Acta Physiol Plant
DOI 10.1007/s11738-011-0722-z
ORIGINAL PAPER
Leaf gas exchange and chlorophyll a fluorescence of Eucalyptus
urophylla in response to Puccinia psidii infection
Alexandre Alonso Alves • Lúcio Mauro da Silva Guimarães •
Agnaldo Rodrigues de Melo Chaves • Fábio Murilo DaMatta
Acelino Couto Alfenas
•
Received: 10 September 2010 / Revised: 10 January 2011 / Accepted: 24 January 2011
Ó Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2011
Abstract One of the most important diseases of eucalyptus plantations is caused by the rust fungus Puccinia
psidii. While the genetic basis of rust resistance has been
addressed recently, little is known about the physiological
aspects of Eucalyptus–P. psidii interaction. In order to fill
this gap, we undertook a study investigating the effects of
P. psidii infection on photosynthetic processes of two
E. urophylla clones with contrasting resistance to the pathogen. Our results show that gas exchange and chlorophyll
a fluorescence parameters were virtually unaffected in the
resistant clone. In the susceptible clone, photosynthetic
rates were chiefly constrained by biochemical limitations to
carbon fixation. Photosynthesis was impaired only in
symptomatic tissues since the reductions in photosynthetic
rates were proportional to the diseased leaf area. Rust
infection provoked chronic photoinhibition to photosynthesis in the susceptible clone. Overall, differences in the
ability for light capture, use and dissipation may play a
Communicated by Z. Gombos.
A. A. Alves
Embrapa Agroenergy, PqEB, Brasilia,
DF 70770-901, Brazil
A. A. Alves A. C. Alfenas
Graduate Program in Genetics and Breeding,
Federal University of Viçosa, Viçosa,
MG 36571-000, Brazil
L. M. S. Guimarães A. C. Alfenas (&)
Department of Plant Pathology, Federal University of Viçosa,
Viçosa, MG 36570-000, Brazil
e-mail: [email protected]
A. R. M. Chaves F. M. DaMatta
Department of Plant Biology, Federal University of Viçosa,
Viçosa, MG 36570-000, Brazil
significant role in explaining the clonal differences in
Eucalyptus in response to P. psidii infection. To our
knowledge, this is the first report of the effect of rust
infection on gas exchange and chlorophyll a fluorescence
parameters in Eucalyptus.
Keywords Eucalyptus Light-saturated photosynthesis Puccinia psidii infection Biochemical and photochemical
impairment
Introduction
Eucalypts are susceptible to a wide range of diseases
involving fungal and bacterial pathogens. One of the most
important diseases that currently affects eucalyptus plantations worldwide is caused by the rust fungus Puccinia
psidii Winter (Coutinho et al. 1998; Glen et al. 2007). Rust
occurs mainly on seedlings in nurseries, on young trees in
the field, on coppice and also on shoots in clonal hedges.
The first symptoms appear several days after infection by
urediniospores of the fungus as pale yellow specks on the
leaf blades. Within 10–12 days, the specks deepen in color
to a characteristic egg-yolk yellow. Thereafter, the pustules
increase in size due to radial growth of the fungus (Coutinho et al. 1998). While the genetic basis of rust resistance
has been addressed recently (Junghans et al. 2003a;
Mamani et al. 2010), virtually nothing is known about
physiological aspects of the Eucalyptus–P. psidii interaction.
As P. psidii is a biotrophic pathogen, i.e., colonizes only
living tissues, it is suggested that it may cause substantial
modification to host physiology, either directly via secretion
of chemicals, or indirectly via induced host responses in the
same manner that occurs in other host–biotrophic pathogen
interactions.
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Acta Physiol Plant
On a physiological basis, one of the major effects of
foliar biotrophic pathogens is on photosynthetic processes
(Berger et al. 2007; Domiciano et al. 2009). Photosynthetic
characteristics such as gas exchange and chlorophyll
a fluorescence parameters have been considered as useful
noninvasive indicators of the behavior of the photosynthetic apparatus under stressful conditions, including attack
by pathogens (Baker and Rosenqvist 2004; Berger et al.
