[en] This review archives the achievements made in the last two decades and presents a brief outline of some significant factors influencing the Agrobacterium-mediated transformation of Sorghum bicolor. Recently, progress in successful transformation has been made for this particular monocot crop through direct DNA delivery method and indirect method via Agrobacterium. However, lower transformation rate still proved to be a bottleneck in genetic modification of sorghum. An efficient Agrobacterium transformation system could be attained by optimizing the preliminary assays, comprising of explant source, growth media, antibiotics, Agrobacterium strains and agro-infection response of callus. The selection of competent strains for genetic transformation is also one of the key factors of consideration. Successful transformation is highly dependent on genome configuration of selected cultivar, where non-tannin genotype proved the best suited. Immature embryos from the field source have higher inherent adaptation chances than that of the greenhouse source. A higher concentration of Agrobacterium may damage the explant source. Utilization of anti-necrotic treatments and optimized tissue culture timeframe are the adequate strategies to lower down the effect of phenolic compounds. Appropriate selection of culture media vessels at different stages of tissue culture may also assist in a constructive manner. In conclusion, some aspects such as culture environment with medium composition, explant sources, and genotypes play an indispensable role in successful Agrobacterium-mediated sorghum transformation system.
Disciplines :
Agriculture & agronomy
Author, co-author :
Ahmed, Rana Imtiaz; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China. imtiazheaven@yahoo.com ; Graduate School of Chinese Academy of Agricultural Science, Beijing 100081, China. imtiazheaven@yahoo.com
Ding, Anming; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China. dinganming@caas.cn
Xie, Minmin ; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China. xieminmin@caas.cn
Kong, Yingzhen; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China. kongyingzhen@caas.cn
Language :
English
Title :
Progress in Optimization of Agrobacterium-Mediated Transformation in Sorghum (Sorghum bicolor).
NSCF - National Natural Science Foundation of China
Funding text :
This work was supported by the National Natural Science Foundation of China (3147029, 31670302, and 31600237), the National Key Technology R&D Program (2015BAD15B03) and the Elite Youth Program of Chinese Academy of Agricultural Sciences (to Y.K.).
Belton, P.S.; Taylor, J.R.N. Sorghum and millets: Protein sources for Africa. Trends Food Sci. Technol. 2004, doi:10.1016/j.tifs.2003.09.002.
Dahlberg, J.; Berenji, J.; Sikora, V.; Latkovic, D. Assessing sorghum [Sorghum bicolor (L.) Moench] germplasm for new traits: Food, fuels and unique uses. Maydica 2011, 56, 85–92.
Chibani, K.; Wingsle, G.; Jacquot, J.-P.; Gelhaye, E.; Rouhier, N. Comparative genomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol. Plant 2009, 2, 308–322, doi:10.1093/mp/ssn076.
Wang, Z.; Gerstein, M.; Snyder, M. RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10, 57–63, doi:10.1038/nrg2484.
Paterson, A.H.; Bowers, J.E.; Bruggmann, R.; Dubchak, I.; Grimwood, J.; Gundlach, H.; Haberer, G.; Hellsten, U.; Mitros, T.; Poliakov, A.; et al. The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457, 551–556.
Cook, D.; Rimando, A.M.; Clemente, T.E.; Schroder, J.; Dayan, F.E.; Nanayakkara, D.; Pan, Z.; Noonan, B.P.; Fishbein, M.; Abe, I.; et al. Alkylresorcinol. synthases expressed in Sorghum bicolor root hairs play an essential role in the biosynthesis of the allelopathic benzoquinone soroleone. Plant Cell 2010, 22, 867–887, doi:10.1105/tpc.109.072397.
Zhu, H.; Muthukrishnan, S.; Krishnaveni, S.; Wilde, G.; Jeoung, J.M.; Liang, G.H. Biolistic transformation of sorghum using a rice chitinase gene. J. Genet. Breed. 1998, 52, 243–252.
Abel, P.P.; Nelson, R.S.; De, B.; Hoffmann, N.; Rogers, S.G.; Fraley, R.T.; Beachy, R.N. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 1986, 232, 738–743, doi:10.1126/science.3457472.
Elkonin, L.A.; Lopushanskaya, R.F.; Pakhomova, N.V. Initiation and maintenance of friable, embryogenic callus of sorghum (Sorghum bicolor (L.) Moench) by amino acids. Maydica 1995, 40, 153–157.
