OR I G I N A L R E S E A R CH
Weaker photosynthetic acclimation to fluctuating than to
corresponding steady UVB radiation treatments in grapevines
Chenxing Su-Zhou1,2,6 | Maxime Durand2 | Pedro J. Aphalo2 |
Javier Martinez-Abaigar3 | Alexey Shapiguzov2,4 | Hirofumi Ishihara2 |
Xu Liu1,6 | T. Matthew Robson2,5
1College of Enology, Northwest A&F
University, Yangling, Shaanxi, China
2Organismal and Evolutionary Biology (OEB),
Viikki Plant Science Centre (ViPS), Faculty of
Biological and Environmental Sciences,
University of Helsinki, Helsinki, Finland
3Faculty of Science and Technology,
University of La Rioja, Spain
4Natural Resources Institute Finland (Luke),
Production Systems, Finland
5National School of Forestry, University of
Cumbria, Ambleside, UK
6Shaanxi Engineering Research Center for
Viti-Viniculture, Yangling, Shaanxi, China
Correspondence
Xu Liu,
Email: liuxu@nwafu.edu.cn
T. Matthew Robson,
Email: matthew.robson@helsinki.fi
Funding information
Research Council of Finland, Grant/Award
Numbers: 324555, 351008; China Scholarship
Council, Grant/Award Number:
202206300065; Novo Nordisk Plant Science,
Agriculture and Food Biotechnology,
Grant/Award Number: NNF20OC0065026;
Government of La Rioja, Grant/Award
Number: Afianza 2023/05
Edited byW.S.(F.) Chow
Abstract
The effects of transient increases in UVB radiation on plants are not well known;
whether cumulative damage dominates or, alternately, an increase in photoprotection
and recovery periods ameliorates any negative effects. We investigated photosynthetic
capacity and metabolite accumulation of grapevines (Vitis vinifera Cabernet Sauvignon)
in response to UVB fluctuations under four treatments: fluctuating UVB (FUV) and
steady UVB radiation (SUV) at similar total biologically effective UVB dose (2.12 and
2.23 kJ m
2 day
1), and their two respective no UVB controls. We found a greater
decrease in stomatal conductance under SUV than FUV. There was no decrease in
maximum yield of photosystem II (Fv/Fm) or its operational efficiency (ɸPSII) under the
two UVB treatments, and Fv/Fm was higher under SUV than FUV. Photosynthetic
capacity was enhanced under FUV in the light-limited region of rapid light-response
curves but enhanced by SUV in the light-saturated region. Flavonol content was simi-
larly increased by both UVB treatments. We conclude that, while both FUV and SUV
effectively stimulate acclimation to UVB radiation at realistic doses, FUV confers
weaker acclimation than SUV. This implies that recovery periods between transient
increases in UVB radiation reduce UVB acclimation, compared to an equivalent dose of
UVB provided continuously. Thus, caution is needed in interpreting the findings of
experiments using steady UVB radiation treatments to infer effects in natural environ-
ments, as the stimulatory effect of steady UVB is greater than that of the equivalent
fluctuating UVB.
1 | INTRODUCTION
In the natural environment, fluctuating light is more common than
steady light because of clouds and because of wind causing canopy
movement (Kaiser et al., 2018). Light is one of the most unstable com-
ponents of plants' environment. Even at the very top of the canopy
on a sunny day, steady light conditions are uncommon. Large
fluctuations in irradiance (sunlight received) happen over short (less
than 1 s; Assmann & Wang, 2001) and long (minutes or longer;
Smith & Berry, 2013) timescales. In natural environments, plant cano-
pies are subject to transient changes in cloudiness through the day,
producing fast changes in irradiance. These changes prompt the need
for mechanisms allowing physiological acclimation to these conditions
(Kromdijk et al., 2016; Barnes et al., 2017; Wu et al., 2023).
Received: 3 March 2024 Revised: 17 May 2024 Accepted: 25 May 2024
DOI: 10.1111/ppl.14383
Physiologia Plantarum
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2024 The Author(s). Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.
Physiologia Plantarum. 2024;176:e14383. wileyonlinelibrary.com/journal/ppl 1 of 14
https://doi.org/10.1111/ppl.14383
In the biosphere, UV radiation is a minor portion of sunlight
(Björn, 2015), and only UVA (315–400 nm) and UVB (280–315 nm)
radiation at wavelengths greater than 290 nm can reach the Earth's
surface. Photon irradiance of UVB radiation is equivalent to, at most,
0.33% of the photosynthetically active radiation (PAR, 400–700 nm;
Aphalo, 2018). Nevertheless, UVB photons carry the most energy
among those spectral regions reaching the Earth's surface. High UVB
irradiance can cause detrimental effects on plants, directly or indi-
rectly, inducing damage to DNA (Landry et al., 1997), proteins
(Schmelzer et al., 1988; Willekens et al., 1994), and membranes
(Britt, 1996). However, testing the effects of UVB radiation in con-
trolled indoor conditions makes any results difficult to extrapolate to
the natural environment. Plant defenses are typically well adapted
to solar UVB radiation; this means that they acclimate effectively to
regional increases in solar UVB radiation caused by stratospheric
ozone depletion and changes in atmospheric pollution (Barnes
et al., 2023). Hence, the focus of most research has shifted to identi-
fying the role of UVB radiation in regulating plant growth and devel-
opment (Hideg et al., 2013; Robson et al., 2015).
Grapevine (Vitis vinifera L.) is an important berry crop widely
grown in many regions of the world (Anderson & Nelgen, 2020). It is a
light-demanding species that grows through the whole summer
(Coombe, 1995). Cabernet Sauvignon is the most common cultivar
worldwide and is planted in more than 80% of countries cultivating
grapevine (Anderson & Nelgen, 2020). The amount of solar radiation
received by grapevines directly affects canopy photosynthesis, and its
spectral quality modifies the accumulation of leaf secondary metabolites
(Del-Castillo-Alonso et al., 2016; Petrie et al., 2003). Despite causing
stimulation of photoprotective pigments, UVB radiation may also
impede carbon fixation by grapevine at high elevations (Berli
et al., 2013). This may consequently affect the source-sink balance and
allocation to primary vs secondary metabolism (Ollat & Gaudillere,
2000). Additionally, the photoassimilate could act as a feedback control
that integrates sugar production with environmental factors to regulate
photosynthesis (Henry et al., 2020; Lastdrager & Smeekens, 2014).
While the response of plants to short- and long-term exposure to
UVB radiation has been compared to assess the induction of photoprotec-
tion (Hazard et al., 1997; Martínez-Lüscher et al., 2013), the question of
how plants respond to fluctuating UVB radiation remains unresolved. Brief
exposure (< 24 h) of non-acclimated plants to UVB radiation can cause
photoinhibition and damage through reactive oxygen species (Hazard
et al., 1997), whereas plants subject to longer exposure (> 24 h) to UVB
radiation typically accumulate UVB-absorbing compounds and display
morphological adaptations to high light. These acclimations often amelio-
rate photoinhibition and alleviate damage caused by acute UVB radiation
through the action of antioxidants (Agati et al., 2012; Martínez-Lüscher
et al., 2013; Shi et al., 2004; Wargent et al., 2011; Zhao et al., 2020). The
phenotype of plants under fluctuating UVB radiation is likely to be a com-
promise between the rapid responses and long-term acclimation to UVB
radiation. It is still unclear whether acute reactions caused by cumulative
transient periods of high light dominate or if the periods in-between UV
exposure are utilized to relax from stress. Discovering the answer to this
question is particularly relevant to field crops, which grow under naturally
fluctuating UVB irradiance. A step towards more confidently inferring the
role of UVB radiation in acclimation vs. damage to the photosynthetic
apparatus under natural conditions is thus to study how plants respond
to well-defined artificial fluctuations in UVB irradiance.
Combinations of UVB radiation and PAR were used here to inves-
tigate the acclimation response of grapevine leaves to fluctuating and
steady UVB radiation. The fluctuating UVB radiation treatment was alter-
nately on and off for 15-minute periods, which is within the range of
sun/shade patterns from sunflecks or under broken cloud (Smith &
Berry, 2013). Both steady and fluctuating UVB treatments provided the
same average biologically effective UVB irradiance on a daily basis. A
background treatment of PAR was provided to allow normal plant pro-
cesses of growth and defence, while not being so strong that potential
effects of UVB radiation might be expected to be masked by responses
to PAR (Roeber et al., 2021). This experiment addresses three questions:
(1) how does photosynthetic capacity differ in response to fluctuating and
steady UVB radiation; (2) are pigments, sugars and starch accumulation
affected differently by fluctuating and steady UVB radiation; and (3) are
there differences in the relationship between photosynthesis and metab-
olite contents under fluctuating and steady UVB radiation?
2 | MATERIALS AND METHODS
2.1 | Plant materials and light treatments
One-year-old grapevine plants (Vitis vinifera L. cv Cabernet Sauvignon)
grafted to 110R rootstocks (Viveros Provedo) were planted in 10 L
pots containing a 7:2:2 mix of peat: sand: vermiculite. Specifically,
these are F6 peat (Kekkilä); blowing sand 0.5–1.2 mm (Weber); Agra-
vermiculite 0–2 mm (Pull Rhenen).