2007; Bonfig et al. 2006; Domiciano et al. 2009; Lichtenthaler and Miehé 1997). When plants are attacked by
pathogens, physiological and photosynthetic properties are
often impaired (Guo et al. 2005; Swiech et al. 2001). A
number of studies have shown that pathogen infection
leads to a decrease in photosynthesis rates (Bastiaans 1991;
Bastiaans and Roumen 1992; Berger et al. 2007; Chou
et al. 2000; Domiciano et al. 2009) and modifications of the
photosynthetic apparatus (Lichtenthaler and Miehé 1997).
These modifications can be due to negative regulation or
damage to the photosynthetic apparatus. Measurements of
chlorophyll a fluorescence have also shown that the photochemical efficiency of photosystem II (PSII) is decreased
by infection (Baker and Rosenqvist 2004; Bassanezi et al.
2003; Bonfig et al. 2006; van Kooten et al. 1990). Recently,
Pinkard and Mohammed (2006) quantified changes in
photosynthetic parameters of Eucalyptus globulus Labill in
response to Mycosphaerella sp. infection using gas
exchange techniques. They showed a negative linear relationship between light-saturated rate of net photosynthesis
(Amax) and leaf-level damage from Mycosphaerella sp.
infection. Reductions in Amax were proportionally greater
than those expected simply from the reduction in green leaf
area, suggesting that asymptomatic tissue was also affected
by Mycosphaerella sp. infection. Changes in mesophyll
or stomatal resistance to CO2, changes in the rates of
biochemical reactions of photosynthesis, changes in the
number or structure of chloroplasts or the secretion of
phytotoxic chemicals into asymptomatic tissue by the pathogen have been associated with changes in the rates of
photosynthesis in diseased plants (Pinkard and Mohammed
2006). In particular, for E. globulus plants infected with
Mycosphaerella sp., the reductions in Amax were not related
to increases in stomatal resistance, but rather to reduced
activity of ribulose bisphosphate (RuBP) carboxylase/
oxygenase (Rubisco) and changes in the capacity for RuBP
regeneration (Pinkard and Mohammed 2006).
In this study, we investigate the effects of P. psidii
infection on photosynthetic processes using two E. urophylla clones with differing resistance to the pathogen. We
hypothesized that (a) the photosynthetic performance,
assessed using gas exchange and chlorophyll a fluorescence parameters, is reduced by P. psidii infection in the
susceptible clone as a result of biochemical and photochemical damage and, alternatively, such a performance is
123
virtually unaffected in the resistant clone; and (b) changes
in photosynthesis are proportional to the development of
the pathogen, i.e., the extent of diseased leaf area (DLA).
Materials and methods
Plant material and experimental design
The experiment was conducted under greenhouse conditions
in Viçosa (20°450 1400 S; 42°520 5300 W; 649 m a.s.l.), Brazil. We
used two E. urophylla S.T. Blake clones, one of the most
planted eucalypt species. Eucalypt hybrids (E. grandis 9
E. urophylla) deployed as clones currently make up a significant proportion of the existing commercial plantations in
Brazil and are recognized as some of the most advanced
genetic materials in forestry (Grattapaglia and Kirst 2008).
One of the clones that we used, U1179, is considered to be
highly resistant while the other, U1183, is highly susceptible
to P. psidii infection (Junghans et al. 2003b). The experiments
were installed in completely randomized designs with four
treatments (inoculated resistant clone, non-inoculated resistant clone, inoculated susceptible clone and non-inoculated
susceptible clone) with six replicates. Each experimental plot
consisted of a pot containing one plant.
