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73
The evolutionary basis of leaf senescence: method to the
madness?
Anthony B Bleecker
Recent studies on the differential expression of genes
associated with leaf senescence support the long-standing
interpretation of plant senescence as an organized, genetically
controlled process. Sequence identities of genes that are
differentially expressed in senescing leaves indicate roles in
the salvage of nutrients. By considering this salvage function
as the selected trait and the degeneration and death of the
tissue a pleiotropic consequence of nutrient redistribution,
the process of leaf senescence can be reconciled with
evolutionary theories on the origins of senescence in animals.
Addresses
Botany Department, 430 Lincoln Drive, University of
Wisconsin-Madison, Madison, WI 50706, USA; e-mail:
Bleecker@facstaff.wisc.edu
Current Opinion in Plant Biology 1998, 1:73–78
http://biomednet.com/elecref/1369526600100073
Current Biology Ltd ISSN 1369-5266
Abbreviation
SAG
senescence-associated gene
Introduction
Understanding the decline in vitality that characterizes the
final stages in the life histories of most higher organisms
may represent one of the greatest challenges to biological
science and medicine. Yet, the field of senescence research
struggles to define even the terms under which it should
operate [1]. Is senescence the direct result of genetic
programming, or is it the opposite — a general breakdown
in systems that have passed the age where natural selective
forces operate to fine tune them?
Much of the debate surrounding the nature of senescence
is focused on animal models. The plant kingdom, however,
provides its own set of unique properties and problems
with respect to senescence. The apparent ability of some
plant species to live indefinitely and the prevailing opinion
that even somatic tissue senescence is a genetically programmed process have set the study of plant senescence
apart from the animal field [2••]. Have plants somehow
escaped from the evolutionary constraints that have made
limited lifespans a fact of life for most animals?
In this article, I will attempt to reconcile the apparent
differences in how senescence in plants and animals is
viewed from an evolutionary perspective. To this end, I
will briefly summarize evolutionary theories that account
for the prevalence of senescence in animals. I will then
discuss some problems with comparing plant and animal
life histories that arise from basic differences in the way
that plants and animals develop. Finally, I will suggest how
the apparent programmed nature of leaf senescence can be
reconciled with evolutionary theories of animal senescence
by considering the individual leaf as the organizational
unit on which selective forces have acted to create the
senescence syndrome.
Senescence in animals and plants:
definitional dichotomy?
In order to consider the evolutionary origin of senescence
in plants, some clarification of what is meant by the
term senescence is necessary. This is a particular problem
when discussing the relationship between senescence in
plants and animals because the term senescence has
been defined in different ways for these two classes of
organisms. In an attempt to clarify this issue, I will first
present a brief summary of the evolution-based definition
of senescence that was developed from animal models
but should apply to all higher organisms. I will then
consider how the unique features of plants have led to
some confusion in attempts to reconcile the evolutionary
theories of senescence developed for animals with the
developmental definition of senescence that is most often
used to describe the process in plants.
The term ‘senescence’ and the related term ‘aging’ have
multiple meanings and so must be defined carefully for
any specific discussion. Finch [1] cautions against the
use of the term aging for any purpose and discusses
using the term senescence to represent the decline in
survival and reproduction associated with advancing age.
While specific determinants of lifespan may be very
different for different species, the evolutionary forces
that shape life history patterns may be common to most
higher forms of life that have defined reproductive phases.
The evolutionary perspective may be summarized as
follows: most organisms have evolved in environments
where mortality is caused by external factors rather
than old age. For any specific species, natural selection
will operate to enhance reproductive output within the
context of this extrinsically imposed lifespan. The lucky
individuals who live well beyond this expected lifespan
will have exited from Darwinian design space; their
survival mechanisms will not have been fined tuned by
natural selection. As reviewed by Finch [1], the idea that
late acting genetic defects would not be eliminated by
natural selection and could thus accumulate and contribute
to senescence was first proposed by JB Haldane in
1941. Subsequently, GC Williams suggested that genes
which have a positive influence on reproduction but a
negative influence on postreproductive survival would be
favored by natural selection. This idea of antagonistic
74
Growth and development
pleiotropy was discussed more recently by Rose [3]. A
different perspective was provided by the ‘disposable
soma’ hypothesis [4], which posits that an organism’s
maximum life span will reflect a tradeoff between the
allocation of resources for the maintenance of somatic
tissues of the adult and the preservation of the germline
through the production of offspring. Given the greater
importance of reproduction for survival of the genome,
longevity of the individual is the inevitable loser.
This being the case, evolutionary theorists have had
difficulty considering how such an active suicide program
could have evolved in plants. Wilson [9••] considered
several alternative explanations for the evolution of
programmed senescence in plants, but was unable to
develop a convincing hypothesis. On the other hand, my
co-workers and I have suggested that leaf senescence in
Arabidopsis may be best explained using the concepts of
antagonistic pleiotropy and the disposable soma [10].
The concepts of antagonistic pleiotropy and the disposable
soma were developed from the study of animal systems
where the soma is largely composed of differentiated,
postmitotic tissues and where the germline is set aside
early in development. Plants, however, present particular
problems when attempting to apply the zoologically
derived definition of senescence. The modular nature of
plant growth and development and the propensity for vegetative reproduction lead to difficulties in defining where
an individual plant begins and ends. Even in the clearest
cases of individual plants, the semiautonomous nature
of plant organ systems presents difficulties in assigning
a specific time of death for the whole organism. These
attributes have caused scientists to make a distinction
between a gamet, which represents all structures arising
from a single seed, and a ramet, which represents some
identifiable somatic structure as an individual (see [2••]).
Individual shoot systems arising from an underground root
system may be defined as ramets, and this definition has
even been extended to the point where a single shoot
may be thought of as a population of ramets composed of
individual nodes [5]. From an evolutionary point of view
it may be more appropriate to consider the life history
of an individual leaf — a terminally differentiated, fairly
autonomous entity — when attempting to reconcile the
similarities and differences between plants and animals.
The question of whether leaf senescence is related to
the zoological definition of senescence or is strictly a
genetically regulated progression of events is not just an
academic one. The current emphasis on differential gene
expression as a paradigm for the study of leaf senescence is
predicated on the underlying assumption that senescence
is a developmentally controlled phenomenon. If this
assumption is essentially correct, then we can hope
that molecular and genetic strategies will succeed in
defining the underlying regulatory pathways that govern
the process. If, on the other hand, leaf senescence is to
some degree driven by the less well defined processes that
are thought to contribute to the evolution of senescence in
animals, then we might anticipate a more difficult time in
sorting out the adaptive processes from chaotic events that
are occurring because of the absence of selection pressure
acting on the system.
