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Genetic linkage facilitates cloning of Ert-m regulating plant architecture in barley and identified a strong candidate of Ant1 involved in anthocyanin biosynthesis

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Abstract

The erectoides-m anthocyanin-less 1 (ert-m ant1) double mutants are among the very few examples of induced double mutants in barley. From phenotypic observations of mutant plants it is known that the Ert-m gene product regulates plant architecture whereas the Ant1 gene product is involved in anthocyanin biosynthesis. We used a near-isogenic line of the cultivar Bowman, BW316 (ert-m.34), to create four F2-mapping populations by crosses to the barley cultivars Barke, Morex, Bowman and Quench. We phenotyped and genotyped 460 plants, allowing the ert-m mutation to be mapped to an interval of 4.7 cM on the short arm of barley chromosome 7H. Bioinformatic searches identified 21 candidate gene models in the mapped region. One gene was orthologous to a regulator of Arabidopsis thaliana plant architecture, ERECTA, encoding a leucine-rich repeat receptor-like kinase. Sequencing of HvERECTA in barley ert-m mutant accessions identified severe DNA changes in 15 mutants, including full gene deletions in ert-m.40 and ert-m.64. Both deletions, additionally causing anthocyanin deficiency, were found to stretch over a large region including two putative candidate genes for the anthocyanin biosynthesis locus Ant1. Analyses of ert-m and ant1 single- and double-deletion mutants suggest Ant1 as a closely linked gene encoding a R2R3 myeloblastosis transcription factor.

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References

  • Allen AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    Article  Google Scholar 

  • Baker NR, Hardwick K (1973) Biochemical and physiological aspects of leaf development in cocoa (Theobroma cacao): i. Development of chlorophyll and photosynthetic activity. New Phytol 72:1315–1324

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bothmer R, van Hintum T, Knüpffer H, Sato K (2003) Diversity in barley. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Cockram J, White J, Zuluaga DL, Smith D, Comadran J, Macaulay M, Luo Z, Kearsey MJ, Werner P, Harrap D, Tapsell C, Liu H, Hedley PE, Stein N, Schulte D, Steuernagel B, Marshall DF, Thomas WTB, Ramsay L, Mackay I, Balding DJ, Waugh R, O’Sullivan DM, AGOUEB Consortium (2010) Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci USA 107(50):21611–21616

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delgado-Vargas F, Jiméne AR, Paredes-López O (2000) Natural pigments: carotenoids, anthocyanins, and betalains—characteristics, biosynthesis, processing and stability. Crit Rev Food Sci Nutr 40:173–289

    Article  CAS  PubMed  Google Scholar 

  • Dockter C, Gruszka D, Braumann I, Druka A, Druka I, Franckowiak J, Gough SP, Janeczko A, Kurowska M, Lundqvist J, Lundqvist U, Marzec M, Matyszczak I, Müller AH, Oklestkova J, Schulz B, Zakhrabekova S, Hansson M (2014) Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the “Green Revolution” genetic toolkit. Plant Physiol. doi:10.1104/pp.114.250738

    PubMed Central  PubMed  Google Scholar 

  • Dörte K-H, Nurisso A, Pietraszewska-Bogiel A, Mbengue M, Camut S, Timmers T, Pichereaux C, Rossignol M, Gadelle TWJ, Imberty A, Lefebvre B, Cullimore JV (2011) Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. J Biol Chem 286:11202–11210

    Article  Google Scholar 

  • Druka A, Kudrna D, Rostoks N, Brueggeman R, von Wettstein D, Kleinhofs A (2003) Chalcone isomerase gene from rice (Oryza sativa) and barley (Hordeum vulgare): physical, genetic and mutation mapping. Gene 302:171–178

    Article  CAS  PubMed  Google Scholar 

  • Druka A, Franckowiak J, Lundqvist U, Bonar N, Alexander J, Houston K, Radovic S, Shahinnia F, Vendramin V, Morgante M, Stein N, Waugh R (2011) Genetic dissection of barley morphology and development. Plant Physiol 155:617–627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Du H, Zhang L, Liu L, Tang XF, Yang WJ, Wu YM, Huang YB, Tang YX (2009) Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry (Moscow) 74:1–11

