Biology
Transformation and genetic editing of sugar cane
López Gerena, J.; Jaimes Quiñónez, HA | NOV 2023 | ISBN 978-958-8449-30-2
Introduction
In the last two decades, research aimed at developing biotechnological tools in sugarcane cultivation has increased (saccharum spp.) to evaluate factors such as the sucrose content of the cane, the tons of cane obtained per hectare (TCH) and its resistance to biotic and abiotic stress, through tissue culture and genetic engineering. This approach is reflected in the improvement of crop productivity indicators. The global production of sugar and bioethanol, as well as the use of sugar cane as a biofactory, raise the need for sustainable production, which requires exhaustive research into the factors that affect the improvement of the crop to counteract the adversities of climate change. , which directly impact crop productivity. These genetic improvements – in any species – especially for quantitatively inherited traits, will be successful only when efficient methods of gene transfer or editing and regeneration of whole plants are available.
This chapter discusses recent advances in sugarcane transformation methods, especially bioballistics and mediated Agrobacterium in the monocotyledonous system of saccharum spp. In addition, it relates findings already applied in sugarcane, such as the new genetic editing techniques based on TALEN effector nucleases, as well as the most recent methodology – which predicts greater application in plants – of genetic editing using the CRISPR–Cas9 system ( clustered and regularly interspaced palindromic repeats). Applying these advances in sugarcane requires an efficient transformation method that includes in the medium term a DNA-free genetic editing system, so that the resulting varieties are considered conventional and unmodified cultivars, as provided in Resolution 29299 of August 2018 of the Colombian Agricultural Institute (ICA).
About the authors
López Gerena, J.
Biologist from the Universidad del Valle. In 2006 he received Ph.D. in Phytopathology with emphasis in Molecular Biology from Kansas State University, USA. He graduated in Bioinformatics in 2016 and Diploma in Senior Management in 2013. Between 1993 and 2000 he was a research assistant in the Biotechnology Unit of the International Center for Tropical Agriculture (CIAT). Since 2006 he is a Biotechnologist in the Biotechnology Area, Variety Program of the Colombian Sugarcane Research Center, Cenicaña. Thirty years of scientific and technical experience, especially in the identification of molecular markers and genes associated with productivity variables, resistance to pests and diseases. Experience at an administrative level in coordination, project management and biosafety of Genetically Modified Organisms (GMO). He has been a tutor for undergraduate and graduate students and principal investigator and co-investigator of projects co-financed by the MinCiencias and the Ministry of Agriculture and Rural Development. He currently leads the line of research in Genetic Transformation and Genome Editing applied to the molecular improvement of sugarcane.
Jaimes Quiñónez, HA
Biologist with an emphasis on genetics graduated from the Universidad del Valle in 2005. He carried out his graduate work on the subject of genetic transformation of Cassava at the International Center for Tropical Agriculture (CIAT) between 2003 and 2005, where he later He worked on research projects related to varietal resistance to pests in beans and molecular evaluation of transgenic rice plants until 2008. As of October 2008, he joined the biotechnology laboratory of the Colombian Sugarcane Research Center, Cenicaña as a research assistant in projects related to genetic transformation/editing, genomics and transcriptomics of sugarcane. He is currently involved in marker-assisted selection projects for the implementation of GWAS and Genomic Selection strategies to assist improvement processes in Cenicaña.
Altpeter, F.; & Oraby, H. (2010). Sugarcane. In: F. Kempken & C. Jung (Eds.). Genetic Modification of Plants, Biotechnology in Agriculture and Forestry, 64 (pp. 453–472). Berlin: Springer-Verlag. https://doi.org/10.1007/978-3-642-02391-0 Altpeter, F.; Springer, N.M.; Bartley, L.E.; Blechl, A.E.; Brutnell, T.P.; Citovsky, V.; Conrad, L.J.; Gelvin, S.B.; Jackson, D.P.; Kausch, AP; Lemaux, P.G. Medford, J.I. Orozco-Cárdenas, ML; Tricoli, DM; Van Eck, J.; Voytas, DF; Walbot, V.; Wang,
K.; Zhang, ZJ & Stewart, CN, Jr (2016). Advancing Crop Transformation in the Era of Genome Editing. The Plant cell, 28(7), pp. 1510-1520. https://doi.org/10.1105/tpc.16.00196
Anderson, DJ; Gnanasambandam, A.; Mills, E.; O'Shea, M.G.; Nielsen, L.K. & Brumbley, S.M. (2011). Synthesis of Short-Chain-Length/Medium-Chain Length Polyhydroxyalkanoate (PHA) Copolymers in Peroxisomes of Transgenic Sugarcane Plants. Tropical Plant Biology 4, pp. 170-184. https://doi.org/10.1007/s12042-011-9080-7
Anderson, DJ & Birch, R.G. (2012). Minimal Handling and Super-Binary Vectors Facilitate Efficient, Agrobacterium-Mediated, Transformation of Sugarcane (Saccharum spp.hybrid). Tropical Plant Biology, 5(2), pp. 183-192 https://doi.org/10.1007/s12042-012-9101-1
Arencibia, AD; Molina, P.; Gutiérrez, C.; Fuentes, A.; Greenidge, V.; Menendez, E.; Selman-Housein, G. (1992). Regeneration of transgenic sugarcane (Saccharum officinarum L.) plants from intact meristematic tissue transformed by electroporation. Applied Biotechnology, 9, pp. 156-165.