A second source of possible confusion with respect to
plants is a semantic one. The term senescence has
been used for many years in the plant literature to
refer specifically to an orderly progression of genetically
controlled events that lead to the degeneration and death
of leaf tissues. Plant scientists have tended to emphasize
the developmental aspects of leaf senescence, often using
the term programmed senescence [2••,6••–8••]. The clear
implication is that this programmed senescence is more
analogous to programmed cell death or apoptosis than
to the formal definition of senescence as a decline in
function related to age. This interpretation is fueled by
experimental evidence that the timing of leaf senescence
can be influenced by hormonal and other developmental
processes [2••,6••,7••] and by the long-standing evidence
that gene expression is required for the senescence
process (see [2••]). The recent that leaf senescence is
developmentally regulated so permeates the literature that
several authors have dismissed the notion that leaf senescence is related to the formal definition of evolutionary
senescence as an age-related decline in function[1,2••,5].
Developmental aspects of the senescence
syndrome in leaves
Natural leaf senescence follows a predictable progression
of events that are collectively referred to as the senescence
syndrome (for recent reviews see [2••,11•]. Ultrastructural changes are first noted in chloroplasts, where the
breakdown of thylakoid membranes is associated with
the visible loss of chlorophyll at the whole leaf level
and a decrease in levels of chloroplast proteins at the
biochemical level. In conjunction with the breakdown
in chloroplast internal structure, decreases in cytoplasmic
volume and in the number of cytoplasmic ribosomes are
often noted. By contrast, the integrity of the plasma
membrane, mitochondria and the nucleus is maintained
until very late in the senescence process. The breakdown
of chloroplast proteins and lipids is associated with a loss
of carbon and nitrogen from the leaf as it senesces. The
senescence syndrome, therefore, is interpreted in terms of
nutrient salvage. Several lines of evidence indicate that
this nutrient salvage system is a developmentally regulated
program. Enucleation of the cell blocks chloroplast degeneration, as do inhibitors of protein and RNA synthesis (see
[2••,6••]). Chloroplast degeneration is also reversible in
some experimental systems [2••]. These observations have
led to the recent interest in applying the techniques of
molecular biology to define the role that differential gene
expression may be playing in the senescence syndrome.
A number of research groups have used recombinant
DNA techniques involving differential and subtractive
The evolutionary basis of leaf senescence Bleecker
75
hybridization to identify cDNA clones that represent
genes that are differentially expressed during senescence.
Recent reviews provide detailed surveys of sequenced
genes and their expression patterns [2••,6••–8••,11•], so
I will only provide a brief summary here. Three broad
classes of cDNAs can be seen based on expression
patterns: first, those that decrease in relative abundance;
second, those that show little change in relative abundance; and third, those that increase in relative abundance
as senescence progresses. A caveat to all of these studies
is the use of total RNA to determine relative mRNA
abundance which can be misleading when one considers
that total RNA declines significantly during senescence.
This problem has been addressed in some studies by
calculating mRNA abundance on a per leaf basis [10,12].
Alternatively, if specific transcription factors are required
at all, they may be present in nonsenescing cells and
activated by whatever decision-making machinery must by
definition be present in presenescent tissues. It is even
conceivable that decreased expression of transcriptional
repressors is the key regulatory event. In any case,
sequence analysis of some SAG 5′ regulatory regions has
not revealed any common sequence elements between
different SAGs [6••,7••]. Taken together with the wide
range of expression patterns observed for SAGs, these
results support the idea that the proximal regulation
of gene expression associated with senescence may be
complex [6••,8••,9••]. This may also be why mutational
analysis in Arabidopsis has yet to provide any mutants that
block the senescence process [13••].
Many of the genes classified as senescence-associated
genes (SAGs) are expressed in green tissues and increase
in relative abundance at later stages of senescence. Some
of these may simply be genes whose levels of expression
are maintained in cells while levels of most mRNA classes
and rRNAs are declining. A smaller set of cloned cDNAs
represents genes that are more clearly expressed only in
senescing cells [7••,12]. The distinction between these
two sets of genes may be important in that although
the former may increase in relative abundance during
senescence (as a consequence of message stability), the
latter are better candidates as genes that are transcriptionally activated during senescence. Attempts to study
expression patterns of SAGs in detail led in one case to the
classification of nine different patterns of expression [7••].
This level of complexity may reflect the operation of many
different pathways operating by different mechanisms.
Lacking a clearly developed picture for proximal regulatory systems, I turn now to the consideration of higher
order regulatory systems that appear to control the timing
and progression of leaf senescence. Reminiscent of the
proverbial blind men and the elephant, one’s concept of
how leaf senescence is controlled depends very much
on which plant system one is examining. The relevant
systems have been the subjects of recent reviews so I will
just mention them briefly here. There are clearly examples
where specific hormones have a controlling influence
over organ senescence. Cytokinins can have a dramatic
effect on delaying leaf senescence in some species [14].
The effectiveness of applied cytokinin, however, varies
considerably between plant species. Ethylene promotes
senescence in many species but several recent studies
indicate that ethylene is neither necessary nor sufficient
to cause senescence in Arabidopsis or tomato [15,16•].
On the other hand ethylene is the key regulatory factor
in the senescence of floral organs in some species [17].
Environmental signals can also trigger senescence. Shading of lower leaves by upper leaves induces senescence
in some species (see [6••]), while deciduous trees are
affected by temperature and day length. Reproductive
development can trigger senescence of vegetative tissue
both proximally and even on a global scale in monocarpic
species. Evidence from soybean is consistent with a
chemical communication system between fruits and leaves
that triggers the senescence syndrome [2••]. Finally, leaf
age may be the best predictor of when senescence will
occur; this seems to be the case in Arabidopsis [10].
Sequence analysis of SAGs has resulted in the identification of a number of genes that are likely to be
involved in salvage functions [2••,6••–8••,11•]. These
include genes encoding proteases, nucleases, lipid- ,
carbohydrate- and nitrogen-metabolizing enzymes and
other enzymes involved in mobilization of nutrients.
Another class of sequences appears to code for protective
or stress response functions [7••]. The latter may act
to protect the increasingly fragile cell while the task of
salvage is being completed, or they may simply respond
blindly to the trauma caused by salvage and perform
no adaptive function at all. Finally, many cloned SAG
sequences have no obvious role in salvage or protection
[7••,11•]. Is the expression of these genes significant or
simply the molecular ramblings of cells going senile?
One class of genes that are conspicuously absent from
SAG populations is those with obvious gene-regulatory
functions. For example, no transcription factor candidates
have been reported. It is possible that messages for
differentially expressed transcription factors are present
but too rare to have been picked up by current techniques.
