Vous êtes sur la page 1sur 16

TREE AND CLIMATE CHANGE: Photosynyhesis and Oxidative stress

Gabriel Camarena Gutirrez

Unidad de Morfologa y Funcin. FES Iztacala. UNAM. Av. De los Barrios # 1.
Los Reyes Iztacala. Tlalnepantla 54090. Mxico

The Intergovernmental Panel on Climate Change (IPCC) assessed the extent to

which recent observed changes in natural biological systems have been caused by
climate change. Organisms alter their gene expression and metabolism to increase
the concentrations of several antistress compounds and to change their
physiology, phenology, growth and reproduction in response to climate change.
Trees evolved to cope with excess energy and elevated concentration of reactive
oxigen species by activating photoprotective and antioxidative defence systems.
Cellular redox homeostasis is considered to be an integrator of information from
metabolism and the environment controlling plant growth and acclimation
responses, as well as cell suicide events.
Higher plants that dominate in terrestrial ecosystems have evolved multiple
adaptive strategies to survive and reproduce in the constantly changing
environment with respect to temperature, light, CO2 , water and nutrient status.
Integration of many signals into a comprehensive signalling network to coordinate
the regulation of growth and developmental processes under fluctuating
environmental conditions is the molecular basis for this flexible response.
Advances in our understanding of this mechanism rely on new concepts of
oxidative stress and redox signalling commonly attributed to a plant response to
environmental constraints.

The Intergovernmental Panel on Climate Change (IPCC) assessed the extent to
which recent observed changes in natural biological systems have been caused by
climate change. Most field biologists are convinced that they are already seeing
important biological impacts of climate change14,69; however, they have
encountered difficulty in convincing other academic disciplines, policy-makers and
the general public. Since 1900, concentration of CO 2 has risen from 290 mol mol-1
to 377 mol mol-1 in 2004 (Keeling & Whorf, 2005), and is currently increasing at a
rate of 1.5 (0.9-2.8) mol mol -1 a-1, which is mainly due to fossil fuel combustion
and deforestation (IPCC, 2001). The prediction is that CO 2 concentration will rise to
over 500 mol mol-1 by 2050 and to almost 700 mol mol-1 by 2100, which will
result in an increase in global average temperature of approximately 2.5 3.5 C
(IPCC, 2001) and forest regions at high latitudes can be heated by almost 10 C
(Christensen et al. 2007). Furthermore, since CO

has a potentially long

atmospheric residence time (5-200 years depending on the rate of uptake by

different removal processes, it can have a radiative forcing effect over decades,
centuries or millennia before natural processes can remove quantities that are
emitted (IPCC, 2001). So even if CO 2 emissions stabilised today, it would still take
a very long time before atmospheric CO2 concentrations would stabilise.
The El-Nio Southern Oscillation has been associated with drought-associated
mortality from the tropical moist forests of Borneo, Central America and the
Amazon, to temperate Nothofagus and Austrocedrus forests in Patagonia and
Terminalia forests in Venezuela (McDowell et al, 2008). In the northern
hemisphere, drought associated mortality has been observed from subboreal
China to tropical regions of Africa. In the temperate zone of Europe, drought
reduced net primary productivity and increased forest mortality. Likewise, regionalscale droughts in North America have recently been correlated with insect
outbreaks and associated mortality of both deciduous and conifer species (e.g
literature cited in McDowell et al, 2008). Widespread tree mortality associated with

drought, increased temperatures, and tree pest/pathogen outbreak is an emerging

threat of global change now documented across all six forested continents. Recent
die-off from tree mortality in western North America now affects over 605 000 km2
of coniferous forests from Mexico to Alaska (Allen et al., 2010). These rapid
changes may exceed the capacities of individuals, populations and communities to
assimilate them. Therefore, an immediate key question in the biology of global
change is how the Earth-life system is coping with this new situation. In this study
we summarize the results of experimental studies quantifying the effects of
elevated CO2, elevated temperature, and altered precipitation regimes on the
photosynthesis and oxidative stres on trees.
Plant productivity influences the functioning of ecosystems, fuels the global food
web, and is the foundation for some of the most diverse habitats in the world.
Vegetation also sustains humanity, directly providing oxygen, food, fiber, and fuel
(e.g., an estimated ~30%-40% of the biosphere production is currently consumed
or coopted by humans)