Arencibia, A.; Molina, PR; de la Riva, G. & Selman-Housein, G. (1995). Production of transgenic sugarcane (Saccharum officinarum L.) plants by intact cell electroporation. Plant cell reports, 14(5), pp. 305-309. https://doi.org/10.1007/BF00232033
Arencibia, A.; Vázquez, RI; Prieto, D.; Téllez, P.; Carmona, ER; Coego, A.; Hernandez, L.; De la Riva, G. & Selman-Housein, G. (1997). Transgenic sugarcane plants resistant to stem borer attack. Molecular Breeding, 3(4), pp. 247-255. https://doi.org/10.1023/A:1009616318854
Arencibia, AD; Carmona, ER; Téllez, P.; Chan, M.T.; Yu, S.M.; Trujillo, LE & Oramas, P. (1998). An efficient protocol for sugarcane (Saccharum spp. L.) transformation mediated by Agrobacterium tumefaciens. Transgenic Research, 7(3), pp. 213-222. https://doi.org/10.1023/A:1008845114531
Arencibia, AD; Carmona, ER; Cornide, M.T.; Castiglione, S.; O'Relly, J.; Chinea, A.; Oramas, P. & Sala, F. (1999). Somaclonal variation in insect-resistant transgenic sugarcane (Saccharum hybrid) plants produced by cell electroporation. Transgenic Research, 8, pp. 349-360. https://doi.org/10.1023/A:1008900230144
Arvinth, S.; Arun, S.; Selvakesavan, R.K. Srikanth, J.; Mukunthan, N.; Ananda Kumar, P.; Premachandran, M.N. & Subramonian, N. (2010). Genetic transformation and pyramiding of aprotinin-expressing sugarcane with cry1Ab for shoot borer (Chilo infuscatellus) resistance. Plant cell reports 29(4), pp. 383-395. https://doi.org/10.1007/s00299-010-0829-5
Aslam, U.; Tabassum, B.; Nasir, IA; Khan, A. & Husnain, T. (2018). A virus-derived short hairpin RNA confers resistance against sugarcane mosaic virus in transgenic sugarcane. Transgenic research, 27(2), pp. 203-210. https://doi.org/10.1007/s11248-018-0066-1
Augustine, S.M.; Narayan, J.A.; Syamaladevi, DP; Appunu, C.; Chakravarthi, M.; Ravichandran, V. & Subramonian, N. (2015). Erianthus arundinaceus HSP70 (EaHSP70) overexpression increases drought and salinity tolerance in sugarcane (Saccharumspp. hybrid). Plant science: an international journal of experimental plant biology, 232, pp. 23-34. https://doi.org/10.1016/j.plantsci.2014.12.012
Augustine, S. M. (2017). CRISPR-Cas9 System as a Genome Editing Tool in Sugarcane. In C. Mohan (Ed.), Sugarcane Biotechnology: Challenges and Prospects (pp. 155-172).Sao Carlos, Brazil: Springer International Publishing. https://doi.org/10.1007/978-3-319-58946-6_11
Avellaneda, MC; Victoria, J. I. (2008). Advances in the transgenic resistance of the CC 85-92 variety to leaf scald (LSD) and soca rickets (RSD). Ashen. Final report. Cali.
Barba, R. & Nickell, L.G. (1969). Nutrition and organ differentiation in tissue cultures of sugarcane, a monocotyledon. Planta, 89(3), pp. 299-302. https://doi.org/10.1007/BF00385034
Barros, GO; Ballen, M.A.; Woodard, SL; Wilken, L.R.; White, S.G.; Damaj, MB; Mirkov, TE & Nikolov, ZL (2013). Recovery of bovine lysozyme from transgenic sugarcane stalks: extraction, membrane filtration, and purification. Bioprocess and biosystems engineering, 36(10), 1407-1416. https://doi.org/10.1007/s00449-012-0878-y
Basnayake, SW; Morgan, T.C.; Wu, L. & Birch, R.G. (2012). Field performance of transgenic sugarcane expressing isomaltulose synthase. Plant biotechnology journal, 10(2), 217-225. https://doi.org/10.1111/j.1467-7652.2011.00655.x
Bonilla, ML (2007). Somatic embryogenesis and transient expression of the GUS gene as a preliminary phase in the development of a genetic transformation methodology in sugarcane (Saccharum spp.) using Agrobacterium tumefaciens. Master's Thesis. National University of Colombia, Palmira Campus. Colombia.
Bonilla, ML; Muñoz, JE; Ángel, F. (2008). Transient expression of the GUS gene in sugarcane using Agrobacterium tumefaciens. Agronomic Act, 57 (3), 161-166.
Beyene, G.; Curtis, I.S.; Damaj, MB; Buenrostro-Nava, MT & Erik, MT (2013). Genetic Engineering of Saccharum. In: HA Paterson (Ed.), Genomics of the Saccharinae, Plant Genetics and Genomics: Crops and Models. New York.
