The use of grafting to improve the net photosynthesisof cucumber

Amanda Cristina Esteves Amaro • Ana Claudia Macedo •

Anamaria Ribeiro Pereira Ramos • Rumy Goto •

Elizabeth Orika Ono • Joao Domingos Rodrigues

Received: 24 April 2014 / Accepted: 6 November 2014

� Brazilian Society of Plant Physiology 2014

Abstract Grafting induces significant changes in the

growth and development of plants. Additionally,

photosynthesis is directly proportional to light, and

the stomatal aperture decreases with decreases in

irradiance. The present study aimed to evaluate daily

gas exchange rates and the response curve of the CO2

assimilation rate as a function of photosynthetic

photon flux density in grafted and non-grafted Japa-

nese cucumber plants with the objective of studying

the underlying physiology. Two similar experiments

were conducted in 2009 and 2010. The Japanese

cucumber hybrid ‘Taisho’ was grafted on the pumpkin

hybrid ‘Excitte Ikki’ using the tongue approach

method. The results indicated that grafting affected

photosynthetic metabolism. As a result of this meta-

bolic change, the grafted plants had a higher net CO2

assimilation rate, a lower maximum quantum yield of

photosynthesis and a higher transpiration rate than the

non-grafted plants. Furthermore, the non-grafted

plants appeared to be more sensitive to environmental

conditions, as they showed a higher water use

efficiency, indicating an improved water saving capa-

bility a lower saturation point of photosynthesis by

light than the grafted plants. This result suggests that

grafted plants tend to tolerate higher radiance levels

than non-grafted plants.

Keywords Cucumis sativus L. � Gas exchanges �Grafted plants � Light

1 Introduction

Grafting is a technique of vegetative propagation,

which involves the union of two parts of plants through

the tissue regeneration, so that the assembly constitutes

a new plant. As a result of this union occur several

physical, biochemical and physiological events, start-

ing with the new vascular connections and ending in

effects on plant growth and development. Plant growth

A. C. E. Amaro (&) � A. C. Macedo � A.

R. P. Ramos � R. Goto

Departamento de Horticultura, Faculdade de Ciencias

Agronomicas, Universidade Estadual Paulista (UNESP),

Campus de Botucatu, CP-237, Botucatu, SP 18603-970,

Brazil

e-mail: amandaamaro@uol.com.br

A. C. Macedo

e-mail: anamacedo85@gmail.com

A. R. P. Ramos

e-mail: anamaria-ramos@oi.com.br

R. Goto

e-mail: rumy@fca.unesp.br

E. O. Ono � J. D. Rodrigues

Departamento de Botanica, Instituto de Biociencias,

Universidade Estadual Paulista (UNESP), Campus de

Botucatu, CP-510, Botucatu, SP 18618-970, Brazil

e-mail: eoono@ibb.unesp.br

J. D. Rodrigues

e-mail: mingo@ibb.unesp.br

123

Theor. Exp. Plant Physiol.

DOI 10.1007/s40626-014-0023-1

can be influenced by several factors as nutritional

status, environmental conditions and hormonal activ-

ity, which are related to various physiological pro-

cesses (Bautista et al. 2011; Martınez-Ballesta et al.

2010).

Thus grafting improves nutrient absorption,

increases plant strength and increases resistance to

abiotic stress such as low temperatures, drought and

salinity, as well as increasing tolerance to heavy

metals and organic pollutants, thus controlling phys-

iological disorders and improving fruit quality. More-

over, the fruit of cucumber grafted plants lose their

wax layer and are brighter and straighter, improving

fruit quality. These effects enhance the consumer

market value of the fruit. All these factors result in

higher production and increase the harvest period

(Davis et al. 2008; He et al. 2009; Rouphael et al.

2010; Schwarz et al. 2010).