A key point here is that a multiplicity of factors may
influence the timing of leaf senescence, but none of them
applies to all cases. At the same time, the senescence
syndrome these signals are acting on is quite similar
in widely different plant species. Also, the senescence
syndrome includes the differential expression of related
suites of genes. To consider how this situation might have
arisen, I will return to the discussion of the evolutionary
basis of leaf senescence.
76
Growth and development
Reconciling the evolutionary origin of
senescence in plants and animals
In considering the evolutionary origin of leaf senescence, I propose that the senescence syndrome, or more
specifically the salvage system that it represents, is a
primitive set of pathways that were recruited early in
the evolution of land plants because these biochemical
pathways contributed to the retention of nutrients by
the whole plant. I use the term recruited because it
seems plausible that the biochemical activities required for
the operation of the senescence syndrome were already
functioning at reduced levels as a component of cellular
maintenance. This may explain why so many SAGs are
still expressed at lower levels in healthy tissue. Perhaps
the senescence syndrome evolved by mechanisms that
shifted the balance of anabolic and catabolic components
of cell metabolism in favor of catabolism. A key element
of this proposal is the idea that the senescence syndrome
was originally selected to salvage nutrients, not to cause
the death of the tissue in which it is expressed.
It is my contention that the many facets of the senescence
syndrome discussed above can be brought into perspective
and reconciled with the evolutionary theories of senescence developed for animal systems if one considers the
individual leaf as the organizational unit on which natural
selection acted thus creating the senescence syndrome.
Obviously, the somatic tissues of the leaf do not contribute
directly to the future of the genetic line, but then, neither
do the somatic tissues of an animal. Leaves do provide
an indirect contribution to the genetic line in the form
of photosynthetic assimilates. One would expect natural
selection to favor the continued survival of a leaf as long
as this assimilatory function is operable.
Despite this expectation a variety of environmental and
developmental factors may limit the functional ‘life
expectancy’ of a leaf. Predation, sporadic and seasonal
climate extremes, and competition for light — both from
competing plants and ultimately from continued growth
of the parent shoot — may contribute to a diminishing
capacity of a leaf to maintain photosynthetic output.
According to the disposable soma hypothesis [4] it is
unlikely that natural selection would favor maintaining
leaves in a healthy state when they age beyond the
functional life expectancy imposed by these external
factors. One would expect that natural selection would
favor the evolution of salvage pathways that are either
activated or enhanced as leaves approach this maximum
functional life expectancy because these salvage systems
would produce a continued contribution to the plant in the
form of salvaged nutrients.
The massive nutrient salvage associated with the senescence syndrome and cell maintenance are not compatible
programs. A pleiotropic consequence of the salvage
pathways is that their activities tend to increase the
mortality rate of the tissues in which they are expressed.
Natural selection will not have a correcting influence
on these negative consequences of salvage if the leaves
at that stage have a low probability of contributing to
reproduction via photosynthesis. In other words, salvage
pathway genes fit the theory of antagonistic pleiotropy
[1,4]. They were selected during evolution for their
contributions to reproductive success, but have a negative
impact on the longevity of the somatic tissues in which
they operate.
Cell death: developmental program or
gratuitous pogrom?
If one accepts the idea that the primal function of the
senescence syndrome was salvage, then the subsequent
death of the leaf could be considered a consequence of the
lack of selection for continued survival. From this point
of view, the senescence syndrome cannot be considered
a cell death program, although this extreme theoretical
viewpoint only considers positive contributions of the leaf
to the whole plant. A leaf that is left in a weakened
state as a result of salvage could become a liability to
the whole plant, for example, as a target for pathogen
invasion. In this case, evolutionary forces could select for
pathways that deliver the coup de grace to senile leaves.
Such pathways could be selected by recruitment of specific
subroutines within the overall syndrome. They could also
evolve as completely different developmental programs,
the abscission process being the primary example [10].
The plant leaf is a semiautonomous unit. It receives
information from its own internal processes and directly
from the environment. The leaf also receives chemical
signals from the parent plant that carry information
as to the nutritional and developmental status of the
plant. Information processing networks that have evolved
within the leaf could couple any combination of these
signals to cause the activation of salvage pathways. The
developmental control of these salvage pathways opens
the possibility that they could be co-opted by evolution
to function more directly in programmed cell death.
For example, the rapid senescence of floral displays
after fertilization [18] may have been selected more as
a protection against predators than as a mechanism of
salvage. Even the monocarpic senescence of crop plants
like soybean and pea [19] could be the result of selective
breeding for ease of human harvest; in which case the
target of selection would be the global death of vegetative
tissues rather than salvage.
Conclusion
I have argued that the senescence syndrome in leaves,
while clearly a developmentally controlled program, can
be reconciled with evolutionary theories of senescence
in animals if one considers the leaf as the organizational
level at which natural selection acts. This simplifies the
comparison of plant and animal systems because both
systems are essentially postmitotic highly differentiated
systems. The programmed nature of the senescence
The evolutionary basis of leaf senescence Bleecker
syndrome is explained if one assumes that the adaptive
significance of the syndrome is in nutrient salvage and that
the associated cell death is a pleiotropic consequence of
the program. Once these salvage pathways are in place,
however, they could be co-opted by natural selection to
function more directly in the death of tissues and organ
systems.
The study of gene expression associated with senescence
indicates that the process is multigenic and complex. No
clear picture of the genetic regulatory mechanisms that
that drive the process has yet emerged out of these studies.
The overall syndrome may best be viewed as a collection
of parallel and branched regulatory pathways that may
form a regulatory grid. These salvage pathways may be
activated when the leaf no longer contributes sufficiently
to photosynthetic function, or they may be coupled to developmental signals that activate programmed senescence
in otherwise healthy tissues.
Challenges facing the study of leaf senescence involve
characterizing the various pathways and the specific
functions they regulate. The genetic approach provides
the greatest promise to produce definitive answers in this
regard. Mutations in SAG genes and in the pathways that
regulate them will help to sort out the different regulatory
pathways involved. Various approaches for achieving this
goal using Arabidopsis as a model system have been
discussed [6••,10]. Specific examples where genetics
has provided interesting insights include the stay-green
mutants in Festuca [18], which are blocked in the turnover
of chlorophyll in the thylakoid membranes but otherwise
show most aspects of the senescence syndrome. In
soybean, mutations at two loci, designated d1 and d2,
cause a delay in leaf senescence. A maternally inherited
mutation, cytG, has a similar effect. The combination of
these mutants appears to block the ability of reproductive
structures to trigger the senescence syndrome in otherwise healthy soybean leaves [2••,19]. Interestingly, these
mutations do not block the activation of abscission in
these leaves. These examples demonstrate that mutations
which affect specific subroutines or signalling pathways
associated with the overall senescence syndrome can help
to unravel the complexities of senescence in plants.
apply. This may seem true from a strictly whole-plant perspective, but not
when one considers the individual leaf as a unit of selection.
