Journal of Experimental Botany, Vol. 52, No. 364, pp. 2151-2159,
November 1, 2001
© 2001 Oxford University Press
Original Papers |
Correlative controls of senescence and plant death in Arabidopsis thaliana (Brassicaceae)
Biology Department, University of Michigan, Ann Arbor, MI 48109-1048, USA
Received 13 March 2001; Accepted 3 July 2001
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Abstract |
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Like most monocarpic plants, longevity of Arabidopsis thaliana plants is controlled by the reproductive structures; however, they appear to work differently from most dicots studied. Neither male- and female-sterility mutations (ms1-1 and bell1, respectively) nor surgical removal of the stems with inflorescences (bolts) at various stages significantly increased the longevity of individual rosette leaves, yet the mutants and treated plants lived 20–50 d longer, measured by the death of the last rosette and/or the last cauline leaf. A series of growth mutations (clv2-4, clv3-2, det3, vam1 enh, and dark green) also increased plant longevity by 20–30 d but did not delay the overall development of the plants. The mutations prolonged plant life through the production of new leaves and stems with inflorescences (bolts) rather than by extending leaf longevity. In growing stems, the newly-formed leaves may induce senescence in the older leaves; however, removal of the younger leaves did not significantly increase the life of the older leaves on the compressed stems of Arabidopsis. Since plants that produce more bolts also live longer, the reproductive load (dry weight) of the bolts did not seem to drive leaf or whole plant senescence here. The developing reproductive structures caused the death of the plant by preventing regeneration of leaves and bolts, which are green and presumably photosynthetic. They also exerted a correlative control (repression) on the development of additional reproductive structures.
Key words: Arabidopsis, correlative controls, leaves, longevity, monocarpy, mutants, senescence.
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Introduction |
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Senescence in plants is an internally regulated and orderly degeneration leading to the death of single cells, organs or even whole plants during their life cycle. Senescence can be particularly dramatic in monocarpic plants, those that reproduce once and then die at the end of their reproductive phase (Noodén and Leopold, 1978
). Usually, monocarpic plants stop replacing their old vegetative organs, for example, leaves, during reproductive development, and the remaining organs are signalled to die (Noodén, 1980). In monocarpic plants, the reproductive structures often govern senescence of the whole plant with especially striking effects on the leaves. Soybean, for example, starts to decrease its growth rate as flowering is initiated (Noodén, 1984, 1988b). By the time the pods start to fill significantly, leaf growth is coming to a close, i.e. the reproductive growth reciprocally replaces vegetative growth. Late in seed development, the leaves begin to senesce (i.e. turn yellow), and the plants are triggered to die. Removal of the pods before the seeds mature prevents the completion of senescence and the death of the plant. In soybean, cessation of growth in the shoot and induction of senescence are clearly separate activities, and depodding does not reinstate much vegetative growth. This influence of one part of an organism on other parts is correlative control, and it plays major roles in co-ordinating development including senescence at the whole plant level. Usually, factors that delay reproductive development in monocarpic plants can thereby also delay the death of the plant (Noodén, 1988b). While control of senescence by the reproductive structures is common among monocarpic plants, this pattern may not occur in all monocarpic plants, and the Brassicaceae including Arabidopsis may be among the exceptions.
Arabidopsis thaliana (Brassicaceae) is monocarpic, and it is a model plant for molecular genetic and related research, because it is small, has a short life cycle and has a relatively small genome (Goldberg, 1998). Despite the discovery of many mutants and the identification of many genes in Arabidopsis, its senescence is not well understood and needs further investigation. In particular, very little is known about the correlative controls of senescence in this plant. Unlike soybean described above, there is some evidence against control of leaf senescence in Arabidopsis by the reproductive structures (Hensel et al., 1993; Noodén et al., 1996). A better understanding of the controls of senescence in Arabidopsis is essential to understanding the life of this plant and is necessary for establishing a broader context in which to view other genes and functions involved in the development of the plant.