and indirectly supporting livelihoods through jobs and

revenue (Mora et al., 2015). However, plant growth is strongly limited by climate
variables such as air temperature, water availability, and solar radiation [1-4], which
are changing in response to ongoing climate change. Terrestrial plants have
evolved complex systems of water management and water conservation that utilize
a suite of adaptive morphological traits (e.g., small vessel elements, thick waxy
cuticles, low specific leaf areas) and physiological processes (e.g., hormonal
signaling, stomatal action), which collectively control plant-water relations and
drought-resistance. Large differences have developed among plant taxa in their
abilities to cope with moisture stress as a result of climate-related natural selection
(Bansal et al., 2015). Bansal et al, 2005 found there was also considerable genetic
variation in drought-resistance among populations originating along climate
gradients. They found that populations originating from warmer, drier climates
generally had lower values of transpiration, water deficit and SLA. Even though
populations from warm climates had relatively high drought-resistance, populations
originating from the coolest climates also exhibited increased drought- resistance.

In this study, we review evidence of current biological impacts of climate change,

the capacity of terrestrial organisms, populations, communities and ecosystemsto
cope with current climate change, and the upscaling of their responses, from the
molecular and genetic level to the levels of community, ecosystem and biosphere
accentuated by stress factors.

Most plant species only grow in a certain temperature range. Thus, some are likely
to adapt to warmer temperatures by changing their growth and development or by
shifting their ranges, provided that the optimum temperatures are not exceeded.
Some species may fail to adapt to this global change and may even become
extinct if the air temperature is too high. Because the leaf is the key organ
performing photosynthesis and transpiration, its development, which varies with
environmental factors, is an important determinant of total plant productivity
[Thomas et al.,

21204]. In a tree crown the leaves are a population whose

individual members have differentiated features and functions. The heterogeneity

of photosynthesis within the crown is primarily due to acclimation to local irradiance
and nitrogen allocation strategies (Yoshimura, 2010). The heterogenity of
photosynthesis es further accentuated by stress factors. The factors that influence
the response the most are probably the age of the leaves and the light available to
them. Gielen et al. (2007) have shown that, in adult Fagus sylvatica L. crowns,
visible symptoms and reduced photosynthetic efficiency affect only a thin layer of
leaves, exerting a limited effect on the crown as a whole.

Photosynthesis is a process by which plants, algae and photosynthetic bacteria

convert solar energy into chemical energy of organic molecules. The process in
plants and algae occurs in chloroplasts involving a series of photochemical and
biochemical reactions. The light energy absorbed by pigments initiates the

reactions leading to primary photochemical reactions associated with the two

photosystems: photosystem I (PS I) and photosystem II (PS II), that are
interconnected with several redox components. This is followed by reactions that
terminate in the production of stable organic compounds (Biswal et al., 2011).
Reports showing quantitative loss in photosynthetic pigments, differential changes
in chlorophyll a and chlorophyll b, remarkable changes in carotenoid composition in
general, and alteration in the composition of xanthophyll cycle pigments in
particular, in response to these stress factors are available in the literature. Among
all the components of the photosynthetic apparatus that are known as the targets
of stress, PS II and ribulose- 1,5-bisphosphate carboxylase oxygenase (Rubisco)
are considered as the major stress sensors. In natural environment, most of the
stresses are sensed by photosynthetic organisms through these components. PSI
is known to be relatively less sensitive, than PS II, to most stresses, but it is highly
sensitive to stresses such as freezing. Both PS I and PS II are photosensitive
devices which absorb photons, transfer them as excitons, trap them and convert
them to electrochemical energy resulting in photoredox reactions (Biswal et al.,
2011). They act in the timescale from femtoseconds to milliseconds. The
photoredox reactions result in the evolution of O 2 by the oxidation of water at the
Mn4Ca metal complex on the electron donor side of PS II and the reduction of
plastoquinone (PQ) to plastoquinol (PQH 2). The system tries to nullify the adverse
effects of the environment as far as possible. Most of the abiotic stresses ultimately
result in oxidative stress. Thus PS II senses the stress and transmits signals for
appropriate response. The most sensitive part of PS II is the metal centre at the
oxygen-evolving complex. Its high sensitivity is associated with the Mn cluster,
which forms stable metal centres with high oxidation states of Mn (III or IV). When
the plant is under stress, the weak interaction also results in the dissociation of
LHC II from the core pro- teins, i.e. D1, D2, Cytb559, 43 kDa (CP43) and 47 kDa
(CP47) polypeptides of the PS II complex. This dissociation may prevent further
photodamage of the PS II core polypeptides under stress. The mechanism of PS II
sens- ing of stress and adaptation to stress at the molecular level remains to be
fully understood (Biswal et al., 2011)