Furthermore, gas exchange in grafted plants are

directly modified by rootstock, because this can

change the vigor and productivity of the scion (Colla

et al. 2012). For example, grafting affects the plant

water relations, whereas sufficient vascular connec-

tion between the rootstock and scion, increases the

flow of nutrients and water, allowing an increase in

photosynthesis (Martınez-Ballesta et al. 2010; Salehi

et al. 2010). Several authors reported that the grafting

improve net CO2 assimilation rate, stomatal conduc-

tance and transpiration, resulting in higher growth and

yield (Yang et al. 2006; He et al. 2009; Salehi et al.

2010; Liu et al. 2011). Because all biomass production

depends on the photosynthetic activity, agricultural

practice aims to maximize the photosynthetic effi-

ciency of the crop and improve the final crop yield in

terms of productivity and quality.

The present work aimed to evaluate the response

curve of the daily gas exchange and the CO2 assim-

ilation rates as a function of photosynthetic photon

flux density (PPFD) in grafted and non-grafted

Japanese cucumber plants (Cucumis sativus L.) under

greenhouse conditions.

2 Materials and methods

The experimental area was located at the Faculdade de

Ciencias Agronomicas (FCA), Universidade Estadual

Paulista (UNESP), located in Sao Manuel city, Sao

Paulo state, Brazil. The study site is located at 22�440S

latitude, 47�340W longitude, and altitude of

750 meters. The climate is mesothermal humid sub-

tropical according to Peel et al. (2007). We used an arc

type greenhouse with the following characteristics:

30 m length, 7 m width and 3 m height, covered with

low-density polyethylene film (150 lm), with the

lateral sides covered with a 75 % shade cloth.

Two similar experiments with grafted and non-

grafted cucumber plants were set up, both in the

second semester (spring-summer), being the first

experiment in 2009 and the second in 2010. The

Japanese cucumber hybrid ‘Taisho’ (scion) was

grafted with the pumpkin hybrid ‘Excitte Ikki’ (root-

stock) using the tongue approach grafting method

(Peil 2003). To ensure that both hypocotyl diameters

were similar, allowing proper grafting at the time of

grafting, pumpkin was sown 4 days before sowing the

cucumber. The grafting was performed 10 days after

sowing the cucumber, and the plants were transplanted

to pots 4 days after grafting. Thereafter, the seedlings

were kept in a moist chamber until they were suitable

for transplantation.

A spacing of 1.0 9 0.5 m was used between

seedlings. The seedlings were conducted with one

stem oriented vertically to avoid damage that could

harm fruit production or fruit quality. We removed all

shoots and eliminated all buds and flowers from the 1st

node through the 5th node, leaving the side branches

growing from the 6th node; the side branches were

topped and tailed after the 3rd internode. The exper-

imental design was completely randomized.

Gas exchange was measured with an infrared CO2

and water vapor analyzer (LI-6400, Li-Cor Inc.,

Lincoln NE, USA). Daily gas exchange was measured

in 12 grafted plants and 12 non-grafted plants, which

were selected and standardized: the second fully

expanded leaves at 42 days after transplanting in the

first experiment and at 70 days after transplanting in

the second experiment. The measurements were

performed every hour from 8:00 am until 10:00 am,

aiming to study gas exchange in the early morning,

and then every 2 h until 6:00 pm. The difference in the

number of days after transplanting to perform the

evaluations, between experiments, was due to the

colder temperatures occurring during 2010, when the

plants took longer to develop. However, the plants

were in the same phenological stage when gas

exchange was measured. The net assimilation rate

(A, lmol CO2 m-2 s-1), transpiration (E, mol H2O

Theor. Exp. Plant Physiol.

123

m-2 s-1) and stomatal conductance (gs, mol H2O m-2

s-1) were evaluated. The water use efficiency (WUE,

lmol CO2 (mol H2O)-1) was determined by the

relationship between net assimilation rate and tran-

spiration (A/E), and the apparent carboxylation effi-

ciency (A/Ci) was determined by the relationship

between the CO2 assimilation rate and the intercellular

CO2 concentration (Ci, lmol CO2 mol air-1). Air

temperature and relative humidity, expressed in

degrees Celsius (�C) and percentage (%), respectively,

were reported (Table 1).

