The barley Uniculme4 gene encodes a BLADE-ON-PETIOLE-like protein that controls tillering and leaf patterning

Plant Physiology

Volumn 168, Issue 1, 2015, Pages 164-174

  Tavakol, Elahe ^a,b   Okagaki, Ron ^c   Verderio, Gabriele ^a   Vahid, Shariati J ^d   Hussien, Ahmed ^a   Bilgic, Hatice ^c   Scanlon, Mike J ^e   Todt, Natalie R ^e   Close, Timothy J ^f   Druka, Arnis ^g   Waugh, Robbie ^g   Steuernagel, Burkhard ^h   Ariyadasa, Ruvini ^h   Himmelbach, Axel ^h   Stein, Nils ^h   Muehlbauer, Gary J ^c   Rossini, Laura ^a,d  

^a UNIVERSITY OF MILAN   (Italy)

^b SHIRAZ UNIVERSITY   (Iran)

^c UNIVERSITY OF MINNESOTA   (United States)

^d PARCO TECNOLOGICO PADANO   (Italy)

^e Parco Tecnologico Padano ^*  (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^h LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; DICOTYLEDONEAE; HORDEUM; HORDEUM VULGARE; LILIOPSIDA; POACEAE; TRITICEAE; TRITICUM AESTIVUM;

ANKYRIN; ARABIDOPSIS PROTEIN; PLANT PROTEIN;

ANATOMY AND HISTOLOGY; ARABIDOPSIS; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MORPHOGENESIS; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT GENE; PLANT LEAF; SHOOT;

ANKYRINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BODY PATTERNING; CLONING, MOLECULAR; FLOWERS; GENES, PLANT; HORDEUM; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS; PLANT SHOOTS;

EID: 84929472043     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.252882     Document Type: Article

References (59)

