Download Physiological aspects of rootstock–scion interactions

Scientia Horticulturae 127 (2010) 112–118
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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti
Review
Physiological aspects of rootstock–scion interactions
M. Carmen Martínez-Ballesta, Carlos Alcaraz-López, Beatriz Muries,
César Mota-Cadenas, Micaela Carvajal ∗
Department of Plant Nutrition. Centro de Edafología y Biología Aplicada del Segura (CEBAS-CSIC), Campus Universitario de Espinardo, Apdo. de Correos 4195, 30080 Murcia, Spain
a r t i c l e
i n f o
Article history:
Received 6 May 2010
Received in revised form 2 July 2010
Accepted 2 August 2010
Keywords:
Water uptake
Water transport
Plant nutrition
CO2 fixation
Growth
Grafting
a b s t r a c t
Due to the high market demand for off-season vegetables and the limited availability of arable land,
vegetable seedlings are cultivated under changing environmental conditions which may induce stress.
These conditions include cold, wet or dry environments, low or high radiation, etc. In addition, marginal
water quality successive cropping can increase salinity and the incidence of pests and soil-borne diseases.
Grafting is a horticultural technology, practiced for many years and in many parts of the world, in order
to overcome many of these problems. The use of grafted plants in vegetable crop production is still rare
compared to the use of grafting in tree crops. However, this technique is now being expanded greatly and
the use of rootstocks can enhance plant yield through vigorous attainment of soil nutrients, avoidance of
infection by soil pathogens and tolerance of low soil temperatures, salinity and wet-soil conditions.
This review focuses on the physiological and biochemical aspects of the rootstock–scion interaction for
both Solanaceae and Cucurbitaceae species, considering the mechanisms involved in graft compatibility,
nutrient and water uptake, assimilation and translocation of solutes and the influence of the rootstock
on the main physiological processes of the scion.
© 2010 Elsevier B.V. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Rootstock–scion interaction as a barrier to water flow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Nutrient uptake and translocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Plant growth and biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
The use of grafted vegetable seedlings has been popular in many
countries during recent years (Lee and Oda, 2003). The cultivated
area of grafted Solanaceae, including a number of important annual
fruit-crop plants such as tomato, eggplant and pepper, and Cucurbitaceae, such as melon, cucumber, watermelon and pumpkin, has
increased in recent years in order to obtain resistance to soil-borne
diseases (Ioannou, 2001; Bletsos et al., 2003; Davis et al., 2008) and
tolerance against abiotic stresses such as salinity, wet soils and high
and low temperatures (Abdelmageed and Gruda, 2009; Ahn et al.,
1999; Estañ et al., 2005; Venema et al., 2008; Rivero et al., 2003a,b),
∗ Corresponding author at: CEBAS-CSIC, P.O. Box 164, 30100 Espinardo, Murcia,
Spain. Tel.: +34 968 39 63 10; fax: +34 968 39 62 13.
E-mail address: [email protected] (M. Carvajal).
0304-4238/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.scienta.2010.08.002
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to enhance water and nutrient uptake and nutrient use efficiency
(Santa-Cruz et al., 2002), to extend the duration of harvest time (Lee,
1994) and to improve fruit quality (Colla et al., 2006; FernándezGarcía et al., 2004a,b). Grafted plants usually show increased uptake
of water and minerals compared with the self-rooted plants, as a
consequence of the vigorous root system used as rootstock.
During formation of the graft union, many researchers have
observed callus proliferation (from both the rootstock and the
scion), callus bridge formation, differentiation of new vascular
tissue from callus cells and the production of secondary xylem
and phloem (Hartmann et al., 1997). A low or incorrect callus
formation between the rootstock and scion could lead to defoliation, reduction of scion growth and low survival of grafted
plants (Oda et al., 2005; Johkan et al., 2009). Thus, the vascular
connection in the rootstock–scion interface may determine water
and nutrient translocation, affecting other physiological traits. In
addition, the influence of the rootstock on nutrient and water
M.C. Martínez-Ballesta et al. / Scientia Horticulturae 127 (2010) 112–118
uptake was attributed principally to physical characteristics, such
as lateral and vertical development of roots, or greater uptake
ability.