To ensure that the experimental conditions were

consistent, the PPFD was standardized through the use

of a light-emitting diode coupled to the photosynthesis

chamber, accordingly the PPFD during each experi-

mental period (Table 1). The reference CO2 concen-

tration used during the evaluation was the ambient

value, ranging from 380–400 lmol mol-1 of air.

The response curve of the CO2 assimilation rate (A,

lmol CO2 m-2 s-1) as a response to PPFD was

obtained by decreasing the PPFD from 2,000 to

0 lmol m-2 s-1, at intervals of 300 lmol m-2 s-1,

until 100 lmol m-2 s-1, and thereafter at intervals of

50 lmol m-2 s-1, for greater accuracy of the slope of

the curve. The temperature used during the evaluation

was the ambient value, ranging from 30 ± 3 �C. We

used four grafted and four non-grafted plants for the

measurements, selected and standardized using the

second fully expanded leaf at 42 days after transplan-

tation in the first experiment.

The response curve was adjusted to the hyperbolic

function A = a ? [(Amax 9 PPFD)/(b ? PPFD)], where

Amax is the maximum net CO2 assimilation rate and a and

b are the parameters of the hyperbolic equation. This

function allows us to calculate the respiration in the dark

(parameter a of the equation) and at the light compensation

point (s, corresponding to the value of PPFD where A is

zero). The saturation point of the light was determined by

fitting a straight line (y = 1) to the higher points of the

curve. The hyperbolic function was fitted with the SAS

9.2 statistical program. The data were subjected to an

analysis of variance (F test), and the means were compared

by Tukey’s test with a 5 % probability and a regression

analysis. To determine the homogeneity of the treatment

variances, the SAS 9.2 statistical software was used to

perform Levene’s test.

3 Results

The grafted plants had a higher net assimilation rate of

CO2 than the non-grafted plants in both 2009 and 2010

(Fig. 1). In 2009, this distinction was observed

between 10:00 am and 4:00 pm, reaching the maxi-

mum at 10:00 am. Equal numbers of grafted and non-

grafted plants assimilated higher levels of CO2 in the

morning (between 10:00 am and 12:00 am). In 2010

(Fig. 1), this behavior was less evident; there was still

a difference between the grafted and the non-grafted

plants, but it was smaller. The smaller difference in

2010 may have been due to low relative humidity

(Table 1), as the relative humidity decreased from 20

to 12 % from 10:00 am until 12:00 am and caused a

partial closing of the stomata. The rates of CO2

assimilation were higher at 10:00 am in both types of

plants. These results agree with those obtained for

stomatal conductance (Fig. 1) in both 2009 and 2010,

with an evident higher stomatal conductance in the

grafted plants. The stomatal conductance, as well as

the rate of net CO2 assimilation, were lower in the

2010 experiment possibly due to the influence of the

low relative humidity (Table 1).

In relation to the stomatal conductance, the non-

grafted plants showed a decrease in the stomatal

conductance at 12:00 am (Fig. 1—2009 experiment),

when the temperature began to rise and the relative

humidity began to decline (Table 1). However, the

stomatal conductance of the grafted plants began to

decrease after 2:00 pm, when the environmental

Table 1 Photosynthetic photon flux density (PPFD,

lmol m-2 s-1), air temperature (�C) and relative humidity of

the air (%) for 2 different years (2009 and 2010), from 8:00 am

to 6:00 pm under greenhouse conditions. FCA/UNESP, Sao

Manuel-SP, Brazil

Day time PPFD

(lmol m-2

s-1)

Air

temperature

(�C)

Relative

humidity (%)

2009 2010 2009 2010 2009 2010

8:00 am 400 500 29.37 34.92 23.84 39.17

9:00 am 700 800 30.63 37.74 22.02 32.14

10:00 am 1,000 1,100 32.38 39.96 20.38 28.69

12:00 am 1,700 1,400 35.90 39.15 12.53 29.94

2:00 pm 1,200 1,300 36.34 42.21 11.46 24.30

4:00 pm 1,000 900 34.34 38.91 14.73 30.55

6:00 pm 400 300 31.60 34.79 15.03 35.28

Theor. Exp. Plant Physiol.

