Scientia Horticulturae 224 (2017) 238–243

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Effects of drought stress on chlorophyll a fluorescence in two rubber tree MARK

clones
Antelmo Ralph Falquetoa, Roque Alves da Silva Júniora, Marcos Thiago Gaudio Gomesa,
⁎
João Paulo Rodrigues Martinsa, , Diolina Moura Silvab, Fábio Luiz Partellia
a
Departamento de Ciências Agrárias e Biológicas, Centro Universitário Norte do Espírito Santo, Universidade Federal do Espírito Santo, BR101 Norte, Km. 60, Bairro
Litorâneo, CEP 29932-540, São Mateus, Espírito Santo, Brazil
b
Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, Avenida Fernando Ferrari, 514, Goiabeiras, CEP
29075-910, Vitória, Espírito Santo, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: This study compared the photosynthetic responses of two clones (RRIM600 and FX3864) of the rubber tree
Hevea brasiliensis (Hevea brasiliensis L.) subjected to drought stress. This stress was imposed by complete removal of watering until
Energetic connectivity the leaf water potential (Ψw) reached critical values, which occurred at 38 days after water deficit (DAWD) for
JIP-test both rubber clones. One-year-old rubber plants were cultivated in 20 L pots filled with a soil:sand:humus ratio of
Oxygen evolution complex
4:3:3. Photosynthetic performance was analyzed by measuring chlorophyll a fluorescence transients at 0, 28, 36,
Photosystem II
Water deficit
and 38 DAWD. The photochemical process was altered to some extent following water deficit. A decrease in Ψw
was observed for both rubber clones at 36 DAWD. The FX3864 clone was more susceptible to drought and
showed a deficiency in photosynthetic electron transport. The RRIM600 rubber clone showed an advantage over
the FX3864 clone in terms of stability and efficiency in utilizing energy in low rainfall sites.

1. Introduction
Low water availability is the major environmental factor limiting
growth, development, and the agricultural production of plants
worldwide (Silva et al., 2013). An estimated one-third of the world’s
terrestrial area suffers from water stress, which is predicted to increase
owing to global warming, enhancing the reduction in crop production
in many key production regions (Tack et al., 2015).
Physiologically, several plant processes are negatively affected by
water stress. These effects occur through osmotic stress and different
biochemical responses in plants such as cell turgidity, stomatal con-
ductance, transpiration, photosynthesis, respiration, antioxidant ac-
tivity, and light absorption and capture, resulting in reduced crop
production (Lawlor and Cornic, 2002; Hsiao et al., 2010; Silva et al.,
2013; Velázquez-Márquez et al., 2015). According to Chaves et al.
(2002), the effects of low water availability on plant physiological
processes are influenced by both the intensity and duration of the en-
vironmental stress as well as the genetic capacity of the genotype/
species to cope with stress. Thus, the maintenance of vital plant me-
tabolism functions as well as the rapid recovery of water status after
rehydration are required for crop tolerance to low water availability
(Waseem et al., 2011).
Chlorophyll a fluorescence (CF) has been used to evaluate the extent
of damage to the photosynthetic apparatus, particularly to photosystem
II (PSII), under several types of environmental stress because the
technique is a non-destructive, simple, and rapid testing method (Mehta
et al., 2010; Zushi and Matsuzoe, 2017). Thus, CF is a useful tool for
monitoring and screening the stress tolerance of plant species and
genotypes (Gonçalves et al., 2010).
Under drought stress, damage to PSII reaction centers (RCs) inhibits
the primary photochemistry affecting the photosynthetic electron
transport process from CRs to the quinone A (QA), quinone B (QB), and
plastoquinone (PQ) pools (Mehta et al., 2010; Zushi and Matsuzoe,
2017). Previous work has described decreases in the maximum
quantum yield of PSII (Fv/Fm) and differences in both energetic con-
nectivity between PSII units (L-band) and stability of the oxygen evo-
lution complex (OEC) (K-band) in barley (Hordeum vulgare L.), passion
fruit (Passiflora edulis Sims) and cowpea (Vigna unguiculata) cultivars
differing in drought tolerance (Souza et al., 2004; Oukarroum et al.,
2007; Gomes et al., 2012). These studies demonstrated that after re-
watering, signals of recovery are observed owing to an increase in
drought resistance. These results suggest that it is possible to differ-
entiate the tolerance of genotypes to drought stress at the level of PSII.
Therefore, the use of drought tolerant genotypes is a viable alternative

