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T-DNA Organization in Tumor Cultures and Transgenic Plants Of Proc. Nati. Acad. Sci. USA Vol. 84, pp. 5345-5349, August 1987 Genetics T-DNA organization in tumor cultures and transgenic plants of the monocotyledon Asparagus officinalis (Agrobacterium tumefaciens/monocotyledon transformation/kanamycin resistance) BENNY BYTEBIER*, FRANCINE DEBOECK*, HENRI DE GREVE*, MARC VAN MONTAGU*t, AND JEAN-PIERRE HERNALSTEENS* *Laboratorium voor Genetische Virologie, Vrije Universiteit Brussel, Paardenstraat 65, B-1640 Sint-Genesius-Rode, Belgium; and tLaboratorium voor Genetica, Rijksuniversiteit Gent, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium Contributed by Marc Van Montagu, April 6, 1987 ABSTRACT Asparagus officinalis was the first monocot- T-DNA is bounded by essentially identical 25-base-pair (bp) yledonous plant from which hormone-independent and opine- direct repeats. These sequences define the T-DNA. The producing crown gall tissue could be isolated. We confirm by junction between plant and bacterial DNA occurs within or DNA hybridization that tumor lines obtained after infection of adjacent to the border sequence in a number of independent this plant by Agrobacterium strains harboring wild-type no- tumor lines (10-13). (ii) The oncogenicity genes that prevent paline and octopine tumor-inducing (Ti) plasmids are stably normal regeneration of transformed tissue are not necessary transformed and contain transferred DNA (T-DNA) segments for T-DNA transfer and integration (5, 7). (iii) Any DNA identical to the T-DNA found in dicotyledonous plants. We sequence inserted between the 25-bp repeats is cotransferred have also infected Asparagus with a nononcogenic T-DNA with the T-DNA to the plant genome (14). Based on these vector that carries a chimeric aminoglycoside phosphotrans- findings a number of vector systems were developed that ferase [NOS-APH(3')IIJ gene and selected transformed tissues today are commonly used to transform dicotyledonous on kanamycin-containing medium. The transformed status of plants. these tissues was then confirmed by DNA hybridization. From Historically monocotyledonous plants were thought insen- these calli we regenerated kanamycin-resistant shoots that were sitive to Agrobacterium infection, although it has been subsequently rooted. Thus we report the isolation oftransgenic reported that at least some monocotyledons are susceptible monocotyledonous plants engineered via the Agrobacterium to infection (for review, see ref. 15). Only recently, however, vector system. has the evidence for transformation extended beyond mor- phological changes in the infected tissue (16-18). Hernal- The soil bacterium, Agrobacterium tumefaciens, causes steens et al. (16) isolated tumor tissue that would grow on crown gall, a neoplastic transformation ofthe wounded tissue hormone-free medium after infecting stem fragments of of a wide range of dicotyledonous plants. All oncogenic Asparagus officinalis, a member ofthe family Liliaceae, with Agrobacterium strains have a large tumor-inducing (Ti) the wild-type A. tumefaciens strain C58. This tissue produced plasmid. Tumor induction is the result of the transfer and the opines nopaline and agrocinopine. However, the physical stable integration of a well-defined portion of the Ti plasmid, organization of T-DNA in the monocotyledon genomne was called the T-region, into the plant genome. The transferred not demonstrated at that time, and therefore it was not known DNA (T-DNA) encodes oncogenic functions involved in whether normal T-DNA integration had occurred in this phytohormone biosynthesis, which cause tumorous prolifer- uncommonly used host. ation of the transformed tissue. The T-DNA also encodes We report on DNA hybridization data of this tissue and of enzymes that synthesize tumor-specific compounds called another tumor line induced by A. tumefaciens strain C58C1 opines. The Ti plasmids are classified according to the type pTiB6S3 harboring an octopine type Ti plasmid. The analysis of opine they specify. Best studied are the nopaline and ofboth Asparagus tumor lines shows that T-DNA integration octopine type Ti plasmids. For a recent review on the is very similar to the pattern of integration found in dicoty- molecular biology of crown gall disease, see ref. 1. ledons. The organization of the T-DNA of both nopaline and Because the oncogenicity genes prevent normal regener- octopine tumors of dicotyledonous plants has been elucidat- ation of transformed tissue, we then tested whether a ed by Southern transfer and hybridization experiments (2-4). nononcogenic Ti plasmid-derived vector containing a domi- nant selectable marker for plant cells could be used to The nopaline T-DNA is a continuous stretch of 23 kilobases construct transgenic monocotyledonous plants. After infect- (kb) (2). Octopine tumors, however, may contain two inde- ing cells with a vector that carried a chimeric kanamycin- pendently transferred T-DNAs (3, 4). The left-hand T-DNA resistance gene, we selected transformed callus on kana- (TL) of 13.2 kb is always