The practical and horticultural aspects of grafting technology
have been described in several reviews (Lee, 1994, 2003; Lee and
Oda, 2003), but less has been compiled about the physiological
implications of the rootstock–scion interaction as a barrier for
the translocation of water and nutrients, especially in non-woody
species, or the effect of the rootstock–scion connection on the
leaf area, morphology, growth, biomass and photosynthesis of the
grafted plant.
2. Rootstock–scion interaction as a barrier to water flow
Water and nutrient uptake could be increased in grafted plants
as a result of the enhancement of vigour by the rootstock root system and its effects on plant yield (Ruiz et al., 1997). Thus, water
relations in the rootstock–scion system, as well as the influence
of the graft union on water transport to the aerial parts, have been
studied with special emphasis on the search for plants able to withstand environmental changes.
Plants form callus at the graft interface, which enables water
to flow from the rootstock to the scion when the callus develops
vascular bundles (Moore, 1984a,b). Insufficient connection of vascular bundles between the scion and the rootstock decreases the
water flow (Torii et al., 1992). When water absorption by roots was
suppressed at the graft interface, stomatal conductance and scion
growth decreased (Atkinson and Else, 2001; Oda et al., 2005). Thus,
hydraulic architecture becomes of fundamental importance, since
the sustained flow of water controls many plant processes such as
growth, mineral nutrition, photosynthesis and transpiration.
The hydraulic barriers resulting from grafting have been analysed by histological techniques (Hartmann et al., 1997; Kawaguchi
et al., 2008) and by observation of the movement of dyes (Oda et
al., 2005; Aloni et al., 2008; Kawaguchi et al., 2008; FernándezGarcía et al., 2004a), but these approaches do not always distinguish
between functional and non-functional vasculature (Tyree and
Ewers, 1991) and may not reflect the pattern of water flow (Canny,
1990). Turquois and Malone (1996) used transducer equipment
to determine hydraulic resistances in tomato graft unions: the
major hydraulic connections became functional over a period of
48 h from the fifth day after grafting, consistent with the appearance of wound xylem bridges where water passed freely. Another
technique to evaluate the grafting interface during the graft union
development is the measurement of electrical wave transmission from the scion to the rootstock, in relation to histological
changes (Lu et al., 1996). However, root hydraulic conductance
(L0 ) measurements made below and above the graft union indicated that the graft union cannot be a barrier to water passage
for a compatible rootstock–scion union (Fernández-García et al.,
2004a).
Graft incompatibility can induce undergrowth or overgrowth
of the scion, which can lead to decreased water and nutrient flow
through the graft union and cause wilting of the plant (for review
see Davis et al., 2008). Grafting incompatibility usually occurs at
early stages, when vascular connections are forming, but it can
appear as late as the fruiting stage, when the plant has a high
demand for water and nutrients. It has been reported that the
supply of warm water to the graft union of grafted tomato and eggplant plants improved the storage quality, reducing water stress
at the beginning of the storage when vascular tissues of the rootstock and scion are not connected yet (Tokuda et al., 2006; Shibuya
et al., 2007). This reduction of water stress by a high graft union
temperature was due to improved water absorption by the scion
(Shibuya et al., 2007). Thus, to avoid physiological wilt, the promo-
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tion of root development and improved management of watering
are important in grafted plants.
