DWARF TILLER1, a WUSCHEL-Related Homeobox Transcription Factor, Is Required for Tiller Growth in Rice

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Plant architecture is important for crop yield. In most plants, branches grow smaller than the main shoot, largely due to the ‘apical dominance’. However, in several cereal crops, including rice, wheat, and barley, the branches (tillers) have a height and size indistinguishable from the main shoot. The genetic basis of uniform tiller growth has remained elusive. We identified DWARF TILLER1, a WUSCHEL-related homeobox (WOX) transcription factor, as a positive regulator of tiller growth. Most dwt1 mutant plants show normal main shoot but dwarf tillers and reduced panicle size. Tiller growth in dwt1 appears to be inhibited by the main shoot, as removal of the main shoot releases the first tiller. The non-elongating internodes in dwt1 show reduced cell number and cell size, while DWT1 was mainly expressed in the panicles but not internodes, suggesting that DWT1 plays a long distance regulatory role in promoting internode elongation. Genome-wide expression analysis revealed that the expression of genes related to cell division and elongation, as well as to homeostasis and signaling of cytokinin and gibberellin were affected in dwt1 un-elongated internodes. This study reveals that a WOX transcription factor controls the growth uniformity of tillers and the main shoot in rice.

Vyšlo v časopise: DWARF TILLER1, a WUSCHEL-Related Homeobox Transcription Factor, Is Required for Tiller Growth in Rice. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004154
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004154

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Zdroje

1. GrilloMA, LiCB, FowlkesAM, BriggemanTM, ZhouAL, et al. (2009) Genetic Architecture for the Adaptive Origin of Annual Wild Rice, Oryza Nivara. Evolution 63: 870–883.

2. MaLY, BaoJ, GuoLB, ZengDL, LiXM, et al. (2009) Quantitative Trait Loci for Panicle Layer Uniformity Identified in Doubled Haploid Lines of Rice in Two Environments. Journal of Integrative Plant Biology 51: 818–824.

3. UozuS, Tanaka-UeguchiM, KitanoH, HattoriK, MatsuokaM (2000) Characterization of XET-related genes of rice. Plant Physiology 122: 853–859.

4. WangYH, LiJY (2008) Molecular basis of plant architecture. Annual Review of Plant Biology 59: 253–279.

5. HongZ, Tanaka-UeguchiM, MATSUOKAM (2004) Brassinosteroids and Rice Architecture. J Pestic Sci 29: 184–188.

6. BreuningerH, RikirschE, HermannM, UedaM, LauxT (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Developmental Cell 14: 867–876.

7. WuX, ChoryJ, WeigelD (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Developmental Biology 309: 306–316.

8. WuXL, DabiT, WeigelD (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Current Biology 15: 436–440.

9. RebochoAB, BliekM, KustersE, CastelR, ProcissiA, et al. (2008) Role of EVERGREEN in the development of the cymose petunia inflorescence. Developmental Cell 15: 437–447.

10. LippmanZB, CohenO, AlvarezJP, Abu-AbiedM, PekkerI, et al. (2008) The Making of a Compound Inflorescence in Tomato and Related Nightshades. Plos Biology 6: 2424–2435.

11. WangW, ChuH, ZhangD, LiangW (2013) Fine mapping and analysis of Dwarf Tiller 1 in controlling rice architecture. Journal of Genetics and Genomics 40: 493–495.

12. TAKEDAK (1977) Gamma Field Symposia. Internode elongation and dwarfism in some gramineous plants 1–18.

13. ThimannKV, SkoogF (1933) Studies on the growth hormone of plants III. The inhibitory action of the growth substance on bud development. Proc Natl Acad Sci USA 19: 714–716.

14. ZhangX, ZongJ, LiuJ, YinJ, ZhangD (2010) Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. Journal of Integrative Plant Biology 52: 1016–1026.

15. van der GraaffE, LauxT, RensingSA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biology 10: 248.

16. BuschW, MiotkA, ArielFD, ZhaoZ, FornerJ, et al. (2010) Transcriptional control of a plant stem cell niche. Developmental Cell 18: 849–861.

17. NagasakiH, MatsuokaM, SatoY (2005) Members of TALE and WUS subfamilies of homeodomain proteins with potentially important functions in development form dimers within each subfamily in rice. Genes Genet Syst 80: 261–267.

18. NardmannJ, ReisewitzP, WerrW (2009) Discrete Shoot and Root Stem Cell-Promoting WUS/WOX5 Functions Are an Evolutionary Innovation of Angiosperms. Molecular Biology and Evolution 26: 1745–1755.

19. HuangX, ZhaoY, WeiX, LiC, WangA, et al. (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44: 32–39.

20. VanstraelenM, InzeD, GeelenD (2006) Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci 11: 167–175.

21. MullerS, HanS, SmithLG (2006) Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Current Biology 16: 888–894.

22. VanstraelenM, Torres AcostaJA, De VeylderL, InzeD, GeelenD (2004) A plant-specific subclass of C-terminal kinesins contains a conserved a-type cyclin-dependent kinase site implicated in folding and dimerization. Plant Physiology 135: 1417–1429.

23. AmbroseJC, CyrR (2007) The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19: 226–236.

24. de JagerSM, MengesM, BauerUM, MurrayJAH (2001) Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities. Plant Molecular Biology 47: 555–568.

