Mol Biotechnol (2007) 37:169–180DOI 10.1007/s12033-007-0031-3 REVIEW PAPER History of plant tissue culture Trevor A. Thorpe Published online: 27 June 2007 Ó Humana Press Inc. 2007 Abstract Plant tissue culture, or the aseptic culture of Introduction cells, tissues, organs, and their components under defined physical and chemical conditions in vitro, is an important Plant tissue culture, also referred to as cell, in vitro, axenic, tool in both basic and applied studies as well as in com- or sterile culture, is an important tool in both basic and mercial application. It owes its origin to the ideas of the applied studies, as well as in commercial application [1]. German scientist, Haberlandt, at the begining of the 20th Plant tissue culture is the aseptic culture of cells, tissues, century. The early studies led to root cultures, embryo cul- organs and their components under defined physical and tures, and the first true callus/tissue cultures. The period chemical conditions in vitro. The theoretical basis for plant between the 1940s and the 1960s was marked by the devel- tissue culture was proposed by Gottlieb Haberlandt in his opment of new techniques and the improvement of those that address to the German Academy of Science in 1902 on his were already in use. It was the availability of these tech- experiments on the culture of single cells [2]. He opined niques that led to the application of tissue culture to five that, to my knowledge, no systematically organized at- broad areas, namely, cell behavior (including cytology, tempts to culture isolated vegetative cells from higher nutrition, metabolism, morphogenesis, embryogenesis, and plants have been made. Yet the results of such culture pathology), plant modification and improvement, pathogen- experiments should give some interesting insight to the free plants and germplasm storage, clonal propagation, and properties and potentialities that the cell, as an elementary product (mainly secondary metabolite) formation, starting in organism, possesses. Moreover, it would provide infor- the mid-1960s. The 1990s saw continued expansion in the mation about the interrelationships and complementary application of the in vitro technologies to an increasing influences to which cells within a multicellular whole number of plant species. Cell cultures have remained an organism are exposed (from the English translation, [3]). important tool in the study of basic areas of plant biology and He experimented with isolated photosynthetic leaf cells biochemistry and have assumed major significance in studies and other functionally differenced cells and was unsuc- in molecular biology and agricultural biotechnology. The cessful, but nevertheless he predicted that one could suc- historical development of these in vitro technologies and cessfully cultivate artificial embryos from vegetative cells. their applications are the focus of this chapter. He, thus, clearly established the concept of totipotency, and further indicated that the technique of cultivating isolated Keywords Cell behavior Cell suspensions Clonal plant cells in nutrient solution permits the investigation of propagation Organogenesis Plantlet regeneration important problems from a new experimental approach. On Plant transformation Protoplasts Somatic embryogenesis the basis of that 1902 address and his pioneering experi- Vector-dependent/independent gene transfer mentation before and later, Haberlandt is justifiably rec- ognized as the father of plant tissue culture. Other studies led to the culture of isolated root tips [4, 5]. This approach T. A. Thorpe (&) of using explants with meristematic cells produced the Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4 successful and indefinite culture of tomato root tips [6]. e-mail:
[email protected] Further work allowed for root culture on a completely and Gautheret [23]. protein hydrolysates. single cells crease in the use of in vitro cultures in the subsequent incorporated in a 1-mm layer of solidified medium formed decades. Nevertheless.170 Mol Biotechnol (2007) 37:169–180 defined medium. carrot root tissues [16. as the breakdown product of herring was followed by the successful rescue of embryos from sperm DNA [30]. but perhaps most importantly. and even made to differentiate resting on well-established callus. tissue. water [33]. However. Based this time that cells in culture underwent a variety of on studies with carrot and Virginia creeper tissues. roots. but Knop’s baceous dicots and gymnosperms. rooting. Callus cultures of sues in vitro were based on the nutrient formulations for numerous species. conditioned medium) [39]. Finally. Success was also achieved with bud cultures [8. and later in the induction of somatic embryos from the callus [42]. yeast extract. The application of coconut (tobacco) from a single cell by Vasil and Hildebrandt [44]. for which they were many [21]. Such root cultures were used initially for Studies by Skoog et al. 28]. and Salix quently discovered in several tissues. This morphogenic model has been shown to operate platanus. and for full embryo development in indefinitely. these changes did not provide this period that most of the in vitro techniques used today optimum growth for tissues. Native cytokinins were subse- Ulmus campestre. increased the number of species that could be cultured num