Habituation of Tobacco Pith Cells for Factors Promoting Cell Division Is Heritable and Potentially Reversible

Binns, Andrew N.; Meins, Frederick

doi:10.1073/pnas.70.9.2660

Cited by 82 publications

(20 citation statements)

References 28 publications

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“…These striking phenotypic changes, like the crown gall transformation, do not persist through sexual reproduction and are occasionally reversed during vegetative propagation (14). Habituation (15,16) …”

Section: Discussionmentioning

confidence: 99%

Studies on the recovery of crown gall tumor cells

Turgeon¹,

Wood²,

Braun³

1976

Proc. Natl. Acad. Sci. U.S.A.

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Our previous studies have shown that, while a persistent but potentially reversible suppression of the tumorous state appears to be a characteristic feature of the vegetative phase of teratoma shoot growth in the crown gafl disease of plants, a recovery from that state occurs during the reproductive phase. An analysis has now been made of the reproductive process in an attempt to define the precise stage at which recovery occurs. The results of this analysis have shown that diploid somatic cells of teratoma-derived flower parts such as those found in petals and filaments are inherently neoplastic. On the other hand, haploid cells of plants grown from anthers of the same flowers and diploid cells of F1 generation plants grown from teratoma-derived seed have, by generally accepted criteria, recovered from the tumorous state. These findings have been interpreted to mean that the loss of neoplastic properties occurs in crown gall teratoma cells during meiosis rather than during fertilization or later stages of the reproductive process.An analysis of more than 2000 teratoma-derived tumor shoots has shown, moreover, that a recovery from the tumorous state may also occur, although apparently as a very rare event, during the vegetative phase of teratoma shoot growth.Cloned lines of crown gall teratoma tissues of tobacco (Nicotiana tabacum L.) are characterized by a~capacity to organize tumor shoots when grown on a basic culture medium. When such teratoma-derived shoots are isolated and grafted at cambial level into appropriate morphologically distinct stock plants a broad spectrum of responses may be obtained (1). These responses range at the one extreme to a breakdown of the implanted shoot with a resulting development of typical disorganized teratomatous growths, while at the other extreme in this spectrum of examples are found shoots that develop quite normally, some of which ultimately flower and set viable seed. The leaves that develop from such teratoma shoots are composed of all of the specialized cell types found in normal leaves and they appear by all generally accepted criteria to be normal. It has been found, however, that when tissues are isolated from the teratoma-derived leaves and planted on a basic culture medium they again assume their neoplastic properties. formed by the T37 strain of the crown gall bacterium Agrobacterium tumefaciens. Procedures used in these studies for grafting teratoma shoots and for culturing cells have previously been described elsewhere (1). Briefly, shoots produced by teratoma tissue grown in liquid culture were grafted at cambial level to detopped stems of healthy tobacco plants of the morphologically distinguishable Turkish cultivar. Pieces of leaf, flower, and pith tissue derived from grafted teratoma and normal shoots were cultured on the agar-containing basic medium of Linsmaier and Skoog (2). The growth hormones naphthalene acetic acid (NAA) (0.5 mg/liter) and kinetin (6-furfurylaminopurine) (0.5 mg/liter) were added to the medium in certain cases as described in ...

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Section: Discussionmentioning

confidence: 99%

Studies on the recovery of crown gall tumor cells

Turgeon¹,

Wood²,

Braun³

1976

Proc. Natl. Acad. Sci. U.S.A.

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“…DCG A + B, tested up to 100 Mm, did not stimulate growth to the levels achieved at the optimal ZR concentration. Primary pith explants of H425 tobacco, also known to require cytokinin for continuous growth and cell division (4) (Fig. 4A) and stimulation of mitotic activity in the leaf callus (Fig.…”

Section: Growth and Cell Divisionmentioning

confidence: 99%

Activity and Accumulation of Cell Division-Promoting Phenolics in Tobacco Tissue Cultures

Teutonico¹,

Dudley²,

Orr³

et al. 1991

Plant Physiol.