3.
Kirkwood TB, Rose MR: Evolution of senescence: late survival
sacrificed for reproduction. Philos Trans R Soc Lond 1991,
332:15-24.
The authors provide an interesting and readable discussion of two prominent
theories that account for the evolution of senescence in animals: antagonistic
pleiotropy and the disposable soma.
5.
1.
Finch CE: Longevity, Senescence, and the Genome. Chicago:
University of Chicago Press: 1990.
Noodén LD, Guiamet JJ: Genetic control of senescence and
aging in plants. In Handbook of the Biology of Aging. Fourth
edition. Edited by Schneider EL, Rowe JW. San Diego: Academic
Press; 1996:94-118.
The authors provide a summary of the field of plant senescence from several
perspectives and include a survey of genes that are differentially expressed
during senescence. They argue that, because leaves may senesce before
or during reproduction, evolutionary models for animal senescence do not
Roach DA: Evolutionary senescence in plants. Genetica 1993,
91:53-64.
6.
Gan S, Amasino RM: Making sense of senescence. Plant Physiol
••
1997, 113:313-319.
This recent review of leaf senescence both considers the recent studies
on gene expression and summarizes the developmental and environmental
pathways that influence the timing of senescence in different systems. The
senescence syndrome is presented as a form of programmed cell death,
but the authors do consider the apparent complexity of regulatory factors
that may operate in the syndrome and suggest a network of parallel and
overlapping pathways that control the process (Figure 3).
7.
Buchanan-Wollaston V: The molecular biology of leaf
••
senescence. J Exp Biol 1997, 307:181-199.
The author focuses on the analysis of differential gene expression during
leaf senescence. This is perhaps the most thorough of recent reviews on
this topic. A flow chart of salvage pathways thought to be active during
leaf senescence is provided and reconciled with the identities of many
senescence-associated gene clones. An attempt is made to classify genes
according to their expression patterns, of which 10 different classes are
identified. It is recognized that the complexity of expression patterns may
indicate a plethora of regulatory pathways. Yet, the author is convinced that
transcriptional control is the key to senescence and that all genes which are
differentially regulated must be important to the process.
8.
Nam HG: The molecular genetic analysis of leaf senescence.
••
Curr Opin Biotechnol 1997, 8:200-207.
In the same vein as other recent reviews [7••], the author use gene expression as the paradigm of control. An emphasis is placed here on the idea
that hormonal and developmental pathways overlap in controlling different
senescence-associated genes (SAGs) and that different forms of senescence (starvation induced, hormonally induced and age related) show differences in which SAGs are elevated. In the conclusion, the importance of
considering post-transcriptional mechanisms for SAG abundance is emphasized. Examples where mRNA and protein abundance data do not necessarily agree are also noted as a cautionary point.
9.
Wilson BJ: An evolutionary perspective on the ‘death hormone’
••
hypothesis in plants. Physiol Plant 1997, 99:511-516.
The author considers the problem of how a developmental system that
causes death could have evolved. Selection at several different levels is considered and the author concludes that nutrient competition between leaves
and fruits is the best candidate. Wilson discounts this mechanism, however,
because even old leaves are not net importers so their death is of no consequence; and also, monocarpic varieties do not show a consistent advantage
over their polycarpic relatives in terms of yield. To the first argument, I would
respond that export from older leaves, not competition for import, is the issue.
Release of stored nitrogen and other nutrients from otherwise unproductive
leaves is the trait under consideration. The second argument, therefore, is
based on flawed experiments. Comparing varieties with multiple genetic differences in species that have been artificially selected by humans and grown
under specialized protected conditions is not likely to be the criterion that
evolutionary processes would use in selecting the trait.
10.
• of special interest
•• of outstanding interest
Rose MR: Evolutionary Biology of Aging. Oxford: Oxford University
Press; 1991.
4.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
77
Hensel LL, Grbic V, Baumgarten DA, Bleecker AB: Developmental
and age related processes that influence the longevity and
senescence of photosynthetic tissues in Arabidopsis. Plant Cell
1993, 5:553-564.
11.
•
Weaver LM, Himelblau E and Amasino RM: Leaf senescence:
gene expression and regulation. In Genetic Engineering, V.19:
Principles and Methods. New York: Plenum; in press.
This is a thorough review of leaf senescence that considers primarily the
biochemical and molecular aspects of the process.
12.
2.
••
13.
••
Lohman KN, Gan S, John MC, Amasino RM: Molecular analysis
of natural leaf senescence in Arabidopsis thaliana. Physiol
Plant 1994, 92:322-328.
Bleecker AB, Patterson SE: Last exit: senescence, abscission
and meristem arrest in Arabidopsis. Plant Cell 1997, 9:11691179.
This review focuses on Arabidopsis as a model system for the study of
senescence and abscission. It includes considerations of somatic tissue
senescence and the growth arrest of meristems that contribute to whole
78
Growth and development
plant senescence. Theoretical discussions relevant to this paper are also
included.
14.
Gan S and Amasino RM: Inhibition of leaf senescence by autoregulated production of cytokinin. Science 1995, 270:19861988.
15.
John I, Drake R, Farrell A, Cooper W, Lee P, Horton P, Grierson
D: Delayed leaf senescence in ethylene deficient ACC-oxidase
antisense tomato plants. Molecular and physiological aspects.
Plant J 1995, 7:483-490.
16.
Grbic V, Bleecker AB: Ethylene regulates the timing of leaf
•
senescence in Arabidopsis. Plant J 1996, 8:595-602.
The authors use ethylene insensitive mutants to investigate the role of ethylene in the timing of leaf senescence. Delayed leaf senescence was observed
but when it did occur it was associated with wild-type levels of senescenceassociated gene mRNAs. It was concluded that ethylene was neither necessary nor sufficient to cause leaf senescence, and that it only influenced
the timing.
17.
O’Neill S, Nadeau JA, Zhang XS, Bui AQ, Halevey AH: Interorgan regulation of ethylene biosynthetic genes by pollination.
Plant Cell 1993, 5:419-432.
18.
Thomas H, Smart CM: Crops that stay green. Ann Appl Biol
1993, 123:193-219.
19.
Guiamet JJ, Giannibelli MV: Nuclear and cytoplasmic ‘stay-green’
mutations of soybean alter the loss of leaf soluble proteins
during senescence. Physiol Plan 1996, 96:655-661.