Although Arabidopsis and other members of the Brassicaceae are monocarpic, they show very different patterns of whole plant senescence from most other flowering plants, particularly the legumes, that have been studied. Leaf senescence in these plants is not linked with the development of the reproductive structures in the same way it is in soybean. For example, studies with delayed-flowering, male-sterile mutants and light treatments show alteration of reproductive development does not change the longevity of individual Arabidopsis leaves (Hensel et al., 1993; Noodén et al., 1996). No information is available on whole plant longevity.
In most monocarpic plants, most of the leaves senesce following reproductive growth, but in some Brassica species, most or all of the leaves may senesce early in seed development. Nonetheless, early removal of the reproductive structures in B. campestris appears to delay senescence of the remaining leaves and the stems (Biswas and Mandal, 1987). The stems of rape (B. napus) and other members of the Brassicaceae including Arabidopsis are green and may also contribute to photosynthesis (Rood et al., 1984). In addition, the stems (including the axis of the inflorescence) serve as temporary storage sites (Major et al., 1978). Thus, the stems are capable of supporting the completion of seed development. Arabidopsis seems to share some of these traits with its relatives in the Brassicaceae.
The overall aim of this report is to examine the correlative controls of leaf and whole plant senescence in Arabidopsis thaliana from a variety of perspectives, i.e. using male-sterile and female-sterile mutants and surgical manipulations to determine the effect of the developing reproductive structures on the longevity of leaves and the whole plant. In addition, several growth-altering mutations such as clavata and det3 were investigated to determine if or how these mutations alter senescence. As a by-product of these studies, the correlative controls of reproductive development were also investigated. Several quite different approaches have yielded similar conclusions about the correlative controls of leaf and whole plant longevity in A. thaliana.
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Materials and methods |
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The plants and their culture
Plant types used:
Table 1
shows the genotypes of Arabidopsis thaliana (L.) Heynh. that were used.
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Plant culture:
These plants were grown on artificial soil under short days (SD) (10 h days with only cool-white fluorescent lights at 300 mmol m-2 s-1) at 27 °C during the days (21 °C nights) as described previously (Noodén et al., 1996). When these plants had produced about 18 leaves, approximately 45 d after planting, they were placed in long days (LD) (16 h days) at the same temperatures and light intensities as before. Culturing initially under SDs delays flowering and produces larger plants. It probably also provides a closer parallel to natural conditions. There is some difference in the timing of development among the different batches due to small differences in the conditions among the different growth chambers used, so the comparison is mainly with the accompanying controls within each cohort.
Treatments
Leaf marking:
Leaves (including the cotyledons) were counted in order of appearance, and four leaf cohorts (leaf number 12, 14, 16, 18, all ±1) were marked near the tip with a small drop of water-soluble typing correction fluid (no discernible effect on development), and each date of emergence was designated as the day when each new leaf reached 1 mm in length (Hensel et al., 1993). It seemed important to use a range of leaves in order to be able to generalize. Care was taken to keep the marked leaves from being covered by later emerging leaves, since this shading could effect the senescence of the leaves (Noodén et al., 1996).
Removal of the reproductive structures:
To study the effect of reproductive growth on senescence, the stems with inflorescences (bolts) and fruits (siliques) were removed at various stages of development. The following treatments were used. (A) Seven plants were left untreated as controls. (B) Only the siliques were removed as they began to form. It was, however, very difficult to remove the siliques with complete confidence that there was no damage to that branch of the inflorescence. Nonetheless, these inflorescences continued to grow. (C) The entire first bolts removed from the base when they had produced ten full siliques. Each secondary bolt was removed when it had produced one full silique (1 cm in length). (D) The entire bolts were removed when they had just begun to form siliques. (E) The entire bolts were cut off at their base when they had produced one open flower. (F) The entire bolts were cut off at their base when they reached 1 cm. For each of the plants in these treatments, the removed bolts were collected and dried in an oven at 100 °C for 10–12 h and placed in jars to be weighed.
Leaf removal:
To test the effect of the younger leaves on the older leaves, all of the leaves produced after leaf no. 21 were removed when leaf no. 21 had almost fully elongated in one set of plants (Noodén, 1980). In another set, all of the younger leaves (after leaf no. 21) and all of the oldest leaves (before leaf no. 11) were excised.
