An integrated analysis of cell-type specific gene expression reveals genes regulated by REVOLUTA and KANADI1 in the Arabidopsis shoot apical meristem

English version

Autoři: Hasthi Ram ^aff001; Sudeep Sahadevan ^aff001; Nittaya Gale ^aff003; Monica Pia Caggiano ^aff001; Xiulian Yu ^aff001; Carolyn Ohno ^aff001; Marcus G. Heisler ^aff001
Působiště autorů: European Molecular Biology Laboratory, Meyerhofstrasse, Heidelberg, Germany ^aff001; National Agri-Food Biotechnology Institute, SAS Nagar, Mohali, Punjab, India ^aff002; School of Life and Environmental Sciences, University of Sydney, NSW, Australia ^aff003
Vyšlo v časopise: An integrated analysis of cell-type specific gene expression reveals genes regulated by REVOLUTA and KANADI1 in the Arabidopsis shoot apical meristem. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008661
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008661

Souhrn

In the Arabidopsis thaliana shoot apical meristem (SAM) the expression domains of Class III Homeodomain Leucine Zipper (HD-ZIPIII) and KANADI (KAN) genes are separated by a narrow boundary region from which new organs are initiated. Disruption of this boundary through either loss of function or ectopic expression of HD-ZIPIII and KAN causes ectopic or suppression of organ formation respectively, raising the question of how these transcription factors regulate organogenesis at a molecular level. In this study we develop a multi-channel FACS/RNA-seq approach to characterize global patterns of gene expression across the HD-ZIPIII-KAN1 SAM boundary. We then combine FACS, RNA-seq and perturbations of HD-ZIPIII and KAN expression to identify genes that are both responsive to REV and KAN1 and normally expressed in patterns that correlate with REV and KAN1. Our data reveal that a significant number of genes responsive to REV are regulated in opposite ways depending on time after induction, with genes associated with auxin response and synthesis upregulated initially, but later repressed. We also characterize the cell type specific expression patterns of auxin responsive genes and identify a set of genes involved in organogenesis repressed by both REV and KAN1.

Klíčová slova:

Auxins – Cytokinins – Epidermis – Gene expression – Gene ontologies – Gene regulation – Organogenesis – Meristems

Zdroje

1. Reinhardt D, Mandel T, Kuhlemeier C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell. 2000;12(4):507–18. doi: 10.1105/tpc.12.4.507 10760240

2. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, et al. Regulation of phyllotaxis by polar auxin transport. Nature. 2003;426(6964):255–60. doi: 10.1038/nature02081 14628043

3. Bhatia N, Bozorg B, Larsson A, Ohno C, Jonsson H, Heisler MG. Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis. Curr Biol. 2016;26(23):3202–8. doi: 10.1016/j.cub.2016.09.044 27818174

4. Caggiano MP, Yu X, Bhatia N, Larsson A, Ram H, Ohno CK, et al. Cell type boundaries organize plant development. eLife. 2017;6. doi: 10.7554/eLife.27421 28895530

5. Pekker I, Alvarez JP, Eshed Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell. 2005;17(11):2899–910. ISI:000232991700007 doi: 10.1105/tpc.105.034876 16199616

6. Guan C, Wu B, Yu T, Wang Q, Krogan NT, Liu X, et al. Spatial Auxin Signaling Controls Leaf Flattening in Arabidopsis. Curr Biol. 2017;27(19):2940–50 e4. doi: 10.1016/j.cub.2017.08.042 28943086

7. de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C, et al. Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci U S A. 2006;103(5):1627–32. doi: 10.1073/pnas.0510130103 16432202

8. Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P. A plausible model of phyllotaxis. Proc Natl Acad Sci U S A. 2006;103(5):1301–6. doi: 10.1073/pnas.0510457103 16432192

9. Merelo P, Xie Y, Brand L, Ott F, Weigel D, Bowman JL, et al. Genome-Wide Identification of KANADI1 Target Genes. Plos One. 2013;8(10). WOS:000325887300080

10. Huang T, Harrar Y, Lin C, Reinhart B, Newell NR, Talavera-Rauh F, et al. Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell. 2014;26(1):246–62. doi: 10.1105/tpc.113.111526 24464295

11. Izhaki A, Bowman JL. KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell. 2007;19(2):495–508. doi: 10.1105/tpc.106.047472 17307928

12. Reinhart BJ, Liu T, Newell NR, Magnani E, Huang T, Kerstetter R, et al. Establishing a framework for the Ad/abaxial regulatory network of Arabidopsis: ascertaining targets of class III homeodomain leucine zipper and KANADI regulation. Plant Cell. 2013;25(9):3228–49. doi: 10.1105/tpc.113.111518 24076978