Inoculation and disease severity assessment
Greenhouse-grown eucalypt cuttings (4–5 months old)
were spray inoculated with an inoculum suspension at
2 9 104 urediniospores mL-1 of a single pustule-isolate of
P. psidii (UFV-2). Inoculated plants were darkness-incubated for 24 h in a moist chamber at 25°C (Ruiz et al.
1989) and then transferred to a greenhouse, where they
were kept until the end of the experiment. The plants were
grown under naturally fluctuating environmental conditions. Greenhouse temperature and leaf temperature were
measured in each evaluation day. Rust severity was
assessed using the software QUANT (Vale et al. 2003) that
allows precise estimation of diseased and green leaf area.
For this purpose, digital images of leaves, taken in each
evaluation day from the third and fourth pair from the apex,
were used to determine the mean percentage of DLA
through the standard procedures of the software. At the end
of the experiment, the leaves were scanned at 600 dpi and
the images were analyzed with QUANT to estimate final
disease severity, or final diseased leaf area (FDLA).
Gas exchange measurements
An LcPro? infrared gas analyzer (Analytical Development
Company, Hoddesdon, UK) was used to measure the lightsaturated rate of net CO2 assimilation (Amax), stomatal
Acta Physiol Plant
conductance (gs), the internal-to-ambient CO2 concentration
ratio (Ci/Ca) and transpiration rate (E). Measurements were
carried out at ambient temperatures and CO2 concentrations
(*380–390 ppm) under saturating photosynthetic photon
flux density (PPFD; 1,000 lmol m-2 s-1). During measurements, daily temperature ranged from 15 to 25°C, and leaf
temperature ranged from 24 to 32°C. The evaluations were
conducted in two leaves (one from third and one from the
fourth pair from the top) per replication of each treatment
between 9:00 and 11:00 am. Each leaf was labeled so as to
allow the measurements to occur in the same location. Evaluations were made 0, 4, 8, 12, 16 and 20 days after inoculation
(DAI) in order to cover the entire disease progression. Readings were recorded after the values of Amax and gs were stable.
Results
Rust severity assessment
Rust severity in resistant plants was virtually negligible
during all the evaluation period since only small fleck
symptoms were observed. In contrast, rust severity in
susceptible plants increased almost linearly during evaluation period, ranging on average from 0% at 0 DAI to 42%
at 20 DAI (Fig. 1). As expected, non-inoculated plants
from both resistant and susceptible clones showed no
evidence of infection and thus were used as control plants.
Photosynthetic performance of the resistant clone
upon inoculation with P. psidii
Chlorophyll a fluorescence measurements
Chlorophyll a fluorescence parameters were estimated
immediately after the gas exchange measurements using a
portable pulse amplitude modulation fluorometer (MINIPAM, Heinz Walz GmbH, Effeltrich, Germany). The
evaluations were made on the same leaves as used for the
gas exchange measurements. Following dark adaptation for
30 min, the leaf tissues were exposed to a weak modulated
measuring beam (0.03 lmol m-2 s-1) to determine the
initial fluorescence (F0). Then, a saturating white light
pulse of 6,000 lmol m-2 s-1 was applied for 1 s to ensure
the maximum fluorescence emission (Fm), from which the
Fv/Fm = [(Fm - F0)/Fm)] ratio was calculated. This ratio
has been used as a measure of the potential photochemical
efficiency of PSII. The electron transport rate (ETR), efficiency of excitation energy capture by open PSII reaction
0
centers (Fv0 =Fm
), the quenching coefficients of photochemical (qP) and non-photochemical (NPQ) events under
actinic light (1,000 lmol m-2 s-1) conditions were calculated as described elsewhere (Araujo et al. 2008; Lima
et al. 2002).
Data analysis
The means obtained for gas exchange and chlorophyll
fluorescence parameters were compared by a t test
(p B 0.05, inoculated vs. non-inoculated plant means at
each time point) using the STATISTICA software (StatSoft
2004). The mean percentage of DLA at each time point
was also correlated to the means obtained for the photosynthetic parameters in order to obtain correlation coefficients between these variables and to test the hypothesis
that gas exchange and chlorophyll fluorescence parameters
are reduced proportionally to the progression of the
disease. The photosynthetic parameter means were also
correlated to gain some insights on how one parameter is
related to another.