The stage of the plant at the moment of grafting is important
with respect to the efficiency of the rootstock–scion interaction. Thus, sweet pepper plants grafted when older showed poor
development in their xylem connections at the graft site, which
resulted in low stomatal resistance and water potential compared
to younger plants (Johkan et al., 2009). Also, the shoot and root
genotype can be crucial for the leaf water content, especially under
stress conditions. The effects of the rootstock genotype on the
graft union and scion water relations were more marked in grafted
melon plants (Agele and Cohen, 2009). Leaf water content was
increased by 35% in grafted plants with an includer character scion
than in self-grafted plants (Santa-Cruz et al., 2002). This capacity
to increase the leaf water content was related to a lesser reduction of shoot growth (Neumann, 1997; Rus et al., 1999). Also,
leaf water content was similar under control conditions in several graft combinations of tomato, but increased to different levels
with salinity—making specific grafting combinations more resistant to salinity (Martínez-Rodríguez et al., 2008). In a similar way,
under water deficit, the leaves of grafted tomato plants maintained
higher leaf water potential than self-grafted plants in spite of higher
water loss through transpiration, indicating a greater ability to
promote water uptake (Weng, 2000). However, salinity had no
significant effect on relative leaf water content in cucumber and
tomato plant rootstocks (Huang et al., 2009; Estañ et al., 2005),
compared with the self-grafted plants, which could be attributed
to changes in the components of the osmotic adjustment (Huang
et al., 2009).
More recently, it was reported that differences in root hydraulics
in response to chilling between cucumber and figleaf gourd were
related to changes in both the activity of aquaporins and root
anatomy (Lee et al., 2005). Thus, the half-times of water exchange
and hydraulic conductivity of cortical cells were related to the
insensitivity of figleaf gourd cells to low temperature, suggesting
that figleaf gourd aquaporins may not close and are able to maintain their water transport activity at low temperature (Lee et al.,
2005). However, the contribution of aquaporins to root hydraulic
conductance in grafted plants of the Solanaceae and Cucurbitaceae,
compared to self-grafted plants, is not conclusive.
3. Nutrient uptake and translocation
Plants store minerals and other nutrients in different organs,
such as roots, stems, leaves and/or fruits. These organs have a
considerable influence on the uptake and translocation of mineral
nutrients in plants and this plays an essential role in physiological
processes such as growth, signal transduction and development
(Wang et al., 2006; Flowers and Colmer, 2008). The influence of
the rootstock on the mineral content in aerial plant parts was
attributed to physical characteristics of the root system, such as lateral and vertical development, which resulted in enhanced uptake
of water and minerals (Heo, 1991; Jang, 1992), this being one of
the main motives for the widespread use of grafted rootstocks
(Lee, 1994). However, in grafted fruit trees, no effect of the rootstock on leaf mineral content was found (Chaplin and Westwood,
1980) and, in these cases, more influence of the scion on leaf
nutrient content was observed. Tagliavani et al. (1993) suggested
that the vigour of both the scion and root system had an important role in the uptake and translocation of nutrients in grafted
fruit trees, while, in pistachio grafted plant (Pistachia vera L.),
changes of rootstock had an influence on the leaf content of certain essential minerals (Brown et al., 1994). Therefore, the contents
of macro- and micronutrients are affected by the rootstock and
scion characteristics, but, depending on the element and environ-
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M.C. Martínez-Ballesta et al. / Scientia Horticulturae 127 (2010) 112–118
mental conditions, the effect of the rootstock and/or scion may
change.
The effects of two different rootstocks on the leaf macronutrient contents of melon plants were tested by Ruiz et al. (1997), who
concluded that, in general, N was influenced more by the rootstock genotype than by the scion. Moreover, nitrate reductase (NR)
activity and nitrate accumulation were measured in grafted melon
plants and compared with non-grafted plants: both parameters
were conditioned significantly by the scion–rootstock interaction
and by the rootstock genotype, whereas the scion genotype did
not show any such effect (Ruiz and Romero, 1999). The characteristics of the rootstocks could result in increased absorption,
upward transport and accumulation of NO3 − in the scion, thereby
stimulating nitrate reductase (NR) and NO3 − assimilation. This
would account for the decreased foliar concentration of NO3 − and
increased NR activity in grafted plants compared to non-grafted
plants (Sivasankar and Oaks, 1996; Ruiz et al., 1998). Similar results
were obtained by Pulgar et al. (2000) for watermelon plants, NO3 −
and NH4 + being lower in leaves of grafted plants than in those of
control plants indicating that some rootstocks improved NR efficiency favouring NO3 − integration into amino acids and proteins
(Ruiz and Romero, 1999; Pulgar et al., 2000; Ruiz et al., 1997).
