Download Senescence and programmed cell death

Journal of Experimental Botany, Vol. 55, No. 406, pp. 2147–2153, October 2004
DOI: 10.1093/jxb/erh264 Advance Access publication 10 September, 2004
REVIEW ARTICLE
Senescence and programmed cell death: substance
or semantics?
Wouter G. van Doorn* and Ernst J. Woltering
Wageningen University and Research Centre, PO Box 17, 6700 AA Wageningen, The Netherlands
Received 27 May 2004; Accepted 26 July 2004
Abstract
The terms senescence and programmed cell death
(PCD) have led to some confusion. Senescence as
visibly observed in, for example, leaf yellowing and
petal wilting, has often been taken to be synonymous
with the programmed death of the constituent cells.
PCD also obviously refers to cells, which show a programme leading to their death. Some scientists noted
that leaf yellowing, if it has not gone too far, can be
reversed. They suggested calling leaf yellowing, before
the point of no return, ‘senescence’ and the process
after it ‘PCD’. However, this runs into several problems.
It is counter to the historical definitions of senescence,
both in animal and plant science, which stipulate that
senescence is programmed and directly ends in death.
It would also mean that only leaves and shoots show
senescence, whereas several other plant parts, where
reversal has not (yet) been shown, have no senescence,
but only PCD. This conflicts with ordinary usage (as in
root and flower senescence). Moreover, a programme
can be reversible and therefore it is not counter to logic
to regard the cell death programme as potentially reversible. In green leaf cells a decision to die, in a programmed way, has been taken, in principle, before the
cells start to remobilize their contents (that is, before
visible yellowing) and only rarely is this decision reversed. According to the arguments developed here
there are no good reasons to separate a senescence
phase and a subsequent PCD phase. Rather, it is asserted, senescence in cells is the same as PCD and the two
are fully synchronous.
Key words: Chloroplast, definitions, developmental context,
hypersensitive response, leaf yellowing, petal wilting, programmed cell death, senescence, terminology, tracheids.
Death is the inevitable end of the process of senescence
CM Child (1915) Senescence and rejuvenescence,
page 461
Introduction
Although this is now mostly forgotten, cell death had
already been noted by the early microscopists, whose
observations were often strikingly correct. Lange (1891),
for example, reported that a decrease in cytoplasm, and
a drastic decrease in the number of organelles preceded cell
death during xylem vessel formation. Prior to death, it was
suggested, macromolecules such as proteins were degraded
to small soluble compounds that were taken up by neighbouring cells. The author did not use the term programmed
cell death, but he insisted that the death of the xylem cells
was determined by their developmental context. He thus
implied that the process was a programmed event. Although the concept of a programmed death has thus existed
for a long time, the term programmed cell deathy (PCD)
was not used before the 1960s.
The term senescence was apparently used in everyday
Latin, and is therefore much older than the term PCD. For
example, Cicero (106–43 BC) wrote, in De senectute (On
old age): Temeritas est videlicet florentis aetatis, prudentia
senescentis (Of course rashness is the note of youth, and
prudence of old age). He added: [Even if our souls] are not
to be immortal, [..] a man must wish to have his life end at
its proper time. For nature puts a limit to living as to
everything else (Cicero, – 44). And Petrarca (1304–1374)
remarked (in Latin): I [..] have grown old amid dangers [..]
and bigger dangers cannot be reserved for my senescence
(Petrarca, 1364). It is not very clear when the word
senescence was introduced in science. In animal science
* To whom correspondence should be addressed. Fax: +31 317 475347. E-mail: [email protected]
y
When referring to the terms senescence and PCD, they are written in italics.
Journal of Experimental Botany, Vol. 55, No. 406, ª Society for Experimental Biology 2004; all rights reserved
2148 van Doorn and Woltering
the term was used at least as early as 1879 (Minot, 1879)
and with reference to plants not later than 1915 (Child,
1915), but its use may have begun considerably earlier.
In cases where outwardly visible senescence symptoms
appear, such as in leaves and petals, the process of senescence and PCD are often taken to be roughly synchronous.