The stomatal conductance (gs) of both inoculated and
control plants varied similarly during the experiment and
no statistical differences were observed in a single time
point (Fig. 2a). As to gs, the net CO2 assimilation rate
(Amax), the internal-to-ambient CO2 concentration ratio (Ci/
Ca) and transpiration rate (E) of inoculated and control
plants also varied similarly (Fig. 2b–d). Means for Amax
and Ci/Ca did not differ significantly between inoculated
and non-inoculated resistant plants, while E values differed
statistically between inoculated and non-inoculated plants
in three time points. However, as these results include time
1 (0 DAI), the differences are likely due to random effects
rather than effects linked to P. psidii inoculation. Taken
together, these results provide evidence that gas exchange
was not affect by inoculation of P. psidii in resistant plants.
As to gas exchange parameters, the curves for chloro0
phyll a fluorescence parameters (F0, Fv/Fm, Fv0 =Fm
, ETR,
qP and NPQ) of both control and inoculated resistant plants
closely resemble each other (Fig. 3a–f). In addition, with
0
few exceptions [F0 (Fig. 3a), Fv0 =Fm
(Fig. 3c) and qP
(Fig. 3e) as measured at 12 DAI], no further significant
differences for chlorophyll a fluorescence parameters
between inoculated and non-inoculated plants were found,
indicating that the photochemical reactions were unlikely
affected by inoculation of P. psidii in resistant plants. As to
gas exchange parameters, the observed day-to-day variations in fluorescence parameters were most probably due to
changing environmental conditions during the experiment.
Photosynthetic performance of the susceptible clone
upon inoculation with P. psidii
Stomatal conductance was greater in non-inoculated plants
at later evaluation times (73% higher at 20 DAI) than in
their inoculated counterparts (Fig. 4a). Interestingly, we
found a significant negative correlation between average
DLA and gs means over time (Table 1), indicating that gs
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Acta Physiol Plant
Fig. 1 Rust severity in plants
inoculated with Puccinia psidii.
a Rust severity in resistant
inoculated plants was virtually
null with only small fleck
symptoms seen at 20 DAI,
b rust severity in susceptible
plant 4 DAI (2% DLA on
average), c rust severity in
susceptible plant 8 DAI (12%
DLA on average), d rust
severity in susceptible plant 12
DAI (16% DLA on average),
e rust severity in susceptible
plant 16 DAI (20% DLA on
average) and f rust severity in
susceptible plant 20 DAI (42%
DLA on average). Noninoculated plants showed no
sign of infection
decreased with the spread of DLA. The higher gs in noninoculated plants resulted in higher E (Fig. 4b), as also
noted by the positive correlation between gs and
E (Table 1). It is noteworthy that, although gs is higher in
non-inoculated plants, the Ci/Ca ratio was significantly
higher in inoculated plants, particularly at later stages of
infection (e.g., 74% higher at 20 DAI; Fig. 4c). Overall,
changes in Amax (Fig. 4d) inversely tracked those of Ci/Ca
ratio (e.g., 46% reduction in Amax at 20 DAI), a fact further
evidenced by the significant negative correlation between
these traits (Table 1) in later stages of infection. Collectively, these data indicate that the mesophyll capacity to fix
CO2 was impaired in inoculated plants. We also found that
there was a significant negative linear relationship between
average DLA and Amax means (Table 1), which might
indicate that the more susceptible the plants are, the more
impacted they should be in terms of net CO2 assimilation.
Another interesting fact is that Amax reduction is comparable to DLA at 20 DAI (reduction of 46% in Amax and
123
reduction of 42% in green leaf area), what might indicate
that photosynthesis in non-symptomatic tissue was not
hindered by P. psidii infection. Although the Ci/Ca ratio
was markedly higher in inoculated plants at 12 DAI
onwards, no significant correlation was detected between
DLA and that ratio (Table 1). Taken together, these results
indicate that gas exchange in susceptible plants was
negatively impacted by inoculation with P. psidii.
