Hairy Canola (Brasssica napus) re-visited: Down-regulating TTG1 in an AtGL3-enhanced hairy leaf background improves growth, leaf trichome coverage, and metabolite gene expression diversity

详细信息    查看全文

• 作者：Ushan I. Alahakoon ; Ali Taheri ; Naghabushana K. Nayidu ; Delwin Epp…
• 关键词：Brassica napus ; GL3 and TTG1 manipulation ; Trichome patterning and growth ; Broad metabolic gene expression changes ; Q ; PCR and RNA sequencing
• 刊名：BMC Plant Biology
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：16
• 期：1
• 全文大小：4,149 KB
• 参考文献：1.Balkunde R, Pesch M, Hülskamp M. Trichome Patterning in Arabidopsis thaliana: From Genetic to Molecular Models. In: Marja CPT, editor. Curr Top Dev Biol, vol. 91. New York: Academic; 2010. p. 299–321.
  2.Ishida T, Kurata T, Okada K, Wada T. A Genetic Regulatory Network in the Development of Trichomes and Root Hairs. Annu Rev Plant Biol. 2008;59:365–86.PubMed CrossRef
  3.Pesch M, Hülskamp M. One, two, three…models for trichome patterning in Arabidopsis? Curr Opin Plant Biol. 2009;12:587–92.PubMed CrossRef
  4.Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ. The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol. 2009;26:85–98.PubMed CrossRef
  5.Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, et al. Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics. 2005;171:765–81.PubMed PubMedCentral CrossRef
  6.Parkin IA, Clarke WE, Sidebottom C, Zhang W, Robinson SJ, Links MG, et al. Towards unambiguous transcript mapping in the allotetraploid Brassica napus. Genome. 2010;53:929–38.PubMed CrossRef
  7.Robinson S, Tang L, Mooney B, McKay S, Clarke W, Links M, et al. An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches. BMC Plant Biol. 2009;9:101.PubMed PubMedCentral CrossRef
  8.Taheri A, Gao P, Yu M, Cui D, Regan S, Parkin I, et al. A landscape of hairy and twisted: hunting for new trichome mutants in the Saskatoon Arabidopsis T-DNA population. Plant Biol (Stuttg). 2015;17:384–94.CrossRef
  9.Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, et al. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell. 1999;11:1337–49.PubMed PubMedCentral CrossRef
  10.Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development (Camb). 2003;130:4859–69.CrossRef
  11.Marks MD, Feldmann KA. Trichome development in Arabidopsis thaliana. I. T-DNA tagging of the GLABROUS1 gene. Plant Cell. 1989;1:1043–50.PubMed PubMedCentral CrossRef
  12.Kirik V, Schnittger A, Radchuk V, Adler K, Hulskamp M, Baumlein H. Ectopic expression of the Arabidopsis AtMYB23 gene induces differentiation of trichome cells. Dev Biol. 2001;235:366–77.PubMed CrossRef
  13.Payne CT, Zhang F, Lloyd AM. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics. 2000;156:1349–62.PubMed PubMedCentral
  14.Larkin JC, Oppenheimer DG, Lloyd AM, Paparozzi ET, Marks MD. Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development. Plant Cell. 1994;6:1065–76.PubMed PubMedCentral CrossRef
  15.Marks MD. Molecular genetic analysis of trichome development in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol. 1997;48:137–63.PubMed CrossRef
  16.West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, et al. LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon Identity in Arabidopsis. Plant Cell. 1994;6:1731–45.PubMed PubMedCentral CrossRef
  17.Gao Y, Gong XM, Cao WH, Zhao JF, Fu LQ, Wang XC, et al. SAD2 in Arabidopsis functions in trichome initiation through mediating GL3 function and regulating GL1, TTG1 and GL2 expression. J Integr Plant Biol. 2008;50:906–17.PubMed CrossRef
  18.Johnson CS, Kolevski B, Smyth DR. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell. 2002;14:1359–75.PubMed PubMedCentral CrossRef
  19.Rerie WG, Feldmann KA, Marks MD. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 1994;8:1388–99.PubMed CrossRef
  20.Wang S, Chen J-G. Arabidopsis transient expression analysis reveals that activation of GLABRA2 may require concurrent binding of GLABRA1 and GLABRA3 to the promoter of GLABRA2. Plant Cell Physiol. 2008;49:1792–804.PubMed CrossRef