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Dehydrodiconiferyl alcohol glucosides (DCGs) Candidates for such a non-adenyl metabolite are the cell division-promoting substances found in fractions isolated from hormone-autonomous Catharanthus roseus crown gall tumors by . These tumors, now also known to synthesize zeatin and ZR (18), were recently reinvestigated ( 16). The fractions isolated by Wood et al.(29) were shown to contain DCG4 isomers capable of replacing cytokinin in the promotion of tobacco pith growth in culture. The individual DCG isomers differed in their ability to stimulate proliferation with isomers A and B (differing only in the enantiomeric nature of the phenylpropanoid dimer) being the most active (5). The relatively inactive isomers D and E differed from A and B only with respect to the location of the glucose moiety, at the C-13 hydroxyl and C'-4 hydroxyl, respectively (5). Moreover, the active DCGs were found in quiescent tobacco pith tissue at low levels (approximately 0.05 yM) but at 20-to 50-fold higher levels in actively growing cultured pith tissue (5). Such results indicated that these naturally occurring, phenolic derivatives could stimulate cell division. To demonstrate that the purified DCGs were, in fact, responsible for the biological activity observed, DCG isomers A and B (hereafter referred to as DCG A + B) have been synthesized chemically and their activities reexamined. The results presented here indicate that synthetic DCG A + B possess cell division-promoting activity but do not share several other biological activities with the adenine-derived cytokinins. In addition, we show that the accumulation of DCG A and DCG B in cultured tobacco pith explants is 4Abbreviations: DCG, dehydrodiconiferyl alcohol glucoside;

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“…R was calculated from the expression ln(W/W0)-kinetin/ ln(W/W0)+kinetin, where W0 and W are the fresh weights of the inoculum and the tissue after 3 weeks, respectively. Tissues giving an average R value greater than 0.4 were judged to be C + (Binns and Meins, 1973). Sampling error in distributions of progeny was estimated by the binomial proportions test (Simpson et al, 1960).…”

Section: Measuring Cytokinin Requirementmentioning

confidence: 99%

“…Methods for isolating tissues, culturing tissues, cloning cells and regenerating plants have been described in detail elsewhere (Binns and Meins, 1973;Meins et al, 1980). In brief, C + tissues were grown on a basal medium containing agar, salts, sucrose, myo-inositol and thiamine at the concentrations recommended by Linsmaier and Skoog (Linsmaier and Skoog, 1965) supplemented with 2.0 mg/l of the auxin α-naphthaleneacetic acid, and 5 mg/l of the pH indicator chlorophenol red.…”

Section: Culture Of Tissues Cell Cloning and Plant Regenerationmentioning

confidence: 99%

Meiotic transmission of epigenetic changes in the cell-division factor requirement of plant cells

Meins

Thomas

2003

Development

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During the development of tobacco plants, cells undergo epigenetic changes that alter their requirement in culture for the cell-division factor cytokinin. Cultured leaf cells alternate between cytokinin-requiring(C–) and cytokinin-independent (C+) states at extremely high rates of approximately 10–2 per cell generation by a process called pseudodirected variation. Here we show that plants regenerated from most C+ clones express the Habituated leaf (Hl) trait, i.e., leaf tissues exhibit the C+ phenotype rather than the wild-type C– phenotype in culture. This new trait then segregates as a monogenic dominant trait indicating that conversion of C– cells to C+ cells is associated with a meiotically transmissible, genetic modification. Two independent mutants, Hl-2 and Hl-3, derived from C+ variants arising in culture were unstable in planta and reverted gametically at rates roughly comparable to pseudodirected variation in culture. Cells of the Hl-2mutant, but not of a stable Hl-1 mutant, reverted phenotypically at high rates in culture. This revertant C– phenotype persisted in some plants regenerated from cloned revertant lines, and then showed irregular segregation in two successive sexual generations. These results show for the first time that meiotically transmissible epimutations can occur reversibly and at high rates in culture.

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Habituation of Tobacco Pith Cells for Factors Promoting Cell Division Is Heritable and Potentially Reversible

Cited by 82 publications

References 28 publications

Studies on the recovery of crown gall tumor cells

Studies on the recovery of crown gall tumor cells

Activity and Accumulation of Cell Division-Promoting Phenolics in Tobacco Tissue Cultures

Meiotic transmission of epigenetic changes in the cell-division factor requirement of plant cells

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