Graft compatibility in Solanaceous plants in relation to plant
nutrition was investigated using cultivars of tomato and pepper,
and no significant differences in nitrogen concentration appeared
among the four graft combinations examined (tomato/tomato,
tomato/pepper, pepper/tomato and pepper/pepper) (Kawaguchi et
al., 2008). Similarly, no significant differences in the nitrogen status were found when different grafted watermelons were tested for
improved alkalinity tolerance (Colla et al., 2010a). In addition to the
rootstock–scion interaction, the nitrogen content depends on the
environmental conditions in which plants develop. Thus, the total
nitrogen concentration in tomato plants increased in self-grafted
plants in response to lower temperatures in the root zone, but no
differences were found when tomato was grafted with a different
scion (Venema et al., 2008).
It has been reported that rootstocks can enhance some morphological and/or physiological characteristics of melon plants,
thereby increasing the absorption of phosphorus (P) from soil and
its translocation to the leaves of the scion (Ruiz et al., 1996). In
1997, Ruiz et al. demonstrated that the P concentration in grafted
melon plants can be affected similarly by the scion and by the
rootstock–scion interaction. However, Kawaguchi et al. (2008) concluded that the rootstock species was the main factor affecting the
absorption and translocation of this element in the graft combinations of Solanaceous plants. The concentrations of P in the leaves
and stems of cucumber plants were affected significantly by the
grafting combination, the values for grafted plants being higher
than for non-grafted plants (Rouphael et al., 2008). Similar results
were obtained for P concentrations in the leaves of grafted watermelon (Colla et al., 2010a; Uygur and Yetisir, 2009) and tomato
(Fernández-García et al., 2004c) plants, demonstrating that the
graft combination can affect P absorption positively. However, no
significant differences in P concentration were found by Huang et
al. (in press) for cucumber plants grafted onto two different rootstocks. All these different results indicate that root morphological
characteristics are not the only factors influencing the absorption
and translocation of P in plants and that the scion genotype and/or
each species must be taken into account also.
In watermelon plants grafted onto Cucurbita maxima, Duch
roots, Ca2+ concentrations were lower than in non-grafted plants,
regardless of the rootstock or scion used, while the opposite
behaviour was observed for Mg2+ (Ruiz et al., 1997). However,
the levels of both minerals decreased when tomato plants were
grafted onto pepper plants and vice versa, with respect to selfgrafted plants (Kawaguchi et al., 2008). These variations could
be explained by the smaller root systems and restricted xylem
hydraulic conductivity of the rootstock relative to the scion. In
other experiments with tomato, significant increases of tissue Mg2+
and Ca2+ were observed when grafted plants were compared with
non-grafted plants (Fernández-García et al., 2004c). However, in
grafted plants, no significant differences were seen for the Ca2+ and
Mg2+ contents in comparison with non-grafted plants of cucumber
(Rouphael et al., 2008; Huang et al., in press), melon (Edelstein et
al., 2005) or tomato (Chen et al., 2003). On the other hand, in grafted
watermelon, no differences in Ca2+ content were observed, but the
concentration of Mg2+ in leaves was influenced significantly by the
grafting combination, the values for plants grafted onto pumpkin
rootstocks being higher than for plants grafted onto bottle gourd
rootstock and for ungrafted plants (Colla et al., 2010b). All the
results indicate that Ca2+ and Mg2+ contents can be influenced significantly by the rootstock, but, in general, there is no effect of the
scion on their uptake. The physiological and physical characteristics of rootstocks probably affect the absorption and translocation
of these minerals in plants.