The grapevines were grown in a greenhouse (17/02/2023–
23/04/2023) divided into compartments partitioned by curtains made
from black-white plastic film blocking solar radiation. The greenhouse
air temperature was maintained at 25C/16C day/night and relative
humidity at 45%/75% day/night. Plants were grown under LED lamps
(AP67 and AP3, Valoya Oy), giving steady photosynthetically active
radiation (PAR; 170 μmol m
2 s
1) from 05:00 to 21:00 (local time).
The UVB treatments commenced when the eighth leaf (counting
from the base to the apex) of each grapevine became mature, and
were administered ±3 h from 12:00 (09:00 to 15:00). The UVB treat-
ments were as follows: (1: FUV) fluctuating UVB radiation treatment
(1.115 ± 0.112 μmol m
2 s
1), the fluctuating UVB radiation treat-
ment was on for 15 min and then turned off for 15 min, and that the
cycle was repeated during the photoperiod for six hours, and (2:
cFUV) its no UVB radiation control; (3: SUV) steady UVB radiation
treatment (0.508 ± 0.065 μmol m
2 s
1) and (4: cSUV) its no UVB
radiation control. Plants under both the FUV and SUV treatments
received the equivalent daily integrated dose of UVB radiation:
total daily photon irradiance of unweighted UVB radiation was
12.05 ± 1.21 and 10.98 ± 1.41 mmol m
2 day
1 calculated as 2.23 ± 0.25
and 2.12 ± 0.35 kJ m
2 day
1 biologically effective UVB energy irra-
diance (Table S1); weighted according to Green's formulation of
2 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Caldwell's Generalized Plant Action Spectrum normalized to the
same irradiance value as the unweighted measurement at 300 nm
(Aphalo et al., 2012). Broadband UVB-313-nm fluorescent tubes
(Q-Lab Europe, Ltd.) were used to produce four UVB radiation treat-
ments. A polyester filter (0.125 mm thick, Autostat CT5; Thermoplast),
which blocks UVB radiation up to 315 nm wavelengths, was used to
create controls without UVB radiation. A cellulose-diacetate filter
(0.095 mm thick, Kotelo-Rauma Oy), which blocks UV-C radiation but
transmits UV radiation over 280 nm, was used to create the UVB
treatments. The cellulose diacetate film was changed weekly to avoid
the transmittance reduction caused by its photodegradation. UVB treat-
ments and controls were created by wrapping filter material around half
the length of each UVB tube. The two halves of each fluorescent tube
were divided using a polyester filter curtain. Each treatment was repli-
cated twice and compartmentalized using black-white plastic film; the
white side always facing the plants. Three plants were grown under four
light treatments in two replicate compartments (i.e., 3 plants  4 treat-
ments  2 replicate blocks = in total 24 plants). The UVB irradiance
was recorded (Figure S1 and Table S1) with a calibrated array spectrora-
diometer (Maya 2000 Pro, Ocean Optics Inc.) using a protocol devised
for this purpose detailed in Robson & Aphalo (2019).
2.2 | Measurements of photosynthetic parameters
Photosynthetic parameters were measured on one leaf from each plant
(on the fourth to sixth leaf from the base to the apex). Stomatal conduc-
tance (gs) and operating efficiency of photosystem II (ɸPSII) were mea-
sured under the light treatments using a leaf porometer/fluorometer
(LI-600, LI-COR). To obtain a time series through the day, measure-
ments of gs and ɸPSII were taken every 15 min; 5 min after each change
of fluctuating UVB radiation. Two measurements were made before the
UVB radiation began (at 07:30 and 08:30) and two after the end of daily
UVB radiation (15:30 and 16:30), every three days from the first day
after UVB treatment commenced for five measurement days in total.
Chlorophyll fluorescence fast-transient analysis (OJIP) was mea-
sured using a FluorPen FR 100 (Photon Systems Instruments (PSI)) in
order to examine the dynamics of photochemistry under fluctuating
light. Leaves were dark-adapted for 30 min using darkening clips,
then exposed to a saturating pulse of photon irradiance
2700 μmol m
2 s
1 (peak at 470 nm wavelength). The fluorescence
intensities at 50 μs (Fo), 2 ms (J-step, Fj), 60 ms (I-step, Fi) and maximum
variable fluorescence at 300 ms (Fm) were used for this calculation.
Relative variable fluorescence at the J-step and I-step were calculated
as Vj = (Fj 
 Fo)/(Fm 
 Fo) and Vi = (Fi 
 Fo)/(Fm 
 Fo). The maximum
quantum yield of photosystem II (Fv/Fm) was calculated as (Fm 
 Fo)/Fm.
The OJIP curves were recorded three times at 08:30 (morning), 12:00
(midday) and 15:30 (afternoon) on the same days as ɸPSII.
Electron transport rate (ETR) and ɸPSII were recorded during rapid
light-response curves (RLCs), where the actinic illumination increased
stepwise from 10 to 1500 μmol photons m
2 s
1 every 30 s
(mini-PAM, Walz GmbH). The ETR PAR-response curve fits the func-
tion of Eilers & Peeters (1988):
ETR¼ PAR
aPAR2þbPARþc ð1Þ
where ETR and PAR are assessed by mini-PAM from the measure-
ments; a, b and c are nondimensional fundamental parameters. From
these, the initial slope in the light-limiting region (α), maximum elec-
tron transport rate (ETRmax), maximum saturating irradiance (Ik) and
operating saturating irradiance (Im) were calculated as:
α¼1=c ð2Þ
ETRmax ¼ 1
bþ2 ffiffiffiffiffiacp ð3Þ
Ik ¼ c
bþ2 ffiffiffiffiffiacp ð4Þ
Im¼
ffiffiffi
c
a
r
ð5Þ
Measurements were carried out from 09:30 to 11:00 for each grape-
vine on the last day of measurements.
2.3 | Measurements of leaf pigments
Optical indices of chlorophyll content and epidermal phenolics (flavo-
nols and anthocyanins) were non-destructively measured by Dualex
Scientific + (FORCE-A) on a per area basis (Cerovic et al., 2012). The
same leaf was used for leaf pigment measurement and photosynthetic
parameters on each plant, and all pigments were recorded at 12:00,
every three days from the first day after UVB treatment commenced
and five measurement days in total.
2.4 | Analysis of Photoassimilates
Glucose, fructose, sucrose, and starch were analyzed from grapevine
leaves harvested at the end of the daily UVB radiation treatment
(15:00), 7 and 13 days after the treatments commenced. A different
leaf from that chosen for photosynthesis parameters and pigments
was measured (but of the same age), frozen in liquid nitrogen immedi-
ately after harvesting, then freeze-dried. Sugars and starch were
extracted and measured as described in Stitt et al. (1989). The super-
natants of ethanolic extracts were used to analyze glucose, fructose
and sucrose using a Megazyme Sucrose, D-Fructose and D-Glucose
kit (Megazyme). The insoluble pellets were used to analyze starch
(Stitt et al., 1989).
2.5 | Data Analysis
Statistical analyses were performed using R version 4.1.3 (R Core
Team, 2022). A linear model was used to test for the effects of
SU-ZHOU ET AL. 3 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
treatments against the parameters of the RLC (a more-complex model
was not used so as to avoid overfitting). All other analyses were done
using linear mixed-effects (LME) models with the package lme4
(Bates et al., 2015) and lmerTest (Kuznetsova et al., 2017). The two
replicate blocks were considered random-effects factors, and
repeated measurements were made on the same leaf. The specific
effects on photosynthetic parameters and metabolite contents of
treatments, the time course (as days after the treatments com-
menced), time of day, and their interactions, were investigated
using a Type II ANOVA with Satterthwaite's method (Kuznetsova
et al., 2017). To accommodate minor differences in the incident
PAR received by leaves caused by small differences in their display
angle or height, PAR (recorded by LI-600) was treated as a covari-
ate in the LME model for gs and ɸPSII. Post-hoc pairwise compari-
sons were performed to test differences among factors with
packages car (Fox & Weisberg, 2019), emmeans (Searle
et al., 1980), and multcomp (Hothorn et al., 2008). Only the differ-
ence between steady and fluctuating UVB treatments, and
between UVB treatment and control, were of interest; thus, the
adjusted P-values (adj. P) were calculated only for the following
contrasts: FUV-SUV, cFUV-cSUV, FUV-cFUV and SUV-cSUV.
Relationships between photosynthetic parameters and metabolite
concentrations were examined using linear models. Pigments, mea-
sured once on each measurement day, were compared against a daily
average for each sample of gs, ɸPSII and Fv/Fm to test for correlation.
Sugars and starch, analysed once at the end of daily UVB radiation on
7 and 13 days after the treatments commenced, were correlated
against the last of gs, ɸPSII and Fv/Fm recordings taken during the daily
UVB radiation period on these days. Differences were considered sta-
tistically significant when P < 0.05.
3 | RESULTS
3.1 | Response of stomatal conductance to
fluctuating and steady UVB radiation
On average through the day, leaf stomatal conductance (gs) was
21.9% lower (adj. P < 0.001) in the steady UVB (SUV) treatment com-
pared to its control (cSUV; Figure 1a; Table S2a,b), and likewise lower
than fluctuating UVB (FUV) by 11.2% (adj. P < 0.001); while gs was
only 8.7% lower (adj. P < 0.001) in FUV compared to its control
(cFUV). The diurnal pattern of gs involved a decline in all treatments
after 11:45 compared to the first daily measurement at 7:30 (adj.