Others take it that senescence refers to (visible changes in)
organs or whole individuals, and PCD to cells. Still others
propose to use these terms such that senescence precedes
PCD. There are good arguments for and against these
views, which will be discussed. It is concluded that the first
view is preferable.
Defining senescence and PCD
The Latin verb senescere means to grow old. About
a century ago, the word ‘senescence’ was conceived of,
in scientific texts, as the end phase of differentiation, the
phase that ends in death. This is reflected by the quote at
the beginning of this paper (Child, 1915). In the 1950s Peter
Medawar launched a new discussion about senescence in
animal biology. His problem was how to explain senescence in evolutionary terms, whereby it was defined as
having death as its endpoint (Medawar, 1952). More
recently, senescence in animals (including humans) is still
usually defined as the process that results in death (Crews,
2003).
In a seminal article, Leopold (1961) defined senescence
in plant cells, along the lines previously proposed by
Medawar (1957), as ‘the deteriorative processes that are
natural causes of death’. As Leopold (1980) explained:
‘Senescence [. . .] refers to those changes that provide for
the endogenous regulation of death. [. . .]. Physiological
changes involved in the autumnal coloring (and subsequent
death) of leaves, or in the dieback of tulips [. . .] in early
summer, or in the yellowing and death of annual and
biennial species after the completion of fruiting [. . .] would
be examples of senescence’. This definition emphasizes the
underlying processes that cause death. It is clear, therefore,
that the tradition about the definition of senescence, both in
the animal and plant fields, holds that its endpoint is death.
Lockshin and Williams (1964, 1965), who investigated
the degeneration of insect muscles during metamorphosis,
coined the term PCD. PCD is a programme whereby a cell
actively kills itself. It is to be distinguished from death by
necrosis where the stimulus is so overwhelming that the cell
is dead within a very short period. Initially, the term PCD
was solely used in animal physiology. In plant science the
term was introduced only by the end of the 1980s (Kirk
et al., 1987; Lascaris and Deacon, 1991), and was not
common until the mid-1990s.
Various definitions of PCD have been given. Martin
et al. (1994) defined it as a functional term, to describe
‘cell death as a normal part of the life of a multicellular
organism’. This definition emphasizes that death is de-
termined by the place of a cell, and by the role of its death
in the developing organism. As discussed above, Lange
(1891) had a similar conception of the programme of cell
death in tracheary elements (although he did not use the
term PCD).
Other definitions put the role of the genome into focus.
For example, according to Zhivotovsky et al. (1997) ‘PCD
is a genetically controlled cell deletion process’. Still
others emphasize the underlying biochemistry. Laytragoon
(1998), for example, writes that PCD is a process whereby
developmental or environmental stimuli activate ‘a specific
series of events that culminate in cell death’. This seems to
be the most comprehensive definition. The definition given
by Laytragoon (1998) for PCD seems rather close to the
one given by Leopold (1961) for senescence.
Whatever the definition of PCD, it is obvious that it
refers to cells, which exhibit a programme that leads to
their death. This programme is often triggered from outside
the cell. PCD comes in two main forms, (i) during the
development of the organism (this includes the reaction to
severe stress) and (ii) as a reaction to an invading microorganism (of which the hypersensitive response is an
example). During developmental PCD, cellular death usually depends on the time and place of a cell in the organism
(i.e. the developmental context of that cell). The term
PCD then refers to the underlying programme in cells
(either studied in isolation, or in an organ or individual),
and may refer to its developmental context. PCD clearly
does not only refer to death itself, which in many cells
occurs within seconds (at least when tonoplast rupture
occurs, which seems to be the moment of death; Obara
et al., 2001). PCD rather refers to the processes that lead to
the moment of death and the degradation (such as in the
nucleus and cell walls) that goes on after this moment.