Air warming and soil drought may have very distinct effects on trees, and their
synergic impact remains unclear (Mittler 2006; Rennenberg et al. 2006).
Temperature can affect photosynthesis through modulation of the rates of activity
of photosynthetic enzymes and the electron transport chain (Sage & Kubien 2007)
and, in a more indirect manner, through leaf temperatures defining the magnitude
of the leaf-to- air vapour pressure difference, a key factor influencing stomatal
conductances. Photosynthetic response to soil drought and air warming is highly
complex. Air warming increases photosynthesis as long as the plant optimal
temperature is not exceeded; after that, photorespiration is stimulated and
photosynthesis inhibited (Berry & Bjo rkman 1980; Brooks & Farquhar 1985; Lea &
Leegood 1999). Moreover, high temperatures can directly affect different phases of
photosynthesis by inhibiting the activity of the both enzimes: ribulose- 1,5carboxylase/oxygenase as well as processes associated with the regeneration of
Rubiscos substrate, ribulose-1,5-bisphosphate (RuBP) through the Calvin cycle
and Rubisco activase enzyme, essential in Rubisco activation, and damage the
thermolabile photosystem II (PSII) (Haldimann & Feller 2004). Stomata open to
maximise dissipation of latent heat (Rennenberg et al. 2006). An increased
assimilation of carbon by plants, can be expected with an elevation of CO 2
concentration and this could increase the amount of carbon stored in vegetation
and below ground (i.e. roots and soil organic matter).

Temperature affects photosynthetic processes associated with light by altering

the pigment content, light-saturated photosynthetic rate, the apparent quantum
yield or photochemical efficiency of PSII and photoinhibition.
In herbaceous plants, the apparent quantum yield (the slope of the curve relating
CO2 uptake to absorbed light) generally decreases between about 15 and 35C.

However, in evergreen trees subject to winter inhibition of photosynthesis, quantum

yield changes during the year with seasonal variation in maximum photochemical
efficiency of PSII. This variation is largely explained by temperature and changes in
pigments of the xanthophyll cycle (Saxe yet al., 2001 ).
But, of course, how abiotic stress factors interact to affect plants will be key to
understanding climate change effects on plants; abiotic stress such as heat and
drought may contribute to plant susceptibility to pathogens or it may induce general
defense pathways which increase resistance. Elevated CO2 levels tend to result in
changed plant structure. At multiple scales, plant organs may increase in size:
Increased leaf area, increased leaf thickness, higher numbers of leaves, higher
total leaf area per plant, and stems and branches with greater diameter have been
observed under elevated CO2 When high-temperature stress is exacerbated, plant
responses may be similar to those induced by water stress, with symptoms
including wilt-ing, leaf burn, leaf folding, and abscission, and physiological
responses including changes in RNA metabolism and protein synthesis, enzymes,
isoenzymes, and plant growth hormones {Garrett 2006}.