Molinari, HBC.; Marur, CJ.; Daros, E.; Campos, MKF.; Carvalho, JF.; Bespalhok, JC.; Pereira, LFP.; Vieira, LGE (2007). Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant 130(2): pp. 218-229. https://doi.org/10.1111/j.1399-3054.2007.00909.x
Cristofoletti, PT; Kemper, EL; Capella, A.N.; Carmago, SR; Cazoto, JL; Ferrari, F.; Galvan, T.L.; Gauer, L.; Monge, GA; Nishikawa, M.A.; Santos, M.; Semeao, AA; Silva, L.; Willse, A.R.; Zanca, A. & Edgerton, M.D. (2018). Development of Transgenic Sugarcane Resistant to Sugarcane Borer. Tropical Plant Biology, pp. 1-14. https://doi.org/10.1007/s12042-018-9198-y
Dermawan, H.; Karan, R.; Jung, J.H.; Zhao, Y.; Parajuli, S.; Sanahuja, G. & Altpeter, F.(2016). Development of an intragenic gene transfer and selection protocol for sugarcane resulting in resistance to acetolactate synthase-inhibiting herbicide. Plant Cell, Tissue and Organ Culture, 126(3), pp. 459-468. https://doi.org/10.1007/s11240-016-1014-5
Dong, S.; Delucca, P.; Geijskes, RJ; Ke, J.; May, K.; Mai, P.; Sainz, M.; Caffall, K.; Moser, T.; Yarnall, M.; Setliff, K.; Jain, R.; Rawls, E.; Smith-Jones, M. & Dunder, E. (2014). Advances in Agrobacterium-Mediated Sugarcane Transformation and Stable Transgene Expression. Sugar Tech. https://doi.org/10.1007/s12355-013-0294-x
Elliott, A.R.; Campbell, J.A.; Dugdale, B.; Brettell, RIS & Grof, CPL (1999). Green-fluorescent protein facilitates rapid in vivo detection of genetically transformed plant cells. Plant Cell Reports, 18, pp. 707-714. https://doi.org/10.1007/s002990050647
Enríquez-Obregón, GA; Vázquez-Padrón, R.; Prieto-Samsónov, DL; De la Riva, G. & Selman-Housein, G. (1998). Herbicide-resistant sugarcane (Saccharum officinarum L.) plants by Agrobacterium-mediated transformation. Planta, 206, pp. 20-27. https://doi.org/10.1007/s004250050369.
Falco, MC; Tulmann Neto, A. & Ulian, EC (2000). Transformation and expression of a gene for herbicide resistance in a Brazilian sugarcane. Plant cell reports, 19(12), pp.1188-1194. https://doi.org/10.1007/s002990000253
Ferreira, SJ; Kossmann, J.; Lloyd, JR & Groenewald, J.H. (2008). The reduction of starch accumulation in transgenic sugarcane cell suspension culture lines. Biotechnology journal, 3(11), pp. 1398-1406. https://doi.org/10.1002/biot.200800106
Gallo-Meagher, M. & Irvine, J.E. (1996). Herbicide Resistant Transgenic Sugarcane Plants Containing the bar Gene. Crop Science, 36(5), 1367. https://doi.org/10.2135/cropsci1996.0011183X003600050047x
Gambley, R.L.; Ford, R. & Smith, G.R. (1993). Microprojectile transformation of sugarcane meristems and regeneration of shoots expressing β-Glucuronidase. Plant cell reports, 12(6), pp. 343-346. https://doi.org/10.1007/BF00237432
Gao, S.; Yang, Y.; Wang, C.; Guo, J.; Zhou, D.; Wu, Q.; Su, Y.; Xu, L. & Que, Y. (2016). Transgenic Sugarcane with a cry1Ac Gene Exhibited Better Phenotypic Traits and Enhanced Resistance against Sugarcane Borer. PloS one, 11(4), e0153929. https://doi.org/10.1371/journal.pone.0153929
Garsmeur, O;, Droc, G.; Antonise, R.; Grimwood, J.; Potier, B.; Aitken, K.; Jenkins, J.; Martin, G.; Charron, C.; Hervouet, C.; Costet, L.; Yahiaoui, N.; Healey, A.; Sims, D.; Cherukuri, Y.; Sreedasyam, A.; Kilian, A.; Chan, A.; Van Sluys, M.A.; Swaminathan,
K.; D'Hont, A. (2018). A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nature communications, 9(1), 2638. https://doi.org/10.1038/s41467-018-05051-5
Gilbert, R.A.; Gallo-Meagher, M.; Comstock, J.C. Miller, J.D.; Jain, M. & Abouzid, A. (2005). Agronomic Evaluation of Sugarcane Lines Transformed for Resistance to Sugarcane mosaic virus Strain E, 45, pp. 2060-2067. Retrieved from https://dl.sciencesocieties.org/publications/cs/abstracts/45/5/2060
Gilbert, R.A.; Glynn, N.C.; Comstock, J.C. & Davis, M.J. (2009). Agronomic performance and genetic characterization of sugarcane transformed for resistance to sugarcane yellow leaf virus. Field Crops Research, 111(1–2), pp. 39-46. https://doi.org/10.1016/j.fcr.2008.10.009
Groenewald, J.H. & Botha, F.C. (2008). Down-regulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes. Transgenic research, 17(1), pp. 85-92. https://doi.org/10.1007/s11248-007-9079-x
Guerzoni, J.T.S.; Belintani, NG; Moreira, RMP; Hoshino, A.A.; Domingues, DS; Filho, JCB & Vieira, LGE (2014). Stress-induced Δ1-pyrroline-5-carboxylate synthetase (P5CS) gene confers tolerance to salt stress in transgenic sugarcane. Acta Physiologiae Plantarum, 36(9), pp. 2309-2319. https://doi.org/10.1007/s11738-014-1579-8
Hall, R.M.; Geijskes, RJ; Harrison, M.D.; Jepson, I.; Kinkema, M.; Miles, S.; Dale, J.L. (2013). Improved Expression of Cellulolytic Enzymes in Sugarcane. In: Proc. Int. Soc. Sugar Cane Technol, vol. 28, pp. 1-12.
