ORIGINAL ARTICLE

Photosynthetic adjustment after rehydration in Annona
emarginata

Luı́s Paulo Benetti Mantoan1 • Luiz Fernando Rolim de Almeida1 •

Ana Claudia Macedo2 • Gisela Ferreira1 • Carmen Silvia Fernandes Boaro1

Received: 8 December 2015 / Revised: 3 March 2016 / Accepted: 12 May 2016 / Published online: 30 May 2016

� Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2016

Abstract Reports indicate that Annona emarginata is tol-

erant to drought and is also used as an alternative rootstock

for atemoya under drought conditions. The photosynthetic

process can be adjusted after rehydration, resulting on total

or partial recovery. The aim of this study was to determine

if A. emarginata shows adjusts in gas exchange and the

chlorophyll a fluorescence pattern after rehydration. Dur-

ing water deficits, the gas exchange and water content in

the leaf decreased. However, after 5 days of rehydration,

the water content in the leaf recovered and rehydrated

plants presented the water use efficiency better than irri-

gated plants. Further remaining gas exchange parameters

were lower in relation to irrigated plants. In chlorophyll

a fluorescence, the rehydrated plants showed higher dissi-

pation of light energy as heat, maintaining high activity of

photoprotection. After rehydration, A. emarginata shows a

positive correlation between transpiration and CO2 assim-

ilation rate, which optimize the water use efficiency. Thus,

A. emarginata presents adjustments in gas exchange and

photochemical process, resulting on a possible long-term

photosynthetic acclimation to water deficiency.

Keywords Water deficit � Photosynthesis � Rootstock �
Recovery � Drought � Annonaceae

Introduction

Lack of water is an environmental constraint for agricultural

production (Chaves et al. 2003; Endres 2007; Sinclair et al.

2008) and for the development of plant communities (Boyer

1982; Verslues et al. 2006). A better understanding of the

drought effect on the physiological processes on plants is a

vital importance to improve practices of management and to

predict the fate of natural vegetation under climate change

(Chaves et al. 2003). Adjustments in the main parameters of

the photosynthetic process occur in response to environ-

mental changes. These adjustments regulate the photosyn-

thesis during the day (Geiger and Servaites 1994). Therefore,

the evaluation of photosynthesis along the day may provide

information about the adaptive potential of plants on the

environment (Li et al. 2015), in special under water deficit

conditions (Tominaga et al. 2014).

Stomatal conductance is sensitive to water deficit (Yor-

danov et al. 2000; Medrano et al. 2002), because the reduc-

tion in stomatal aperture controls water loss (Chaves et al.

2003; David et al. 2007) and prevents xylem cavitation

(David et al. 2007). However, the low stomatal conductance

regulates photosynthesis in plants (Yordanov et al. 2000;

Medrano et al. 2002), which restricts the entrance of CO2 and

reduces the photosynthetic carbon assimilation (Flexas et al.

2004, 2007). Furthermore, the CO2 assimilation of plants

under a water deficit can also be limited by metabolic issues,

such as damage on the enzymes of photosynthesis and on

photochemical processes that are responsible for generate

energy used to CO2 reduction (Grassi and Magnani 2005;

Galmés et al. 2007; Varone et al. 2012; Ashraf and Harris

Communicated by S. Weidner.

& Luı́s Paulo Benetti Mantoan

luismantoan@hotmail.com

1 Departamento de Botânica, Instituto de Biociências,

Universidade Estadual Paulista ‘‘Júlio de Mesquita Filho’’

(UNESP), Botucatu, SP 18618-689, Brazil

2 Departamento de Horticultura, Faculdade de Ciências

Agronômicas, Universidade Estadual Paulista ‘‘Júlio de

Mesquita Filho’’ (UNESP), Botucatu, SP 18610-307, Brazil

123

Acta Physiol Plant (2016) 38:157

DOI 10.1007/s11738-016-2171-1

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2013). Thus, photosynthesis plays a key role on plant phys-

iological performance under drought conditions (Pinheiro

and Chaves 2011).