Reactive oxigen species

Temperature stress is known to induce plants to produce reactive oxygen species
(ROS) and malondialdehyde (MDA), which can damage both the leaf structure and
function [15,16]. To alleviate the damage, plants generally enhance the production
of reactive oxigen species scavenging enzymes, such as superoxide dismutase
(SOD) and catalase (CAT), and osmoprotectants like proline and carbohydrates .
One of the most important antioxidant enzymes of the first line of defence against
ROS is superoxide dismutase (SOD). SOD converts superoxide anion radical (O2
) to hydrogen peroxide and oxygen. Based on the metals present at the active site
of an enzyme three main classes of SOD have been identified: iron (Fe-SOD),
manganese (Mn-SOD) and copper/zinc (Cu/Zn-SOD) (Alscher et al. , 2002). The

Mn-SOD and Fe-SOD are phylogenetically related to each other and they are very
similar in their primary and tertiary structures, whereas Cu/Zn-SOD shows different
structural features (Fink & Scandalios, 2002). Foyer and Allen (2003) suggest that
redox signalling was the first type of sensory regulation that evolved in nature.
Sequence similarities in higher plants to cyanobacterial redox signalling
components indicate homology and suggest conserved sensory and signalling
functions (Forsberg et al., 2001). Photosynthetic organisms have perfected the art
of redox control. It is now widely accepted that redox signals are key regulators of
plant metabolism, morphology, development, growth, and eventual death (Foyer &
Allen, 2003). One of the major ways in which plants transmit information about the
changing environmental factors is the ROS sensing, producing and scavenging
system. Abiotic and biotic stressors regardless of the first target site of their action,
affect the cellular balance between different redox buffers and oxidants, called
redox homeostasis (Apel & Hirt, 2004; Dizengremel et al. , 2009). A lot of evidence
points to this phenomenon as a common background of most, if not all,
environmental stresses perceived not only as a source of oxidative stress, but also
as a mechanism controlling the main aspects of plant adaptation to various growth
conditions (Foyer & Noctor, 2005a; 2009). The interplay between ROS production
and scavenging determines the steady-state level of ROS in cells, as well as the
ROS signature, i.e. the duration, localization, and amplitude of ROS signals
conditioning stress responses (Mahalingham & Fedoroff, 2003; Miller et al ., 2008).
The ascorbate-glutathione (AA-GSH) cycle serves as the main antioxidant pathway
in plant cells linking the protection against ROS to the redox-regulated plant
acclimation response (Foyer & Noctor, 2005b). The AA-GSH cycle involves
successive oxidations and reductions of ascorbate and glutathione catalysed by
the enzymes constituting the cycle, namely ascorbate peroxidase (APX, EC,





dehydroascorbate reductase (DHAR, EC and glutathione reductase (GR,

EC (Polle, 2001; Noctor, 2006). It operates in all cellular compartments in
which ROS detoxification is needed, i.e. in apoplast, cytosol, chloroplasts,
mitochondria and peroxisomes (Foyer & Noctor, 2003; Potters et al. , 2002). Apart

from its direct antioxidant role, the AA-GSH cycle functions in ROS sensing and
signalling (Foyer & Noctor, 2005a, 2005b). Recent genetic evidence suggests that
ROS do not trigger PCD or senescence by causing damage to the cell but they act
as signals that activate pathways of gene expression that lead to genetically
regulated cell death (Foyer & Noctor, 2005a; Dietz, 2008).
Under these stressful conditions imbalance between light energy absorbed through
PSII and the ultimate consumption of the photosynthetic electrons through
metabolic pathways

such as the Calvin cycle, photorespiration and nutrient

assimilation occurs. This leads to an increased formation of ROS and to

photooxidative stress.
Three classes of redox signals originating from chloroplasts can be considered to
be important in governing the plant adaptive/stress response in natural
environments (Pfannschmidt et al. , 2001). Class 1 originates from specific redox
pairs in the photosynthetic electron transport (PET) chain e.g. the reduced and
oxidized plastoquinone and the cytochrome b6f complex. Class 2 depends on the
redox state of stromal thioredoxin, NAD(P)H, glutathione and ascorbate whereas
class 3 is mediated by ROS. These signals act in chloroplasts to ensure the most
effective operation of photosynthesis (Andrezej et al, 2010).
Jim et al., (2011) conclude that ffects of experimental warming on leaf functional
traits, leaf structure, and leaf biochemistry in A. thaliana, apart from fitness
components. Several findings are worth noting. Firstly, moderate simulated climatic
warming benefited Arabidopsis growth, whereas severe warming produced
detrimental effects. This implies that global warming can have both beneficial and
detrimental impacts on plants, especially on those belonging to the same functional
group as Arabidopsis, i.e., moderate warming is beneficial to plants when it is
below their optimum temperature, whereas higher levels of warming are
detrimental to plants. Secondly, the increase in A we observed under moderately
warm conditions may be attributed to the increase in SD, chlorophyll content, and
number of chloroplasts. Thirdly, starch accumulation in chloroplasts may be the