Hamerli, D. & Birch, R.G. (2011). Transgenic expression of trehalulose synthase results in high concentrations of the sucrose isomer trehalulose in mature stems of field-grown sugarcane. Plant biotechnology journal, 9(1), pp. 32-37. https://doi.org/10.1111/j.1467-7652.2010.00528.x
Harrison, M.D.; Geijskes, J.; Coleman, H.D.; Shand, K.; Kinkema, M.; Palupe, A.; Hassall, R.; Sainz, M.; Lloyd, R.; Miles, S. & Dale, J.L. (2011). Accumulation of recombinant cellobiohydrolase and endoglucanase in the leaves of mature transgenic sugar cane. Plant biotechnology journal, 9(8), pp. 884-896. https://doi.org/10.1111/j.1467-7652.2011.00597.x
Heinz, DJ & Mee, G.W.P. (1969). Plant Differentiation from Callus Tissue of Saccharum Species. Crop Science, 9(3), 346 pp. https://doi.org/10.2135/cropsci1969.0011183X000900030030x
Ingelbrecht, I.L.; Irvine, J.E. & Mirkov, T.E. (1999). Posttranscriptional gene silencing in transgenic sugarcane. Dissection Of homology-dependent virus resistance in a monocot that has a complex polyploid genome. Plant physiology, 119(4), pp. 1187-1198. https://doi.org/10.1104/pp.119.4.1187
ISAAA. (2013). Indonesia Approves First GM Sugarcane- Crop Biotech Update (5/22/2013) | ISAAA.org/KC. Retrieved April 10, 2018, from http://www.isaaa.org/kc/cropbiotechupdate/article/default.asp?ID=10989
ISAAA. (2017). Brazil Approves GM Sugarcane for Commercial Use- Crop Biotech Update (6/14/2017) | ISAAA.org/KC. Retrieved April 10, 2018, from http://www.isaaa.org/kc/cropbiotechupdate/article/default.asp?ID=15510
Jackson, M.A.; Nutt, K.A.; Hassall, R. & Rae, A.L. (2010). Comparative efficiency of subcellular targeting signals for expression of a toxic protein in sugarcane. Functional Plant Biology, 37(8), pp. 785-793. https://doi.org/10.1071/FP09243
Jain, M.; Chengalrayan, K.; Abouzid, A. & Gallo, M. (2007). Prospecting the utility of a PMI/mannose selection system for the recovery of transgenic sugarcane (Saccharumspp. hybrid) plants. Plant cell reports, 26(5), pp. 581-590. https://doi.org/10.1007/s00299-006-0244-0
Jinek, M.; Chylinski, K.; Fonfara, I.; Hauer, M.; Doudna, J. A. & Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science (New York, NY), 337(6096), pp. 816-821. https://doi.org/10.1126/science.1225829
Joyce, P.A.; McQualter, R.B.; Bernard, M.J. and Smith, G.R. (1998). Engineering for resistance to SCMV in sugarcane. Hortic Act. 461, pp. 385-392. https://doi:10.17660/ActaHortic.1998.461.44
Joyce, P.; Kuwahata, M.; Turner, N. & Lakshmanan, P. (2010). Selection system and co-cultivation medium are important determinants of Agrobacterium-mediated transformation of sugarcane. Plant cell reports, 29(2), 173–183. https://doi.org/10.1007/s00299-009-0810-3
Joyce, P.; Hermann, S.; O'Connell, A.; Dinh, Q.; Shumbe, L. & Lakshmanan, P. (2014). Field performance of transgenic sugarcane produced using Agrobacterium and biolistics methods. Plant biotechnology journal, 12(4), pp. 411-424. https://doi.org/10.1111/pbi.12148
Jung, J.H.; Fouad, W.M.; Vermerris, W.; Gallo, M. & Altpeter, F. (2012). RNAi suppression of lignin biosynthesis in sugarcane reduces recalcitrance for biofuel production from lignocellulosic biomass. Plant biotechnology journal, 10(9), pp. 1067-1076. https://doi.org/10.1111/j.1467-7652.2012.00734.x
Jung, J.H.; Vermerris, W.; Gallo, M.; Fedenko, JR; Erickson, J.E. & Altpeter, F. (2013). RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane. Plant biotechnology journal, 11(6), pp. 709-716. https://doi.org/10.1111/pbi.12061
Jung, J.H.; & Altpeter, F. (2016). TALEN mediated targeted mutagenesis of the caffeic acid O-methyltransferase in highly polyploid sugarcane improves cell wall composition for production of bioethanol. Plant molecular biology, 92 (1-2), pp. 131-142. https://doi.org/10.1007/s11103-016-0499-y
Jung, J.H.; Kannan, B.; Dermawan, H.; Moxley, G.W. & Altpeter, F. (2016). Precision breeding for RNAi suppression of a major 4-coumarate:coenzyme A ligase gene improves cell wall saccharification from field grown sugarcane. Plant molecular biology, 92 (4-5), pp. 505-517. https://doi.org/10.1007/s11103-016-0527-y
Kannan, B.; Jung, J.H.; Moxley, G.W.; Lee, S.M. & Altpeter, F. (2018). TALEN-mediated targeted mutagenesis of more than 100 COMT copies/alleles in highly polyploid sugarcane improves saccharification efficiency without compromising biomass yield. Plant biotechnology journal, 16 (4), pp. 856-866. https://doi.org/10.1111/pbi.12833
Kim, J.Y.; Nong, G.; Rice, J.D.; Gallo, M.; Preston, J.F. & Altpeter, F. (2017). In planta production and characterization of a hyperthermostable GH10 xylanase in transgenic sugarcane. Plant molecular biology, 93 (4-5), pp. 465-478. https://doi.org/10.1007/s11103-016-0573-5
Kinkema, M.; Geijskes, J.; Delucca, P.; Palupe, A.; Shand, K.; Coleman, H.D.; Brinin, A.; Williams, B.; Sainz, M. & Dale, J.L. (2014). Improved molecular tools for sugar cane biotechnology. Plant molecular biology, 84 (4-5), pp. 497-508. https://doi.org/10.1007/s11103-013-0147-8
Lakshamanan, P.; Geijskes, RJ; Karen, A.; Grof, CLP; Bonnett, G.D. & Smith, G.R. (2005). Invited review: sugarcane biotechnology: the challenges and opportunities. In Vitro Cell. Dev. Biol. Plant, 41, pp. 345-363.
