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0 Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045 USA
Received for publication February 22, 2000. Accepted for publication May 25, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSLITERATURE CITED |
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Key Words: abscisic acid • bud formation • cytokinin • Funaria hygrometrica • moss • plant developmental biology
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSLITERATURE CITED |
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; Bopp, 1990
; Bhatla, 994
). Indeed, the ability to count buds on protonemata has allowed bud formation to be a quantitative bioassay for cytokinin activity. Exposure to most cytokinins results in log-linear dose-dependent increases in bud number. Stimulation of bud formation can usually be detected at concentrations of 
10-8 mol/L, and maximal numbers of buds result from exposures to optimal concentrations, usually 10-6 mol/L (Brandes and Kende, 1968
; Hahn and Bopp, 1968
; Valadon and Mummery, 1971
).
The temporal order of certain biochemical and cytological events during the process of bud formation under standard laboratory conditions has been well documented. Cells respond within minutes to exogenous cytokinin by changes in Ca2+ current and intracellular [Ca2+] (Saunders, 1986
). While the very first stages in the initiation of a side branch or a bud are thought to be identical by some workers, others present evidence that buds initiate slightly closer to the end wall of the mother cell and that the first cell division inserts a wall that connects the side and end wall of the mother cell (Saunders, 1986
). There is universal agreement that growth of the single-celled bud initial proceeds via homogenous growth of the cell wall, a marked contrast to the tip growth seen in filamentous side branches. Although morphological development is not synchronous, additional divisions in bud initials result in the first 5–6 celled buds containing a distinct, tetrahedral, apical cell some 72 h after addition of cytokinin.
While cytokinin exposure triggers bud formation, cytokinin exposure is not a necessary and sufficient condition for the induction of shoot buds in Funaria. Not all filamentous cells are competent to respond to cytokinin. In Funaria, the first-formed protonemal filaments contain chloroplast-rich cells with transverse septa; these filaments do not make buds in response to cytokinin exposure. Under the influence of auxin, however, these filaments begin to grow as caulonema and contain cells with distinct morphological and cytological characteristics: spindle-shaped chloroplasts, oblique septa, and, with time, reddish-brown wall pigments. Such caulonemal filaments will form buds upon exposure to cytokinin, although the molecular nature of this competence to respond to hormone is not known.
Even for caulonemal filaments, other external factors must also be present if buds are to form. Experiments show that bud formation also requires light as well as the presence of sufficient levels of external calcium (Simon and Naef, 1981
; Saunders and Hepler, 1983
). The requirement for light is mediated by phytochrome; experiments transferring cytokinin-stimulated caulonema to the dark after various periods of time in the light find reduced numbers of buds when the light exposure is <2 d (Simon and Naef, 1981
).
Just as the exposure to light must have a sufficient duration, the effect of cytokinin on bud initiation is also more than a simple trigger for bud formation. Two kinds of experiments demonstrate that cytokinin must be present throughout the first few days of bud formation. Initiating the calcium cascade with the calcium ionophore A23187 will not result in full development of buds unless cytokinin is also supplied (Saunders and Hepler, 1982
). Similarly, washing cytokinin from the stimulated protonema during the first 72 h of bud formation leads to reversion of buds (Brandes and Kende, 1968
). Biochemical and developmental work is showing that these two effects of cytokinin are quite distinct. Experiments with antagonists and agonists of voltage-regulated calcium channels and biochemical characterization of such channels in moss link initial perception to a membrane-localized DHPR-sensitive Ca2+ channel regulating internal G-proteins (Conrad and Hepler, 1988
; Schumaker and Gizinski, 1993
). Other experiments show that the effect of cytokinin concentration on bud number can be localized to the second involvement of cytokinin in bud formation, but not to initial perception, and that the synthetic cytokinin diphenylurea can initiate bud formation, but will not permit nascent buds to complete their development (Christianson, 1998b
; Christianson and Hornbuckle, 1999
).
While the characterization of these positive effectors of bud formation has resulted in a much more detailed picture of the process of bud formation, the incredibly detailed understanding of development in other organisms (e.g., Aspergillis, Arabidopsis, Drosophila) has resulted from the analysis of mutants that are blocked in normal development. Temperature-sensitive mutations have been particularly useful in dissecting the temporal aspects of gene action in development. As described in Suzuki's (1970)
still excellent review, a timed series of reciprocal shifts from permissive to nonpermissive conditions localizes the time period during which the gene product must be active if development is to proceed normally. Such experiments have their conceptual basis in the observations made in the first half of the 20th century. Exposure to ether vapor produced specific developmental defects in Drosophila but only if staged embryos were exposed at a particular time during development (Gloor, 1947
), the so-called phenocritical time (Goldschmidt, 1938
).