The initial fluorescence (F0) means tended to be higher
in inoculated than non-inoculated plants, with statistical
differences noted at two time points (Fig. 5a). However, no
significant correlation between DLA and F0 was found
(Table 2). The Fv/Fm ratio was also higher in non-inoculated plants, and in inoculated plants this efficiency rapidly
decreased after 12 DAI (Fig. 5b). In contrast to F0, we
found a negative significant correlation between DLA and
Fv/Fm (Table 2). As the decrease of Fv/Fm has been
associated with photoinhibition of photosynthesis, we
compared the behavior of these two parameters. In doing
Acta Physiol Plant
Fig. 2 Changes in gas
exchange parameters of
Puccinia psidii-resistant
Eucalyptus urophylla. Infectiontime courses of a stomatal
conductance (gs), b net CO2
assimilation rate (Amax),
c internal-to-ambient CO2
concentration ratio (Ci/Ca) and
d transpiration rate (E) in
resistant plants inoculated (RI)
and non-inoculated (RNI). Each
point represents the mean of six
replicates. Bars represent the
standard error. Asterisks
indicate means that differ
significantly in the given time
points (t test, p B 0.05)
so, a remarkable coincidence in the shape of the Amax and
Fv/Fm curves was seen in both inoculated and non-inoculated plants (Figs. 4d, 5b). As then expected, these variables were positively correlated with each other (r = 0.41,
p = 0.014). As to F0 and Fv/Fm values, ETR means were
significantly lower in inoculated susceptible plants at later
stages of infection (12–20 DAI) (Fig. 5d), although no
significant correlation between ETR and DLA was found.
0
Similar results were found for the Fv0 =Fm
ratio (Fig. 5c) as
well as for the photochemical (qP) (Fig. 5e) and non-photochemical (NPQ) quenching (Fig. 5f) across different
times. Although no significant correlation was obtained
between these parameters and DLA or with Amax (data not
shown), significant positive and negative correlations were
observed between many of these parameters (Table 2),
0
including Fv/Fm and Fv0 =Fm
and Fv/Fm and F0. It follows
from the above that chlorophyll fluorescence parameters in
susceptible plants were negatively impacted by inoculation
with P. psidii.
Discussion
To date, the major attempts to examine the effects of
P. psidii infection in resistant and susceptible Eucalyptus
clones have been concentrated on histological, genetic and
molecular aspects (Junghans et al. 2003a; Mamani et al.
2010; Xavier et al. 2001). To the best of our knowledge,
this is the first report of the effect of rust infection on gas
exchange and chlorophyll a fluorescence parameters in
Eucalyptus plants, and the second such report for a eucalypt disease (Pinkard and Mohammed 2006).
Our results show that gas exchange and chlorophyll
a fluorescence parameters were virtually unaffected in
the resistant clone after inoculation with P. psidii, thus
matching the good performance of this clone as empirically
noted under field conditions. In contrast, we show that
gas exchange parameters were dramatically impacted by
P. psidii infection in the susceptible clone.
It has been shown that a lower gs is one of the major
constraints to photosynthesis in diseased plants by limiting CO2 influx into leaves (Erickson et al. 2003).
Apparently, however, this is not the case in the Eucalyptus–P. psidii pathosystem since the lower gs in later
stages of infection (which probably occurred due to
pustule development, which breaks up the cuticle causing
a spread in DLA in later stages of infection) was coupled
with a higher Ci/Ca ratio in inoculated plants. This suggests that the reduction in Amax was unlikely to have been
associated with less CO2 entry into leaves, but rather with
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Acta Physiol Plant
Fig. 3 Changes of fluorescence
parameters in Puccinia psidiiresistant Eucalyptus urophylla.