1. Agusti J, Greb T (2013) Going with the wind: adaptive dynamics of plant secondary meristems. Mech Dev 130: 34–44
2. Ahlstrand GG (1996) Low-temperature low-voltage scanning microscopy (LTLVSEM) of uncoated frozen biological materials: a simple alternative. In G Bailey, J Corbett, R Dimlich, J Michael, N Zaluzec, eds, Proceedings of Microscopy Microanalysis. San Francisco Press, San Francisco, pp 918–919
3. Arber A (1918) The phyllode theory of the monocotyledonous leaf, with special reference to anatomical evidence. Ann Bot 32: 465–501
4. Babb S, Muehlbauer GJ (2003) Genetic and morphological characterization of the barley uniculm2 (cul2) mutant. Theor Appl Genet 106: 846–857
5. Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341: 95–113
6. Bolduc N, O’Connor D, Moon J, Lewis M, Hake S (2012) How to pattern a leaf. Cold Spring Harb Symp Quant Biol 77: 47–51
7. Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, et al (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10: 582
8. Couzigou JM, Zhukov V, Mondy S, Abu el Heba G, Cosson V, Ellis TH, Ambrose M, Wen J, Tadege M, Tikhonovich I, et al (2012) NODULE ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell 24: 4498– 4510
9. Dabbert T, Okagaki RJ, Cho S, Boddu J, Muehlbauer GJ (2009) The genetics of barley low-tillering mutants: absent lower laterals (als). Theor Appl Genet 118: 1351–1360
10. Dabbert T, Okagaki RJ, Cho S, Heinen S, Boddu J, Muehlbauer GJ (2010) The genetics of barley low-tillering mutants: low number of tillers-1 (lnt1). Theor Appl Genet 121: 705–715
11. Dahleen L, Franckowiak J, Lundqvist U (2007) Descriptions of barley genetic stocks for 2007. Barley Genet Newsl 37: 188–301
12. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15: 2181–2191
13. Després C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12: 279–290
14. Donald CM (1968) The breeding of crop ideotypes. Euphytica 17: 385–403
15. Druka A, Franckowiak J, Lundqvist U, Bonar N, Alexander J, Houston K, Radovic S, Shahinnia F, Vendramin V, Morgante M, et al (2011) Genetic dissection of barley morphology and development. Plant Physiol 155: 617–627
16. Fan JB, Oliphant A, Shen R, Kermani BG, Garcia F, Gunderson KL, Hansen M, Steemers F, Butler SL, Deloukas P, et al (2003) Highly parallel SNP genotyping. Cold Spring Harb Symp Quant Biol 68: 69–78
17. Feuillet C, Stein N, Rossini L, Praud S, Mayer K, Schulman A, Eversole K, Appels R (2012) Integrating cereal genomics to support innovation in the Triticeae. Funct Integr Genomics 12: 573–583
18. Franckowiak JD, Foster AE, Pederson VD, Pyler RE (1985) Registration of ‘Bowman’ barley. Crop Sci 25: 883
19. Ha CM, Jun JH, Nam HG, Fletcher JC (2004) BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45: 1361–1370
20. Ha CM, Jun JH, Nam HG, Fletcher JC (2007) BLADE-ON-PETIOLE 1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 19: 1809–1825
21. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG (2003) The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130: 161–172
22. Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW(2005) BLADE-ON PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 17: 1434–1448
23. Hussien A, Tavakol E, Horner DS, Muñoz-Amatriaín M, Muehlbauer GJ, Rossini L (2014) Genetics of tillering in rice and barley. Plant Genome 7: 1–20
24. Janssen BJ, Drummond RS, Snowden KC (2014) Regulation of axillary shoot development. Curr Opin Plant Biol 17: 28–35
25. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004) MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428: 84–88
26. Jun JH, Ha CM, Fletcher JC (2010) BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in Arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 22: 62–76
27. Kaplan DR (1973) The problem of leaf morphology and evolution in the monocotyledons. Q Rev Biol 48: 437–457
28. Kebrom TH, Spielmeyer W, Finnegan EJ (2013) Grasses provide new insights into regulation of shoot branching. Trends Plant Sci 18: 41–48
29. Keller T, Abbott J, Moritz T, Doerner P (2006) Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18: 598–611
30. Khan M, Xu H, Hepworth SR (2014) BLADE-ON-PETIOLE genes: setting boundaries in development and defense. Plant Sci 215-216: 157–171
31. Khan M, Xu M, Murmu J, Tabb P, Liu Y, Storey K, McKim SM, Douglas CJ, Hepworth SR (2012) Antagonistic interaction of BLADE-ONPETIOLE1 and 2 with BREVIPEDICELLUS and PENNYWISE regulates Arabidopsis inflorescence architecture. Plant Physiol 158: 946–960
32. Leroy P, Guilhot N, Sakai H, Bernard A, Choulet F, Theil S, Reboux S, Amano N, Flutre T, Pelegrin C, et al (2012) TriAnnot: a versatile and high performance pipeline for the automated annotation of plant genomes. Front Plant Sci 3: 5
33. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, et al (2003) Control of tillering in rice. Nature 422: 618–621
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402–408
35. Mascher M, Jost M, Kuon JE, Himmelbach A, Aßfalg A, Beier S, Scholz U, Graner A, Stein N (2014) Mapping-by-sequencing accelerates forward genetics in barley. Genome Biol 15: R78
36. Mayer KF, Martis M, Hedley PE, Simková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23: 1249– 1263
37. Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711–716
38. Mohapatra PK, Panda BB, Kariali E (2011) Plasticity of tiller dynamics in wild rice Oryza rufipogon Griff.: a strategy for resilience in suboptimal environments. Int J Agron 2011: 543237
39. Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18: 586–597
40. Ng PC, Henikoff S (2001) Predicting deleterious amino acid substitutions. Genome Res 11: 863–874
41. Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132: 2203–2213
42. Osnato M, Stile MR, Wang Y, Meynard D, Curiale S, Guiderdoni E, Liu Y, Horner DS, Ouwerkerk PBF, Pozzi C, et al (2010) Cross talk between the KNOX and ethylene pathways is mediated by intron-binding transcription factors in barley. Plant Physiol 154: 1616–1632
43. Paux E, Faure S, Choulet F, Roger D, Gauthier V, Martinant JP, Sourdille P, Balfourier F, Le Paslier MC, Chauveau A, et al (2010) Insertion sitebased polymorphism markers open new perspectives for genome saturation and marker-assisted selection in wheat. Plant Biotechnol J 8: 196– 210
44. Pozzi C, di Pietro D, Halas G, Roig C, Salamini F (2003) Integration of a barley (Hordeum vulgare) molecular linkage map with the position of genetic loci hosting 29 developmental mutants. Heredity (Edinb) 90: 390–396
45. Ruzin SE (1999) Plant Microtechnique and Microscopy. Oxford University Press, Oxford
46. Schmitz G, Theres K (2005) Shoot and inflorescence branching. Curr Opin Plant Biol 8: 506–511
47. Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci USA 99: 1064–1069
48. Schulte D, Ariyadasa R, Shi B, Fleury D, Saski C, Atkins M, deJong P, Wu CC, Graner A, Langridge P, et al (2011) BAC library resources for mapbased cloning and physical map construction in barley (Hordeum vulgare L.). BMC Genomics 12: 247
49. Seavers GP, Wright KJ (1999) Crop canopy development and structure influence weed suppression. Weed Res 39: 319–328
50. Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3: 739–744
51. Steuernagel B, Taudien S, Gundlach H, Seidel M, Ariyadasa R, Schulte D, Petzold A, Felder M, Graner A, Scholz U, et al (2009) De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley. BMC Genomics 10: 547
52. Sussex IM (1989) Developmental programming of the shoot meristem. Cell 56: 225–229
53. Sylvester AW, Cande WZ, Freeling M (1990) Division and differentiation during normal and liguleless-1 maize leaf development. Development 110: 985–1000
54. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79: 607–622
55. Walsh J, Waters CA, Freeling M (1998) The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary. Genes Dev 12: 208–218
56. Wu XM, Yu Y, Han LB, Li CL, Wang HY, Zhong NQ, Yao Y, Xia GX (2012) The tobacco BLADE-ON-PETIOLE2 gene mediates differentiation of the corolla abscission zone by controlling longitudinal cell expansion. Plant Physiol 159: 835–850
57. Xu M, Hu T, McKim SM, Murmu J, Haughn GW, Hepworth SR (2010) Arabidopsis BLADE-ON-PETIOLE1 and 2 promote floral meristem fate and determinacy in a previously undefined pathway targeting APETALA1 and AGAMOUS-LIKE24. Plant J 63: 974–989
58. Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96: 6523–6528
59. Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant Microbe Interact 13: 191–202