Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the green revolution genetic toolkit

Plant Physiology

Volumn 166, Issue 4, 2014, Pages 1912-1927

  Dockter, Christoph ^a   Gruszka, Damian ^b   Braumann, Ilka ^a   Druka, Arnis ^c   Druka, Ilze ^c   Franckowiak, Jerome ^d   Gough, Simon P ^a   Janeczko, Anna ^e   Kurowska, Marzena ^b   Lundqvist, Joakim ^a   Lundqvist, Udda ^f   Marzec, Marek ^b   Matyszczak, Izabela ^a   Müller, André H ^a   Oklestkova, Jana ^g,h   Schulz, Burkhard ⁱ   Zakhrabekova, Shakhira ^a   Hansson, Mats ^a  

^a CARLSBERG LABORATORY   (Denmark)

^b UNIVERSITY OF SILESIA   (Poland)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d Agri Science Queensland ^*  (Australia)

^e THE FRANCISZEK GÓRSKI INSTITUTE OF PLANT PHYSIOLOGY   (Poland)

^f Nordic Genetic Resource Center   (Sweden)

^g PALACKÝ UNIVERSITY   (Czech Republic)

^h INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

ⁱ UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HORDEUM;

AMINO ACID; BRASSINOSTEROID;

ALLELE; CHROMOSOMAL MAPPING; COMPUTER SIMULATION; DNA SEQUENCE; FOOD GRAIN; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; SIGNAL TRANSDUCTION; STRUCTURAL MODEL; TEMPERATURE; WEATHER;

ALLELES; AMINO ACIDS; BASE SEQUENCE; BRASSINOSTEROIDS; CHROMOSOME MAPPING; COMPUTER SIMULATION; EDIBLE GRAIN; GENE EXPRESSION REGULATION, PLANT; HORDEUM; MODELS, STRUCTURAL; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TEMPERATURE; WEATHER;

EID: 84914146005     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.250738     Document Type: Article

References (56)

1. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810-817.
2. Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62: 1027-1046.
3. Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M (2014) Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J 78: 31-43.
4. Bosshard HR, Marti DN, Jelesarov I (2004) Protein stabilization by salt bridges: concepts, experimental approaches and clarification of some misunderstandings. J Mol Recognit 17: 1-16.
5. Chandler PM, Harding CA (2013) 'Overgrowth' mutants in barley and wheat: new alleles and phenotypes of the 'Green Revolution' DELLA gene. J Exp Bot 64: 1603-1613.
6. Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D, Takeda K, Takatsuto S, Hoshino T, Watanabe Y (2003) A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol 133: 1209-1219.
7. Dahleen LS, Vander Wal LJ, Franckowiak JD (2005) Characterization and molecular mapping of genes determining semidwarfism in barley. J Hered 96: 654-662.
8. Daoura BG, Chen L, Du Y, Hu YG (2014) Genetic effects of dwarfing gene Rht-5 on agronomic traits in common wheat (Triticum aestivum L.) and QTL analysis on its linked traits. Field Crops Res 156: 22-29.
9. 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.
10. Franckowiak JD, Lundqvist U (2012) Descriptions of barley genetic stocks for 2012. Barley Genet Newsl 42: 36-792.
11. Fujioka S, Noguchi T, Takatsuto S, Yoshida S (1998) Activity of brassinosteroids in the dwarf rice lamina inclination bioassay. Phytochemistry 49: 1841-1848.
12. Greeve I, Hermans-Borgmeyer I, Brellinger C, Kasper D, Gomez-Isla T, Behl C, Levkau B, Nitsch RM(2000) The human DIMINUTO/DWARF1 homolog seladin-1 confers resistance to Alzheimer's disease-associated neurodegeneration and oxidative stress. J Neurosci 20: 7345-7352.
13. Gruszka D, Szarejko I, Maluszynski M (2011a) Identification of barley DWARF gene involved in brassinosteroid synthesis. Plant Growth Regul 65: 343-358.
14. Gruszka D, Szarejko I, Maluszynski M (2011b) New allele of HvBRI1 gene encoding brassinosteroid receptor in barley. J Appl Genet 52: 257-268.
15. Hartwig T, Corvalan C, Best NB, Budka JS, Zhu JY, Choe S, Schulz B (2012) Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS ONE 7: e36625.
16. Hay A, Hake S (2004) The dominant mutant Wavy auricle in blade1 disrupts patterning in a lateral domain of the maize leaf. Plant Physiol 135: 300-308.
17. Hedden P (2003) The genes of the Green Revolution. Trends Genet 19: 5-9.
18. Hellewell KB, Rasmusson DC, Gallo-Meagher G (2000) Enhancing yield in semidwarf barley. Crop Sci 40: 352-358.
19. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ (2001) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci USA 98: 2065-2070.
20. Honda I, Zeniya H, Yoneyama K, Chono M, Kaneko S, Watanabe Y (2003) Uzu mutation in barley (Hordeum vulgare L.) reduces the leaf unrolling response to brassinolide. Biosci Biotechnol Biochem 67: 1194-1197.
21. Hong Z, Jin H, Tzfira T, Li J (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20: 3418-3429.
22. Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, Matsuoka M (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.
23. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474: 467-471.
24. Houston K, Druka A, Bonar N, Macaulay M, Lundqvist U, Franckowiak J, Morgante M, Stein N, Waugh R (2012) Analysis of the barley bract suppression gene Trd1. Theor Appl Genet 125: 33-45.
25. Houston K, McKim SM, Comadran J, Bonar N, Druka I, Uzrek N, Cirillo E, Guzy-Wrobelska J, Collins NC, Halpin C, et al (2013) Variation in the interaction between alleles of HvAPETALA2 and microRNA172 determines the density of grains on the barley inflorescence. Proc Natl Acad Sci USA 110: 16675-16680.
26. Janeczko A, Biesaga-Koscielniak J, Oklešťková J, Filek M, Dziurka M, Szarek-Łukaszewska G, Koscielniak J (2010) Role of 24-epibrassinolide in wheat production: physiological effects and uptake. J Agron Crop Sci 196: 311-321.
27. Jia Q, Zhang J, Westcott S, Zhang XQ, Bellgard M, Lance R, Li C (2009) GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Funct Integr Genomics 9: 255-262.
28. Kim BK, Fujioka S, Takatsuto S, TsujimotoM, Choe S (2008) Castasterone is a likely end product of brassinosteroid biosynthetic pathway in rice. Biochem Biophys Res Commun 374: 614-619.
29. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61: 681-704.
30. Kurowska M, Labocha-Pawłowska A, Gnizda D, Maluszynski M, Szarejko I (2012) Molecular analysis of point mutations in a barley genome exposed to MNU and gamma rays. Mutat Res 738-739: 52-70.
31. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
32. Marzec M, Melzer M, Szarejko I (2013) Asymmetric growth of root epidermal cells is related to the differentiation of root hair cells in Hordeum vulgare (L.). J Exp Bot 64: 5145-5155.
33. 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.
34. Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M, Sato M, Nasu S, Minobe Y (2002) Positional cloning of rice semidwarfing gene, sd-1: rice "green revolution gene" encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9: 11-17.
35. Nagano H, Onishi K, Ogasawara M, Horiuchi Y, Sano Y (2005) Genealogy of the "Green Revolution" gene in rice. Genes Genet Syst 80: 351-356.
36. National Climate Assessment Development Advisory Committee (2013) The U. S. Global Change Research Program http://ncadac. globalchange. gov/.
37. Noguchi T, Fujioka S, Choe S, Takatsuto S, Yoshida S, Yuan H, Feldmann KA, Tax FE (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol 121: 743-752.
38. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
39. Porter JR, Semenov MA (2005) Crop responses to climatic variation. Philos Trans R Soc Lond B Biol Sci 360: 2021-2035.
40. Prajapati RS, Sirajuddin M, Durani V, Sreeramulu S, Varadarajan R (2006) Contribution of cation-pi interactions to protein stability. Biochemistry 45: 15000-15010.
41. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18: 111-119.
42. Rajkumara S (2008) Lodging in cereals. Agric Rev 29: 55-60.
43. Saisho D, Tanno K, Chono M, Honda I, Kitano H, Takeda K (2004) Spontaneous brassinolide-insensitive barley mutants "uzu" adapted to East Asia. Breed Sci 54: 409-416.
44. Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, et al (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24: 105-109.
45. Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341: 889-892.
46. Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, KobayashiM, Khush GS, et al (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416: 701-702.
47. She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, Shi S, Wang J, Yang M, Wang ZY, et al (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474: 472-476.
48. Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S (2001) Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol 126: 770-779.
49. Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99: 9043-9048.
50. Sun Y, Han Z, Tang J, Hu Z, Chai C, Zhou B, Chai J (2013) Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 23: 1326-1329.
51. Swaczynová J, Novák O, Hauserová E, Funksová K, Šíša M, Strnad M (2007) New techniques for estimation of naturally occurring brassinosteroids. J Plant Growth Regul 26: 1-14.
52. The International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711-716.
53. Wada K, Kondo H, Marumo S (1985) A simple bioassay for brassinosteroids: A wheat leaf-unrolling test. Agric Biol Chem 49: 2249-2251.
54. Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch-Pedersen H, Holme IB (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. PlantMol Biol 83: 279-285.
55. Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24: 842-857.
56. Zakhrabekova S, Gough SP, Braumann I, Müller AH, Lundqvist J, Ahmann K, Dockter C, Matyszczak I, Kurowska M, Druka A, et al (2012) Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. Proc Natl Acad Sci USA 109: 4326-4331.