main factor influencing chloroplast ultrastructure, and elevated temperature

regulates plant respiration by probably affecting mitochondrial size. Finally, high
SOD and CAT activities may enable plants grown at elevated temperatures to
exhibit relatively high tolerance to temperature stress, thus alleviating the harmful
effects of superoxide anion radicals and hydrogen peroxide.
High light, together with low temperature, induces stress in trees because of
photoinhibition, and down regulation of PSII, as well as desiccation (DeLucia et al.,
1991; Pavel & Fereres, 1998; Stecher et al., 1999). Photoinhibition in


banksiana was less when growing at relatively low temperatures. This was
attributable in part to cold induced production of filtering anthocyanin in the
epidermis and in part because of increased photosynthetic capacity, most likely
caused by an increased capacity at low temperatures to keep QA, the first stable
quinone electron acceptor of PSII, oxidized at high irradiance (Krol et al., 1995).
Antioxidant enzymes also play a role in protecting against freezing
temperatures (Tao et al., 1998; Garca-Plazaola et al., 1999), even in roots (Zhao &
Blumwald, 1998). But if night time temperatures are too low, photoinhibition
increases. Under such conditions a 1C increase in average night-time
temperature allowed Abies lasiocarpa seedlings to avoid photoinhibition during the
day, and increased photosynthesis by 650% (Germino & Smith, 1999). By contrast,
80% shading increased photo-synthesis by only 40%.
Drought is a globally important abiotic factor limiting tree growth, with acute
drought events commonly causing forest and woodland dieback (Allen et al. 2010).
Forests contain up to 80% of the global above-ground and 40% of the belowground carbon in terrestrial ecosystems (Dixon et al. 1994). Therefore, the impact
of drought on trees might become an important factor influencing the global carbon
cycle and thereby further boost global warming because of reduced CO2 fixation.
Trees have evolved various mechanisms which help them to cope with limited

water supply. Responses to drought include: (1) reducing the water deficit by
developing root systems able to take up water deep in the soil; (2) minimizing
water losses through stomatal closure and producing small leaves; and (3)
accumulating osmoprotective substances (Kozlowski & Pallardy 2002).
Drought may become more severe and more prevalent with predictions of
raising global air temperatures and, locally, decreasing rainfall, especially in areas
where problems with water supply already exist (IPCC 2007). Predictions are that
more areas may become affected by drought and, as a result, forest health, growth
and productivity may be impaired (IPCC 2007). Potential adaptive management
may include the preferred selection of more tolerant species or genotypes in some
areas (Marris 2009). The determination of the degree of drought tolerance of tree
and shrub species, or of genotypes within species, is currently not straightforward,
especially if selections are desired at a seedling or sapling stage. A number of
underlying physiological mechanisms and biochemical compounds have been
proposed as markers for drought stress and tolerance, among them anti-oxidative
and photoprotective defence systems (Smirnoff 1993, Tausz et al. 2004).
Antioxidative and photoprotective defence systems keep reactive oxygen species,
produced under conditions of photo-oxidative stress, under control. Upon drought
exposure, photo-oxidative stress can occur when stomatal closure restricts CO 2
input into the leaf (Smirnoff 1993, Chaves et al. 2009). Reducing equivalents
(NADPH) produced in the light reactions which are not used in carbon fixation can
be consumed in alternative pathways such as Mehler reaction or pho-torespiration,
resulting in the production of ROS (Flexas and Medrano 2002a, Asada 2006). If
consumption of reducing equivalents decreases, the imbalances between electron
use and energy consumption under continuing light-driven electron transport can
cause a situation of 'excess excitation energy' (Flexas and Medrano 2002a, Tausz
et al. 2004, Asada 2006). Excess energy in itself as well as the alternative electron
transport pathways produce ROS. Reactive oxygen species can disrupt cell
membranes, nucleic acids and other cellular functions (Asada 2006, Gill and Tuteja
2010). Despite their potentially destructive consequences, ROS can also act as