The hormone abscisic acid (ABA) was shown to inhibit the cytokinin-stimulated formation of buds in the moss Funaria hygrometrica (Valadon and Mummery, 1971
). While that report showed that the inhibition was dose dependent and was sufficiently quantitative to be used as a bioassay for ABA, the details of how or when ABA disrupts bud formation were left undescribed. This paper reports experiments that localize the inhibitory action of ABA to a particular time in the process of bud formation. Experiments using reciprocal transfers of protonema between medium supplemented with cytokinin and medium additionally supplemented with ABA find that bud formation is most inhibited by an ABA exposure late, not early, in the process of bud formation: ABA does not block initial perception of cytokinin. Experiments that compare numbers of buds when bud-forming protonema are transferred to hormone-free basal medium or when transferred to ABA-supplemented cytokinin medium find no difference between the two treatments, showing that the presence of ABA precludes the cytokinin-mediated commitment of nascent buds. Further characterization of this inhibition by classic Lineweaver-Burk plots finds that ABA is not a competitive inhibitor of the cytokinin-mediated stable commitment of nascent buds. The sensitivity to ABA identifies an additional regulatory event in the process of bud formation in moss.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSLITERATURE CITED |
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), are maintained by serial subculture, and are stored as cryopreserved stocks (Christianson, 1998a
).
As described previously (Christianson, 1998b
), rather than select light-grown colonies of moss just as the first caulonemal (cytokinin-responsive) filaments appear (Brandes and Kende, 1968
), these experiments use the cytokinin-responsive protonema generated as dark-grown caulonema (Doonan et al., 1986
). Three small pieces of a stock culture are inoculated onto sterile 7 cm Whatman number 1 filter papers placed on basal medium and incubated in the dark for 14 d. Culture plates are oriented edgewise so the negatively geotropic protonemal filaments grow along the surface of the filter papers. The collection of filaments derived from each spot of inoculum is termed a "colony," and bud formation after exposure to cytokinin and continuous light (Sylvania GroLux bulbs) is quantified by counting the number of buds formed by each protonemal colony 7 d after the initial exposure to cytokinin. Since mean numbers of buds and the variance associated with those means are not independent, statistical comparisons between treatments use data transformed to achieve homogeneity of variance (details in Christianson and Warnick, 1983
); significance was judged at the 5% level.
The amount of inoculum and the duration of growth in the dark can be varied, resulting in colonies that make 20 buds on our benzyladenine (BA) standard medium, colonies that make 60 buds on our BA standard medium (compare 
Fig. 2 and Fig. 3), or colonies with other amounts of potential for bud formation. Since replicate experiments, done with colonies that differ in bud-forming potential, give identical results when means are converted to percentage the mean of the BA standard, we are confident that our results report a general property of bud formation from moss protonema, and do not depend on the absolute numbers of buds being formed, i.e., the mass or age of the protonema being assayed.
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formulation of Knop's major salts, including iron supplied as FeNaEDTA, and the microelements used by Fred Sack (Ohio State University, Columbus, Ohio, USA): 70 µmol/L H3BO3, 14 µmol/L MnCl2, 10 µmol/L NaCl, 1 µmol/L ZnSO4, 0.5 µmol/L CuSO4, 0.2 µmol/L NaMoO4, and 10 nmol/L CoCl2. Medium was usually solidified with 8 g/L Difco BactoAgar; the increased gel strength of 18 g/L was needed for plates to be incubated edgewise in the dark. All media included sucrose at 10.2 g/L. Medium for maintenance of stock cultures included parachloroisobutyric acid at 20 µmol/L to retard the formation of caulonema (Sood and Hackenberg, 1979
). Medium for induction of buds included the cytokinin benzyladenine added before autoclaving. To perturb bud formation, inductive medium was supplemented with abscisic acid (ABA) immediately before pouring, using stock solutions prepared in DMSO. Control experiments showed no effect of these levels of DMSO on bud formation. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSLITERATURE CITED |
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with aged light-grown moss. Valadon and Mummery (1971) reported that the numbers of buds from cytokinin-treated protonema were reduced by half in the presence of 4 x 10-8 mol/L ABA and some 90% at 4 x 10-5 mol/L. The dark-grown protonema used in the experiments reported here show similar results. Some reduction in bud number was seen with as little as 10-9 mol/L ABA, and the inhibition increased in a dose-dependent way to an 50-fold reduction in bud number at 3 x 10-5 mol/L ABA (compare pairs of data points at day 0 or day 7; Fig. 1).