Elkonin, L.A.; Pakhomova, N.V. Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum. Plant Cell Tissue Organ Cult. 2000, 61, 115, doi:10.1023/A:1006472418218.
Jeoung, J.M.; Krishnaveni, S.; Muthukrishnan, S.; Trick, H.N.; Liang, G.H. Optimization of sorghum transformation parameters using genes for green fluorescent protein and b-glucuronidase as visual markers. Hereditas 2002, 137, 20–28, doi:10.1034/j.1601-5223.2002.1370104.x.
Hill-Ambroz, K.L.; Weeks, J.T. Comparison of constitutive promoters for sorghum transformation. Cereal Res. Commun. 2001, 29, 17–24.
Kaeppler, H.F.; Pederson, J.F. Evaluation of 41 elite and exotic inbred sorghum genotypes for high quality callus production. Plant Cell Tissue Organ Cult. 1997, 48, 71–75, doi:10.1023/A:1005765009568.
Karami, O.; Esna-Ashari, M.; Kurdistani, G.K.; Aghavaisi, B. Agrobacterium-mediated genetic transformation of plants: The role of host. Biol. Plant 2009, doi:10.1007/s10535-009-0041-z.
Nirwan, R.S.; Kothari, S.L. High copper levels improve callus induction and plant regeneration in Sorghum bicolor (L.) Moench. In Vitro Cell. Dev. Biol. Plant 2003, 39, 161–164, doi:10.1079/IVP2002385.
Howe, A.; Sato, S.; Dweikat, I.; Fromm, M.; Clemente, T. Rapid and reproducible Agrobacterium-mediated transformation of sorghum. Plant Cell Rep. 2006, 25, 784–791, doi:10.1007/s00299-005-0081-6.
Jambagi, S.; Bhat, R.; Bhat, S.; Kuruvinashetti, M. Agrobacterium-mediated transformation studies in sorghum using an improved gfp reporter gene. SAT eJournal 2010, 8, 1–5.
Lu, L.; Wu, X.; Yin, X.; Morrand, J.; Chen, X.; Folk, W.R.; Zhang, Z.J. Development of marker-free transgenic sorghum [Sorghum bicolor (L.) Moench] using standard binary vectors with bar as a selectable marker. Plant Cell Tissue Organ Cult. 2009, 99, 97–108, doi:10.1007/s11240-009-9580-4.
Nguyen, T.-V.; Thu, T.T.; Claeys, M.; Angenon, G. Agrobacterium-mediated transformation of sorghum [Sorghum bicolor (L.) Moench] using an improved in vitro regeneration system. Plant Cell Tissue Organ Cult. 2007, 91, 155–164, doi:10.1007/s11240-007-9228-1.
Jogeswar, G.; Ranadheer, D.; Anjaniah, V.; Kishor, P.B.K. High frequency somatic embryogenesis and regeneration in different genotypes of Sorghum bicolor (L.) Moench from immature explants. In Vitro Cell. Dev. Biol. Plant 2007, 43, 159–166, doi: 10.1007/s11627-007-9033-x.
Kaeppler, H.F.; Pedersen, J.F. Media effects on phenotype of callus cultures initiated from photoperiod-insensitive, elite inbred sorghum lines. Maydica 1996, 41, 83–89.
Pola, S.; Mani, N.S.; Ramana, T. Long-Term Maintenance of Callus Cultures from Immature Embryo of Sorghum bicolor. World J. Agric. Sci. 2009, 5, 415–421.
Pola, S.; Mani, N.S. Somatic embryogenesis and plantlet regeneration in Sorghum bicolor (L.) Moench, from leaf explants. J. Cell Mol. Biol. 2006, 5, 99–107.
Sato, S.; Clemente, T.; Dweikat, I. Identification of an elite sorghum genotype with high in vitro performance capacity. In Vitro Cell. Dev. Biol. 2004, 40, 57, doi:10.1079/IVP2003475.
Pola, S.; Saradamani, N.; Ramana, T. Enhanced shoot regeneration in tissue culture studies of Sorghum bicolor. J. Agric. Technol. 2007, 1, 275–286.
Dai, S.; Zheng, P.; Marmey, P.; Zhang, S.; Tian, W.; Chen, S.; Beachy, R.N.; Fauquet, C. Comparative analysis of transgenic rice plants obtained by Agrobacterium-mediated transformation and particle bombardment. Mol. Breed. 2001, 7, 25–33.