It is known that the CO2 assimilation rate decreases during

moderate water deficits or in response of decreased humidity

(Chaves et al. 2003). However, few studies reported the

photosynthetic response to rehydration (Izanloo et al. 2008;

Xu et al. 2009). In general, the recovery of the photosynthetic

rate after rehydration can occur quickly and completely or

slow and partially (Miyashita et al. 2005; Chaves et al. 2009).

In Populus euphratica Oliv. under water deficit followed by

rehydration, Bogeat-Triboulot et al. (2007) observed partial

recovery of CO2 assimilation and stomatal conductance in

rehydrated plants, suggesting a possible long-term acclima-

tion to water deficit, due to an increase of the instantaneous

water use efficiency. However, in Setaria viridis (L.) Beauv.

and Digitaria ciliaris (Retz.) Pers., which were also subjected

to rehydration after a period of water deficit, Luo et al. (2010)

observed a complete recovery of CO2 assimilation and

stomatal conductance. This can result in fast growth

resumption on these plants, which would provide an advan-

tage of competition for available water (Luo et al. 2010).

The use of rootstocks tolerant to drought is a strategy

used to increase the resistance to water deficiency in

commercial plants (Colla et al. 2010; Martı́nez-Ballesta

et al. 2010). The species Annona emarginata (Schltdl.) H.

Rainer (araticum-de-terra-fria) has good compatibility

with atemoya (Annona squamosa L. 9 Annona cherimola

Mill.), which results in orchards with a higher survival rate

and tolerance to root fungus. In addition, reports of farmers

indicate that A. emarginata species has a tolerance to soil

with water shortages (Tokunaga 2000). According to the

information above, the hypothesis of this study was that

after rehydration, A. emarginata presents changes in gas

exchange and photochemical process to optimize photo-

synthesis and water consumption, resulting on a possible

photosynthetic acclimation to the water deficit. Therefore,

the aim of this study was to evaluate if A. emarginata after

rehydration shows adjustments in the patterns of gas

exchange and chlorophyll a fluorescence.

Materials and methods

Plant material and experimental design

The experiment was conducted on the experimental area of

the Botany Department at the Universidade Estadual Pau-

lista ‘‘Júlio de Mesquita Filho’’ (UNESP) of Botucatu,

State of São Paulo, Brazil (228530S, 488260W).

The seedlings ofA. emarginatawere obtained from seeds,

which were cultivated in 4.5 L polyethylene bags filled with

vermiculite and maintained in an environment with a 50 %

reduction in sunlight. During growth, plants were irrigated

twice a day until the occurrence of water percolation, and

once a week, we applied a Hoagland and Arnon (1950)

solution at 50 % ionic strength. After 524 days of sowing,

which was the moment of the start of the treatments, the

plants were maintained under plastic cover with a 50 %

reduction in sunlight to prevent the interruption of the water

deficit treatment by the rain. The daytime averages of air

temperature, relative humidity, vapor pressure deficit of the

air (VPD) and photosynthetic photon flux density (PPFD)

during the treatment were 28.5 �C, 48.8 %, 2.2 kPa and

757 lmol m-2 s-1, respectively.

The experimental design used was a randomized block

with treatments: irrigation, where the vessels were hydrated

twice a day, until the observation of water percolation;

suspension of irrigation, where the irrigation was stopped;

and rehydration, where irrigation was stopped until 38 days

after the start of the treatment (DAST), when leaves pre-

sented withered, with posterior rehydration. This experi-

ment utilized 24 plants of A. emarginata. Of this total, 12

plants were used for the evaluation of gas exchange and

chlorophyll a fluorescence, with three treatments and four

repetitions of one plant. The 12 remaining plants were

subjected only to suspension of irrigation treatment with

rehydration, to monitor the level of dehydration. For this,

was evaluated the relative water content in leaves (RWC)

using four repetitions of one plant.