⁎
Corresponding author.
E-mail addresses: jprmartinss@gmail.com, jprmartinss@yahoo.com.br (J.P.R. Martins).

http://dx.doi.org/10.1016/j.scienta.2017.06.019
Received 27 September 2016; Received in revised form 10 June 2017; Accepted 14 June 2017
0304-4238/ © 2017 Elsevier B.V. All rights reserved.
A.R. Falqueto et al.
to increase plant productivity in water-deficient environments (Waseem
et al., 2011).
The rubber tree (Hevea brasiliensis L.) is a Euphorbiaceae native to
Amazônia (Brazil), a tropical region. Rubber trees have been cultivated
in all other Brazilian regions and in several countries around the world.
However, the climatic conditions of most of the new cultivation regions
show reduced rainfall during certain periods of the year (Macedo et al.,
2002). Therefore, the maximal agricultural production of rubber trees
has only been made possible through irrigation practices. However,
because water availability can be limited during certain periods of the
year due to low rainfall, the use of drought-tolerant genotypes is a vi-
able alternative to improve productivity. The objective of this study was
to compare the photosynthetic changes of two clones (RRIM600 and
FX3864) of the rubber tree (H. brasiliensis) subjected to water stress,
through analysis of transient fluorescence kinetics for chlorophyll a.
2. Materials and methods
2.1. Plants, growth conditions, and drought treatment
The experiment was performed using seedlings of two rubber tree
(Hevea brasiliensis L.) clones, RRIM600 and FX3864, which are the most
commonly cultivated genotypes in Brazil. One-year-old rubber seed-
lings, approximately 50 cm tall with 10 leaves, were obtained from a
commercial nursery (Linhares, Espírito Santo State, Brazil) and culti-
vated in 20-L pots (one plant per pot) filled with a soil:sand:humus ratio
of 4:3:3. For 30 days, the pots were maintained under greenhouse
conditions with an average midday photosynthetic photon flux (PPF) of
800 μmol (photons) m−2s−1. Next, two different irrigation regimes
were applied to each rubber clone: 25 plants were maintained under
water-deficit (non-irrigated plants) and 13 plants were maintained in
well-watered conditions (plants were irrigated daily and used as a
control).
Because rubber trees show fall foliar when maintained under water
deficit, a higher number of plants were used for the water deficit
treatment to ensure sufficient CF and leaf water potential (Ψw) mea-
surements, which was made on 12 and five randomly selected plants/
treatment, respectively. Drought stress was imposed by completely re-
moving irrigation. The plants remained under persistent drought for
38 days until the Ψw values were sufficiently negative (approximately
−2.0 MPa).
2.2. Chlorophyll a fluorescence
Transient chlorophyll a fluorescence was measured at 0, 28, 36, and
38 DAWD, using a Plant Efficiency Analyzer (Handy-PEA, Hansatech,
King’s Lynn, Northfolk, England, UK). The measurements were made on
12 leaves (third or fourth leaf from the apex) that were dark-adapted for
30 min using a leaf clip (Hansatech). The light intensity reaching the
leaf was 3000 μmol (photons) m−2s−1, which was sufficient to generate
maximal fluorescence for all treatments. The fast fluorescence kinetics
(F0 to Fm) was recorded from 10 μs to 1 s. The fluorescence intensity at
20 μs (considered F0), 100 μs, 300 μs, 2 ms (FJ), and 30 ms (FI), and
maximum fluorescence (Fm) were recorded and analyzed according to
the JIP-test (Strasser et al., 2004; Stibert and Govindjee, 2011).
2.3. Leaf water potential (Ψw)
The predawn xylem water tension (MPa) was measured at 0, 28, 36,
and 38 days with a Scholander-type pressure chamber (Scholander
et al., 1965) in five plants (one leaf per plant) per treatment. When
necessary, latex extravasated by petiole was removed using a paper
towel.
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Scientia Horticulturae 224 (2017) 238–243
Days after water deficit (DAWD)
0,0
0 28 36 38
Leaf water potential (MPa)
-0,5
-1,0
-1,5 RRIM600-C
RRIM600-T
FX3860-C
-2,0 FX3860-T *
-2,5
Fig. 1. Leaf water potential (Ψw) of two rubber genotypes RRIM600 and FX3864 sub-
mitted to an imposed water stress during 38 days. The data shows value ± standard
errors. Values are means for five plants. * indicate significative difference (p ≤ 0.05)
between clones. C – control, T – treatment (drought stress).
2.4. Statistical analyses
A completely randomized design in a factorial scheme was adopted
[two water treatments (water deficit and well-watered) × four time
points (0, 28, 36, and 38 days)] for each clone. Microsoft Excel 2007
was used to create graphs for the OJIP transients. Leaf water potential
and JIP-test parameters were evaluated through variance analysis.
Means and standard errors ( ± S.E.) were reported with statistical sig-
nificance (p < 0.05) determined by Tukey’s test.
3. Results
3.1. Leaf water potential (Ψw)
Decrease in leaf water potential (Ψw) was evident after 36 DAWD
(Fig. 1). However, a significant difference between rubber clones was