P = 0.028). The gs under SUV was lower than that under cSUV from
the first day of UVB treatment (Figure 1b), and it remained consis-
tently lowest in this treatment during the whole experiment. The dif-
ference between the effects of SUV and cSUV mostly remained
between 10–20%, except on Day 7 when it increased to 28.6%. The
overall decrease in gs due to UVB radiation was greater for SUV than
for FUV (related to their respective controls) over the whole experi-
ment. The results indicated that steady UVB, and to a lesser extent
fluctuating UVB treatments, suppressed leaf gas exchange and that
the effect was sustained over several days of treatments.
3.2 | Response of photosynthetic apparatus to
fluctuating and steady UVB radiation
Both FUV and SUV radiation treatments were accompanied by
increases in operating efficiency of photosystem II (ɸPSII) in grapevine
leaves compared with their no UVB controls (Figure 2). Under FUV,
0.00
0.05
0.10
0.15
7:30 8:30 9:00 12:00 15:00 15:30 16:30
0.00
0.05
0.10
0.15
1 4 7 10 13
Time of day Days after the commencement of the treatments
St
om
at
al
 c
on
du
ct
an
ce
 (m
ol
 m
-2
 s
-1
)
(a) (b)
St
om
at
al
 c
on
du
ct
an
ce
 (m
ol
 m
-2
 s
-1
)
cFUV
FUV
cSUV
SUV
F IGURE 1 Stomatal conductance (gs) of grapevine leaves grown under fluctuating and steady UVB treatments and controls. (a) Changes in gs
during the day. (b) Changes in gs with days after the UVB treatment commenced. Measurements on grapevine leaves grown under fluctuating
UVB radiation (FUV, dark purple) and its attenuated UVB controls (cFUV, light purple), steady UVB radiation (SUV, dark green) and its attenuated
UVB controls (cSUV, light green). One day before the UVB radiation commenced, the daily average of gs was 0.110 ± 0.004, with no significant
difference across the treatment combinations. Data presented are the mean ± SE across replicate blocks (n = 6 replicate compartments in which
plants were measured in (a) and n = 168 total daily measurements in (b)).
4 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
mean ɸPSII was 0.70 ±< 0.01 and under cFUV 0.67 ±< 0.01 (adj.
P < 0.001; Table S3a,b). Under SUV mean ɸPSII was 0.70 ±< 0.01 and
under cSUV 0.68 ±< 0.01 (adj. P < 0.001). The difference in ɸPSII
between FUV and SUV is statistically significant (marginally higher in
SUV adj. P < 0.001), but unlikely to be biologically important. Over
the course of the experiment, ɸPSII increased in all four treatments
(F = 38.0; P < 0.001). Notably, the gradual increase in ɸPSII caused by
FUV (adj. P < 0.001) and SUV (adj. P < 0.001) compared to each of
the control treatment was apparent from the first day of UVB treat-
ment (Figure 2).
The chlorophyll a fluorescence transient (OJIP) was further used
to probe the function of photosystem (PS) II and photosynthetic elec-
tron transport (Figure 3a). When kinetics profiles were normalized to
Fo, the increase in intensity of chlorophyll fluorescence was larger in
SUV than in FUV, and both were larger than their corresponding con-
trols. Analysis of relative shapes of OJIP profiles revealed significantly
lower relative variable fluorescence at the J-step (Vj) and the I-step
(Vi) in SUV compared to cSUV (adj. P = 0.028, 0.010), and lower Vj in
SUV compared to FUV (adj. P = 0.001) (Figure 3b,c; Table S4a,b). A
similar but smaller difference was found in Vi of FUV compared to
cFUV (adj. P = 0.002). Taken together, these results indicated differ-
ent redox states of the photosynthetic electron transport chain under
different treatments. There was an increase in maximum quantum
yield of PSII (Fv/Fm) in SUV (adj. P < 0.001) and FUV (adj. P < 0.001)
compared with their respective no UVB controls (Figure 3d;
Table S4a,b). Additionally, the increase in Fv/Fm under SUV (0.75
±< 0.01) was marginally higher than FUV (0.74 ± < 0.01, adj.
P = 0.060). The OJIP curves and pulse-saturation census both found
that UVB radiation increased the maximum quantum yield of PSII, par-
ticularly under SUV.
The parameters of light-limited and light-saturated regions of
rapid light curves (RLCs) were calculated to investigate the effect
of UVB radiation on photosynthetic capacity (Tables 1 & S5). Plants
grown under FUV responded to RLCs with a steeper initial slope (α)
than plants from cFUV (adj. P = 0.021), but this was not the case
when comparing SUV and cSUV (adj. P = 0.228). However, the maxi-
mum electron transport rate (ETRmax), maximum saturating irradiance
(Ik) and the operating saturating irradiance (Im) increased in SUV com-
pared to cSUV (adj. P = 0.008, 0.009 and 0.026 respectively), but not
in FUV compared to cFUV (adj. P = 0.641, 0.486 and 0.542 respec-
tively; Table S5B). Thus, FUV mainly enhanced the light-limited
period, and SUV enhanced the light-saturated region of RLCs.
3.3 | Response of chlorophyll and epidermal
pigments to fluctuating and steady UVB radiation
Epidermal flavonols accumulated during the treatment period; more
so under the FUV (adj. P = 0.008) and SUV (adj. P = 0.009) radiation
treatments than their controls from 7 days after treatment com-
menced onwards (Table S6a,c), while there was no significant differ-
ence between the FUV and SUV overall (adj. P = 0.294; Figure 4a;
Table S6b). Epidermal flavonol and leaf chlorophyll accumulation
covaried over the UVB treatment period (R = 0.76, P < 0.001;
Figure S2a). The chlorophyll content in both FUV (32.4 ± 0.5) and
SUV (34.2 ± 0.7) was significantly higher than that in cFUV (28.3
± 0.8, adj. P < 0.001) and cSUV respectively (29.9 ± 1.0, adj.
P < 0.001; Figure 4b; Table S6a,b). However, the accumulation of epi-
dermal anthocyanins in response to UVB radiation responded gener-
ally in the opposite way to epidermal flavonols (R = 
0.66,
P = 0.002; Figure S2b). The concentration of anthocyanins in the
upper epidermis of FUV (0.231 ± 0.002) and SUV (0.226 ± 0.003)
leaves was lower than cFUV (0.251 ± 0.004, adj. P < 0.001) and cSUV
(0.247 ± 0.005, adj. P < 0.001) respectively. Additionally, pigment
concentrations were correlated with chlorophyll fluorescence parame-
ters in grapevine leaves (Figure 5). Epidermal flavonol and leaf chloro-
phyll concentrations were positively correlated, and epidermal
anthocyanins negatively correlated with both Fv/Fm (R = 0.49,
P = 0.027; R = 0.59, P = 0.006; R = 
0.65, P = 0.002, respectively)
and ɸPSII (R = 0.76, P < 0.001; R = 0.87, P < 0.001; R = 
0.82,
P < 0.001, respectively). Over the whole experiment, FUV and SUV
had similar effects on pigment accumulation of mature grapevine
leaves: increases in chlorophylls and epidermal flavonols, and a
decrease in epidermal anthocyanins.
3.4 | Response of leaf photoassimilate content to
fluctuating and steady UVB radiation
Leaf glucose accumulated more under SUV than cSUV both 7 days
(by 76.1%, adj. P = 0.039) and 13 days (by 54.2%, adj. P < 0.001) after
0.60
0.65
0.70
1 4 7 10 13
Days after the commencement of the treatments
O
pe
ra
tin
g 
ef
fic
ie
nc
y 
of
 p
ho
to
sy
st
em
 II
 (ɸ
PS
II) 
cFUV
FUV
cSUV
SUV
F IGURE 2 Operating efficiency of photosystem II (ɸPSII) of
grapevine leaves grown under fluctuating and steady UVB treatments
and controls. Treatments are fluctuating UVB radiation (FUV, dark
purple) and its attenuated UVB controls (cFUV, light purple), steady
UVB radiation (SUV, dark green) and its attenuated UVB controls
(cSUV, light green). Data are the mean ± SE across replicate blocks
(n = 168 total daily measurements).