123

conditions became more extreme (i.e., a higher

temperature and a lower relative humidity); the

strategy of partially closing the stomata is usually

adopted by plants to prevent the loss of large amounts

of water. These results suggest that the decrease in net

CO2 assimilation rates after 12:00 am is related to the

partial closure of the stomata. In the 2010 experiment,

the non-grafted plants exhibited generally constant

stomatal conductance throughout the day, most likely

due to more adequate meteorological conditions

during this experiment. These conditions resulted in

a smaller stomatal aperture than in the 2009 experi-

ment for both types of plants.

In the 2009 experiment, even though higher tran-

spiration rates were observed in both types of plants,

we verified that the transpiration rate was higher in the

grafted plants (peak at 12:00 am, Fig. 2), indicating

more water loss, consistent with the relatively large

stomatal opening, and high net CO2 assimilation rate.

In the 2010 experiment, however, the transpiration

Fig. 1 Net CO2 assimilation rate (A, lmol m-2 s-1) and

stomatal conductance (gs, mol m-2 s-1) of grafted and non-

grafted Japanese cucumber plants (Cucumis sativus L.) for 2

different years (2009 and 2010), from 8:00 am to 6:00 pm under

greenhouse conditions. Values are meant ± S.E. (n = 12).

FCA/UNESP, Sao Manuel-SP, Brazil

Theor. Exp. Plant Physiol.

123

rates of the grafted plants remained higher than those

of the non-grafted plants through most of the day (8:00

am to 4:00 pm), with a peak at 12:00 am for both types

of plants. This increase in transpiration rate is most

likely connected to the increase in temperature and the

decrease in relative humidity as well as the higher

PPFD and stomatal opening.

The water use efficiency (Fig. 2) was similar

between the grafted and the non-grafted plants

throughout the day in the 2009 experiment, except at

6:00 pm, when the non-grafted plants were more

efficient than the grafted plants. However, this pattern

was not observed in 2010. Once again, we attribute

this difference as a result of the relative humidity in the

two experiments, as the relative humidity in the 2010

experiment was 15 %, approximately half of the 2009

value of 35 %.

The leaf temperature (Fig. 3) for both types of

plants in both experiments was similar and followed

the air temperature. The calculated apparent carbox-

ylation efficiency (A/Ci) for 2009 (Fig. 3) was more

efficient in the grafted plants, with higher values

Fig. 2 Transpiration (E, mol H2O m-2 s-1) and water use

efficiency (A/E, lmol CO2 (mol H2O)-1) in grafted and non-

grafted Japanese cucumber plants (Cucumis sativus L.) for 2

different years (2009 and 2010), from 8:00 am to 6:00 pm under

greenhouse conditions. Values are meant ± S.E. (n = 12).

FCA/UNESP, Sao Manuel-SP, Brazil

Theor. Exp. Plant Physiol.

123

observed between 10:00 am and 2:00 pm. These

results are consistent with those obtained for the net

CO2 assimilation rate. In 2010, the grafted plants

continued to be more efficient than the non-grafted

plants, however, this difference was smaller due to the

environmental conditions, resulting in lower stomatal

conductance and lower CO2 assimilation.