13. Xie Y, Straub D, Eguen T, Brandt R, Stahl M, Martinez-Garcia JF, et al. Meta-Analysis of Arabidopsis KANADI1 Direct Target Genes Identifies a Basic Growth-Promoting Module Acting Upstream of Hormonal Signaling Pathways. Plant Physiol. 2015;169(2):1240–53. doi: 10.1104/pp.15.00764 26246448

14. Brandt R, Salla-Martret M, Bou-Torrent J, Musielak T, Stahl M, Lanz C, et al. Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J. 2012;72(1):31–42. doi: 10.1111/j.1365-313X.2012.05049.x 22578006

15. Mustroph A, Zanetti ME, Jang CJ, Holtan HE, Repetti PP, Galbraith DW, et al. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A. 2009;106(44):18843–8. doi: 10.1073/pnas.0906131106 19843695

16. Deal RB, Henikoff S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell. 2010;18(6):1030–40. doi: 10.1016/j.devcel.2010.05.013 20627084

17. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, et al. A gene expression map of the Arabidopsis root. Science. 2003;302(5652):1956–60. doi: 10.1126/science.1090022 14671301

18. Yadav RK, Tavakkoli M, Xie M, Girke T, Reddy GV. A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche. Development. 2014;141(13):2735–44. doi: 10.1242/dev.106104 24961803

19. Sessions A, Weigel D, Yanofsky MF. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 1999;20(2):259–63. doi: 10.1046/j.1365-313x.1999.00594.x 10571886

20. Subach OM, Gundorov IS, Yoshimura M, Subach FV, Zhang J, Gruenwald D, et al. Conversion of red fluorescent protein into a bright blue probe. Chem Biol. 2008;15(10):1116–24. doi: 10.1016/j.chembiol.2008.08.006 18940671

21. Yadav RK, Girke T, Pasala S, Xie M, Reddy GV. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci U S A. 2009;106(12):4941–6. doi: 10.1073/pnas.0900843106 19258454

22. Samalova M, Brzobohaty B, Moore I. pOp6/LhGR: a stringently regulated and highly responsive dexamethasone-inducible gene expression system for tobacco. Plant J. 2005;41(6):919–35. ISI:000227350700010 doi: 10.1111/j.1365-313X.2005.02341.x 15743454

23. Gardiner J, Sherr I, Scarpella E. Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol. 2010;54(8–9):1389–96. doi: 10.1387/ijdb.093006jg 20563990

24. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science. 2009;323(5910):95–101. doi: 10.1126/science.1164627 19095898

25. Wang B, Chu J, Yu T, Xu Q, Sun X, Yuan J, et al. Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. Proc Natl Acad Sci U S A. 2015;112(15):4821–6. doi: 10.1073/pnas.1503998112 25831515

26. Wenkel S, Emery J, Hou BH, Evans MM, Barton MK. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell. 2007;19(11):3379–90. doi: 10.1105/tpc.107.055772 18055602

27. Wu G, Lin WC, Huang T, Poethig RS, Springer PS, Kerstetter RA. KANADI1 regulates adaxial-abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2. Proc Natl Acad Sci USA. 2008;105(42):16392–7. doi: 10.1073/pnas.0803997105 18849474

28. Merelo P, Ram H, Pia Caggiano M, Ohno C, Ott F, Straub D, et al. Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proc Natl Acad Sci U S A. 2016. doi: 10.1073/pnas.1516110113 27698117

29. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development. 1999;126(18):4117–28. 10457020

30. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, et al. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 2005;17(2):616–27. ISI:000227043800022 doi: 10.1105/tpc.104.026690 15659623

31. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100(6):635–44. doi: 10.1016/s0092-8674(00)80700-x 10761929

32. Strabala TJ, O'Donnell P J, Smit AM, Ampomah-Dwamena C, Martin EJ, Netzler N, et al. Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol. 2006;140(4):1331–44. doi: 10.1104/pp.105.075515 16489133

33. Skylar A, Hong F, Chory J, Weigel D, Wu X. STIMPY mediates cytokinin signaling during shoot meristem establishment in Arabidopsis seedlings. Development. 2010;137(4):541–9. doi: 10.1242/dev.041426 20110319

34. Serikawa KA, Martinez-Laborda A, Zambryski P. Three knotted1-like homeobox genes in Arabidopsis. Plant Mol Biol. 1996;32(4):673–83. doi: 10.1007/bf00020208 8980519

35. Zhou Y, Honda M, Zhu H, Zhang Z, Guo X, Li T, et al. Spatiotemporal sequestration of miR165/166 by Arabidopsis Argonaute10 promotes shoot apical meristem maintenance. Cell Rep. 2015;10(11):1819–27. doi: 10.1016/j.celrep.2015.02.047 25801022

36. Lee DK, Geisler M, Springer PS. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development. 2009;136(14):2423–32. doi: 10.1242/dev.031971 19542355