Zhao, Z.Y.; Glassman, K.; Sewalt, V.; Wang, N.; Miller, M.; Chang, S.; Thompson, T.; Catron, S.; Wu, E.; Bidney, D.; et al. Nutritionally improved transgenic sorghum. In Plant Biotechnology 2002 and Beyond, 1st ed.; Vasil, I.K., Ed.; Springer: Dordrecht, The Netherlands, 2003; pp. 413–416, doi:10.1007/978-94-017-2679-5_85.
Girijashankar, V.; Sharma, H.C.; Sharma, K.K.; Swathisree, V.; Prasad, L.S.; Bhat, B.V.; Royer, M.; Secundo, B.S.; Narasu, M.L.; Altosaar, I.; et al. Development of transgenic sorghum for insect resistance against the spotted stem borer (Chilo partellus). Plant Cell Rep. 2005, 24, 513–522, doi:10.1007/s00299-005-0947-7.
Dykes, L.; Rooney, L.W. Sorghum and millet phenols and antioxidants. J. Cereal Sci. 2006, 44, 236–251, doi:10.1016/j.jcs.2006.06.007.
Hahn, D.; Faubion, J.; Rooney, L. Sorghum phenolic acids, their high-performance liquid-chromatography separation and their relation to fungal resistance. Cereal Chem. 1983, 60, 255–259.
Kumar, V.; Campbell, L.M.; Rathore, K.S. Rapid recovery-and characterization of transformants following Agrobacterium-mediated T-DNA transfer to sorghum. Plant Cell Tissue Organ Cult. 2010, 104, 137–146, doi:10.1007/s11240-010-9809-2.
Do, P.T.; Lee, H.; Mookkan, M.; Folk, W.R.; Zhang, Z.J. Rapid and efficient Agrobacterium-mediated transformation of sorghum (Sorghum bicolor) employing standard binary vectors and bar gene as a selectable marker. Plant Cell Rep. 2016, 35, 2065–2076, doi:10.1007/s00299-016-2019-6.
Wu, E.; Lenderts, B.; Glassman, K.; Berezowska-Kaniewska, M.; Christensen, H.; Asmus, T.; Zhen, S.; Chu, U.; Cho, M.-J.; Zhao, Z.-Y. Optimized Agrobacterium-mediated sorghum transformation protocol and molecular data of transgenic sorghum plants. In Vitro Cell. Dev. Biol. Plant 2014, 50, 9–18, doi:10.1007/s11627-013-9583-z.
Pandey, A.K.; Bhat, B.V.; Balakrishna, B.; Seetharama, N. Genetic Transformation of Sorghum (Sorghum bicolor (L.) Moench.) Int. J. Biotechnol. Biochem. 2010, 6, 45–53.
Hiei, Y.; Komari, T.; Kubo, T. Transformation of rice mediated by Agrobacterium tumefaciens. Plant Mol. Biol. 1997, 35, 205–218, doi:10.1023/A:1005847615493.
Cheng, M.; Lowe, B.A.; Spencer, T.M.; Ye, X.; Armstrong, C.L. Factors influencing Agrobacterium-mediated transformation of monocotyledonous species. In Vitro Cell. Dev. Biol. 2004, 40, 31–45, doi:10.1079/IVP2003501.
Cheng, M.; Fry, J.E.; Pang, S.; Zhou, H.; Hironaka, C.M.; Duncan, D.R.; Conner, T.W.; Wan, Y. Genetic transformation of wheat mediated by Agrobacterium tumefaciens. Plant Physiol. 1997, 115, 971–980, doi:10.1104/pp.115.3.971.
Ishida, Y.; Saito, H.; Ohta, S.; Hiei, Y.; Komari, T.; Kumashiro, T. High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat. Biotechnol. 1996, 14, 745, doi:10.1038/nbt0696-745.
Zhao, Z.Y.; Gu, W.; Cai, T.; Tagliani, L.; Hondred, D.; Bond, D.; Schroeder, S.; Rudert, M.; Pierce, D. High throughput genetic transformation mediated by Agrobacterium tumefaciens in maize. Mol. Breed. 2001, 8, 323– 333, doi:10.1023/A:1015243600325.
Tingay, S.; McElroy, D.; Kalla, R.; Fieg, S.; Wang, M.; Thornton, S.; Brettell, R. Agrobacterium tumefaciens-mediated barley transformation. Plant J. 1997, 11, 1369–1376, doi:10.1046/j.1365-313X.1997.11061369.x.