In tomato, no significant differences between the Na+ and K+
contents of grafted and non-grafted plants were found (SantaCruz et al., 2002; Chen et al., 2003; He et al., 2009), but in
other reports significant increases of K+ and no differences in
Na+ concentrations were obtained (Fernández-García et al., 2004c;
Martínez-Rodríguez et al., 2008). Similar results were obtained
by Goreta et al. (2008) in grafted watermelon. Also, in grafted
cucumber, significant increases in the K+ content were observed
by Rouphael et al. (2008) in all plant tissues except the fruits, these
being affected by the grafting combination. However, differences in
behaviour occurred in some experiments with melon plants. Thus,
Ruiz et al. (1997) showed significant decreases of both minerals in
grafted plants, indicating that the Na+ and K+ concentrations were
affected by the use of certain rootstocks. No differences in the K+
content were found in cucumber by Huang et al. (in press) or in
melon by Edelstein et al. (2005) when comparing grafted and nongrafted melon plants, but in this case a large decrease was observed
in the Na+ content for grafted plants. These differences between
their Na+ concentrations suggest that the grafted plants exclude
more Na+ than the non-grafted plants and so limit its concentration in their leaves. Similar results were obtained by Colla et al.
(2006, 2010a) for melon and watermelon plants.
Micronutrients are essential for plant growth and they are
involved in virtually all metabolic and cellular functions, like energy
metabolism, primary and secondary metabolism, cell protection,
gene regulation, hormone perception, signal transduction and
reproduction (Hansch and Mendel, 2009). Roots of cucumber plants
grafted onto commercial Shintoza rootstock and of non-grafted
plants accumulated larger amounts of Cu than the above-ground
parts, particularly the leaves (Rouphael et al., 2008), such that there
were higher Cu levels in roots than in shoots while the aerial parts
of grafted plants accumulated less Cu than those of non-grafted
plants. Similar results were found for Cu, Fe and Mg in tomato
plants with lower translocation of these elements to the leaves
of plants grafted onto ‘He-Man’ variety in comparison with the
self-grafted plants (Savvas et al., 2009). These results suggest that
grafted plants can limit Cu transport from roots to leaves more
efficiently, reducing the detrimental effect of Cu toxicity on plant
growth and yield. The improved performance of grafted cucumber
plants was attributed to their strong ability to inhibit Cu accumulation in their aerial parts and to maintain a better plant nutritional
status. In this experiment, no significant differences were observed
for Fe, Mn or Zn in grafted cucumber plants, compared with nongrafted plants, in control conditions. Huang et al. (in press) observed
a decrease of total microelements, but there were no significantly
different values for Fe, Mn, Cu or Zn when comparing non-grafted
cucumber plants with cucumber grafted onto Cucurbita ficifolia. In
M.C. Martínez-Ballesta et al. / Scientia Horticulturae 127 (2010) 112–118
this study, the decrease of total micronutrients in cucumber leaves
may have been attributable to ion interactions, precipitation and
increases in the ionic strength of the nutrient solution. For watermelon plants, lower accumulation of B in leaves was obtained when
they were grafted onto squash, highlighting the ability of the rootstock to exclude B and limit its transport to the leaves (Edelstein et
al., 2005).
Tomato plants grafted onto pepper rootstock showed lower concentrations of Cu, Mn and Zn, but no significant differences for
B, Fe or Mo, relative to control plants. On the other hand, when
pepper plants were grafted onto tomato rootstock no significant
differences in the Cu, Fe or Mn concentrations were obtained while
B, Mo and Zn showed significant decreases when compared with
control plants (Kawaguchi et al., 2008). Hence, in general, decreased
levels of these minerals were observed in grafted plants; this may
be explained by the smaller root system and restricted xylem
hydraulic conductivity from the rootstock to the scion.