Infection-time courses of
a initial fluorescence (F0),
b maximum photochemical
efficiency of photosystem II
(PSII) (Fv/Fm), c efficiency of
excitation energy capture by
open PSII reaction centers
0
), d electron transport
(Fv0 =Fm
rate (ETR), e the quenching
coefficients of photochemical
(qP) and f non-photochemical
events (NPQ) in resistant plants
inoculated (RI) and noninoculated (RNI). Each point
represents the mean of six
replicates. Bars represent the
standard error. Asterisks
indicate means that differ
significantly in the given time
points (t test, p B 0.05)
some biochemical limitation to CO2 fixation at the chloroplast level. Similar findings were reported for E. globulus plants infected with Mycosphaerella sp. (Pinkard and
Mohammed 2006). As Mycosphaerella spp. are hemibiotrophic pathogens, they may potentially share common
infection strategies as those of biotroph pathogens, such
as P. psidii, by impairing some biochemical steps of the
carbon fixation reactions.
In the majority of leaf diseases, Amax is reduced from the
beginning of the infection (Berger et al. 2007; Domiciano
et al. 2009). In fact, many pathogens may impair photosynthesis in asymptomatic, though colonized, tissues, i.e.,
the often called virtual lesion (Bastiaans 1991; Berger et al.
2007; Domiciano et al. 2009). In contrast, our results
123
demonstrate that photosynthesis was only impaired in
symptomatic tissues since (a) the reductions in Amax were
proportional to the DLA, and (b) such reductions were
initially noted only at 12 DAI, which corresponds almost
exactly to the incubation period of P. psidii, i.e., the time
spent between inoculation and appearance of the first
signs of infection (Xavier et al. 2001). Therefore, we
propose that the extent of DLA may be a good indicator
of the potential impact of the disease on the net CO2
assimilation.
In the susceptible clone, rust infection provoked
decreases in the maximum photochemical efficiency of
PSII (analyzed through the Fv/Fm ratio) paralleling
increases in F0, thus suggesting the occurrence of chronic
Acta Physiol Plant
Fig. 4 a Changes in gas
exchange parameters of
Puccinia psidii-susceptible
Eucalyptus urophylla. Infectiontime courses of a stomatal
conductance (gs), b transpiration
rate (E), c internal-to-ambient
CO2 concentration ratio (Ci/Ca)
and d net CO2 assimilation rate
(Amax) in susceptible plants
inoculated (SI) and noninoculated (SNI). Each point
represents the mean of six
replicates. Bars represent the
standard error. Asterisks
indicate means that differ
significantly in the given time
points (t test, p B 0.05)
Table 1 Correlation coefficients (above diagonal), and their respective probability values (below diagonal), between DLA, Amax, gs, Ci/
Ca and E measured in susceptible plants inoculated with Puccinia
psidii
Parameters
DLA
Amax
E
gs
Ci/Ca
DLA
1
-0.47
-0.53
-0.53
0.17
Amax
0.004*
1
0.79
0.65
-0.59
E
0.001*
0*
1
0.43
-0.54
gs
0.001*
0*
0.009*
1
0.18
Ci/Ca
0.336
0*
0.01*
0.29
1
DLA disease leaf area; Amax light-saturated net rate of CO2 assimilation; E transpiration rate; gs stomatal conductance; Ci/Ca internal-toambient CO2 concentration ratio
* Significant correlations (t test, p B 0.05)
photoinhibition to photosynthesis (Krause and Weis
1991). Concurrent decreases in the efficiency of excitation
energy capture by open PSII reaction centers (estimated
0
through the Fv0 =Fm
ratio) and in the fraction of absorbed
light that is dissipated photochemically (analyzed as qP)
were also found, suggesting that the infected plants were
not able to fully capture and exploit the collected energy.
