Plant Trait Gene Expression Cassette Design

  • Michael Nuccio
  • Xi Chen
  • Jared Conville
  • Ailing Zhou
  • Xiaomei Liu

Abstract

Plant biotechnology depends on robust control of trait gene expression to produce an adequate level of protein or RNA in the appropriate cells at the correct time. Early biotechnology products depended on high protein production in most plant cells, and relied on relatively few well-characterized “promoters.” This demand continues and has expanded into other classes of expression control, such as tissue specificity and environmental responsiveness, as new trait technologies are pursued. Genomic information can be leveraged to meet this demand now and well into the future. A method has been developed of identifying donor genes in genomic data, and simplifying their annotation to facilitate design and development of effective expression cassettes. This approach greatly reduces the effort and expense of producing novel trait gene expression tools. Coupled with chemical DNA synthesis technology, this approach makes it possible to develop reliable expression cassettes from virtually any plant gene.

Keywords

Plant-gene regulation Promoter Terminator Transgene expression control Transgene cassette Transgene design Promoter discovery 

References

  1. Allen GC, Spiker S, Thompson WF (2000) Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol Biol 43:361–376CrossRefPubMedGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466CrossRefPubMedGoogle Scholar
  4. An G (1986) Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoter in transformed tobacco cells. Plant Physiol 81:86–91PubMedCentralCrossRefPubMedGoogle Scholar
  5. Ancillo G, Hoegen E, Kombrink E (2003) The promoter of the potato chitinase C gene directs expression to epidermal cells. Planta 217:566–576CrossRefPubMedGoogle Scholar
  6. Barker T, Campos H, Cooper M, Dolan D, Edmeades G, Habben J, Schussler J, Write D, Zinselmeier C (2005) Improving drought tolerance in maize. Plant Breed Rev 25:173–253Google Scholar
  7. Bartlett JG, Snape JW, Harwood WA (2009) Intron-mediated enhancement as a method for increasing transgene expression levels in barley. Plant Biotechnol J 7:856–866CrossRefPubMedGoogle Scholar
  8. Benfey PN, Chua NH (1990) The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250:959–966CrossRefPubMedGoogle Scholar
  9. Birch RG (1997) PLANT TRANSFORMATION: problems and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48:297–326CrossRefPubMedGoogle Scholar
  10. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280CrossRefPubMedGoogle Scholar
  11. Butaye KM, Goderis IJ, Wouters PF, Pues JM, Delaure SL, Broekaert WF, Depicker A, Cammue BP, De Bolle MF (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39:440–449CrossRefPubMedGoogle Scholar
  12. Cattivelli L, Rizza F, Badeck F-W, Mazzucotelli E, Mastrangelo AM, Francia E, Mare C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14CrossRefGoogle Scholar
  13. Chang CW, Sun TP (2002) Characterization of cis-regulatory regions responsible for developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant Mol Biol 49:579–589CrossRefPubMedGoogle Scholar
  14. Chen QJ, Zhou HM, Chen J, Wang XC (2006) A Gateway-based platform for multigene plant transformation. Plant Mol Biol 62:927–936CrossRefPubMedGoogle Scholar
  15. Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y, Hetzel JA, Kuo F, Kim J, Cokus SJ, Casero D, Bernal M, Huijser P, Clark AT, Kramer U, Merchant SS, Zhang X, Jacobsen SE, Pellegrini M (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466:388–392.PubMedCentralCrossRefPubMedGoogle Scholar
  16. Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5:213–218CrossRefPubMedGoogle Scholar
  17. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Current Biol 15:1196–1200CrossRefGoogle Scholar