Li, J.F.; Norville, J.E.; Aach, J.; McCormack, M.; Zhang, D.; Bush, J.; Church, G. M. & Sheen, J. (2013). Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature biotechnology, 31 (8), pp. 688-691. https://doi.org/10.1038/nbt.2654
Li, J.; Phan, T.T.; Li, Y.R.; Xing, Y.X. & Yang, L.T. (2018). Solation, transformation and overexpression of sugarcane SoP5CS gene for drought tolerance improvement. Sugar Tech, 20 (4), pp. 464–473. https://doi.org/10.1007/s12355-017-0568-9
Ma, H.; Albert, H.H.; Paull, R. & Moore, P.H. (2000). Metabolic engineering of invertase activities in different subcellular compartments affects sucrose accumulation in sugarcane cells. Functional Plant Biology, 27 (11), pp. 1021-1030. Retrieved from https://doi.org/10.1071/PP00029
Manickavasagam, M.; Ganapathi, A.; Anbazhagan, V.R.; Sudhakar, B.; Selvaraj, N.; Vasudevan, A.; & Kasthurirengan, S. (2004). Agrobacterium-mediated genetic transformation and development of herbicide-resistant sugarcane (Saccharum species hybrids) using axillary buds. Plant cell reports, 23 (3), pp. 134-143. https://doi.org/10.1007/s00299-004-0794-y
Mayavan, S.; Subramanyam, K.; Arun, M.; Rajesh, M.; Kapil Dev, G.; Sivanandhan, G.; Jaganath, B.; Manickavasagam, M.; Selvaraj, N. & Ganapathi, A. (2013). Agrobacterium tumefaciens-mediated in planta seed transformation strategy in sugarcane. Plant cell reports, 32 (10), pp. 1557-1574. https://doi.org/10.1007/s00299-013-1467-5
Mayavan, S.; Subramanyam, K.; Jaganath, B.; Sathish, D.; Manickavasagam, M. & Ganapathi, A. (2015). Agrobacterium-mediated in planta genetic transformation of sugarcane sets. Plant cell reports, 34 (10), pp. 1835-1848. https://doi.org/10.1007/s00299-015-1831-8
McQualter, R.B.; Dale, J.L. Harding, R.M.; McMahon, J. A. & Smith, G. R. (2004). Production and evaluation of transgenic sugarcane containing a Fiji disease virus (FDV) genome segment S9-derived synthetic resistance gene. Australian Journal of Agricultural Research, 55 (2), pp. 139-145. https://doi.org/10.1071/AR03131
McQualter, R.B.; Chong, B.F.; Meyer, K.; Van Dyk, D.E.; O'Shea, M.G.; Walton, NJ; Viitanen, P.V. & Brumbley, S.M. (2005). Initial evaluation of sugarcane as a production platform for p-hydroxybenzoic acid. Plant biotechnology journal, 3 (1), pp. 29-41. https://doi.org/10.1111/j.1467-7652.2004.00095.x
McQualter, R.B. & Dookun-Saumtally, A. (2007). Expression profiling of abiotic-stress-inducible genes in sugarcane. In: Proc Int Soc Sugar Cane Technol, vol. 26, pp. 878-888).
Mohan C. (2016). Genome Editing in Sugarcane: Challenges Ahead. Frontiers in plant science, 7, 1542 pp. https://doi.org/10.3389/fpls.2016.01542
Moore, P.H.; Paterson, A.H. & Tew, T. (2013). Sugarcane: The Crop, the Plant, and Domestication. In: Sugarcane: Physiology, Biochemistry, and Functional Biology (pp. 1-17). Chichester, UK: John Wiley & Sons Ltd. https://doi.org/10.1002/9781118771280.ch1
Mosquera, PA (2011). Transient expression of the Gus Plus(R) gene in sugarcane (Saccharum sp.) embryogenic callus by microparticle bombardment using the Hepta-Cenicaña device. Undergraduate thesis. Universidad del Valle, Cali. Colombia.