Nonetheless, it is unlikely that the photochemical reactions may have a major impact on the rates of CO2
assimilation since the decreases in ETR were smaller than
those in Amax. Hence, the photochemical energy could not
be fully dissipated through CO2 assimilation, the usual
main sink for the absorbed light in chloroplasts. Consequently, the generation of an excess of reducing power is
to be expected. To protect the cells, surplus excitation
energy must be dissipated in alternative ways (e.g., thermal dissipation), otherwise extensive oxidative damage
could arise (Krause and Weis 1991; Lima et al. 2002).
Nevertheless, the fraction of absorbed light energy that is
dissipated thermally (analyzed as NPQ) was reduced in the
susceptible clone in later stages of infection, implying that
a fraction of PSII reactions centers is prone to suffer
photoinhibitory damage by chronic overexcitation. Noteworthy, most of the chlorotic and necrotic symptoms
were observed only in later stages of infection, probably
as a result of oxidative injury. We propose, therefore,
that insufficient adjustments in light capture, use and
dissipation may play a significant role in explaining the
clonal differences in Eucalyptus in response to P. psidii
infection.
In summary, our results suggest that (a) photosynthetic
rates were impaired by P. psidii infection in the susceptible
clone, but not in its resistant counterpart, as a result of
biochemical constraints to carbon fixation; (b) impairments
to photosynthesis were proportional to the development of
the pathogen; and (iii) overall, differences in the ability for
light capture, use and dissipation may play a significant
role in explaining the clonal differences in Eucalyptus in
response to the P. psidii infection.
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Acta Physiol Plant
Fig. 5 Changes of fluorescence
parameters in Puccinia psidiisusceptible Eucalyptus
urophylla. Infection-time
courses of a initial fluorescence
(F0), b maximum
photochemical efficiency of
photosystem II (PSII) (Fv/Fm),
c efficiency of excitation energy
capture by open PSII reaction
0
), d electron
centers (Fv0 =Fm
transport rate (ETR), e the
quenching coefficients of
photochemical (qP) and f nonphotochemical events (NPQ) in
susceptible plants inoculated
(SI) and non-inoculated (SNI).
Each point represents the mean
of six replicates. Bars represent
the standard error. Asterisks
indicate means that differ
significantly in the given time
points (t test, p B 0.05)
Table 2 Correlation coefficients (above diagonal), and their respective probability values (below diagonal), between DLA, F0, Fv/Fm, ETR,
Fv0 =Fm0 , qP and NPQ measured in susceptible plants inoculated with Puccinia psidii
Parameters
DLA
F0
Fv/Fm
ETR
NPQ
qP
0
Fv0 =Fm
DLA
1
0.25
-0.55
-0.12
-0.30
0.09
-0.17
F0
0.16
1
-0.55
-0.36
0.10
-0.31
-0.51
Fv/Fm
0.001*
0.001*
1
0.24
0.32
0.06
0.45
ETR
0.48
0.03*
0.17
1
-0.25
0.72
0.36
-0.52
-0.70
NPQ
0.07
0.50
0.06
0.15
1
qP
0.59
0.07
0.74
0*
0.001*
1
0.47
0
Fv0 =Fm
0.33
0.002*
0.007*
0*
0*
0.004*
1
DLA, disease leaf area; F0, initial fluorescence; Fv/Fm, maximum photochemical efficiency of photosystem II (PSII); ETR, electron transport
0
, efficiency of excitation energy capture by open PSII reaction centers; qP and NPQ, the quenching coefficients of photochemical and
rate; Fv0 =Fm
non-photochemical events, respectively
* Significant correlations (t test, p B 0.05)
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Acta Physiol Plant
Acknowledgments We would like to thank Gisele P. Domiciano
(UFV) and Dr. Charles Hodges (North Carolina State University) for
the detailed revision of the manuscript. This work was supported by
FAPEMIG with a research grant, and by the Brazilian National
Research Council, CNPq, with a PhD fellowship to AAA, a post-doc
fellowship to LMSG and a research fellowship to ACA and FMDM.
We also wish to thank Veracel SA for providing the clones used in
this study, and the anonymous reviewers for the detailed revision and
useful comments.
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