Arnold, M.L.; Hodges, S.A. Reply from M.L. Arnold and S.A. Hodges. Trends Ecol. Evol. 1995, doi:10.1016/0169-5347(95)90023-3.
Brandão, L.R.; Portilho, N.; de Oliveira, A.C.; Coelho, G.T.C.P.; Almeida, A. Genetic Transformation of Immature Sorghum Inflorescence via Microprojectile Bombardment. In Transgenic Plants—Advances and Limitations; InTech: Rijeka, Croatia, 2012; doi:10.5772/33627.
Li, J.; Zhan, Q.; Fan, F.; Zhao, T.; Wan, H. Development of a Simple and Efficient Method for Agrobacterium-Mediated Transformation in Sorghum. Int. J. Agric. Biol. 2016, 134–138, doi:10.17957/IJAB/15.0075.
Hansen, G. Evidence for Agrobacterium-induced apoptosis in maize cells. Mol. Plant Microbe Interact. 2000, 13, 649–657, doi:10.1094/MPMI.2000.13.6.649.
Pu, X.; Goodman, R.N. Induction of necrogenesis by Agrobacterium tumefaciens on grape explants. Physiol. Mol. Plant Pathol. 1992, 41, 241–254, doi:10.1016/0885-5765(92)90024-P.
Aronen, T.S. Interactions between Agrobacterium tumefaciens and coniferous defence compounds alpha-pinene and trans-stilbene. Eur. J. For. Pathol. 1997, 27, 55–67.
Dong, J.; Kharb, P.; Teng, W.; Hall, T.C. Characterization of rice transformed via an Agrobacterium-mediated inflorescence approach. Mol. Breed. 2001, 7, 187–194.
Negrotto, D.; Jolley, M.; Beer, S.; Wenck, A.R.; Hansen, G. The use of phosphomannose isomerase as a selectable marker to recover transgenic maize plants (Zea mays L.) via Agrobacterium transformation. Plant Cell Rep. 2000, 19, 798–803.
Khanna, H.; Daggard, G. Agrobacterium tumefaciens-mediated transformation of wheat using a superbinary vector and a polyamine-supplemented regeneration medium. Plant Cell Rep. 2003, 21, 429–436, doi:10.1007/s00299-002-0529-x.
Frame, B.R.; Shou, H.; Chikwamba, R.K.; Zhang, Z.; Xiang, C.; Fonger, T.M.; Pegg, S.E.K.; Li, B.; Nettleton, D.S.; Pei, D.; et al. Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol. 2002, 129, 13–22.
Zhang, M.; Tang, Q.; Chen, Z.; Liu, J.; Cui, H.; Shu, Q.; Xia, Y.; Altosaar, I. [Genetic transformation of Bt gene into sorghum (Sorghum bicolor L.) mediated by Agrobacterium tumefaciens]. Sheng Wu Gong Cheng Xue Bao 2009, 25, 418–423.
Arulselvi, P.I.; Michael, P.; Umamaheswari, S.; Krishnaveni, S. Agrobacterium mediated transformation of Sorghum bicolor for disease resistance. Int. J. Pharma Bio Sci. 2010, 1, 272–281.
Ignacimuthu, S.; Premkumar, A. Development of transgenic Sorghum bicolor (L.) Moench resistant to the Chilo partellus (Swinhoe) through Agrobacterium-mediated transformation. Mol. Biol. Genet. Eng. 2014, 2, 1, doi:10.7243/2053-5767-2-1.
Mookkan, M.; Nelson-Vasilchik, K.; Hague, J.; Zhang, Z.J.; Kausch, A.P. Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2. Plant Cell Rep. 2017, 36, 1–15, doi: 10.1007/s00299-017-2169-1.
Hagio, T.; Blowers, A.D.; Earle, E.D. Stable transformation of sorghum cell cultures after bombardment with DNA-coated microprojectiles. Plant Cell Rep. 1991, 10, 260–264, doi:10.1007/BF00232571.
Able, J.A.; Rathus, C.; Godwin, I.D. The investigation of optimal bombardment parameters for transient and stable transgene expression in sorghum. In Vitro Cell. Dev. Biol. Plant 2001, 37, 341–348.
Emani, C.; Sunilkumar, G.; Rathore, K.S. Transgene silencing and reactivation in sorghum. Plant Sci. 2002, 162, 181–192, doi:10.1016/S0168-9452(01)00559-3.