austriacum [11]. Later. Greater detail on the early pioneering events in some cell colonies [40]. as well as crown-gall solution and that of Uspenski and Uspenskia were used the tissues. the changes. and provided less than 200 mg/l of total salts. finally led to reali- the development of new techniques and the improvement zation of Haberlandt’s dream of producing a whole plant of those already available. grown in medium in which tissues had already been grown ertheless. The 1940s. whole plants. these findings set the stage for the dramatic in. success was achieved in the culture of mechanically based on an earlier review by the author [24] (used with isolated mature differentiated mesophyll cells of Macleaya permission from Elsevier).. ognition that the exogenous balance of auxin and kinetin in viding one of the earliest applications of in vitro culture. the medium influenced the morphogenic fate of tobacco The phenomenon of precocious germination was also callus [31]. The development and improvement of techniques Lolium and rose in simple sparged 20-L carboys [43]. and with tumor tissue of a The culture of single cells (and small cell clumps) was Nicotiana glauca M Nicotiana langsdorffii hybrid [18]. As well. but only in the presence of vascular tissue. water (often incorrectly referred to as coconut milk) al. 1950s. and was habituation [26. including a variety of woody and her. The utilization of coconut water as an additive to fresh medium. in and Razdan [22].e. The first large-scale culture of plant cells was obtained from cell suspensions of Ginkgo. and coconut water. cordata [41]. Nev. A relative high level of auxin to kinetin favored encountered [13]. Further Embryo culture also had its beginning early in the first studies using nucleic acids led to the discovery of the first decade of the last century with barley embryos [10]. including monocots. holly. thus pro. The formation of bipolar somatic embryos glucose and cysteine hydrochloride. Robinia pseudoacacia. such as were largely developed. of indole acetic acid and the addition of B vitamins allowed 35] and Steward [36] in addition to the formation of for the more or less simultaneous demonstrations with unipolar shoot buds and roots. It was recognized at most. based on work with Jerusalem formed from callus [27. including coconut capraea using agar-solidified medium of Knop’s solution. giving rise to the roots and shoots [19. This current article is 1959. (i. tematic pith tissues to be cultured and produced shoots and 9]. the reverse led to shoot formation and intermediate The first true plant tissue cultures were obtained by levels to the proliferation of callus or wound parenchyma Gautheret [14. 27]. Bhojwani cloning cells and in protoplast culture [22]. tobacco. [29] showed that the addition of viral studies and later as a major tool for physiological adenine and high levels of phosphate allowed nonmeris- studies [7]. He also obtained success with similar explants of in numerous species [32]. 38]. it was during artichoke [46]. single cells could be used by these pioneers included meristematic tissue. thus demonstrating the totipotency of plant cells. and subsequently placing them on filter paper uously grown in culture. all the initial explants so-called nurse culture [37. Later. 17]. 20]. achieved by shaking callus cultures of Tagetes erecta and which did not require auxin. including loss of sensitivity to applied auxin or concentration of salts was increased twofold [45]. and 1960s proved an exciting time for instead of using conditioned medium. 4 g/l. were established as well [23]. the availability (carrot) was first reported independently by Reinert [34. This cytokinin (kinetin). and complex addenda. lowed for the culture of young embryos [25] and other The earliest nutrient media used for growing plant tis- recalcitrant tissues. as well as variability of meristems further increased ca. This technique is widely used for plant tissue culture could be found in White [21]. 15] from cambial tissue of Acer pseudo. The availability of kinetin further nonviable seeds of a cross between Linum perenne M Li. led to the rec- some early ripening species of fruit trees [12]. However. that tissues could be contin. . Vasil [74]. The 100 years ago. In a different approach. among several sources. sues.Mol Biotechnol (2007) 37:169–180 171 were frequently required. This Braun’s work served as the foundation for Agrobacterium- was confirmed when virus-free Dahlia plants were ob. it is not surprising that. in a new era. It was later observed that the nature of the TIP was worked out in the 1970s [72]. glauca M tissue culture. there was a dramatic increase in their Compared to studies with embryos. a carbon source. namely: (1) cell behavior. not only at the inoculated [9]. The method was further refined [54]. but virus titer in the shoot meristem was very low [52]. and Papaver somniferum [59]. primary. and cultured cells and pollen grains. it was the finding of Guha well as morphogenesis and pathology of cultured tissues and Maheshwari [63. The tips were free of viruses [51]. free of bacteria. Plantlets were successfully produced by culturing shoot Braun [69] showed that in sunflower Agrobacterium tips with a couple of primordia of Lupinus and Tropaeolum tumefaciens could induce tumors. Takebe et al. Nevertheless. and growth regulators [48]. Plantlet regeneration via and germplasm storage. (3) pathogen-free plants were from immature maize [57]. Studies on the structure and physiology of quiescent tained from cultured anthers of Datura innoxia that opened cells in explants. many of ment of protoplast technology in the 1970s. These secondary tumors were until later when this approach to obtain virus-free orchids. Further experiments showed that crown gall potential was rapidly exploited. but the importance of this finding was not recognized sites. The first them using only a defined medium consisting of macro. and the first fusion was achieved in 1909 concentration of some salts was 25 times that of Knop’s [23]. Virus elimination was possible because vascular tis. based on Plant protoplasts or cells without cell walls were first an examination of the ash of tobacco callus. cell colonies were ob- tained from Ginkgo pollen grains in culture [61]. successful ovule cul. within which the viruses move. The MS salt formulation mesophyll protoplasts. free of bacteria and their cells could be cultured without its potential for clonal propagation was realized [49]. This was followed by the regener- is now the most widely used nutrient medium in plant ation of the first interspecific hybrid plants (N. product formation [1]. DNA remained controversial for more than a decade. the levels of NO3 and NH4 were until the use of a fungal cellulase by Cocking [66] ushered very high and the arrays of micronutrients were increased. which was probably a macromolecule [71]. The commercial availability of cell wall MS formulation allowed for a further increase in the degrading enzymes led to their wide use and the develop- number of plant species that could be cultured. at distant points. do not extend into the root or shoot apex. contained a tumor-inducing prin- mentals [50]. this remained an unexplored technology solution. These applications can be divided conveniently into regulating embryo and fruit development [56]. particularly with orna. In particular. However. as escantia reflexa [62]. (2) plant continuously growing tissue cultures from an endosperm modification and improvement. [67]. and now routinely used. Detailed information on the approaches used can be In vitro pollination and fertilization was pioneered using gleaned from Bhojwani and Razdan [22]. Studies with both ovaries and ovules ture. starting accompanied by rooting of pedicels in several species [56]. who obtained tobacco plants from mins. excised ovules and pollen grains together in the same medium and has been used to produce interspecific and Cell behavior intergeneric hybrids [60]. and (5) organogenesis was later achieved in Exocarpus cupressi. (4) clonal propagation. cytology. reduced N. Murashige mechanically isolated from plasmolysed tissues well over and Skoog (MS) [47] developed a new medium. Haploid plants of tobacco the induction of division in these explants and the char- were also obtained [65]. but. changes in cell structure associated with the new area of androgenesis. in the mid-1960s. N. Early studies had shown that cultured root ciple (TIP). langsdorffii) [68]. It should also be noted that the finding tained from infected plants by culturing their shoot tips by Ledoux [73] that plant cells could take up and integrate [53]. 64] that haploid plants could be ob. Earlier. agricul- ture is very limited. demonstration of the totipotency of protoplasts was by and micro-nutrients. based transformation. and secondary metabolism. [1]. The recent past Techniques for in vitro culture of floral and seed parts were developed during this period [55]. horticulture. The first attempts Based on the availability of the various in vitro techniques at ovary culture yielded limited growth of the ovaries discussed in Subheading 2. The auxin [70]. The first five broad areas.. protoplasts have been carried out using light and electron . nutrition. formis [58]. application to various problems in basic biology. and forestry through the 1970s and have been geared mainly to an understanding of factors 1980s. B vita. tissues. and Included under this heading are studies dealing with haploid callus was obtained from whole anthers of Trad. The approach involves culturing Vasil and Thorpe [75]. thus confirming the totipotency of acteristics of developing callus. and although aimed mainly at plant Nutrition was the earliest aspect of plant tissue culture improvement (see next section) provided good fundamen- investigated. chemical differences. In plants [114].g. overcoming seed dormancy and related problems [111. tinued to influence research on this topic. Nuclear cytology studies have shown resistance. for isolation of variants [116]. but this potential has not yet been realized. in vitro methods were increasingly used and viable organelles were obtained for study (e. with Agrobacteria. important role in producing interspecific and intergeneric ated. such as (e. These include cells showing bio- conifers. cases has it been possible to regenerate plants with the igenesis [106]. In addition to bulky explants. habituation). somatic embryogenesis. 