Mudge, S.R.; Basnayake, SW; Moyle, R.L.; Osabe, K.; Graham, M.W.; Morgan, T.E. & Birch, R.G. (2013). Mature-stem expression of a silencing-resistant sucrose isomerase gene drives isomaltulose accumulation to high levels in sugarcane. Plant biotechnology journal, 11 (4), pp. 502-509. https://doi.org/10.1111/pbi.12038
Nayyar, S.; Sharma, B.K.; Kaur, A.; Kalia, A.; Sanghera, G.S; Thind, K.S.; Yadav, I.S. & Sandhu, J.S. (2017). Red rot resistant transgenic sugarcane developed through expression of β-1,3-glucanase gene. PloS one, 12 (6), e0179723. https://doi. org/10.1371/journal.pone.0179723
Petrasovits, LA; McQualter, R.B.; Gebbie, L.K.; Blackman, D.M.; Nielsen, L.K. & Brumbley, S.M. (2013). Chemical inhibition of acetyl coenzyme A carboxylase as a strategy to increase polyhydroxybutyrate yields in transgenic sugarcane. Plant biotechnology journal, 11 (9), pp. 1146-1151. https://doi.org/10.1111/pbi.12109 Podevin, N.; Davies, H.V.; Hartung, F.; Nogué, F. & Casacuberta, JM (2013). Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends in biotechnology, 31 (6), 375-383. https://doi.org/10.1016/j.tibtech.2013.03.004
Ramasamy, M.; Mora, V.; Damaj, MB; Padilla, CS; Ramos, N.; Rossi, D.; Solís-Gracia, N.; Vargas-Bautista, C.; Irigoyen, S.; DaSilva, JA; Mirkov, T.E. & Mandadi, K.K. (2018). A biolistic-based genetic transformation system applicable to a broad-range of sugarcane and energycane varieties. GM crops & food, 9 (4), pp. 211-227. https://doi.org/10.1080/21645698.2018.1553836
Rangel, MP; Tabares Z., E.; Lentini, Z.; Tohme M., J.; Mirkov, E.; Victoria Kafure, J.I. & Angel, F. (2002). Transformation of sugar cane plants susceptible to yellow leaf syndrome = Transformation of sugar cane plants susceptible to yellow leaf virus. Colombian Journal of Biotechnology, 4 (1), 54-60.
Rangel, MP; Gómez, L.; Victoria, J.I. & Angel, F. (2005). Transgenic plants of CC 84-75 resistant to the virus associated with the sugarcane yellow leaf disease. In: Proc. ISSCT, vol. 25, pp. 564-570). Guatemala city.
Rathus, C. & Birch, R. G. (1992). Stable transformation of callus from electroporated sugarcane protoplasts. Plant Science, 82 (1), pp. 81-89. https://doi.org/10.1016/0168-9452(92)90010-J
Reis, RR; da Cunha, BA; Martins, P.K.; Martins, M.T.; Alekcevetch, JC; Chalfun, A., Jr; Andrade, AC; Ribeiro, AP; Qin, F.; Mizoi, J.; Yamaguchi-Shinozaki, K.; Nakashima, K.; Carvalho, J.; de Sousa, CA; Nepomuceno, AL; Kobayashi, A.K. & Molinari, H.B. (2014). Induced over-expression of AtDREB2A CA improves drought tolerance in sugarcane. Plant science: an international journal of experimental plant biology, 221-222, pp. 59-68. https://doi.org/10.1016/j.plantsci.2014.02.003
Ribeiro, CW; Soares-Costa, A.; Falco, MC; Chabregas, SM; Ulian, EC; Cotrin, SS; Carmona, AK; Santana, LA; Oliva, ML & Henrique-Silva, F. (2008). Production of a His-tagged canecystatin in transgenic sugarcane and subsequent purification. Biotechnology progress, 24 (5), pp. 1060-1066. https://doi.org/10.1002/btpr.45
Roberts, R.J. (2018). The Nobel Laureates Campaign Supporting GMO. Journal of Innovation & Knowledge, Volume 3, Issue 2, pp. 61-65. https://doi.org/10.1016/j.jik.2017.12.006
Rossouw, D.; Bosch, S.; Kossmann, J.; Botha, F.C. & Groenewald, J.H. (2007). Downregulation of neutral invertase activity in sugarcane cell suspension cultures leads to a reduction in respiration and growth and an increase in sucrose accumulation. Functional plant Biology: FPB, 34 (6), pp. 490-498. https://doi.org/10.1071/FP06214
Rossouw, D.; Kossmann, J.; Botha, F.C. & Groenewald, J.H. (2010). Reduced neutral invertase activity in the culm tissues of transgenic sugarcane plants results in a decrease in respiration and sucrose cycling and an increase in the sucrose to hexose ratio. Functional Plant Biology, 37 (1), 22-31. https://doi.org/10.1071/FP08210
Sanford, J.C. (1990). Biolistic plant transformation. Physiologia Plantarum, 79 (1), 206-209. https://doi.org/10.1111/j.1399-3054.1990.tb05888.x
Schneider, V.K. Soares-Costa, A.; Chakravarthi, M.; Ribeiro, C.; Chabregas, SM; Falco, MC & Henrique-Silva, F. (2017). Transgenic sugarcane overexpressing CaneCPI-1 negatively affects the growth and development of the sugarcane weevil Sphenophorus levis. Plant cell reports, 36 (1), pp. 193-201. https://doi.org/10.1007/s00299-016-2071-2
Shan, Q.; Wang, Y.; Li, J.; Zhang, Y.; Chen, K.; Liang, Z.; Zhang, K.; Liu, J.; Xi, J.J. Qiu, J.L. & Gao, C. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nature biotechnology, 31 (8), pp. 686-688. https://doi.org/10.1038/nbt.2650
