ФИЗИОЛОГИЯ РАСТЕНИЙ, 2012, том 59, № 4, с. 509-520
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УДК 581.1
Dedicated to the memory of Academician Mikhail Kh. Chailakhyan, on the occasion of the 110th anniversary of his birthday, for his insightful early work on the induction of flowering, the plant process preceding the senescence of the whole plant
Towards an Integrated View of Monocarpic Plant Senescence1 © 2012 P. J. Davies, S. Gan
Departments of Plant Biology and Horticulture, Cornell University, Ithaca, New York
Received August 6, 2011
After the flowering of an annual plant, the whole plant will senesce and die. For the process to go to completion, this monocarpic senescence must include three coordinated processes, which have not previously been considered as a total syndrome: (1) the arrest of growth and senescence of the shoot apical meristem; (2) senescence of the leaves; and (3) the suppression of axillary bud growth. Concurrently there is a shift in resource allocation from continued vegetative growth to reproductive growth, combined with a withdrawal of nutrients, especially nitrogen compounds, from the leaves and the transfer of these nutrients to the developing seeds. The start of the senescence process is caused by a shift, almost certainly in gene expression, very early in the reproductive phase. Continuation of the resource transfer and senescence of the vegetative plant involves hormonal regulation and continued changes in gene expression. Each of these processes is examined, especially with reference to the transfer of resources from vegetative to reproductive growth.
Keywords: Pisum sativum — Arabidopsis thaliana — Spinacia oleracea — senescence — monocarpic — whole plant — resource allocation — leaf — apical bud — axillary buds — flowering — reproduction — sugar — nitrogen
INTRODUCTION
After the flowering of an annual plant (and the production of seeds by a hermaphrodite or female plant), the whole plant will senesce and die [1—4]. This represents one extreme of a life cycle strategy, whereby the adult is sacrificed for maximal reproductive success, which is presumed to be an optimal lifestyle for shifting environmental conditions [1]. For the process to go to completion, this monocarpic senescence must include three coordinated processes: (1) the arrest of growth, and possibly senescence, of the shoot apical meristem(s) (SAM); (2) senescence of somatic organs and tissues such as leaves; and (3) the prevention of re-growth by suppression of axillary buds [5], as otherwise either growth will continue and/or the reserves will not be available for optimal seed production. Concurrently there is a shift in resource allocation from continued vegetative growth to reproductive growth, combined with a withdrawal of nutrients from the leaves and the transfer of these nutrients to the developing seeds. However, these processes, particularly
1 The article is published in the original.
Abbreviations'. JA — jasmonic acid; LD — long day; SD — short day.
Corresponding author. Peter J. Davies. Departments of Plant Biology and Horticulture, Cornell University, Ithaca, New York, 14853 USA. E-mail. pjd2@cornell.edu
leaf senescence, are frequently dealt in isolation with no attempt to examine the whole syndrome. Indeed, the role of axillary bud regrowth has been largely overlooked until recently. We will now attempt to integrate these various facets of monocarpic plant senescence and the relationships between them. Further we will examine the controls at the physiological and molecular levels and suggest mechanisms that underlie the entire syndrome.
GROWTH ARREST AND SENESCENCE OF THE SHOOT APICAL MERISTEM
Apical senescence has been most studied in peas (Pisum sativum). Impending senescence is first noticed as a slowing of apical growth: the apical bud decreases in size and often assumes a more open appearance due to the presence of numerous flower buds, at the same time as elongation growth is reduced (fig. 1). Apical growth then ceases, and the apical tissues become chlorotic. Although the apical buds at this stage are clearly in the mid-stages of the senescence process, they are not dead and can be rejuvenated [6]. Such re-growth often occurs as the fruits and seeds mature, although in such cases the regrowth is a very brief weak flush of growth, which, upon the development of one or two more pods, soon ceases, and the progress of senescence continues. As time progresses, further degra-
Fig. 1. Shoot tips of G2 pea plants just after the start of flowering, grown in (a) short days, in which indeterminate growth occurs, and (b) long days, in which senescence takes place after the production of a certain number of flowers and fruits; insert (c) shows the apical bud of a LD-grown plant (x4 magnification) in a state of arrest and senescence after further growth has ceased. Note that under LD the development of flowers and fruits is more rapid than under SD, so that flower buds open closer to the stem apex, even right up amongst the developing leaves of the apical bud, causing the apical bud displays a more open appearance. This shows that the signal initiating the transfer of resources to reproductive growth and impending senescence starts very early in the reproductive phase. See [13].