present. It includes the genes mycin-containing medium. DNA hybridization confirmed responsible for tumorous proliferation of the transformed that T-DNA integration had occurred normally. From this tissue (5-7) in addition to the octopine synthase gene (5, 8). tissue we could regenerate transgenic Asparagus plants. The right-hand T-DNA segment (TR) is 7.9 kb in length and originates from a part ofthe plasmid located to the right ofthe TL region. The TR-DNA encodes the genes for the synthesis MATERIALS AND METHODS of agropine and mannopine (9). It is often absent from crown Hybridization Analysis. DNA was prepared (19) from gall tumor cultures (3, 4). axenically cultured tumor tissue. Before the final DNA Three other findings were ofimportance in our understand- precipitation step, S ,tl of a 2.5 mg of pancreatic RNase A per ing of the A. tumefaciens DNA transfer system: (i) The ml solution was added, and the reaction mixture was incu- The publication costs of this article were defrayed in part by page charge Abbreviations: Ti, tumor inducing; TL, left-hand 13.2-kb transferred payment. This article must therefore be hereby marked "advertisement" DNA of octopine tumors; TR, right-hand 7.9-kb transferred DNA of in accordance with 18 U.S.C. §1734 solely to indicate this fact. octopine tumors; T-DNA, transferred DNA. 5345 Downloaded by guest on September 26, 2021 5346 Genetics: Bytebier et al. Proc. Natl. Acad. Sci. USA 84 (1987) bated at 370C for 15 min. Ten micrograms of DNA was medium with 0.1 mg of 6-benzylaminopurine per liter for digested, electrophoresed through a 0.8% agarose gel, and shoot proliferation. Clumps of shoots were divided into parts transferred onto GeneScreenPlus (New England Nuclear) or containing 3-10 spears each and put on LS medium with 0.5 Hybond N (Amersham) membranes according to the manu- mg of indole-3-acetic acid (26) for rooting. Rooted plants facturers' instructions. 32P-labeled DNA probes were pre- were transferred into glass jars containing a 3-cm layer of pared by nick-translation (20) or by the procedure described sterile horticultural perlite (Sibli, Liege, Belgium) moistened by Feinberg and Vogelstein (21, 22). Hybridization and with half-strength MS mineral medium, and covered with washing was done using standard procedures (23). The filters plastic film. Daily the plastic cover was punctured until the were exposed to x-ray films using an intensifying screen at plants were completely exposed to their surroundings; they -700C. were then transferred to pots filled with perlite and watered Transformation and Selection. Asparagus transformation with fertilizer-containing solution (Peters 20+20+20; 200 mg by A. tumefaciens strain C58C1 pTiB6S3 was done as per liter). described by Hernalsteens et al. (16). The transformation procedure used for A. tumefaciens strain C58C1 pGV- 3850::1103neo(dim) (24) relied on the same protocol. In RESULTS AND DISCUSSION vivo-grown Asparagus spears were surface-sterilized and cut into 3-cm-long pieces, which were inverted and planted 5 mm Analysis of Asparagus Tumor DNA Transformed by A. deep in half-strength Murashige and Skoog (MS) medium tumefaciens Strain C58. Fig. 1 presents the nucleic acid (35). A. tumefaciens C58C1 pGV3850::1103neo(dim) was hybridization data that shows the T-DNA in this tissue is cultured on Luria-Bertani medium (23) with 25 mg of kan- integrated into the Asparagus genome. Internal fragments amycin per liter and applied directly to the upper end of the spanning the T-DNA from EcoRI fragment 16 on the left- Asparagus segment with a spatula. One month after infec- hand side to the BamHI fragment 10 on the right-hand side tion, a 2-mm-thick slice ofinfected tissue was incubated twice can be detected in the different lanes. These fragments cover on Linsmaier and Skoog (LS) medium (36) with 200 mg of the T-DNA over a length of 23 kb, which means that no glutamine per liter, 1 mg of 6-benzylaminopurine per liter, detectable deletions resulted from transfer or integration. and 1 mg of a-naphthaleneacetic acid per liter (25) for 1 mo. The BamHI, HindIlI, and Sal I-digested DNA fragments The tissue was then transferred to the same callus-inducing were hybridized with a probe homologous to the right-border medium now supplemented with 50 mg of kanamycin sulfate region (HindIII fragment 23); each lane shows four composite per liter. fragments of different lengths (the BamHI lane contains a Regeneration. Kanamycin-resistant callus was transferred fifth fragment of 5 kb, which is the internal BamHI fragment to LS medium with 200 mg of glutamine per liter, 40 mg of 10). Therefore, we conclude that at least four copies of the adenine per liter, 4 mg of 6-benzylaminopurine per liter, and T-DNA are integrated into the Asparagus genome. Because 1 mg of a-naphthaleneacetic acid per liter (25) on which it this tumorous tissue is not of clonal origin, we do not know regenerated shoots. These shoots were then moved to LS whether these copies represent multiple T-DNA insertions A Probe A Probe 8 Probe C Probe D ~co c9 .Vf-.
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