Measurements
Leaf death, plant death, and reproductive development:
Leaves were scored as dead when they were flaccid or dried over more than half their surface (Hensel et al., 1993). This final collapse of leaf tissue happened rapidly, going from fresh and turgid to wilted or even dry in 1 d, so leaf death could be determined within 1 d. A measure of whole plant death was devised to explore further the controls of whole plant senescence in Arabidopsis in addition to leaf longevity. Plants were scored as dead when the last leaf in the rosette or the last cauline leaf, small leaves on the stem below the inflorescence (whichever is last) had reached the criterion for death described above. Usually, when the last cauline leaf was dead, the stems and all the rosette leaves had died. At this time, there was no indication of any remaining life in the plant. Therefore, this seemed to be a useful measure of whole plant death. The extra leaves that formed as a result of the treatments or the mutations were too numerous to be counted accurately or without some damage. Moreover, earlier formed leaves under the new ones would already have died and decomposed, so the plants were simply photographed to show the effects.
Because alterations of the earlier stages of development of these plants could indirectly alter senescence and death, several key developmental parameters were measured, i.e. the advent of individual leaves, the date at which the initial stem with the inflorescence or ‘bolt’ had reached 1 cm (referred to as ‘bolting’), the opening of one flower (white petals showing), five flowers open, one full silique and five full siliques. For the experiments where sterile mutants were examined, the stems with the inflorescences were removed, dried in an oven at 100 °C and weighed as an additional measure of reproductive growth.
Chlorophyll:
Because the stems with the inflorescences lost their chlorophyll (i.e. turned a beige colour), and this change was prevented by some mutations, the chlorophyll contents of these structures was measured. The top 3 cm were removed from these structures in the wild-type, ms1-1, and bell1 plants when the wild-type plants were senescing, i.e. leaf 18 had been scored dead but not all of the rosette or cauline leaves had died. These tops were chopped, weighed, and placed in 2 ml of N,N-dimethylformamide (DMF) in darkness for 24 h for chlorophyll extraction as described previously (Canfield et al., 1995).
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Results |
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Analysis of correlative controls of senescence
Sterile mutants:
Since reproductive control of senescence has been seen in many monocarpic species, mutations that alter seed formation (Table 1
) were used to examine the effect of reproductive structures on senescence in Arabidopsis. Because monocarpic senescence is tied into the overall developmental timetable, the effects of the mutations on key developmental parameters were also checked. Both male- (ms1-1) and female- (bell1) sterile plants produced leaves, bolted, and flowered at the same time that wild-type plants did, but they produced siliques with no seeds. ms1-1 did not alter leaf longevity; however, bell1 seemed to shorten leaf longevity (c. 10 d) for some leaves. This confirms and also extends the findings of Hensel et al. (Hensel et al., 1994). The most pronounced difference seen in the sterile mutants was the increased and prolonged production of bolts and leaves. The sterile mutants continued to initiate new bolts and produce new cauline leaves and flowers even after the wild-type plants had died (Fig. 1). Likewise, they produced additional rosette leaves. This led to a significant delay in the death of the last rosette and the last cauline leaf for the mutant plants. In both mutants, the last rosette leaf died about 10 d later than the wild type and the last cauline leaf died about 20 d later than the wild type.
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The stems of Arabidopsis are green and probably photosynthetic until late in reproductive development at which time they become beige-coloured and dry up. These sterility mutations inhibited this visible colour change, and the analysis of chlorophyll content showed that the bolts of the sterile mutants not only stayed green longer but had much more chlorophyll. The sterile mutants produced more bolts and had larger final dry weights than the wild type, despite the lack of seed production (Fig. 1
; Table 2). Hensel et al. also found that ms1-1 plants continued to proliferate bolts (Hensel et al., 1994). Thus, the mutant plants that invested more of their resources in the reproductive structures lived longer than the wild type.