Control of irrigation

The monitoring of the substrate water content (SWC) was

performed according to Thameur et al. (2012), where the

mass of the vessel during application of the treatments

(MVtreatments) was compared with the mass of these same

vessels when irrigated until they achieved a maximum

water holding capacity (MV100 %). The MV100 % was

obtained through irrigation until the occurrence of perco-

lation of the excess of water, which occurred at night, and

for the later weighing vessel, the following morning. The

SWC was calculated using the formula: SWC = (MVtreat-

ments/MV100 %) 9 100 (Varone et al. 2012).

Relative water content in the leaves

The relative water content in the leaf (RWC) was evaluated

once a week in plants submitted to suspension of irrigation

followed by rehydration, using four replicates of one plant.

For this, a leaf sample of 2 9 2 cm was removed from the

second or third fully expanded leaf of each plant. This sample

was weighed to determine the fresh mass (FM) and immersed

in deionized water during 4 hours to determine the turgid

mass (TM). Then, the sample was placed in a forced air

circulation oven at 70 �C until a constant mass was achieved

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to determine the dry matter (DM). The RWC was calculated

by RWC = (FM - DM)/(TM - DM) 9 100 (Weatherley

1949).

Gas exchange

The gas exchange were monitored during the DAST for

irrigation and suspension of irrigation treatments at 10 h,

and at the 43rd DAST (5 days after rehydration) for the

irrigation, suspension of irrigation and rehydration treat-

ments, at 9, 10, 11, 12, 14, and 16 h through an infrared gas

analyzer (IRGA) (LI-6400, LI-COR, USA). Four replicate

measurements were performed per treatment in the second

and third fully expanded leaves. The average of the read-

ings was used to evaluate the gas exchange in these plants.

The parameters evaluated were: the CO2 assimilation rate

(ANet, lmol CO2 m-2 s-1), the stomatal conductance (gS,

mol H2O m-2 s-1), the transpiration rate (E, mmol

H2O m-2 s-1), the internal CO2 concentration in the sub-

stomatal chamber (Ci, lmol CO2 mol-1 ar), the carboxy-

lation efficiency (ANet/Ci) and the water use efficiency

(ANet/E) (lmol CO2 mmol H2O-1).

Chlorophyll a fluorescence

The chlorophyll a fluorescence was evaluated at 44 DAST

(6 days after rehydration) in the irrigation and rehydration

treatments at 12 h (period of greatest luminosity) using a

modulated pulse fluorometer (JUNIOR-PAM, Walz, Ger-

many). Four replicate measurements were performed per

treatment, and these measures were derived from the

average of the readings collected in the second and third

fully expanded leaves.

Before starting the measurements, the leaves were adap-

ted to the dark during 30 min. After this period, a saturation

pulse of 10,000 lmol m-2 s-1 of PPFD was applied during

0.6 s to obtain the Fm (maximum fluorescence adapted to

darkness) and Fm’ (maximum fluorescence adapted to light).

The values of Fo (minimal fluorescence adapted to dark) and

Fo’ (minimal fluorescence adapted to light) were also

obtained. After determination of Fm, predefined pulses of

125, 190, 285, 420, 625, 820, 1150, and 1500 lmol m-2 s-1

of PPFD were applied for 15 s.

The following parameters were calculated: the fraction

of light absorbed by the photosystem II (PSII) antenna used

to photochemical electron transport (P, photochemical), the

fraction of light absorbed by the PSII antenna that is dis-

sipated as heat (D, heat dissipation), the fraction of exci-

tation energy not dissipated in the antenna that cannot be

utilized for photochemistry (E, excess energy) (Demmig-

Adams et al. 1996) and the efficiency of excitation energy

captured by open PSII reaction centers (/exc) ((Fm’ - Fo’)/

Fm’) (Zribi et al. 2009).

