Site icon Propagate One

History of plant tissue culture: Trevor A. Thorpe

Prop Master 2K

Plant tissue culture, also referred to as cell, in vitro, axenic, or sterile culture, is an important tool in both basic and applied studies, as well as in commercial application [1]. Plant tissue culture is the aseptic culture of cells, tissues, organs and their components under defined physical and chemical conditions in vitro. The theoretical basis for plant tissue culture was proposed by Gottlieb Haberlandt in his address to the German Academy of Science in 1902 on his experiments on the culture of single cells [2]. He opined that, to my knowledge, no systematically organized at- tempts to culture isolated vegetative cells from higher plants have been made. Yet the results of such culture experiments should give some interesting insight to the properties and potentialities that the cell, as an elementary organism, possesses. Moreover, it would provide infor- mation about the interrelationships and complementary influences to which cells within a multicellular whole organism are exposed (from the English translation, [3]). He experimented with isolated photosynthetic leaf cells and other functionally differenced cells and was unsuc- cessful, but nevertheless he predicted that one could suc- cessfully cultivate artificial embryos from vegetative cells. He, thus, clearly established the concept of totipotency, and further indicated that the technique of cultivating isolated plant cells in nutrient solution permits the investigation of important problems from a new experimental approach. On the basis of that 1902 address and his pioneering experi- 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 of using explants with meristematic cells produced the successful and indefinite culture of tomato root tips [6]. Further work allowed for root culture on a completely

defined medium. Such root cultures were used initially for viral studies and later as a major tool for physiological studies [7]. Success was also achieved with bud cultures [8, 9].

Embryo culture also had its beginning early in the first decade of the last century with barley embryos [10]. This was followed by the successful rescue of embryos from nonviable seeds of a cross between Linum perenne M Li- num austriacum [11], and for full embryo development in some early ripening species of fruit trees [12]; thus pro- viding one of the earliest applications of in vitro culture.

The phenomenon of precocious germination was also encountered [13].

The first true plant tissue cultures were obtained by Gautheret [14, 15] from cambial tissue of Acer pseudo- platanus. He also obtained success with similar explants of Ulmus campestre, Robinia pseudoacacia, and Salix capraea using agar-solidified medium of Knop’s solution, glucose and cysteine hydrochloride. Later, the availability of indole acetic acid and the addition of B vitamins allowed for the more or less simultaneous demonstrations with carrot root tissues [16, 17], and with tumor tissue of a

Nicotiana glauca M Nicotiana langsdorffii hybrid [18],

which did not require auxin, that tissues could be contin- uously grown in culture; and even made to differentiate roots and shoots [19, 20]. However, all the initial explants used by these pioneers included meristematic tissue. Nev- ertheless, these findings set the stage for the dramatic in- crease in the use of in vitro cultures in the subsequent decades. Greater detail on the early pioneering events in plant tissue culture could be found in White [21], Bhojwani and Razdan [22], and Gautheret [23]. This current article is based on an earlier review by the author [24] (used with permission from Elsevier).

The development and improvement of techniques

The 1940s, 1950s, and 1960s proved an exciting time for the development of new techniques and the improvement of those already available. The application of coconut water (often incorrectly referred to as coconut milk) al- lowed for the culture of young embryos [25] and other recalcitrant tissues, including monocots. Callus cultures of numerous species, including a variety of woody and her- baceous dicots and gymnosperms, as well as crown-gall tissues, were established as well [23]. It was recognized at this time that cells in culture underwent a variety of changes, including loss of sensitivity to applied auxin or habituation [26, 27], as well as variability of meristems formed from callus [27, 28]. Nevertheless, it was during this period that most of the in vitro techniques used today were largely developed.

Studies by Skoog et al. [29] showed that the addition of adenine and high levels of phosphate allowed nonmeris- tematic pith tissues to be cultured and produced shoots and roots, but only in the presence of vascular tissue. Further studies using nucleic acids led to the discovery of the first cytokinin (kinetin), as the breakdown product of herring sperm DNA [30]. The availability of kinetin further increased the number of species that could be cultured indefinitely, but perhaps most importantly, led to the rec- ognition that the exogenous balance of auxin and kinetin in the medium influenced the morphogenic fate of tobacco callus [31]. A relative high level of auxin to kinetin favored rooting, the reverse led to shoot formation and intermediate levels to the proliferation of callus or wound parenchyma tissue. This morphogenic model has been shown to operate in numerous species [32]. Native cytokinins were subse- quently discovered in several tissues, including coconut water [33]. The formation of bipolar somatic embryos (carrot) was first reported independently by Reinert [34, 35] and Steward [36] in addition to the formation of unipolar shoot buds and roots.

The culture of single cells (and small cell clumps) was achieved by shaking callus cultures of Tagetes erecta and tobacco, and subsequently placing them on filter paper resting on well-established callus, giving rise to the so-called nurse culture [37, 38]. Later, single cells could be grown in medium in which tissues had already been grown (i.e., conditioned medium) [39]. As well, single cells incorporated in a 1-mm layer of solidified medium formed some cell colonies [40]. This technique is widely used for cloning cells and in protoplast culture [22]. Finally, in 1959, success was achieved in the culture of mechanically isolated mature differentiated mesophyll cells of Macleaya cordata [41], and later in the induction of somatic embryos from the callus [42]. The first large-scale culture of plant cells was obtained from cell suspensions of Ginkgo, holly, Lolium and rose in simple sparged 20-L carboys [43]. The utilization of coconut water as an additive to fresh medium, instead of using conditioned medium, finally led to reali- zation of Haberlandt’s dream of producing a whole plant (tobacco) from a single cell by Vasil and Hildebrandt [44], thus demonstrating the totipotency of plant cells.

The earliest nutrient media used for growing plant tis- sues in vitro were based on the nutrient formulations for whole plants, for which they were many [21]; but Knop’s solution and that of Uspenski and Uspenskia were used the most, and provided less than 200 mg/l of total salts. Based on studies with carrot and Virginia creeper tissues, the concentration of salts was increased twofold [45], and was further increased ca. 4 g/l, based on work with Jerusalem artichoke [46]. However, these changes did not provide optimum growth for tissues, and complex addenda, such as yeast extract, protein hydrolysates, and coconut water,

were frequently required. In a different approach, based on an examination of the ash of tobacco callus, Murashige and Skoog (MS) [47] developed a new medium. The concentration of some salts was 25 times that of Knop’s solution. In particular, the levels of NO3 and NH4 were very high and the arrays of micronutrients were increased. MS formulation allowed for a further increase in the number of plant species that could be cultured, many of them using only a defined medium consisting of macro- and micro-nutrients, a carbon source, reduced N, B vita- mins, and growth regulators [48]. The MS salt formulation is now the most widely used nutrient medium in plant tissue culture.

Plantlets were successfully produced by culturing shoot tips with a couple of primordia of Lupinus and Tropaeolum [9], but the importance of this finding was not recognized until later when this approach to obtain virus-free orchids, its potential for clonal propagation was realized [49]. The potential was rapidly exploited, particularly with orna- mentals [50]. Early studies had shown that cultured root tips were free of viruses [51]. It was later observed that the virus titer in the shoot meristem was very low [52]. This was confirmed when virus-free Dahlia plants were ob- tained from infected plants by culturing their shoot tips [53]. Virus elimination was possible because vascular tis- sues, within which the viruses move, do not extend into the root or shoot apex. The method was further refined [54], and now routinely used.

Techniques for in vitro culture of floral and seed parts were developed during this period [55]. The first attempts at ovary culture yielded limited growth of the ovaries accompanied by rooting of pedicels in several species [56]. Compared to studies with embryos, successful ovule cul- ture is very limited. Studies with both ovaries and ovules have been geared mainly to an understanding of factors regulating embryo and fruit development [56]. The first continuously growing tissue cultures from an endosperm were from immature maize [57]. Plantlet regeneration via organogenesis was later achieved in Exocarpus cupressi- formis [58].