  18. Dalakouras A, Dadami E, Zwiebel M, Krczal G, Wassenegger M (2012) Transgenerational maintenance of transgene body CG but not CHG and CHH methylation. Epigenetics 7:1071–1078PubMedCentralCrossRefPubMedGoogle Scholar
  19. Das M, Harvey I, Chu LL, Sinha M, Pelletier J (2001) Full-length cDNAs: more than just reaching the ends. Physiol Genomics 6:57–80PubMedGoogle Scholar
  20. De Bodt S, Raes J, Van de Peer Y, Theissen G (2003) And then there were many: MADS goes genomic. Trends Plant Sci 8:475–483CrossRefPubMedGoogle Scholar
  21. Duvick J, Fu A, Muppirala U, Sabharwal M, Wilkerson MD, Lawrence CJ, Lushbough C, Brendel V (2008) PlantGDB: a resource for comparative plant genomics. Nucleic Acids Res 36:D959–965Google Scholar
  22. Emami S, Arumainayagam D, Korf I, Rose AB (2013) The effects of a stimulating intron on the expression of heterologous genes in Arabidopsis thaliana. Plant Biotechnol J 11:555–563CrossRefPubMedGoogle Scholar
  23. Flavell RB (1994) Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc Natl Acad Sci U S A 91:3490–3496PubMedCentralCrossRefPubMedGoogle Scholar
  24. Fujisawa M, Takita E, Harada H, Sakurai N, Suzuki H, Ohyama K, Shibata D, Misawa N (2009) Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation. J Exp Bot 60:1319–1332CrossRefPubMedGoogle Scholar
  25. Gallie DR, Walbot V (1992) Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucleic Acids Res 20:4631–4638PubMedCentralCrossRefPubMedGoogle Scholar
  26. Gibson DG, Benders GA, Axelrod KC, Zaveri J, Algire MA, Moodie M, Montague MG, Venter JC, Smith HO, Hutchison CA 3rd (2008) One-step assembly in yeast of 25 overlapping DNA fragments to form a complete synthetic mycoplasma genitalium genome. Proc Natl Acad Sci U S A 105:20404–20409PubMedCentralCrossRefPubMedGoogle Scholar
  27. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi ZQ, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA, 3rd, Smith HO, Venter JC (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:52–56CrossRefPubMedGoogle Scholar
  28. Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci U S A 85:7089–7093PubMedCentralCrossRefPubMedGoogle Scholar
  29. Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20:1203–1207CrossRefPubMedGoogle Scholar
  30. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. Japonica). Science 296:92–100CrossRefPubMedGoogle Scholar
  31. Gruissem W (1990) Of fingers, zippers and boxes. Plant Cell 2:827–828PubMedCentralCrossRefGoogle Scholar
  32. Halpin C (2005) Gene stacking in transgenic plants–the challenge for 21st century plant biotechnology. Plant Biotechnol J 3:141–155CrossRefPubMedGoogle Scholar
  33. Halpin C, Cooke SE, Barakate A, Amrani AE, Ryan MD (1999) Self-processing 2A-polyproteins-a system for co-ordinate expression of multiple proteins in transgenic plants. Plant J 17:453–459CrossRefPubMedGoogle Scholar
  34. Hunt AG (1994) Messenger RNA 3′ end formation in plants. Annu Rev Plant Biol 45:47–60CrossRefGoogle Scholar
  35. Hunt AG (2008) Messenger RNA 3′ end formation in plants. Curr Top Microbiol Immunol 326:151–177PubMedGoogle Scholar
  36. Ingelbrecht IL, Herman LM, Dekeyser RA, Van Montagu MC, Depicker AG (1989) Different 3′ end regions strongly influence the level of gene expression in plant cells. Plant Cell 1:671–680PubMedCentralPubMedGoogle Scholar
  37. Ingham DJ, Beer S, Money S, Hansen G (2001) Quantitative real-time PCR assay for determining copy number in transformed plants. Biotech 31:132–140Google Scholar
  38. Jiang L, Yu X, Qi X, Yu Q, Deng S, Bai B, Li N, Zhang A, Zhu C, Liu B, Pang J (2013) Multigene engineering of starch biosynthesis in maize endosperm increases the total starch content and the proportion of amylose. Transgenic Res 22:1133–1142CrossRefPubMedGoogle Scholar
  39. Jordano J, Almoguera C, Thomas TL (1989) A sunflower helianthinin gene upstream sequence ensemble contains an enhancer and sites of nuclear protein interaction. Plant Cell 1:855–866PubMedCentralCrossRefPubMedGoogle Scholar