81]. androgenesis had been reported in application [1]. auxotrophs.. and nuclear fragmen. endomitosis. it is clear from the literature that several addi. placenta. The technique of regulation of inorganic nitrogen and sulfur assimilation controlled in vitro pollination on the stigma. Cell cultures have also played an important role in plant However. that endoreduplication. with altered developmental systems have been selected in cess.g. it was only in the 1970s that attempts cotyledons. and those carrot [105] has allowed for an in depth study of the pro. The third area of simple in origin [118. herbicide. legumes. but also on the biochemistry of virus mul. 101.. carbohydrate metabolism [87]. and photosynthetic ovule has been used for the production of interspecific and carbon metabolism [88. as they offer advantages tional factors. In addition. as indicated earlier. 99] have been used in traditional morpho. Morphogenesis or the origin of form is an area of 112]. Most of the work on secondary metabolism was related to ovary.172 Mol Biotechnol (2007) 37:169–180 microscopy [76–79]. Although tissue culture- interact with auxin and cytokinin to bring about de novo produced variants that have been known since the 1940s organogenesis [97].g. embryo rescue has played a most research with which tissue culture has long been associ. the production of double haploids allowed for hybrid pro- ported more recently by transformation of cells with duction and their integration into breeding programs. The classical findings of Skoog and Miller detect mutations and for recovery of unique recombinants.. a concept sup. Xylogenesis or tracheary element forma. Progress has been made in tal information [96]. In particular. Without doubt the most important studies in this area dealt tation are common features of culture cells [80. and disease methyl tryptophan-resistant Datura innoxia [122]. Successful also been possible to produce a wide spectrum of mutant culture was achieved with cereals. 83]. cell suspensions have been used to study the modification and improvement of plants. particularly as affected by phytoalexins [109]. appropriately modified Agrobacterium T-DNA [95. because there is no masking of recessive alleles. As well. modification and improvement. many of which were important crop tion has been used to study cytodifferentation [92–94]. as well as to produce de novo organs and in a population of cells. also developed in plantlets have potential agricultural and horticultural sig- this period with over 130 species reported to form the nificance. It has bipolar structures by the early 1980s [103. and the induction of haploid plants [110]. desired traits (e. The variation may be genetic or epigenetic and is not have been carried out [97. hypocotyls. 96]. as an adjunct to traditional breeding methods for the oles) [85]. 104]. . thus clearly showing the use. and callus [97]. overcoming sexual self-incompati- fulness of cell cultures for elucidating pathway activity. previously considered to be recalcitrant groups. 119]. and stress The development of a single cell to embryo system in resistance. grasses. Embryo. including other growth active substances. 89]. 102]. herbicide-resistant tobacco) [121]. bility. vacu. antibiotic. not only in tumor. duced. and one to which tissue culture has made significant hybrids [113]. culture. embryo inviability. particularly cell suspensions have become very useful Plant modification and improvement in the study of both primary and secondary metabolism [84]. and ovule cultures have been used in overcoming the potential of cultured cells to form commercial products. the culture of photoautotrophic cells [82. and tiplication [107]. autotrophs. thin (superficial) were made to utilize them for plant improvement. somaclonal variation is dependent on the natural variation genic studies. The changes in the regenerated morphogenesis. 100]. phytotoxin action [108]. 91]. either pre-existing or culture-in- plantlets in hundreds of plant species [50. [31] on the hormonal balance for organogenesis has con. in only a few the study of plant-microbe interaction. intergeneric hybrids. Gynogenesis was reported in some 15 species. contributions both in terms of fundamental knowledge and By the early 1980s. In vitro cul- tures. As well. However. This cell layers [98. and is usually observed in regenerated plantlets physiological and biochemical studies on organogenesis [117]. or [86]. particular the optimization of the Zinnia mesophyll single in some of which androgenesis was not successful [115]. cell system has dramatically improved our knowledge of The value of these haploids was that they could be used to this process. monoploid production in barley and in but has also yielded basic biochemical information [90. In addition to providing protoplasts from which intact During this period. and cells in culture [120]. some 171 species. usually the application of the selective agent in the Cell cultures have continued to play an important role in presence of a mutagen is required. is frozen and stored problem being the ability to regenerate plants from the at the temperature of liquid nitrogen (ca. [50. The selected plants contained B. production of date. 135].. 134]. with polyethylene cryopreservation [135]. but they are generally genetically true- dent methods with protoplasts include electroporation to-type. In this last approach. and microinjection [129]. only a few such examples exist to These are enhancing axillary bud breaking. Vector-indepen. liposome fusion [128]. As well. number of plantlets. 125].. 