only observed at 38 DAWD (−1.85 and −1.57 MPa for RRIM600 and
FX3864, respectively) (Fig. 1).
3.2. Chlorophyll a fluorescence
Relative to the control, an increase in the J-step fluorescence level
was the most evident characteristic of CF and OJIP transients for both
rubber tree clones following water deficit. In both clones, the J-step
fluorescence levels increased over time with water deprivation (Fig. 2a
and b). Although an increase in J-step fluorescence levels in RRIM600
relative to control was observed at 28, 36, and 38 DAWD, no difference
in J-step fluorescence levels was observed at 28 and 36 DAWD for the
FX3864 rubber clone (Fig. 2a and b).
To further elucidate the differences between clones in response to
drought stress, the relative fluorescence between the steps O and K [20 and
300 μs, respectively = VOK = (Ft − F0)/(FK − F0)] and O and J [20 μs and
2 ms, respectively = VOJ = (Ft − F0)/(FJ − F0)] were normalized and are
shown as the kinetic difference ΔVOK = VOK(treatment) − VOK(control) and
ΔVOJ = VOJ(treatment) − VOJ(control), respectively (Fig. 2c–f). The kinetic dif-
ferences ΔVOK and ΔVOJ make the L- and K-bands visible, respectively.
These bands have a peak around 0.15 and 0.3 ms, respectively. The L and K-
band are an indicator of energetic connectivity or grouping between PSII
units and the stability of OEC, respectively (Strasser and Stirbet, 1998). In
this study, the response of the L- and K-bands to water deficit was different
for two rubber clones. In RRIM600, the energetic connectivity and the
stability of OEC decreased from 28 DAWD and reached a maximum de-
crease at 38 DAWD (Fig. 2c and e). In FX3864, the appearance of positive L-
and K-bands occurred only at 36 DAWD (Fig. 2d and f). Notably, at 38
DAWD, the maximum values for both the L- and K-bands were higher for
A.R. Falqueto et al.
FX3864 than for RRIM600 (approximately 0.08–0.12 and 0.08–0.16 for
ΔVOK and ΔVOJ in RRIM600 and FX3864, respectively).
For the RRIM600 rubber clone, no significant change relative to
control was observed in the values of initial fluorescence (F0) until 36
DAWD (Fig. 3a). However, at 36 DAWD, F0 values were significantly
higher for FX3864 than for the control (Fig. 3b). Both clones reached
the maximum values of F0 at 38 DAWD (750 and 700 for FX3864 and
RRIM600, respectively). There was no significant variation in the
maximum fluorescence (Fm) values (data not shown). Nevertheless,
water deficit reduced the maximum quantum yield for primary photo-
chemistry (Fv/Fm) values, starting from 36 and 28 DAWD in RRIM600
and FX3864, respectively (Fig. 3c and d).
The specific energy fluxes expressed per RC, ABS/RC (absorption),
and DI0/RC (dissipation) values are presented in Fig. 3e–h. Relative to
the control, the ABS/RC and DI0/RC of the FX3864 plants under water
deprivation increased at 36 and 38 DAWD, whereas differences in ABS/
RC were only observed at 38 DAWD in RRIM600 (Fig. 3e–h). For
FX3864, DI0/RC values were higher at 38 DAWD compared to RRIM600
(1.7 and 0.8 for FX3864 and RRIM600, respectively). The performance
index (PItotal) behaved similarly between the two clones under drought
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Scientia Horticulturae 224 (2017) 238–243
Fig. 2. Fluorescence induction OJIP curves with
double normalization between Fo and FM [VOP =
(FT − F0)/(FM − F0)] plotted on logarithmic time
scale from 10 μs to 1 s (A and B), kinetic differences
of VOK (C and D) and VOJ (E and F) obtained after
double normalization between the steps O–K
[ΔVOK = VOK(treatment) − VOK(control)] and O–J
[ΔVOJ = VOJ(treatment) − VOJ(control)], respectively, of
two rubber genotypes RRIM600 (A, C and E) and
FX3864 (B, D and F) submitted to an imposed water
stress during 38 days. Values are means for 12
plants.
stress and a significant decrease in values was observed at 36 DAWD
(Fig. 4).
4. Discussion
The decrease in Ψw values observed at 38 DAWD represents a re-
duction of approximately four-fold compared to control plants, which
could be observed in the form of wilting, leaf fall, and desiccation of
seedlings. Ψw values are used to assess the severity of water deficit and
may not change under moderate drought stress (Lee et al., 2016). A
previous study reported that under drought stress, no change in Ψw was
observed in mung bean plants (Vigna radiata L.) owing to an increased
leaf turgor potential (Afzal et al., 2014). In the present study, a similar
observation regarding Ψw values in both rubber tree clones maintained
under water deficit could be related to two factors: similar water-con-
ducting capacity and similar stomatal behavior in response to a specific
hydraulic signal (Sinclair et al., 2008). Gomes et al. (2012) reported
similar results when comparing the water status between two passion
fruit cultivars (FB200 and FB300) growing under water deficit.
Guimarães et al. (2006) and Santos et al. (2010) reported that small
A.R. Falqueto et al. Scientia Horticulturae 224 (2017) 238–243