  40. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, Segal E (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458:362–366PubMedCentralCrossRefPubMedGoogle Scholar
  41. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ, Weber RJ, Haussler D, Kent WJ (2003) The UCSC Genome Browser Database. Nucleic Acids Res 31:51–54PubMedCentralCrossRefPubMedGoogle Scholar
  42. Katagiri F, Chua NH (1992) Plant transcription factors: present knowledge and future challenges. Trends Genet 8:22–27CrossRefPubMedGoogle Scholar
  43. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler F, Peterhansel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnol 25:593–599CrossRefGoogle Scholar
  44. Khurana R, Kapoor S, Tyagi AK (2013) Spatial and temporal activity of upstream regulatory regions of rice anther-specific genes in transgenic rice and Arabidopsis. Transgenic Res 22:31–46CrossRefPubMedGoogle Scholar
  45. Kohli A, Griffiths S, Palacios N, Twyman RM, Vain P, Laurie DA, Christou P (1999) Molecular characterization of transforming plasmid rearrangements in transgenic rice reveals a recombination hotspot in the CaMV 35S promoter and confirms the predominance of microhomology mediated recombination. Plant J 17:591–601CrossRefPubMedGoogle Scholar
  46. Korf IF, Rose AB (2009) Applying word-based algorithms: the IMEter. Methods Mol Biol 553:287–301CrossRefPubMedGoogle Scholar
  47. Koyama T, Ono T, Shimizu M, Jinbo T, Mizuno R, Tomita K, Mitsukawa N, Kawazu T, Kimura T, Ohmiya K, Sakka K (2005) Promoter of Arabidopsis thaliana phosphate transporter gene drives root-specific expression of transgene in rice. J Biosci Bioengineer 99:38–42CrossRefGoogle Scholar
  48. Kozak M (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1–34CrossRefPubMedGoogle Scholar
  49. Koziel MG, Carozzi NB, Desai N (1996) Optimizing expression of transgenes with an emphasis on post-transcriptional events. Plant Mol Biol 32:393–405CrossRefPubMedGoogle Scholar
  50. Kudla G, Murray AW, Tollervey D, Plotkin JB (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255–258PubMedCentralCrossRefPubMedGoogle Scholar
  51. Law JA, Jacobsen SE (2009) Dynamic DNA methylation. Science 323:1568–1569CrossRefPubMedGoogle Scholar
  52. Lee M, Nuccio M, Clarke J, Inventors (2013) Plant regulatory Sequences. United States Patent 8,344,209, granted January 1, 2013Google Scholar
  53. Lessard PA, Kulaveerasingam, H, York, GM, Strong, A, Sinskey, AJ (2002) Manipulating gene expression for the metabolic engineering of plants. Metabolic Eng 4:67–79CrossRefGoogle Scholar
  54. Liang C, Jaiswal P, Hebbard C, Avraham S, Buckler ES, Casstevens T, Hurwitz B, McCouch S, Ni J, Pujar A, Ravenscroft D, Ren L, Spooner W, Tecle I, Thomason J, Tung CW, Wei X, Yap I, Youens-Clark K, Ware D, Stein L (2008) Gramene: a growing plant comparative genomics resource. Nucleic Acids Res 36:D947–953CrossRefGoogle Scholar
  55. Lidder P, Gutierrez RA, Salome PA, McClung CR, Green PJ (2005) Circadian control of messenger RNA stability. association with a sequence-specific messenger RNA decay pathway. Plant Physiol 138:2374–2385PubMedCentralCrossRefPubMedGoogle Scholar
  56. Liu ZZ, Wang JL, Huang X, Xu WH, Liu ZM, Fang RX (2003) The promoter of a rice glycine-rich protein gene, Osgrp-2, confers vascular-specific expression in transgenic plants. Planta 216:824–833PubMedGoogle Scholar
  57. Lopez I, Anthony RG, Maciver SK, Jiang CJ, Khan S, Weeds AG, Hussey PJ (1996) Pollen specific expression of maize genes encoding actin depolymerizing factor-like proteins. Proc Natl Acad Sci U S A 93:7415–7420PubMedCentralCrossRefPubMedGoogle Scholar
  58. Luehrsen KR, Walbot V (1991) Intron enhancement of gene expression and the splicing efficiency of introns in maize cells. Mol Gen Genet 225:81–93CrossRefPubMedGoogle Scholar