139]. including field and reports of stable transformation [131. and Genetic modification of plants has been achieved by somatic embryogenesis directly or indirectly on explants direct DNA transfer via vector-independent and vector. hybrid cells [124. Meristem-tip important plant products are either not formed in suffi- culture is often coupled with thermotherapy or chemo. napus the technology. there are many lab-scale mediated transfer has progressed very rapidly since the first protocols for other classes of plants. napus phe. produce unique nuclear-cytoplasmic combinations. in the lowest number of plant species. resolved (e. This latter method can be executed with cells. regenerable or. asexual embryos. Much of the research activity utilizing these tools has focused on engineering important Product formation agricultural traits for the control of insects. Furthermore. Commercially. and organs. Brassica campestris chloroplasts coding for Clonal propagation atrazine resistance (obtained from protoplasts) were trans- ferred into B. Unfortunately. secondary metabolites. which are of pharmaceutical and industrial Pathogen-free plants and germplasm storage interest. –196°C) [135. and could be used for hybrid seed production three ways by which micropropagation can be achieved. Higher plants produce a large number of diverse organic chemicals. The use of Agrobacterium in vector. adventitious buds directly or indirectly via callus. cell suspen- glycol [PEG]) and physical means (e.g. 138].g. stems. although some problems still need to be from R. and abscisic acid [ABA]) regenerated from protoplasts [123]. by 1987. germplasm has been maintained as seed. It has been used with all classes of plants nuclei. plantation. bud breaking [140]. had the desired traits in a B. producers of secondary metabolites than the respective tericidal and fungicidal agents can be used successfully plants [143]. and fungi by culturing meristem-tips has cell cultures was considered feasible [142]. and young plantlets. [126]. and plant protoplasts by chemical (e. Three in vitro approaches have been linked immunosorbent assay (ELISA) and radioimmuno- developed.g. weeds. fruit. abberant plants). There are notype.. been widely used since the 1960s. listics) [130].g. The first attempt at the large-scale culture of plant cells for the production of pharmaceuticals took place in Although these two uses of in vitro technology may appear the 1950s at the Charles Pfizer Co. In one such example. but is induced well as high-velocity microprojectile bombardment (bio. Unfortunately. but cost early transformations utilized protoplasts. as to produce the greatest number of plantlets. mainly via axillary tissues. Although the vegetable crops. The failure of this effort unrelated. of production is often a limiting factor in their use gans such as leaves. 132]. sativus.Mol Biotechnol (2007) 37:169–180 173 By 1985. there were 30 cell culture systems that were better ticularly needed for virus-infected material. chloroplasts from B. The ability to fuse [136]. and forest trees. electrofusion) sions. Protoplast fusion has been used to 137]. low-nonfreezing temperatures (1–9°C) [22]. hyperhydricity. quently used [133. napus protoplasts with Raphanus sativus The use of tissue culture technology for the vegetative cytoplasm (which confers cytoplasmic male sterility from propagation of plants is the most widely used application of its mitochondria). allowed for production of somatic hybrid plants. These include cell cloning and the but the ability to regenerate whole plants from somatic and repeated selection of high-yielding strains from heteroge- gametic cells and shoot apices has led to their use for nous cell populations [142. Different approaches have been taken to enhance yields of Traditionally. campestris and mitochondria [138. commercially [141]. and roots have been subse. maleic hydrazide. The ability to rid plants of development. so that by 1978 the industrial application of viruses. bacteria.. nearly 100 species of angiosperms could be (e. led to across international borders [1]. Axillary bud breaking produces the smallest dependent means since the early 1980s. the major after treatment with a cryoprotectant. a major use of pathogen-free plants is for limited research in this area in the United States. whereas somatic embryogenesis has the potential [127]. numerous ornamentals are produced. therapy for virus eradication [135]. ciently large quantities or not at all by plant cell cultures. Another approach involves . because bac. 144] and by using enzyme storage [22. many of the economically in ridding plants of bacteria and fungi [22]. namely use of growth retarding compounds assay techniques [145]. B995. but work germplasm storage and the movement of living material elsewhere in Germany and Japan in particular. The approach is par. and plant diseases. shoot apices. achieved in exploiting somaclonal variation [165]. and has concentrated on agronomic traits of direct remained largely unfulfilled [167]. and em. possible for the particular species. 