Statistical analysis

Statistical analyses were performed using SigmaPlot soft-

ware (version 12). The data were submitted to the nor-

mality test of Shapiro–Wilk (P\ 0.05). Therefore, to

evaluate the differences between treatments in the gas

exchange, a one way analysis of variance ANOVA for

repeated measures followed by Tukey’s test (P\ 0.05)

was conducted. For chlorophyll a fluorescence, a two way

ANOVA (treatments 9 PPFD) was performed followed by

Tukey’s test (P\ 0.05). The gas exchange parameters of

the rehydration treatment were submitted to the Pearson

correlation test (P\ 0.05).

Results

Monitoring the water deficit

Plants of A. emarginata submitted to the suspension of

irrigation showed decreased of SWC and RWC, reaching

values of 28 and 73 %, respectively, at 38 DAST (last day

of water shortage) (Fig. 1a, b). After rehydration, the SWC

was 99 % at 45 DAST and the RWC was 90 % at 44 DAST

(Fig. 1a, b).

In the gas exchange monitored over the DAST, the

plants under suspension of irrigation showed negative ANet

from 30 DAST and low gS from 16 DAST (Fig. 2a, b). At

31 DAST, the SWC and RWC were 36 and 82 %,

respectively, and at 17 DAST the SWC and RWC were 52

and 87 %, respectively (Fig. 1a, b).

Gas exchange throughout the day

Under rehydration, A. emarginata showed lower ANet at 9

and 10 h (Fig. 3a), lower gS at 9, 10, 11, and 12 h

(Fig. 3b), lower E at 9, 10, 11, and 12 h (Fig. 3c), lower

Ci at 9, 10, and 11 h (Fig. 3d) and lower ANet/Ci at 9 h

(Fig. 3e), in relation to irrigation treatment at 43 DAST

(5 days after rehydration). However, the rehydrated plants

had higher ANet/E at 10 and 11 h (Fig. 3f) and higher

ANet/Ci at 11 and 14 h (Fig. 3e) compared to the irrigated

plants.

A. emarginata subjected to water deficit showed lower

gS and E during the day compared to irrigated and

rehydrated plants (Fig. 3b, c). The ANet, ANet/Ci and ANet/

E parameters of the suspension of irrigation treatment

were not presented because they are negative, indicating

that at 43 DAST this treatment was under a severe water

deficit.

The air temperature, relative humidity, VPD and PPFD

during the evaluations of gas exchange over the hours of

43rd DAST are in the Fig. 4a–d.

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Correlation between gas exchange parameters

At 43 DAST, significant correlations were observed

between the gas exchange parameters of the rehydration

treatment at 9, 10, 11, and 12 h (Table 1). Positive corre-

lations were observed between ANet and ANet/Ci at 9 and

12 h, between ANet and gS at 10 and 11 h, between ANet and

E at 10 h and between gS and E at 10, 11, and 12 h

(Table 1). Negative correlations were found between Ci

and ANet/Ci at 9 h, between ANet and ANet/E at 11 h,

between gS and ANet/E at 10, 11 and 12 h and between

E and ANet/E at 10 and 11 h (Table 1).

Chlorophyll a fluorescence

At 44 DAST, two-way ANOVA indicated no interaction

between treatments and PPFD for P, D, E and /exc

(Table 2), demonstrating that the light intensity did not

influence the treatments.

Comparing the treatments, it was observed reduction on

the capture of light energy (/exc) and use of light energy

(P) in plants subjected to rehydration. However, in this

same treatment there was no damage to the PSII, as

observed by the low dissipation of energy excess not uti-

lized by photochemical (E) and by the high dissipation of

the light energy as heat (D) (Table 2). Comparing the

different PPFD levels, it was observed an increase of D and

E and reduction of P and /exc with increase of light

intensity (Table 2).

Discussion

The cellular volume is determinant to the metabolic

activity on the leaf (Sinclair and Ludlow 1985). According

to Sinclair and Ludlow (1985), the relative water content in

Fig. 1 The substrate water content (SWC; %) (n = 4) of the

irrigation (black circle) and the suspension of irrigation treatment

followed by rehydration (white circle) (a). Relative water content in

the leaf (RWC; %) (n = 4) of the suspension of irrigation (gray bars)

and the rehydration treatment (white bar) (b). Vertical lines indicate

the standard deviation

Fig. 2 Monitoring of the gas exchange of the irrigation (black circle)

and the suspension of irrigation treatments (white circle) (n = 4).