The evolutionary basis of leaf senescence: method to the
madness?
Anthony B Bleecker
Recent studies on the differential expression of genes
associated with leaf senescence support the long-standing
interpretation of plant senescence as an organized, genetically
controlled process. Sequence identities of genes that are
differentially expressed in senescing leaves indicate roles in
the salvage of nutrients. By considering this salvage function
as the selected trait and the degeneration and death of the
tissue a pleiotropic consequence of nutrient redistribution,
the process of leaf senescence can be reconciled with
evolutionary theories on the origins of senescence in animals.
Addresses
Botany Department, 430 Lincoln Drive, University of
Wisconsin-Madison, Madison, WI 50706, USA; e-mail:
Bleecker@facstaff.wisc.edu
Current Opinion in Plant Biology 1998, 1:73–78
http://biomednet.com/elecref/1369526600100073
Current Biology Ltd ISSN 1369-5266
Abbreviation
SAG
senescence-associated gene
Introduction
Understanding the decline in vitality that characterizes the
final stages in the life histories of most higher organisms
may represent one of the greatest challenges to biological
science and medicine. Yet, the field of senescence research
struggles to define even the terms under which it should
operate [1]. Is senescence the direct result of genetic
programming, or is it the opposite — a general breakdown
in systems that have passed the age where natural selective
forces operate to fine tune them?
Much of the debate surrounding the nature of senescence
is focused on animal models. The plant kingdom, however,
provides its own set of unique properties and problems
with respect to senescence. The apparent ability of some
plant species to live indefinitely and the prevailing opinion
that even somatic tissue senescence is a genetically programmed process have set the study of plant senescence
apart from the animal field [2••]. Have plants somehow
escaped from the evolutionary constraints that have made
limited lifespans a fact of life for most animals?
In this article, I will attempt to reconcile the apparent
differences in how senescence in plants and animals is
viewed from an evolutionary perspective. To this end, I
will briefly summarize evolutionary theories that account
for the prevalence of senescence in animals. I will then
discuss some problems with comparing plant and animal
life histories that arise from basic differences in the way
that plants and animals develop. Finally, I will suggest how
the apparent programmed nature of leaf senescence can be
reconciled with evolutionary theories of animal senescence
by considering the individual leaf as the organizational
unit on which selective forces have acted to create the
senescence syndrome.
Senescence in animals and plants:
definitional dichotomy?
In order to consider the evolutionary origin of senescence
in plants, some clarification of what is meant by the
term senescence is necessary. This is a particular problem
when discussing the relationship between senescence in
plants and animals because the term senescence has
been defined in different ways for these two classes of
organisms. In an attempt to clarify this issue, I will first
present a brief summary of the evolution-based definition
of senescence that was developed from animal models
but should apply to all higher organisms. I will then
consider how the unique features of plants have led to
some confusion in attempts to reconcile the evolutionary
theories of senescence developed for animals with the
developmental definition of senescence that is most often
used to describe the process in plants.
The term ‘senescence’ and the related term ‘aging’ have
multiple meanings and so must be defined carefully for
any specific discussion. Finch [1] cautions against the
use of the term aging for any purpose and discusses
using the term senescence to represent the decline in
survival and reproduction associated with advancing age.
While specific determinants of lifespan may be very
different for different species, the evolutionary forces
that shape life history patterns may be common to most
higher forms of life that have defined reproductive phases.
The evolutionary perspective may be summarized as
follows: most organisms have evolved in environments
where mortality is caused by external factors rather
than old age. For any specific species, natural selection
will operate to enhance reproductive output within the
context of this extrinsically imposed lifespan. The lucky
individuals who live well beyond this expected lifespan
will have exited from Darwinian design space; their
survival mechanisms will not have been fined tuned by
natural selection. As reviewed by Finch [1], the idea that
late acting genetic defects would not be eliminated by
natural selection and could thus accumulate and contribute
to senescence was first proposed by JB Haldane in
1941. Subsequently, GC Williams suggested that genes
which have a positive influence on reproduction but a
negative influence on postreproductive survival would be
favored by natural selection. This idea of antagonistic
74
Growth and development
pleiotropy was discussed more recently by Rose [3]. A
different perspective was provided by the ‘disposable
soma’ hypothesis [4], which posits that an organism’s
maximum life span will reflect a tradeoff between the
allocation of resources for the maintenance of somatic
tissues of the adult and the preservation of the germline
through the production of offspring. Given the greater
importance of reproduction for survival of the genome,
longevity of the individual is the inevitable loser.
This being the case, evolutionary theorists have had
difficulty considering how such an active suicide program
could have evolved in plants. Wilson [9••] considered
several alternative explanations for the evolution of
programmed senescence in plants, but was unable to
develop a convincing hypothesis. On the other hand, my
co-workers and I have suggested that leaf senescence in
Arabidopsis may be best explained using the concepts of
antagonistic pleiotropy and the disposable soma [10].
The concepts of antagonistic pleiotropy and the disposable
soma were developed from the study of animal systems
where the soma is largely composed of differentiated,
postmitotic tissues and where the germline is set aside
early in development. Plants, however, present particular
problems when attempting to apply the zoologically
derived definition of senescence. The modular nature of
plant growth and development and the propensity for vegetative reproduction lead to difficulties in defining where
an individual plant begins and ends. Even in the clearest
cases of individual plants, the semiautonomous nature
of plant organ systems presents difficulties in assigning
a specific time of death for the whole organism. These
attributes have caused scientists to make a distinction
between a gamet, which represents all structures arising
from a single seed, and a ramet, which represents some
identifiable somatic structure as an individual (see [2••]).
Individual shoot systems arising from an underground root
system may be defined as ramets, and this definition has
even been extended to the point where a single shoot
may be thought of as a population of ramets composed of
individual nodes [5]. From an evolutionary point of view
it may be more appropriate to consider the life history
of an individual leaf — a terminally differentiated, fairly
autonomous entity — when attempting to reconcile the
similarities and differences between plants and animals.
The question of whether leaf senescence is related to
the zoological definition of senescence or is strictly a
genetically regulated progression of events is not just an
academic one. The current emphasis on differential gene
expression as a paradigm for the study of leaf senescence is
predicated on the underlying assumption that senescence
is a developmentally controlled phenomenon. If this
assumption is essentially correct, then we can hope
that molecular and genetic strategies will succeed in
defining the underlying regulatory pathways that govern
the process. If, on the other hand, leaf senescence is to
some degree driven by the less well defined processes that
are thought to contribute to the evolution of senescence in
animals, then we might anticipate a more difficult time in
sorting out the adaptive processes from chaotic events that
are occurring because of the absence of selection pressure
acting on the system.