900 Fig. 3. Initial fluorescence (F0–A,B), maximum quantum yield for

(A) Water deficit (B) Water deficit primary photochemistry (Fv/Fm – C,D), specific energy fluxes of ab-
850
Control Control sorption (ABS/RC – E,F) and dissipation (DI0/RC – G,H) expressed per
c
800 RC of two rubber genotypes RRIM600 (A, C, E and G) and FX3864 (B,
D, F and H) submitted to an imposed water stress during 38 days. The
750 b b values correspond to the average ± standard errors for 12 plants.
700 The small letters indicate significant difference between days of water
Fo (a.u.)

650 ab deprivation (to plants control, no significant difference was observed

a between days). Asterisks indicate significant difference (p ≤ 0.05)
600
a a a
between treatments (irrigated and non-irrigated plants).
550
500 *
* *
450
400
(C) (B)
0.9

0.78 a a a
a a
a
*
Fv/Fm (a.u.)

0.66 * a
*
0.54

0.42

0.3

(E) (F) c
3.6

3 a

a b
2.4
ABS/RC (a.u.)

a a a
1.8 a

1.2 * * *

0.6

0
(G) (H) b
1.8

1.5

1.2 b
DIo/RC (a.u.)

ab
0.9 ab

0.6 a a
a a
0.3
*
* *
0
0 28 36 38 0 28 36 38
Days after water deprivation

variations in Ψw may be verified after water deficit when plants activate
tolerance mechanisms, such as the synthesis and accumulation of
compounds with osmotic activity, modifications in volumetric elastic
modulus (ε) that increase or decrease the cell wall rigidity, and the
formation of small cells (Chaves et al., 2003; Lambers et al., 2008;
Redillas et al., 2011).
Despite the similar behavior of Ψw values between the two rubber
clones, the effects of water deficit differentially affected the photo-
chemical parameters of the plants, as analyzed through CF transient
measurements. This allowed for a comparison between the
photochemical mechanisms that may be involved in the physiological
responses of the two rubber tree clones subjected to drought stress as
well as the site of action of drought stress on the electron transport
chain in each rubber clone. In this study, the effects of drought stress on
the CF transient parameters for RRIM600 and FX3864 rubber clones are
presented in Figs. 2–4. Under water deficit, the electron transference in
PSII beyond QA was delayed and this physiological event should result
in a fast increase of the J-step level. The increase in fluorescence in-
tensity at the J-step level is interpreted as a decrease in electrons
transported beyond reduced QA or to the peak concentrations of QA−QB