In vitro pollination and fertilization was pioneered using Papaver somniferum [59]. The approach involves culturing excised ovules and pollen grains together in the same medium and has been used to produce interspecific and intergeneric hybrids [60]. Earlier, cell colonies were ob- tained from Ginkgo pollen grains in culture [61], and haploid callus was obtained from whole anthers of Trad- escantia reflexa [62]. However, it was the finding of Guha and Maheshwari [63, 64] that haploid plants could be ob- tained from cultured anthers of Datura innoxia that opened the new area of androgenesis. Haploid plants of tobacco were also obtained [65], thus confirming the totipotency of pollen grains.

Plant protoplasts or cells without cell walls were first mechanically isolated from plasmolysed tissues well over 100 years ago, and the first fusion was achieved in 1909 [23]. Nevertheless, this remained an unexplored technology until the use of a fungal cellulase by Cocking [66] ushered in a new era. The commercial availability of cell wall degrading enzymes led to their wide use and the develop- ment of protoplast technology in the 1970s. The first demonstration of the totipotency of protoplasts was by Takebe et al. [67], who obtained tobacco plants from

mesophyll protoplasts. This was followed by the regener- ation of the first interspecific hybrid plants (N. glauca M N. langsdorffii) [68].

Braun [69] showed that in sunflower Agrobacterium tumefaciens could induce tumors, not only at the inoculated sites, but, at distant points. These secondary tumors were free of bacteria and their cells could be cultured without auxin [70]. Further experiments showed that crown gall tissues, free of bacteria, contained a tumor-inducing prin- ciple (TIP), which was probably a macromolecule [71]. The nature of the TIP was worked out in the 1970s [72], but Braun’s work served as the foundation for Agrobacterium– based transformation. It should also be noted that the finding by Ledoux [73] that plant cells could take up and integrate DNA remained controversial for more than a decade.

The recent past

Based on the availability of the various in vitro techniques discussed in Subheading 2., it is not surprising that, starting in the mid-1960s, there was a dramatic increase in their application to various problems in basic biology, agricul- ture, horticulture, and forestry through the 1970s and 1980s. These applications can be divided conveniently into five broad areas, namely: (1) cell behavior, (2) plant modification and improvement, (3) pathogen-free plants and germplasm storage, (4) clonal propagation, and (5) product formation [1].

Detailed information on the approaches used can be gleaned from Bhojwani and Razdan [22], Vasil [74], and Vasil and Thorpe [75], among several sources.

Cell behavior

Included under this heading are studies dealing with cytology, nutrition, primary, and secondary metabolism, as well as morphogenesis and pathology of cultured tissues [1]. Studies on the structure and physiology of quiescent cells in explants, changes in cell structure associated with the induction of division in these explants and the char- acteristics of developing callus, and cultured cells and protoplasts have been carried out using light and electron

microscopy [76–79]. Nuclear cytology studies have shown that endoreduplication, endomitosis, and nuclear fragmen- tation are common features of culture cells [80, 81].

Nutrition was the earliest aspect of plant tissue culture investigated, as indicated earlier. Progress has been made in the culture of photoautotrophic cells [82, 83]. In vitro cul- tures, particularly cell suspensions have become very useful in the study of both primary and secondary metabolism [84]. In addition to providing protoplasts from which intact and viable organelles were obtained for study (e.g., vacu- oles) [85], cell suspensions have been used to study the regulation of inorganic nitrogen and sulfur assimilation [86], carbohydrate metabolism [87], and photosynthetic carbon metabolism [88, 89]; thus clearly showing the use- fulness of cell cultures for elucidating pathway activity. Most of the work on secondary metabolism was related to the potential of cultured cells to form commercial products, but has also yielded basic biochemical information [90, 91]. Morphogenesis or the origin of form is an area of research with which tissue culture has long been associ- ated; and one to which tissue culture has made significant contributions both in terms of fundamental knowledge and application [1]. Xylogenesis or tracheary element forma- tion has been used to study cytodifferentation [92–94]. In particular the optimization of the Zinnia mesophyll single cell system has dramatically improved our knowledge of this process. The classical findings of Skoog and Miller

[31] on the hormonal balance for organogenesis has con- tinued to influence research on this topic; a concept sup- ported more recently by transformation of cells with appropriately modified Agrobacterium T-DNA [95, 96]. However, it is clear from the literature that several addi- tional factors, including other growth active substances, interact with auxin and cytokinin to bring about de novo organogenesis [97]. In addition to bulky explants, such as cotyledons, hypocotyls, and callus [97], thin (superficial) cell layers [98, 99] have been used in traditional morpho- genic studies, as well as to produce de novo organs and plantlets in hundreds of plant species [50, 100]. As well, physiological and biochemical studies on organogenesis have been carried out [97, 101, 102]. The third area of morphogenesis, somatic embryogenesis, also developed in this period with over 130 species reported to form the bipolar structures by the early 1980s [103, 104]. Successful culture was achieved with cereals, grasses, legumes, and conifers, previously considered to be recalcitrant groups. The development of a single cell to embryo system in carrot [105] has allowed for an in depth study of the pro- cess.

Cell cultures have continued to play an important role in the study of plant-microbe interaction, not only in tumor- igenesis [106], but also on the biochemistry of virus mul- tiplication [107], phytotoxin action [108], and disease

resistance, particularly as affected by phytoalexins [109]. Without doubt the most important studies in this area dealt with Agrobacteria, and although aimed mainly at plant improvement (see next section) provided good fundamen- tal information [96].

Plant modification and improvement

During this period, in vitro methods were increasingly used as an adjunct to traditional breeding methods for the modification and improvement of plants. The technique of controlled in vitro pollination on the stigma, placenta, or ovule has been used for the production of interspecific and intergeneric hybrids, overcoming sexual self-incompati- bility, and the induction of haploid plants [110]. Embryo, ovary, and ovule cultures have been used in overcoming embryo inviability, monoploid production in barley and in overcoming seed dormancy and related problems [111, 112]. In particular, embryo rescue has played a most important role in producing interspecific and intergeneric hybrids [113].

By the early 1980s, androgenesis had been reported in some 171 species, many of which were important crop plants [114]. Gynogenesis was reported in some 15 species, in some of which androgenesis was not successful [115]. The value of these haploids was that they could be used to detect mutations and for recovery of unique recombinants, because there is no masking of recessive alleles. As well, the production of double haploids allowed for hybrid pro- duction and their integration into breeding programs.

Cell cultures have also played an important role in plant modification and improvement, as they offer advantages for isolation of variants [116]. Although tissue culture- produced variants that have been known since the 1940s (e.g., habituation), it was only in the 1970s that attempts were made to utilize them for plant improvement. This somaclonal variation is dependent on the natural variation in a population of cells, either pre-existing or culture-in- duced, and is usually observed in regenerated plantlets [117]. The variation may be genetic or epigenetic and is not simple in origin [118, 119]. The changes in the regenerated plantlets have potential agricultural and horticultural sig- nificance, but this potential has not yet been realized. It has also been possible to produce a wide spectrum of mutant cells in culture [120]. These include cells showing bio- chemical differences, antibiotic, herbicide, and stress resistance. In addition, auxotrophs, autotrophs, and those with altered developmental systems have been selected in culture; usually the application of the selective agent in the presence of a mutagen is required. However, in only a few cases has it been possible to regenerate plants with the desired traits (e.g., herbicide-resistant tobacco) [121], and methyl tryptophan-resistant Datura innoxia [122].

By 1985, nearly 100 species of angiosperms could be regenerated from protoplasts [123]. The ability to fuse plant protoplasts by chemical (e.g., with polyethylene glycol [PEG]) and physical means (e.g., electrofusion) allowed for production of somatic hybrid plants; the major problem being the ability to regenerate plants from the hybrid cells [124, 125]. Protoplast fusion has been used to produce unique nuclear-cytoplasmic combinations. In one such example, Brassica campestris chloroplasts coding for atrazine resistance (obtained from protoplasts) were trans- ferred into B. napus protoplasts with Raphanus sativus cytoplasm (which confers cytoplasmic male sterility from its mitochondria). The selected plants contained B. napus nuclei, chloroplasts from B. campestris and mitochondria from R. sativus, had the desired traits in a B. napus phe- notype, and could be used for hybrid seed production [126]. Unfortunately, only a few such examples exist to date.

