Advertisement

Molecular Breeding

, 39:63 | Cite as

Creation of elite growth and development features in PAP1-programmed red Nicotiana tabacum Xanthi via overexpression of synthetic geranyl pyrophosphate synthase genes

  • Gui Li
  • Xiaoming Ji
  • Jing Xi
  • De-Yu XieEmail author
  • Xiaohua SuEmail author
Article
  • 72 Downloads

Abstract

We report effects of overexpression of synthetic cDNAs encoding two forms of geranyl pyrophosphate synthase (GPPS) on growth and development performance of Production of Anthocyanin Pigment 1 (PAP1) gene-programmed tobacco (Nicotiana tabacum Xanthi) plants. Isogenic PAP1-programmed tobacco plants have a new trait that highly expresses anthocyanin biosynthetic pathway in all plant tissues, thus being considered a novel material for different studies. We recently used a homomeric Myzus persicae GPPS (MpGPPS) cDNA as a template to synthesize two new cDNA forms, sMpGPPS-HA and PTP-sMpGPPS-HA, which were designed to localize encoded proteins in the cytosol and plastids, respectively. One binary construct containing sMpGPPS-HA, the other binary construct containing PTP-sMpGPPS-HA, and another control construct were introduced to PAP1-programmed plants, respectively. Twenty to twenty-two T0 plants were generated for each construct. Seeds were collected from all plants to select T1 progeny with one single copy of the transgenes. Based on the Mendel law of inheritance, four T0 lines for each construct were identified to contain one single copy of transgene. A large number of T1 progeny from these T0 plants were selected for evaluation of plant development performance. The resulting data showed that the overexpression of each synthetic cDNA significantly enhanced fast growth, increased internodes and leaf numbers, increased leaf sizes, promoted earlier flowering, and approximately doubled plant biomass. This study indicates that a simultaneous enhancement of plant anthocyanin and terpenoid pathways creates novel elite PAP1-programmed plant varieties.

Keywords

Synthetic geranyl pyrophosphate synthase Plant synthetic biology Production of anthocyanin pigment 1 Nicotiana tabacum Plant biomass Metabolic engineering 

Notes

Acknowledgements

This research was supported by RJ Reynolds. We are grateful to Rika Judd, a PhD candidate, for her critical editing. We thank Phytotron and Greenhouse at North Carolina State University for their excellent technical assistance on plant growth.

Supplementary material

11032_2019_968_MOESM1_ESM.jpg (605 kb)
Fig. S1 (JPG 604 kb)
11032_2019_968_MOESM2_ESM.jpg (968 kb)
Fig. S2 (JPG 968 kb)
11032_2019_968_MOESM3_ESM.jpg (3.1 mb)
Fig. S3 (JPG 3193 kb)
11032_2019_968_MOESM4_ESM.jpg (931 kb)
Fig. S4 (JPG 931 kb)
11032_2019_968_MOESM5_ESM.jpg (1.1 mb)
Fig. S5 (JPG 1096 kb)
11032_2019_968_MOESM6_ESM.jpg (611 kb)
Fig. S6 (JPG 610 kb)