CO2 assimilation rate (ANet; lmol CO2 m-2 s-1) (a) and stomatal

conductance (gS; mol H2O m-2 s-1) (b). Vertical lines indicate the

standard deviation

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the leaf (RWC) of plants under water deficit tends to have

values below 80 %. However, even with reduction on

substrate water content (SWC) (Fig. 1a), the RWC of the

suspension of irrigation treatment did not change until 24

DAST (days after the start of the treatment) (Fig. 1b). The

reduction observed in the stomatal conductance (gS) at 12

Fig. 3 The gas exchange of A. emarginata evaluated at 43 DAST at

9, 10, 11, 12, 14 and 16 h in the irrigation (black circle), rehydration

(white circle) and suspension of irrigation treatments (white square)

(n = 4). CO2 assimilation rate (ANet; lmol CO2 m-2 s-1) (a),

stomatal conductance (gS; mol H2O m-2 s-1) (b), transpiration rate

(E; mmol H2O m-2 s-1) (c), internal CO2 concentration in the sub-

stomatal chamber (Ci; lmol CO2 mol-1 ar) (d), water use efficiency

(ANet/E) (lmol CO2 mmol H2O-1) (e) and carboxylation efficiency

(ANet/Ci) (F). The different letters indicate significant differences

(Tukey’s test, P\ 0.05) between the treatments. The vertical lines

indicate the standard deviation

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DAST in the plants with suspension of irrigation (Fig. 1b)

may have influenced the maintenance of RWC and cell

turgor pressure (Lawlor and Tezara 2009), because 90 % of

a plant’s water loss is through stomatal transpiration (Wan

et al. 2009).

According to Bartlett et al. (2014), the relative water

content at the turgor loss point (RWCtlp), which is analogous

to the water potential at the turgor loss point (ptlp), is the point

of the occurrence of wilting on leaves in conjunction with the

disruption of growth and gas exchange. In A. emarginata

subjected to suspension of irrigation treatment, the RWCtlp

may have been reached at 38 DAST when the CO2 assimi-

lation rate (ANet) was negative and the leaves presented

visual wilting with 73 % of RWC. Any value below the point

of turgor loss indicates that there is not enough water

absorption by the plant to recover it from wilting (Lenz et al.

2006; Blackman et al. 2010; Bartlett et al. 2012). In many

species, photosynthesis becomes irreversibly reduced when

the RWC falls from approximately 70–60 % (Lawlor and

Cornic 2002). Even with an RWC of 73 % presented by A.

emarginata subjected to the water deficit (Fig. 1b), the

rehydration treatment showed partial recovery in gas

exchange compared with irrigated plants at 43 DAST

(5 days after rehydration) (Fig. 3a–f).

The rehydration treatment had lower values of gS and

transpiration rate (E) at 9, 10, 11, and 12 h in relation to the

irrigated plants (Fig. 3b–c). Marron et al. (2002), Bogeat-

Triboulot et al. (2007) and Flexas et al. (2009) also

observed slow recovery of the stomatal opening after

rehydration. Positive correlations were found between gS
and E at 10, 11, and 12 h of the rehydration treatment

(Table 1), which indicate that in these hours, the loss of

water was limited by the stomata. A similar correlation was

observed in Jatropha curcas L. under water deficit,

demonstrating the influence of the stomatal closure to

water control (Santos et al. 2013). Endres (2007) found

reduction of gS in Annona squamosa L. irrigated under

conditions of high vapor pressure deficit of the air (VPD),

which is similar to our study for irrigated plants (Figs. 3b,

4c). The same author also suggests that the high VPD has a

Fig. 4 The mean of air temperature (�C) (a), relative humidity (%) (b), vapor pressure deficit (VPD, kPa) (c) and photosynthetic photon flux

density (PPFD, lmol m-2 s-1) (d) for the hours of the 43rd DAST

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detrimental effect on the stomatal opening in Annonaceae

regardless of the plant hydration. However, in A. emargi-

nata submitted to rehydration, there was no significant

correlation between gS and VPD (Table 1).