Genetic modification of plants has been achieved by direct DNA transfer via vector-independent and vector- dependent means since the early 1980s. Vector-indepen- dent methods with protoplasts include electroporation [127], liposome fusion [128], and microinjection [129], as well as high-velocity microprojectile bombardment (bio- listics) [130]. This latter method can be executed with cells, tissues, and organs. The use of Agrobacterium in vector- mediated transfer has progressed very rapidly since the first reports of stable transformation [131, 132]. Although the early transformations utilized protoplasts, regenerable or- gans such as leaves, stems, and roots have been subse- quently used [133, 134]. Much of the research activity utilizing these tools has focused on engineering important agricultural traits for the control of insects, weeds, and plant diseases.

Pathogen-free plants and germplasm storage

Although these two uses of in vitro technology may appear unrelated, a major use of pathogen-free plants is for germplasm storage and the movement of living material across international borders [1]. The ability to rid plants of viruses, bacteria, and fungi by culturing meristem-tips has been widely used since the 1960s. The approach is par- ticularly needed for virus-infected material, because bac- tericidal and fungicidal agents can be used successfully in ridding plants of bacteria and fungi [22]. Meristem-tip culture is often coupled with thermotherapy or chemo- therapy for virus eradication [135].

Traditionally, germplasm has been maintained as seed, but the ability to regenerate whole plants from somatic and gametic cells and shoot apices has led to their use for storage [22, 135]. Three in vitro approaches have been developed, namely use of growth retarding compounds

(e.g., maleic hydrazide, B995, and abscisic acid [ABA]) [136], low-nonfreezing temperatures (1–9°C) [22], and cryopreservation [135]. In this last approach, cell suspen- sions, shoot apices, asexual embryos, and young plantlets, after treatment with a cryoprotectant, is frozen and stored at the temperature of liquid nitrogen (ca. –196°C) [135, 137].

Clonal propagation

The use of tissue culture technology for the vegetative propagation of plants is the most widely used application of the technology. It has been used with all classes of plants [138, 139], although some problems still need to be resolved (e.g., hyperhydricity, abberant plants). There are three ways by which micropropagation can be achieved. These are enhancing axillary bud breaking, production of adventitious buds directly or indirectly via callus, and somatic embryogenesis directly or indirectly on explants [50, 138]. Axillary bud breaking produces the smallest number of plantlets, but they are generally genetically true- to-type; whereas somatic embryogenesis has the potential to produce the greatest number of plantlets, but is induced in the lowest number of plant species. Commercially, numerous ornamentals are produced, mainly via axillary bud breaking [140]. As well, there are many lab-scale protocols for other classes of plants, including field and vegetable crops, fruit, plantation, and forest trees, but cost of production is often a limiting factor in their use commercially [141].

Product formation

Higher plants produce a large number of diverse organic chemicals, which are of pharmaceutical and industrial interest. The first attempt at the large-scale culture of plant cells for the production of pharmaceuticals took place in the 1950s at the Charles Pfizer Co. The failure of this effort limited research in this area in the United States, but work elsewhere in Germany and Japan in particular, led to development, so that by 1978 the industrial application of cell cultures was considered feasible [142]. Furthermore, by 1987, there were 30 cell culture systems that were better producers of secondary metabolites than the respective plants [143]. Unfortunately, many of the economically important plant products are either not formed in suffi- ciently large quantities or not at all by plant cell cultures. Different approaches have been taken to enhance yields of secondary metabolites. These include cell cloning and the repeated selection of high-yielding strains from heteroge- nous cell populations [142, 144] and by using enzyme linked immunosorbent assay (ELISA) and radioimmuno- assay techniques [145]. Another approach involves

selection of mutant cell lines that overproduce the desired product [146]. As well, both abiotic factors—such as ultraviolet (UV) irradiation, exposure to heat or cold and salts of heavy metals and biotic elicitors of plant and microbial origin, have been shown to enhance secondary product formation [147, 148]. Lastly, the use of immobi- lized cell technology has also been examined [149, 150].

Central to the success of producing biologically active substances commercially is the capacity to grow cells on a large scale. This is being achieved using stirred tank reactor systems and a range of air-driven reactors [141]. For many systems, a two-stage (or two-phase) culture process has been tried [151, 152]. In the first stage, rapid cell growth and biomass accumulation are emphasized, whereas the second stage concentrates on product synthesis with minimal cell division or growth. However, by 1987 the naphthoquinone, shikonin was the only commercially produced secondary metabolite by cell cultures [153].

The present

During the 1990s, continued expansion in the application of in vitro technologies to an increasing number of plant species was observed. Tissue culture techniques are being used with all types of plants, including cereals and grasses [154], legumes [155], vegetable crops [156], potato [157], other root and tuber crops [158], oilseeds [159], temperate [160], tropical [161] fruits, plantation crops [162], forest trees [163], and, of course, ornamentals [164]. As can be seen from these articles, the application of in vitro cell technology went well beyond micropropagation, and em- braced all the in vitro approaches that were relevant or possible for the particular species, and the problem(s) being addressed. However, only limited success has been achieved in exploiting somaclonal variation [165], or in the regeneration of useful plantlets from mutant cells [166]; also, the early promise of protoplast technology has remained largely unfulfilled [167]. Substantial progress has been made in extending cryopreservation technology for germplasm storage [168] and in artificial seed technology [169]. Some novel approaches for culturing cells such as on rafts, membranes, and glass rods, as well as manipulation of the culture environment by use of nonionic surfactants have been successfully developed [170].

Cell cultures have remained an important tool in the study of plant biology. Thus progress is being made in cell biology, for example, in studies of the cytoskeleton [171], on chromosomal changes in cultured cells [172], and in cell-cycle studies [173, 174]. Better physiological and biochemical tools have allowed for a re-examination of neoplastic growth in cell cultures during habituation and hyperhydricity, and relate it to possible cancerous growth

in plants [175]. Cell cultures have remained an extremely important tool in the study of primary metabolism; for example, the use of cell suspensions to develop in vitro transcription systems [176], or the regulation of carbohy- drate metabolism in transgenics [177]. The development of medicinal plant cell-culture techniques has led to the identification of more than 80 enzymes of alkaloid bio- synthesis (reviewed in ref. 178). Similar information aris- ing from the use of cell cultures for molecular and biochemical studies on other areas of secondary metabo- lism, is generating research activity on metabolic engi- neering of plant secondary metabolite production [179].

Cell cultures remain an important tool in the study of morphogenesis, even though the present use of develop- mental mutants, particularly of Arabidopsis, is adding valuable information on plant development (see ref. 180). Molecular, physiological, and biochemical studies have allowed for an indepth understanding of cytodifferentia- tion, mainly tracheary element formation [181], organo- genesis [182, 183], and somatic embryogenesis [184–186]. Advances in molecular biology are allowing for the genetic engineering of plants, through the precise insertion of foreign genes from diverse biological systems. Three major breakthroughs have played major roles in the devel- opment of this transformation technology [187]. These are the development of shuttle vectors for harnessing the natural gene transfer capability of Agrobacterium [188], the meth- ods to use these vectors for the direct transformation of regenerable explants obtained from plant organs [189], and the development of selectable markers [190]. For species not amenable to Agrobacterium-mediated transformation, physical, chemical, and mechanical means are used to get the DNA into the cells. With these latter approaches, particularly biolistics [191], it has become possible to

transform virtually any plant species and genotype.