241
A.R. Falqueto et al.
4 Fig. 4. Performance index (PItotal) of two rubber genotypes RRIM600
(A) Water deficit (B) Water deficit
b b
3.5 Control Control
3 days of water deprivation. Asterisks indicate significant difference
a a
ab
PItotal (a.u.)
2.5 a a
2
1.5
b b
b b
1 a
a a
0.5 a
* *
0
0 28 36 38 0 28
Days after water deprivation
(Haldiman and Strasser, 1999; Chen et al., 2015). In general, the ac-
cumulation of reduced QA− is a common response for plants exposed to
environmental stress, specifically drought stress.
To elucidate the differences in drought tolerance between RRIM600
and FX3864, the relative fluorescence between the steps O and K (VOK)
and O and J (VOJ) were normalized and are shown as the kinetic dif-
ference ΔVOK and ΔVOJ, respectively, permitting us to identify the ap-
pearance of the L- and K-bands. The L-band is an indicator of energetic
connectivity or grouping between PSII units. Positive L-band values are
interpreted as lower energetic connectivity or weakened use of the
excitation energy and reduced stability of the system (Strasser and
Stirbet, 1998; Strasser et al., 2004; Zhang et al., 2016). Further, the
inactivation of the OEC and/or an increase in the functional PSII an-
tenna size result from positive K-band values (Yusuf et al., 2010). In
FX3864 clone, a larger difference in the L- and K-bands between the
control (day zero) and stressed plants was observed only at 36 DAWD.
However, at 38 DAWD, the values of both the L- and K-bands were
higher in FX3864 than in RRIM600. The higher L- and K-band values
after 38 DAWD suggest greater damage to the energy connectivity or
grouping between PSII units and to the OEC, respectively. These results
indicate that FX3864 is able to maintain the balance between the
electrons at the acceptor and donor sites within PSII when subjected to
moderate water stress (28 DAWD) but not to severe stress (38 DAWD).
In plants, certain physiological mechanisms are activated to protect the
photosynthetic apparatus from stress. Osmoregulation appears to be an
efficient mechanism protecting the OEC of plants during water deficit
and high salinity (De Ronde et al., 2004), explaining the differences in
OEC stability between different plants and conditions. L- and K-bands
with positive amplitudes were previously recorded for unicellular green
algae (Scenedesmus obliquus) (Strasser, 1997), barley (Oukarroum et al.,
2007), transgenic Brassica juncea plants overexpressing the γ-TMT gene
(Yusuf et al., 2010), rice (Redilhas et al., 2011), and passion fruit
(Gomes et al., 2012).
The behavior of F0 differed between genotypes, with FX3864 de-
monstrating a higher sensitivity to water deprivation (notably, F0 va-
lues increased from 36 DAWD for FX3864). The cause of the increase in
F0 is likely an inhibition of the PSII reaction center, which inhibits the
electron flow from QA to QB and decreases the efficiency of energy
trapping at PSII. According to Strasser and Strasser (1995), an increase
in F0 has been associated with rapidly reversible damage to the D1
protein linked to PSII. In this study, the increase of F0 observed mainly
in FX3864, was further reflected by a significant increase in the ABS/RC
and DI0/RC ratios relative to the control. In the present study, the ABS/
RC ratio increased by approximately 62% and 126% after 36 and 38
DAWD, respectively. In RRIM600, the ratio only increased at 38 DAWD
and was approximately 50% of the control. Similarly, on the day of
maximum stress, the DI0/RC ratio increased by approximately 247%
and 695% in RRIM600 and FX3864, respectively.
According to Mehta et al. (2010), the ABS/RC ratio is calculated as