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Removal of the reproductive structures:
In order to examine the effects of the reproductive structures on senescence further, they were removed from wild-type plants at various stages. Like the sterile mutations, these treatments increased bolt initiation. However, the earlier the bolts were removed from the plant, the more bolts the plant produced (Table 3A). Removal of the reproductive structures did not significantly or consistently alter the longevity of the rosette leaves, and this agrees with the data from the sterility mutants. Rosette leaf production was also increased in the plants where the bolts were removed, and again, the earlier in development the bolts were removed, the more leaves were produced (Fig. 2). Comparing Figs 1 and 2, it can be seen that removal of the bolts stimulated leaf production more than the sterility mutations did. This continued production of parts also increased longevity of the plants, i.e. the treated plants had live rosette leaves longer (Table 3B).
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Leaf removal:
Since growing shoots and young leaves seem to induce the senescence of older leaves in some plants (Noodén, 1980), an attempt was made to increase leaf longevity by removing the younger leaves. Neither removal of all the younger leaves (after leaf no. 21) nor removal of both the younger and the oldest (before leaf no. 11) significantly extended the life of leaves 11 and 21 (Table 4). Interestingly, where both the older and younger leaves were excised, the remaining leaves grew larger and the axis formed a ball (diameter c. 1 cm) of small rosettes, presumably from secondary and even higher order axillary buds.
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Effects of selected growth mutations on senescence
Clavata mutants:
Among several mutations rumoured to alter senescence are the clavata mutants. The clavata genes regulate the growth and function of the shoot meristem, and mutations in these genes lead to an excess of undifferentiated cells in the meristem and a club-like appearance (Table 1; Clark et al., 1996). The clavata3-2 and 2-4 mutations did not alter several important aspects of development measured in this experiment. These plants initially grew like the wild-type plants, producing leaves and bolting at about the same time (Table 5). These mutants were not sterile; and in the end, the mutant plants were about the same size as wild type. The proportion of reproductive to vegetative structures produced by the mutants looked similar to wild type. The clavata mutations did not increase leaf longevity; however, they did increase whole plant longevity, and this was due to prolonged production of new leaves and bolts. The clavata plants lived between 20–30 d longer than the wild-type plants, i.e. the last leaves both in the rosettes and on the stems died 3–4 weeks after the wild-type plants were completely dead.
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vam1 enh mutants:
The vam1 enh (rev-1) mutation affects the growth of the shoot meristem, causing the shoot apical meristems that normally form at the axillary position of rosette and cauline leaves to be absent or replaced with a leaf or filament (Table 1; Pogany et al., 1998; Otsuga et al., 2001). vam1 enh plants occasionally form flowers with no internal organs, so they may also be partially sterile. The vam1 enh plants looked different from the wild-type plants, and the final plants were slightly smaller than wild type. They also produced leaves, bolted, flowered, and produced siliques about 10 d sooner than the wild-type plants did (Table 6). Interestingly, many of the vam1 enh mutant's leaves lived longer (10–20 d) than those of the wild type. Another unusual feature in the vam1 enh mutants is that they were the only plants studied where the cauline leaves died before their last rosette leaves. Nonetheless, the mutants did live longer; i.e. their last rosette leaves died 20 d later than the wild type.
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dark green and det3 mutants:
dark-green and det3 mutations have also been thought to alter senescence. Both of these mutants tend to have darker green leaves and are dwarf compared to wild type. The det3 plants do not develop the elongated (etiolated) morphology when grown in darkness (Table 1; Schumacher et al., 1999). Nonetheless, the dark-green and det3 mutants bolted, flowered and produced leaves at about the same time that wild-type plants did. The mature mutant plants were not sterile, and they were normally proportioned even though they were diminutive. Still, these mutations did delay death of the last rosette and cauline leaves (data not shown).
In contrast to most other mutants, leaves 12–18 on the dark-green mutants lived longer (3–8 d) than the wild type. The last rosette and the cauline leaves persisted much longer (about 30 d).
Interestingly, the rosette leaves on the det3 mutants had a slightly shorter longevity (1–5 d less) than the wild type. Nonetheless, the det3 mutation delayed whole plant death. For det3 plants, the last cauline leaf died about 20 d later than the wild type, but the timing of death of the last rosette leaf was very similar to the wild type.