Senescence and PCD: historical development
In animal science the term senescence was initially mainly
used for the processes leading to the death of individuals
(Child, 1915), but later on it also became used for processes
at the level of organs and cells (Witten, 1983). The term
PCD is applied to the death of cells, both in culture and in
the intact organism. In animal science, PCD is largely used
as a synonym for senescence at the cellular level (and is
used where previously the term senescence would have
been used). Plant scientists, applied the term senescence
mainly to the death of individuals and to that of organs, but
also in conjunction with death in tissues (e.g. endosperm
senescence) or individual cells. Plant scientists gradually
adopted the PCD terminology already in use in work on
animal systems. The term PCD first emerged in studies on
small groups of cells that die during the early developmental stages of a plant, i.e. not related to the death of an organ
or individual. Later on the term PCD became increasingly
popular in relation to the final stages of development of
Senescence and programmed cell death
organs (where previously the term senescence would have
been used). As the features of death in these cells fulfilled
the requirements for PCD in animal cells, such as the
presence of chromatin condensation and DNA cleavage, it
was not incorrect to use the term PCD instead of senescence. But these developments also had an aspect of
fashion. A colleague put this aptly: ‘PCD is sexy and
senescence is not, thus papers get published and grants get
funded when dealing with PCD and not when you call it
senescence’ (AD Stead, personal communication 2004).
The upshot of this observation is important: in practice the
two terms became used as synonyms, at least for some
examples of plant cell death.
Since PCD clearly refers to cells, the use of the terms for
organs or individuals may be rather imprecise if the focus is
not on (specific groups of) cells, with or without the context
of their development in the organ or organism. Imprecision,
can come about, for example, when the heterogeneity of
cell types in organs is overlooked. It has been known for
a long time that the cells in both leaves and petals do not die
at the same time. Cells in the mesophyll usually die before
those in the epidermis, and cells in the vascular bundles stay
alive longer than epidermal ones (Bancher, 1938). In
addition, cell death in any of these tissues usually does
not occur uniformly over the leaf blade. Chopping up
a whole leaf and studying ‘its’ PCD is therefore in error,
as one may ask to which cells the term PCD refers. Nonetheless, if emphasis is laid on (specific groups of) cells, it
seems that no logical error is made when replacing the term
senescence by PCD, provided that the definitions given
above for the two terms are accepted.
Delineation between senescence and PCD: the
opinions
Part of the confusion seems to be here: PCD and senescence
have become overlapping ideas, but it is unclear to what
degree they overlap. In most papers and reviews on PCD
and plant senescence it is tacitly assumed that the two
somehow overlap in time (Beers et al., 2000). However, it
is usually not spelled out where this overlap begins and
ends. Among those that do define the degree of overlap, two
points of view have been defended. According to the
majority opinion the overlap is complete (Noodén, 2004),
whilst in some recent papers there is no overlap at all
(Delorme et al., 2000; Thomas et al., 2003).
Delorme et al. (2000) and Thomas et al. (2003) see
senescence as a special case of plant cell differentiation,
designated transdifferentiation. The latter is defined as
‘change of a cell or tissue from one differentiated state
to another’. In their view, the conversion of chloroplasts
into gerontoplasts in senescing cells is comparable to the
conversion of chloroplasts into chromoplasts in ripening
fruit and developing flower petals, and can be seen as
a differentiation process. The period in which the transition
2149
of chloroplasts to gerontoplasts is reversible serves to
distinguish senescence from PCD.
More than 20 years ago Wang and Woolhouse (1982)
also argued that the point of no return was important in leaf
senescence. They suggested using the term senescence for
the processes that occur after the point of no return. This is
in contrast to Delorme et al. (2000) and Thomas et al.
(2003) who propose to use the term senescence for developments before this point.
The definition of the term senescence, according to the
view of Thomas et al. (2003), is opposite to the other one
that is often used, in which senescence as such ends in
death. According to their definition, senescence per se
does not result in death (but it can result in death, through
PCD).
According to still another use of the terms, they apply to
different parts of the plant. Senescence, in this view, is the
process that leads to the death of organs and whole plants,
while PCD refers to the death of (a relatively small number
of) cells (Noodén, 2004). This use of the terms is similar
to another one, which restricts the term senescence to
developmental processes in which the close-to-death symptoms are visible to the naked eye (as in leaf yellowing,
petal wilting, and withering of whole plants at the end of
their life span). In this view, the term PCD applies to all
other forms of cell death, such as in root aerenchyma formation after flooding, or the death of the embryo suspensor
cells.