Shu-Zhen, Z.; Ben-Peng, Y.; Cui-Lian, F.; Ru-Kai, C.; Jing-Ping, L.; Wen-Wei, C. & FeiHu, L. (2006). Expression of the Grifola frondosa Trehalose Synthase Gene and Improvement of Drought-Tolerance in Sugarcane (Saccharum officinarum L.). Journal of Integrative Plant Biology, 48 (4), pp. 453-459. https://doi.org/10.1111/j.1744-7909.2006.00246.x
Snyman SJ (2004). Sugarcane Transformation. In: Curtis IS (eds). Transgenic Crops of the World. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-2333-0_8
Snyman, S.J.; Meyer, GM; Richards, J.M.; Haricharan, N.; Ramgareeb, S. & Huckett, B. I. (2006). Refining the application of direct embryogenesis in sugarcane: Effect of the developmental phase of leaf disc explants and the timing of DNA transfer on transformation efficiency. Plant cell reports, 25 (10), 1016-1023. https://doi.org/10.1007/s00299-006-0148-z
Snyman, S.J.; Hajari, E.; Watt, M.P.; Lu, Y. & Kridl, J.C. (2015). Improved nitrogen use efficiency in transgenic sugarcane: phenotypic assessment in a pot trial under low nitrogen conditions. Plant cell reports, 34 (5), pp. 667-669. https://doi.org/10.1007/s00299-015-1768-y
Songstad, D.D.; Petolino, JF; Voytas, D.F. & Reichert, N.A. (2017). Genome Editing of Plants. Critical Reviews in Plant Sciences, 36 (1), pp. 1-23. https://doi.org/10.1080/07352689.2017.1281663
Taparia, Y.; Fouad, W.M.; Gallo, M. & Altpeter, F. (2012). Rapid production of transgenic sugarcane with the introduction of simple loci following biolistic transfer of a minimal expression cassette and direct embryogenesis. In Vitro Cellular and Developmental Biology – Plant, 48 (1), pp. 15-22. https://doi.org/10.1007/s11627-011-9389-9
Taparia, Y.; Gallo, M. & Altpeter, F. (2012). Comparison of direct and indirect embryogenesis protocols, biolistic gene transfer and selection parameters for efficient genetic transformation of sugarcane. Plant Cell, Tissue and Organ Culture, 111, pp. 131-141. https://doi.org/10.1007/s11240-012-0177-y
Trujillo, JH. (2020). Assembly of a sugarcane genome and molecular fingerprint using high-throughput sequencing. Doctoral Thesis. Universidad del Valle and Colombian Sugar Cane Research Center, Cenicaña. Cali, Colombia.
van Beek, C.R.; Fernhout, J.J.; Kossmann, J.; Lloyd, JR & van der Vyver, C. (2018). Use of a Mutated Protoporphyrinogen Oxidase Gene as an Effective In Vitro Selectable Marker System that Also Conveys in planta Herbicide Resistance in Sugarcane. Tropical Plant Biology, 11 (3–4), 154-162. https://doi.org/10.1007/s12042-018-9208-0
Vickers, J.E.; Grof, CPL; Bonnett, G.D.; Jackson, P.A. & Morgan, T.E. (2005). Effects of tissue culture, biolistic transformation, and introduction of PPO and SPS gene constructs on performance of sugarcane clones in the field. Australian Journal of Agricultural Research, 56 (1), pp. 57-68. https://doi.org/10.1071/AR04159
Vickers, J.E.; Grof, CPL; Bonnett, G.D.; Jackson, PA; Knight, D.P.; Roberts, S.E. & Robinson, S.P. (2005). Overexpression of Polyphenol Oxidase in Transgenic Sugarcane Results in Darker Juice and Raw Sugar. Crop Science, 45 (1), pp. 354-362. https://doi.org/10.2135/cropsci2005.0354.
van der Vyver, C. (2010). Genetic transformation of the euploid Saccharum officinarum via direct and indirect embryogenesis. Sugar Tech, 12 (1), pp. 21-25. https://doi.org/10.1007/s12355-010-0005-9
van der Vyver, C.; Conradie, T.; Kossmann, J. & Lloyd, J. (2013). In vitro selection of transgenic sugarcane callus utilizing a plant gene encoding a mutant form of acetolactate synthase. In vitro cellular & developmental biology. Plant: journal of the Tissue Culture Association, 49 (2), pp. 198-206. https://doi.org/10.1007/s11627-013-9493-0
Wang, M.L.; Goldstein, C.; Su, W.; Moore, P.H. & Albert, H.H. (2005). Production of biologically active GM-CSF in sugar cane: a secure biofactory. Transgenic research, 14 (2),pp. 167-178. https://doi.org/10.1007/s11248-004-5415-6
Wang, Z.Z. Zhang, S.Z. Yang, B.P. & Li, Y.R. (2005). Trehalose synthase gene transfer mediated by Agrobacterium tumefaciens enhances resistance to osmotic stress in sugarcane. Sugar Tech, 7 (1), pp. 49-54. https://doi.org/10.1007/BF02942417
Wang, A.Q. Dong, W.Q. Wei, Y.W.; Huang, C.M.; He, LF; Yang, L.T. & Li, Y.R. (2009). Transformation of sugarcane with ACC oxidase antisense gene. Sugar Tech, 11 (1), pp. 39-43. https://doi.org/10.1007/s12355-009-0007-7
Wang, Y.; Cheng, X.; Shan, Q.; Zhang, Y.; Liu, J.; Gao, C. & Qiu, J.L. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature biotechnology, 32 (9), pp. 947-951. https://doi.org/10.1038/nbt.2969