  21.Szymanski DB, Marks MD. GLABROUS1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell. 1998;10:2047–206222.PubMed PubMedCentral CrossRef
  22.Wang S, Barron C, Schiefelbein J, Chen JG. Distinct relationships between GLABRA2 and single-repeat R3 MYB transcription factors in the regulation of trichome and root hair patterning in Arabidopsis. New Phytol. 2010;185:387–400.PubMed CrossRef
  23.Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, et al. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell. 2007;19:2531–43.PubMed PubMedCentral CrossRef
  24.Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, et al. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. Embo J. 2002;21:5036–46.PubMed PubMedCentral CrossRef
  25.Wada T, Tachibana T, Shimura Y, Okada K. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science (New York, NY). 1997;277:1113–6.CrossRef
  26.Kirik V, Simon M, Huelskamp M, Schiefelbein J. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol. 2004;268:506–13.PubMed CrossRef
  27.Tominaga R, Iwata M, Sano R, Inoue K, Okada K, Wada T. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development. 2008;135:1335–45.PubMed CrossRef
  28.Wang S, Kwak S-H, Zeng Q, Ellis BE, Chen X-Y, Schiefelbein J, et al. TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development. 2007;134:3873–82.PubMed CrossRef
  29.Gan L, Xia K, Chen J-G, Wang S. Functional characterization of TRICHOMELESS2, a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis. BMC Plant Biol. 2011;11:176.PubMed PubMedCentral CrossRef
  30.Larkin JC, Young N, Prigge M, Marks MD. The control of trichome spacing and number in Arabidopsis. Development. 1996;122:997–1005.PubMed
  31.Zhang J, Lu Y, Yuan Y, Zhang X, Geng J, Chen Y, et al. Map-based cloning and characterization of a gene controlling hairiness and seed coat color traits in Brassica rapa. Plant Mol Biol. 2009;69:553–63.PubMed CrossRef
  32.Nayidu NK, Kagale S, Taheri S, Withana-Gamage TS, Parkin AP, Sharpe AG, et al. Comparison of five major trichome regulatory genes in Brassica villosa with orthologues within the Brassicaceae. PLoS One. 2014;9:e95877.PubMed PubMedCentral CrossRef
  33.Nayidu NK, Tan Y, Taheri A, Li X, Bjorndahl TC, Nowak J, et al. Brassica villosa, a system for studying non-glandular trichomes and genes in the Brassicas. Plant Mol Biol. 2014;85:519–39.PubMed CrossRef
  34.Palaniswamy P, Bodnaryk RP. A wild Brassica from Sicily provides trichome-based resistance against flea beetles, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae). Can Entomol. 1994;126:1119–30.CrossRef
  35.Gruber MY, Wang S, Ethier S, Holowachuk J, Bonham-Smith PC, Soroka J, et al. “HAIRY CANOLA”--Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol Biol. 2006;60:679–98.PubMed CrossRef
  36.Soroka JJ, Holowachuk JM, Gruber MY, Grenkow LF. Feeding by flea beetles (Coleoptera: Chrysomelidae; Phyllotreta spp.) is decreased on canola (Brassica napus) seedlings with increased trichome density. J Econ Entomol. 2011;104:125–36.PubMed CrossRef
  37.Alahakoon U, Adamson, J, Grenkow L, Soroka J, Bonham-Smith P, and Gruber M. Field growth traits and insect-host plant interactions of two transgenic canola lines with elevated trichome numbers. Can Entomol. 2016; 148: Accepted.
  38.Nagaharu U. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. J Japan Bot. 1935;7:389–452.
  39.The Brassica rapa Genome Sequencing Project Consortium. The genome of the mesopolyploid crop species Brassica rapa. Nat Genet. 2011;43:1035–9.CrossRef
  40.Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, et al. Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol. 2014;15:R77.PubMed PubMedCentral CrossRef
  41.De Block M, De Brouwer D, Tenning P. Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the BAR and NEO genes in the transgenic plants. Plant Physiol. 1989;91:694–701.PubMed PubMedCentral CrossRef
  42.Ushan AI. Effect of TRANSPARENT TESTA GLABRA1 on trichome development, growth, and insect resistance in a Brassica napus AtGLABRA3+ background. PhD thesis, Department of Biology, University of Saskatchewan; 2012.
  43.Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, et al. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res. 2012;40(Web Server issue):W622–7.PubMed PubMedCentral CrossRef
  44.Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562–78.PubMed PubMedCentral CrossRef
  45.Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004;37:914–39.PubMed CrossRef
  46.SAS Institute. SAS User’s Guide, Version 9.2. Cary: SAS Institute; 2008.
  47.Sawa S. Overexpression of the AtMYBL2 gene represses trichome development in Arabidopsis. DNA Res. 2002;9:31–4.PubMed CrossRef
  48.Kirk CA. The DELLA protein family and gibberellin signal transduction: A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Biochemistry. Palmerston North, New Zealand: Massey University; 2013.
  49.Koornneef M. The complex syndrome of TTG mutants. Arabidopsis Information Service. 1981;18:6.
  50.Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development. 2008;135:1991–9.PubMed CrossRef
  51.Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-ccale biological data sets. PLoS One. 2007;2:e718. doi:10.​1371/​journal.​pone.​0000718 .PubMed PubMedCentral CrossRef
  52.Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005;37:501–6. Epub Apr 3.PubMed CrossRef
  53.Laubinger S, Zeller G, Henz SR, Sachsenberg T, Widmer CK, Naouar N, et al. At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol. 2008;9:R112. doi:10.​1186/​gb-2008-9-7-r112 .PubMed PubMedCentral CrossRef
  54.Hulskamp M, Misra S, Jurgens G. Genetic dissection of trichome cell development in Arabidopsis. Cell. 1994;76:555–66.PubMed CrossRef
  55.Szymanski DB, Jilk RA, Pollock SM, Marks MD. Control of GL2 expression in Arabidopsis leaves and trichomes. Development. 1998;125:1161–71.PubMed
  56.Hung CY, Lin Y, Zhang M, Pollock S, Marks MD, Schiefelbein J. A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol. 1998;117:73–84.PubMed PubMedCentral CrossRef
  57.Larkin JC, Walker JD, Bolognesi-Winfield AC, Gray JC, Walker AR. Allele-specific interactions between ttg and gl1 during trichome development in Arabidopsis thaliana. Genetics. 1999;151:1591–604.PubMed PubMedCentral
  58.Morohashi K, Zhao M, Yang M, Read B, Lloyd A, Lamb R, et al. Participation of the Arabidopsis bHLH Factor GL3 in trichome initiation regulatory events. Plant Physiol (Rockv). 2007;145:736–46.CrossRef
  59.Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L. TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J. 2004;39:366–80.PubMed CrossRef
  60.Petroni K, Tonelli C. Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci. 2011;181:219–29.PubMed CrossRef
  61.Feyissa DN, Lovdal T, Olsen KM, Slimestad R, Lillo C. The endogenous GL3, but not EGL3, gene is necessary for anthocyanin accumulation as induced by nitrogen depletion in Arabidopsis rosette stage leaves. Planta. 2009;230:747–54.PubMed CrossRef
  62.Gonzalez A, Zhao M, Leavitt JM, Lloyd AM. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 2008;53:814–27.PubMed CrossRef
  
• 作者单位：Ushan I. Alahakoon (1) (3)
  Ali Taheri (1) (4)
  Naghabushana K. Nayidu (1) (2)
  Delwin Epp (1)
  Min Yu (1)
  Isobel Parkin (1)
  Dwayne Hegedus (1)
  Peta Bonham-Smith (2)
  Margaret Y. Gruber (1)
  
  1. Saskatoon Research Centre, Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, SK, S7N0X2, Canada
  3. Present address: DOW Agro-Sciences, 101-421 Downey Rd., Saskatoon, SK, S7N4L8, Canada
  4. Present address: Department of Agriculture and Environmental Sciences, Tennessee State University, 3500 John A Merritt Blvd., Nashville, TN, 37209, USA
  2. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N5E2, Canada
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Through evolution, some plants have developed natural resistance to insects by having hairs (trichomes) on leaves and other tissues. The hairy trait has been neglected in Brassica breeding programs, which mainly focus on disease resistance, yield, and overall crop productivity. In Arabidopsis, a network of three classes of proteins consisting of TTG1 (a WD40 repeat protein), GL3 (a bHLH factor) and GL1 (a MYB transcription factor), activates trichome initiation and patterning. Introduction of a trichome regulatory gene AtGL3 from Arabidopsis into semi-glabrous Brassica napus resulted in hairy canola plants which showed tolerance to flea beetles and diamondback moths; however plant growth was negatively affected. In addition, the role of BnTTG1 transcription in the new germplasm was not understood.