University of Groningen Molecular aspects of ageing and the onset of leaf senescence Schippers, Jozefus Hendrikus Maria IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2008 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Schippers, J. H. M. (2008). Molecular aspects of ageing and the onset of leaf senescence. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 27-05-2021
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University of Groningen
Molecular aspects of ageing and the onset of leaf senescenceSchippers, Jozefus Hendrikus Maria
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.
Document VersionPublisher's PDF, also known as Version of record
Publication date:2008
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):Schippers, J. H. M. (2008). Molecular aspects of ageing and the onset of leaf senescence. s.n.
CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.
Total 827 385 335 257 99 110 Data sources: Buchanan-Wollaston et al. (2005); C/N: carbon and nitrogen supply (Expression patterns of genes induced by sugar accumulation during early leaf senescence; Zimmerman et al., 2004).
The most frequently used SAG to monitor developmental senescence, and perhaps
one of the few SAGs which is specifically induced by developmental senescence, is
SAG12. SAG12 transcripts were found to be very low or below the detection level in
young and mature green leaves, contrasting to the levels of the transcripts of SAG13
and SAG14 (Figure 7.1; Lohman et al., 1994). Unlike other SAGs, including SAG13,
SEN1 and SAG14 whose expression could be enhanced in young leaves by a range
of senescence-inducing treatments such as detachment, hormonal exposure,
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darkness, drought, wounding and pathogen challenge, SAG12 was only occasionally
found to change its expression under these circumstances (Oh et al., 1997; Park et
al., 1998; Weaver et al., 1998; Noh and Amasino, 1999; Brodersen et al., 2002).
Figure 1. SAG12 and SAG13 expression during Arabidopsis development. Expression levels
of both SAG12 and SAG13 are increased during senescence. In contrast to SAG12, basal
SAG13 expression levels are present throughout development. Data source:
GENEVESTIGATOR (Zimmermann et al., 2004).
Thus, SAG12 is considered the best marker for developmental senescence that
relies on leaf age, whereas SAG13 and SAG14 may represent stress-induced
senescence or general cell-death markers. That the SAG12 promoter has been used
for the autoregulated production of cytokinin to delay senescence in a number of
species including tobacco (Gan and Amasino, 1995; Ori et al., 1999), lettuce
(McCabe et al., 2001), petunia (Chang et al., 2003) and Arabidopsis (Huynh et al.,
2005) suggests that the developmental senescence regulation of SAG12 is
conserved across species. Moreover, a conserved cis-element of the SAG12
promoter was also found in the Asparagus officinalis asparagine synthetase promoter
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and was responsible for the induction of transcription of this gene by senescence
(Winichayakul et al., 2004). Thus, monocotyledonous and dicotyledonous plants
appear to share this senescence cis-element, further confirming the conservation of
the regulation of developmental senescence across species. Extensive studies on
the expression of SAGs, including SAG12, have provided exciting new insights into
the developmental regulation of senescence, and future research will likely result in a
better understanding of developmental senescence.
Integrating hormonal action into developmental senescence
Reproduction has specific timing and all the programs need to be timely in place to
ensure successful reproduction. The indirect consequence is that the various
strategies embedded in the programs will initiate developmental senescence in an
age-dependent manner. Thus, developmental senescence is the consequence of
time-specific action of genes. Understanding the timing of the various senescence
strategies is a necessary step for elucidating the molecular mechanisms of
developmental senescence. In this section we intend to put together the action of the
hormones that control leaf senescence and thus developmental ageing in
Arabidopsis.
Previously, we proposed a senescence window concept to explain the involvement of
ethylene in leaf senescence (Jing et al., 2002, 2003). Depending on whether and
how senescence can be induced by ethylene, the life span of a leaf can be split into
three distinct phases (Figure 2A). The experimental evidence supporting this view is
briefly summarized as follows. (1) When plants were exposed to a short-pulse (e.g.
1–3 days) ethylene treatment, no senescence symptoms could be induced in young
leaves (Grbić and Bleecker, 1995;Weaver et al., 1998; Jing et al., 2002). (2) Leaf
senescence is not accelerated in the ctr1 mutants (Kieber et al., 1993). This indicated
that there exists a never-senescence phase in which senescence cannot be induced
by ethylene. (3) Furthermore, in a certain range of leaf ages, the effect of ethylene on
leaf senescence increases with the increase in leaf age (Grbić and Bleecker, 1995;
Weaver et al., 1998; Jing et al., 2002), indicative of an ethylene-dependent
senescence phase. (4) Finally, beyond certain leaf ages, senescence will start even
without the participation of ethylene as shown in the etr1 and ein2 mutants in which
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Figure 2. The senescence window concept. (A) The senescence window concept as
deduced from the effects of ethylene on leaf senescence. At early leaf development,
ethylene is not able to induce leaf senescence. This is the so-called never-senescence
phase in the model. Only after a certain developmental stage, ethylene can induce leaf
senescence, depending on the environmental conditions. Further development of the leaf will
always result in senescence, even in the absence of ethylene. (B) Hormonal action during
leaf development is age dependent. The action of the senescence-promoting hormones is
strongest at late developmental stages, and is antagonistic to that of the stay-green
hormones. The onset of leaf senescence is achieved by a depletion of the stay-green
hormones, concomitant with an increase in ethylene levels followed by JA, ABA and
eventually SA. Hormone levels and sensitivity change during development, as indicated by
the triangles. The age-related changes limit the action of the various plant hormones to their
own specific age window.