Abscisic acid acts after initial perception of cytokinin
Exposure to ABA might act by interfering with the action of cytokinin, either during initial perception or later during the cytokinin-mediated stable commitment of nascent buds. Alternatively, ABA might inhibit the process of bud formation by diverting cells or nascent buds into alternate developmental paths at some other time. A simple experiment, exposing responsive protonema to medium with cytokinin alone or cytokinin supplemented with ABA, followed by a regular program of timed transfers to the other medium, followed by counting and analyzing the numbers of buds produced from each treatment combination, would localize or "map" the time at which ABA exerts its inhibitory effect. If, for example, ABA inhibits the initial perception of cytokinin, only those protonema that were placed on cytokinin plus ABA at the beginning of the experiment would show low numbers of buds. Protonema moved to ABA-supplemented medium after 1 d on cytokinin alone would show no reduction in number of buds.
When such an experiment was performed, ABA was not found to interfere with initial perception of cytokinin (Fig. 1, note log scale). Protonema placed on cytokinin for 1 d (which allows all the initial events of cytokinin perception and signal transduction to occur) and then moved to cytokinin plus ABA made only a few buds. Conversely, while protonema placed on ABA-supplemented medium for 1 d, and then moved to cytokinin-alone medium, did make fewer buds than protonema cultured continuously on cytokinin-alone medium (see later), such protonema still made relatively large numbers of buds and far more buds than protonema exposed to ABA from day 0. The number of buds produced from responsive protonema does not depend on whether ABA is present initially. The number of buds does depend on whether ABA is present later during the process of bud formation.
While the curve describing the numbers of buds from protonema moved onto medium supplemented with ABA shows a smooth and regular advance, the curve showing the results of the successive transfers of protonema from ABA-supplemented medium is not a mirror image of the first curve. The numbers of buds per colony transferred from ABA-supplemented medium falls from an initial value of 30 buds per colony (moved to ABA-free medium immediately on day 0) to an intermediate value of 3 buds per colony (protonema transferred after 2–4 d on ABA) before declining to values similar to those for protonema cultured continuously on ABA (Fig. 1). The intermediate value may reflect some retention of ABA by the transferred cells.
The protonema and their filter paper supports were washed in ABA-free medium as a part of the medium-transfer protocol to eliminate hormone carryover. Such washing does successfully remove cytokinin from protonema, evidenced both by the reduced numbers of buds formed by washed filaments and direct observation that radiolabeled cytokinin is no longer present in washed filaments (Brandes and Kende, 1968
; Christianson, 1998b
). While washing will certainly remove ABA associated with the filter paper supports, it may well not remove all of the ABA from the protonema themselves. Even a small percentage carryover within cells exposed to 3 x 10-5 mol/L ABA-supplemented medium before transfer to ABA-free medium could be expected to reduce bud number dramatically: a residual 0.1% is equivalent to exposure to 3 x 10-8 mol/L, a concentration that does reduce bud number. Replicate experiments (data not shown) using medium supplemented with concentrations of ABA lower than 3 x 10-5 mol/L show less overall inhibition of bud formation and show larger but still intermediate values for buds from protonema transferred from ABA after 2–4 d. Experiments increasing the number and the length of the washes did not eliminate these intermediate values. Experiments using radiolabeled ABA to assess the overall efficiency of the washing protocol are possible, but would not substitute for experiments that directly corroborate the suggestion that ABA exerts its inhibitory effect on bud formation well after initial perception of cytokinin.
Transfer to cytokinin + ABA mimics transfer to basal medium
Electrophysiological, cytological, and various biochemical studies all contribute to an understanding of the events connected with the initial perception of cytokinin during bud formation. The second cytokinin-mediated event, the stable commitment of nascent buds, is understood only as a developmental event and detected only as the results seen after experimental manipulation (discussed in Meins and Binns, 1979
). Once nascent buds acquire a stable commitment as a bud, they are able to continue development in the absence of exogenous cytokinin. A series of transfers of bud-forming protonema to hormone-free basal medium, followed by observation of the number of buds that complete development, documents the successive commitment of nascent buds and measures the second effect of cytokinin during bud formation. If ABA inhibits bud formation by interfering with the second effect of cytokinin, a series of transfers to cytokinin + ABA medium will give the same numbers of buds as a parallel set of transfers to hormone-free medium. Such an experiment gave exactly those results (Fig. 2).