The ANet of the rehydration treatment was partially

recovered in relation to the irrigated plants at 9 and 10 h

(Fig. 3a). Generally, plants subjected to severe water def-

icit only recover 40–60 % of the maximum photosynthetic

rate on the day after rehydration, and continue to recover

on the following days (Sofo et al. 2004; Bogeat-Triboulot

et al. 2007; Chaves et al. 2009). The ANet can be limited by

stomatal factors, such as increase of stomatal resistance to

CO2 entry, or by non-stomatal factors, such as decrease of

rubisco activity and photochemical efficiency of PSII

(Silva and Arrabaca 2004; Flexas et al. 2006; Xu et al.

2009).

Table 1 Pearson correlation (P\ 0.05) (n = 4) between the gas exchange parameters of the rehydration treatment evaluated at 43 DAST at 9,

10, 11 and 12 h

9 h GS E Ci ANet/E ANet/Ci VPD Temp air

ANet 0.80 0.01 -0.93 0.42 0.99** -0.83 -0.81

gS 0.41 -0.54 -0.05 0.73 -0.74 -0.67

E 0.16 -0.90 -0.05 0.30 0.40

Ci -0.56 -0.96* 0.68 0.70

ANet/E 0.48 -0.61 -0.70

ANet/Ci -0.80 -0.80

VPD 0.99**

10 h gS E Ci ANet/E ANet/Ci VPD Temp air

ANet 0.99** 0.99** 0.36 -0.99** 0.67 -0.12 0.33

gS 0.98* 0.47 -0.97* 0.57 -0.19 0.28

E 0.38 -0.98* 0.65 -0.02 0.43

Ci -0.26 -0.45 -0.23 0.07

ANet/E -0.74 0.10 -0.33

ANet/Ci 0.12 0.31

VPD 0.89

11 h gS E Ci ANet/E ANet/Ci VPD Temp air

ANet 0.96* 0.94 -0.45 -0.88 0.90 0.30 0.73

gS 0.99** -0.21 -0.96* 0.75 0.53 0.84

E -0.15 -0.96* 0.70 0.59 0.87

Ci 0.19 -0.79 0.71 0.28

ANet/E -0.67 -0.53 -0.74

ANet/Ci -0.15 0.37

VPD 0.84

12 h gS E Ci ANet/E ANet/Ci VPD Temp air

ANet 0.38 0.42 0.25 -0.11 0.98* -0.03 0.75

gS 0.99** 0.89 -0.95* 0.23 -0.85 -0.23

E 0.90 -0.94 0.27 -0.83 -0.19

Ci -0.83 0.07 -0.61 -0.14

ANet/E 0.04 0.95 0.51

ANet/Ci 0.08 0.79

VPD 0.64

The CO2 assimilation rate (ANet; lmol CO2 m-2 s-1), stomatal conductance (gS; mol H2O m-2 s-1), transpiration rate (E; mmol H2O m-2 s-1),

internal CO2 concentration in the sub-stomatal chamber (Ci; lmol CO2 mol-1 ar), water use efficiency (ANet/E) (lmol CO2 mmol H2O-1),

carboxylation efficiency (ANet/Ci), vapor pressure deficit (VPD; kPa) and air temperature (Temp air;. �C)

* Indicates significant correlation at P\ 0.05

** Indicates significant correlation at P\ 0.01

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Changes on the patterns of stomatal conductance and

carbon concentration inside the mesophyll can provide

information regarding to the causes of limitation on the

photosynthetic rate (Farquhar and Sharkey 1982; Mielke

et al. 2003; Herrera et al. 2008). The carboxylation effi-

ciency (ANet/Ci) also permits differentiation between

stomatal and non-stomatal limitations (Ennahli and Earl

2005). Under rehydration, A. emarginata showed partial

recovery of ANet/Ci at 9 h compared to irrigated plants

(Fig. 3e). At this same time, the rehydrated plants showed a

positive correlation between ANet and ANet/Ci and a nega-

tive correlation between ANet/Ci and internal CO2 con-

centration in the sub-stomatal chamber (Ci) (Table 1).