References

  1. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12(12):2383–2394.  https://doi.org/10.1105/tpc.12.12.2383 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bouvier F, Suire C, d'Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24(2):241–252.  https://doi.org/10.1046/j.1365-313x.2000.00875.x CrossRefPubMedGoogle Scholar
  3. Butelli E, Titta L, Giorgio M, Mock H-P, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26(11):1301–1308 http://www.nature.com/nbt/journal/v26/n11/suppinfo/nbt.1506_S1.html. Accessed 26 Oct 2008
  4. Dalal J, Lopez H, Vasani NB, Hu ZH, Swift JE, Yalamanchili R, Dvora M, Lin XL, Xie DY, Qu RD, Sederoff HW (2015) A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa. Biotechnol Biofuels 8:175CrossRefGoogle Scholar
  5. Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28CrossRefGoogle Scholar
  6. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198(1):16–32.  https://doi.org/10.1111/nph.12145 CrossRefPubMedGoogle Scholar
  7. Gilg AB, Bearfield JC, Tittiger C, Welch WH, Blomquist GJ (2005) Isolation and functional expression of an animal geranyl diphosphate synthase and its role in bark beetle pheromone biosynthesis. Proc Natl Acad Sci 102(28):9760–9765.  https://doi.org/10.1073/pnas.0503277102 CrossRefPubMedGoogle Scholar
  8. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53(5):814–827.  https://doi.org/10.1111/j.1365-313X.2007.03373.x CrossRefPubMedPubMedCentralGoogle Scholar
  9. He X, Li Y, Lawson D, Xie D-Y (2017) Metabolic engineering of anthocyanins in dark tobacco varieties. Physiol Plant 159:2–12CrossRefGoogle Scholar
  10. Kang NK, Jeon S, Kwon S, Koh HG, Shin SE, Lee B, Choi GG, Yang JW, Jeong BR, Chang YK (2015) Effects of overexpression of a bHLH transcription factor on biomass and lipid production in Nannochloropsis salina. Biotechnol Biofuels 8:200CrossRefGoogle Scholar
  11. Kircher M (2015) Sustainability of biofuels and renewable chemicals production from biomass. Curr Opin Chem Biol 29:26–31.  https://doi.org/10.1016/j.cbpa.2015.07.010 CrossRefPubMedGoogle Scholar
  12. Kruger NJ, Ratcliffe RG (2008) Metabolic organization in plants: a challenge for the metabolic engineer. In: Bohnert HJ, Nguyen H, Lewis NG (eds) Bioengineering and molecular biology of plant pathways, vol 1. Advances in plant biochemistry and molecular biology. Pergamon-Elsevier Science Ltd, Kidlington, pp 1–27.  https://doi.org/10.1016/s1755-0408(07)01001-6 CrossRefGoogle Scholar
  13. Li J, Gao HW, Jiang JS, Dzyubenko N, Chapurin V, Wang Z, Wang XM (2013) Overexpression of the Galega orientalis gibberellin receptor improves biomass production in transgenic tobacco. Plant Physiol Biochem 73:1–6.  https://doi.org/10.1016/j.plaphy.2013.07.015 CrossRefPubMedGoogle Scholar
  14. Li G, Xi J, Ji X, Li M-Z, Xie D-Y (2018) Non-plastidial expression of a synthetic insect geranyl pyrophosphate synthase effectively increases tobacco plant biomass. J Plant Physiol 221:144–155.  https://doi.org/10.1016/j.jplph.2017.12.014 CrossRefPubMedGoogle Scholar
  15. Liu Z, Shi MZ, Xie DY (2014) Regulation of anthocyanin biosynthesis in Arabidopsis thaliana red pap1-D cells metabolically programmed by auxins. Planta 239(4):765–781.  https://doi.org/10.1007/s00425-013-2011-0 CrossRefPubMedGoogle Scholar
  16. Martin C, Li J (2017) Medicine is not health care, food is health care: plant metabolic engineering, diet and human health. New Phytol 216(3):699–719.  https://doi.org/10.1111/nph.14730 CrossRefPubMedGoogle Scholar
  17. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  18. Peel GJ, Pang Y, Modolo LV, Dixon RA (2009) The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago. Plant J 59(1):136–149CrossRefGoogle Scholar
  19. Rai A, Smita SS, Singh AK, Shanker K, Nagegowda DA (2013) Heteromeric and homomeric geranyl diphosphate synthases from Catharanthus roseus and their role in monoterpene indole alkaloid biosynthesis. Mol Plant 6(5):1531–1549.  https://doi.org/10.1093/mp/sst058 CrossRefPubMedGoogle Scholar
  20. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10(2):63–70CrossRefGoogle Scholar
  21. Rossi L, Borghi M, Yang JF, Xie DY (2017) Overexpression of Populus x canescens isoprene synthase gene in Camelina sativa leads to alterations in its growth and metabolism. J Plant Physiol 215:122–131.  https://doi.org/10.1016/j.jplph.2017.06.005 CrossRefPubMedGoogle Scholar