Tadesse, Y.; Sagi, L.; Swennen, R.; Jacobs, M. Optimisation of transformation conditions and production of transgenic sorghum (Sorghum bicolor) via microparticle bombardment. Plant Cell Tissue Organ Cult. 2003, 75, 1–18.
Grootboom, A.; Mkhonza, N.; O’Kennedy, M. Biolistic mediated sorghum (Sorghum bicolor L. Moench) transformation via mannose and bialaphos based selection systems. Int. J. Bot. 2010, 6, 89–94.
Fraley, R.T.; Rogers, S.G.; Horsch, R.B.; Sanders, P.R.; Flick, J.S.; Adams, S.P.; Bittner, M.L.; Brand, L.A.; Fink, C.L.; Fry, J.S.; et al. Expression of bacterial genes in plant cells. Proc. Natl. Acad. Sci. USA 1983, 80, 4803–4807, doi:10.1073/pnas.80.15.4803.
Gritz, L.; Davies, J. Plasmid-encoded hygromycin B resistance: The sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccaromyces cerevisiae. Gene 1983, 26, 179–188, doi:10.1016/0378-1119(83)90223-8.
Thompson, C.J.; Movva, N.R.; Tizard, R.; Crameri, R.; Davies, J.E.; Lauwereys, M.; Botterman, J. Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J. 1987, 6, 2519, doi:10.1021/jf703567t.
Barry, G.; Kishore, G.; Padgette, S.; Taylor, M.; Kolacz, K.; Weldon, M.; Re, D.; Eichholtz, D.; Fincher, K.; Hallas, L. Inhibitors of amino acid biosynthesis: Strategies for imparting glyphosate tolerance to crop plants. Curr. Top. Plant Physiol. 1992, 7, 139–145.
Penna, S.; Sági, L.; Swennen, R. Positive selectable marker genes for routine plant transformation. In Vitro Cell. Dev. Biol. Plant 2002, 38, 125–128, doi:10.1079/IVP2001272.
Joersbo, M.; Okkels, F.T. A novel principle for selection of transgenic plant cells: Positive selection. Plant Cell Rep. 1996, 16, 219–221, doi:10.1007/BF01890871.
Reed, J.; Privalle, L.; Powell, L.; Meghji, M.; Dawson, J.; Dunder, E.; Suttie, J.; Wenck, A.; Launis, K.; Kramer, C.; et al. Phosphomannose isomerase: An efficient selectable marker for plant transformation. In Vitro Cell. Dev. Biol. Plant 2001, 37, 127–132, doi:10.1079/IVP2000162.
Sheen, J.; Hwang, S.; Niwa, Y.; Kobayashi, H.; Galbraith, D.W. Green-fluorescent protein as a new vital marker in plant cells. Plant J. 1995, 8, 777–784, doi:10.1046/j.1365-313X.1995.08050777.x.
Murashige, T.; Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant 1962, 15, 473–497, doi:10.1111/j.1399-3054.1962.tb08052.x.
Gamborg, O.L.; Miller, R.A.; Ojima, K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 1968, 50, 151–158, doi:10.1016/0014-4827(68)90403-5.
Winans, S.C.; Kerstetter, R.A.; Nester, E.W. Transcriptional regulation of the virA and virG genes of Agrobacterium tumefaciens. J. Bacteriol. 1988, 170, 4047–4054.
Enriquez-Obregon, G.A.; Vazquez-Padron, R.I.; Prieto-Samsonov, D.L.; de-a-Riva, G.A.; Selman-Housein, G. Herbicide-resistant sugarcane (Saccharum officinarum L.) plants by Agrobacterium-mediated transformation. Planta 1998, 206, 20–27, doi:10.1007/s004250050369.
Olhoft, P.M.; Flagel, L.E.; Somers, D.A. T-DNA locus structure in a large population of soybean plants transformed using the Agrobacterium-mediated cotyledonary-node method. Plant Biotechnol. J. 2004, 2, 289– 300, doi:10.1111/j.1467-7652.2004.00070.x.
Rafat, A.; Aziz, M.A.; Rashid, A.A.; Abdullah, S.N.A.; Kamaladini, H.; Sirchi, M.H.T.; Javadi, M.B. Optimization of Agrobacterium tumefaciens-mediated transformation Biotechnology and Genetic Engineering Reviews 19 and shoot regeneration after co-cultivation of cabbage (Brassica oleracea subsp. capitata) cv. KY Cross with AtHSP101 gene. Sci. Hort. 2010, 124, 1–8.