4. Plant growth and biomass
Plant growth is influenced by several factors (environmental
conditions, plant nutritional status and hormone activities) related
to different physiological processes. The development of an adequate root system structure has been related to improved growth
of melon plants grafted onto Cucurbita species (Bletsos, 2005). Lagenaria sicerarias (Mol.) Standley is one of the species commonly used
as rootstock for watermelon to increase plant growth and enhance
water transport and plant nutrition (Lee, 1994; Oda, 1995; Yetisir
and Sari, 2003). According to Yetisir et al. (2007), all the grafted
plants of watermelon showed a higher number of leaves and greater
dry weight than the non-grafted control plants (Yetisir et al., 2007).
Similar results were found when transgenic plants were used as
rootstocks. Thus, bottle gourd rootstock with a cation exchanger
genetically modified, improved watermelon quality through the
translocation of nutrients and/or water to the scion, which allow
enhancing its biomass (Han et al., 2009).
In studies with mutants, it has been found that the effect of
mutation can be reversible either in the scion or rootstock. In
tomato plants, leaf area was not affected by grafting of wild-type
shoots onto an ABA-deficient mutant, compared with wild-type
self-grafts (Chen et al., 2002; Holbrook et al., 2002). Also, the shoot
phenotype of mutant/WT plants can differ from that of mutant selfgrafts, with partial phenotypic reversions of leaf area and growth
(Cornish and Zeevaart, 1988; Holbrook et al., 2002).
The morphology of the vascular system is modified during
graft union formation. Many reports have pointed out that callus
bridge formation between the rootstock and scion and the differentiation of new vascular tissue from callus cells, together with
the production of secondary xylem and phloem, are crucial for a
good rootstock–scion interaction (Andrews and Marquez, 1993;
Hartmann et al., 1997). Thus, Kawaguchi et al. (2008) observed that
the growth inhibition and high mortality in tomato/pepper and
pepper/tomato grafts were due to discontinuities in the vascular
bundles at the graft union.
After graft assemblage between the cells of the rootstock and
scion has occurred, differentiation of the new vascular system
begins. For this to occur, xylem differentiation and lignification are
necessary. Many studies have suggested that peroxidases play a
role in lignification (Whetten et al., 1998; Quiroga et al., 2000).
During growth development of the stem of herbaceous plants,
xylem cells are highly lignified. Observation of the structure of
the graft union showed formation of xylem and phloem vessels
through the graft union 8 days after grafting in tomato plants
(Fernández-García et al., 2004b). Also, root hydraulic conductance
measurements indicated that the graft union was fully functional 8
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days after grafting, which coincided with an increase of peroxidase
and catalase activities, suggesting that these activities are involved
in graft development in tomato plants and are necessary for optimal
rootstock–scion communication.
In this way, the results obtained by grafting cucumber onto
figleaf gourd rootstock (Curcurbita ficifolia Bouché) suggest that not
only the rootstock but also the scion affects the stomatal performance, producing a higher CO2 assimilation rate and less stomatal
resistance than in non-grafted and/or self-grafted plants (Ahn et
al., 1999; Yetisir et al., 2007; Rouphael et al., 2008; He et al., 2009;
Zheng et al., 2009). More recently, it has been suggested that the
restriction of leaf area may result from inhibition of net photosynthesis, which decreases the availability of assimilates for leaf
growth. This has been observed in non-grafted watermelon plants,
compared with those grafted onto pumpkin rootstocks (Colla et al.,
2010a), and in cucumber plants grafted onto pumpkin rootstocks,
which showed higher shoot yield, probably due to their ability to
maintain higher net CO2 assimilation. Also, it has been reported that
the higher CO2 assimilation in cucumber plants grafted on figleaf
gourd could result partly from the greater sink strength of the figleaf
gourd roots (Zhou et al., 2009).
Alkaline soils are widespread throughout agricultural regions,
particularly those with semi-arid climates (Campbell and Nishio,
2000). Results have demonstrated that plants respond to elevated
NaHCO3 concentrations in soil with decreases in shoot and root
growth (Alhendawi et al., 1997; Campbell and Nishio, 2000; Zribi
and Gharsalli, 2002), leaf number, fresh and dry mass and shoot
elongation. However, grafting may alleviate some of these effects:
under highly alkaline conditions, watermelon plants grafted onto
pumpkin rootstocks showed less change in the root/shoot biomass
ratio than non-grafted plants or those grafted onto bottle gourd
rootstocks (Colla et al., 2010a).