Senescence as a precedent of PCD
Thomas et al. (2003) cite the peculiar relationship between
leaf yellowing and leaf death as a reason why they propose
their use of the terms senescence and PCD. In some cases
the leaves become yellow but if this process has not gone
too far such leaves can become green again. It must be
admitted that it is logically incorrect to call yellowing that is
later on reversed, programmed cell death, because in this
case the yellowing does not lead to death.
What is going on in tissues that regreen after becoming
yellow? The chloroplasts have initially lost considerable
quantities of proteins and chlorophyll, but are somehow
able to reverse the degradation process and synthesize
various compounds again (Krul, 1974). Instead of dying,
these chloroplast-containing cells will live on, at least until
the next signal for cell death comes around.
Such regreening is rare. It has been observed in the peel
of developing oranges, which attains maximum orange
colour during winter and slightly regreens by harvest time
the following summer (Coggins and Lewis, 1972; Goldschmidt, 1988). Similarly, in some rare cases petals can
regreen, and then live relatively long. This was observed,
for example, in a mutant chrysanthemum (Winkler, 1902),
and in a few orchids, after pollination (Phalaenopsis
cornu-cervi, P. violacea, Promenaea sp., and Epidendrum
2150 van Doorn and Woltering
macrochilum; Fitting, 1910). Regreening also occurs in the
spathe of Zantedeschia, as a normal part of its development
(Tavares et al., 1998) and in sepals of Helleborus niger,
which lose chlorophyll and serve to attract pollinators, then
become green again after pollination (Salopek-Sondi et al.,
2002).
If regreening is rare in fruit, petals, and sepals, how
general is leaf regreening? Only a few examples have been
described, all based on laboratory experiments in which
a large part of the shoot was removed. Krul (1974), for
example, noted that removal of the epicotyl of soybean can
reverse visible senescence in the cotyledons. Similarly,
yellow leaves of tobacco plants can regreen if the
whole top of the plant is cut off, leaving only one leaf
(Zavaleta-Mancera et al., 1999a, b). Regreening can also be
induced in Phaseolus vulgaris, which undergoes whole
plant senescence once it has formed seeds. Removal of all
parts of the shoot except a yellowing leaf and its subtending
part of the stem, could induce the leaf to become green
again (Jenkins and Woolhouse, 1981). Lack of water or
nutrients results in leaf yellowing in many plant species,
which in some species can be reversed upon removing the
stress, as shown in laboratory experiments (Girardin et al.,
1985; Zhang et al., 1995). This may also occur under
natural conditions, but no such cases have apparently been
described in plants growing in the field.
In young pea plants, which show an extreme case of
apical dominance, removal of the epicotyl (containing the
initial apical meristem) results in two equal small branches,
each with their own meristem. One of these branches soon
becomes dominant, and induces visible senescence symptoms and complete death in the weaker one. Removal of the
dominant branch, prior to the death of the weak one, rapidly
and completely reverses the death process in the latter.
This reversal can take place even after increased expression
of SAG12, encoding a common senescence-associated
cysteine protease involved in mass protein degradation
(Belenghi et al., 2004). Although this has not been described, such reversal of the cell death processes could, in
principle, also occur in nature, upon grazing.
The conclusion of this section is that regreening may
occur in nature, but that it seems rather rare.
Chloroplasts and life span
Thomas et al. (2003) attach great importance to the role
of functioning chloroplasts in preventing plant cell death,
citing evidence that tissues without such chloroplasts, such
as petals, tend to have a short life. This connection is not
general. Apart from the petals in some species that can live
up to 80 d (Molisch, 1929, page 75), there are several other
examples of cells that are devoid of chlorophyll but live for
many years. Some sclereids, for example, can live for as
much as 4–5 years. Wood fibres also have no chloroplasts,
but can live for as long as 20 years (Fahn 1990, Chapter 6).