The initial wave of research in plant biotechnology has been driven mainly by the seed and agri-chemical indus- tries, and has concentrated on agronomic traits of direct relevance to these industries, namely the control of insects, weeds, and plant diseases [192]. At present, over 100 species of plants have been genetically engineered, including nearly all the major dicotyledonous crops and an increasing number of monocotyledonous ones, as well as some woody plants. Current research is leading to routine gene transfer systems for all-important crops; for example, the production of golden rice [193]. In addition, technical improvements are further increasing transformation effi- ciency, extending transformation to elite commercial germplasm and lowering transgenic plant production costs. The next wave in agricultural biotechnology is already in progress with biotechnological applications of interest to the food processing, speciality chemical, and pharmaceu- tical industries.

The current emphasis and importance of plant biotech- nology can be gleamed from the last three International Congresses on Plant Tissue and Cell Culture and Bio- technology held in Israel in June 1998, in the United States in June 2002, and in China in August 2006. The theme of the Israeli Congress was Plant Biotechnology and In Vitro Biology in the 21st Century, at the U.S. Congress was Plant Biotechnology 2002 and Beyond, and the theme of the last Congress was Biotechnology and Sustainable Agriculture 2006 and Beyond. The proceedings for the ’98 and ’02 Congresses [194, 195], as well as the ’06 Congress, were developed through a scientific program that focused on the most important developments, both basic and applied, in the areas of plant tissue culture and molecular biology and their impact on plant improvement and biotechnology. They clearly show where tissue culture is today and where it is heading (i.e., as an equal partner with molecular biology), as a tool in basic plant biology and in various areas of application. In fact, progress in applied plant biotechnology is fully matching and is without doubt stimulating fundamental scientific progress, which remains the best hope for achieving sustainable and environmen- tally stable agriculture [196]. Indeed, the advancements made in the last 100 years with in vitro technology have gone well beyond what Haberlandt and the other pioneers could have imagined.

References

  1. Thorpe, T. A. (1990). The current status of plant tissue culture. In S. S. Bhojwani (Ed.), Plant tissue culture: Applications and limitations (pp. 1–33). Amsterdam: Elsevier.
  2. Haberlandt, G. (1902). Kulturversuche mit isolierten Pflan- zenzellen. Sitzungsber. Akad. Wiss. Wien. Math.-Naturwiss. Kl., Abt. J, 111, 69–92.
  3. Krikorian, A. D., & Berquam, D. L. (1969). Plant cell and tissue cultures: the role of Haberlandt. Botanical Review, 35, 59–67.
  4. Kotte, W. (1922). Kulturversuche mit isolierten Wurzelspitzen.

Beitra¨ge Allgemeine Botanik, 2, 413–434.

  1. Robbins, W. J. (1922). Cultivation of excised root tips and stem tips under sterile conditions. Botanical Gazette, 73, 376–390.
  2. White, P. R. (1934). Potentially unlimited growth of excised tomato root tips in a liquid medium. Plant Physiology, 9, 585– 600.
  3. Street, H. E. (1969). Growth in organized and unorganized systems. In F. C. Steward (Ed.), Plant physiology (Vol. 5B, pp. 3–224). New York: Academic Press.
  4. Loo, S. W. (1945). Cultivation of excised stem tips of asparagus in vitro. American Journal of Botany, 32, 13–17.
  5. Ball, E. (1946). Development in sterile culture of stems tips and subjacent regions of Tropaeolum malus L. and of Lupinus albus

L. American Journal of Botany, 33, 301–318.

  1. Monnier, M. (1995). Culture of zygotic embryos. In T. A. Thorpe (Ed.), In Vitro embryogenesis in plants (pp. 117–153). Dordrecht, The Netherlands: Kluwer Academic.
  2. Laibach, F. (1929). Ectogenesis in plants. Methods and genetic possibilities of propagating embryos otherwise dying in the seed. The Journal of Heredity, 20, 201–208.
  3. Tukey, H. B. (1934). Artificial culture methods for isolated embryos of deciduous fruits. Proceedings of the American Society for Horticultural Science, 32, 313–322.
  4. LaRue, C. D. (1936). The growth of plant embryos in culture.

Bulletin of Torrey Botanical Club, 63, 365–382.

  1. Gautheret, R. J. (1934). Culture du tissus cambial. Comptes Rendus Hebdomadaires des Se´ances de l’Acade´mie des Sci- ences, 198, 2195–2196.
  2. Gautheret, R. J. (1935). Recherches sur la culture des tissus ve´ge´taux. Ph.D. Thesis, Paris.
  3. Gautheret, R. J. (1939). Sur la possibilite´ de re´aliser la culture inde´finie des tissus de tubercules de carotte. Comptes Rendus Hebdomadaires des Se´ances de l’Acade´mie des Sciences, 208, 118–120.
  4. Nobe´court, P. (1939). Sur la pe´rennite´ et l’augmentation de volume des cultures de tissues ve´ge´taux. Comptes Rendus des Se´ances de la Socie´te´ de Biologie et de ses Filiales, 130, 1270– 1271.
  5. White, P. R. (1939). Potentially unlimited growth of excised plant callus in an artificial nutrient. American Journal of Botany, 26, 59–64.
  6. Nobe´court, P. (1939). Sur les radicelles naissant des cultures de tissus ve´ge´taux. Comptes Rendus Des Se´ances de la Socie´te´ de Biologie et de ses Filiales, 130, 1271–1272.
  7. White, P. R. (1939). Controlled differentiation in a plant tissue culture. Bulletin of Torrey Botanical Club, 66, 507–513.
  8. White, P. R. (1963). The cultivation of animal and plant cells

(2nd ed.). New York: Ronald Press.

  1. Bhojwani, S. S., & Razdan, M. K. (1983). Plant tissue culture: Theory and practice. developments in crop science, (Vol. 5). Amsterdam: Elsevier.
  2. Gautheret, R. J. (1985). History of plant tissue and cell culture: A personal account. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 2, pp. 1–59). New York: Academic Press.
  3. Thorpe, T. A. (2000). History of plant cell culture. Chap. 1. In R.

H. Smith (Ed.), Plant tissue culture: Techniques and Experi- ments (2nd ed., pp. 1–32). California: Academic Press, (With permission from Elsevier).

  1. Van Overbeek, J., Conklin, M. E., & Blakeslee, A. F. (1941). Factors in coconut milk essential for growth and development of very young Datura embryos. Science, 94, 350–351.
  2. Gautheret, R. J. (1942). He´te´ro-auxines et cultures de tissus ve´ge´taux. Bulletin de la Socie´te´de Chimie Biologique, 24, 13–41.
  3. Gautheret, R. J. (1955). Sur la variabilite´ des proprie´te´s physi- ologiques des cultures de tissues ve´ge´taux. Revista General de Botaˆnica, 62, 5–112.
  4. Nobe´court, P. (1955). Variations de la morphologie et de la structure de cultures de tissues ve´ge´taux. Berichte der Schwei- zerische Botanischen Gesellschaft, 65, 475–480.
  5. Skoog, F., & Tsui, C. (1948). Chemical control of growth and bud formation in tobacco stem segments and callus cultured in vitro. American Journal of Botany, 35, 782–787.
  6. Miller, C., Skoog, F., Von Saltza, M. H., & Strong, F. M. (1955). Kinetin, a cell division factorfrom desoxyribonucleic acid. Journal of the American Chemical Society, 77, 1392.
  7. Skoog, F., & Miller, C. O. (1957). Chemical regulation of growth and organ formation in plant tissue cultures in vitro. Symposia of the Society for Experimental Biology, 11, 118–131.
  8. Evans, D. A., Sharp, W. R., & Flick, C. E. (1981). Growth and behavior of cell cultures: Embryogenesis and organogenesis. In

T. A. Thorpe (Ed.), Plant tissue culture: Methods and applica- tions in agriculture (pp. 45–113). New York: Academic Press.