In some studies (Jones et al., 1987; Sharp et al., 2000; Dodd,
2003), ABA-deficient tomato mutants had a decreased leaf area
compared with wild-type (WT) plants. However, the leaf area of
the ABA-deficient tomato scions grafted onto WT rootstocks was
greater when compared with self-grafts, even though transpiration
rates were as high as in the self-grafts, implying that different processes are differentially sensitive to root-synthesised ABA (LeNoble
et al., 2004) Therefore, as these effects cannot be attributed to
improved water relations, an effect on ethylene synthesis has
been suggested. Also, it has been hypothesised that some signals
originating from roots (i.e. ABA and cytokinins) protect leaf photosynthesis in the shoots of stress-sensitive plants due to grafting,
since the chlorophyll content of potato scions decreased when an
ABA(−) line was used as rootstock, while it increased in an ABA(−)
potato scion grafted onto a salt-resistant rootstock (Etehadnia et
al., 2008). In this way, Zhou et al. (2007) observed an increased
concentration of cytokinin, involved in chloroplast build-up and
chlorophyll formation, and a decreased ABA concentration in xylem
sap, resulting in higher Rubisco content and activity. However, a
study in potato (Etehadnia et al., 2008) indicated a significant influence of the scion on the rootstock, in addition to the effect of the
rootstock on the scion, since the use of a resistant genotype as scion
had a positive impact—increasing the root biomass of the ABA(−)
mutant rootstock. This might have been due to a higher rate of
photosynthesis of the more-vigorous scions, leading to a greater
potential for partitioning of assimilates to the rootstock (Chen et
al., 2003).
An increased ABA concentration in xylem sap could induce a
series of physiological responses: for example, closure of stomata and enhancement of the antioxidant system. However, closure
of stomata could lead to decreased CO2 fixation and increased
ROS generation. Increased activities of antioxidant enzymes were
observed in leaves of tomato plants after grafting onto tomato
(Rivero et al., 2003a), as well as in cucumber plants grafted on
116
M.C. Martínez-Ballesta et al. / Scientia Horticulturae 127 (2010) 112–118
figleaf gourd, producing a higher photosynthetic rate in grafted
plants (Zhou et al., 2009). The lower ROS level in grafted plants,
probably due to cytokinins which could up-regulate the activities
of ROS-scavenging enzymes (Tachibana, 1988; Pogany et al., 2003),
is one of the possible reasons for decreased photoinhibition (Zhou
et al., 2009). Grafting also improved photosynthesis, by enhancing
the activities of antioxidant enzymes, in tomato (He et al., 2009)
and eggplant (Liu et al., 2007).
Changes in leaf biochemistry that result in down-regulation of
the photosynthetic metabolism may occur in response to lower
availability of carbon substrates under prolonged stresses (Chaves
and Oliveira, 2004; Flexas et al., 2006). The reduction of photochemical activity is considered to be one of the non-stomatal factors that
limit photosynthesis (Souza et al., 2004). Hence, it has been shown
that different stresses decrease the chlorophyll content (Liu et al.,
2007; Rouphael et al., 2008; Etehadnia et al., 2008) and the photochemical efficiency of photosystem II (PSII) (Ahn et al., 1999; Zheng
et al., 2009; He et al., 2009), but these effects can be improved by
grafting.
In vivo measurement of chlorophyll fluorescence has been
used to detect the effects of stress on the functioning of the
photosynthetic system (Lichtenthaler and Rinderle, 1988). The
photosynthetic activity of chloroplasts is considered to be one of
the most-heat-sensitive cell functions (Berry and Björkman, 1980;
Yordanov et al., 1986). Abdelmageed and Gruda (2009) indicated
that grafted plants developed better under heat-stress conditions
than non-grafted ones when a heat-sensitive tomato was grafted
on a heat-tolerant tomato cultivar and an eggplant cultivar, due to
the significantly higher chlorophyll fluorescence at the late-fruiting
stage.