In several species, the pith cells can live for as long as
11–20 years. Exceptionally long-lived pith cells were found
in Tilia parvifolia (28 years), Sorbus aucuparia (35–40
years), Betula alba (27–40 years) (Molisch, 1929, pages
89–90). Ray cells in woody stems can also grow very old.
In several species they lived for 24–36 years, with exceptions of up to 45 (Abies alba), 86 (Sorbus terminalis),
and about 100 years (Sequoia sempervirens) (Molisch,
1929, pages 91–92). Noodén (1988, pages 506–507)
mentioned other examples: (i) brightly coloured cacti, if
grafted onto a green nurse plant, (ii) shoots of albina (white)
soybean and tobacco mutants, if they are grafted onto
a green plant, and (iii) leaves that lack chloroplasts, in
chimeral plants. So there seems nothing fundamental about
the presence or absence of chloroplasts for the life span of
a cell. As long as the cell is able to get sugars and other
necessities, and does not, by internal or external signals,
become committed to die, it will live.
What may be true, nonetheless, is that the actual reversal
of the programme that leads to death, as is sometimes
observed, depends on the regaining of function in chloroplasts. If this is so, it is quite interesting. What is it in the
chloroplast that has this effect? Is it a matter of energy? If
so, does this mean that lack of energy is the factor that
causes death? (van Doorn, 2004). More than just sugars
seem to be required. Isolated petals or leaves held in an
aqueous solution containing an antibacterial compound and
a sugar may live longer than those held in the same solution
without sugar (or in water), but in most species they still die
rather soon.
Objections to the use of the term senescence
for a process that does not result in death
There are a few arguments against the idea of using the term
senescence for the period that precedes PCD. The first
argument refers to what is common use in plant biology.
If the definitions as given above are accepted, there is no
clear difference between senescence and PCD. A common
connotation of the concept of senescence, moreover, is that
it leads to death.
A second, and related, argument points to the consequences of the new definitions. The use of the terminology
as suggested by Thomas et al. (2003) conflicts with the
ordinary usage of the terms (root senescence, petal senescence; some scientists also speak of fruit senescence;
Castillejo et al., 2004). If the new terminology were to be
adopted, this would mean that only a few organs such as
leaves and shoots show senescence, and only during a,
usually unknown, part of their yellowing period. Insofar as
the senescence of whole plants is reversible, the term would
also be applicable to the trajectory before the point of no
return. As far as is presently known, there are no examples
of the reversal of senescence in organs other than leaves
and shoots and, possibly, individual plants. For this reason,
Senescence and programmed cell death
organs such as roots, petals, stigmas, styles, and anthers
would only have PCD, no senescence.
Third, it may well be argued that a programme can be
reversible. A programme of differentiation can be suspended, put in lower or higher gear, become terminated,
and also reversed. The reversal of a differentiation programme, however, does not mean that things that went in
the order a–c will now go in the order c–a. It seems more
like a train that is diverted to another track and therefore
will, this time, not go to station F but to station G, and in
some cases still may end up in station F. A well-known case
of such a reversal occurs during the development of female
flowers, whereby the anthers, which have already differentiated, disappear (Caporali et al., 2003). Similarly, a programme that would normally be leading to cell death can
also be reversed. Both senescence and PCD, the latter with
emphasis on the programme (and not on death), can both be
considered to be reversible in principle.
Fourth (and perhaps most important), in cells that undergo large-scale remobilization, the decision to die has
been taken prior to the remobilization phase. Remobilization in leaves, of which yellowing is a clear sign, is, on this
view, part of the programme that normally leads to death.
PCD starts when the decision to die is acted upon. On this
view, therefore, PCD starts at the time when the programme
that (usually) leads to death is initiated.
Senescence as related to whole organs,
and PCD to cells
For some, the term senescence refers to the death of organs
and whole individuals, and the term PCD for the death of
(small groups of) cells, during the early stages of development of an individual. This can be understood because of
historical developments (see above). Senescence was studied by physiologists, who worked with organs and whole
individuals that showed morphological signs of old age. At
the same time, plant anatomists noted cell death during
development, during spore formation, egg formation, embryo development, etc. (Fahn, 1990). However, it is now
known that the processes that lead to most cases of developmental cell death, at early and late stages, are the same.