    Article  CAS  Google Scholar 

  • Franckowiak JD, Lundqvist U (2012) Descriptions of barley genetic stocks for 2012. BGN 42:36–173

    Google Scholar 

  • Gou X, He K, Yang H, Yuan T, Lin H, Clouse SD, Li J (2010) Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana. BMC Genom 11:19

    Article  Google Scholar 

  • Hanks SK, Quinn AM (1991) Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Meth Enzymol 200:38–62

    Article  CAS  PubMed  Google Scholar 

  • Himi E, Yamashita Y, Haruyama N, Yanagisawa T, Maekawa M, Taketa S (2012) Ant28 gene for proanthocyanidin synthesis encoding the R2R3 MYB domain protein (Hvmyb10) highly affects grain dormancy in barley. Euphytica 188:141–151

    Article  CAS  Google Scholar 

  • Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel J, Wilson IA, Chory J (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467–471

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • IBSC (International Barley Sequencing Consortium) (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716

    Google Scholar 

  • Jende-Strid B (1984) Coordinator’s report: anthocyanin genes. Barley Genet Newsl 14:76–79

    Google Scholar 

  • Jende-Strid B (1993) Genetic control of flavonoid biosynthesis in barley. Hereditas 119:187–204

    Article  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1994) A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33:3038–3049

    Article  CAS  PubMed  Google Scholar 

  • Kristiansen KN, Rohde W (1991) Structure of the Hordeum vulgare gene encoding dihydroflavonol-4-reductase and molecular analysis of ant18 mutants blocked in flavonoid synthesis. Mol Gen Genet 230:49–59

    Article  CAS  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Lease KA, Lau NY, Schuster RA, Torii KU, Walker JC (2001) Receptor serine/threonine protein kinases in signaling: analysis of the erecta receptor-like kinase of Arabidopsis thaliana. New Phytol 151:133–143

    Article  CAS  Google Scholar 

  • Lee DW, Brammeier S, Smith AP (1987) The selective advantage of anthocyanins in developing leaves of mango and cacao. Biotropica 19:40–49

    Article  Google Scholar 

  • Lundqvist U (1992) Mutation research in barley. Dissertation, Swedish University of Agricultural Sciences

  • Lundqvist U (2009) Eighty years of Scandinavian barley mutation genetics and breeding. In: Shu QY (ed) Induced mutations in the genomics era. FAO, Rome, pp 39–43

    Google Scholar 

  • Lundqvist U (2014) Scandinavian mutation research in barley—a historical review. Hereditas. doi:10.111/hrd2.2.00077

    PubMed  Google Scholar 

  • Mayer KFX, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubalakova M, Suchankova P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Dolezel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Michalek W, Künzel G, Graner A (1999) Sequence analysis and gene identification in a set of mapped RFLP markers in barley (Hordeum vulgare). Genome 42:849–853

    Article  CAS  PubMed  Google Scholar 

  • Nakamura A, Fujioka S, Sunohara H, Kamiya N, Hong Z, Inukai Y, Miura K, Takatsuto S, Yoshida S, Ueguchi-Tanaka M, Hasegawa Y, Kitano Matsuoka M (2006) The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol 140:580–590

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ngaki MN, Louie GV, Philippe RN, Manning G, Pojer F, Bowman ME, Li L, Larsen E, Wurtele ES, Noel JP (2012) Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis. Nature 485:530–533

    CAS  PubMed  Google Scholar 

  • Noodén LD, Hillsberg JW, Schneider MJ (1996) Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiol Plant 96:491–495

    Article  Google Scholar 

  • Oh M-H, Wanng X, Kim SY, Wu X, Clouse SD, Huber SC (2014) The carboxy-terminus of BAK1 regulates kinase activity and is required for normal growth of Arabidopsis. Front Plant Sci. 5:16

    PubMed Central  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Persson G, Hagberg A (1969) Induced variation in a quantitative character in barley. Morphology and cytogenetics of erectoides mutants. Hereditas 61:115–178

    Article  Google Scholar 

  • Pilu R, Piazza P, Petroni K, Ronchi A, Martin C, Tonelli C (2003) pl-bol3, a complex allele of the anthocyanin regulatory pl1 locus that arose in a naturally occurring maize population. Plant J 36:510–516