In addition, the presence of grafting changed the

light-response curves (Fig. 4; Table 2). The light

compensation point (s) did not differ statistically

between grafted and non-grafted plants (38.83 and

33.06, respectively), and such a result indicates that

these plants need similar photosynthetic photons to

assimilate the same amount of CO2. Although

exchanges of CO2 may not occur, the absorption of

CO2 will follow the increase in radiation linearly until

it reaches the saturation point if the stomata are open

and no other environmental factors are limiting the gas

exchange after the light compensation point. The

maximum quantum yield of photosynthesis for the

Fig. 3 Leaf temperature (�C) and carboxylation efficiency (A/

Ci) in grafted and non-grafted Japanese cucumber plants

(Cucumis sativus L.) for 2 different years (2009 and 2010),

from 8:00 am to 6:00 pm under greenhouse conditions. Values

are mean ± S.E. (n = 12). FCA/UNESP, Sao Manuel-SP,

Brazil

Theor. Exp. Plant Physiol.

123

leaves is indicated in this portion of the curve by its

slope; and was higher in the non-grafted plants than in

the grafted plants (0.03620 and 0.02692 lmol CO2-

lmol photons-1, respectively), suggesting that graft-

ing decrease the Calvin cycle efficiency in terms of the

utilization of ATP and NADPH. In general, the grafted

plants assimilated more CO2 than the non-grafted

plants and reached a different saturation plateau. The

non-grafted plants showed a tendency for photosyn-

thesis saturation at PPFD values above

1,218 lmol m-2 s-1, whereas the saturation plateau

occurred at 1,502 lmol m-2 s-1 for the grafted plants.

4 Discussion

The analysis of the daily gas exchange rates demon-

strated that the grafted plants had a higher net CO2

assimilation rate, as well as a higher transpiration rate,

than the non-grafted plants, whereas the non-grafted

these appear to be more sensitive to environmental

conditions because they decreased stomatal conduc-

tance as a result of an increase in temperature and a

decrease in relative humidity.

These results are similar to those found in musk-

melon and tomato plants, which have been shown to

increase their net CO2 assimilation rate, stomatal

conductance and transpiration rate with grafting (He

et al. 2009; Salehi et al. 2010; Liu et al. 2011).

Moreover, grafted muskmelon plants enhanced the

translocation of carbohydrates by increasing acid

invertase and neutral invertase activity as the chloro-

phyll content and leaf area also increased markedly

(Liu et al. 2011). The improvement in CO2 assimila-

tion may result in enhancements of growth potential,

dry matter accumulation, yields and perhaps fruit

quality.

Most studies of grafting suggest that changes in the

scion are controlled by the rootstock through controlled

Fig. 4 Net CO2

assimilation rate (A,

lmol m-2 s-1) as a function

of photosynthetic photon

flux density (PPFD,

lmol m-2 s-1) in grafted

and non-grafted Japanese

cucumber plants (Cucumis

sativus L.). FCA/UNESP,

Sao Manuel-SP, Brazil

Table 2 Light compensation point (s, lmol m-2 s-1), light

saturation point (lmol m-2 s-1) and maximum quantum yield

of photosynthesis (lmol CO2�lmol photons-1), in grafted and

non-grafted Japanese cucumber plants (Cucumis sativus L.).

FCA/UNESP, Sao Manuel-SP, Brazil

Light

compensation

point

Light

saturation

point

Maximum

quantum yield of

photosynthesis

Non-grafted 33.06a 1,217.84b 0.03620a

Grafted 55.60a 1,502.54a 0.02692b

Valor de F 1.21 ns 12.33* 7.93*

C.V. (%) 20.68 8.43 14.76

The means followed by the same letter do not differ

significantly by Tukey’s test at a 5 % probability

ns not significant (P C 0.05)

* Significant at 5 % probability (P \ 0.05)

Theor. Exp. Plant Physiol.

123

uptake, synthesis, and translocation of water, minerals,

and plant hormones (Martınez-Ballesta et al. 2010).

One possible explanation of this process in the context

of the present study is that the rootstock roots are more

vigorous than the cucumber (scion), and this vigor may

increase the sink strength of the plant due to an increase

in rootstock growth (Zhou et al. 2009). Moreover, water

and nutrient uptake could be increased in grafted plants

as a result of the enhancement of root vigor (Lee et al.