  59. Maas C, Laufs J, Grant S, Korfhage C, Werr W (1991) The combination of a novel stimulatory element in the first exon of the maize Shrunken-1 gene with the following intron 1 enhances reporter gene expression up to 1000-fold. Plant Mol Biol 16:199–207CrossRefPubMedGoogle Scholar
  60. McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163–171PubMedCentralCrossRefPubMedGoogle Scholar
  61. Mehrotra R, Gupta G, Sethi R, Bhalothia P, Kumar N, Mehrotra S (2011) Designer promoter: an artwork of cis engineering. Plant Mol Biol 75:527–536CrossRefPubMedGoogle Scholar
  62. Moore MJ, Proudfoot NJ (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136:688–700CrossRefPubMedGoogle Scholar
  63. Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Perez Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci U S A 106:7762–7767PubMedCentralCrossRefPubMedGoogle Scholar
  64. Nuccio M, Inventor (2013) Guard cell expression cassettes compositions and methods of use thereof. United States Patent Application No. 61/787,781, filed 15 March 2013Google Scholar
  65. Nuccio M, Richmond A, Inventors (2013) Epidermal tissue promoter derived from potato for monocots. United States Patent 8,304,607, granted 6 Nov 2012Google Scholar
  66. Nuccio ML (1997) Identification and characterization of ATS1 and ATS3, two novel seed-specific genes in Arabidopsis thaliana. PhD Thesis, Texas A & M University, College StationGoogle Scholar
  67. Nuccio ML, Lagrimini LM, Meghji M, Inventors (2012) Regulatory sequences for expressing gene products in plant reproductive tissue. United States Patent 8,129,588, granted 6 March 2012Google Scholar
  68. Nunberg AN, Li Z, Bogue MA, Vivekananda J, Reddy AS, Thomas TL (1994) Developmental and hormonal regulation of sunflower helianthinin genes: proximal promoter sequences confer regionalized seed expression. Plant Cell 6:473–486PubMedCentralCrossRefPubMedGoogle Scholar
  69. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–887CrossRefGoogle Scholar
  70. Palmer KE, Thomson JA, Rybicki EP (1999) Generation of maize cell lines containing autonomously replicating maize streak virus-based gene vectors. Arch Virol 144:1345–1360CrossRefPubMedGoogle Scholar
  71. Parra G, Bradnam K, Rose AB, Korf I (2011) Comparative and functional analysis of intron-mediated enhancement signals reveals conserved features among plants. Nucleic Acids Res 39:5328–5337PubMedCentralCrossRefPubMedGoogle Scholar
  72. Peremarti A, Twyman RM, Gomez-Galera S, Naqvi S, Farre G, Sabalza M, Miralpeix B, Dashevskaya S, Yuan D, Ramessar K, Christou P, Zhu C, Bassie L, Capell T (2010) Promoter diversity in multigene transformation. Plant Mol Biol 73:363–378CrossRefPubMedGoogle Scholar
  73. Pimentel DS, Raven PH (2000) Bt corn pollen impacts on nontarget lepidoptera: assessment of effects in nature. Proc Natl Acad Sci U S A 97:8198–8199PubMedCentralCrossRefPubMedGoogle Scholar
  74. Potenza C, Aleman L, Sengupta-Gopalan C (2004) Targeting Transgene expression in research, agrigultural, and environmental applications: promoters used in plant transformation. In Vitro Cell Dev Biol Plant 40:1–22CrossRefGoogle Scholar
  75. Que Q, Chilton MD, de Fontes CM, He C, Nuccio M, Zhu T, Wu Y, Chen JS, Shi L (2010) Trait stacking in transgenic crops: challenges and opportunities. GM Crops 1:220–229CrossRefPubMedGoogle Scholar
  76. Raab JR, Kamakaka RT (2010) Insulators and promoters: closer than we think. Nat Rev Genet 11:439–446PubMedCentralCrossRefPubMedGoogle Scholar
  77. Ritchie SW, Hanway JJ, Benson GO (1992) How a corn plant develops. Special Report No. 48, Iowa State University of Science and Technology, Ames, Iowa: 1–21Google Scholar
  78. Rombauts S, Florquin K, Lescot M, Marchal K, Rouze P, van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiol 132:1162–1176PubMedCentralCrossRefPubMedGoogle Scholar
  79. Rose AB (2004) The effect of intron location on intron-mediated enhancement of gene expression in Arabidopsis. Plant J 40:744–751CrossRefPubMedGoogle Scholar