    Article  CAS  PubMed  Google Scholar 

  • She J, Han Z, Kim T-W, Wang J, Cheng W, Chang J, Shi S, Wang J, Yang M, Wang Z-Y, Chai J (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474:472–476

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shih CH, Chu H, Tang LK, Sakamoto W, Maekawa M, Chu IK, Wang M, Lo C (2014) Functional characterization of key structural genes in rice flavonoid biosynthesis. Plant Cell Environ 37:1716–1721

    Article  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh R, Low E-TL, Ooi LC-L, Ong-Abdullah M, Nookiah R, Ting N-C, Marjuni M, Chan P-L, Ithnin M, Manaf MAA, Nagappan J, Chan K-L, Rosli R, Halim MA, Azizi N, Budiman MA, Lakey N, Bacher B, van Brunt A, Wang C (2014) The oil palm VIRESCENS gene controls fruit colour and encodes a R2R3-MYB. Nat Commun 5:4106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opinion Plant Biol 4:447–456

    Article  CAS  Google Scholar 

  • Torii KU (2013) Mix-and-match: ligand-receptor pairs in stomatal development and beyond. Trends Plant Sci 17:711–719

    Article  Google Scholar 

  • Torii K, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier R, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8:735–746

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Zanten M, Snoek LB, Proveniers MCG, Peeters AJM (2009) The many functions of ERECTA. Trends Plant Sci 14:214–218

    Article  PubMed  Google Scholar 

  • von Wettstein D, Jende-Strid B, Ahrenst-Larsen B, Erdal K (1977) Biochemical mutant in barley renders chemical stabilization of beer superfluous. Carlsberg Res Commun 42:341–351

    Article  Google Scholar 

  • Wang X, Olsen O, Knudsen S (1993) Expression of the dihydroflavonol reductase gene in an anthocyanin-free barley mutant. Hereditas 119:67–75

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Liu J, Sudom A, Ayres M, Li S, Wesche H, Powers JP, Walker NP (2006) Crystal structures of IRAK-4 kinase in complex with inhibitors: a serine/threonine kinase with tyrosine as a gatekeeper. Structure 14:1835–1844

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Huang J, Li B, Wang Y (2008) Is kinase activity essential for biological functions of BRI1? Cell Res 18:472–478

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi M, Toda S, Tasaki K (2014) The novel allele of the LhMYB12 gene is involved in splatter-type spot formation on the flower tepals of Asiatic hybrid lilies (Lilium spp.). New Phytologist 201:1009–1020

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Mateusz Kania for excellent technical assistance. This work was supported by the Carlsberg Foundation, GUDP (Denmark, 34009-12-0522), Deutsche Forschungsgemeinschaft (Germany, DO1482/1-1), the Nilsson-Ehle Foundation at the Royal Physiographic Society in Lund, and the Erik Philip-Sörensen Foundation.

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    Authors and Affiliations

    1. Carlsberg Laboratory, Gamle Carlsberg Vej 10, 1799, Copenhagen V, Denmark

      Christoph Dockter, Katharina Ahmann, Ilka Braumann, Simon P. Gough & Toni Wendt

    2. Nordic Genetic Resource Center (NordGen), Smedjevägen 3, 23053, Alnarp, Sweden

      Udda Lundqvist

    3. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), OT Gatersleben, 06466, Stadt Seeland, Germany

      Martin Mascher & Nils Stein

    4. Department of Biology, Lund University, Sölvegatan 35, 22362, Lund, Sweden

      Shakhira Zakhrabekova & Mats Hansson

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    1. Shakhira Zakhrabekova
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    Carlsberg has supported and financed a major part of this work and the right to publish is granted under the provision that Carlsberg maintains all rights (incl. future intellectual property rights granted to new industrial collaborators) to use the genes, traits and phenotypes described in the publication to advance current and future commercial interests of the Carlsberg Group.

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    Shakhira Zakhrabekova and Christoph Dockter have contributed equally to this work.

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    Zakhrabekova, S., Dockter, C., Ahmann, K. et al. Genetic linkage facilitates cloning of Ert-m regulating plant architecture in barley and identified a strong candidate of Ant1 involved in anthocyanin biosynthesis. Plant Mol Biol 88, 609–626 (2015). https://doi.org/10.1007/s11103-015-0350-x

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