Scientia Horticulturae 224 (2017) 238–243
(A) and FX3864 (B) submitted to an imposed water stress during
38 days. The values correspond to the average ± standard errors for
ab 12 plants. The small letters indicate significant difference between
(p ≤ 0.05) between treatments (irrigated and non-irrigated plants).
* *
36 38
the total number of photons absorbed by chlorophyll molecules from all
RCs divided by the total number of active RCs, and is affected by the
ratio of active:inactive RCs. There are two possible explanations for the
increase in ABS/RC: (1) the increase in apparent antenna size or (2) the
decrease in active RC, i.e., by being transformed into QA-reducing
centers (Strasser and Stirbet, 1998; Yusuf et al., 2010). In this study, the
second explanation gives us some insight into the increase in ABS/RC
because changes in the L-band were observed after water deprivation in
both rubber clones, particularly in FX3864, for which highly positive L-
band values were observed. The higher values observed in the FX3864
rubber clone confirm its higher sensitivity to drought treatment. The
same observation using JIP-test parameters for stressed plants has been
reported elsewhere (Gomes et al., 2012).
In general, high DI0/RC values associated with reduced values of Fv/
Fm is linked to the occurrence of photoinhibition in plants (Martins
et al., 2015; Hazratia et al., 2016), because reductions in Fv/Fm occur
when the structure and function of PSII is impaired by stress (Souza
et al., 2004). In this physiological condition, protective mechanisms are
overwhelmed by water deprivation, resulting in membrane-related
damage (Souza et al., 2004). The maximum quantum yield of PSII
photochemistry is widely considered a sensitive indicator of environ-
mental stress (Lee et al., 2016). In this sense, the absorbed energy by
the photosynthetic system was released as heat, as shown by the vari-
able DI0/RC values. These results indicate a higher photoinhibition in
the FX3864 rubber clone, considering the reduction in electron trans-
port and an increased deviation of absorbed light energy as heat or
fluorescence (Araújo and Deminicis, 2009). In addition, the photo-
inhibition for this clone may be due to the absence of anthocyanin
pigments in its leaves which play a photoprotective role. Reductions in
Fv/Fm are characteristics of drought events. Ennajeh et al. (2009) ex-
amined olive tree cultivars both tolerant and sensitive to drought and
also found a decline in Fv/Fm as desiccation became more severe. Re-
ductions in Fv/Fm imply reduced efficiency of the photochemical con-
version process, which may suggest possible damage and inhibition of
PSII activity (Martins et al., 2015). Finally, an increase in the ABS/RC
and DI0/RC ratios, combined with the reduction in Fv/Fm, resulted in a
decrease in PItotal for both rubber clones. PItotal values represent the
energy flow efficiency of the photosynthetic transport chain (Yusuf
et al., 2010). PItotal is closely related to the overall growth and survival
of plants under stress conditions and has been described as a very
sensitive parameter for the JIP-test (Martins et al., 2015). Similar re-
sults were described by Sousa et al. (2014) in rice plants after exposure
to herbicides.
5. Conclusion
The decrease in Ψw values had a significant effect on the photo-
chemical activity of rubber tree seedlings, reducing the photosynthetic
performance, although the Ψw values had the same progression
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A.R. Falqueto et al. Scientia Horticulturae 224 (2017) 238–243