  1. Letham, D. S. (1974). Regulators of cell division in plant tissues. The cytokinins of coconut milk. Physiologia Plantarum, 32, 66– 70.
  2. Reinert, J. (1958). Utersuchungen die Morphogenese an Gew- ebeku1turen. Berichte der Deutschen Botanischen Gesellschaft, 71, 15.
  3. Reinert, J. (1959). Uber die Kontrolle der Morphogenese und die Induktion von Adventivembryonen an Gewebekulturen aus Karotten. Planta, 53, 318–333.
  4. Steward, F. C., Mapes, M. O., & Mears, K. (1958). Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cells. American Journal of Botany, 45, 705–708.
  5. Muir, W.H., Hildebrandt, A.C., & Riker, A.J. (1954). Plant tissue cultures produced from single isolated plant cells. Sci- ence, 119, 877–878.
  6. Muir, W. H., Hildebrandt, A. C., & Riker, A. J. (1958). The preparation, isolation and growth in culture of single cells from higher plants. American Journal of Botany, 45, 585–597.
  7. Jones, L. E., Hildebrandt, A. C., Riker, A. J., & Wu, J. H. (1960). Growth of somatic tobacco cells in microculture. American Journal of Botany, 47, 468–475.
  8. Bergmann, L. (1959). A new technique for isolating and cloning cells of higher piarits. Nature, 184, 648–649.
  9. Kohlenbach, H. W. (1959). Streckungs-und Teilungswachstum isolierter Mesophyllzellen von Macleaya cordata (Wild.) R. Br. Naturwissenschaften, 46, 116–117.
  10. Kohlenbach, H. W. (1966). Die Entwicklungspotenzen explan- tierter und isolierter Dauerzellen. I. Das Strechungs-und Te- ilungswachstum isolierter Mesophyllzellen von Macleaya cordata. Zeitschrift fu¨r Pflanzenphysiologie, 55, 142–157.
  11. Tulecke, W., & Nickell, L. G. (1959). Production of large amounts of plant tissue by submerged culture. Science, 130, 863–864.
  12. Vasil, V., & Hildebrandt, A. C. (1965). Differentiation of to- bacco plants from single, isolated cells in micro cultures. Sci- ence, 150, 889–892.
  13. Heller, R. (1953). Recherches sur la nutrition minerale des tissus ve´ge´taux cultive´ in vitro. Annales des Sciences Naturelles-Bot- anique et Biologie Vegetale, 14, 1–223.
  14. Nitsch, J. P., & Nitsch, C. (1956). Auxin-dependent growth of excised Helianthus tuberosus tissues. American Journal of Botany, 43, 839–851.
  15. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.
  16. Gamborg, O. L., Murashige, T., Thorpe, T. A., & Vasil, I. K. (1976). Plant tissue culture media. In Vitro, 12, 473–478.
  17. Morel, G. (1960). Producing virus-free cymbidium. American Orchid Society Bulletin, 29, 495–497.
  18. Murashige, T. (1974). Plant propagation through tissue culture.

Annual Review of Plant Physiology, 25, 135–166.

  1. White, P. R. (1934). Multiplication of the viruses of tobacco and Aucuba mosaics in growing excised tomato root tips. Phytopa- thology, 24, 1003–1011.
  2. Limasset, P., & Cornuet, P. (1949). Recherche du virus de la mosa¨ıque du tabac dans les me´riste`mes des plantes infecte´es. Comptes Rendus Hebdomadaires des Se´ances de l’Acade´mie des Sciences, 228, 1971–1972.
  3. Morel, G., & Martin, C. (1952). Gue´rison de dahlias atteints d’une maladie a´ virus. Comptes Rendus Hebdomadaires des Se´ances de l’Acade´mie des Sciences, 235, 1324–1325.
  4. Quak, F. (1961). Heat treatment and substances inhibiting virus multiplication, in meristem culture to obtain virus-free plants. Advances in Horticultural Science and Their Applications, 1, 144–148.
  5. LaRue, C. D. (1942). The rooting of flowers in culture. Bulletin of Torrey Botanical Club, 69, 332–341.
  6. Rangan, T. S. (1982). Ovary, ovule and nucellus culture. In B.

M. Johri (Ed.), Experimental embryology of vascular plants (pp. 105–129). Berlin: Springer-Verlag.

  1. LaRue, C. D. (1949). Culture of the endosperm of maize.

American Journal of Botany, 36, 798.

  1. Johri, B. M., & Bhojwani, S. S. (1965). Growth responses of mature endosperm in cultures. Nature, 208, 1345–1347.
  2. Kanta, K., Rangaswamy, N. S., & Maheshwari, P. (1962). Test- tube fertilization in flowering plants. Nature, 194, 1214–1217.
  3. Zenkteler, M., Misiura, E., & Guzowska, I. (1975). Studies on obtaining hybrid embryos in test tubes. In H. Y. Mohan Ram, J.

J. Shaw, & C. K. Shaw (Eds.), Form1, structure and function in plants (pp. 180–187). Meerut, India: Sarita Prakashan.

  1. Tulecke, W. (1953). A tissue derived from the pollen of Ginkgo biloba. Science, 117, 599–600.
  2. Yamada, T., Shoji, T., & Sinoto, Y. (1963). Formation of calli and free cells in a tissue culture of Tradescantia reflexa. Botanical Magazine, 76, 332–339.
  3. Guha, S., & Maheshwari, S. C. (1964). In vitro production of embryos from anthers of Datura. Nature, 204, 497.
  4. Guha, S., & Maheshwari, S. C. (1966). Cell division and dif- ferentiation of embryos in the pollen grains of Datura in vitro. Nature, 212, 97–98.
  5. Bourgin, J. P., & Nitch, J. P. (1967). Obtention de Nicotiana haploides a` partir de’e´tamines cultive´es in vitro. Annals of Physiologie Ve´ge´tale, 9, 377–382.
  6. Cocking, E. C. (1960). A method for the isolation of plant protoplasts and vacuoles. Nature, 187, 927–929.
  7. Takebe, I., Labib, C., & Melchers, G. (1971). Regeneration of whole plants from isolated mesophyll protoplasts of tobacco. Naturwissenschaften, 58, 318–320.
  8. Carlson, P. S., Smith, H. H., & Dearing, R. D. (1972). Para- sexual interspecific plant hybridization. Proceedings of the Na- tional Academy of Sciences of the United States of America, 69, 2292–2294.
  9. Braun, A. C. (1941). Development of secondary tumor and tu- mor strands in the crown-gall of sunflowers. Phytopathology, 31, 135–149.
  10. Braun, A. C., & White, P. R. (1943). Bacteriological sterility of tissues derived from secondary crown-gall tumors. Phytopa- thology, 33, 85–100.
  11. Braun, A. C. (1950). Thermal inactivation studies on the tumor inducing principle in crown-gall. Phytopathology, 40, 3.
  12. Zaenen, I., van Larebeke, N., Touchy, H., Van Montagu, M., & Schell, J. (1974). Super-coiled circular DNA in crown-gall inducing Agrobacterium strains. Journal of Molecular BioIogy, 86, 109–127.
  13. Ledoux, L. (1965). Uptake of DNA by living cells. Progress in Nucleic Acid Research and Molecular Biology, 4, 231–267.
  14. Vasil, I. K. (Ed.) (1994). Cell culture and somatic cell genetics of plants (Vol. 1). Laboratory procedures and their applications. New York: Academic Press.
  15. Vasil, I. K., & Thorpe, T. A. (Eds.). (1994). Plant cell and tissue culture. Dordrecht, The Netherlands: Kluwer Acad. Publ.
  16. Yeoman, M. M., & Street, H. E. (1977). General cytology of cultured cells. In H. E. Street (Ed.), Plant tissue and cell culture (pp. 137–176). Oxford: Blackwell Scientific.
  17. Lindsey, K., & Yeoman, M. M. (1985). Dynamics of plant cell cultures. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 2, pp. 61–101). New York: Academic Press.
  18. Fowke, L.C. (1986). Ultrastructural cytology of cultured plant tissues, cells, and protoplasts. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 3, pp. 323–342). New York: Academic Press.
  19. Fowke, L. C. (1987). Investigations of cell structure using cul- tured cells and protoplasts. In C. E. Green, D. A. Somers, W. P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell culture (pp. 17–31). New York: A. R. Liss.
  20. D’Amato, F. (1978). Chromosome number variation in cultured cells and regenerated plants. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 287–295). Intl. Assoc. Plant Tis- sue Culture, Univ. of Calgary Printing Services.
  21. Nagl, W., Pohl, J., & Radler, A. (1985). The DNA endoredu- plication cycles. In J. A. Bryant, & D. Francis (Eds.), The cell division cycle in plants (pp. 217–232). Cambridge: Cambridge University Press.
  22. Yamada, Y., Fumihiko, S., & Hagimori, M. (1978). Photoau- totropism in green cultured cells. In T. A., Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 453–462) Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  23. Hu¨semann, W. (1985). Photoautotrophic growth of cells in culture. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants, (Vol. 2, pp. 213–252). New York: Academic Press.
  24. Neumann, K.-H., Barz, W., & Reinhard E. (Eds.). (1985). Pri- mary and secondary metabolism of plant cell cultures. Berlin: Springer-Verlag.
  25. Leonard, R. T., & Rayder, L. (1985). The use of protoplasts for studies on membrane transport in plants. In L. C. Fowke, & F. Constabel (Eds.), Plant protoplasts (pp. 105–118). Boca Raton, Florida: CRC Press.
  26. Filner, P. (1978). Regulation of inorganic nitrogen and sulfur assimilation in cell suspension cultures. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 437–442). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  27. Fowler, M. W. (1978). Regulation of carbohydrate metabolism in cell suspension cultures. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 443–452). Intl. Assoc. Plant Tis- sue Culture, Univ. of Calgary Printing Services.
  28. Bender, L., Kumar, A., & Neumann, K.-H. (1985). On the photosynthetic system and assimilate metabolism of Daucus and Arachis cell cultures. In K.-H. Neumann, W. Barz, & E. Rein- hard (Eds.), Primary and secondary metabolism of plant cell cultures (pp. 24–42). Berlin: Springer-Verlag.
  29. Herzbeck, H., & Husemann, W. (1985). Photosynthetic carbon metabolism in photoautotrophic cell suspension cultures of Chenopodium rubrum L. In K. -H. Neumann, W. Barz, & E. Reinhard (Eds.), Primary and secondary metabolism of plant cell culture (pp. 15–23). Berlin: Springer-Verlag.
  30. Constabel, F., & Vasil, I. K. (Eds.), (1987). Cell culture and somatic cell genetics of plants (Vol. 4). New York: Academic Press.
  31. Constabel, F., & Vasil, I. K. (Eds.), (1988). Cell Culture and somatic cell genetics of plants (Vol. 5). New York: Academic Press.
  32. Roberts, L. W. (1976). Cytodifferentiation in plants: Xylogen- esis as a model system. Cambridge: Cambridge University Press.
  33. Phillips, R. (1980). Cytodifferentiation. International Review of Cytology. Supplement, 11A, 55–70.
  34. Fukuda, H., & Komamine, A. (1985). Cytodifferentiation. In I.

