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YB100028.tex
McGraw-Hill 2010 YearBook of Science & Technology
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Article Title: Leaf senescence and autumn leaf coloration
Article ID: YB100028
1st Classification Number: 571110
2nd Classification Number: 571130
Sequence Number:
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Leaf senescence and autumn leaf coloration
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Leaf senescence and autumn leaf
coloration
When viewed by astronauts, Earth is the blue planet.
When imaged by Earth observation satellites, the
planet is green. This reflects the fact that water
and chlorophyll are the signatures of life in the
solar system. Satellite images show the green color
of vegetation ebbing and flowing with the seasons
(Fig. 1). A whole season of the year in temperate
regions is named for the fall of leaves that follows
the seasonal replacement of chlorophyll with the
yellows, oranges, reds, purples, and browns of autumn foliage. Such a global-scale biological event
must surely have a purpose and a mechanism. We
are now learning the how of color change in plants;
the why is more elusive, but new insights from genetics and evolutionary biology are providing possible
answers.
Light is essential for green plants, but can be harmful too. The small ephemeral weed Arabidopsis
thaliana is botany’s laboratory rat: a universally studied model organism that does just about everything
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July 2007
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Fapar Index
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Fig. 1. Photosynthetic pigments of foliage on a global scale, measured by the Envisat satellite in Fapar units (Fapar =
fraction of absorbed photosynthetically active radiation). The images are monthly averages comparing coverage in January
and July 2007, showing the extent of seasonal variation in chlorophyll, particularly in northern temperate regions. (Courtesy
of European Space Agency Envisat satellite, MERIS data)
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YB100028.tex
Leaf senescence and autumn leaf coloration
a flowering plant should do, in an experimentally
tractable way. Like those of trees and crop species, its
leaves develop into the green solar panels that power
growth through photosynthesis, then, when their
productive job is done, they initiate senescence, turn
yellow, and eventually die. There are many Arabidopsis mutants with alterations in genes controlling development, physiological function, and environmental response. Among these mutants is acd2, a genetic
variant that suffers from lesions on older leaves in the
light (Fig. 2). When the acd2 gene was finally cloned
and identified in 2001, it turned out to be an inactive
form of a gene encoding red chlorophyll catabolite
(RCC) reductase, an enzyme of chlorophyll breakdown. This provides a clue as to why plants take the
trouble to expend physiological energy on changing
the colors of leaves that are destined to die: chlorophyll and its derivatives, if not carefully processed
by organized biochemical pathways in green cells,
can be toxic when illuminated. The mutant’s name,
acd2, stands for accelerated cell death-2 and clearly
expresses the consequences of disrupting pigment
metabolism in senescing green tissues.
The behavior of acd2 can be understood in evolutionary terms by considering how certain single-cell
algae dispose of chlorophyll. If cultures of Chlorella
protothecoides growing photosynthetically in the
light are transferred to darkness and deprived of a
nitrogen source, they turn yellow by a process that
resembles the yellowing of senescing leaves. At the
same time, the culture medium accumulates a red
pigment that chemical analysis shows to be a chlorophyll derivative. A similar red chlorophyll catabolite
(RCC) is an intermediate in the metabolism of chlorophyll during leaf senescence (Fig. 2). RCC is potentially harmful because it generates reactive oxygen
species and free radicals that destroy the fabric of
living cells. Single-cell aquatic plants deal with the
threat from RCC by pumping it out of the cell. Multicellular land plants do not have this option and
have evolved a detoxification mechanism that begins with the conversion of RCC to a colorless product by RCC reductase. In the mutant acd2, RCC
reductase is missing. As a consequence, when
chlorophyll is degraded, RCC builds up and mediates cell death in the light. The ultimate destination
of the product of the RCC reductase reaction is the
central vacuole, the large membrane-limited aqueous
compartment that occupies most of the volume of
the green cell. Sequestering products out of harm’s
way in the vacuole is a further detoxification measure employed by land plants. It seems that the progression from green to yellow that is characteristic of
foliar senescence is a highly visible symptom of toxin
disposal.
Recycling is a way of life for green plants. If eliminating chlorophyll is a hazardous business requiring
stringent detoxification measures, why doesn’t the
plant simply abandon the pigment by dropping it unchanged within falling leaves? The answer is that the
removal of chlorophyll is associated with, and necessary for, the salvage of protein nitrogen from the
senescing leaf to support the development of young
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Chlorophyll-protein complexes of
the photosynthetic membrane
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protein released
for recycling
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chlorophyll b
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chlorophyll a
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phytol
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phytol
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phytol
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pheophorbide a
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phytol
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pheophytin a
RCC
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FCC
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chloroplast
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cytosol
various modifications
and conjugations
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vacuole
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Fig. 2. The cellular mechanism of chlorophyll breakdown in plant senescence. The
enzymes and transporters responsible for the sequence of biochemical transformations
are as follows: [1] stay-green; [2] chlorophyll b reductase; [3] dechelation reaction;
[4] pheophytinase; [5] pheophorbide a oxygenase; [6] RCC reductase; [7] ATP-dependent
catabolite transporter; and [8] ABC transporter. The Arabidopsis mutant, acd2, is blocked
at reaction [6] and suffers from light-dependent leaf lesions as a consequence of the
anomalous buildup of the normally transient phototoxic intermediate RCC.
(FCC = fluorescent chlorophyll catabolite.)
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YB100028.tex
Leaf senescence and autumn leaf coloration
organs or storage tissues. In many crops and natural
plant communities, nitrogen is an important limiting factor for growth and productivity. Senescence
evolved as a way of liquidating the investment of nitrogen in green tissues when they become old and
unproductive and reinvesting it in younger, betteradapted structures.