A second source of possible confusion with respect to
plants is a semantic one. The term senescence has
been used for many years in the plant literature to
refer specifically to an orderly progression of genetically
controlled events that lead to the degeneration and death
of leaf tissues. Plant scientists have tended to emphasize
the developmental aspects of leaf senescence, often using
the term programmed senescence [2••,6••–8••]. The clear
implication is that this programmed senescence is more
analogous to programmed cell death or apoptosis than
to the formal definition of senescence as a decline in
function related to age. This interpretation is fueled by
experimental evidence that the timing of leaf senescence
can be influenced by hormonal and other developmental
processes [2••,6••,7••] and by the long-standing evidence
that gene expression is required for the senescence
process (see [2••]). The recent that leaf senescence is
developmentally regulated so permeates the literature that
several authors have dismissed the notion that leaf senescence is related to the formal definition of evolutionary
senescence as an age-related decline in function[1,2••,5].
Developmental aspects of the senescence
syndrome in leaves
Natural leaf senescence follows a predictable progression
of events that are collectively referred to as the senescence
syndrome (for recent reviews see [2••,11•]. Ultrastructural changes are first noted in chloroplasts, where the
breakdown of thylakoid membranes is associated with
the visible loss of chlorophyll at the whole leaf level
and a decrease in levels of chloroplast proteins at the
biochemical level. In conjunction with the breakdown
in chloroplast internal structure, decreases in cytoplasmic
volume and in the number of cytoplasmic ribosomes are
often noted. By contrast, the integrity of the plasma
membrane, mitochondria and the nucleus is maintained
until very late in the senescence process. The breakdown
of chloroplast proteins and lipids is associated with a loss
of carbon and nitrogen from the leaf as it senesces. The
senescence syndrome, therefore, is interpreted in terms of
nutrient salvage. Several lines of evidence indicate that
this nutrient salvage system is a developmentally regulated
program. Enucleation of the cell blocks chloroplast degeneration, as do inhibitors of protein and RNA synthesis (see
[2••,6••]). Chloroplast degeneration is also reversible in
some experimental systems [2••]. These observations have
led to the recent interest in applying the techniques of
molecular biology to define the role that differential gene
expression may be playing in the senescence syndrome.
A number of research groups have used recombinant
DNA techniques involving differential and subtractive
The evolutionary basis of leaf senescence Bleecker
75
hybridization to identify cDNA clones that represent
genes that are differentially expressed during senescence.
Recent reviews provide detailed surveys of sequenced
genes and their expression patterns [2••,6••–8••,11•], so
I will only provide a brief summary here. Three broad
classes of cDNAs can be seen based on expression
patterns: first, those that decrease in relative abundance;
second, those that show little change in relative abundance; and third, those that increase in relative abundance
as senescence progresses. A caveat to all of these studies
is the use of total RNA to determine relative mRNA
abundance which can be misleading when one considers
that total RNA declines significantly during senescence.
This problem has been addressed in some studies by
calculating mRNA abundance on a per leaf basis [10,12].
Alternatively, if specific transcription factors are required
at all, they may be present in nonsenescing cells and
activated by whatever decision-making machinery must by
definition be present in presenescent tissues. It is even
conceivable that decreased expression of transcriptional
repressors is the key regulatory event. In any case,
sequence analysis of some SAG 5′ regulatory regions has
not revealed any common sequence elements between
different SAGs [6••,7••]. Taken together with the wide
range of expression patterns observed for SAGs, these
results support the idea that the proximal regulation
of gene expression associated with senescence may be
complex [6••,8••,9••]. This may also be why mutational
analysis in Arabidopsis has yet to provide any mutants that
block the senescence process [13••].
Many of the genes classified as senescence-associated
genes (SAGs) are expressed in green tissues and increase
in relative abundance at later stages of senescence. Some
of these may simply be genes whose levels of expression
are maintained in cells while levels of most mRNA classes
and rRNAs are declining. A smaller set of cloned cDNAs
represents genes that are more clearly expressed only in
senescing cells [7••,12]. The distinction between these
two sets of genes may be important in that although
the former may increase in relative abundance during
senescence (as a consequence of message stability), the
latter are better candidates as genes that are transcriptionally activated during senescence. Attempts to study
expression patterns of SAGs in detail led in one case to the
classification of nine different patterns of expression [7••].
This level of complexity may reflect the operation of many
different pathways operating by different mechanisms.
Lacking a clearly developed picture for proximal regulatory systems, I turn now to the consideration of higher
order regulatory systems that appear to control the timing
and progression of leaf senescence. Reminiscent of the
proverbial blind men and the elephant, one’s concept of
how leaf senescence is controlled depends very much
on which plant system one is examining. The relevant
systems have been the subjects of recent reviews so I will
just mention them briefly here. There are clearly examples
where specific hormones have a controlling influence
over organ senescence. Cytokinins can have a dramatic
effect on delaying leaf senescence in some species [14].
The effectiveness of applied cytokinin, however, varies
considerably between plant species. Ethylene promotes
senescence in many species but several recent studies
indicate that ethylene is neither necessary nor sufficient
to cause senescence in Arabidopsis or tomato [15,16•].
On the other hand ethylene is the key regulatory factor
in the senescence of floral organs in some species [17].
Environmental signals can also trigger senescence. Shading of lower leaves by upper leaves induces senescence
in some species (see [6••]), while deciduous trees are
affected by temperature and day length. Reproductive
development can trigger senescence of vegetative tissue
both proximally and even on a global scale in monocarpic
species. Evidence from soybean is consistent with a
chemical communication system between fruits and leaves
that triggers the senescence syndrome [2••]. Finally, leaf
age may be the best predictor of when senescence will
occur; this seems to be the case in Arabidopsis [10].
Sequence analysis of SAGs has resulted in the identification of a number of genes that are likely to be
involved in salvage functions [2••,6••–8••,11•]. These
include genes encoding proteases, nucleases, lipid- ,
carbohydrate- and nitrogen-metabolizing enzymes and
other enzymes involved in mobilization of nutrients.
Another class of sequences appears to code for protective
or stress response functions [7••]. The latter may act
to protect the increasingly fragile cell while the task of
salvage is being completed, or they may simply respond
blindly to the trauma caused by salvage and perform
no adaptive function at all. Finally, many cloned SAG
sequences have no obvious role in salvage or protection
[7••,11•]. Is the expression of these genes significant or
simply the molecular ramblings of cells going senile?
One class of genes that are conspicuously absent from
SAG populations is those with obvious gene-regulatory
functions. For example, no transcription factor candidates
have been reported. It is possible that messages for
differentially expressed transcription factors are present
but too rare to have been picked up by current techniques.