throughout the experiment in both rubber clones. The FX3864 clone during acclimatization in response to light levels. In Vitro Cell Dev. Biol. Plant. 51,
471–481.
showed a lower photochemical ability to tolerate water deficit. Under Mehta, P., Allakhverdiev, S.I., Jajoo, A., 2010. Characterization of photosystem II het-
low water availability, the reduction in active RCs decreased the energy erogeneity in response to high salt stress in wheat leaves (Triticum aestivum).
capture by both rubber clones, but affected the FX3864 clone to a Photosynth. Res. 105, 249–255.
Oukarroum, A., Madidi, S.E., Schansker, G., Strasser, R.J., 2007. Probing the responses of
greater extent. Thus, the RRIM600 rubber clone demonstrates an ad- barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under
vantage over the FX3864 clone in terms of stability and efficiency in drought stress and re-watering. Environ. Exp. Bot. 60, 438–446.
utilizing energy under low water availability conditions. Redillas, M.C.F.R., Strasser, R.J., Jeong, J.S., Kim, Y.S., Kim, J.K., 2011. The use of JIP
test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10. Plant
Biotechnol. Rep. 5, 169–175.
References Santos, F.S., Lima, G.P.P., Morgado, L.B., 2010. Tolerância e caracterização bioquímica
em feijão-caupi submetido a estresse hídrico na pré-floração. Naturalia 33, 34–44.
Scholander, P.F., Hammel, H.T., Bradstreet, E.D., Hemminbsen, E.A., 1965. Sap pres-sure
Afzal, A., Gulzar, I., Shahbaz, M., Ashraf, M., 2014. Water deficit-induced regulation of
in vascular plants. Science 148, 339–346.
growthgas exchange, chlorophyll fluorescence, inorganic nutrient accumulation and
Silva, P.E.M., Cavatte, P.C., Morais, L.E., Medina, E.F., DaMatta, F.M., 2013. The func-
antioxidative defense mechanism in mungbean [Vigna radiata (L.)Wilczek]. J. Appl.
tional divergence of biomass partitioning, carbon gain and water use in Coffea ca-
Bot. Food Qual. 87, 147–156.
nephora in response to the water supply: implications for breeding aimed at im-
Araújo, S.A.C., Deminicis, B.B., 2009. Fotoinibição da Fotossíntese. Revista Brasileira de
proving drought tolerance. Environ. Exp. Bot. 87, 49–57.
Biociências 7, 463–472.
Sinclair, T.R., Wieniecki, M.A., Holbrook, N.M., 2008. Low leaf hydraulic con-ductance
Chaves, M.M., Pereira, J.S., Maroco, J., Rodrigues, M., Ricardo, C.P.P., Osório, M.L.,
associated with drought tolerance in soybean. Physiol. Plant. 132, 446–451.
Carvalho, I., Faria, T., Pinheiro, C., 2002. How plants cope with water stress in the
Sousa, C.P., Pinto, J.J.O., Martinazzo, E.G., Perboni, A.T., Farias, M.E., Bacarin, M.A.,
field: photosynthesis and growth. Ann. Bot. 89, 907–916.
2014. Chlorophyll a fluorescence in rice plants exposed of herbicides of group imi-
Chen, S., Kang, Y., Zhang, M., Wang, X., Strasser, R.J., Zhou, B., Qiang, S., 2015.
dazolinone. Planta Daninha 32, 141–150.
Differential sensitivity to the potential bioherbicide tenuazonic acid probed by the
Souza, R.P., Machado, E.C., Silva, J.A.B., Lagoa, A.M.M.A., Silveira, J.A.G., 2004.
JIP-test based on fast chlorophyll fluorescence kinetics. Environ. Exp. Bot. 112, 1–15.
Photosynthetic gas exchange, chlorophyll fluorescence and some associated meta-
De Ronde, J.A., Cress, W.A., Kruger, G.H.J., Strasser, R.J., Van Staden, J., 2004.
bolic changes in cowpea (Vigna unguiculata) during water stress and recovery.
Photosynthetic response of transgenic soybean plants, containing an Arabidopsis
Environ. Exp. Bot. 51, 45–56.
P5CR gene, during heat and drought stress. J. Plant Physiol. 161, 1211–1224.
Stibert, A., Govindjee, 2011. On the relation between the Kautsky effect (Chlorophyll a
Ennajeh, M., Mohamed, A., Khemira, H., 2009. Osmoregulation and osmoprotection in
fluorescence induction) and photosystem II: basics and applications of the OJIP
the leaf cells of two olive 32 Jafari et al. cultivars subjected to severe water deficit.
fluorescence transient. J. Photochem. Photobiol. B: Biol. 104, 236–257.
Acta Physiol. Plant. 31, 711–721.
Strasser, R.J., Stirbet, A.D., 1998. Heterogeneity of photosystem II probed by the nu-
Gomes, M.T.G., Luz, A.C., Santos, M.R., Batitucci, M.C.P., Silva, D.M., Falqueto, A.R.,