Comparison of the two ecotypes Columbia and Landsberg:
Another set of observations has emerged incidentally from the many studies with these two ecotypes; basically, Columbia plants tended to live longer (c. 24 d) than Landsberg plants. Interestingly, Columbia has a bushier, more branched habit and seems to grow longer than Landsberg.
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Discussion |
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Measures of senescence
In most studies of leaf or whole plant (monocarpic) senescence, chlorophyll content has been used as the measure of senescence, but sometimes leaf longevity has been employed. For reasons explained elsewhere (Noodén, 1988
a), chlorophyll and other plastidic measures have some limitations; longevity is often better. In these experiments with Arabidopsis thaliana, leaf longevity is generally not altered by changing reproductive growth or by several vegetative growth mutations believed to delay senescence in these plants. Nevertheless, these mutations clearly altered whole plant senescence/longevity.
Measures of plant longevity
In order to examine whole plant senescence, measures of whole plant longevity had to be developed. It certainly is not practical, and may not even be possible, to measure the demise of the very last cell in a plant; however, the death of the last rosette and cauline (on the stem below the inflorescences) leaves seem to be good indicators of the death of the whole plant. The two tend to go together. In addition, other manifestations of whole plant death occur about this time, for example, the stems lose their chlorophyll (become beige-coloured) and die.
Developmental correlations
Especially for a study on correlative controls, it is essential to determine whether or not the senescence-delaying mutations altered the time frame of the overall development of the plant by measuring several key developmental parameters, for example, birth of the 12th leaf and opening of the first flower. A developmental time shift could affect senescence and longevity secondarily (Noodén, 1980), but these data indicate that the mutants (except vam1 enh which will be discussed below) affect overall development of the plant only relatively late. Thus, the mutants do not cause a developmental shift that could account for the delay in plant death.
Effect of blocking reproductive development on senescence and longevity
Male- and female-sterility mutations do not extend the longevity of the individual basal rosette leaves. Nonetheless, they delay the death of the last rosette and cauline leaves indicating that the reproductive structures do control whole plant longevity in Arabidopsis.
In order to cross check and complement the studies with the sterility mutations, experiments were also conducted with surgical excision of the reproductive structures at various stages, ranging from the removal of the early (1 cm) bolts to removal of just the siliques. As with genetic blockage of the seed development (sterility mutations), removal of the reproductive structures does not prolong leaf longevity but does lengthen the life of the plant especially if done early (i.e. 1 cm bolts).
Excision of the reproductive structures promotes both bolt and leaf production, whereas, the sterility mutations mainly increase bolt production. Interestingly, increased production of bolts, which are presumably photosynthetic, probably accounts for the increased longevity in the sterility mutants. Thus, it appears that the reproductive structures do exert correlative controls of whole plant senescence in Arabidopsis; however, it is different from most other flowering plants in that they act on regenerative growth (rosette leaves and photosynthetic bolts) rather than on leaf senescence.
Effects of growth-altering mutations on senescence and longevity
The mutations studied here increase the longevity of the plant, but apparently not through prolonging leaf survival. The clavata genes do not alter rosette leaf longevity, while vam1 enh (rev-1) and dark-green prolong it, and det3 actually shortens it slightly. Unlike the other mutations, vam1 enh accelerates the early stages of development; however, it does not hasten plant death. vam1 enh exerts other effects that compensate for the accelerated development. The mutant plants studied here continue to produce leaves and bolts longer than wild type, so the life of the organism is lengthened without necessarily delaying senescence of individual leaves. Interestingly, what all of these mutations have in common is that they alter growth, apparently meristem activity. In this way, they prolong the ability of the plant to regenerate its vital parts. Further study is required to explain these effects more specifically.
Correlative control of leaf senescence by younger leaves
Because Arabidopsis leaf longevity is not controlled by the reproductive structures, it seemed important to consider other possible correlative controls of leaf longevity. As plants grow, the oldest (basal) leaves usually senesce (progressive senescence) as new (apical) leaves are formed, and the senescence of the old leaves can be delayed by removing the young leaves and/or the growing shoot apex (Noodén, 1980). The Arabidopsis leaf rosettes represent a parallel situation (except that the stem is compressed), and this raised the possibility that senescence of the older leaves is controlled by the younger leaves instead of the reproductive structures. Since removal of the younger leaves (or both the younger and the oldest leaves) does not extend the longevity of the midrange leaves, this possibility seems excluded. Again, Arabidopsis is an unusual case.