SU-ZHOU ET AL. 5 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
UVB radiation commenced (Figure 6a; Table S7a,b). Similarly, leaf
fructose content under SUV was significantly higher than under cSUV
on Day 13 (adj. P < 0.001; Figure 6b; Table S7a,b). Additionally, the
pattern of leaf sucrose accumulation in response to SUV differed from
those of glucose and fructose. Although sucrose concentration
appeared to have decreased slightly after 7 days under SUV compared
to cSUV, any change was not statistically significant (adj. P = 0.292;
Figure 6c; Table S7a,b). However, after 13 days under SUV there was
R
el
at
iv
e 
va
ria
bl
e 
flu
or
es
ce
nc
e 
at
 th
e 
J-
st
ep
 (2
 m
s)
 fr
om
 O
JI
P 
te
st
 (V
j) 
R
el
at
iv
e 
va
ria
bl
e 
flu
or
es
ce
nc
e 
at
 th
e 
I-s
te
p 
(6
0 
m
s)
 fr
om
 O
JI
P 
te
st
 (V
i) 
M
ax
im
um
 q
ua
nt
um
 y
ie
ld
 o
f p
ho
to
sy
st
em
 ll
 
(F
v/
Fm
)
0.00
0.70
4
0.75
4
4
0.00
0.75
0.80
0.00
0.60
0.65
0.70
Treatment
Treatment
cFUV FUV cSUV SUV
Treatment
cFUV FUV cSUV SUV
Time (msec) 
cFUV FUV cSUV SUV
(b)
(c) (d)
0.1 1 10 100 1000
Ch
lo
ro
ph
yl
l F
lu
or
es
ce
nc
e 
No
rm
al
ize
d 
to
 F
o 4
3
2
1 Fo
Fj
Fm
Fi
cFUV
FUV
cSUV
SUV
(a) **
*
* ***
**
***
F IGURE 3 Chlorophyll fluorescence fast-transient analysis (OJIP) of grapevine leaves grown under fluctuating and steady UVB treatments
and controls. (a) Kinetics of OJIP, normalized to Fo, with time plotted on a logarithmic axis. (b) Relative variable fluorescence at the J-step (Vj).
(c) Relative variable fluorescence at the I-step (Vi). (d) Maximum quantum yield of photosystem II (Fv/Fm). Measurements were taken in the 30 min
dark-adapted leaves grown under fluctuating UVB radiation (FUV, dark purple) and its attenuated UVB controls (cFUV, light purple), steady UVB
radiation (SUV, dark green) and its attenuated UVB controls (cSUV, light green). Data in b, c, d are presented as the mean ± SE across replicate
blocks (n = 90 OJIP curves). Significant difference for adjusted P-values (adj. P) *< 0.05, **< 0.01 and ***< 0.001.
TABLE 1 Initial slope in the light limiting region (α), maximum electron transport rate (ETRmax), maximum saturating irradiance (Ik) and
operating saturating irradiance (Im) derived from rapid light-response curves. Data represent mean values ± SE with n = 6 for each treatment.
Treatments α electron/photons ETRmax μmol electronsm
2 s
1 Ik μmol electronsm
2 s
1 Im μmol electronsm
2 s
1
cFUV 0.306 ± 0.007 116.1 ± 8.2 380.3 ± 28.8 1076.0 ± 89.0
FUV 0.337 ± 0.007 120.4 ± 6.4 357.8 ± 20.8 997.6 ± 49.3
cSUV 0.314 ± 0.007 110.4 ± 6.8 323.6 ± 22.4 1044.9 ± 50.8
SUV 0.331 ± 0.007 142.9 ± 3.2 434.8 ± 15.6 1297.1 ± 64.7
6 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
a clear effect of SUV (45.3% relative reduction, adj. P = 0.009). Like-
wise, leaves in SUV contained, on average, 45.2% less starch
than those in cSUV (adj. P = 0.008; Figure 6d; Table S7a,b). Over-
all, differences between the FUV and cFUV, while presenting
similar trends to those of SUV and cSUV, were much less pro-
nounced and generally not significant (Figure 6). With respect to
the contents of photoassimilates (sugars and starch), no signifi-
cant correlation with photosynthetic capacity was detected
(Figure S3).
4 | DISCUSSION
4.1 | Steady UVB stimulates stomatal closure more
than equivalent fluctuating UVB
Stomatal movements are one of the main processes regulating photo-
synthesis in higher plants. In this study, a decrease in gs of grapevine
leaves was recorded under steady UVB relative to its control, whereas
a generally smaller decline in gs was caused by fluctuating UVB than
0.20
0.40
0.60
1 4 7 10 13
Days after the commencement of the treatments
U
pp
er
 E
pi
de
rm
al
 F
la
vo
no
l A
bs
. 3
75
 n
m
0.20
0.25
0.30
1 4 7 10 13
Days after the commencement of the treatments
U
pp
er
 E
pi
de
rm
al
 A
nt
ho
cy
an
in
 A
bs
. 5
15
 n
m
20
30
40
1 4 7 10 13
Days after the commencement of the treatments
Le
af
 C
hl
or
op
hy
ll 
C
on
te
nt
 (O
pt
ic
al
 In
de
x)
(b)
(c)
(a)
cFUV
FUV
cSUV
SUV
F IGURE 4 Pigments content in grapevine leaves grown under fluctuating and steady UVB treatments and controls. The y-axis scale is the
optical index from Dualex Scientific + (arbitrary units) on a per-leaf-area basis. (a) Epidermal flavonols, (b) leaf chlorophyll, (c) epidermal
anthocyanin. Measurements were taken under fluctuating UVB radiation (FUV, dark purple) and its attenuated UVB controls (cFUV, light purple),
steady UVB radiation (SUV, dark green) and its attenuated UVB controls (cSUV, light green). Data are the mean ± SE across replicate blocks
(n = 6). One day prior to the UVB radiation commenced, the daily averages were: epidermal flavonols 0.32 ± 0.01, leaf chlorophyll 28.07 ± 0.77
and epidermal anthocyanin 0.213 ± 0.006, with no significant difference across the treatment combination.
SU-ZHOU ET AL. 7 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
its control (Figure 1). This decrease in gs caused by UVB radiation is in
line with that reported for leaves of Vitis vinifera L. cv. Malbec (Berli
et al., 2013). Because gs depends in part on the stomatal aperture, this
result is also consistent with the decrease in stomatal aperture from
around 2.8 to 2.2 μm reported for Arabidopsis thaliana after a UVB
treatment of 3 h at 1.5 μmol m
2 s
1, or 1 h at 5.5 μmol m
2 s
1
(Tossi et al., 2014). In our study, FUV and SUV treatments, at equiva-
lent total integrated UVB doses, produced different effects on gs of
grapevines. This implies that not only the total UVB dose but also the
highest transient UVB irradiance and the exposure period all affect gs
response. A recent meta-analysis suggests that gs is mediated by a
network of UVB-regulated signalling pathways (Jansen et al., 2022;
He et al., 2013). The reduced effect of FUV on gs, compared with
SUV, may occur because 15 min UVB radiation in FUV is not long
enough to induce a signal that would suppress stomatal conductance.
In SUV, gs was lower than in its control on the first day after the start
of UVB irradiation, and it continued to decline from Day 1 to Day 7.
The comparative dynamics of these responses indicate that the estab-
lishment of stomatal signalling pathways may result in persistent sup-
pression of gs, but the mechanism of these pathways is yet to be
determined. Recovery following transient UV radiation has been
reported to increase stomatal density and aperture in Mentha spicata
L., allowing greater stomatal control in UV treatment plants than in
plants never exposed to UV radiation (Crestani et al., 2023). Accord-
ingly, a 15-min relaxation period following UVB in FUV treatments
may ameliorate UVB-induced effects on the functioning and/or devel-
opment of stomata.
4.2 | Steady and fluctuating UVB differ in the
extent to which they affect photosynthesis
The effects of fluctuating and steady UVB radiation on photosyn-
thetic capacity were compared through measurements of quantum
0.30
0.35
0.40
0.45
0.50
0.55
0.60
Ep
id
er
m
al
 F
la
vo
no
l C
on
te
nt
 (A
.3
75
 n
m
) (a)
R = 0.49 | P = 0.027
20
25
30
35
40
Le
af
 C
hl
or
op
hy
ll 
C
on
te
nt
 (O
pt
ic
al
 In
de
x) (c)
R = -0.59 | P = 0.006
0.20
0.22
0.24
0.26
Ep
id
er
m
al
 A
nt
ho
cy
an
in
 C
on
te
nt
 (A
.5
15
 n
m
)
Maximum Quantum Yield of PSII
(e)
R = 0.65 | P = 0.002
(b)
R = 0.76 | P  < 0.001
(d)
R = -0.87 | P  < 0.001
0.66 0.72
Effective Quantum Yield of PSII
(f)
R = 0.82 | P < 0.001
Day 1 
Day 4
Day 7
Day 10
Day 13
cFUV
FUV
cSUV
SUV
0.71 0.72 0.73 0.74 0.75 0.76 0.68 0.70
F IGURE 5 The relationship between
photosynthetic capacities and pigments
content in the grapevine leaves grown
under fluctuating and steady UVB
treatments and controls. Panels present
photosynthetic capacities (maximum
quantum yield of photosystem II, Fv/Fm,
and operating efficiency of photosystem
II, ɸPSII) against epidermal flavonol index
(a, b), chlorophyll content index (c, d) and
epidermal anthocyanin index (e, f). Leaves
were grown under fluctuating UVB
radiation (FUV, filled circles) and its
attenuated UVB controls (cFUV, open
circles), steady UVB radiation (SUV, filled
squares) and its attenuated UVB controls
(cSUV, open squares). Measurement days
are represented by the colour scale. Data
are the mean ± SE across replicate blocks,
n = 6 for pigments, n = 90 recorded
(3 times per day, 5 days in total) for Fv/Fm
and n = 168 for ɸPSII. The fitted lines and
statistics square root of the coefficient of
determination and significance (P-values)
are given from linear regression (R) based
on the mean across replicates for each
treatment combination and date.