signal and sensing factors triggering plant stress responses (Foyer and Noctor
2009). Trees can cope with excess excitation energy and photo-oxidative stress in
several ways. Acclimation to high light conditions can include decreased
chlorophyll contents, which reduces the amount of light absorbed in the first
place (Niinemets 2007). The thylakoid pigment zeaxanthin is involved in the
dissipation of excess energy as heat (Flexas and Medrano 2002a,


Adams and Adams 2006). Dissipation of excess energy can minimize the formation
of ROS and prevent photoinhibition. If energy dissipation is insufficient, ROS
generation in the photosynthetic membranes or as a result of photorespiration or
the Mehler reaction can be enhanced (Noctor et al. 2002, Tausz et al. 2004).
Reactive oxygen species are detoxified by antioxidants, and both antioxidants and
ROS have important role in signalling pathways in response to stress (MunnBosch et al. 2012). Low-molecular-weight antioxidants (carotenoids, ascorbic acid,
glutathione and -tocopherol) function as alternative electron acceptors (Tausz et
al. 2004). These antioxidants are involved in essential and complex pathways,
where excess energy is eliminated and ROS detoxified (Foyer and Shigeoka
2010). While antioxidants can serve as chemical reductants, their functions and
their regeneration are also linked in enzymatic cycles, such as the ascorbateglutathione cycle where ascorbic acid is regenerated by glutathione (Foyer and
Noctor 2011). Ascorbic acid has a role in conversion of zeaxanthin in the
xanthophyll cycle and also in the regeneration of -tocopherol, a membrane-bound
lipophilic antioxidant (Foyer and Shigeoka 2010, Munn-Bosch et al. 2012).
Besides taking part in scavenging of ROS, -tocopherol functions as a stabilizer of
cell membranes (Munn-Bosch and Alegre 2002). Glutathione and ascorbic acid
are near-ubiquitous water-soluble antioxidants and they take part in many
physiological processes (i.e., growth regulation), apart from their defence role
under stress (Foyer and Noc tor 2011, Smirnof f 2011). They are present in two
forms: reduced and oxidized (Apel and Hirt 2004, Foyer and Noctor 2011), which
together make up the total pool of the antioxidant. During the removal of ROS,
antioxidants are transformed into their oxidized form, and must be regenerated
(Apel and Hirt 2004, Foyer and Noctor 2011). Antioxidants are normally thought to

be kept in largely reduced form in plants under non-stress conditions. Increased

proportions of the oxidized form may indicate stress conditions (Foyer and Noctor
2011). Many studies reported responses of antioxidants and photo-protective
carotenoids to stress in general and to drought stress in particular. The
concentration of antioxidants can rise with progressing stress, commonly
interpreted as a strengthening of defence systems and therefore an indication of
acclimation to stress (Smirnoff 1993, Tausz et al. 2004). However, concentrations
of antioxidants can also decrease upon stress exposure, possibly when stress
becomes more severe, leading to irreversible damage and, potentially, oxidation
and depletion of antioxi-dant pools. In other cases, antioxidant concentrations
remained unchanged (Smirnoff 1993, Tausz et al. 2004). In addition to the degree
of stress experienced, species, tree age, other tolerance (or avoidance)
mechanisms that may moderate the degree of photo-oxidative stress experienced
under drought, and other factors have been suggested to modify antioxidant
responses to stress (Smirnoff 1993, Tausz et al. 2004, Sofo et al. 2010). Because
of numerous and sometimes conflicting reports (Smirnoff 1993, Sofo et al. 2010)
about stress responses of antioxidative and photoprotective compounds in leaves
of trees, we undertook a meta-analysis of literature reporting on the most
ubiquitous low-molecular-weight antioxidants and photoprotectants: ascorbic acid,
glutathione, -tocopherol and protective xanthophylls. Meta-analysis is a statistical
method that allows the joint evaluation of many independent studies using effect
size (ES) values, also increasingly used in biological studies and studies on trees
in particular (Thomas and Winner 2002, Richards et al. 2010). We tested the
general hypothesis that (i) drought triggers increases in concentrations of
antioxidants and photo-protective compounds. We also used moderator variables
to explore the following sub-questions: (ii) the response depends on stress
intensity with more severe stress causing the defence systems to degrade and
oxidize; (iii) trees and shrubs with evergreen foliage withstand drought better than
deciduous species and this is reflected in different responses of defence systems
to drought; (iv) defence system responses to drought differ between species from
humid and those from arid habi-tats; and (v) results vary depending on whether