A key point here is that a multiplicity of factors may
influence the timing of leaf senescence, but none of them
applies to all cases. At the same time, the senescence
syndrome these signals are acting on is quite similar
in widely different plant species. Also, the senescence
syndrome includes the differential expression of related
suites of genes. To consider how this situation might have
arisen, I will return to the discussion of the evolutionary
basis of leaf senescence.
76
Growth and development
Reconciling the evolutionary origin of
senescence in plants and animals
In considering the evolutionary origin of leaf senescence, I propose that the senescence syndrome, or more
specifically the salvage system that it represents, is a
primitive set of pathways that were recruited early in
the evolution of land plants because these biochemical
pathways contributed to the retention of nutrients by
the whole plant. I use the term recruited because it
seems plausible that the biochemical activities required for
the operation of the senescence syndrome were already
functioning at reduced levels as a component of cellular
maintenance. This may explain why so many SAGs are
still expressed at lower levels in healthy tissue. Perhaps
the senescence syndrome evolved by mechanisms that
shifted the balance of anabolic and catabolic components
of cell metabolism in favor of catabolism. A key element
of this proposal is the idea that the senescence syndrome
was originally selected to salvage nutrients, not to cause
the death of the tissue in which it is expressed.
It is my contention that the many facets of the senescence
syndrome discussed above can be brought into perspective
and reconciled with the evolutionary theories of senescence developed for animal systems if one considers the
individual leaf as the organizational unit on which natural
selection acted thus creating the senescence syndrome.
Obviously, the somatic tissues of the leaf do not contribute
directly to the future of the genetic line, but then, neither
do the somatic tissues of an animal. Leaves do provide
an indirect contribution to the genetic line in the form
of photosynthetic assimilates. One would expect natural
selection to favor the continued survival of a leaf as long
as this assimilatory function is operable.
Despite this expectation a variety of environmental and
developmental factors may limit the functional ‘life
expectancy’ of a leaf. Predation, sporadic and seasonal
climate extremes, and competition for light — both from
competing plants and ultimately from continued growth
of the parent shoot — may contribute to a diminishing
capacity of a leaf to maintain photosynthetic output.
According to the disposable soma hypothesis [4] it is
unlikely that natural selection would favor maintaining
leaves in a healthy state when they age beyond the
functional life expectancy imposed by these external
factors. One would expect that natural selection would
favor the evolution of salvage pathways that are either
activated or enhanced as leaves approach this maximum
functional life expectancy because these salvage systems
would produce a continued contribution to the plant in the
form of salvaged nutrients.
The massive nutrient salvage associated with the senescence syndrome and cell maintenance are not compatible
programs. A pleiotropic consequence of the salvage
pathways is that their activities tend to increase the
mortality rate of the tissues in which they are expressed.
Natural selection will not have a correcting influence
on these negative consequences of salvage if the leaves
at that stage have a low probability of contributing to
reproduction via photosynthesis. In other words, salvage
pathway genes fit the theory of antagonistic pleiotropy
[1,4]. They were selected during evolution for their
contributions to reproductive success, but have a negative
impact on the longevity of the somatic tissues in which
they operate.
Cell death: developmental program or
gratuitous pogrom?
If one accepts the idea that the primal function of the
senescence syndrome was salvage, then the subsequent
death of the leaf could be considered a consequence of the
lack of selection for continued survival. From this point
of view, the senescence syndrome cannot be considered
a cell death program, although this extreme theoretical
viewpoint only considers positive contributions of the leaf
to the whole plant. A leaf that is left in a weakened
state as a result of salvage could become a liability to
the whole plant, for example, as a target for pathogen
invasion. In this case, evolutionary forces could select for
pathways that deliver the coup de grace to senile leaves.
Such pathways could be selected by recruitment of specific
subroutines within the overall syndrome. They could also
evolve as completely different developmental programs,
the abscission process being the primary example [10].
The plant leaf is a semiautonomous unit. It receives
information from its own internal processes and directly
from the environment. The leaf also receives chemical
signals from the parent plant that carry information
as to the nutritional and developmental status of the
plant. Information processing networks that have evolved
within the leaf could couple any combination of these
signals to cause the activation of salvage pathways. The
developmental control of these salvage pathways opens
the possibility that they could be co-opted by evolution
to function more directly in programmed cell death.
For example, the rapid senescence of floral displays
after fertilization [18] may have been selected more as
a protection against predators than as a mechanism of
salvage. Even the monocarpic senescence of crop plants
like soybean and pea [19] could be the result of selective
breeding for ease of human harvest; in which case the
target of selection would be the global death of vegetative
tissues rather than salvage.
Conclusion
I have argued that the senescence syndrome in leaves,
while clearly a developmentally controlled program, can
be reconciled with evolutionary theories of senescence
in animals if one considers the leaf as the organizational
level at which natural selection acts. This simplifies the
comparison of plant and animal systems because both
systems are essentially postmitotic highly differentiated
systems. The programmed nature of the senescence
The evolutionary basis of leaf senescence Bleecker
syndrome is explained if one assumes that the adaptive
significance of the syndrome is in nutrient salvage and that
the associated cell death is a pleiotropic consequence of
the program. Once these salvage pathways are in place,
however, they could be co-opted by natural selection to
function more directly in the death of tissues and organ
systems.
The study of gene expression associated with senescence
indicates that the process is multigenic and complex. No
clear picture of the genetic regulatory mechanisms that
that drive the process has yet emerged out of these studies.
The overall syndrome may best be viewed as a collection
of parallel and branched regulatory pathways that may
form a regulatory grid. These salvage pathways may be
activated when the leaf no longer contributes sufficiently
to photosynthetic function, or they may be coupled to developmental signals that activate programmed senescence
in otherwise healthy tissues.
Challenges facing the study of leaf senescence involve
characterizing the various pathways and the specific
functions they regulate. The genetic approach provides
the greatest promise to produce definitive answers in this
regard. Mutations in SAG genes and in the pathways that
regulate them will help to sort out the different regulatory
pathways involved. Various approaches for achieving this
goal using Arabidopsis as a model system have been
discussed [6••,10]. Specific examples where genetics
has provided interesting insights include the stay-green
mutants in Festuca [18], which are blocked in the turnover
of chlorophyll in the thylakoid membranes but otherwise
show most aspects of the senescence syndrome. In
soybean, mutations at two loci, designated d1 and d2,
cause a delay in leaf senescence. A maternally inherited
mutation, cytG, has a similar effect. The combination of
these mutants appears to block the ability of reproductive
structures to trigger the senescence syndrome in otherwise healthy soybean leaves [2••,19]. Interestingly, these
mutations do not block the activation of abscission in
these leaves. These examples demonstrate that mutations
which affect specific subroutines or signalling pathways
associated with the overall senescence syndrome can help
to unravel the complexities of senescence in plants.
apply. This may seem true from a strictly whole-plant perspective, but not
when one considers the individual leaf as a unit of selection.