merically simulated chlorophyll a fluorescence rise (O–J–I–P). Math. Comput.
2012. Drought tolerance of passion fruit plants assessed by the OJIP chlorophyll a
Simulat. 48, 3–9.
fluorescence transiente. Sci. Hort. 142, 49–56.
Strasser, B.J., Strasser, R.J., 1995. Measuring fast fluorescent transients to address en-
Gonçalves, E.R., Ferreira, V.M., Silva, J.V., Endres, L., Barbosa, T.P., Duarte, W.G., 2010.
vironmental questions: the JIP-test. In: Mathis, P. (Ed.), Photosynthesis: From Light to
Trocas gasosas e fluorescência da clorofila a em variedades de cana-de-açúcar sub-
Biosphere. V. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp.
metidas à deficiência hídrica. Rev. Bras. Eng. Agríc. Ambient. 14, 378–386.
977–980.
Guimarães, C.M., Stone, L.F., Brunini, O., 2006. Adaptação do feijoeiro comum (Phaseolus
Strasser, R.J., Tsimilli-Micheal, M., Srivastava, A., 2004. Analysis of the chlorophyll a
vulgaris L.) à seca. Rev. Bras. Eng. Agríc. Ambient. 10, 70–75.
fluorescence transient. In: Govindjee, Papageorgiou, G.C. (Eds.), Chlorophyll a
Haldiman, P., Strasser, R.J., 1999. Effects of anaerobiosis as probed by the polyphasic
Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and
chlorophyll a fluorescence rise kinetic in pea (Pisum sativum L.). Photosynth. Res. 62,
Respiration. Springer, Berlin, pp. 321–362.
67–83.
Strasser, J.B., 1997. Donor side capacity of Photosystem II probed by chlorophyll a
Hazratia, S., Tahmasebi-Sarvestania, Z., Modarres-Sanavya, S.A.M., Mokhtassi-Bidgolia,
fluorescence transients. Photosynth. Res. 52, 147–155.
A., Nicola, S., 2016. Effects of water stress and light intensity on chlorophyll fluor-
Tack, J., Barkley, A., Nalley, L.L., 2015. Effect of warming temperatures on US wheat
escence parameters and pigments of Aloe vera L. Plant Physiol. Biochem. 106,
yields. Proc. Nat. Acad. Sci. 112, 6931–6936.
141–148.
Velázquez-Márquez, S., Conde-Martínez, V., Trejo, C., Delgado-Alvarado, A., Carballo, A.,
Hsiao, S., Chen, S., Yang, I., Chen, C., Tsai, C., Chuang, Y., Wang, F., Chen, Y., Linc, T., Lo,
Suárez, R., Mascorro, J.O., Trujillo, A.R., 2015. Effects of water deficit on radicle apex
Y., 2010. Evaluation of plant seedling water stress using dynamic fluorescence index
elongation and solute accumulation in Zea mays L. Plant Physiol. Bioc. 96, 29–37.
with blue LED-based fluorescence imaging. Comput. Electron. Agric. 72, 127–133.
Waseem, M., Ali, A., Tahir, M., Nadeem, M.A., Ayub, M., Tanveer, A., Ahmad, R., Hus-
Lambers, H., Chapin III, F.S., Pons, T.L., 2008. Plant Physiological Ecology, second ed.
sain, M., 2011. Mechanism of drought tolerance in plant and it management through
Springer, New York, pp. 175–178.
different methods. Cont. J. Agric. Sci. 5, 10–25.
Lawlor, D.W., Cornic, G., 2002. Photosynthetic carbon assimilation and associated me-
Yusuf, M.A., Kumar, D., Rajwanshi, R., Strasser, R.J., Tsimilli-Michael, M., Govindjee
tabolism in relation to water deficits in higher plants. Plant Cell Environ. 25,
Sarin, N.B., 2010. Overexpression of (-tocopherol methyl transferase gene in trans-
275–294.
genic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a
Lee, T.Y., Woo, S.Y., Kwak, M.J., Inkyin, K., Lee, K.E., Jang, J.H., Kim, I.R., 2016.
fluorescence measurements. Biochim. Biophys. Acta 1797, 1428–1438.
Photosynthesis and chlorophyll fluorescence responses of Populus sibirica to water
Zhang, L., Li, Y., Liu, J., 2016. Complete inactivation of photosynthetic activity during
deficit in a desertification area in Mongolia. Photosynthetica 54, 317–320.
desiccation and rapid recovery by rehydration in the aerial microalga Trentepohlia
Macedo, R.L.G., Kamel, T.O., Venturim, N., Gomes, J.E., 2002. Introdução de clones de
jolithus. Plant Biol. 18, 1058–1061.
seringueira no Nordeste do Estado de Minas Gerais. Cerne 8, 124–133.
Zushi, K., Matsuzoe, N., 2017. Using of chlorophyll a fluorescence OJIP transients for
Martins, J.P.R., Schimildt, E.R., Alexandre, R.S., Falqueto, A.R., Otoni, W.C., 2015.
sensing salt stress in the leaves and fruits of tomato. Sci. Hort. 219, 216–221.
Chlorophyll a fluorescence and growth of Neoregelia concentrica (Bromeliaceae)

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