These correlations indicate that the increase in ANet is

dependent on the increase in ANet/Ci, and the increase in

ANet/Ci is not dependent on the increase of Ci. Therefore, it

is possible that at 9 h there is a predominance of non-

stomatal limitation of ANet in A. emarginata submitted to

rehydration. In J. curcas under water deficit conditions,

Santos et al. (2013) observed a negative correlation

between ANet and Ci, which suggests that ANet was not

limited by CO2 input.

At 10 h, there was a positive correlation between ANet

and gS in the rehydration treatment (Table 1), which indi-

cate that ANet was influenced by the gS. The high correla-

tion between these parameters demonstrates strong

stomatal control over the rate of photosynthesis (Costa

França et al. 2000; Tesfaye et al. 2008; Ninou et al. 2013).

In addition, at 10 h, rehydrated plants showed less Ci and

no difference on ANet/Ci in relation to the irrigated plants

(Fig. 3d–e). Thus, it is possible that, at this time, the

rehydration treatment presents a predominance of stomatal

limitation of ANet.

Although the lower gS limits the photosynthetic recov-

ery, the water use efficiency (ANet/E) may increase (Bo-

geat-Triboulot et al. 2007; Gallé et al. 2007; Galmés et al.

2007) due to a reduction on E (Roelfsema and Hedrich

2005; Nilson and Assmann 2007). In A. emarginata, the

ANet/E of the rehydration treatment was higher compared to

the irrigation treatment at 10 and 11 h (Fig. 3f). At both

time points, negative correlations were observed between

ANet/E and gS and between ANet/E and E, which indicate

that gS and E have an inverse relationship with ANet/

E (Table 1).

Interestingly, there was a negative correlation between

ANet/E and ANet at 10 h (Table 1), which demonstrates that

with an increase of ANet, the ANet/E reduces. This fact may

be related to the positive correlation found on the same

time between ANet and E (Table 1), where the increase of

ANet leads to increases E. This correlation may suggest that

in A. emarginata, E and ANet are regulated during rehy-

dration to maintain high water use efficiency without major

losses on the photosynthetic rate. After rehydration,

Quercus pubescens Willd. (Miyashita et al. 2005) and

Phaseolus vulgaris L. (Galle et al. 2007) present the ANet

recovery faster than the recovery of gS, resulting on an

increase of instantaneous water use efficiency. It is possible

that during the water deficit, plants may present adjust-

ments to avoid water loss. During rehydration, these

adjustments could help to mitigate the effect of future

deficit events (Gallé et al. 2007).

At 44 DAST, the chlorophyll fluorescence in rehydrated

plants has lower efficiency of excitation energy captured by

open PSII (/exc) and P (photochemical) in relation to

irrigated plants (Table 2), which indicate reduction on both

capture of energy and use of energy for the photochemical

Table 2 Mean values (n = 4)