experiments are done on potted trees under controlled conditions (cham-bers,

glasshouses) or under field conditions.

Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in
controlling oxidative stress in plants. J Exp Bot 53: 13311341.
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M,
Kitzberger T, Rigling A, Breshears DD, Hogg EH et al. 2010. A global
overview of drought and heat-induced tree mortality reveals emerging
climate change risks for forests. Forest Ecology and Management 259: 660
Andrzej Kornas, Elzbieta Kuzniak, Ireneusz Slesak and Zbigniew Miszalski. 2010
The key role of the redox status in regulation of metabolism in
photosynthesizing organisms. Acta Biochimia Polonica vol 57, No. 2: 143
Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and
signal transduction. Annu Rev Plant Biol 55: 373399.
Biswal B, Joshi N.P, Raval M.K y Biswal U.C. 2011. Photosynthesis, a global
sensor of environmental stress in green plants: stress signalling and
adaptation. CURRENT SCIENCE, VOL. 101, NO. 1: 47-56
Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes.
Physiol Plantarum 133: 459468.
Dizengremel P, Le Thiec D, Hasenfratz-Sauder M-P, Vaultier M-N, Bagard M,

Jolivet Y (2009) Metabolic-dependent changes in plant cell redox power

after ozone exposure. Plant Biol 11: 3542.
Fink RC, Scandalios JG (2002) Molecular evolution and structurefunction
relationships of the superoxide dismutase gene families in angiosperms and








dismutases. Arch Biochem Biophys 399: 1936.

Forsberg J, Rosenquist M, Fraysse L, Allen JF (2001) Redox signalling in
chloroplasts and mitochondria: genomic and biochemical evidence for two
component regulatory systems in bioenergetic organelles. Biochem Soc
Trans 29: 403407.
Foyer CH, Allen JF (2003) Lessons from redox signaling in plants. Antioxid Redox
Signal 5: 35.
Foyer CH, Noctor G (2005a) Oxidant and antioxidant signalling in plants: a re
evaluation of the concept of oxidative stress in a physi- ological context.
Plant Cell Environ 28:


Foyer CH, Noctor G (2005b) Redox homeostasis and antioxidant sig- naling: A







responses. Plant Cell 17: 18661875.

Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms:
Garret 2006

acclimation, and practical implications. Antiox Redox Signal 11:

Mahalingam R, Fedoroff N (2003) Stress response, cell death and signalling: the
many faces of reactive oxygen species. Physiol Plant 119: 5668.
Miller G, Coutu J, Shulaev V, Mittler R (2008) Reactive oxygen signalling in plants.
In Annual Plant Reviews: Intracellular Signaling in Plants. Yang Z, ed, vol.
33, pp 189201. Blackwell, Oxford.
Noctor G (2006) Metabolic signalling in defence and stress: the central roles of
soluble redox couples. Plant Cell Environ 29: 409425.
Pfannschmidt T, Allen JF, Oelmller R (2001) Principles of redox control in
photosynthesis gene expression. Physiol Plant 112: 19.
Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione
pathway in chloroplasts by metabolic modeling. Computer simulations as a
step towards flux analysis. Plant Physiol 126: 445462.
Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione:
guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40: