Journal of Experimental Botany, Vol. 49, No. 328, pp. 1775–1788, November 1998
REVIEW ARTICLE
Ozone depletion and increased UV-B radiation:
is there a real threat to photosynthesis?
Damian J. Allen1, Salvador Nogués and Neil R. Baker2
Department of Biological Sciences, University of Essex, Colchester, Essex CO4 3SQ, UK
Received 14 May 1998; Accepted 9 July 1998
Abstract
This critical review of recent literature questions earlier predictions that photosynthetic productivity of
higher plants is vulnerable to increased ultraviolet-B
(UV-B) radiation as a result of stratospheric ozone (O )
3
depletion. Direct UV-B-induced inhibition of photosynthetic competence is observed only at high UV-B irradiances and primarily involves the loss of soluble Calvin
cycle enzymes and adaxial stomatal closure in amphistomatous plants. However, even under these extreme
UV-B exposures, acclimation (e.g. induction of UV-B
absorbing flavonoids) can protect the photosynthetic
processes. In plants irradiated with UV-B throughout
development a reduction in productivity is usually
associated with a reduced ability to intercept light (i.e.
smaller leaf area) and not an inhibition of photosynthetic competence. Finally, a review of field experiments utilizing realistic UV-B enhancement is made to
evaluate whether the mechanisms involved in UV-Binduced depressions of photosynthesis are likely to
impact on the photosynthetic productivity of crops and
natural vegetation in the future. Predictions of plant
responses to O depletion are suspect from square3
wave irradiance experiments in the field and controlled
environments due to the increased sensitivity of plants
to UV-B at relatively low photosynthetically-active
photon flux densities (PPFD) and ultraviolet-A (UV-A)
irradiances. Realistic modulated UV-B irradiances in
the field do not appear to have any significant effects
on photosynthetic competence or light-interception. It
is concluded that O depletion and the concurrent rise
3
in UV-B irradiance is not a direct threat to photosynthetic productivity of crops and natural vegetation.
Key words: Biomass, development, ozone depletion,
photosynthesis, ultraviolet-B.
Introduction
It has been predicted frequently that photosynthetic productivity of higher plants is vulnerable to increased
ultraviolet-B ( UV-B) radiation (280–320 nm) due to stratospheric ozone depletion ( Tevini and Teramura, 1989;
Bornman, 1989; Bornman and Teramura, 1993; Tevini,
1993; Teramura and Sullivan, 1994; Jordan, 1996;
Teramura and Ziska, 1996). However, recent studies have
cast serious doubt over such assertions. Recent literature
is reviewed in this paper in order to evaluate critically
whether future predicted increases in UV-B radiation are
likely to have a significant effect on photosynthetic productivity. The changing UV-B environment and the penetration of plant tissue by UV-B are discussed initially and
this is followed by a critical examination of the mechanisms by which UV-B may inhibit photosynthetic
productivity. In considering how UV-B can reduce photosynthetic productivity a clear distinction is made between
mechanisms which directly inhibit photosynthetic competence and changes in plant development in response to
UV-B which indirectly affect photosynthetic productivity.
1 Present address: United States Department of Agriculture/Agricultural Research Service, Photosynthesis Research Unit, Urbana, Illinois
61801-3838, USA.
2 To whom correspondence should be addressed. Fax +44 1206 873416. E-mail: [email protected]
Abbreviations: w , relative quantum efficiency of photosystem II photochemistry; A , light-saturated net CO assimilation rate; FBPase, chloroplastic
PSII
sat
2
fructose 1,6-bisphosphatase; F /F , maximum quantum efficiency of photosystem II photochemistry; g , stomatal conductance to CO ; J , maximum
v m
s
2 max
potential rate of electron transport contributing to ribulose,5-biphosphate regeneration; PPFD, photosynthetically-active photon flux density; PRKase,
phosphoribulokinase; PSII, photosystem II; Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; RuBP, ribulose 1,5-bisphosphate; SBPase,
sedohepulose 1,7-bisphosphatas; V
, maximum carboxylation velocity of ribulose 1,5-bisphosphate carboxylase/oxygenase.
c,max
© Oxford University Press 1998
1776
Allen et al.
Finally, a review of field experiments utilizing realistic
UV-B enhancement is made to evaluate whether the
mechanisms involved in UV-B-induced depressions of
photosynthetic activities are likely to impact on the photosynthetic productivity of crops and natural vegetation in
the future.
The UV-B environment
The amount of UV-B radiation reaching the surface of
the earth is highly variable as it is influenced by many
factors. The solar zenith angle and day length, determined
by season and latitude, account for the majority of this
variation ( Webb, 1997). Ozone (O ) is the primary UV-B
3
absorbing component of the atmosphere with approximately 90% of this atmospheric ozone column being in
the stratosphere (the ‘ozone-layer’) and the remainder
in the troposphere ( WMO, 1995). The amount of O in
3
both of these atmospheric regions has a great deal of
temporal and spatial variability ( Webb, 1997). Clouds,
aerosols and surface albedo are also significant factors in
determining the UV-B irradiation at a particular location
and time ( Webb, 1997). These factors tend to result in
UV-B irradiances being highest in the summer, at lower
latitudes and at higher altitudes (Madronich et al., 1995).
This natural UV-B distribution has been significantly
affected by anthropogenic activity, primarily through the
release of man-made chlorine and bromine compounds
(e.g. CFCs) which result in stratospheric O depletion
3
( WMO, 1995). The greatest depletion has occurred in
the spring at the highest latitudes when sunlight returns
to the very cold stratospheric clouds in the polar vortices
which provide conditions for very rapid chlorine and
bromine catalysed O destruction (SORG, 1996). This
3
has been most apparent over Antarctica where total ozone
in October is less than 40% of that observed in the 1960s
(SORG, 1996). This ozone hole results in greater UV-B
irradiation in the spring at Palmer Station, Antarctica
(64° S), than at any time of the year in San Diego, USA
(32° N ), despite much lower incident sunlight (Madronich
et al., 1995). Whilst not being as dramatic as the Antarctic
O hole, significant spring ozone depletion has occurred
3
over the Arctic particularly in the 1990s (Rex et al.,
1997; Pyle, 1997). International implementation of the
Montreal Protocol (1987) and its Amendments and
Adjustments (1990, 1992) is already reducing the impact
of anthropogenic emissions on the stratospheric O layer
3
and should eventually eliminate this depletion ( WMO,
1995). Assuming full compliance by all nations, O deple3
tion is predicted to peak around 1998 and then slowly
recover by about 2045, other things being equal ( WMO,
1995). Therefore the maximum O loss over the northern
3
mid-latitudes, relative to the situation in the 1960s, is
expected to be increases of 12–13% in the winter/spring
and 6–7% in the summer/autumn, producing increases in
UV-B (based on an erythemal action spectrum) of 15%
and 8%, respectively ( WMO, 1995). However, it is currently not clear whether the assumptions on which these
predictions rely are valid. Firstly, full compliance with
the Montreal Protocol is uncertain (Greene, 1995) and
secondly, anthropogenic emissions of greenhouse gases
and other pollutants have the potential to change tropospheric O concentrations, cloud cover and stratospheric
3
air temperatures resulting in altered UV-B irradiation
( Webb, 1997). A recent analysis using a global climate
model predicted that rising CO and other greenhouse
2
gases may cause stratospheric cooling and more stable
polar vortices in winter, delaying recovery in O concen3
trations for approximately 15 years after declines in CFC
emissions (Shindell et al., 1998).
UV-B penetration of plant tissue
In order for UV-B to have any direct or developmental
effects on photosynthetic productivity, UV-B must penetrate through the leaf and be absorbed by chromophores
associated with the photosynthetic apparatus or associated genes and gene products. Leaves absorb over 90%
of incident UV-B; leaf surface reflectance in this wavelength range is generally below 10% and there is negligible
transmission of UV-B through leaves (Robberecht et al.,
1980; Cen and Bornman, 1993; Gonzalez et al., 1996).
Cellular components which can absorb UV-B directly
include nucleic acids, proteins, lipids and quinones
(Jordan, 1996). Leaves also contain water-soluble phenolic pigments, such as flavonoids, which strongly absorb
UV-B radiation whilst not absorbing photosynthetically
active radiation. These UV-B absorbing pigments are
present through the leaf but accumulate significantly in
adaxial epidermal cells (Cen and Bornman, 1993; Ålenius
et al., 1995). Epidermal UV-B penetration, measured
with a fiber-optic microprobe, has been found to be
effectively zero in conifer needles, 3–12% in woody
dicotyledons and grasses, and 18–41% in herbaceous
dicotyledons (Day et al., 1992). Epidermal UV-B penetration has been negatively correlated with UV-B-absorbing
pigment concentration and epidermal thickness (Day,
1993). The induction of UV-B-absorbing compounds in
leaves is one of the best described and most widespread
responses of plant species to UV-B irradiation ( Tevini
et al., 1991; Cen and Bornman, 1993; Middleton and
Teramura, 1993; Strid, 1993; Yalpani et al., 1994; Day
and Vogelmann, 1995). UV-B irradiation stimulates the
expression of the genes encoding phenylalanine ammonialyase (PAL), the first stage of the phenylpropanoid pathway, and chalcone synthase (CHS), the key stage which
commits the pathway to flavonoid synthesis (for reviews
see Bornman and Teramura, 1993; Beggs and Wellmann,
1994; Jenkins et al., 1997). Consequently, in many leaves
UV-B: a threat to photosynthesis?
UV-B penetration to sites where it might be damaging to
the photosynthetic apparatus may be minimal.
Mechanisms of direct UV-B-induced inhibition of
photosynthetic competence
UV-B-induced inhibition of mature leaf photosynthesis
in many plant species was demonstrated over 20 years
ago ( Van et al., 1976; Basiouny et al., 1978). It is evident
that UV-B can potentially impair the performance of all
three main component processes of photosynthesis, the
photophosphorylation reactions of the thylakoid membrane, the CO -fixation reactions of the Calvin cycle and
2
stomatal control of CO supply ( Fig. 1). The activities of
2
many components of photosynthesis are regulated by the
rates of other photosynthetic reactions (Stitt, 1991;
Harbinson, 1994) and therefore examination of a single
process or component, such as the carboxylation velocity of ribulose 1,5-bisphosphate carboxylase/oxygenase
( Rubisco), the quantum efficiency of photosystem II
(PSII ) photochemistry or stomatal conductance, does
not allow identification of the primary UV-B-induced
limitation.
1777
Photophosphorylation
Numerous investigations have demonstrated that PSII is
the most sensitive component of the thylakoid membrane
photosynthetic apparatus ( Fig. 1) on exposure to UV-B
irradiation (Noorudeen and Kulandaivelu, 1982; Iwanzik
et al., 1983; Renger et al., 1989; Kulandaivelu et al., 1991;
Melis et al., 1992). Consequently, in many reviews PSII
damage has often been implicated as the major potential
limitation to photosynthesis in UV-B irradiated leaves
(Bornman, 1989; Caldwell et al., 1989; Stapleton, 1992;
Teramura and Sullivan, 1994; Fiscus and Booker, 1995),
as is the case in the photoinhibition of photosynthesis by
excess photosynthetically-active radiation (400–700 nm)
(Baker and Bowyer, 1994), although it has been suggested
that the mechanism of UV-B induced damage may be
different (Friso et al., 1994; Jansen et al., 1996). However,
mature leaves of glasshouse grown pea (Pisum sativum L.
cv. Meteor), irradiated with a high UV-B intensity
(40 kJ m−2 d−1 weighted with a generalized plant action
spectrum; Caldwell, 1971) concurrent with a photosynthetically-active photon flux density (PPFD) greater than
450 mmol m−2 s−1, demonstrated that UV-B can induce
decreases in the light-saturated CO assimilation rate
2
Fig. 1. A schematic representation of the main processes in C photosynthesis in higher plants, of photophosphorylation, Calvin cycle and stomatal
3
conductance. Photophosphorylation starts with the absorption of PPFD by the antenna complexes associated with photosystem II (PSII ) and
photosystem I (PSI ) in the chloroplast thylakoid membrane, which drives electron transport, producing reducing power (NADPH ) and a H+
electrochemical potential gradient across the membrane. Dissipation of this gradient by the passage of H+ back across the membrane through the
ATPase drives the production of ATP. The diffusion of atmospheric CO (c ) into the leaf (and water vapour out of the leaf ) is regulated by the
2 a
stomata in the epidermis. Ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalyses the assimilation (A) of intercellular CO (c ) with
2 i
ribulose 1,5-bisphosphate (RuBP) in the carboxylation reaction of the Calvin cycle in the stroma of the chloroplast. Further Calvin cycle reactions
utilize NADPH and ATP from photophosphorylation to produce triose phosphates (triose-P) which are required for the synthesis of carbohydrates,
lipids, amino acids, etc. The Calvin cycle is completed by the regeneration of RuBP involving fructose 1,6-bisphosphatase (FBPase), sedoheptulose
1,7-bisphosphatase (SBPase) and phosphoribulokinase (PRKase), the first two of which, along with Rubisco, catalyse effectively irreversible
reactions and therefore are important in regulating the rate of the cycle.
1778
Allen et al.
(A ) in the absence of any major inhibition of the
sat
quantum efficiency of PSII photochemistry (w ) measPSII
ured simultaneously with A , or after dark-adaptation
sat
(F /F ), or the capacity of thylakoids isolated from the
v m
leaves to bind atrazine, thus demonstrating that no significant photodamage to PSII complexes had occurred
(Nogués and Baker, 1995). More recent data from mature
leaves of glasshouse-grown oilseed rape (Brassica napus
L. cv. Apex), irradiated with a high UV-B intensity
(32 kJ m−2 d−1 weighted with a generalized plant action
spectrum) concurrent with a PPFD greater than
500 mmol m−2 s−1, also demonstrated that UV-B can
induce decreases in A in the absence of any major
sat
inhibition of w
measured simultaneously with A , or
PSII
sat
after dark-adaptation (F /F ) as shown in Fig. 2 (Allen
v m
et al., 1997). A similar inhibition of photosynthesis without an appreciable effect on PSII photochemistry has also
been observed in soybean (Middleton and Teramura,
1993), rice ( Ziska and Teramura, 1992) and algae (Lesser,
1996). Consequently, it is clear that UV-B inhibition of
PSII photochemistry is not a ubiquitous primary limitation to photosynthesis.
Calvin cycle
Analysis of the relationship between net CO assimilation
2
(A) and intercellular CO concentration (c ) allows separa2
i
tion of the relative limitations imposed by stomata,
Rubisco carboxylation velocity and the capacity for regeneration of ribulose 1,5-bisphosphate (RuBP) on leaf
photosynthesis (Fig. 1) according to the model of von
Caemmerer and Farquhar (1981). Using this A/c
i
analysis, it was demonstrated that the UV-B-induced
decreases in A in mature leaves of oilseed rape were
sat
associated with a reduction in the maximum carboxylation velocity of Rubisco (V
) (Fig. 2), and this
c,max
was confirmed by in vitro biochemical assays of Rubisco
activity (Allen et al., 1997). A decline in Rubisco activity
may be attributed to a deactivation (i.e. a reduction in
the specific activity) or a loss of the enzyme (Quick et al.,
1991). In mature leaves of oilseed rape the UV-B-induced
decline in Rubisco activity was due to a reduction in the
amount of Rubisco present, not simply a deactivation, as
the specific activity of Rubisco carboxylation did not
significantly decline in response to 4 d of UV-B irradiation
(Allen et al., 1997). UV-B-induced reductions in both
Rubisco activity and content have been previously
reported in higher plants ( Vu et al., 1982, 1984; Strid
et al., 1990; Nedunchezhian and Kulandaivelu, 1991;
Jordan et al., 1992; He et al., 1993, 1994; Huang et al.,
1993; Kulandaivelu and Nedunchezhian, 1993) and algae
(Lesser, 1996). Wilson et al. (1995) reported the appearance of a 66 kDa protein during UV-B exposure in oilseed
rape, pea, tomato, and tobacco which they attributed to
a photomodified form of the large subunit of Rubisco.
Fig. 2. Changes in photosynthetic parameters over 5 d of irradiation of
mature leaves of oilseed rape (Brassica napus L. cv. Apex) with
32 kJ m−2 d−1 UV-B (weighted with the generalized plant action
spectrum) in a glasshouse with a minimum PPFD of 500 mmol m−2 s−1.
The light-saturated CO assimilation rate (A ), maximum carboxylation
2
sat
velocity of Rubisco (V
), maximum potential rate of electron
c,max
transport contributing to RuBP regeneration (J ) and stomatal
max
limitation were estimated from A/c analysis at 1600 mmol m−2 s−1
i
PPFD using an IRGA (Li-6262, Licor, Lincoln, Nebraska, USA). A
modulated fluorimeter (PAM–2000, Walz, Effeltrich, Germany) was
used to estimate w simultaneously with A , and F /F was measured
PSII
sat
v m
after 30 min dark-adaptation. Data are the mean (± standard error of
the mean) of 6–8 replicates. Significant differences (P<0.05) between
treatments for each time point were estimated with the t-test and
indicated by *. Data modified from Allen et al. (1997).
UV-B: a threat to photosynthesis?
Levels of mRNA coding for both the large and small
subunits of Rubisco have been reported to decline before
any effect at the protein level was evident (Jordan et al.,
1992), thus indicating that Rubisco itself may not necessarily be the UV-B radiation photoreceptor.
Analysis of mature oilseed rape leaves irradiated with
UV-B also revealed a decline in the maximum rate of
electron transport contributing to RuBP regeneration
(J ) concurrent with the reduction in A as seen in
max
sat
Fig. 2 (Allen et al., 1997). RuBP regeneration could be
limited either by an inability to supply reductants and
ATP from electron transport or an inactivation or loss of
Calvin cycle enzymes other than Rubisco ( Fig. 1). It is
clear, however, that any inability of the thylakoids to
supply reductants and ATP cannot be attributable to a
reduction in the ability to perform PSII photochemistry,
since depressions in J
occur in the absence of any
max
major photodamage to PSII reaction centres ( Fig. 2). In
vitro assays of the content of key Calvin cycle enzymes
involved in the regeneration of RuBP, by Western blot
analyses, indicated that UV-B irradiation of mature leaves
of oilseed rape induced a reduction in the content of
sedoheptulose 1,7-bisphosphatase (SBPase), but not
chloroplastic fructose 1,6-bisphosphatase (FBPase) or
phosphoribulokinase (PRKase) on a leaf area basis
( Fig. 3; Allen, 1998). This large decline in enzyme content
would be expected to reduce SBPase activity unless the
enzyme was significantly in excess in control plants.
Recent work on transgenic tobacco with SBPase contents
reduced by antisense RNA suggest a good correlation
between activity and content (Harrison et al., 1998). In
addition, RuBP-regeneration, as estimated from J , was
max
reduced in tobacco plants with SBPase activities which
were 47% (Harrison et al., 1998) and 64% (BA Bryant,
personal communication) of wild-type controls. Therefore
this decline in SBPase content may be responsible for the
reduced RuBP regeneration observed in J
in oilseed
max
rape ( Fig. 2), although this analysis does not exclude the
possibility of the involvement of regenerative Calvin cycle
enzymes other than the three measured. These data also
suggest that the decline in J
is not just a downmax
regulation of excess capacity of this activity in response
to vastly reduced rates of RuBP carboxylation by Rubisco
(Long and Drake, 1992; Wullschleger, 1993), but rather
a direct UV-B effect on the amount of SBPase present.
Reductions in the maximum rate of RuBP regeneration
observed previously in leaves on exposure to UV-B have
been attributed to a decline in electron transport rates
(Strid et al., 1990; Ziska and Teramura, 1992; Liu et al.,
1995). These results indicate that the maximum rate of
RuBP regeneration can decline and result in a decrease
in RuBP regeneration in the absence of any significant
effects on the quantum efficiencies of PSII photochemistry
( Fig. 2).
1779
Fig. 3. Changes in the relative contents of three Calvin cycle enzymes,
estimated by Western blot analysis, during 4 d of irradiation of mature
leaves of oilseed rape (Brassica napus L. cv. Apex) with 32 kJ m−2 d−1
UV-B (weighted with the generalized plant action spectrum) in a
glasshouse with a minimum PPFD of 500 mmol m−2 s−1 (growth
conditions as in Allen et al., 1997). Total protein was extracted by
grinding an equal leaf area from three replicate leaves together in
lithium phosphate buffer and lithium dodecyl sulphate as described by
Mae et al. (1993). Proteins were resolved on a 15% SDS-PAGE loaded
on an equal leaf area basis, and transferred to Immobilon-P membrane
following manufacturers instructions (Millipore Co., Bedford, MA,
USA). Membranes were probed with antibodies raised against either
wheat chloroplastic fructose 1,6-bisphosphatase (FBPase), sedoheptulose 1,7-bisphosphatase (SBPase) or phosphoribulokinase (PRKase),
followed by a secondary antibody of sheep anti-rabbit IgG conjugated
to horse radish peroxidase. Immunolabelled proteins were detected
using enhanced chemoluminesence ( ECL) as described by the manufacturer (Amersham International plc., Little Chalfont, UK ). Antibodies
were generously provided by TA Dyer of the John Innes Centre for
Plant Science Research, Norwich, UK. Data modified from Allen
(1998).
The process by which UV-B irradiation is absorbed
and induces this loss of Calvin cycle enzymes is currently
unknown and warrants further investigation. The selective
loss of specific enzymes suggest that this mechanism is
not a non-specific oxidation of leaf proteins resulting
from UV-B absorption by these proteins, or a UV-Binduced production of reactive oxygen species, unless
these particular proteins are not easily repaired or are
relatively unprotected by antioxidants. An alternative
mechanism may be the induction by UV-B of proteases
specific to the proteins that are degraded. It is possible
that UV-B is inducing such a senescence-like response, as
has been implicated in plant responses to tropospheric
ozone where specific proteins are degraded that are spatially separated from the site of primary oxidative damage
(Nie et al., 1993).
Stomata
Several studies have demonstrated a reduction in stomatal
conductance (g ) in response to UV-B irradiation
s
( Teramura et al., 1983; Negash, 1987; Negash et al., 1987;
Dai et al., 1992; Middleton and Teramura, 1993).
However, UV-B-induced inhibition of another component
1780
Allen et al.
of photosynthesis may result in stomatal closure in
response to reduced demand for CO . In order to identify
2
direct UV-B effects on stomata of mature leaves of oilseed
rape relative to changes in other photosynthetic parameters, stomatal limitation, i.e. the percentage decrease
in light-saturated photosynthesis that is attributable to
stomatal conductance ( Farquhar and Sharkey, 1982),
was estimated from A/c analysis ( Fig. 2; Baker et al.,
i
1997). While stomatal limitation tended to be higher in
UV-B irradiated leaves, the magnitude of these increases
was clearly not sufficient to account for the large depressions in photosynthesis (Fig. 2). The slight increases in
stomatal limitation observed in oilseed rape (Fig. 2) and
soybean (Middleton and Teramura, 1993) and a reduction
in c in pea (Day and Vogelmann, 1995) suggests that
i
there may be a direct UV-B effect on stomatal function.
Stomatal effects have not been found to affect photosynthesis in a range of studies (Murali and Teramura, 1986;
Sullivan and Teramura, 1989; Teramura et al., 1991; Ziska
and Teramura, 1992). Studies on leaves developing in
elevated UV-B levels have demonstrated direct effects on
stomatal conductance that were not limiting for CO
2
assimilation (see following section).
The mechanisms responsible for UV-B-induced
stomatal closure have received little attention. Stomatal
opening follows a K+ influx along an electrochemical
gradient formed by ATPase outward proton pumps situated in the guard cell plasmalemma ( Zeiger, 1983). Wright
and Murphy (1982) have shown that UV-B radiation can
induce stomatal closure directly by inhibiting K+ accumulation, and Negash et al. (1987) demonstrated the leakage
of 86Rb+ from guard cells in response to UV-B irradiation. One potential mechanism by which UV-B irradiation may reduce adaxial g is an inhibition of ATP
s
synthesis by electron transport in guard cell thylakoids.
A second mechanism may involve a direct inhibition by
UV-B of the plasmalemma ATPase proton pump.
However, the relative insensitivity to UV-B of PSII electron transport in mesophyll cells suggests that electron
transport and ATPase activity may not be the primary
site of inhibition. Alternatively, UV-B may not directly
affect the generation of the guard cell turgor pressure,
but rather the effect of this turgor on pore size through
UV-B-induced changes in the elasticity of the cell walls
or cytoskeleton of guard cells and the neighbouring
epidermal cells.
Indirect UV-B effects on photosynthetic
productivity
Many of the experiments examining the mechanism of
damage to photosynthesis involve irradiation of mature
leaves (Brandle et al., 1977; Negash et al., 1987; Strid
et al., 1990; Kulandaivelu and Nedunchezhian, 1993; He
et al., 1994; Jordan et al., 1992; Wilson et al., 1995;
Nogués and Baker, 1995; Allen et al., 1997). However,
plants will normally be exposed to UV-B radiation during
development and not just at full leaf expansion. Leaves
growing under elevated UV-B will receive a greater cumulative exposure throughout the lifetime of leaves than
mature leaves irradiated after developing without UV-B.
In addition, Bornman and Teramura (1993) suggested
that early stages of seedling development may be particularly sensitive to UV-B and Teramura and Caldwell
(1981) reported greater inhibition of photosynthesis in
developing leaves of soybean than those irradiated at fullexpansion. However, exposure to UV-B throughout leaf
and plant development allows the induction of protective
mechanisms, such as the induction of UV-B-absorbing
flavonoids, which may serve to reduce the effects of UV-B
irradiation.
To examine whether UV-B irradiation during development influenced the response of mature leaves to UV-B,
photosynthesis was measured in glasshouse-grown oilseed
rape irradiated with 32 kJ m−2 d−1 UV-B and a minimum
PPFD of 500 mmol m−2 s−1 from planting. There was no
significant UV-B effect on A , V
, J , w or F /F
sat c,max max PSII
v m
at full-expansion of the second leaves after irradiation
throughout development ( Table 1). This is in contrast to
mature leaves of glasshouse-grown plants exposed to the
same UV-B irradiation in which CO assimilation was
2
reduced by over 50% after 5 d of irradiation with concurrent declines in V
and J
(Fig. 2; Allen et al., 1997).
c,max
max
Oilseed rape clearly has the ability to acclimate to UV-B
during development to prevent damage to photosynthesis.
This acclimation is likely to be a result of reduced UV-B
penetration into leaves due to the induction of UV-Babsorbing pigments, such as flavonoids (Table 1).
Table 1. Photosynthesis parameters of oilseed rape (Brassica
napus L. cv. Apex) irradiated from sowing with 32 kJ m−2 d−1
UV-B (weighted with the generalized plant action spectrum) in a
glasshouse with a minimum PPFD of 500 mmol m−2 s−1
All measurements were made on the second true leaf, at full expansion.
A ,V
,J
w
and F /F were measured as described in Fig. 2.
sat c,max max PSII
v m
Adaxial and abaxial g were estimated under growth conditions using
s
an automatic transit-time porometer (AP4, Delta-T Devices, Cambridge,
UK ). Relative flavonoid content (A ) was estimated from the
300
absorbance at 300 nm of acidified methanol leaf extracts, and expressed
on a leaf area basis. Values are the mean (±standard error of the
mean) of six replicate leaves. Significant UV-B effects (P<0.05),
estimated from a t-test, are denoted by *. Data modified from
Allen (1998).
Parameter
Control
UV-B
A ( mmol m−2 s−1)
sat
V
(mmol m−2 s−1)
c,max
J
( mmol m−2 s−1)
max
w
PSII
F /F
v m
Adaxial g (mmol m−2 s−1)
s
Abaxial g (mmol m−2 s−1)
s
Flavonoids (A cm−2)
300
Leaf area (cm2)
18.8±1.2
107.5±8.4
174.1±8.3
0.229±0.008
0.797±0.009
387±34
574±69
4.29±0.22
48.1±2.2
17.7±3.7
95.9±13.2
219.2±51.9
0.268±0.041
0.792±0.008
136±10*
578±107
5.41±0.31*
33.6±0.2*
UV-B: a threat to photosynthesis?
1781
Table 2. Adaxial and abaxial g of pea (Pisum sativum L. cv. Meteor) irradiated from sowing with 32 kJ m−2 d−1 UV-B (weighted
s
with the generalized plant action spectrum) in a glasshouse with a minimum PPFD of 500 mmol m−2 s−1
All measurements were made on the sixth leaf under growth conditions with a porometer as described in Table 1. After growth from sowing under
control of UV-B treatments, the sixth leaf pair were held in an inverted position using fine nylon line for 8 d. After growth from sowing under
UV-B irradiation, plants were transferred to the control treatment for 5 d to determine recovery. Values are the mean (±standard error of the
mean) of six replicate leaves.
Parameter
Adaxial g (mmol m−2 s−1)
s
Abaxial g (mmol m−2 s−1)
s
Growth treatment
Leaf inverted for 8 d
Recovery
from UV-B
Control
UV-B
Control
UV-B
422±75
472±82
128±52
419±88
71±26
584±126
17±6
226±39
However, adaxial but not abaxial g is significantly
s
reduced in these leaves ( Table 1). This decline in adaxial
g can not be attributed to reduced photosynthesis, sugs
gesting a direct UV-B effect on the stomata.
Experiments on pea (Pisum sativum L. cv. Meteor)
using the same high UV-B irradiance also observed an
absence of reductions in A , V
and J
(Nogués
sat c,max
max
et al., 1998) with a similar direct inhibition of adaxial g ,
s
but not abaxial g (Table 2; Nogués et al., 1998), sugs
gesting that this may be a common response in amphistomatous plants. This inhibitory effect on adaxial g was
s
mediated by changes in aperture, as there was no reduction in stomatal density in these pea leaves (Nogués et al.,
1998). It is worth noting that the adaxial stomata will
receive much greater UV-B irradiation than the mesophyll
cells and abaxial stomata due to attenuation through the
leaf by UV-B-absorbing pigments. To investigate whether
this inhibition of adaxial g is a direct result of higher
s
UV-B irradiances on this surface, mature pea leaves were
turned over for 8 d. In control plants this resulted in a
big reduction in adaxial g as this surface now received
s
less PPFD, and an increase in abaxial g as this surface
s
was now illuminated directly with PPFD ( Table 2). In
UV-B irradiated plants, a similar inversion also reduced
adaxial g as PPFD was reduced, however, abaxial g also
s
s
decreased due to the simultaneous increase in UV-B
irradiation, despite the increase in PPFD ( Table 2). This
confirms that it is the greater UV-B irradiance, and not
any other characteristic of the adaxial stomata, which is
responsible for the inhibition of adaxial g as a similar
s
inhibition of abaxial g is observed when the abaxial
s
surface is directly irradiated with UV-B. There was also
no significant recovery in adaxial g in pea during 5 d
s
when plants were transferred from the UV-B to the
control treatment, suggesting permanent damage has
occurred ( Table 2).
A review by Caldwell and Flint (1994) concluded that
reports of reduced growth and morphological changes in
response to UV-B were more frequent than reports of
reduced photosynthetic competence. Plant photosynthetic
productivity is a product of leaf area and the photosynthetic rate per unit area. Reductions in leaf area have
211±84
410±135
been observed in many species including oilseed rape
( Table 1; Cen and Bornman, 1993), pea (Gonzalez et al.,
1996, 1998), cucumber (Teramura et al., 1983; Adamse
and Britz, 1992; Hunt and McNeil, 1998), marrow
(Sisson, 1981), Datura ferox (Ballaré et al., 1996),
soybean (Murali and Teramura, 1986), loblolly pine
(Naidu et al., 1993) and sweetgum (Sullivan, 1994).
Whilst some of these studies demonstrated a decline in
both leaf area and photosynthetic competence (Sisson,
1981; Teramura et al., 1983; Murali and Teramura, 1986;
Cen and Bornman, 1993), these reductions in leaf area
have been observed in the absence of UV-B-induced
inhibition of photosynthesis ( Table 1; Adamse and Britz,
1992; Naidu et al., 1993; Ballaré et al., 1996; Gonzalez
et al., 1996, 1998; Hunt and McNeil, 1998). Examination
of the impact of UV-B on leaf area has received much
less attention than the effect of UV-B irradiation on
photosynthetic competence, despite the importance of
both of these two components in determining plant
productivity. In fact, a review by Bornman and Teramura
(1993) suggested that reduced leaf area in response to
UV-B is generally believed to be a protective modification,
by reducing the amount of tissue exposed to UV-B
irradiation, with no reference made to the impact this
inhibition of leaf area will have on plant productivity.
The reasons for UV-B induced reductions of leaf area
have so far received comparatively little attention with
few studies making the distinction between leaf size and
leaf number as components of plant leaf area. The study
on pea responses to growth under 32 kJ m−2 d−1 UV-B
in a glasshouse by Nogués et al. (1998) found that plant
leaf area was reduced mainly by smaller rather than fewer
leaves, indicating UV-B inhibition of either cell division
or cell expansion in developing leaves. The growth of
many plant organs such as stems, coleoptiles, hypocotyls,
and petioles are controlled by the rate of expansion of
the epidermis (for reviews see Green, 1980; Dale, 1988;
Kutschera, 1989). It is widely assumed that leaf growth
is also regulated by the rate of expansion of the epidermis
(MacAdam et al., 1989; Beemster and Masle, 1996).
Therefore, the reduction of leaf growth observed in oilseed
rape, may be due to a UV-B-induced inhibition of the
1782
Allen et al.
growth of the adaxial epidermis, which receives a significantly higher incident UV-B flux than the other leaf cells.
UV-B inhibition of cell expansion has been observed in
cucumber cotyledons (Ballaré et al., 1991), tomato hypocotyls (Ballaré et al., 1995b), wheat (Hopkins, 1997), and
barley leaves (Liu et al., 1995). UV-B could reduce cell
expansion by changing turgor pressure or cell wall extensibility. Tevini and Iwanzik (1986) suggested that direct
oxidation of the auxin, indole-acetic acid, by UV-B results
in a reduction in cell wall expansion. Cell wall extensibility
can also be reduced by the formation of crosslinks
between cell wall carbohydrate and ferulic acid (Dale,
1988). Liu et al. (1995) reported an increase in the
proportion of epidermal ferulic acid which was bound to
cell walls in response to UV-B irradiation, which may
have limited leaf expansion. The study by Nogués et al.
(1998) examined the size and number of epidermal and
mesophyll cells during the development of the sixth leaf
pair of pea. In the palisade mesophyll and both epidermal
layers, the largest contributor to a 39% reduction in leaf
size in UV-B irradiated plants was fewer cells per leaf
(26–38% lower than control plants), rather than smaller
cells (2–13% reduction in size) (Nogués et al., 1998). This
suggests that the primary cause of the reduced area of
the sixth leaf of pea was UV-B-induced inhibition of cell
division. A recent study on pea irradiated with UV-B in
growth chambers revealed a similar reduction in leaf size
associated with an inhibition of epidermal cell division,
but not cell expansion, also in the absence of any direct
inhibition of photosynthesis (Gonzalez et al., 1998).
UV-B induced inhibition of cell division has been
reported in wheat leaves (Hopkins, 1997), cucumber
cotyledons ( Tevini and Iwanzik, 1986), parsley cell suspension cultures (Logemann et al., 1995) and petunia
leaf protoplasts (Staxén et al., 1993). Repair of UV-B
damage to DNA before replication and direct UV-B
induced oxidation of tubulin delaying microtubule formation have been suggested as mechanisms for direct reduction of the rate of cell division (Staxén et al., 1993).
However, it is not clear whether this UV-B-induced
reduction in cell division is a direct inhibitory effect on
cells with the potential for division, or the result of a
co-ordinated plant response to elevated UV-B irradiation.
Logemann et al. (1995) found that histone synthesis
(which was correlated with cell division rates) was transcriptionally repressed at the same time, and by the same
relative extent, as phenylalanine ammonia-lyase (one of
the key enzymes in the flavonoid biosynthesis pathway)
was transcriptionally induced by UV-B irradiation, and
both these responses could be induced by the same
oligopeptide elicitor. This suggests that UV-B may inhibit
cell division by a similar signal transduction pathway that
induces flavonoid synthesis in response to UV-B irradiation (Logemann et al., 1995), implying an adaptive
rather than injurious response.
Are predicted increases in UV-B a threat to
photosynthesis?
Whilst these glasshouse and growth cabinet studies utilizing high UV-B irradiances are useful tools in identifying
the potential mechanisms by which UV-B can affect
photosynthesis, it can be potentially misleading to use
such data to predict vegetation responses to O depletion
3
in field situations. This is because of the unrealistically
low UV-A (320–400 nm) and PPFD (400–700 nm) compared to UV-B radiation in glasshouse and growth cabinet
studies (Caldwell and Flint, 1994; Fiscus and Booker,
1995; McLeod, 1997). The sensitivity of plants to UV-B
irradiation is much greater at low PPFD and UV-A levels
in many species ( Teramura, 1980; Teramura et al., 1980;
Warner and Caldwell, 1983; Mirecki and Teramura, 1984;
Cen and Bornman, 1990). Caldwell et al. (1994) found
significant UV-B effects on soybean biomass only when
PPFD and UV-A were reduced to half of their flux in
full sunlight. UV-A was particularly effective at ameliorating UV-B damage when PPFD was low, but had no effect
at higher PPFDs (Caldwell et al., 1994). The mechanisms
responsible for this interaction between UV-B irradiation
and other wavelengths have yet to be convincingly demonstrated and this issue warrants further examination.
Flavonoid synthesis can be increased by elevating PPFD
and UV-A levels ( Warner and Caldwell, 1983; Bruns
et al., 1986; Cen and Bornman, 1990), and this may
involve UV-A and blue light stimulation of the expression
of the chalcone synthase gene of the flavonoid biosynthesis pathway (Ohl et al., 1989; Jenkins et al., 1997).
The rate of repair of UV-B-induced damage to DNA is
more rapid in the light due to the processes of photorepair
(Pang and Hays, 1991; Taylor et al., 1997). However,
these photorepair processes appear to be saturated at
relatively low PPFD and so are unlikely to be the main
reason for the greater tolerance of plants to UV-B at
higher PPFD. Alternatively, high PPFDs may confer
protection from UV-B damage by increasing photosynthesis and the available biochemical energy for defence
and/or repair processes. This hypothesis was supported
by the observations that UV-B-induced reductions in
plant growth were less severe when elevated CO concen2
trations were used to increase photosynthesis in the
absence of any change in flavonoid content (Adamse and
Britz, 1992). The influence of PPFD on UV-B effects on
photosynthetic gene expression has been investigated by
Mackerness et al. (1996), who reported that declines in
the mRNA transcript levels of component proteins of
PSII and Rubisco, induced by UV-B irradiation concurrent with 150 mmol m−2 s−1 PPFD, were ameliorated
when PPFD was raised to 350 mmol m−2 s−1. Other
possible reasons for the protection PPFD offers against
UV-B inhibition include elevated PPFD increasing antioxidant activity (Jordan, 1996) or altering leaf and plant
UV-B: a threat to photosynthesis?
morphology (Bornman, 1989; Bornman and Vogelmann,
1991). Much of the variability in plant responses to UV-B
irradiation in the literature canm be attributed to variation in the UV-B5UV-A5PPFD ratio in different experiments (Caldwell and Flint, 1994; Fiscus and Booker,
1995).
To enable accurate prediction of vegetation responses
to O depletion, field experiments with realistic UV-B,
3
UV-A and PPFD irradiances are required. Three main
types of UV-B field experiments have been undertaken to
date, i.e. UV-B exclusion, square-wave supplementation
and modulated supplementation, which need to be
considered.
UV-B exclusion
A few recent studies have utilized filters to compare near
ambient UV-B with below ambient UV-B irradiances to
identify whether current UV-B levels are detrimental to
plants. No inhibition of plant growth by current ambient
UV-B was observed in Sphagnum bog or Carex fen ecosystems in Tierra del Fuego (55° S ), which had been
exposed to a 10–20% increase in UV-B radiation over 14
years due to the Antarctic ‘ozone hole’ (Searles et al.,
1998), or in a coastal grassland in the Netherlands at 52°
N ( Tosserams et al., 1996). Current ambient UV-B was
found to significantly inhibit growth of seedlings of
Datura ferox at 34° S in Argentina (Ballaré et al., 1996),
but this was associated with a reduction in leaf area and
stem elongation and not assimilation rate. This supports
the conclusion from glasshouse studies ( Table 1; Nogués
et al., 1998) that any inhibition of biomass accumulation
in response to UV-B is primarily through reductions in
leaf area and not direct damage to photosynthetic competence. Exclusion experiments, however, do not enable
predictions to be made about the impact of future UV-B
increases, in response to continued O depletion. For such
3
predictions UV-B supplementation in the field is required.
Square-wave supplementation
The majority of field experiments examining the impact
of elevated UV-B on plants use a square-wave UV-B
irradiation system with lamps producing constant supplementary UV-B, calculated from a chosen O depletion
3
scenario on a particular day of the year and assuming
cloud-free conditions. Reductions in plant productivity
and photosynthesis have been observed in many field
square-wave experiments (Murali and Teramura, 1986;
Sullivan and Teramura, 1990; Teramura et al., 1990;
Naidu et al., 1993; Sullivan et al., 1994; Sullivan, 1994;
Nikolopoulos et al., 1995; Drilias et al., 1997). However,
the inhibitions observed are generally less pronounced
than similar UV-B supplementation under glasshouse
conditions with lower PPFD (Caldwell and Flint, 1994),
and some studies have demonstrated no inhibition of
1783
photosynthetic productivity (Sinclair et al., 1990; Ziska
et al., 1993; Fiscus et al., 1994; Dillenburg et al., 1995).
As suggested by Fiscus et al. (1994) in many of these
field experiments the supplementary UV-B irradiance
represents a significantly larger O depletion scenario
3
than stated, firstly due to an overestimation of the model
(Green et al., 1980) commonly used for calculating supplementary UV-B for a given O depletion, and secondly
3
because there has usually been no adjustment of supplementary UV-B levels when the ambient UV-B irradiance
changes with season and weather conditions. Not only is
the UV-B supplementation greater than intended, but the
ratio of UV-B to PPFD and UV-A is unrealistically
variable and much larger than will occur in response to
O depletion. As discussed earlier, UV-B sensitivity
3
is much greater at low PPFD and UV-A irradiances.
Whilst it is impossible to eliminate these unrealistic
UV-B5PPFD5UV-A ratios, these can be reduced by using
a more accurate model for calculating supplemental UV-B
(Björn and Murphy, 1985), by using more, smaller, step
changes in supplementation throughout the day and
altering lamp output as ambient UV-B irradiance changes
with season. As in all field experiments, adequate replication is essential for accurate prediction of future plant
responses. Studies which use individual plants within a
treatment block of lamps as the sampling unit, and not
the blocks themselves, risk pseudoreplication and as such
need to be interpreted with caution (Petropoulou et al.,
1995; Nikolopoulos et al., 1995; Drilias et al., 1997).