  22. Schmidt A, Gershenzon J (2008) Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69(1):49–57.  https://doi.org/10.1016/j.phytochem.2007.06.022 CrossRefPubMedGoogle Scholar
  23. Shi M-Z, Xie D-Y (2010) Features of anthocyanin biosynthesis in pap1-D and wild-type Arabidopsis thaliana plants grown in different light intensity and culture media conditions. Planta 231:1385–1400CrossRefGoogle Scholar
  24. Shi MZ, Xie DY (2011) Engineering of red cells of Arabidopsis thaliana and comparative genome-wide gene expression analysis of red cells versus wild-type cells. Planta 233(4):787–805.  https://doi.org/10.1007/s00425-010-1335-2 CrossRefPubMedGoogle Scholar
  25. Shi M-Z, Xie D-Y (2014) Biosynthesis and metabolic engineering of anthocyanins in Arabidopsis thaliana. Recent Pat Biotechnol 8(1):47–60CrossRefGoogle Scholar
  26. Soler E, Feron G, Clastre M, Dargent R, Gleizes M, Ambid C (1992) Evidence for a geranyl-diphosphate synthase located within the plastids of Vitis vinifera L cultivated in vitro. Planta 187(2):171–175CrossRefGoogle Scholar
  27. Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42(2):218–235CrossRefGoogle Scholar
  28. Vandermoten S, Charloteaux B, Santini S, Sen SE, Beliveau C, Vandenbol M, Francis F, Brasseur R, Cusson M, Haubruge E (2008) Characterization of a novel aphid prenyltransferase displaying dual geranyl/farnesyl diphosphate synthase activity. FEBS Lett 582(13):1928–1934.  https://doi.org/10.1016/j.febslet.2008.04.043 CrossRefPubMedGoogle Scholar
  29. Vanhercke T, El Tahchy A, Liu Q, Zhou XR, Shrestha P, Divi UK, Ral JP, Mansour MP, Nichols PD, James CN, Horn PJ, Chapman KD, Beaudoin F, Ruiz-Lopez N, Larkin PJ, de Feyter RC, Singh SP, Petrie JR (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J 12(2):231–239.  https://doi.org/10.1111/pbi.12131 CrossRefPubMedGoogle Scholar
  30. Voloshin RA, Rodionova MV, Zharmulzhamedou SK, Veziroglu TN, Allakhverdiev SI (2016) Review: biofuel production from plant and algal biomass. Int J Hydrog Energy 41(39):17257–17273.  https://doi.org/10.1016/j.ijhydene.2016.07.084 CrossRefGoogle Scholar
  31. Welker CM, Balasubramanian VK, Petti C, Rai KM, DeBolt S, Mendu V (2015) Engineering plant biomass lignin content and composition for biofuels and bioproducts. Energies 8(8):7654–7676.  https://doi.org/10.3390/en8087654 CrossRefGoogle Scholar
  32. Wilson SA, Roberts SC (2014) Metabolic engineering approaches for production of biochemicals in food and medicinal plants. Curr Opin Biotechnol 26:174–182.  https://doi.org/10.1016/j.copbio.2014.01.006 CrossRefPubMedGoogle Scholar
  33. Xi J, Rossi L, Lin X, Xie D-Y (2016) Overexpression of a synthetic insect–plant geranyl pyrophosphate synthase gene in Camelina sativa alters plant growth and terpene biosynthesis. Planta 244:215–230.  https://doi.org/10.1007/s00425-016-2504-8 CrossRefPubMedGoogle Scholar
  34. Xie D-Y, Dixon RA (2005) Proanthocyanidin biosynthesis—still more questions than answers? Phytochemistry 66(18):2127–2144CrossRefGoogle Scholar
  35. Xie D-Y, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299(5605):396–399.  https://doi.org/10.1126/science.1078540 CrossRefPubMedGoogle Scholar
  36. Xie D-Y, Sharma SB, Wright E, Wang Z-Y, Dixon RA (2006) Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor. Plant J 45(6):895–907.  https://doi.org/10.1111/j.1365-313X.2006.02655.x CrossRefPubMedGoogle Scholar
  37. Zhou L-L, Zeng H-N, Shi M-Z, Xie D-Y (2008) Development of tobacco callus cultures over expressing Arabidopsis PAP1/MYB75 transcription factor and characterization of anthocyanin biosynthesis. Planta 229:37–51CrossRefGoogle Scholar
  38. Zhou LL, Shi MZ, Xie DY (2012) Regulation of anthocyanin biosynthesis by nitrogen in TTG1-GL3/TT8-PAP1-programmed red cells of Arabidopsis thaliana. Planta 236(3):825–837.  https://doi.org/10.1007/s00425-012-1674-2 CrossRefPubMedGoogle Scholar
  39. Zuluaga DL, Gonzali S, Loreti E, Pucciariello C, Degl'Innocenti ED, Guidi L, Alpi A, Perata P (2008) Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. Funct Plant Biol 35(7):606–618.  https://doi.org/10.1071/FP08021 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Tree Genetics and Breeding, Research Institute of ForestryChinese Academy of Forestry; Key Laboratory of Tree Breeding and Cultivation, National Forestry and Grassland AdministrationBeijingChina
  2. 2.Hunan Academy of ForestryChangshaChina
  3. 3.Department of Plant and Microbial BiologyNorth Carolina State UniversityRaleighUSA

Personalised recommendations