneChip data at the probe level. Bioinfo. 2004;20(3):307–15. doi: 10.1093/bioinformatics/btg405%J Bioinformatics. 14960456
81. Smyth GK. limma: Linear Models for Microarray Data. In: Gentleman RC, Carey VJ, Huber W, Irizarry RA, Dudoit S, editors. Bioinformatics and computational biology solutions using R and Bioconductor. New York, NY: Springer New York; 2005. p. 397–420.
82. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statist Appl Genet Mol Biol. 2004;3(1):1–26. Epub 2006/05/02. doi: 10.2202/1544-6115.1027 16646809
83. Czechowski T, Bari RP, Stitt M, Scheible W, Udvardi MK. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J. 2004;38(2):366–79. doi: 10.1111/j.1365-313X.2004.02051.x 15078338
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 12
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Exploiting codon usage identifies intensity-specific modifiers of Ras/MAPK signaling in vivo
- Common maternal and fetal genetic variants show expected polygenic effects on risk of small- or large-for-gestational-age (SGA or LGA), except in the smallest 3% of babies
- PEA15 loss of function and defective cerebral development in the domestic cat
- Precision medicine in cats—The right biomedical model may not be the mouse!