37. Borghi L, Bureau M, Simon R. Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell. 2007;19(6):1795–808. doi: 10.1105/tpc.106.047159 17557810

38. Levin JZ, Meyerowitz EM. UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell. 1995;7(5):529–48. doi: 10.1105/tpc.7.5.529 7780306

39. Alvarez JP, Goldshmidt A, Efroni I, Bowman JL, Eshed Y. The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell. 2009;21(5):1373–93. doi: 10.1105/tpc.109.065482 19435933

40. Kuusk S, Sohlberg JJ, Magnus Eklund D, Sundberg E. Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J. 2006;47(1):99–111. doi: 10.1111/j.1365-313X.2006.02774.x 16740146

41. Crawford BC, Ditta G, Yanofsky MF. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol. 2007;17(13):1101–8. doi: 10.1016/j.cub.2007.05.079 17600712

42. Barbez E, Kubes M, Rolcik J, Beziat C, Pencik A, Wang B, et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 2012;485(7396):119–22. doi: 10.1038/nature11001 22504182

43. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998;282(5397):2226–30. doi: 10.1126/science.282.5397.2226 9856939

44. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell. 2002;108(5):661–73. doi: 10.1016/s0092-8674(02)00656-6 11893337

45. Peret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell. 2012;24(7):2874–85. doi: 10.1105/tpc.112.097766 22773749

46. Mancuso S, Marras AM, Mugnai S, Schlicht M, Zarsky V, Li G, et al. Phospholipase dzeta2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav. 2007;2(4):240–4. doi: 10.4161/psb.2.4.4566 19516994

47. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990;346(6279):35–9. doi: 10.1038/346035a0 1973265

48. Payne CT, Zhang F, Lloyd AM. GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. Genetics. 2000;156(3):1349–62. 11063707

49. Lee BH, Kwon SH, Lee SJ, Park SK, Song JT, Lee S, et al. The Arabidopsis thaliana NGATHA transcription factors negatively regulate cell proliferation of lateral organs. Plant Mol Biol. 2015;89(4–5):529–38. doi: 10.1007/s11103-015-0386-y 26433582

50. Lampugnani ER, Kilinc A, Smyth DR. PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. Plant J. 2012;71(5):724–35. doi: 10.1111/j.1365-313X.2012.05023.x 22507233

51. Kuusk S, Sohlberg JJ, Long JA, Fridborg I, Sundberg E. STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development. Development. 2002;129(20):4707–17. 12361963

52. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, Hepworth SR, et al. The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell. 2007;19(9):2719–35. doi: 10.1105/tpc.106.048769 17873098

53. Shuai B, Reynaga-Pena CG, Springer PS. The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol. 2002;129(2):747–61. doi: 10.1104/pp.010926 12068116

54. Cheng Y, Dai X, Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 2006;20(13):1790–9. doi: 10.1101/gad.1415106 16818609

55. Mai YX, Wang L, Yang HQ. A gain-of-function mutation in IAA7/AXR2 confers late flowering under short-day light in Arabidopsis. J Integr Plant Biol. 2011;53(6):480–92. doi: 10.1111/j.1744-7909.2011.01050.x 21564544

56. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development. 2005;132(18):4107–18. doi: 10.1242/dev.01955 16107481

57. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell. 2012;24(2):519–35. doi: 10.1105/tpc.111.092858 22374393

58. Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y. Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems. Plant Cell. 2008;20(5):1217–30. doi: 10.1105/tpc.107.057877 18469164

59. Lee YK, Kim GT, Kim IJ, Park J, Kwak SS, Choi G, et al. LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development. 2006;133(21):4305–14. doi: 10.1242/dev.02604 17038516

60. Zurcher E, Liu J, di Donato M, Geisler M, Muller B. Plant development regulated by cytokinin sinks. Science. 2016;353(6303):1027–30. doi: 10.1126/science.aaf7254 27701112

61. Hardtke CS, Berleth T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 1998;17(5):1405–11. doi: 10.1093/emboj/17.5.1405 9482737

62. Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta. 1996;200(2):229–37. doi: 10.1007/bf00208313 8904808

63. Redman JC, Haas BJ, Tanimoto G, Town CD. Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J. 2004;38(3):545–61. ISI:000220853200014 doi: 10.1111/j.1365-313X.2004.02061.x 15086809

64. Nemhauser JL, Hong F, Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006;126(3):467–75. doi: 10.1016/j.cell.2006.05.050 16901781

65. Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, et al. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 2008;55(3):526–42. doi: 10.1111/j.0960-7412.2008.03510.x 18419781

66. Yang XQ, Lee S, So JH, Dharmasiri S, Dharmasiri N, Ge L, et al. The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J. 2004;40(5):772–82. ISI:000225188000012 doi: 10.1111/j.1365-313X.2004.02254.x 15546359