Wang, W.Z. Yang, B.P.; Feng, C.L.; Wang, J.G.; Xiong, G.R.; Zhao, T.T. & Zhang, S.Z. (2017). Efficient Sugarcane Transformation via bar Gene Selection. Tropical Plant Biology, pp. 1-9. https://doi.org/10.1007/s12042-017-9186-7
Weng, L.X.; Deng, H.; Xu, J.L.; Li, Q.; Wang, L.H.; Jiang, Z.; Zhang, H.B.; Li, Q. & Zhang, L.H. (2006). Regeneration of sugarcane elite breeding lines and engineering of stem borer resistance. Pest management science, 62 (2), pp. 178-187. https://doi.org/10.1002/ps.1144
Weng, L.X.; Deng, H.H.; Xu, J.L.; Li, Q.; Zhang, Y.Q. Jiang, Z.D.; Li, Q.W.; Chen, J.W. & Zhang, L.H. (2011). Transgenic sugarcane plants expressing high levels of modified cry1Ac provide effective control against stem borers in field trials. Transgenic research, 20 (4), pp. 759-772. https://doi.org/10.1007/s11248-010-9456-8
Wu, H.; Awan, F.S.; Vilarinho, A.; Zeng, Q.; Kannan, B.; Phipps, T.; McCuiston, J.; Wanf, W.; Caffall, K. & Altpeter, F. (2011). Transgene integration complexity and expression stability following biolistic or Agrobacterium-mediated transformation of sugarcane. In Vitro Cellular & Developmental Biology – Plant (November). https://doi.org/10.1007/s11627-015-9710-0
Wu, L. & Birch, R.G. (2007). Doubled sugar content in sugarcane plants modified to produce a sucrose isomer. Plant biotechnology journal, 5 (1), pp. 109-117. https://doi.org/10.1111/j.1467-7652.2006.00224.x
Wu, Y.; Zhou, H.; What, YX; Chen, R.K. & Zhang, M.Q. (2008). Cloning and identification of promoter Prd29A and its application in sugarcane drought resistance. Sugar Tech, 10 (1), pp. 36-41. https://doi.org/10.1007/s12355-008-0006-0
Yao, W.; Ruan, M.; Qin, L.; Yang, C.; Chen, R.; Chen, B. & Zhang, M. (2017). Field Performance of Transgenic Sugarcane Lines Resistant to Sugarcane Mosaic Virus. Frontiers in plant science, 8, pp. 104. https://doi.org/10.3389/fpls.2017.00104
Zale, J.; Jung, J.H.; Kim, J.Y.; Pathak, B. Karan, R.; Liu, H.; Chen, X.; Wu, H.; Candreva, J.; Zhai, Z.; Shanklin, J. & Altpeter, F. (2016). Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant biotechnology journal, 14 (2), pp. 661-669. https://doi.org/10.1111/pbi.12411
Zhang, J.; Zhang, X.; Tang, H.; Zhang, Q.; Hua, X.; Ma, X.; Zhu, F.; Jones, T.; Zhu, X.; Bowers, J.; Wai, C.M.; Zheng, C.; Shi, Y.; Chen, S.; Xu, X.; Yue, J.; Nelson, D.R.; Huang, L.; Li, Z.; Xu, H.; Ming, R. (2018). Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nature genetics, 50 (11), pp. 1565-1573. https://doi.org/10.1038/s41588-018-0237-2
Zhang, L.; Xu, J. & Birch, R.G. (1999). Engineered detoxification confers resistance against a pathogenic bacterium. Nature biotechnology, 17 (10), pp. 1021-1024. https://doi.org/10.1038/13721
Zhang, M.; Zhuo, X.; Wang, J.; Wu, Y.; Yao, W. & Chen, R. (2015). Effective selection and regeneration of transgenic sugarcane plants using positive selection system. In Vitro Cellular & Developmental Biology – Plant, 51, pp. 52-61. https://doi.org/10.1007/ s11627-014-9644-y
Zhang, M.; Zhuo, X.; Wang, J.; Yang, C.; Powell, C. A. & Chen, R. (2015). Phosphomannose isomerase affects the key enzymes of glycolysis and sucrose metabolism in transgenic sugarcane overexpressing the manA gene. Molecular breeding: new strategies in plant improvement, 35(3), p. 100. https://doi.org/10.1007/s11032-015-0295-4
Zhangsun, D.; Luo, S.; Chen, R. & Tang, K. (2007). Improved Agrobacterium-mediated genetic transformation of GNA transgenic sugarcane. Biology, 62, 386–393. https://doi.org/10.2478/s11756-007-0096-2
Zhao, Y.; Kim, J.Y.; Karan, R.; Jung, J.H.; Pathak, B.; Williamson, B.; Kannan, B.; Wang, D.; Fan, C.; Yu, W.; Dong, S.; Srivastava, V. & Altpeter, F. (2019). Generation of a selectable marker free, highly expressed single copy locus as landing pad for transgene stacking in sugarcane. Plant molecular biology, 100 (3), pp. 247-263. https://doi.org/10.1007/s11103-019-00856-4
Zhu, Y.J.; McCafferty, H.; Osterman, G.; Lim, S.; Agbayani, R.; Lehrer, A.; Schenck, S. & Komor, E. (2011). Genetic transformation with untranslatable coat protein gene of sugarcane yellow leaf virus reduces virus titers in sugarcane. Transgenic research, 20 (3), pp. 503-512. https://doi.org/10.1007/s11248-010-9432-3
- Sugar cane. 2. Genetic transformation. 3. Gene editing. 4. Bioballistics. 5. Agrobacterium tumefaciens. 6. CRISPR–Cas9.
López Gerena, J. & Jaimes Quiñónez, HA (2023). Transformation and genetic editing of sugar cane. In: Colombian Sugarcane Research Center (Ed). Sugar cane agroindustry in Colombia. Cinderella