K. Vasil (Ed.), Cell culture and somatic cell genetics of plants

(Vol. 2, pp. 149–212). New York: Academic Press.

  1. Schell, J., van Montague, M., Holsters, M., et al. (1982). Plant cells transformed by modified Ti plasmids: A model system to study plant development. In L. Jaenicke (Ed.), Biochemistry of Differentiation and Morphogenesis (pp. 65–73). Berlin: Springer-Verlag.
  2. Schell, J. S. (1987). Transgenic plants as tools to study the molecular organization of plant genes. Science, 237, 1176–1183.
  3. Thorpe, T. A. (1980). Organogenesis in vitro: Structural, phys- iological, and biochemical aspects. International Review of Cytology. Supplement, 11A, 71–111.
  4. Tran Thanh Van, K., & Trinh, H. (1978). Morphogenesis in thin cell layers: Concept, methodology and results. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 37–48). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  5. Van Tran Thanh, K. (1980). Control of morphogenesis by inherent and exogenously applied factors in thin cell layers. International Review of Cytology. Supplement, 11A, 175–194.
  6. Murashige, T. (1979). Principles of rapid propagation. In K. W. Hughes, R. Henke, & M. Constantin (Eds.), Propagation of higher plants through tissue culture: A bridge between research and application (pp. 14–24). Tech. Information Center, U.S. Dept. of Energy.
  7. Brown, D. C. W., & Thorpe, T. A. (1986). Plant regeneration by organogenesis. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 3, pp. 49–65). New York: Academic Press.
  8. Thompson, M. R., & Thorpe, T. A. (1990). Biochemical per- spectives in tissue culture for crop improvement. In K. R. Khanna (Ed.), Biochemical aspects of crop improvement (pp. 327–358). Boca Raton, Florida: CRC Press.
  9. Ammirato, P. V. (1983). Embryogenesis. In D. A. Evans, W. R. Sharp, P. V. Ammirato, & Y. Yamada (Eds.), Handbook of plant cell culture (Vol. 1, pp. 82–123). New York: MacMillan.
  10. Thorpe, T. A. (1988). In vitro somatic embryogenesis. ISI Atlas of Science: Animal and Plant Sciences, pp. 81–88.
  11. Nomura, K., & Komamine, A. (1985). Identification and isola- tion of single cells that produce somatic embryos at a high frequency in a carrot suspension culture. Plant Physiology, 79, 988–991.
  12. Butcher, D. N. (1977). Plant tumor cells. In H. E. Street (Ed.), Plant tissue and cell culture (pp. 429–461). Oxford: Blackwell Scientific.
  13. Rottier, P. J. M. (1978). The biochemistry of virus multiplication in leaf cell protoplasts. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 255–264). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  14. Earle, E. D. (1978). Phytotoxin studies with plant cells and protoplasts. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 363–372). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  15. Miller, S. A., & Maxwell, D. P. (1983). Evaluation of disease resistance. In D. A. Evans, W. R. Sharp, P. V. Ammirata, & Y. Yamada (Eds.), Handbook of plant cell culture (Vol. 1, pp. 853– 879). New York: Macmillan.
  16. Yeung, E. C., Thorpe, T. A., & Jensen, C .J. (1981). In vitro fertilization and embryo culture. In T. A. Thorpe (Ed.), Plant tissue culture: Methods and applications in agriculture (pp. 253–271). New York: Academic Press.
  17. Zenkteler, M. (1984). In vitro pollination and fertilization. In I.

K. Vasil (Ed.), Cell culture and somatic cell genetics of plants

(Vol. 1, pp. 269–275). New York: Academic Press.

  1. Raghavan, V. (1980). Embryo culture. International Review of Cytology. Supplement, 11B, 209–240.
  2. Collins, G. B., & Grosser, J. W. (1984). Culture of embryos. In I.

K. Vasil (Ed.), Cell culture and somatic cell genetics of plants

(Vol. 1, pp. 241–257). New York: Academic Press.

  1. Hu, H., & Zeng, J. Z. (1984). Development of new varieties of anther culture. In P. V. Ammirato, D. A. Evans, W. R. Sharp, &

Y. Yamada (Eds.), Handbook of plant cell culture (Vol. 3, pp. 65–90). New York: Macmillan.

  1. San, L. H., & Gelebart, P. (1986). Production of gynogenetic haploids. In I. K. Vasil (Ed.), Cell culture and somatic cell

genetics of plants (Vol. 3, pp. 305–322). New York: Academic Press.

  1. Flick, C. E. (1983). Isolation of mutants from cell culture. In P.

V. Ammirato, D. A. Evans, W. R. Sharp, & Y. Yamada (Eds.), Handbook of plant cell culture (Vol. I, pp. 393–441). New York: Macmillan.