There is, therefore, no good reason to distinguish between
cell death in a whole organ or plant, and death in a small
group of cells early on during development. The term PCD
can therefore also be applied to death of (the cells in) organs
and whole individuals, at the end of their life span.
Conversely, the term senescence may well be applied to
the process that leads to the death in relatively small groups
of cells during the early stages of development, or even to
cell death associated with the hypersensitive response.
In still another use, the term senescence refers to developmental processes in which the senescence symptoms
are visible to the naked eye. The term PCD applies to cell
death, including the death of cells in the organ that shows
2151
the visible symptoms. The visible features of senescence,
however, are a result of the cell death programme in the
cells of the organ that show these features. When the cells
that give rise to the visible symptoms are studied, chloroplast degradation, loss of turgor etc. will be found.
A number of publications have ‘programmed cell death
during senescence’ in their title (Simeonova et al., 2000;
Xu and Hanson, 2000; Coupe et al., 2004). The authors
apparently used senescence in one of the two ways described in this section. But if the reasoning here is followed,
it is a tautology to speak of PCD during senescence.
In conclusion
This paper addresses a rather fundamental confusion in
the field of plant biology interested in the developmental
programmes that ultimately lead to the death of cells, organs,
and individual plants. The confusion centres on the application of the terms senescence and PCD: whether they describe
similar events, distinct events or overlapping events.
Although it is proposed here that the terms senescence
and PCD can be used as synonyms (if referring to specific
groups of cells, with or without their developmental
context), the point made by Thomas et al. (2003) is a good
one. In the case of reversal of leaf yellowing it seems
logically incorrect to say that the yellow leaf, prior to its
regreening, was undergoing PCD. This is so because the
yellowing did not lead to cellular death. They suggest
applying the term senescence for the trajectory before the
reversal, and PCD for the part after it. However, they may
be right on a not very relevant point. Reversal of the
senescence symptoms seems rather rare in nature.
The terminology as suggested by Thomas et al. (2003)
leads to several problems. Their definitions are counter to
the older definitions of senescence, which maintain that
it leads directly to death. Furthermore, according to the
terminology of Thomas et al. (2003) only cells in which
the process is reversible can be called senescent, which,
given the present absence of proof for such reversal in
plant parts other than leaves and shoots, restricts the term
senescence only to these parts.
A way out of the problem is to consider a programme
reversible. If so, PCD, being a reversible programme, can
be considered to start when the signal for cell death has
arrived and is acted upon. PCD would thus start at the first
biochemical change that would normally lead to death, if
the programme were not somewhere reversed. Senescence
of cells is then equal to PCD, and fully synchronous with it.
The signal to die, it should be remembered, is given prior to
the dismantling of the cell, thus prior to PCD/senescence.
The present view thus concurs with Noodén (2004) who
stated that senescence, as (usually) conceived of in plant
biology, is in fact PCD. There is agreement that both PCD
and senescence are terms that denote the processes that lead
to the programmed death of individual cells during the early
2152 van Doorn and Woltering
stages of development, and to the death of cells in organs
and whole plants at the end of their life span.
Acknowledgements
We thank Sid (Howard) Thomas, Tony (Anthony D.) Stead, Abe
Halevy, and Larry Noodén for critical reading of the manuscript and
for their comments.
References
Bancher E. 1938. Zellphysiologische Untersuchung über den
Abblühvorgang bei Iris und Gladiolus. Österreichische botanische
Zeitschrift 87, 221–238.
Beers EP, Woffenden BJ, Zhao C. 2000. Plant proteolytic enzymes:
possible roles during programmed cell death. Plant Molecular
Biology 44, 399–415.
Belenghi B, Salomon M, Levine A. 2004. Caspase-like activity in
the seedlings of Pisum sativum eliminates weaker shoots during
early vegetative development by induction of cell death. Journal of
Experimental Botany 55, 889–897.
Caporali E, Spada A, Marziani G, Failla O, Scienza A. 2003. The
arrest of development of abortive reproductive organs in the
unisexual flower of Vitis vinifera ssp. silvestris. Sexual Plant
Reproduction 15, 291–300.