2010; Martınez-Ballesta et al. 2010). Thus, the

increased availability of water in the plant causes the

water flow to increase, keeping the stomata open longer

even during the hottest hours of the day and ultimately

providing higher rates of transpiration and CO2

assimilation.

The root-scion combination may alter the amount

of plant hormones produced and their influence on the

organs of the grafted plant. Thus, this difference in net

CO2 assimilation rates between the grafted and the

non-grafted plants can be explained by factors such as

an increase in the concentration of cytokinins (Zhou

et al. 2007). Cytokinins are involved in the accumu-

lation and synthesis of chlorophyll as well as in the

decrease in the abscisic acid (ABA) concentration in

the xylem of grafted plants, resulting in an increase in

the activity and content of ribulose-1,5-bisphosphate

carboxylase-oxygenase (Rubisco), and protection of

the photosynthetic apparatus (Zhou et al. 2009). If, the

composition of cytokinins in the xylem sap is altered

in a relatively short time in the scion (Lee et al. 2010),

it is possible that this change may have occurred in the

grafting of cucumber on pumpkin, thus explaining the

increase in the rate of CO2 assimilation and the rate of

translocation of photoassimilates.

Another possibility is that the rootstocks (pumpkin)

of the grafted plants are more vigorous than those of the

cucumber, leading to increased water uptake and an

increase in K? ions in the shoot (Rouphael et al. 2008).

This greater availability of water increases the water

flow in the xylem, as K? ions are responsible for several

of the changes in guard cell turgor during stomatal

movement. As a result, the stomatal opening is wider. In

addition, K? ions are cofactors for enzymes involved in

respiration and photosynthesis (Maathuis 2009). Due to

its strong influence on stomatal movement, this

increased stomatal opening produced higher CO2

assimilation and transpiration rates.

The light-response curves determined in this study

showed that the maximum quantum yield of

photosynthesis for the leaves was higher in the non-

grafted plants than in the grafted plants. Suggesting

that grafting decrease the Calvin cycle efficiency, in

terms of the utilization of ATP and NADPH, probably

due to the stress caused by grafting. This portion of the

curve is limited by the rate of electron transport and by

RuBP regeneration (Jones 1998).

Nevertheless, as demonstrated by daily gas

exchange rates, the grafted plants assimilated more

CO2 than the non-grafted plants, and the non-grafted

plants showed a tendency for photosynthesis satura-

tion at lower PPFD values than the grafted plants.

Indicating that the grafted plants take better advantage

of incident radiation, taking longer to limit their net

CO2 assimilation rate by light; again demonstrating

that non-grafted plants are more sensitive to environ-

mental conditions.

Under intense radiation, there is not a significant

increase in photosynthesis in this situation, the pho-

tosynthesis is saturated by radiation, and the assimi-

lation rate of CO2 is no longer limited by

photochemical reactions (Habermann et al. 2003).

Thus, factors such as the electron transport reaction,

Rubisco activity or the metabolism of triose phos-

phates become more limiting in non-grafted plants.

Therefore, non-grafted plants showed a lower satura-

tion point of photosynthesis by light than those of the

grafted plants. This result suggests that grafted plants

tend to tolerate higher radiance levels than non-grafted

plants. Overall, the results of this study indicated that

grafting affected photosynthetic metabolism by means

of net CO2 assimilation rate improvement and

decrease of the maximum quantum yield of photo-

synthesis. Furthermore, the non-grafted plants

appeared to be more sensitive to environmental

conditions.

Acknowledgments The authors thank the Fundacao de

Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) for its

financial support of this study and to Prof.a Dr.a Martha Maria

Mischan (Universidade Estadual Paulista, Instituto de

Biociencias, Departamento de Bioestatıstica) for the

substantial help with the statistics.

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