  1. Larkin, P. J., & Scowcroft, W. R. (1981). Somaclonal variation -a novel source of variability from cell culture for plant improvement. Theoretical and Applied Genetics, 60, 197–214.
  2. Larkin, P. J., Brettell, R. I. S., Ryan, S. A., Davies, P. A., Pal- lotta, M. A., & Scowcroft, W. R. (1985). Somaclonal variation: impact on plant biology and breeding strategies. In P. Day, M. Zaitlin, & A. Hollaender (Eds.), Biotechnology in plant science (pp. 83–100). New York: Academic Press.
  3. Scowcroft, W. R., Brettell, R. I. S., Ryan, S. A., Davies, P. A., & Pallotta, M. A. (1987). Somaclonal variation and genomic flux. In C. E. Green, D. A. Somers, W. P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell culture (pp. 275–286). New York:

A. R. Liss.

  1. Jacobs, M., Negrutiu, I., Dirks, R., & Cammaerts, D. (1987). Selection programmes for isolation and analysis of mutants in plant cell cultures. In C. E. Green, D. A. Somers, W. P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell culture (pp. 243– 264). New York: A. R. Liss.
  2. Hughes, K. (1983). Selection for herbicide resistance. In P. V. Ammirato, D. A. Evans, W. R. Sharp, & Y. Yamada (Eds.), Handbook of plant cell culture (Vol. 1, pp. 442–460). New York: Macmillan.
  3. Ranch, J. P., Rick, S., Brotherton, J. E., & Widholm, J. (1983). Expression of 5 methyltryptophan resistance in plants regener- ated from resistant cell lines of Datura innoxia. Plant Physiol- ogy, 71, 136–140.
  4. Binding, H. (1986). Regeneration from protoplasts. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 3, pp. 259–274). New York: Academic Press.
  5. Evans, D. A., Sharp, W. R., & Bravo, J. E. (1984). Cell culture methods for crop improvement. In W. R. Sharp, D. A. Evans, P.

V. Ammirato, & Y. Yamada (Eds.), Handbook of plant cell culture (Vol. 2, pp. 47–68). New York: Macmillan.

  1. Schieder, O., & Kohn, H. (1986). Protoplast fusion and gener- ation of somatic hybrids. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 3, pp. 569–588). New York: Academic Press.
  2. Chetrit, P., Mathieu, C., Vedel, F., Pelletier, G., & Primard, C. (1985). Mitochondrial DNA polymorphism induced by proto- plast fusion in Cruciferae. Theoretical and Applied Genetics, 69, 361–366.
  3. Potrykus, I., Shillito, R. D., Saul, M., & Paszkowski, J. (1985). Direct gene transfer: State of the art and future potential. Plant Molecular Biology Reporter, 3, 117–128.
  4. Deshayes, A., Herrera-Estrella, L., & Caboche, M. (1985). Liposome-mediated transformation of tobacco mesophyll pro- toplasts by an Escherichia coli plasmid. The EMBO Journal, 4, 2731–2739.
  5. Crossway, A., Oakes, J. V., Irvine, J. M., Ward, B., Knauf, V. C., & Shewmaker, C. K. (1986). Integration of foreign DNA following microinjection of tobaccomesophyll protoplasts. Molecular & General Genetics, 202, 179–185.
  6. Klein, T. M., Wolf, B. D., Wu, R., & Sanford, J. C. (1987).

High-velocity microprojectiles for delivering nucleic acids into living cells. Nature, 327, 70–73.

  1. DeBlock, M., Herrera-Estrella, L., van Montague, M., Schell, J., & Zambryski, P. (1984). Expression of foreign genes in regen- erated plants and in their progeny. The EMBO Journal, 3, 1681– 1689.
  2. Borsch, R. B., Fraley, R. T., Rogers, S. G., Sanders, F. R., Lloyd, A., & Boffmann, N. (1984). Inheritance of functional foreign genes in plants. Science, 223, 496–498.
  3. Gasser, C. S., & Fraley, R. T. (1989). Genetically engineering plants for crop improvement. Science, 244, 1293–1299.
  4. Uchimiya, H., Handa, T., & Brar, D. S. (1989). Transgenic plants. Journal of Biotechnology, 12, 1–20.
  5. Kartha, K.K. (1981). Meristem culture and cryopreservation methods and applications. In T. A. Thorpe (Ed.), Plant tissue culture: Methods and applications in agriculture (pp. 181–211). New York: Academic Press.
  6. Dodds, J. (1989). Tissue culture for germplasm management and distribution, in Strengthening Collaboration. In J. I. Cohen (Ed.), Biotechnology: International agricultural research and the private sector (pp. 109–128). Washington, D.C.: Bureau of Science and Technology, AID.
  7. Withers, L. A. (1985). Cryopreservation of cultured cells and meristems. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 2, pp. 253–316). New York: Academic Press.
  8. Murashige, T. (1978). The impact of plant tissue culture on agriculture. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 15–26). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  9. Conger B. V. (Ed.) (1981). Cloning agricultural plants via in vitro techniques. Boca Raton, Florida: CRC Press.
  10. Murashige, T. (1990). Plant propagation by tissue culture: practice with unrealized potential. In P. V. Ammirato, D. A. Evans, W. R. Sharp, & Y. P. S. Bajaj (Eds.), Handbook of plant cell culture (Vol. 5, pp. 3–9). New York: McGraw-Hill.
  11. Zimmerman, R. H. (1986). Regeneration in woody ornamentals and fruit trees. In I. K. Vasil (Ed.), Cell culture and somatic cell genetics of plants (Vol. 3, pp. 243–258). New York: Academic Press.
  12. Zenk, M. H. (1978). The impact of plant cell culture on industry. In T. A. Thorpe (Ed.), Frontiers of plant tissue culture 1978 (pp. 1–13). Intl. Assoc. Plant Tissue Culture, Univ. of Calgary Printing Services.
  13. Wink, M. (1987). Physiology of the accumulation of secondary metabolites with special reference to alkaloids. In F. Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 17–42). New York: Academic Press.
  14. Dougall, D. K. (1987). Primary metabolism and its regulation. In

C. E. Green, D. A. Somers, W. P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell culture (pp. 97–117). New York: A.

R. Liss.

  1. Kemp, H. A., & Morgan, M. R. A. (1987). Use of immunoassays in the detection of plant cell products. In F. Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 287–302). New York: Academic Press.
  2. Widholm, J. M. (1987). Selection of mutants which accumulate desirable secondary products. In F. Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 125–137). New York: Academic Press.
  3. Eilert, U. (1987). Elicitation: Methodology and aspects of application. In F. Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 153–196). New York: Academic Press.
  4. Kurz, W.G.W. (1988). Semicontinuous metabolite production through repeated elicitation of plant cell cultures: A novel pro- cess. In T. J. Mabry (Ed.), Plant biotechnology (pp. 93–103). Austin: IC2 Institute.
  5. Brodelius, P. (1985). The potential role of immobilisation in plant cell biotechnology. Trends in Biotechnology, 3, 280–285.
  6. Yeoman, M. M. (1987). Techniques, characteristics, properties, and commercial potential of immobilized plant cells. In F.

Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 197–215). New York: Academic Press.

  1. Fowler, M. W. (1987). Process systems and approaches for large-scale plant cell culture. In C. E. Green, D. A. Somers, W.

P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell cul- ture (pp. 459–471). New York: A. R. Liss.

  1. Beiderbeck, R., & Knoop, B. (1987). Two-phase culture. In F. Constabel, & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 4, pp. 255–266). New York: Academic Press.
  2. Fujita, Y., & Tabata, M. (1987). Secondary metabolites from plant cells—phar-maceutical applications and progress in com- mercial production. In C. E. Green, D. A. Somers, W. P. Hackett, & D. D. Biesboer (Eds.), Plant tissue and cell culture (pp. 169–185). New York: A. R. Liss.
  3. Vasil, I. K., & Vasil, V. (1994). In vitro culture of cereals, grasses. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 293–312). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  4. Davey, M. R., Kumar, V., & Hammatt, N. (1994). In vitro culture of legumes. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 313–329). Dordrecht, The Nether- lands: Kluwer Acad. Publ.
  5. Reynolds, J. F. (1994). In vitro culture of vegetable crops. In I.