Modulated supplementation
Modulated UV-B irradiation systems continually monitor
ambient UV-B and adjust lamp output to ensure a
constant percentage increase in UV-B radiation, avoiding
the unrealistic UV-B:PPFD:UV-A ratios observed in
square-wave systems and, therefore, providing the most
accurate data for predictions of future plant responses to
stratospheric O depletion. A 30% modulated increase in
3
UK (52° N ) summer ambient UV-B (erythymallyweighted ) induced no reductions in pea biomass, leaf
area, light-saturated steady-state photosynthesis ( Table 3)
or in situ CO assimilation rate and stomatal conductance
2
in the field (Allen et al., 1998). This was confirmed by
an absence of UV-B effects on pre-dawn F /F or
v m
the major components contributing to light-saturated
CO assimilation; V
, J
and stomatal limitation
2
c,max max
( Table 3). A similar tolerance has been observed in other
modulated UV-B field experiments where UV-B had no
effect either on biomass accumulation in pea (Day et al.,
1996; Stephen et al., 1998), rice ( Kim et al., 1996), barley
(Stephen et al., 1998), oak (Newsham et al., 1996), wheat
and wild oat (Barnes et al., 1988; Beyschlag et al., 1988),
or on photosynthetic parameters, e.g. light-saturated CO
2
assimilation ( Flint et al., 1985; Beyschlag et al., 1988;
1784
Allen et al.
Table 3. Growth and photosynthetic parameters of pea (Pisum
sativum L. cv. Meteor) grown under a modulated 30% enhancement of ambient summer UV-B irradiance (erythemally-weighted)
in the field at the Institute of Terrestrial Ecology, Monks Wood,
Cambs., UK (for details see Allen et al., 1998)
Energized UV-B lamps were filtered with Mylar-D for the control
treatment, and cellulose diacetate for the UV-B treatment resulting in
mean irradiances of 1.89 and 2.44 kJ m−2 d−1, respectively. All
measurements were undertaken six weeks from sowing. A , V
,
sat
c,max
J
and stomatal limitation were estimated from A/c analysis at
max
i
1200 mmol m−2 s−1 PPFD using an IRGA (CIRAS-1, PP Systems,
Hitchin, UK ) on the youngest fully-expanded leaf. Pre-dawn F /F was
v m
measured using a modulated fluorimeter (PAM-2000, Walz, Effeltrich,
Germany). Three plants were measured from each of four replicate
lamp arrays, and the values given are the means (±standard error of
the mean) of the four replicate arrays. No significant UV-B effects
(P>0.05) were detected in any of these parameters in the analysis of
variance of the complete data set in Allen et al. (1998).
Parameter
Control
UV-B
A ( mmol m−2 s−1)
sat
V
( mmol m−2 s−1)
c,max
J
( mmol m−2 s−1)
max
Stomatal limitation (%)
Pre-dawn F /F
v m
Total leaf area (cm2)
Total dry weight (g)
14.9±1.2
107.1±7.9
272.0±15.8
42.9±3.4
0.812±0.004
363±34
2.73±0.29
13.8±1.7
97.1±13.9
256.4±27.0
43.4±3.2
0.807±0.007
366±22
3.04±0.10
Mepsted et al., 1996), stomatal conductance (Flint et al.,
1985; Beyschlag et al., 1988), maximum or steady-state
w (Caldwell et al., 1994; Mepsted et al., 1996; Stephen
PSII
et al., 1998). The weight of evidence emerging from these
modulated UV-B field experiments suggests that current
predictions for O depletion will not adversely affect plant
3
productivity and photosynthesis in crops directly. The
discrepancy between the results from square-wave and
modulated UV-B field supplementation systems does support the contention that square-wave systems may exaggerate plant responses to UV-B supplementation, as
suggested by Fiscus et al. (1994). In a comparison of
these two types of irradiation system Sullivan et al. (1994)
attempted to simulate a 25% O depletion scenario in
3
Maryland, USA (39° N ). Reductions in soybean photosynthetic capacity, leaf area and seed yield were observed
under the square-wave but not the modulated treatment.
These reductions were associated with a 30% greater
UV-B irradiance and larger UV-B5PPFD5UV-A ratios
in the square-wave system as it could not respond to
intermittent cloud cover, unlike the modulated system
(Sullivan et al., 1994).
and adaxial stomatal closure. However, even under these
extreme UV-B exposures, acclimation (e.g. induction of
UV-B absorbing flavonoids) can protect the photosynthetic processes. Photosynthetic productivity can be
depressed by UV-B interfering with development processes. A reduction in productivity is usually associated
with a reduced ability to intercept light (i.e. smaller leaf
area) and not an inhibition of photosynthetic competence.
Predictions of plant responses to O depletion are suspect
3
from square-wave irradiance experiments in the field and
controlled environments due to the increased sensitivity
of plants to UV-B at low PPFD and UV-A irradiances.
Effects on photosynthetic competence and lightinterception under conditions of high UV-B intensities,
relative to PPFD and UV-A, do not appear to have any
significance under field conditions with realistic modulated UV-B irradiances. However, UV-B may induce
subtle changes in plant morphology and secondary metabolism (flavonoids and related phenolic compounds like
furanocoumarin and lignin; Caldwell et al., 1995) which
could have important ecosystem-level effects such as
changes in competitive balance between plant species
(Barnes et al., 1995; Johanson et al., 1995), alterations in
disease, herbivory and decomposition (McCloud and
Berenbaum, 1994; Orth et al., 1990; Panagopoulos et al.,
1992; Newsham et al., 1996) and interactions with other
environmental stresses and pollutants (for reviews see
Bornman and Teramura, 1993; Tevini, 1993; Teramura
and Sullivan, 1994; Caldwell and Flint, 1994; Jordan,
1996). It was concluded that O depletion and the concur3
rent rise in UV-B irradiance is not a direct threat to
photosynthetic productivity of crops and natural vegetation and it may be more appropriate to focus on the
effects of elevated UV-B on plant development and the
associated processes.
Acknowledgements
This work was supported by a research studentship to DJA
from the UK Biotechnology and Biological Sciences Research
Council and research grants to NRB from the UK Natural
Environment Research Council and to SN from Generalitat de
Catalunya (19976BEAI300006222). We are grateful to James
Morison ( University of Essex, UK ) for discussions on stomata,
and to Andy McLeod ( University of Edinburgh, UK ) and
Peter Greenslade (Institute of Terrestrial Ecology, Monks
Wood, UK ) for access to the UV-B field facility and
spectroradiometer.
Conclusions
In answer to the question of whether it is likely that O
3
depletion is likely to lead to inhibition of photosynthetic
productivity, the following findings need to be considered.
Direct UV-B-induced inhibition of photosynthetic competence is observed only at high UV-B irradiances and
primarily involves the loss of soluble Calvin cycle enzymes
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