25. StevensR, MaricontiL, RossignolP, PerennesC, CellaR, et al. (2002) Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. Journal of Biological Chemistry 277: 32978–32984.

26. LeeJ, DasA, YamaguchiM, HashimotoJ, TsutsumiN, et al. (2003) Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. Plant Journal 34: 417–425.

27. YuY, SteinmetzA, MeyerD, BrownS, ShenWH (2003) The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation. Plant Cell 15: 2763–2777.

28. LeeY, KendeH (2002) Expression of alpha-expansin and expansin-like genes in deepwater rice. Plant Physiology 130: 1396–1405.

29. KurasawaK, MatsuiA, YokoyamaR, KuriyamaT, YoshizumiT, et al. (2009) The AtXTH28 gene, a xyloglucan endotransglucosylase/hydrolase, is involved in automatic self-pollination in Arabidopsis thaliana. Plant Cell Physiol 50: 413–422.

30. HiroseN, MakitaN, KojimaM, Kamada-NobusadaT, SakakibaraH (2007) Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol 48: 523–539.

31. RaskinI, KendeH (1984) Role of Gibberellin in the Growth-Response of Submerged Deep-Water Rice. Plant Physiology 76: 947–950.

32. HoffmannbenningS, KendeH (1992) On the Role of Abscisic-Acid and Gibberellin in the Regulation of Growth in Rice. Plant Physiology 99: 1156–1161.

33. ItohH, Ueguchi-TanakaM, SatoY, AshikariM, MatsuokaM (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14: 57–70.

34. IkedaA, Ueguchi-TanakaM, SonodaY, KitanoH, KoshiokaM, et al. (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13: 999–1010.

35. Harlan JR (1992) Crops and Man (2nd edition), Jack R. Harlan. Madison, Wisconsin: American Society of Agronomy. 295 pp.

36. HaeckerA, Gross-HardtR, GeigesB, SarkarA, BreuningerH, et al. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657–668.

37. StuderA, ZhaoQ, Ross-IbarraJ, DoebleyJ (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43: 1160–1163.

38. DomagalskaMA, LeyserO (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12: 211–221.

39. BrewerPB, KoltaiH, BeveridgeCA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6: 18–28.

40. VadasseryJ, RitterC, VenusY, CamehlI, VarmaA, et al. (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21: 1371–1383.

41. ChenCM, ErtlJR, LeisnerSM, ChangCC (1985) Localization of cytokinin biosynthetic sites in pea plants and carrot roots. Plant Physiology 78: 510–513.

42. NordstromA, TarkowskiP, TarkowskaD, NorbaekR, AstotC, et al. (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci U S A 101: 8039–8044.

43. TanakaM, TakeiK, KojimaM, SakakibaraH, MoriH (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant Journal 45: 1028–1036.

44. SakamotoT, MiuraK, ItohH, TatsumiT, Ueguchi-TanakaM, et al. (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiology 134: 1642–1653.

45. YamamuroC, IharaY, WuX, NoguchiT, FujiokaS, et al. (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591–1605.

46. HongZ, Ueguchi-TanakaM, UmemuraK, UozuS, FujiokaS, et al. (2003) A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15: 2900–2910.

47. TanabeS, AshikariM, FujiokaS, TakatsutoS, YoshidaS, et al. (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17: 776–790.

48. Ueguchi-TanakaM, AshikariM, NakajimaM, ItohH, KatohE, et al. (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693–698.

49. HwangI, SheenJ, MullerB (2012) Cytokinin signaling networks. Annual Review of Plant Biology 63: 353–380.

50. ZhaoY, HuYF, DaiMQ, HuangLM, ZhouDX (2009) The WUSCHEL-Related Homeobox Gene WOX11 Is Required to Activate Shoot-Borne Crown Root Development in Rice. Plant Cell 21: 736–748.

51. LeibfriedA, ToJP, BuschW, StehlingS, KehleA, et al. (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438: 1172–1175.

52. Greenboim-WainbergY, MaymonI, BorochovR, AlvarezJ, OlszewskiN, et al. (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17: 92–102.

53. ItohJ, NonomuraK, IkedaK, YamakiS, InukaiY, et al. (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46: 23–47.

54. SuzakiT, ItoM, KawaguchiM (2013) Genetic basis of cytokinin and auxin functions during root nodule development. Front Plant Sci 4: 42.

55. SuzakiT, YanoK, ItoM, UmeharaY, SuganumaN, et al. (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139: 3997–4006.

56. HieiY, KomariT, KuboT (1997) Transformation of rice mediated by Agrobacterium tumefaciens. Plant Molecular Biology 35: 205–218.

57. WangD, XiaY, LiX, HouL, YuJ (2013) The Rice Genome Knowledgebase (RGKbase): an annotation database for rice comparative genomics and evolutionary biology. Nucleic Acids Res 41: D1199–1205.

58. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

59. KumarS, TamuraK, NeiM (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150–163.

60. GampalaSS, KimTW, HeJX, TangW, DengZ, et al. (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Developmental Cell 13: 177–189.

61. AlexaA, RahnenfuhrerJ, LengauerT (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600–1607.

62. ChuHW, QianQ, LiangWQ, YinCS, TanHX, et al. (2006) The floral organ number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiology 142: 1039–1052.

63. IkedaK, SunoharaH, NagatoY (2004) Developmental course of inflorescence and spikelet in rice. Breeding Science 54: 147–156.