The fact that transfer to cytokinin + ABA mimics transfer to cytokinin-free medium corroborates the conclusion drawn from the previous experiment (Fig. 1). ABA does not interfere with the initial events of bud formation, but it does prevent the successive stable commitment of nascent buds during days 2–4 of bud formation. The close match between the results of transfer to ABA-supplemented medium or to basal medium is most easily explained as indicating a direct and immediate inhibitory effect of ABA on cytokinin or the cytokinin receptor, reproducing the actual removal of the cytokinin by washing the protonema and culture on hormone-free medium. Fortunately this suggestion of a direct interaction between ABA and BA can be tested by examining the formal kinetics of the interaction between ABA and cytokinin.
The interaction of ABA and cytokinin is not a competitive interaction
The number of buds formed from responsive protonema is controlled by the concentration of cytokinin present during the stable commitment of nascent buds (Christianson, 1998b
). If ABA reduces the effective concentration of cytokinin, either by some direct effect on the cytokinin molecules themselves (e.g., stimulating turnover) or by an effect on the target or receptor for cytokinin, then this interaction can be revealed by the same technique used to characterize enzyme inhibitors, the Lineweaver-Burk plot (Dixon and Webb, 1979
). Rather than assay an enzyme over a range of substrate concentrations in the presence of an inhibitor, the experiment would measure bud formation from protonema exposed to a range of cytokinin concentrations in the presence of ABA. Such an experiment, using ABA at 10-8, 10-7, and 3 x 10-7 mol/L, shows the well-known relationship between numbers of buds and concentration of cytokinin, and the effectiveness of ABA in reducing the numbers of buds at every concentration of cytokinin (Fig. 3, upper panel).
Replotting these data in the form of a Lineweaver-Burk or double-reciprocal plot results in two lines (Fig. 3, lower panel). If ABA and cytokinin both competed for the same receptor, and ABA inhibited bud formation by blocking the interaction of cytokinin with its receptor, the inhibitory effect of ABA would disappear when cytokinin concentrations were high. When the cytokinin concentration is very high, 1/[cytokinin] approaches zero; a competitive interaction between ABA and cytokinin would give two lines that intersect at 1/[cytokinin] = 0. In fact, however, the two regression lines do not intersect at that point (Fig. 3, lower panel), and statistical tests of the two y-intercepts show them to be distinct, P < 0.05. This analysis shows that while the kinetics of ABA inhibition mimic the effects of washing out the cytokinin (Fig. 2), the interaction between ABA and cytokinin is not a competitive interaction. There is no direct interference by ABA on the ability of the cytokinin receptor to perceive cytokinin.
The double-reciprocal plot (Fig. 3, lower panel) shows the two lines meeting near one point on the abscissa, and statistical testing finds no difference between the two intercepts. Intersection at the x-axis is evidence of a noncompetitive interaction. While noncompetitive interactions of substrates and inhibitors in assays of purified enzymes usually indicate distinct sites for binding of the inhibitor and for the substrate, this analysis of a whole-organism bioassay should not be used to postulate an ABA-binding site on the putative cytokinin receptor. While the slopes calculated for the lines in the plot (Fig. 3, lower panel) are numerically different, statistical testing does not find the slopes to be significantly different. This alternative possibility, a double-reciprocal plot showing two parallel lines with distinct y-intercepts, is evidence for an uncompetitive interaction. Indeed, like substrates and inhibitors for several well-characterized enzymes (Dixon and Webb, 1979
), the formal interaction between ABA and cytokinin may be a mixed-competitive interaction, neither non- nor uncompetitive.
The apparent lack of resolution between non- and uncompetitive kinetics for the interaction between ABA and cytokinin does not weaken the conclusion that ABA and cytokinin do not interact in a competitive way. Given that the land plant cytokinin and ABA signalling pathways are both known to use Ca2+ and G-proteins (Ward, Pei, and Schroeder, 1995
; Schumaker and Gizinski, 1996
; Irving, 1998
), there are likely to be several ways that distinct ABA- and cytokinin-signal transduction pathways could interact. Such cross-talk in signal transduction pathways is both a well-documented phenomenon and an increasingly useful conceptual framework for interpreting developmental physiology in higher plants (Hooley, 1998
; Iten, Hoffman, and Grill, 1999
).