8 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
yield, OJIP kinetics and RLCs. Small increases in ɸPSII and Fv/Fm were
found under both UVB radiation treatments compared with controls
(Figures 2 and 3d), which runs contrary to the negative effects of UVB
radiation often reported (Albert et al., 2011; Allen et al., 1998; Surabhi
et al., 2009). While it might be expected that high-UVB irradiance
could produce photoinhibition (Kilian et al., 2007; Brosché &
Strid, 2003), this is not necessarily the case. There is evidence that net
photosynthetic rate (Anet) can actually increase under UVB radiation;
as found in Lactuca sativa, where Anet increased by >2 μmol m

2 s
1
(21% higher) and recovery of Fv/Fm following high PAR was faster in
plants receiving solar UV-B radiation than those under UVB attenu-
ated treatments (Wargent et al., 2011; Wargent et al., 2015). Besides,
plants growing under artificial PAR and UVB treatments do not
receive all of the spectral information perceived by photoreceptors in
the full solar spectrum, potentially imposing limitations on photosyn-
thetic performance and acclimation (Landi et al., 2019). Supplemental
UVB radiation stimulating UV RESISTANCE LOCUS 8 (UVR8)-
mediated responses (O'Hara et al., 2019) may account for the higher
values of Fv/Fm and ɸPSII attained once plants are acclimated to the
UVB radiation treatments.
OJIP transients were used to assess the effects of the treatments
on the functions of PSII and the photosynthetic electron transport
chain (Figure 3). UVB treatments affected the shape of chlorophyll
fluorescence dynamics at all phases, including the earliest photochem-
ical phase (Fo-Fj) that reflects processes inside the PSII reaction centre
(Figure 3a-c). This, together with higher Fv/Fm (Figure 3d) and ɸPSII
(Figure 2), indicated that SUV, and to a lesser extent FUV, were
accompanied by higher efficiency of PSII light harvesting. The
0
50
100
150
200
7 13
Days after the commencement of the treatments
0
50
100
150
7 13
Days after the commencement of the treatments
0
50
100
150
200
7 13
Days after the commencement of the treatments
0
500
1000
1500
7 13
Days after the commencement of the treatments
Fr
uc
to
se
 C
on
te
nt
(µ
m
ol
g
-1
DW
)
St
ar
ch
 C
on
te
nt
(µ
m
ol
(G
lu
)
g
-1
DW
)
G
lu
co
se
 C
on
te
nt
(µ
m
ol
g
-1
DW
)
Su
cr
os
e 
C
on
te
nt
(µ
m
ol
g
-1
DW
)
*
***
***
*
**
(a) (b)
(c) (d)
cFUV
FUV
cSUV
SUV
F IGURE 6 Sugar and starch contents in grapevine leaves grown under fluctuating and steady UVB treatments and controls. Treatments are
fluctuating UVB radiation (FUV, dark purple) and its attenuated UVB controls (cFUV, light purple), steady UVB radiation (SUV, dark green) and its
attenuated UVB controls (cSUV, light green). Leaves were harvested at the end of daily period of UVB radiation (15:00), after 7 and 13 days of
UV treatment. Data are the mean ± SE across replicate blocks (n = 6). Significant difference for adjusted P-values (adj. P) *< 0.05, **< 0.01
and ***< 0.001.
SU-ZHOU ET AL. 9 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
mechanisms whereby UVB radiation enhanced PSII function remain
unknown but may be linked to altered abundance and/or connectivity
of light-harvesting complex II (LHCII) antennae. LHCII function is sup-
ported by higher chlorophyll content, as was found under both SUV
and FUV treatment (Figure 4c) because LHCII complexes contain the
largest fraction of cellular chlorophyll. Involvement of LHCII is consis-
tent with reported increases in oligomeric forms of LHCII caused by
UVB radiation (Sfichi & Kotzabasis, 2004). In addition to LHCII abun-
dance, UVB treatments may alter the distribution of LHCII between
PSII and PSI. Dynamic reversible relocations of the mobile LHCII pool
between PSII (state 1; St1) and PSI (state 2; St2), the so-called state
transitions, allow acclimation of photosynthesis under changing spec-
tral composition by modifying the light absorption properties of the
two photosystems (Longoni & Goldschmidt-Clermont, 2021). Our
results suggest that UVB treatments promoted the transition to St1
(Figure 3a), decreasing spillover of excitation energy to PSII and
increasing PSII light capture and, thus, the PSII photochemical
and fluorescence yield (He et al., 2015). Interestingly, FUV had a smal-
ler effect than SUV on promoting St1 than their respective no UVB
controls. The fluctuation period of 15 min is within the range over
which state transitions occur (Goldschmidt-Clermont & Bass, 2015),
meaning that the “recovery period” between UVB doses may offer
the opportunity for the grapevine to partially shift back from St1 to
St2. Additionally, once the plants have adapted to their treatment
conditions, an equilibrium between the excitation of St1 and St2 is
likely to be reached (Su et al., 2019). Once this equilibrium is estab-
lished in SUV, the shift to St1 caused by UVB may be greater than
that in FUV.
The effect of sunlight on plants not only depends on the average
irradiance but also on the range of low/high light intensity and the
duration of fluctuations (Flannery et al., 2021; Wu et al., 2023;
Zhu et al., 2010). Arabidopsis thaliana plants subjected to steady
light from LED lamps in a controlled chamber are reported to have
a greater photosynthetic capacity than plants grown at the same
total irradiances under LED lamps simulating diurnal fluctuations in
irradiance (Vialet-Chabrand et al., 2017). Likewise, in our experi-
ment, the ɸPSII increase in grapevine leaves was lower under FUV
than under SUV (Figure 2), even though overall UVB irradiance
was equivalent across the two treatments. The 15 min light fluctu-
ations used here may have increased energy dissipation, meaning
that less energy could be directed toward carbon assimilation
(Alter et al., 2012; Vialet-Chabrand et al., 2017). A greenhouse
experiment with grapevines reported significant reductions in
ɸPSII, gs and net photosynthesis during the first 20 days of expo-
sure to 9.66 KJ m
2 d
1 of UVB; effects which were ameliorated
after 75 days of treatments (Martínez-Lüscher et al., 2013). While
negative effects on photosynthesis were not apparent following
initiation of the 2.2 kJ m
2 day
1 biologically effective UVB radia-
tion treatments used here, this and other studies reporting
improved performance over the time course of experiments
(Bassman et al., 2002; Shi et al., 2004) provide evidence for long-
term acclimation to chronic UVB radiation at moderate UVB doses
against low background PAR.
Grapevine leaves under FUV and SUV differed in their
response to light-limited and light-saturated conditions during
RLCs (Table 1). Under light-limiting irradiance, the RLC in FUV had
a steeper initial slope; this indicated a higher efficiency for light
capture (Schreiber, 2004). Whereas, under light-saturated irradi-
ance, leaves pre-conditioned to SUV had a higher maximum elec-
tron transport rate, maximum saturating irradiance and operating
saturating irradiance. Together, this suggests that a higher photo-
synthetic rate can be maintained under strong irradiance in the
leaves of plants grown under SUV than FUV (Ralph &
Gademann, 2005), and FUV leaves became light-saturated more
easily; findings which have parallels with acclimation to irradiance
conditions during growth (e.g., “sun and shade leaves; Earles
et al., 2017).
4.3 | Metabolite content correlated with
photosynthesis under fluctuating and steady
UVB radiation
High leaf flavonol concentration is often associated with acclimation
to UVB radiation (Agati et al., 2012) and has previously been found in
grapevine leaves in response to UVB treatments (Berli et al., 2013;
Majer and Hideg, 2012; Del-Castillo-Alonso et al., 2015; Del-
Castillo-Alonso et al., 2016). Increases in flavonol accumulation under
UVB radiation measured as increases in epidermal flavonol index can
happen quickly (within one day), as reported in okra (Abelmoschus
esculentus) (Neugart et al., 2021). Still, there are large differences in
the ability of different species to quickly adjust their epidermal UV-
screening, and grapevine is not among those species considered to
produce diurnal changes in flavonol content (Barnes et al., 2015;
Barnes et al., 2016). While a small decrease in flavonols in grapevine
leaves from morning to evening has been reported, this decrease was
not correlated with diurnal solar UVB radiation (Csepregi et al., 2019).
Thus, flavonol accumulation in grapevine may typically take days of
UVB radiation to be fully manifested. In our experiment, UVB treat-
ments had positive effects on leaf epidermal flavonol accumulation,
but there were no significant differences between the effects of FUV
and SUV (Figure 4a). This suggests that the accumulation of epidermal
UV-screening flavonols may acclimate to the average UVB radiation
dose rather than the maximum dose, as found when tracking seasonal
change in forest understorey plants (Hartikainen et al., 2020). Flavo-
nols absorb UV radiation and scavenge reactive oxygen species non-
enzymatically to protect chloroplasts from photooxidative damage
(Agati et al., 2012; Ioku et al., 1995). There was a positive relationship
between the accumulation of epidermal flavonols and chlorophyll
(Figure S2a), and likewise with Fv/Fm and ɸPSII (Figure 5a-d). High pho-
tosynthetic capacity and pigment content imply that the energy from
absorbed light is used efficiently, which is beneficial for plants under
low light. A few studies have found anthocyanin content to increase
under UVB treatments in some species (Liu-Gitz et al., 1995;
Newsham et al., 2005), but no effect is typically found in grapevine
(Berli et al., 2010; Majer & Hideg, 2012). This confirms that
10 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
anthocyanins are not among the major protective pigments respond-
ing to UVB radiation in mature grapevine leaves.