Castillejo C, de la Fuente JI, Iannetta P, Botella MA, Valpuesta
V. 2004. Pectin esterase gene family in strawberry fruit: study of
FaPE1, a ripening-specific isoform. Journal of Experimental
Botany 55, 909–918.
Child CM. 1915. Senescence and rejuvenescence. Chicago, IL:
University of Chicago Press.
Cicero MT. – 44. De senectute (On old age). Also called: Cato Maior
De Senectute. The first quote is from the end of Section VI, the
second from section XXIII, 85. Translated into English by
E.S. Shuckburgh, 1895. London: Macmillan.
Coggins CW, Lewis LN. 1962. Regreening of Valencia orange as
influenced by potassium gibberellate. Plant Physiology 37,
625–627.
Coupe SA, Watson LM, Ryan DJ, Pinkney TT, Eason JR. 2004.
Molecular analysis of programmed cell death during senescence in
Arabidopsis thaliana and Brassica oleracea: cloning broccoli
LSD1, Bax inhibitor and serine palmitoyltransferase homologues.
Journal of Experimental Botany 55, 59–68.
Crews D. 2003. Human senescence. Cambridge: Cambridge University Press.
Delorme VGR, McCabe PF, Kim DJ, Leaver CJ. 2000. A matrix
metalloproteinase gene is expressed at the boundary of senescence
and programmed cell death in cucumber. Plant Physiology 123,
917–927.
Fahn A. 1990. Plant anatomy, 4th edn. Oxford: Pergamon Press.
Fitting H. 1910. Weitere entwicklungsphysiologische Untersuchungen an Orchideenblüten. Zeitschrift für Botanik 49,
187–263.
Girardin P, Tollenaar M, Deltour A. 1985. Effect of temporary
nitrogen starvation in maize (Zea mays) on leaf senescence.
Canadian Journal of Plant Science 65, 819–830.
Goldschmidt E. 1988. Regulatory aspects of the chloro-chromoplast
interconversions in senescing Citrus fruit peel. Israel Journal of
Botany 37, 123–130.
Jenkins GI, Woolhouse HW. 1981. Photosynthetic electron transport during senescence of the primary leaves of Phaseolus vulgaris
cultivar The Prince. 1. Non-cyclic electron transport. Journal of
Experimental Botany 32, 467–478.
Kirk DL, Baran GJ, Harper JF, Huskey RJ, Huson KS,
Zogris N. 1987. Stage-specific hypermutability of the Reg-A
locus of Volvox: a gene regulating the germ-soma dichtomy. Cell
48, 11–24.
Krul WR. 1974. Nucleic acid and protein metabolism of senescing and regenerating soybean cotyledons. Plant Physiology 54,
36–40.
Lange T. 1891. Beiträge zur Kenntniss der Entwicklung der Gefässe
und Tracheiden. Flora 74, 391–434.
Lascaris D, Deacon JW. 1991. Relationship between root cortical
senescence and growth of wheat as influenced by mineral nutrition,
Idriella bolleyi (Sprague) von Arx and pruning of leaves. New
Phytologist 118, 391–396.
Laytragoon LN. 1998. Programmed cell death: the influence of
CD40, CD95 (Fas or Apo-I) and their ligands. Medical Oncology
15, 15–19.
Leopold AC. 1961. Senescence in plant development. Science 134,
1727–1734.
Leopold AC. 1980. Aging and senescence in plant development. In:
Thimann KV, ed. Senescence in plants. Boca Raton FL: CRC
Press, 1–12.
Lockshin RA, Williams CM. 1964. Programmed cell death. II.
Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. Journal of Insect Physiology 10,
643–649.
Lockshin RA, Williams CM. 1965. Programmed cell death. I.
Cytology of degeneration in the intersegmental muscles of the
Pernyi silkmoth. Journal of Insect Physiology 11, 123–133.
Martin SJ, Green DR, Cotter TG. 1994. Dicing with death:
dissecting the components of the apoptosis machinery. Trends in
Biochemical Sciences 19, 26–30.
