Accession-specific modifiers act with ZWILLE/ARGONAUTE10 to maintain shoot meristem stem cells during embryogenesis in Arabidopsis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Tucker, Matthew R ^a,b   Roodbarkelari, Farshad ^a   Truernit, Elisabeth ^a,d   Adamski, Nikolai M ^a,e   Hinze, Annika ^a   Lohmüller, Barbara ^a   Würschum, Tobias ^c   Laux, Thomas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF HOHENHEIM   (Germany)

^d ETH ZURICH   (Switzerland)

^e JOHN INNES CENTRE   (United Kingdom)

Author keywords

Accession; Arabidopsis; ARGONAUTE; QTL; Shoot meristem; Stem cells; ZWILLE

Indexed keywords

ALLELE; ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ANALYSIS; GERMANY; INBRED STRAIN; MERISTEM; NEAR ISOGENIC LINE; NONHUMAN; PROMOTER REGION; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; SEEDLING; SHOOT; TRANSCRIPTOMICS; ANTIBODY SPECIFICITY; BREEDING; CHROMOSOME MAP; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLANT GENOME; PLANT SEED; STEM CELL;

AGO10 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGONAUTE PROTEIN; CYCLOPHILIN; SQN PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; BREEDING; CHROMOSOME MAPPING; CYCLOPHILINS; GENE EXPRESSION; GENOME, PLANT; MERISTEM; ORGAN SPECIFICITY; PHENOTYPE; PHYLOGENY; QUANTITATIVE TRAIT LOCI; SEEDS; STEM CELLS;

EID: 84887752987     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-809     Document Type: Article

References (56)