Kowalski, B.; van Staden, J. In vitro culture of two threatened South African medicinal trees—Ocotea bullata and Warburgia salutaris. Plant Growth Regul. 2001, 34, 223–228, doi: 10.1023/A:1013362615531.
Dillen, W.; Clercq, J.; Kapila, J.; Zambre, M.; Montagu, M.; Angenon, G. The effect of temperature on Agrobacterium tumefaciens-mediated gene transfer to plants. Plant J. 1997, 12, 1459–1463, doi:10.1046/j.1365-313x.1997.12061459.x.
Salas, M.; Park, S.; Srivatanakul, M.; Smith, R. Temperature influence on stable T-DNA integration in plant cells. Plant Cell Rep. 2001, 20, 701–705, doi:10.1007/s002990100374.
Rashid, H.; Yokoi, S.; Toriyama, K.; Hinata, K. Transgenic plant production mediated by Agrobacterium in indica rice. Plant Cell Rep. 1996, 15, 727–773, doi:10.1007/BF00232216.
Arencibia, A.D.; Carmona, E.R.; Tellez, P.; Chan, M.-T.; Yu, S.-M.; Trujillo, L.E.; Oramas, P. An efficient protocol for sugarcane (Saccharum spp. L.) transformation mediated by Agrobacterium tumefaciens. Transgen. Res. 1998, 7, 213–222, doi:10.1023/A:1008845114531.
Hashizume, F.; Tsuchiya, T.; Ugaki, M.; Niwa, Y.; Tachibana, N.; Kowyama, Y. Efficient Agrobacterium-mediated transformation and the usefulness of a synthetic GFP reporter gene in leading varieties of Japonica rice. Plant Biotechnol. 1999, 16, 397–401, doi:10.5511/plantbiotechnology.16.397.
Kondo, T.; Hasegawa, H.; Suzuki, M. Transformation and regeneration of garlic (Allium sativum L.) by Agrobacterium-mediated gene transfer. Plant Cell Rep. 2000, 19, 989–993, doi:10.1007/s002990000222.
Adkins, S. Cereal callus cultures: Control of headspace gases can optimise the conditions for callus proliferation. Aust. J. Bot. 1992, 40, 737–749, doi: 10.1071/bt9920737.
Kozai, T.; Smith, M.A.L. Environmental control in plant tissue culture. In Automation and Environmental Control in Plant Tissue Culture; Aitken-Christie, J., Kozai, T., Smith, M.A.L., Eds.; Kluwer Academic Publishers: Spain, 1995; pp. 301–318; ISBN 978-94-015-8461-6.
Chateau, S.; Sangwan, R.S.; Sangwan-Norreel, B.S. Competence of Arabidopsis thaliana genotypes and mutants for Agrobacterium tumefaciens-mediated gene transfer: Role of phytohormones. J. Exp. Bot. 2000, 51, 1961–1968, doi:10.1093/jexbot/51.353.1961.
Gordon-Kamm, W.; Dilkes, B.P.; Lowe, K.; Hoerster, G.; Sun, X.; Ross, M.; Church, L.; Bunde, C.; Farrell, J.; Hill, P.; et al. Stimulation of the cell cycle and maize transformation by disruption of the plant retinoblastoma pathway. Proc. Natl. Acad. Sci. USA 2002, 99, 11975–11980, doi:10.1073/pnas.142409899.
Ezeogu, L.I.; Duodu, K.G.; Taylor, J.R.N. Effects of endosperm texture and cooking conditions on the in vitro starch digestibility of sorghum and maize flours. J. Cereal Sci. 2005, 42, 33–44, doi:10.1016/j.jcs.2005.02.002.
Wu, Y.; Messing, J. RNA interference-mediated change in protein body morphology and seed opacity through loss of different zein proteins. Plant Physiol. 2010, 153, 337–347, doi:10.1104/pp.110.154690.
Oria, M.P.; Hamaker, B.R.; Axtell, J.D.; Huang, C.-P. A highly digestible sorghum mutant cultivar exhibits a unique folded structure of endosperm protein bodies. Proc. Natl. Acad. Sci. USA 2000, 97, 5065–5070, doi:10.1073/pnas.080076297.