183]. or the regulation of carbohy- microbial origin. and biochemical studies have produced secondary metabolite by cell cultures [153]. The present Advances in molecular biology are allowing for the genetic engineering of plants. Better physiological and The next wave in agricultural biotechnology is already in biochemical tools have allowed for a re-examination of progress with biotechnological applications of interest to neoplastic growth in cell cultures during habituation and the food processing. Current research is leading to routine have been successfully developed [170]. As well. Cell cultures have remained an extremely product [146]. These are used with all types of plants. for example. ornamentals [164]. and. tropical [161] fruits. As can be the development of selectable markers [190]. In the first stage. temperate ods to use these vectors for the direct transformation of [160]. Three of in vitro technologies to an increasing number of plant major breakthroughs have played major roles in the devel- species was observed. the meth- other root and tuber crops [158]. as well as of the culture environment by use of nonionic surfactants some woody plants. is adding with minimal cell division or growth. cell-cycle studies [173. Tissue culture techniques are being opment of this transformation technology [187]. in studies of the cytoskeleton [171]. ciency. plantation crops [162]. morphogenesis. chemical. With these latter approaches. However. and plant diseases [192]. However. particularly of Arabidopsis. gene transfer capability of Agrobacterium [188]. and the problem(s) being particularly biolistics [191]. through the precise insertion During the 1990s. Similar information aris- substances commercially is the capacity to grow cells on a ing from the use of cell cultures for molecular and large scale. oilseeds [159]. been made in extending cryopreservation technology for weeds. gene transfer systems for all-important crops. Cell cultures have remained an important tool in the the production of golden rice [193]. and trees [163]. by 1987 valuable information on plant development (see ref. including cereals and grasses the development of shuttle vectors for harnessing the natural [154]. as well as manipulation increasing number of monocotyledonous ones. 174]. even though the present use of develop- whereas the second stage concentrates on product synthesis mental mutants. [169]. Thus progress is being made in cell improvements are further increasing transformation effi- biology. only limited success has been transform virtually any plant species and genotype. and pharmaceu- hyperhydricity. physical. organo- genesis [182. the early promise of protoplast technology has tries. it has become possible to addressed. shikonin was the only commercially Molecular. lism. over 100 germplasm storage [168] and in artificial seed technology species of plants have been genetically engineered. potato [157]. continued expansion in the application of foreign genes from diverse biological systems.174 Mol Biotechnol (2007) 37:169–180 selection of mutant cell lines that overproduce the desired in plants [175]. . physiological. technology went well beyond micropropagation. 148]. speciality chemical. for ultraviolet (UV) irradiation. the naphthoquinone. membranes. 180). 178). the use of cell suspensions to develop in vitro salts of heavy metals and biotic elicitors of plant and transcription systems [176]. medicinal plant cell-culture techniques has led to the lized cell technology has also been examined [149. extending transformation to elite commercial on chromosomal changes in cultured cells [172]. allowed for an indepth understanding of cytodifferentia- tion. forest regenerable explants obtained from plant organs [189]. and somatic embryogenesis [184–186]. This is being achieved using stirred tank biochemical studies on other areas of secondary metabo- reactor systems and a range of air-driven reactors [141]. and mechanical means are used to get braced all the in vitro approaches that were relevant or the DNA into the cells. and in germplasm and lowering transgenic plant production costs. Substantial progress has relevance to these industries. been driven mainly by the seed and agri-chemical indus- also. rapid Cell cultures remain an important tool in the study of cell growth and biomass accumulation are emphasized. of course. technical study of plant biology. is generating research activity on metabolic engi- For many systems. and glass rods. and relate it to possible cancerous growth tical industries. Lastly. the use of immobi. 150]. process has been tried [151. For species seen from these articles. In addition. The development of product formation [147. mainly tracheary element formation [181]. the application of in vitro cell not amenable to Agrobacterium-mediated transformation. At present. 152]. both abiotic factors—such as important tool in the study of primary metabolism. Some novel approaches for culturing cells such as on including nearly all the major dicotyledonous crops and an rafts. legumes [155]. identification of more than 80 enzymes of alkaloid bio- Central to the success of producing biologically active synthesis (reviewed in ref. namely the control of insects. vegetable crops [156]. exposure to heat or cold and example. a two-stage (or two-phase) culture neering of plant secondary metabolite production [179]. have been shown to enhance secondary drate metabolism in transgenics [177]. for example. or in the The initial wave of research in plant biotechnology has regeneration of useful plantlets from mutant cells [166]. 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