67. Sun J, Qi L, Li Y, Zhai Q, Li C. PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell. 2013;25(6):2102–14. doi: 10.1105/tpc.113.112417 23757399

68. Zhang Z, Tucker E, Hermann M, Laux T. A Molecular Framework for the Embryonic Initiation of Shoot Meristem Stem Cells. Dev Cell. 2017;40(3):264–77 e4. doi: 10.1016/j.devcel.2017.01.002 28171749

69. Del Carmen Martinez-Ballesta M, Moreno DA, Carvajal M. The physiological importance of glucosinolates on plant response to abiotic stress in Brassica. Int J Mol Sci. 2013;14(6):11607–25. doi: 10.3390/ijms140611607 23722664

70. Ma Y, Miotk A, Sutikovic Z, Ermakova O, Wenzl C, Medzihradszky A, et al. WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nature communications. 2019;10(1):5093. doi: 10.1038/s41467-019-13074-9 31704928

71. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O. The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol. 2006;16(6):553–63. doi: 10.1016/j.cub.2006.01.058 16546078

72. Talbert PB, Adler HT, Parks DW, Comai L. The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development. 1995;121(9):2723–35. 7555701

73. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, et al. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol. 2003;13(20):1768–74. doi: 10.1016/j.cub.2003.09.035 14561401

74. Karimi M, Inze D, Depicker A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002;7(5):193–5. doi: 10.1016/s1360-1385(02)02251-3 11992820

75. Barrell PJ, Conner AJ. Minimal T-DNA vectors suitable for agricultural deployment of transgenic plants. Biotechniques. 2006;41(6):708–10. doi: 10.2144/000112306 17191614

76. S. A. Babraham Bioinformatics—FastQC A Quality Control Tool for High Throughput Sequence Data 2013. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

77. Martin M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnetjournal 2011;17(1):10–2.

78. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11. WOS:000265523300002 doi: 10.1093/bioinformatics/btp120 19289445

79. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. doi: 10.1093/bioinformatics/btu638 25260700

80. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281

81. Alexa A, Rahnenfuhrer, J. topGO: Enrichment Analysis for Gene Ontology 2010. Available from: https://rdrr.io/bioc/topGO/.

82. Goder A, Filkov V. Consensus Clustering Algorithms: Comparison and Refinement. Siam Proc S. 2008:109–17. WOS:000289650200011

83. Page L, Brin, S., Motwani, R., Winograd, T. The Pagerank Citation Ranking: Bringing Order to the web. technical report. Stanford InfoLab Publication Server: 1999 Contract No.: 422.

84. Rosvall M. AD, Bergstrom C. T. The map equation. The European Physical Journal Special Topics. 2009;178:13–23.

85. Csardi G, Nepusz T. The igraph software package for complex network research. InterJournal, Complex Systems. 2006.

86. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology. 2005;15(21):1899–911. WOS:000233422900019 doi: 10.1016/j.cub.2005.09.052 16271866

87. Cole M, Chandler J, Weijers D, Jacobs B, Comelli P, Werr W. DORNROSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development. 2009;136(10):1643–51. doi: 10.1242/dev.032177 19369397

88. Chandler JW, Jacobs B, Cole M, Comelli P, Werr W. DORNROSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima. Plant Mol Biol. 2011;76(1–2):171–85. doi: 10.1007/s11103-011-9779-8 21547450

89. Yamaguchi N, Jeong CW, Nole-Wilson S, Krizek BA, Wagner D. AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 Induce LEAFY Expression in Response to Auxin to Promote the Onset of Flower Formation in Arabidopsis. Plant Physiol. 2016;170(1):283–93. doi: 10.1104/pp.15.00969 26537561

Článek High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements

Článek XPF-ERCC1 protects liver, kidney and blood homeostasis outside the canonical excision repair pathways

Článek The nanophthalmos protein TMEM98 inhibits MYRF self-cleavage and is required for eye size specification

Článek Is imprinting the result of “friendly fire” by the host defense system?

Článek XPF–ERCC1: Linchpin of DNA crosslink repair

Článek Molecular genetics of maternally-controlled cell divisions

Článek Loss-of-function tolerance of enhancers in the human genome

Článek Is adaptation limited by mutation? A timescale-dependent effect of genetic diversity on the adaptive substitution rate in animals

Článek Tryptamine accumulation caused by deletion of MrMao-1 in Metarhizium genome significantly enhances insecticidal virulence

Článek Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids

Článek Pathological mechanism and antisense oligonucleotide-mediated rescue of a non-coding variant suppressing factor 9 RNA biogenesis leading to hemophilia B

Článek Loss of FOXM1 in macrophages promotes pulmonary fibrosis by activating p38 MAPK signaling pathway