3.
Kirkwood TB, Rose MR: Evolution of senescence: late survival
sacrificed for reproduction. Philos Trans R Soc Lond 1991,
332:15-24.
The authors provide an interesting and readable discussion of two prominent
theories that account for the evolution of senescence in animals: antagonistic
pleiotropy and the disposable soma.
5.
1.
Finch CE: Longevity, Senescence, and the Genome. Chicago:
University of Chicago Press: 1990.
Noodén LD, Guiamet JJ: Genetic control of senescence and
aging in plants. In Handbook of the Biology of Aging. Fourth
edition. Edited by Schneider EL, Rowe JW. San Diego: Academic
Press; 1996:94-118.
The authors provide a summary of the field of plant senescence from several
perspectives and include a survey of genes that are differentially expressed
during senescence. They argue that, because leaves may senesce before
or during reproduction, evolutionary models for animal senescence do not
Roach DA: Evolutionary senescence in plants. Genetica 1993,
91:53-64.
6.
Gan S, Amasino RM: Making sense of senescence. Plant Physiol
••
1997, 113:313-319.
This recent review of leaf senescence both considers the recent studies
on gene expression and summarizes the developmental and environmental
pathways that influence the timing of senescence in different systems. The
senescence syndrome is presented as a form of programmed cell death,
but the authors do consider the apparent complexity of regulatory factors
that may operate in the syndrome and suggest a network of parallel and
overlapping pathways that control the process (Figure 3).
7.
Buchanan-Wollaston V: The molecular biology of leaf
••
senescence. J Exp Biol 1997, 307:181-199.
The author focuses on the analysis of differential gene expression during
leaf senescence. This is perhaps the most thorough of recent reviews on
this topic. A flow chart of salvage pathways thought to be active during
leaf senescence is provided and reconciled with the identities of many
senescence-associated gene clones. An attempt is made to classify genes
according to their expression patterns, of which 10 different classes are
identified. It is recognized that the complexity of expression patterns may
indicate a plethora of regulatory pathways. Yet, the author is convinced that
transcriptional control is the key to senescence and that all genes which are
differentially regulated must be important to the process.
8.
Nam HG: The molecular genetic analysis of leaf senescence.
••
Curr Opin Biotechnol 1997, 8:200-207.
In the same vein as other recent reviews [7••], the author use gene expression as the paradigm of control. An emphasis is placed here on the idea
that hormonal and developmental pathways overlap in controlling different
senescence-associated genes (SAGs) and that different forms of senescence (starvation induced, hormonally induced and age related) show differences in which SAGs are elevated. In the conclusion, the importance of
considering post-transcriptional mechanisms for SAG abundance is emphasized. Examples where mRNA and protein abundance data do not necessarily agree are also noted as a cautionary point.
9.
Wilson BJ: An evolutionary perspective on the ‘death hormone’
••
hypothesis in plants. Physiol Plant 1997, 99:511-516.
The author considers the problem of how a developmental system that
causes death could have evolved. Selection at several different levels is considered and the author concludes that nutrient competition between leaves
and fruits is the best candidate. Wilson discounts this mechanism, however,
because even old leaves are not net importers so their death is of no consequence; and also, monocarpic varieties do not show a consistent advantage
over their polycarpic relatives in terms of yield. To the first argument, I would
respond that export from older leaves, not competition for import, is the issue.
Release of stored nitrogen and other nutrients from otherwise unproductive
leaves is the trait under consideration. The second argument, therefore, is
based on flawed experiments. Comparing varieties with multiple genetic differences in species that have been artificially selected by humans and grown
under specialized protected conditions is not likely to be the criterion that
evolutionary processes would use in selecting the trait.
10.
• of special interest
•• of outstanding interest
Rose MR: Evolutionary Biology of Aging. Oxford: Oxford University
Press; 1991.
4.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
77
Hensel LL, Grbic V, Baumgarten DA, Bleecker AB: Developmental
and age related processes that influence the longevity and
senescence of photosynthetic tissues in Arabidopsis. Plant Cell
1993, 5:553-564.
11.
•
Weaver LM, Himelblau E and Amasino RM: Leaf senescence:
gene expression and regulation. In Genetic Engineering, V.19:
Principles and Methods. New York: Plenum; in press.
This is a thorough review of leaf senescence that considers primarily the
biochemical and molecular aspects of the process.
12.
2.
••
13.
••
Lohman KN, Gan S, John MC, Amasino RM: Molecular analysis
of natural leaf senescence in Arabidopsis thaliana. Physiol
Plant 1994, 92:322-328.
Bleecker AB, Patterson SE: Last exit: senescence, abscission
and meristem arrest in Arabidopsis. Plant Cell 1997, 9:11691179.
This review focuses on Arabidopsis as a model system for the study of
senescence and abscission. It includes considerations of somatic tissue
senescence and the growth arrest of meristems that contribute to whole
78
Growth and development
plant senescence. Theoretical discussions relevant to this paper are also
included.
14.
Gan S and Amasino RM: Inhibition of leaf senescence by autoregulated production of cytokinin. Science 1995, 270:19861988.
15.
John I, Drake R, Farrell A, Cooper W, Lee P, Horton P, Grierson
D: Delayed leaf senescence in ethylene deficient ACC-oxidase
antisense tomato plants. Molecular and physiological aspects.
Plant J 1995, 7:483-490.
16.
Grbic V, Bleecker AB: Ethylene regulates the timing of leaf
•
senescence in Arabidopsis. Plant J 1996, 8:595-602.
The authors use ethylene insensitive mutants to investigate the role of ethylene in the timing of leaf senescence. Delayed leaf senescence was observed
but when it did occur it was associated with wild-type levels of senescenceassociated gene mRNAs. It was concluded that ethylene was neither necessary nor sufficient to cause leaf senescence, and that it only influenced
the timing.
17.
O’Neill S, Nadeau JA, Zhang XS, Bui AQ, Halevey AH: Interorgan regulation of ethylene biosynthetic genes by pollination.
Plant Cell 1993, 5:419-432.
18.
Thomas H, Smart CM: Crops that stay green. Ann Appl Biol
1993, 123:193-219.
19.
Guiamet JJ, Giannibelli MV: Nuclear and cytoplasmic ‘stay-green’
mutations of soybean alter the loss of leaf soluble proteins
during senescence. Physiol Plan 1996, 96:655-661.