ABA and the second cytokinin-mediated event in bud formation
While the molecular events associated with the initial perception of cytokinin during bud formation are increasingly well characterized (Saunders, 1986
; Conrad and Hepler, 1988
; Schumaker and Gizinski, 1993, 1996
), the second involvement of cytokinin in the process of bud formation is only characterized developmentally. Studies of the physiology of bud formation do demonstrate the critical importance of this second cytokinin-mediated event. Not only does this second event convert nascent buds into stably committed buds (Brandes and Kende, 1968
), this event is also responsible for the concentration-dependent regulation of the overall number of buds that will be produced from individual protonemata (Christianson, 1998b
). The only information about the molecular nature of this second interaction with cytokinin is the suggestion that it uses a cytokinin receptor distinct from the receptor used during initial perception (Christianson and Hornbuckle, 1999
). The demonstration in this paper that the ABA inhibition of bud formation mimics cytokinin withdrawl (Fig. 2), somehow precluding or preventing the second cytokinin-mediated event, suggests an examination of the ABA signal transduction pathway for clues to the molecular events controlled by cytokinin.
Plant cells respond to ABA in a variety of ways. It is, however, becoming increasingly clear that ABA-induced actions are of two types (Iten, Hoffmann, and Grill, 1999
). Fast responses to ABA such as the triggering of stomatal closure seem ultimately to be mediated by membrane-localized ion channels, both cation channels for potassium and calcium as well as anion channels; since ABA has been shown to increase the activity of GTP hydrolysis (Irving, 1998
), the involvement of G proteins in this regulation seems likely. The slower responses to ABA operate through ABA regulation of gene expression. Assays of gene constructs that are ABA responsive in angiosperms have shown this signaling pathway is already present in mosses (Knight et al., 1995
), but it is not yet known whether these constructs would be activated in bud-forming protonema exposed to ABA. While understanding of the complexity of the ABA inhibition of seed germination has been facilitated by the well-known antagonism between ABA and gibberellins and the ability to recover mutants variously defective for that interaction in Arabidopsis (Steber, Cooney, and McCourt, 1998
), gibberellin treatments do not antagonize the ABA inhibition of bud formation in Funaria hygrometrica (data not shown).
The experiments reported in this paper result in a greatly improved understanding of the inhibition of bud formation in moss by ABA first reported by Valadon and Mummery (1971)
. The inhibitory effect is not a result of some interference with the initial perception of cytokinin. ABA inhibits bud formation well after initial perception of cytokinin; the inhibition interferes with the subsequent cytokinin-mediated commitment of nascent buds. The quantitative effect of ABA on bud number (Valadon and Mummery, 1971
) results from the quantitative control of bud number by cytokinin concentration as nascent buds commit (Christianson, 1998b
). This effect is not produced by direct competition between ABA and cytokinin and may reflect cross-talk between components of the ABA signal transduction pathway and the signaling pathway used during the second interaction with cytokinin.
This characterization of the inhibitory effects of ABA on bud formation in moss also lays the groundwork for experiments to characterize the molecular nature of the cytokinin-mediated commitment of nascent buds. While the initial perception of cytokinin is increasingly well characterized (Schumaker and Gizinski, 1993, 1996
), the second cytokinin-mediated event is poorly understood, despite its importance as the developmental event that generates the commitment of nascent buds. The existence of this temporally distinct second requirement for the presence of cytokinin (Brandes and Kende, 1968
) has been confirmed by experiments showing buds initiated by exposures to a calcium ionophore require subsequent exposure to cytokinin to complete development (Saunders and Hepler, 1982
). However, neither observation sheds light on a mechanism. The sole mechanistic detail is the indication that initial perception of cytokinin and the second cytokinin-mediated event use chemically distinct cytokinin receptors (Christianson and Hornbuckle, 1999
). Given the successes in using antagonism between hormones as an experimental tool in angiosperms (e.g., the antagonism between GA and ABA in the developmental dissection of seed dormancy; Steber, Cooney, and McCourt, 1998