The ratio of variable fluorescence to maximal fluorescence
(Fv /Fm ), which indicates the photochemical efficiency of PSII
(Öquist and Wass, 1988), was improved at low temperature by
grafting cucumber leaves on figleaf gourd (Ahn et al., 1999). These
results are in agreement with those of Zheng et al. (2009), who
found that grafting reduced damage to the photosynthetic apparatus. A similar effect was observed when grafting tomato with a
salt-tolerant rootstock, since this maintained higher photochemical activity of PSII (He et al., 2009). According to this, Albacete et
al. (2009) related a rootstock-induced increase in crop productivity
to changes in leaf area and photosynthetic capacity (Albacete et al.,
2009).
In the last step of graft union, the formation of vascular connections is considered by most authors to be a basic requirement for a
successful graft (Moore, 1984a,b; Wang and Kollmann, 1996). Discontinuous sieve-tube connections at the graft union may inhibit
the translocation of assimilates from the scion to the rootstock,
resulting in higher carbohydrate concentrations above the graft
union and lower concentrations below it (Kawaguchi et al., 2008).
A limited assimilate supply to the rootstock could then reduce the
size of the root system. This would decrease the carbohydrate concentration in the rootstock and/or greatly restrict xylem hydraulic
conductivity at the graft union. Also, phloem regeneration across
the graft interface has been the subject of some investigations for
herbaceous species (Tiedemann, 1989; Kollmann and Glockmann,
1990; Golecki et al., 1998).
It has been observed that there were no differences in root
carbohydrate contents at 14 days after grafting melon (Cucumis
melo L. ‘Arava’) onto compatible (RS59) and incompatible (RS62)
Cucurbita rootstocks, while there was a significant decrease 24
days after grafting in the incompatible rootstock, possibly due to
the decreased metabolic activity in the root sink and deterioration of root tissue at that stage (Aloni et al., 2008). These results
agree with those of Wang and Kollmann (1996), who reported
that the import of labelled sucrose (14C-sucrose) from the Nicandra physaloides (L.) Gaertn. scion into the Solanum lycopersicum L.
rootstock increased with the onset of phloem regeneration about
5–7 days after grafting, but decreased again about 4 weeks after
grafting. Using 14C-labelling techniques, it has been shown that an
increasing number of sieve tubes in the graft unions was correlated
with an increasing rate of assimilate transport (Rachow-Brandt and
Kollmann, 1992; Schöning and Kollmann, 1997).
5. Conclusions
The scion–rootstock connection is fundamental for optimal
growth, water and nutrient uptake and transport. A deficiency in
mineral nutrients and water might cause suppressed growth of the
scion and low carbohydrate concentrations in the root will decrease
root growth, contributing to low water and nutrient uptake, and
decrease the availability of carbohydrates as energy resources for
the active uptake of ions. In other words, the physiological disturbances induced by vascular union discontinuities at the graft union
may lead to growth inhibition due to restricted communication
between scion and rootstock. Therefore, besides the compatibility and the right scion and rootstock combination for the intended
purpose (stress resistance), care must be taken when grafting to
achieve the optimal bundle connection between rootstock and
scion.
Acknowledgements
The authors thank Dr. David J. Walker, for correction of the written English in the manuscript. The work was funded by the Regional
Agency for Science and Technology of Murcia–Fundación Séneca
(Project ref. 08753/PI/08). Part of this work was also funded by the
Spanish CICYT National Research Programme (AGL2009–12720).
M.C. Martínez-Ballesta thanks the Spanish Ministerio de Ciencia
e Innovación and CSIC for funding through the “Ramón y Cajal”
programme (Ref. RYC-2009-04574).
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