Most of the salvageable nitrogen in green cells is
located in the chloroplasts (cell plastids occurring
in the green parts of plants, containing chlorophyll
pigments, and functioning in photosynthesis and
protein synthesis). A large fraction of this protein
is bound to chlorophyll. Chlorophyll (and protein)
degradation begins with the controlled unpacking of
pigment-protein complexes (Fig. 2). Observations on
mutants indicate that nitrogen from pigment-binding
proteins cannot be released and relocated to destination tissues unless chlorophyll is removed. For
example, a mutant gene called stay-green (sgr) renders plants that carry it unable to deliver chlorophyll
from pigment-protein complexes to the chlorophyll
breakdown machinery. Such plants cannot mobilize
chlorophyll-associated protein, which remains more
or less unchanged in the leaf even as the nitrogen
from other proteins is being recycled during senescence.
Yellow pigments are revealed during senescence.
The picture that we are developing of color changes
in senescing leaves is of the controlled detachment
of chlorophylls from their nitrogen-rich binding proteins in chloroplast membranes, followed by a series of transformations via transient green and red
intermediates, culminating in colorless end products that accumulate in the cell vacuole (Fig. 2).
In ripening crops and many other species, green is
replaced by golden yellow. Carotenoids, the chemical group responsible for the yellow and orange
pigments of senescing foliage, are already present in green leaves and are unmasked as chlorophyll is removed. Some carotenoids are built into
chlorophyll-protein complexes. As the complexes
and chloroplast membranes are taken apart,
carotenoids coalesce in intensely colored lipid-rich
globules within the senescing chloroplast (Fig. 3).
Leaves tend not to make more carotenoids during
senescence; however, in other senescencelike processes such as the ripening of tomatoes, bell peppers, and other colorful fruit, substantial amounts of
new carotenoids may be synthesized. Carotenoids
are potent antioxidants, retained during leaf senescence as part of the cellular equipment defending
against photodamage.
Some senescing leaves turn red. In many regions
of the world, such as the forests of New England in
the United States, senescing leaves turn spectacularly
red. Anthocyanins, the chemical constituents commonly responsible for the fiery colors of autumnal
foliage, are water-soluble pigments that (in contrast
to the fat-soluble carotenoids) are actively synthesized by senescing photosynthetic tissues and accumulated in the vacuoles of leaf cells (Fig. 3). Genes
for carotenoid synthesis are extremely ancient, exhibiting a high degree of conservation from flower-
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ing plants all the way to unicellular organisms resembling those present at the origin of life. On the
other hand, recognizable genes for metabolism of
anthocyanin-like compounds do not occur until the
algae evolved, became integrated into development
only once land plants began to appear, and are characteristic of the relatively recent (in evolutionary
terms) flowering plant groups.
Autumn colors evolved to defend against a hostile environment. It has been suggested that anthocyanins
are sunblockers, defending vulnerable tissues from
the harmful effects of excess light. There is also evidence that anthocyanins can act as antioxidants. An
alternative or additional explanation for the origin of
foliar anthocyanin is coevolution. According to this
hypothesis, autumn coloration is a signal of quality,
directed at insects that migrate to the trees in autumn. The red color of foliage may be symptomatic
of the plant’s unsuitability as a host because of high
levels of chemical defenses, of poor nutritional status, of imminent leaf fall, or of any other characteristic that would induce a lower fitness in the insects.
Mathematical models based on signaling theory generally support the coevolution explanation and emphasize the significance of insect visual systems and
behavior and of the nature of the link between leaf
color, defense status, and plant vigor.
Outlook. In conclusion, researchers studying the
meaning of color in senescing leaves are able to enjoy the pleasures of engaging with biological events
that are both scientifically challenging and esthetically satisfying.
For background information see ABSCISSION;
CAROTENOID; CHLOROPHYLL; COLOR; DECIDUOUS
PLANTS; LEAF; PHOTOSYNTHESIS; PIGMENTATION;
PLANT ANATOMY; PLANT PHYSIOLOGY; PLANT PIGMENT in the McGraw-Hill Encyclopedia of Science
& Technology.
Howard Thomas
Key Words: plant, leaf, senescence, chlorophyll,
carotenoid, anthocyanin, autumn, color
Bibliography. M. Archetti et al., Unravelling the
evolution of autumn colours: An interdisciplinary
approach, Trends Ecol. Evol., 24:166–173, 2009;
H. Ougham et al., The control of chlorophyll
catabolism and the status of yellowing as a biomarker
of leaf senescence, Plant Biol., 10(suppl. 1):4–14,
2008; H. J. Ougham, P. Morris, and H. Thomas, The
colors of autumn leaves as symptoms of cellular recycling and defenses against environmental stresses,
Curr. Top. Dev. Biol., 66:135–160, 2005.
URLs
The Essence of Senescence
http://www.sidthomas.net/SenEssence/index.htm
Plant Biology: Senescence of Plant Leaves
http://www.plant-biology.com/Leaf-Senescence.php
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Chlorophyll degradation
reveals the yellow carotenoid
pigments that concentrate in
the plastoglobules of the
senescing chloroplast
Red anthocyanins are
water-soluble pigments that
accumulate in the central
vacuoles of the cells of
autumn leaves
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Fig. 3. Detail of the ultrastructure of a senescing cell showing the different locations of the yellow (carotenoid) and red
(anthocyanin) pigments of autumn leaves.