The increases reported in glucose and fructose under our UVB
treatments are consistent with the typical effects of UVB radiation on
these soluble sugars (Barsig et al., 1998; Hilal et al., 2004; Phoenix
et al., 2000; Figure 6a,b). Soluble sugars play pivotal roles in primary
metabolism, cellular- and plant-level carbon allocation and signalling
pathways controlling, among other functions, photosynthesis (Henry
et al., 2020; Lastdrager & Smeekens, 2014; Sheen, 1990; Yan
et al., 2019). However, no significant correlations were found
between soluble sugar (glucose, fructose and sucrose) concentrations
and Fv/Fm or ɸPSII (Figure S3). This implies that photosynthesis was
not affected by the increase in glucose and fructose, or the decrease
in sucrose, reported here. In Betula pendula, increased bark glucose
content under UVB treatments can be associated with a reduced sink
demand for photosynthate (Tegelberg et al., 2002). A similar reduced
sink strength may provide an alternative explanation for the increase
of glucose in grapevine leaves also found under our UVB radiation
treatments. Starch accumulates as a carbon reserve during the day in
chloroplasts and is depleted during the night to sustain growth and
metabolism of the plants (Kölling et al., 2015; Robinson, 1996). Here,
there was a reduction in starch accumulation under UVB radiation
(Figure 6d), which is consistent with other studies into the effects of
UVB radiation showing, e.g., a higher ratio of soluble-sugars-to-starch
reported in Calamagrostis purpurea (Gwynn-Jones, 2001), reduced
starch in Vaccinium ulginiosum (Phoenix et al., 2000), and a decrease in
starch volume density in Brassica napus and Helianthus annuus
(Fagerberg & Bornman, 1997; Fagerberg, 2007).
5 | CONCLUSIONS
Most studies into the effects of UVB radiation on plants are con-
ducted under steady UVB radiation in controlled conditions rather
than fluctuating light outdoors. Even field experiments with UV filters
or modulated lamp systems cannot specifically focus on the effect of
fluctuating compared with equivalent steady UVB radiation. Here, a
major cultivar of grapevine (Vitis vinifera L. cv Cabernet Sauvignon)
was used to investigate how equivalent doses of fluctuating (FUV) vs
steady (SUV) UVB radiation affect photosynthesis and metabolite
accumulation. It was found that: (1) SUV decreased gs more than FUV;
(2) there was no evidence of damage to PSII caused by the UVB treat-
ments but even a small increase in the Fv/Fm and ɸPSII; (3) epidermal
flavonol content was increased by both SUV and FUV compared with
their controls.
Overall, acclimation to FUV was weaker than to SUV across the
parameters measured. This implies that experiments examining UVB
responses of plants in controlled conditions under steady irradiance
may overestimate the effect size when compared to the same daily
average of biologically effective UVB radiation in natural environ-
ments where UVB radiation is subject to fluctuations. To obtain more
reliable estimates, future experiments should consider the total UVB
dose, the amplitude of fluctuations in irradiance, and the duration and
frequency of these fluctuations when assessing the factors governing
plant responses to UVB radiation. This approach would allow a sys-
tematic understanding of plants' acclimation mechanisms under the
kind of patterns of UVB radiation found in nature, to which plants
have adapted over many generations.
AUTHOR CONTRIBUTIONS
Chenxing Su-Zhou designed and carried out the experiment, analyzed
the data and wrote the manuscript. Maxime Durand helped with data
collection, writing and ideas behind the manuscript. Pedro J. Aphalo
advised data analysis. Javier Martinez-Abaigar provided grapevines
and expertise on their growth. Alexey Shapiguzov helped design and
measure and interpret the OJIP survey. hirofumi ishihara helped with
sugar and starch analysis. T. Matthew Robson proposed and designed
the original experiment and supervised all the work. All authors edited
and approved the manuscript.
ACKNOWLEDGMENTS
The research was funded by the Research Council of Finland (decision
324555 to T. Matthew Robson, decision 351008 to Maxime Durand
and decision 346140 to Alexey Shapiguzov); the China Scholarship
Council (Grant 202206300065 to Chenxing Su-Zhou) and the Gov-
ernment of La Rioja (project “Afianza” 2023/05 to Javier Martinez-
Abaigar). We thank Saijaliisa Kangasjärvi for her support and advice
on the sugar and starch analysis, funded by Novo Nordisk Plant Sci-
ence, Agriculture and Food Biotechnology (NNF20OC0065026).
DATA AVAILABILITY STATEMENT
The raw data from this experiment are available in the Appendix.
ORCID
Chenxing Su-Zhou https://orcid.org/0009-0005-0195-2913
Maxime Durand https://orcid.org/0000-0002-8991-3601
Pedro J. Aphalo https://orcid.org/0000-0003-3385-972X
Javier Martinez-Abaigar https://orcid.org/0000-0002-9762-9862
Alexey Shapiguzov https://orcid.org/0000-0001-7199-1882
Hirofumi Ishihara https://orcid.org/0000-0002-7658-0473
Xu Liu https://orcid.org/0009-0001-4049-4020
T. Matthew Robson https://orcid.org/0000-0002-8631-796X
REFERENCES
Agati, G., Azzarello, E., Pollastri, S. & Tattini, M. (2012) Flavonoids as anti-
oxidants in plants: location and functional significance. Plant Science:
An International Journal of Experimental Plant Biology, 196, 67–76.
Albert, K.R., Mikkelsen, T.N., Ro-Poulsen, H., Arndal, M.F. & Michelsen, A.
(2011) Ambient UV-B radiation reduces PSII performance and net
photosynthesis in high Arctic Salix arctica. Environmental and Experi-
mental Botany, 72, 439–447.
Allen, D.J., Nogués, S. & Baker, N.R. (1998) Ozone depletion and increased
UV-B radiation: is there a real threat to photosynthesis? Journal of
Experimental Botany, 49, 1775–1788.
Alter, P., Dreissen, A., Luo, F.L. & Matsubara, S. (2012) Acclimatory
responses of Arabidopsis to fluctuating light environment: comparison
of different sunfleck regimes and accessions. Photosynthesis Research,
113(1–3), 221–237.
SU-ZHOU ET AL. 11 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Anderson, K. & Nelgen, S. (2020) Which Winegrape Varieties Are Grown
Where: A Global Empirical Picture. (Revised ed). University of Adelaide
Press: Adelaide, Australia.
Aphalo, P.J. (2018) Exploring temporal and latitudinal variation in the solar
spectrum at ground level with the TUV model. UV4Plants Bulletin,
2018(2), 45–56.
Aphalo, P.J., Albert, A., Björn, L.-O., McLeod, A., Robson, T.M., &
Rosenqvist, E., (2012) Beyond the visible: A handbook of best practice
in plant UV photobiology. COST Action FA0906. ISBN 1479133442.
Assmann, S.M. & Wang, X.Q. (2001) From milliseconds to millions of years:
guard cells and environmental responses. Current Opinion in Plant Biol-
ogy, 4(5), 421–428.
Barnes, P.W., Flint, S.D., Tobler, M.A. & Ryel, R.J. (2016) Diurnal adjust-
ment in ultraviolet sunscreen protection is widespread among higher
plants. Oecologia, 181, 55–63.
Barnes, P.W., Robson, T.M., Tobler, M.A., Bottger, I.N. & Flint, S.D. (2017)
Plant responses to fluctuating UV environments. Chapter 6 in B.
Jordan. Plant UV Biology, CABI publishers, 72–89.
Barnes, P.W., Robson, T.M., Zepp, R.G., Bornman, J.F., Jansen, M.A.K.,
Ossola, R., Wang, Q.W., Robinson, S.A., Foereid, B., Klekociuk, A.R.,
Martinez-Abaigar, J., Hou, W.C., Mackenzie, R. & Paul, N.D. (2023)
Interactive effects of changes in UV radiation and climate on terrestrial
ecosystems, biogeochemical cycles, and feedbacks to the climate sys-
tem. Photochemical & Photobiological Sciences, 22(5), 1049–1091.
Barsig, M., Schneider, K. & Gehrke, C. (1998) Effects of UV-B radiation on
fine structure, carbohydrates, and pigments in Polytrichum commune.
Bryologist, 101, 358–365.
Bassman, J., Edwards, G. & Robberecht, R. (2002) Long-term exposure to
enhanced UV-B radiation is not detrimental to growth and photosyn-
thesis in Douglas-fir. New Phytologist, 154, 107–120.
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015) Fitting Linear Mixed-
Effects Models Using lme4. Journal of Statistical Software, 67(1), 1–48.
Berli, F. J., Moreno, D., Piccoli, P., Hespanhol-Viana, L., Silva, M. F.,
Bressan-Smith, R., Cavagnaro, J. B. & Bottini, R. (2010) Abscisic acid is
involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tis-
sues to ultraviolet-B radiation by enhancing ultraviolet-absorbing com-
pounds, antioxidant enzymes and membrane sterols. Plant, Cell &
Environment, 33(1), 1–10.
Berli, F.J., Alonso, R., Bressan-Smith, R. & Bottini, R. (2013) UV-B impairs
growth and gas exchange in grapevines grown in high altitude. Physio-
logia Plantarum, 149(1), 127–140.
Björn, L.O. (2015) Ultraviolet-A, B, and C. UV4Plants Bulletin, 2015(1)
17–18.
Britt, A.B. (1996) DNA damage and repair in plants. Annual Review of Plant
Physiology and Plant Molecular Biology, 47, 75–100.
Brosché, M. & Strid, Å. (2003) Molecular events following perception of
ultraviolet-B radiation by plants. Physiologia Plantarum, 117, 1–10.
Cerovic, Z.G., Masdoumier, G., Ghozlen, N.B. & Latouche, G. (2012) A new
optical leaf-clip meter for simultaneous non-destructive assessment of
leaf chlorophyll and epidermal flavonoids. Physiologia Plantarum, 146,
251–260.
Coombe, B.G. (1995) Growth stages of the grapevine: Adoption of a sys-
tem for identifying grapevine growth stages. Australian Journal of
Grape and Wine Research, 1, 104–110.
Crestani, G., Cunningham, N., Csepregi, K., Badmus, U.O. & Jansen, M.A.K.
(2023) From stressor to protector, UV-induced abiotic stress resis-
tance. Photochemical & Photobiological Sciences, 22(9), 2189–2204.
Csepregi, K., Teszlák, P., K}orösi, L. & Hideg, E. (2019) Changes in grapevine
leaf phenolic profiles during the day are temperature rather than irra-
diance driven. Plant Physiology and Biochemistry, 137, 169–178.
Del-Castillo-Alonso, M.A´., Diago, M.P., Monforte, L., Tardaguila, J.,
Martínez-Abaigar, J. & Núñez-Olivera, E. (2015) Effects of UV exclu-
sion on the physiology and phenolic composition of leaves and berries
of Vitis vinifera cv. Graciano. Journal of the Science of Food and Agricul-
ture, 95(2), 409–416.
Del-Castillo-Alonso, M.A´., Diago, M.P., Tomás-Las-Heras, R., Monforte, L.,
Soriano, G., Martínez-Abaigar, J. & Núñez-Olivera, E. (2016) Effects of
ambient solar UV radiation on grapevine leaf physiology and berry
phenolic composition along one entire season under Mediterranean
field conditions. Plant Physiology and Biochemistry, 109, 374–386.
Earles, J.M., Théroux-Rancourt, G., Gilbert, M.E., McElrone, A.J. &
Brodersen, C.R. (2017) Excess diffuse light absorption in upper meso-
phyll limits CO2 drawdown and depresses photosynthesis. Plant Physi-
ology, 174(2), 1082–1096.
Eilers, P.H.C. & Peeters, J.C.H. (1988) A model for the relationship
between light intensity and the rate of photosynthesis in phytoplank-
ton. Ecological Modelling, 42, 199–215.
Fagerberg, W.R. & Bornman, J.F. (1997) Ultraviolet-B radiation causes
shade-type ultrastructural changes in Brassica napus. Physiologia Plan-
tarum, 101, 833–844.
Fagerberg, W.R. (2007) Below-ambient levels of UV induce chloroplast
structural change and alter starch metabolism. Protoplasma, 230(1–2),
51–59.
Flannery, S.E., Hepworth, C., Wood, W.H.J., Pastorelli, F., Hunter, C.N.,
Dickman, M.J., Jackson, P.J. & Johnson, M.P. (2021) Developmental
acclimation of the thylakoid proteome to light intensity in Arabidopsis.
Plant Journal, 105, 223–244.
Fox, J. & Weisberg, S. (2019) An R Companion to Applied Regression, Third
edition. Sage, Thousand Oaks CA.
Goldschmidt-Clermont, M. & Bassi, R. (2015) Sharing light between two
photosystems: mechanism of state transitions. Current Opinion in Plant
Biology, 25, 71–78.
Gwynn-Jones, D. (2001) Short-term impacts of enhanced UV-B radiation
on photo-assimilate allocation and metabolism: a possible interpreta-
tion for time-dependent inhibition of growth. Plant Ecology, 154,
67–73.
Hartikainen, S.M., Pieristè, M., Lassila, J. & Robson, T.M. (2020) Seasonal
Patterns in Spectral Irradiance and Leaf UV-A Absorbance Under For-
est Canopies. Frontiers in Plant Science, 10, 1762.
Hazard, C., Lesser, M.P. & Kinzie, R.A. (1997) Effects of Ultraviolet Radia-
tion on Photosynthesis in the Subtropical Marine Diatom, Chaetoceros
gracilis (Bacillariophyceae). Journal of Phycology, 33, 960–968.
He, J.M., Ma, X.G., Zhang, Y., Sun, T.F., Xu, F.F., Chen, Y.P., Liu, X. &
Yue, M. (2013) Role and interrelationship of Ga protein, hydrogen per-
oxide, and nitric oxide in ultraviolet B-induced stomatal closure in Ara-
bidopsis leaves. Plant Physiology, 161, 1570–1583.
He, J., Yang, W., Qin, L., Fan, D.-J. & Chow, W.S. (2015) Photoinactivation
of Photosystem II in wild-type and chlorophyll b-less barley leaves:
which mechanism dominates depends on experimental circumstances.
Photosynthesis Research, 126, 399–407.
Henry, C., Watson-Lazowski, A., Oszvald, M., Griffiths, C., Paul, M.J.,
Furbank, R.T. & Ghannoum, O. (2020) Sugar sensing responses to low
and high light in leaves of the C4 model grass Setaria viridis. Journal of
Experimental Botany, 71(3), 1039–1052.
Hideg, E., Jansen, M.A. & Strid, A. (2013) UV-B exposure, ROS, and stress:
inseparable companions or loosely linked associates? Trends in Plant
Science, 18(2), 107–115.
Hilal, M., Parrado, M.F., Rosa, M., Gallardo, M., Orce, L., Massa, E.M.,
González, J.A. & Prado, F.E. (2004) Epidermal lignin deposition in qui-
noa cotyledons in response to UV-B radiation. Photochemistry and
Photobiology, 79(2), 205–210.
Hothorn, T., Bretz, F. & Westfall, P. (2008) Simultaneous Inference in Gen-
eral Parametric Models. Biometrical Journal, 50(3), 346–363.
Ioku, K., Tsushida, T., Takei, Y., Nakatani, N. & Terao, J. (1995) Antioxida-
tive activity of quercetin and quercetin monoglucosides in solution
and phospholipid bilayers. Biochimica et Biophysica Acta, 1234(1),
99–104.
Jansen, M.A.K., Acˇ, A., Klem, K. & Urban, O. (2022) A meta-analysis of the
interactive effects of UV and drought on plants. Plant, Cell & Environ-
ment, 45(1), 41–54.
12 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Kaiser, E., Morales, A. & Harbinson, J. (2018) Fluctuating Light Takes Crop
Photosynthesis on a Rollercoaster Ride. Plant Physiology, 176(2),
977–989.
Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O.,
D'Angelo, C., Bornberg-Bauer, E., Kudla, J. & Harter, K. (2007) The
AtGenExpress global stress expression data set: protocols, evaluation
and model data analysis of UV-B light, drought and cold stress
responses. The Plant Journal, 50(2), 347–363.
Kölling, K., Thalmann, M., Müller, A., Jenny, C. & Zeeman, S.C. (2015) Car-
bon partitioning in Arabidopsis thaliana is a dynamic process controlled
by the plant's metabolic status and its circadian clock. Plant, Cell &
Environment, 38(10), 1965–1979.
Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K. &
Long, S.P. (2016) Improving photosynthesis and crop productivity by
accelerating recovery from photoprotection. Science, 354(6314),
857–861.
Kuznetsova, A., Brockhoff, P.B. & Christensen, R.H.B. (2017) lmerTest
Package: Tests in Linear Mixed Effects Models. Journal of Statistical
Software, 82(13), 1–26.
Landi, M., Zˇivcˇák, M., Sytar, O., Bresticˇ, M. & Allakhverdiev, S.I. (2019) Plas-
ticity of photosynthetic processes and the accumulation of secondary
metabolites in plants in response to monochromatic light environments:
A review. Biochimica et Biophysica Acta. Bioenergetics, 1861, 148131.
Landry, L., Stapleton, A., Lim, J., Hoffman, P., Hays, J. B., Walbot, V. &
Last, R. (1997) An Arabidopsis photolyase mutant is hypersensitive to
UV-B radiation. Proceedings of the National Academy of Sciences of the
United States of America, 94, 328–332.
Lastdrager, J., Hanson, J. & Smeekens, S. (2014) Sugar signals and the con-
trol of plant growth and development. Journal of Experimental Botany,
65, 799–807.
Liu-Gitz, L., Gitz, D. & McClure, J.W. (1995) Effects of UV-B on flavonoids,
ferulic acid, growth and photosynthesis in barley primary leaves. Phy-
siologia Plantarum, 93, 725–733.
Longoni, F.P. & Goldschmidt-Clermont, M. (2021) Thylakoid Protein Phos-
phorylation in Chloroplasts. Plant & Cell Physiology, 62(7), 1094–1107.
Majer, P. & Hideg, E. (2012) Developmental stage is an important factor
that determines the antioxidant responses of young and old grapevine
leaves under UV irradiation in a green-house. Plant Physiology and Bio-
chemistry, 50(1), 15–23.