of the fraction of light absorbed

by PSII antenna used in the

photochemical electron

transport (P), of the fraction of

light absorbed by PSII antenna

that is dissipated as heat (D), of

the fraction of excitation energy

not dissipated in the antenna

that cannot be utilized for

photochemistry (E) and of the

efficiency of excitation energy

captured by open PSII reaction

centers (/exc) of the irrigation

and rehydration treatments at 44

DAST in 125, 190, 285, 420,

625, 820, 1150, and

1500 lmol m-2 s-1 of PPFD

Treatment P D E /exc

Irrigation 0.132 a 0.577 b 0.292 a 0.423 a

Rehydration 0.121 b 0.624 a 0.255 b 0.376 b

PPFD

125 0.192 a 0.506 c 0.303 a 0.494 a

190 0.175 ab 0.557 bc 0.268 a 0.443 ab

285 0.162 bc 0.587 ab 0.250 a 0.413 bc

420 0.141 c 0.607 ab 0.252 a 0.393 bc

625 0.106 d 0.624 ab 0.269 a 0.376 bc

820 0.094 de 0.633 a 0.273 a 0.367 c

1150 0.075 e 0.640 a 0.285 a 0.360 c

1500 0.066 e 0.646 a 0.287 a 0.354 c

Significance

Treatment P\ 0.05 P\ 0.001 P\ 0.01 P\ 0.001

PPFD P\ 0.001 P\ 0.001 ns P\ 0.001

Treatment 9 PPFD ns ns ns ns

Different letters indicate significant differences in Tukey’s test (P\ 0.05)

157 Page 8 of 11 Acta Physiol Plant (2016) 38:157

123



process, respectively. However, this reduction did not

represent damage on the photochemical process, because

rehydrated plants had low values of E (energy not used in

photochemical step). The accumulation of this energy

excess can result in the formation of the triplet state of

chlorophyll, which leads to the formation of singlet oxygen

(1O2) that causes damage to PSII (Demmig-Adams et al.

1996; Kato et al. 2003). Therefore, the reduction of

E indicates the absence of damage to PSII. Mantoan et al.

(2015) also did not observe damage to the PSII of A.

emarginata subjected to a water deficit followed by

rehydration.

According to Demmig-Adams et al. (1996), the sum of

the parameters P, D and E is one. Therefore, any reduction

in one of those parameters results on the increase of the

others. Thus, during rehydration, the increase of the dissi-

pation of the excitation energy as heat (D), which is

modulated by photoprotection mechanisms (xanthophyll

cycle) (Demmig-Adams et al. 1996; Kato et al. 2003), is

due to the reduction in the photochemical dissipation

(P) and in the dissipation of energy excess (E). According

to Baker and Rosenqvist (2004), plants tend to avoid

damage to the PSII, reducing the energy for photochemical

step (P) and increasing the dissipation of this energy as

heat. Therefore, the occurrence of high D after 6 days of

rehydration indicates the maintenance of photoprotection,

which represents a possible photochemical acclimation to

water deficit in A. emarginata.

Conclusion

After rehydration, A. emarginata shows balance between

transpiration and CO2 assimilation rate to optimize the water

use efficiency. Also, in the photochemical process, the

rehydrated plants maintain high activity of photoprotection.

Thus, A. emarginata presents adjustments on gas exchange

and photochemical process, resulting in a possible long-term

photosynthetic acclimation to the water deficit.

Author contribution statement Luı́s Paulo Benetti

Mantoan conducted the experiment, performed the

chlorophyll a fluorescence measurements, analyzed the

data and wrote the manuscript. Ana Claudia Macedo per-

formed the gas exchange measurements. Luiz Fernando

Rolim de Almeida, Gisela Ferreira and Carmen Silvia

Fernandes Boaro helped to review and edit this manuscript.

Acknowledgments We would like to thank the postgraduate pro-

gram in Biological Sciences (Botany), the Universidade Estadual

Paulista ‘‘Júlio de Mesquita Filho’’ UNESP, the Institute of Bio-

sciences, Department of Botany, Botucatu—SP Brazil and the Con-

selho Nacional de Desenvolvimento Cientı́fico e Tecnológico—CNPq

for the granted scholarships.

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	Photosynthetic adjustment after rehydration in Annona emarginata
	Abstract
	Introduction
	Materials and methods
	Plant material and experimental design
	Control of irrigation
	Relative water content in the leaves
	Gas exchange
	Chlorophyll a fluorescence
	Statistical analysis

	Results
	Monitoring the water deficit
	Gas exchange throughout the day
	Correlation between gas exchange parameters
	Chlorophyll a fluorescence

	Discussion
	Conclusion
	Acknowledgments
	References