K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture

(pp. 331–362). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Jones, M. G. K. (1994). In vitro culture of potato In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 363– 378). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  2. Krikorian, A. D. (1994). In vitro culture of root, tuber crops. In I.

K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture

(pp. 379–411). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Palmer, C. E., & Keller, W. A. (1994). In vitro culture of oil- seeds. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 413–455). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  2. Zimmerman, R. H., & Swartz, H. J. (1994). In vitro culture of temperate fruits. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 457–474). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  3. Grosser, I. W. (1994). In vitro culture of tropical fruits. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 475–496). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  4. Krikorian, A. D. (1994). In vitro culture of plantation crops. In I.

K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture

(pp. 497–537). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Harry, I. S., & Thorpe, T. A. (1994). In vitro culture of forest trees. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 539–560). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  2. Debergh, P. (1994). In vitro culture of ornamentals. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 561–573). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  3. Karp, A. (1994). Origins, causes and uses of variation in plant tissue cultures. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 139–151). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  4. Dix, P. J. (1994). Isolation and characterisation of mutant cell lines. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 119–138). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  5. Feher, A., & Dudits, D. (1994). Plant protoplasts for cell fusion and direct DNA uptake: culture and regeneration systems. In I.

K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture

(pp. 71–118). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Kartha, K. K., & Engelmann, F. (1994). Cryopreservation and geffi1plasm storage. In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 195–230). Dordrecht. The Nether- lands: Kluwer Acad. Publ.
  2. Redenbaugh K. (Ed.) (1993). Synseeds: Applications of synthetic seeds to crop improvement. Boca Raton, FL: CRC Press.
  3. Lowe, K. C., Davey, M. R., & Power, J. B. (1996). Plant tissue culture: past, present and future. Plant Tiss. Cult. Biotechnol, 2, 175–186.
  4. Kong, L., Attree, S. M., Evans, D. E., Binarova, P., Yeung, E. C., & Fowke, L. C. (1998). Somatic embryogenesis in white spruce: studies of embryo development, cell biology. In S. M. Jain, & P. K. Gupta (Eds.), Somatic embryogenesis in woody plants (Vol. 4, pp. 1–28). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  5. Kaeppler, S. M., & Phillips, R. L. (1993). DNA methylation and tissue culture-induced variation in plants. In Vitro Cellular & Developmental Biology, 29P, 125–130.
  6. Komamine, A., Ito, M., & Kawahara, R. (1993). Cell culture systems as useful tools for investigation of developmental biology in higher plants: analysis of mechanisms of the cell cycle and differentiation using plant cell cultures. In W. Y. Soh,

J. R., Liu, & A., Komamine (Eds.), Advances in developmental biology and biotechnology of higher plants (pp. 289–310). Proceedings First Asia Pacific Conference on Plant Cell and Tissue Culture, held in Taedok Science Town, Taejon, Korea, 59 Sept. 1993,. The Korean Society of Plant Tissue Culture.

  1. Trehin, C., Planchais, S., Glab, N., Perennes, C., Tregear, J., & Bergounioux, C. (1998). Cell cycle regulation by plant growth regulators: involvement of auxinand cytokinin in the re-entry of Petunia protoplasts into the cell cycle. Planta, 206, 215– 224.
  2. Gaspar, T. (1995). The concept of cancer in in vitro plant cul- tures and the implication of habituation to hormones and hy- perhydricity. Plant Tissue Culture & Biotechnology, 1, 126–136.
  3. Suguira, M. (1997). In vitro transcription systems from sus- pension-cultured cells. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 383–398.
  4. Stitt, M., & Sonnewald, U. (1995). Regulation of carbohydrate metabolism in transgenics. Annual Review of Plant Physiology and Plant Molecular Biology, 46, 341–368.
  5. Kutchin, T. M. (1998). Molecular genetics of plant alkaloid biosynthesis. In G. Cordell (Ed.), The alkaloids (Vol. 50, pp. 257–316). San Diego: Academic Press.
  6. Verpoorte, R., van der Heijden, R., ten Hoopen, H. J. G., & Memclink, J. (1998). Metabolic engineering for the improve- ment of plant secondary metabolite production. Plant Tissue Culture & Biotechnology, 4, 3–20.
  7. The plant cell, Special Issue, July 1997.
  8. Fukuda, H. (1997). Xylogenesis: initiation, progression, and cell death. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 299–325.
  9. Thorpe, T.A. (1993). Physiology and biochemistry of shoot bud formation in vitro. In W. Y. Soh, J. R. Liu, & A. Komamine (Eds.), Advances in developmental biology and biotechnology of higher plants (pp. 210–224). Proceedings First Asia Pacific Confer-ence on Plant Cells and Tissue Culture, held in Taedok Science Town, Taejon, Korea, 5–9 Sept. 1993, The Korean Society of Plant Tissue Culture.
  10. Joy, IV R. W., & Thorpe, T. A. (1999). Shoot morphogenesis: Structure, physiology, biochemistry and molecular biology. In

W. Y. Soh, & S. S. Bhojwani (Eds.), Morphogenesis in plant tissue cultures (pp. 171–214). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Nomura, K., & Komamine, A. (1995). Physiological and bio- chemical aspects of somatic embryogenesis. In T. A. Thorpe

(Ed.), In vitro embryogenesis in plants (pp. 249–265). Dordr- echt, The Netherlands: Kluwer Acad. Publ.

  1. Dudits, D., Gyo¨rgyey, J., Bo¨gre, L., & Bako´, L. (1995).

Molecular biology of somatic embryogenesis. In T. A. Thorpe (Ed.), In vitro embryogenesis in plants (pp. 267–308). Dordr- echt, The Netherlands: Kluwer Acad. Publ.

  1. Thorpe, T. A., & Stasolla, C. (2001). Somatic embryogenesis. In

S. S. Bhojwani, & W. Y. Soh (Eds.), Current trends in the embryology of angiosperms (pp. 279–236). Dordrecht, The Netherlands: Kluwer Acad. Publ.

  1. Hinchee, M. A. W., Corbin, D. R., Armstrong, C. L., et al. (1994). Plant transformation, In I. K. Vasil, & T. A. Thorpe (Eds.), Plant cell and tissue culture (pp. 231–270). Dordrecht, The Netherlands: Kluwer Acad. Publ.
  2. Fraley, R. T., Rogers, S. G., Borsch, R. B., et al. (1985). The SEV system: a new disarmed Ti plasmid vector system for plant transformation. Bio/Technology, 3, 629–635.
  3. Horsch, R. B., Fry, J., Hoffman, N., et al. (1985). A simple and general method for transferring genes into plants. Science, 227, 1229–1231.
  4. Cloutier, S., & Landry, B. S. (1994). Molecular markers applied to plant tissue culture. In vitro Cellular & Developmental Biology, 31P, 32–39.
  5. Sanford, J. C. (2000). The development of the biolistic process.

In vitro Cellular & Developmental Biology. Plant, 36, 303–308.

  1. Fraley, R. (1992). Sustaining the food supply. Bio/Technology, 10, 40–43.
  2. Potrykus, I. (2001). The Golden Rice tale. In vitro Cellular & Developmental Biology. Plant, 37, 93–100.
  3. Altman, A., Ziv, M., & Izhar, S. (Eds.) (1999). Plant biotech- nology and in vitro biology in the 21st century. Proceedings of the IXth International Congress of the International Association for Plant Tissue Culture and Biotechnology, Jerusalem, Israel, 14–19 June, 1998. Dordrecht, The Netherlands: Kluwer Acad. Publ.
  4. Vasil, I. K. (Ed.) (2003). Plant biotechnology 2002 and beyond. Proceedings of the 10th IAPTC&B Congress, June 23–28, 2002, Orlando, FL, USA.Dordrecht, The Netherlands: Kluwer Acad. Publ.
  5. Schell J. (1995). Progress in plant sciences is our best hope to achieve an economically rewarding, sustainable and environ- mentally stable agriculture. Plant Tissue Culture & Biotech- nology, 1, 10–12.
Exit mobile version