dative processes of senescence continue in the arrested apex, so that the tissues become necrotic and die. At this stage no further apical growth can occur. Starting at about the time of apical arrest, the leaves and the rest of the plant visibly start to senesce. The completion of this leaf senescence follows the death of the apical bud. In peas, apical senescence is thus the first part of the three senescence processes in the whole plant.
A genetic line of peas, bred by G.A. Marx and named G2, was found to have indefinite growth with no senescence in a greenhouse in winter. Unlike wildtype peas, where senescence invariably follows fruiting, apical senescence in the G2 peas was found to be regulated by photoperiod. Under long days (LD), the G2 plants flower, fruit, and senesce, while under short days (SD) the plants flower and fruit, but continue vigorous growth (fig. 1). Although dwarf (as judged by internode length), the plants can reach a height of 3 m. As the photoperiod is extended beyond 12 h, the number of nodes produced before senescence declines, reaching a minimum at 18 h [6].
The presence of fruits is needed to induce senescence in most peas, including G2 in LD. If all the flowers are removed, growth of G2 continues, even in
LD, although the internodes shorten, the apical bud assumes a very open shape as distinct from the normal "clamshell" appearance of a pea apical bud, and the leaves become very dark green and convoluted. In such circumstances, the cessation of flower removal leads to a very rapid fruit growth and a more rapid senescence than would normally take place. If not all flowers are removed, then there is an effective titration between the number of fruits developing at any given time and the time prior to the development of senescence symptoms [6]. Under these circumstances, apical death does not occur, being replaced by continued weak growth or a series of growth stops and starts. The start of senescence symptoms in the apical bud occurs with the initial development of the first fruits and reaches a maximum when these fruits are fully elongated [7]. The senescence-promoting effect of the fruits seems to decline thereafter, so that with the completion of seed development the fruits no longer contribute to the senescence response.
The photoperiodic regulation of senescence in G2 peas is associated with a particular genotype dictated by the presence of two dominant alleles, Sn and Hr [8, 9]. Genotypes of pea recessive at either or both these loci undergo senescence after a period of reproduction
regardless of photoperiod. Wild-type plants are sn, hr. Sn is the prime regulator and operates to delay flowering [10], with Hr amplifying the effect [11]. Sn appears to be responsible for the production of a graft-transmissible substance that delays flowering [12]. Both Sn and Hr could possibly be transcription factors regulating growth or negative regulators of the initiation of reproduction, resource redistribution, and senescence. Before visible senescence symptoms appear in the bud, the differences in the development of flowers and pods show a differential commitment to reproduction triggered by the different day lengths, under which the plants were growing. The flowers and pods of the pre-senescent long-day plants develop far more rapidly (fig. 1), correlating with the greater resource allocation to reproduction, well before senescence symptoms are visible [13].
Cellular changes associated with the initiation of apical senescence in G2 peas were found soon after the start of flowering [14]. Cell death in the apical meristem, as detected by the labeling of breaks in the DNA (that is generally referred to as TUNEL assay), started soon after floral initiation in LD, and steadily increased with time up to 80 days post floral initiation, as did DNase activity and oxidative stress (as measured by MDA content). Under SD there was no cell death in the apical meristem and very little increase in MDA content or nuclease activity. Gibberellin (GA3) application will prevent senescence in G2 plants grown under LD, and GA3 treatment inhibited the occurrence of cell death, MDA accumulation, and nuclease activation in the apical buds of LD-grown plants. LD thus function by promoting nuclear degeneration and cell death from early on in the reproductive process, and these changes are inhibited by SD, possibly through the elevation of GA levels.
THE ROLE OF REPRODUCTIVE GROWTH IN MONOCARPIC SENESCENCE
The timing of senescence
The initiation of the senescence program appears to occur very early in the flowering period, and, in most cases, senescence can only be delayed, not prevented, by surgery or hormone application. In G2 peas the cha
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