Martínez-Lüscher, J., Morales, F., Delrot, S., Sánchez-Díaz, M., Gomés, E.,
Aguirreolea, J. & Pascual, I. (2013) Short- and long-term physiological
responses of grapevine leaves to UV-B radiation. Plant Science, 213,
114–122.
Neugart, S., Tobler, M.A. & Barnes, P.W. (2021) Rapid adjustment in epi-
dermal UV sunscreen: Comparison of optical measurement techniques
and response to changing solar UV radiation conditions. Physiologia
Plantarum, 173(3), 725–735.
Newsham, K., Geissler, P.A., Nicolson, M.J., Peat, H. & Lewis-Smith, R.
(2005) Sequential reduction of UV-B radiation in the field alters the
pigmentation of an Antarctic leafy liverwort. Environmental and Experi-
mental Botany, 54, 22–32.
O'Hara, A., Headland, L., Diaz, A., Morales, L., Strid, Å. & Jenkins, G. (2019)
Regulation of Arabidopsis gene expression by low fluence rate UV-B
independently of UVR8 and stress signaling. Photochemical and Photo-
biological Sciences, 18, 1675–1684.
Ollat, N. & Gaudillere, J.P. (2000) Carbon balance in developing grapevine
berries. Acta Horticulturae, 526, 345–350.
Petrie, P.R., Trought, M.C., Howell, G.S. & Buchan, G.D. (2003) The effect
of leaf removal and canopy height on whole-vine gas exchange and
fruit development of Vitis vinifera L. Sauvignon Blanc. Functional Plant
Biology, 30, 711–717.
Phoenix, G.K., Gwynn-Jones, D., Lee, J.A. & Callaghan, T.V. (2000) The
impacts of UV-B radiation on the regeneration of a sub-arctic heath
community. Plant Ecology, 146, 67–75.
R Core Team (2022) R: A language and environment for statistical computing.
R Foundation for Statistical Computing, Vienna, Austria.
Ralph, P.J. & Gademann, R. (2005) Rapid light curves: A powerful tool to
assess photosynthetic activity. Aquatic Botany, 82, 222–237.
Robinson, J.M. (1996) Leaflet photosynthesis rate and carbon metabolite
accumulation patterns in nitrogen-limited, vegetative soybean plants.
Photosynthesis research, 50(2), 133–148.
Robson, T.M. & Aphalo, P.J. (2019) Transmission of ultraviolet, visible and
near-infrared solar radiation to plants within a seasonal snow pack.
Photochemical & Photobiological Sciences, 18(8), 1963–1971.
Robson, T.M., Klem, K., Urban, O. & Jansen, M.A. (2015) Re-interpreting
plant morphological responses to UV-B radiation. Plant, Cell & Environ-
ment, 38(5), 856–866.
Roeber, V.M., Bajaj, I., Rohde, M., Schmülling, T. & Cortleven, A. (2021)
Light acts as a stressor and influences abiotic and biotic stress
responses in plants. Plant, Cell & Environment, 44(3), 645–664.
Schmelzer, E., Jahnen, W. & Hahlbrock, K. (1988) In situ localization of
light-induced chalcone synthase mRNA, chalcone synthase, and flavo-
noid end products in epidermal cells of parsley leaves. Proceedings of
the National Academy of Sciences of the United States of America, 85(9),
2989–2993.
Schreiber, U. (2004) Pulse-amplitude (PAM) fluorometry and saturation
pulse method. In: Papageorgiou, G., Govindjee, (Eds.), Chlorophyll fluo-
rescence: A Signature of Photosynthesis. Advances in Photosynthesis
and Respiration Series. Kluwer Academic Publishers, Dordrecht, The
Netherlands.
Searle, S.R., Speed, F.M. & Milliken, G.A. (1980) Population marginal means
in the linear model: an alternative to least squares means. The Ameri-
can Statistician, 34: 216–221.
Sfichi, L., Ioannidis, N. & Kotzabasis, K. (2004) Thylakoid-associated poly-
amines adjust the UV-B sensitivity of the photosynthetic apparatus by
means of light-harvesting complex II changes. Photochemistry and Pho-
tobiology, 80(3), 499–506.
Sheen, J. (1990) Metabolic repression of transcription in higher plants. The
Plant cell, 2(10), 1027–1038.
Shi, S., Zhu, W., Li, H., Zhou, D., Han, F., Zhao, X. & Tang, Y. (2004) Photo-
synthesis of Saussurea superba and Gentiana straminea is not reduced
after long-term enhancement of UV-B radiation. Environmental and
Experimental Botany, 51, 75–83.
Smith, W.K. & Berry, Z.C. (2013) Sunflecks? Tree Physiology, 33, 233–237.
Stitt, M., Lilley, R. M., Gerhardt, R. & Heldt, H. W. (1989) Metabolite levels
in specific cells and subcellular compartments of plant-leaves. Methods
in Enzymology, 174, 518–552.
Su, X., Ma, J., Pan, X., Zhao, X., Chang, W., Liu, Z., Zhang, X. & Li, M. (2019)
Antenna arrangement and energy transfer pathways of a green algal
photosystem-I-LHCI supercomplex. Nature Plants, 5(3), 273–281.
Surabhi, G., Reddy, K.R. & Singh, S.K. (2009) Photosynthesis, fluorescence,
shoot biomass and seed weight responses of three cowpea (Vigna
unguiculata (L.) Walp.) cultivars with contrasting sensitivity to UV-B
radiation. Environmental and Experimental Botany, 66, 160–171.
Tegelberg, R., Aphalo, P.J. & Julkunen-Tiitto, R. (2002) Effects of long-
term, elevated ultraviolet-B radiation on phytochemicals in the bark of
silver birch (Betula pendula). Tree Physiology, 22, 1257–1263.
Tossi, V., Lamattina, L., Jenkins, G. I. & Cassia, R. O. (2014) Ultraviolet-B-
induced stomatal closure in Arabidopsis is regulated by the UV RESIS-
TANCE LOCUS8 photoreceptor in a nitric oxide-dependent mecha-
nism. Plant physiology, 164(4), 2220–2230.
Vialet-Chabrand, S., Matthews, J.S., Simkin, A.J., Raines, C. A. & Lawson, T.
(2017) Importance of fluctuations in light on plant photosynthetic
acclimation. Plant Physiology, 173(4), 2163–2179.
Wargent, J.J., Elfadly, E.M., Moore, J.P. & Paul, N.D. (2011) Increased
exposure to UV-B radiation during early development leads to
enhanced photoprotection and improved long-term performance in
Lactuca sativa. Plant, Cell & Environment, 34(8), 1401–1413.
SU-ZHOU ET AL. 13 of 14
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Wargent, J.J., Nelson, B.C.W., Mcghie, T.K. & Barnes, P.W. (2015) Acclima-
tion to UV-B radiation and visible light in Lactuca sativa involves up-
regulation of photosynthetic performance and orchestration of
metabolome-wide responses. Plant, Cell & Environment, 38, 929–940.
Willekens, H., Van Camp, W., Van Montagu, M., Inze, D., Langebartels, C. &
Sandermann, H. (1994) Ozone, sulfur dioxide, and ultraviolet B have simi-
lar effects on mRNA accumulation of antioxidant genes in Nicotiana plum-
baginifolia L. Plant Physiology, 106(3), 1007–1014.
Wu, H.Y., Qiao, M.Y., Zhang, Y.J., Kang, W.J., Ma, Q.H., Gao, H.Y.,
Zhang, W.F. & Jiang, C.D. (2023) Photosynthetic mechanism of maize
yield under fluctuating light environments in the field. Plant Physiology,
191(2), 957–973.
Yan, Y., Stoddard, F.L., Neugart, S., Sadras, V.O., Lindfors, A.,
Morales, L. O. & Aphalo, P. J. (2019) Responses of flavonoid profile
and associated gene expression to solar blue and UV radiation in two
accessions of Vicia faba L. from contrasting UV environments. Photo-
chemical & Photobiological Sciences, 18(2), 434–447.
Zhao, B., Wang, L., Pang, S., Jia, Z., Wang, L., Li, W. & Jin, B. (2020) UV-B
promotes flavonoid synthesis in Ginkgo biloba leaves. Industrial Crops
and Products, 151, 112483.
Zhu, X.G., Long, S.P. & Ort, D.R. (2010) Improving photosynthetic effi-
ciency for greater yield. Annual review of plant biology, 61,
235–261.
SUPPORTING INFORMATION
Additional supporting information can be found online in the Support-
ing Information section at the end of this article.
How to cite this article: Su-Zhou, C., Durand, M., Aphalo, P.J.,
Martinez-Abaigar, J., Shapiguzov, A., Ishihara, H. et al. (2024)
Weaker photosynthetic acclimation to fluctuating than to
corresponding steady UVB radiation treatments in grapevines.
Physiologia Plantarum, 176(3), e14383. Available from: https://
doi.org/10.1111/ppl.14383
14 of 14 SU-ZHOU ET AL.
Physiologia Plantarum
 13993054, 2024, 3, D
ow
nloaded from
 https://onlinelibrary.w
iley.com
/doi/10.1111/ppl.14383 by Luonnonvarakeskus, W
iley O
nline Library on [13/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on W
iley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License