1. Aichinger E, Kornet N, Friedrich T, Laux T. Plant stem cell niches. Annu Rev Plant Biol 2012, 63:615-636. 10.1146/annurev-arplant-042811-105555, 22404469.
2. Murray JA, Jones A, Godin C, Traas J. Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell 2012, 24(10):3907-3919. 10.1105/tpc.112.102194, 3517227, 23110895.
3. Tucker MR, Laux T. Connecting the paths in plant stem cell regulation. Trends Cell Biol 2007, 17(8):403-410. 10.1016/j.tcb.2007.06.002, 17766120.
4. Knauer S, Holt AL, Rubio-Somoza I, Tucker EJ, Hinze A, Pisch M, Javelle M, Timmermans MC, Tucker MR, Laux T. A protodermal miR394 signal defines a region of stem cell competence in the arabidopsis shoot meristem. Dev Cell 2013, 24(2):125-132. 10.1016/j.devcel.2012.12.009, 23333352.
5. Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 1998, 95:805-815. 10.1016/S0092-8674(00)81703-1, 9865698.
6. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100:635-644. 10.1016/S0092-8674(00)80700-X, 10761929.
7. 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, 289:617-9. 10.1126/science.289.5479.617, 10915624.
8. Moussian B, Schoof H, Haecker A, Jürgens G, Laux T. Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 1998, 17(6):1799-1809. 10.1093/emboj/17.6.1799, 1170527, 9501101.
9. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 1998, 17(1):170-180. 10.1093/emboj/17.1.170, 1170368, 9427751.
10. Tucker MR, Hinze A, Tucker EJ, Takada S, Jurgens G, Laux T. Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 2008, 135(17):2839-2843. 10.1242/dev.023648, 18653559.
11. Mallory AC, Hinze A, Tucker MR, Bouche N, Gasciolli V, Elmayan T, Lauressergues D, Jauvion V, Vaucheret H, Laux T. Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet 2009, 5(9):e1000646. 10.1371/journal.pgen.1000646, 2730571, 19763164.
12. Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2011, 145(2):242-256. 10.1016/j.cell.2011.03.024, 21496644.
13. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 1999, 126(3):469-481.
14. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320(5880):1185-1190. 10.1126/science.1159151, 18483398.
15. Vaucheret H. Plant ARGONAUTES. Trends Plant Sci 2008, 13(7):350-358. 10.1016/j.tplants.2008.04.007, 18508405.
16. Manavella PA, Weigel D, Wu L. Argonaute10 as a miRNA locker. Cell 2011, 145(2):173-174. 10.1016/j.cell.2011.03.045, 21496638.
17. Liu Q, Yao X, Pi L, Wang H, Cui X, Huang H. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and leaf polarity establishment by repressing miR165/166 in Arabidopsis. Plant J 2008, 58(1):27-40.
18. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 2008, 49(4):493-500. 10.1093/pcp/pcn043, 18344228.
19. Vollbrecht E, Reiser L, Hake S. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 2000, 127:3161-3172.
20. Moussian B, Haecker A, Laux T. ZWILLE buffers meristem stability in Arabidopsis thaliana. Dev Genes Evol 2003, 213(11):534-540. 10.1007/s00427-003-0359-z, 14564520.
21. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 1996, 8:735-746. 161133, 8624444.
22. Platt A, Horton M, Huang YS, Li Y, Anastasio AE, Mulyati NW, Agren J, Bossdorf O, Byers D, Donohue K, et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet 2010, 6(2):e1000843. 10.1371/journal.pgen.1000843, 2820523, 20169178.
23. Lister C, Dean C. Recombinant inbred lines for mapping rflp and phenotypic markers in arabidopsis-thaliana. Plant J 1993, 4(4):745-750.
24. Berardini TZ, Bollman K, Sun H, Poethig RS. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 2001, 291(5512):2405-2407. 10.1126/science.1057144, 11264535.
25. Prunet N, Morel P, Thierry AM, Eshed Y, Bowman JL, Negrutiu I, Trehin C. REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell 2008, 20(4):901-919. 10.1105/tpc.107.053306, 2390727, 18441215.
26. Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B, Weijers D, Poethig RS. Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc Natl Acad Sci USA 2009, 106(13):5424-5429. 10.1073/pnas.0812729106, 2664006, 19289849.
27. Weigel D. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol 2012, 158(1):2-22. 10.1104/pp.111.189845, 3252104, 22147517.
28. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 2010, 465(7298):627-631. 10.1038/nature08800, 3023908, 20336072.
29. Zhai J, Liu J, Liu B, Li P, Meyers BC, Chen X, Cao X. Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet 2008, 4(4):e1000056. 10.1371/journal.pgen.1000056, 2289841, 18437202.
30. Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB. Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the evolution of selfing. Proc Natl Acad Sci USA 2004, 101(45):16070-16074. 10.1073/pnas.0406970101, 528763, 15505209.
31. Mouchel CF, Briggs GC, Hardtke CS. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 2004, 18(6):700-714. 10.1101/gad.1187704, 387244, 15031265.
32. Lall S, Nettleton D, DeCook R, Che P, Howell SH. Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in Arabidopsis. Genet 2004, 167(4):1883-1892.
33. DeCook R, Lall S, Nettleton D, Howell SH. Genetic regulation of gene expression during shoot development in Arabidopsis. Genet 2006, 172(2):1155-1164.
34. Wang Y, Meng Y, Zhang M, Tong X, Wang Q, Sun Y, Quan J, Govers F, Shan W. Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol Plant Pathol 2011, 12(2):187-201. 10.1111/j.1364-3703.2010.00659.x, 21199568.
35. Grant MR, McDowell JM, Sharpe AG, de Torres ZM, Lydiate DJ, Dangl JL. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci USA 1998, 95(26):15843-15848. 10.1073/pnas.95.26.15843, 28132, 9861058.
36. Seren U, Vilhjalmsson BJ, Horton MW, Meng D, Forai P, Huang YS, Long Q, Segura V, Nordborg M. GWAPP: a Web application for genome-wide association mapping in arabidopsis. Plant Cell 2012, 24(12):4793-4805. 10.1105/tpc.112.108068, 3556958, 23277364.
37. Cockram J, White J, Zuluaga DL, Smith D, Comadran J, Macaulay M, Luo Z, Kearsey MJ, Werner P, Harrap D, et al. Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci USA 2010, 107(50):21611-21616. 10.1073/pnas.1010179107, 3003063, 21115826.
38. Alheit KV, Maurer HP, Reif JC, Tucker MR, Hahn V, Weissmann EA, Wurschum T. Genome-wide evaluation of genetic diversity and linkage disequilibrium in winter and spring triticale (x Triticosecale Wittmack). BMC Genomics 2012, 13:235. 10.1186/1471-2164-13-235, 3464613, 22691168.
39. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinf 2008, 2008:420747.
40. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 2011, 477(7365):419-423. 10.1038/nature10414, 21874022.
41. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 2011, 43(10):956-963. 10.1038/ng.911, 21874002.
42. Wang X, Weigel D, Smith LM. Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet 2013, 9(2):e1003255. 10.1371/journal.pgen.1003255, 3567156, 23408902.
43. Laux T, Mayer KFX, Berger J, Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 1996, 122:87-96.
44. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
45. Wurschum T, Gross-Hardt R, Laux T. APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 2006, 18(2):295-307. 10.1105/tpc.105.038398, 1356540, 16387832.
46. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL. Arabidopsis map-based cloning in the post-genome era. Plant Physiol 2002, 129(2):440-450. 10.1104/pp.003533, 1540230, 12068090.
47. Utz HF. PlabMQTL Manual - Software for meta-QTL analysis with composite interval mapping. Version 0.5s 2012, University of Hohenheim: Institute of Plant Breeding, Seed Science and Population Genetics.
48. Jansen RC, Stam P. High resolution of quantitative traits into multiple loci via interval mapping. Genet 1994, 136(4):1447-1455.
49. Zeng ZB. Precision mapping of quantitative trait loci. Genet 1994, 136(4):1457-1468.
50. Haley CS, Knott SA. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity (Edinb) 1992, 69(4):315-324. 10.1038/hdy.1992.131, 16718932.
51. Baierl A, Bogdan M, Frommlet F, Futschik A. On locating multiple interacting quantitative trait loci in intercross designs. Genet 2006, 173(3):1693-1703.
52. Churchill GA, Doerge RW. Empirical threshold values for quantitative trait mapping. Genet 1994, 138(3):963-971.
53. D'Onofrio C, Cox A, Davies C, Boss PK. Induction of secondary metabolism in grape cell cultures by jasmonates. Funct Plant Biol 2009, 36(4):323-338.
54. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 2006, 18(5):1121-1133. 10.1105/tpc.105.039834, 1456875, 16531494.
55. Hellens R, Mullineaux P, Klee H. Technical focus:a guide to agrobacterium binary Ti vectors. Trends Plant Sci 2000, 5(10):446-451. 10.1016/S1360-1385(00)01740-4, 11044722.
56. Eschenfeldt WH, Lucy S, Millard CS, Joachimiak A, Mark ID. A family of LIC vectors for high-throughput cloning and purification of proteins. Methods Mol Biol 2009, 498:105-115. 10.1007/978-1-59745-196-3_7, 2771622, 18988021.