Medawar PB. 1952. An unsolved problem of biology. London: H.K.
Lewis & Co.
Medawar PB. 1957. The uniqueness of the individual. New York:
Basic Books.
Minot CS. 1879. Growth as a function of cells. Proceedings of
the Boston Society of Natural History 20, 190–209.
Molisch H. 1929. Die Lebensdauer der Pflanze. Jena: Gustav Fisher
Verlag (translated into English: Molisch H. 1938. The longevity of
plants. Lancaster, PA: Science Press) [page references are to the
original in German]
Noodén LD. 1988. Postlude and prospects. In: Noodén LD, Leopold
AC, eds. Senescence and aging in plants. San Diego: Academic
Press, 499–517.
Noodén LD. 2004. Introduction. In: Noodén LD. Plant cell death
processes. Amsterdam: Elsevier. 1–18.
Obara K, Kuriyama H, Fukuda H. 2001. Direct evidence of active
and rapid nuclear degradation triggered by vacuole rupture during
programmed cell death in zinnia. Plant Physiology 125, 615–626.
Petrarca F. 1364. Rerum familiarium, Book 1. Translated into
English by John F. Tinkler, and published on the internet:
Petrarch’s Preface to his Familiar Letters. [The year of this work
is not precise, some sources date it c. 1350].
Salopek-Sondi B, Kova M, Prebeg T, Magnus V. 2002. Developing
fruit direct post-floral morphogenesis in Helleborus niger L.
Journal of Experimental Botany 53, 1949–1957.
Simeonova E, Sikora A, Charzynska M, Mostowska A. 2000.
Aspects of programmed cell death during leaf senescence of monoand dicotyledonous plants. Protoplasma 214, 93–101.
Tavares RM, Morais F, Melo N, Pais MSS. 1998. Thylakoid
membrane reorganization during Zantedeschia aethiopica spathe
regreening: consequences of the absence of DELTA3-transhexadecenoic acid in photochemical activity. Phytochemistry 47,
979–984.
Thomas H, Ougham HJ, Wagstaff C, Stead AD. 2003. Defining
senescence and death. Journal of Experimental Botany 54,
1127–1132.
Senescence and programmed cell death
van Doorn WG. 2004. Is petal senescence due to sugar starvation?
Plant Physiology 134, 35–42.
Wang TL, Woolhouse HW. 1982. Hormonal aspects of senescence
in plant development. In: Jackson MB, Grout B, Mackenzie IA,
eds. Growth regulators in plant senescence. Monograph no 8.
Wantage (UK): Plant Growth Regulator Group, 5–25.
Winkler H. 1902. Über die nachträgliche Umwandlug von Blüthenblätter und Narben in Laubblätter. Berichte der deutschen botanischen Gesellschaft 20, 81–125.
Witten M. 1983. A return to time cells systems and aging: rethinking
the concept of senescence in mammalian organisms. Mechanisms
of Ageing and Development 21, 69–82.
Xu Y, Hanson MR. 2000. Programmed cell death during pollinationinduced petal senescence in Petunia. Plant Physiology 122,
1323–1333.
2153
Zavaleta-Mancera HA, Franklin KA, Ougham HJ, Thomas H,
Scott IM. 1999a. Regreening of senescent Nicotiana leaves. I.
Reappearance of NADPH-protochlorophyllide oxidoreductase
and light-harvesting chlorophyll a/b-binding protein. Journal of
Experimental Botany 50, 1677–1682.
Zavaleta-Mancera HA, Thomas BJ, Thomas H, Scott IM. 1999b.
Regreening of senescent Nicotiana leaves. II. Redifferentiation of
plastids. Journal of Experimental Botany 50, 1683–1689.
Zhang C, Roemheld V, Marschner H. 1995. Retranslocation of
iron from primary leaves of bean plants grown under iron deficiency. Journal of Plant Physiology 146, 268–272.
Zhivotovsky B, Burgess DH, Vanags DM, Orrenius S. 1997.
Involvement of cellular proteolytic machinery in apoptosis.
Biochemical and Biophysical Research Communications 230,
481–488.