Correlative control of reproductive development
A parallel picture of correlative control of reproductive development (interaction between reproductive structures) is emerging. Examination of the sterile mutants and the removal of bolts shows that when the plants do not produce seeds, they produce more bolts and flowers, supposedly in extended attempts to produce seeds. Most likely, there are multiple levels of controls at work in Arabidopsis as in soybean (Noodén, 1984), but that needs further investigation.
The removal of bolts promotes the production of rosette leaves, axillary rosettes and additional bolts. In the case where the bolts themselves were removed, an increased production of rosette leaves was seen, and this increase in leaves can prolong the life of the plant as well. Absence of the seeds in sterile mutants also increases the production of bolts, but with less effect on rosette leaf formation. It seems that the seeds reduce the number of bolts initiated, but the bolts themselves suppress the production of rosette leaves and other bolts. Removal of just the siliques did not have much effect on regeneration growth, perhaps because the bolts had already exerted their inhibition at an earlier stage or because some seeds were able to form in some siliques before they were removed. Apparently, Arabidopsis like many other plants has back-up mechanisms to replace lost or failed reproductive structures, but these are repressed until needed. Since the removal of reproductive structures at different stages and the genetic blockages have somewhat different effects, there must be several levels of correlative control here as in soybean (Noodén, 1984).
Again, evidence shows that neither leaf nor whole plant senescence in Arabidopsis is driven by the reproductive load. Clearly, these plants do not die sooner because they invest more in their reproductive structures. On the contrary, the surgically-treated plants and the sterile mutants put more into their reproductive structures and live longer.
Monocarpic senescence in Arabidopsis
Arabidopsis is a relatively short-lived plant and unlike most other species, such as soybean, that have been studied in senescence research, it invests little in its somatic tissue. In many monocarpic species, the reproductive structures control leaf longevity (Noodén, 1980, 1988b), but Arabidopsis shows a remarkable disconnection between the reproductive structures and the lives of individual leaves. The leaves do not seem to have much potential for living longer, although det2 (Chory et al., 1992), etr1-1 (Grbic and Bleecker, 1995), dark-green and vam1 enh all seem to be able to extend leaf longevity somewhat. In general, these data support the idea (Hensel et al., 1994) that Arabidopsis leaf longevity is a function of age rather than correlative controls. Plant longevity, however, seems to be determined by the ability of the plant to regenerate photosynthetic organs, leaves and stems, and this regeneration is under internal controls. The importance of regeneration seems to be borne out further by comparing the Landsberg ecotype with Columbia which forms more bolts and lives longer. Thus, the loss of meristem activity appears to be central to whole plant senescence in Arabidopsis. Likewise, it appears that continued growth and regeneration is a factor allowing perenniality (Thomas et al., 2000). Arabidopsis seems to be a prime example of Kirkwood's disposable soma (Kirkwood, 1985), i.e. Arabidopsis seems to form ‘cheap’, disposable leaves.
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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When seed production is inhibited, the plants live longer and they attempt to produce more stems and flowers (bolts). If, however, the entire bolt is excised, the plants make more rosette leaves and bolts. This increased and prolonged production of photosynthetic structures extends the life of the plant, but these plants eventually exhaust their ability to produce new tissue and then die. The seeds and first-formed bolts exert an inhibitory influence on the later-formed bolts; however, the bolts and the seeds seem to exert different correlative controls. Further research is needed to understand these correlative controls and to determine how the plant eventually loses its ability to produce more tissue. Because Arabidopsis is such an important research tool, it seems valuable to get a better understanding of its controls at the whole organism level.
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Acknowledgments |
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We are indebted to the Arabidopsis Biological Resource Center and Steve Clark for providing several of the mutants used in this study. We thank Amy E Stewart for providing the data on leaf removal (Table 4
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Notes |
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1 To whom correspondence should be addressed. Fax: +1 734 647 0884. E-mail: ldnum{at}umich.eduKey
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References |
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