  80. Rose AB, Elfersi T, Parra G, Korf I (2008) Promoter-proximal introns in Arabidopsis thaliana are enriched in dispersed signals that elevate gene expression. Plant Cell 20:543–551PubMedCentralCrossRefPubMedGoogle Scholar
  81. Rothnie HM (1996) Plant mRNA 3′-end formation. Plant Mol Biol 32:43–61CrossRefPubMedGoogle Scholar
  82. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, pp 999Google Scholar
  83. Sanger M, Daubert S, Goodman RM (1990) Characteristics of a strong promoter from figwort mosaic virus: comparison with the analogous 35S promoter from cauliflower mosaic virus and the regulated mannopine synthase promoter. Plant Mol Biol 14:433–443CrossRefPubMedGoogle Scholar
  84. Schulze-Lefert P, Becker-Andre M, Schulz W, Hahlbrock K, Dangl JL (1989) Functional architecture of the light-responsive chalcone synthase promoter from parsley. Plant Cell 1:707–714PubMedCentralCrossRefPubMedGoogle Scholar
  85. Schünmann PHD, Surin B, Waterhouse PM (2003) A suite of novel promoters and terminators for plant biotechnology. II. The pPLEX series for use in monocots. Funct Plant Biol 30:453–460CrossRefGoogle Scholar
  86. Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365PubMedCentralCrossRefPubMedGoogle Scholar
  87. Skirycz A, Vandenbroucke K, Clauw P, Maleux K, De Meyer B, Dhondt S, Pucci A, Gonzalez N, Hoeberichts F, Tognetti VB, Galbiati M, Tonelli C, Van Breusegem F, Vuylsteke M, Inze D (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nature Biotechnol 29:212–214CrossRefGoogle Scholar
  88. Springer NM (2013) Epigenetics and crop improvement. Trends Genet 29:241–247CrossRefPubMedGoogle Scholar
  89. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771CrossRefPubMedGoogle Scholar
  90. Vaucheret H, Fagard M (2001) Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet 17:29–35CrossRefPubMedGoogle Scholar
  91. Venter M (2007) Synthetic promoters: genetic control through cis engineering. Trends Plant Sci 12:118–124CrossRefPubMedGoogle Scholar
  92. Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95:177–187CrossRefPubMedGoogle Scholar
  93. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR (2007) Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19:3437–3450PubMedCentralCrossRefPubMedGoogle Scholar
  94. Walschus U, Witt S, Wittmann C (2002) Development of monoclonal antibodies against Cry1Ab protein from Bacillus thuringiensis and their application in an ELISA for detection of transgenic Bt-maize. Food Agric Immunol 14:231–240CrossRefGoogle Scholar
  95. Wheelan SJ, Church DM, Ostell JM (2001) Spidey: a tool for mRNA-to-genomic alignments. Genome Res 11:1952–1957PubMedCentralPubMedGoogle Scholar
  96. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8:625–637CrossRefPubMedGoogle Scholar
  97. Xing A, Moon BP, Mills KM, Falco SC, Li Z (2010) Revealing frequent alternative polyadenylation and widespread low-level transcription read-through of novel plant transcription terminators. Plant Biotechnol J 8:772–782CrossRefPubMedGoogle Scholar
  98. Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4:1–15CrossRefGoogle Scholar
  99. Yu H, Goh CJ (2000) Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol 123:1325–1336PubMedCentralCrossRefPubMedGoogle Scholar
  100. Zhao H, Zheng J, Li QQ (2011) A novel plant in vitro assay system for pre-mRNA cleavage during 3′-end formation. Plant Physiol 157:1546–1554PubMedCentralCrossRefPubMedGoogle Scholar
  101. Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci U S A 105:18232–18237PubMedCentralCrossRefPubMedGoogle Scholar
  102. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2015

Authors and Affiliations

  • Michael Nuccio
    • 1
  • Xi Chen
    • 2
  • Jared Conville
    • 1
  • Ailing Zhou
    • 1
  • Xiaomei Liu
    • 1
  1. 1.Syngenta Biotechnology, Inc.Research Triangle ParkUSA
  2. 2.Syngenta Biotechnology (China) Co. LtdBeijingChina

Personalised recommendations