the senescence progresses normally once started (Grbić and Bleecker, 1995; Park et
al., 1998; Buchanan-Wollaston et al., 2005), which suggests the existence of an
ethylene-independent senescence phase. This senescence window concept
emphasizes the developmental control of leaf senescence and considers leaf age as
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an ultimate determinant of senescence progression. Clearly, genes that control the
phase transitions of the senescence window are important for the onset of
developmental senescence, and evidence suggests that many genetic loci are
required (Jing et al., 2002, 2005). Thus, the senescence window concept provides an
explanation why the senescence-promoting effect of ethylene is variable during
development.
The senescence window concept can, perhaps, integrate the action of all plant
hormones involved in leaf senescence. In Arabidopsis the different hormones seem
to control the onset and progression of senescence in an age-related manner. Figure
2B is an extension of the senescence window concept developed from the interaction
between leaf age and ethylene and shows a tentative model illustrating the timing
and action of the different hormones during developmental senescence. In this
model, age-related changes, and thus development, are considered the primary
regulator of leaf senescence. During ageing, developmental cues lead to the
diminished action of the senescence-retarding hormones such as auxin, GA and
cytokinins, as well as the concomitant strengthening of the action of senescence
enhancing hormones such as ethylene, JA, ABA and SA. The action of the different
hormones during the initiation of leaf senescence does not change suddenly but
gradually, allowing a gradual integration of all the hormones controlling the process.
This suggests that the senescence process is partly reversible by fine-tuning
hormone action and hence amenable for modulation.
The model provides a basis for the explanation of experimental data. For instance,
the major senescence-retarding compound cytokinin can delay senescence when its
level is maintained. However, in transgenic SAG12–IPT plants the senescence
process will start eventually and progresses normally (Gan and Amasino, 1995; Ori et
al., 1999), suggesting that cytokinin action is restricted to certain developmental
stages. On the other hand, cytokinin biosynthesis mutants showed a shorter leaf life
span (Masferrer et al., 2002). This might be explained by assuming that the effect of
the senescence-promoting hormones is antagonistic to those blocking senescence;
older leaves may become less sensitive for cytokinin and more sensitive for
senescence-promoting hormones like JA and ABA (Weaver et al., 1998). Similarly,
blocking the ethylene pathway increases leaf longevity. Finally, however, the leaves
go into senescence because the influence of JA, ABA and SA may increase with the
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age of the leaf. Thus, the age-related changes limit the action of the various
hormones to their own specific window.
Taken together, although plant hormones are almost universally involved in every
aspect of plant life, they may participate into developmental senescence only in very
specific age windows. The proposed senescence window concept and the model for
hormonal action provide a developmental view to examine the modulation of
developmental senescence by hormones, which certainly requires more experimental
evidence for validation.
Outlook and perspectives
Thanks to the availability of cutting-edge technology and the use of model species
with known whole-genome sequences that have enabled senescence studies to be
carried out at a scale that was not imaginable even 15 years ago, our knowledge on
the regulation of developmental senescence has been advanced tremendously. It is
clear that hormonal modulation, metabolic flux, ROS and protein degradation are the
major cellular and molecular processes that are important for senescence regulation.
Strikingly, these processes are embedded in the genome programs that regulate
plant life maintenance, responses to biotic and abiotic stresses, and growth and
development for the sake of successful reproduction. Thus, leaf senescence can be
viewed as an indirect consequence of genome optimization for reproduction. This
perspective is exciting and worthy of further exploitation, since it coincides with the
evolutionary theory of senescence developed from animal ageing studies. In-depth
molecular genetic studies are required to dress the evolutionary basis of leaf
senescence. In particular, identification of regulatory genes with pleiotropic functions
or late-life deleterious effects should be a priority for further senescence studies.
The complexity of leaf senescence is mainly due to the involvement of multiple
components that exhibit overlapping effects. This is particularly true for the action of
hormones. The proposed senescence window concept provides a theoretic
framework to dissect the action of hormones during senescence depending on their
time of action, which is important to separate the effect of hormones on senescence
from their other effects. Using this concept, it is possible to study genetic components
that control the action of hormones during development, which is an essential step for
ultimately understanding the mode of action of hormones during development.
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Combined with the genetic dissection, whole-genome analysis should be employed
to define the networking of various regulatory circuits.
In conclusion, senescence is one of the biological phenomena with extreme
complexity. In the current postgenome era, we are provided with both opportunities
and the challenge to dissect the molecular genetic mechanisms of leaf senescence.
The findings in the past have enabled us to look at senescence regulation from a
fresh perspective of genome optimization. We have evolutionary and developmental
theories that guard us to define the proper targets. We are also armed with cutting-
edge technologies and tools. Thus, a concerted effort will eventually unveil the
mystery of senescence regulation and provide a genetic basis for senescence
manipulation.
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