), the ABA-mediated inhibition of bud formation characterized in this paper can be used in schemes for the isolation of mutations that will reveal the identity of the proximate molecular cause of the stable developmental commitment of nascent buds in moss.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSLITERATURE CITED |
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Bopp, M. 1990 Hormones of the moss protonema. In R. N. Chopra and S.C. Bhatla [eds.], Bryophyte development: physiology and biochemistry, 55–77. CRC Press, Boca Raton, Florida, USA
Brandes, H., and H. Kende. 1968 Studies on cytokinin-controlled bud formation in moss protonema. Plant Physiology 43: 827–837
Chopra, R. N., and P. K. Kumar. 1988 Biology of bryophytes. John Wiley & Sons, New York, New York, USA
Christianson, M. L. 1998a A simple protocol for cryopreservation of mosses. Bryologist 101: 32–35[ISI]
———. 1998b The quantitative response to cytokinin in the moss Funaria hygrometrica does not reflect differential sensitivity of initial target cells. American Journal of Botany 85: 144–148[Abstract]
———, and J. S. Hornbuckle. 1999 Phenylurea cytokinins assayed for induction of shoot buds in the moss Funaria hygrometrica. American Journal of Botany 86: 1645–1648
———, and D. A. Warnick. 1983 Competence and determination in the process of in vitro shoot organogenesis. Developmental Biology 95: 288–293[CrossRef][ISI][Medline]
Conrad, P. A., and P. K. Hepler. 1988 The effect of 1,4-dihydropyridines on the initiation and development of gametophore buds in the moss Funaria. Plant Physiology 86: 684–687
Dixon, M., and E. C. Webb. 1979 Enzymes, 3rd ed. Academic Press, New York, New York, USA
Doonan, J. H., G. I. Jenkins, D. J. Cove, and C. W. Lloyd. 1986 Microtubules connect the migrating nucleus to the prospective division site during side branch formation in the moss, Physcomitrella patens. European Journal of Cell Biology 41: 157–164[ISI]
Gloor, H. 1947 Phänokopie-Versuche mit äther an Drosophila. Revue Suisse de Zoologie 54: 637–712
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Iten, M., T. Hoffmann, and E. Grill. 1999 Receptors and signaling components of plant hormones. Journal of Receptor and Signal Transduction Research 19: 41–58[ISI][Medline]
Knight, C. D., A. Sehgal, K. Atwal, J. C. Wallace, D. J. Cove, D. Coates, R. S. Quatrano, S. Bahdur, P. G. Stockley, and A. C. Cumming. 1995 Molecular responses of abscisic acid and stress are conserved between moss and cereals. Plant Cell 7: 499–506[Abstract]
Meins, F., Jr., and A. N. Binns. 1979 Cell determination in plant development. BioScience 29: 221–225[CrossRef][ISI]
Saunders, M. J. 1986 Cytokinin-activation and redistribution of plasma-membrane ion channels in Funaria. Planta 167: 402–409[CrossRef][ISI]
———, and P. K. Hepler. 1982 Calcium ionophore A23187 stimulates cytokinin-like mitosis in Funaria. Science 217: 943–945
———, and ———. 1983 Calcium antagonists and calmodulin inhibitors block cytokinin-induced bud formation in Funaria. Developmental Biology 99: 41–49[CrossRef][ISI][Medline]
Schumaker, K. S., and M. J. Gizinski. 1993 Cytokinin stimulates dihydropyridine-sensitive calcium uptake in moss protoplasts. Proceedings of the National Academy of Sciences, USA 90: 10937–10941
———, and ———. 1996 G proteins regulate dihydropyridine binding to moss plasma membranes. Journal of Biological Chemistry 271: 21292–21296
Shaw, A. J. 1991 The genetic structure of sporophytic and gametophytic populations of the moss, Funaria hygrometrica. Evolution 45: 1260–1274[CrossRef][ISI]
Simon, P. E., and J. B. Naef. 1981 Light dependency of the cytokinin-induced bud initiation in protonema of the moss Funaria hygrometrica. Physiologia Plantarum 53: 13–18
Sood, S., and D. Hackenberg. 1979 Interaction of auxin, antiauxin and cytokinin in relation to the formation of buds in moss protonema. Zeitschrift für Pflanzenphysiologie 91: 385–397
Steber, C. M., S. E. Cooney, and P. McCourt. 1998 Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149: 509–521
Suzuki, D. T. 1970 Temperature sensitive mutations in Drosophila melanogaster. Science 170: 695–706
Valadon, L. R. G., and R. S. Mummery. 1971 Quantitative relationship between various growth substances and bud production in Funaria hygrometrica: a bioassay for abscisic acid. Physiologia Plantarum 24: 232–234[CrossRef]
Ward, J. M., Z.-M. Pei, and J. I. Schroeder. 1995 Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7: 833–844[CrossRef][ISI][Medline]
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