Anda di halaman 1dari 11

Scientia Horticulturae 106 (2005) 1–11


A review of new advances in mechanism

of graft compatibility–incompatibility
Ana Pina, Pilar Errea *
Unidad de Fruticultura, Centro de Investigación y Tecnologı́a Agroalimentaria (CITA)-DGA,
Ctra. Montañana, no. 930, 50080 Zaragoza, Spain
Received 22 June 2004; received in revised form 7 March 2005; accepted 26 April 2005


The mechanism of graft incompatibility is not yet fully understood and many reports focus on
this problem in order to understand the mechanisms of graft development. These reports refer to
both cytological and biochemical responses occurring at an early phase in response to grafting, as
well as the consequences of these events on the future graft response. Some theories argued the
possibility that the phenomena of cellular recognition could be involved in the development of a
functional vascular connection since the first callus are formed. However, callus formation can be a
passive response to a wound with no implications in the future compatibility responses. We sum up
different reasons that may have an influence on graft success: inherent system of cellular
incompatibility, formation of plasmodesmata, vascular tissue connections, and the presence of
growth regulators and peroxidases. In addition, phloem-mobile proteins have been reported that
cross the graft interface when graft bridging is established and it is functional. This review provides
an overview of the graft response and recent advances in the knowledge of the mechanism involved
in the early responses to grafting for the development of cohesion between the stock and scion
during graft ontogeny.
# 2005 Elsevier B.V. All rights reserved.

Keywords: Cellular responses; Graft-compatibility; Plasmodesmata; Proteins; Wounding

* Corresponding author. Tel.: +34 976 71 63 12; fax: +34 976 71 63 35.
E-mail address: (P. Errea).

0304-4238/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
2 A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11


1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Callus formation: the beginning of the graft process . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Plasmodesmata and its role in cellular communication . . . . . . . . . . . . . . . . . . . . . . . 4
4. Vascular connections in the graft process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

1. Introduction

Plant grafting is a widely used means of plant propagation and growth control that is of
considerable importance in the adaptation of interesting cultivars in appropriate areas. The
grafted partners can belong to the same species or genus, but usually components that are
more genetically divergent are used. In these cases the stock and scion do not always
constitute a successful graft and show their disagreement in the form of incompatibility.
Several authors have defined the sequence of structural events during the healing of the
grafts in woody and herbaceous plants. Hartmann et al. (2002) overview in their review of
the sequence of events.

1. Cut scion tissue capable of meristematic activity is brought into secure, intimate contact
with similarly cut stock tissue in such a manner that the cambial regions of both are in
close proximity in order to interconnect through the callus bridge. Once the two
components of the graft, stock and scion, are in intimate contact, new parenchymatous
cells proliferate from both stock and scion producing the callus tissue that soon
intermingles and interlocks, filling up the spaces between the two components
connecting the scion and the rootstock.
2. New cambial cells differentiate from the newly formed callus, forming a continuous
cambial connection between rootstock and scion. Furthermore, prior to the binding of
vascular cambium across the callus bridge, initial xylem and phloem may be
differentiated. The wound-repair xylem is generally the first differentiated tissue to
bridge the graft union, followed by wound-repair phloem.
3. In the last step of the graft establishment process, the newly formed cambial layer in the
callus bridge begins typical cambial activity forming new vascular tissues. Production
of new xylem and phloem thus permits the vascular connection between the scion and
rootstock. For the majority of authors, this is considered as the basic requirement for a
successful graft (Moore and Walker, 1981a,b; Yeoman, 1984; Tiedemann, 1989).
The mechanism, in which incompatibility is expressed, is not clear and several
hypotheses have been advanced in an attempt to explain incompatibility. The majority of
hypothesis referred to an early stage of development has been related to herbaceous
systems. However, few studies have been made on early establishment in woody plants,
where in many cases incompatibility is manifested by the breaking of the trees at the point
of the union particularly when they have been growing for some years (apricot on Prunus
grafts, pear on quince grafts).
A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11 3

This review provides a summary of the new advances in studies on the mechanism of
graft compatibility focused on the early responses of grafting and how these studies can be
correlated with the changes observed in some Prunus combinations at early stages.

2. Callus formation: the beginning of the graft process

The formation of callus tissue at the graft interface is the first response to grafting.
Whereas it has been found that grafting failure can be characterized by a lack of callus
formation at the graft interface (Weatherhead, 1986), other studies have revealed that the
new callus formed is a passive event that occurs in compatible and incompatible grafts and
is a common response to wounding (Moore and Walker, 1981a,b). This conclusion is also
supported by the fact that callus formation is independent of other events in graft
Once the callus has formed, the events that follow this initial formation, when the callus
cells first touch, seem to be essential for the critical event deciding the development of
future vascular connections. Yeoman was the first to document structural events correlated
with the changes in wall cells occurring during graft formation in Solanacea describing a
cell recognition mechanism in which opposing cells of graft partners touch (Yeoman et al.,
1978; Yeoman, 1984). The basis of this recognition system is that protein molecules
released from the plasmalemmas combine to form a complex with catalytic activity that
subsequently initiates a developmental sequence resulting in the formation of a successful
graft. Neither the nature of these proteins nor their roles have been describes up to date.
When this complex is not formed, due to differences between the cells in contact, a special
kind of protein called lectin, produces a mutual rejection of the opposing graft cells leading
to the formation of incompatible grafts (Yeoman and Brown, 1976).
Further works studying the formation of callus tissue imply some of these compounds in
the mechanism of adhesion of the graft partners. Wart-like projections on the cell wall
surface have been reported in callus cells at the graft union (Jefree and Yeoman, 1983;
Barnett and Weatherhead, 1988). In Sitka spruce, adhesion between cells of the scion and
rootstock is aided by a ‘‘cement’’ or binding material, which projects beadlike projections
from the callus that consist of a homogeneous matrix made up of a mixture of pectin,
carbohydrate, protein and fatty acids, and a fibril/vesicular component comprised mainly
by carbohydrate and pectins (Miller and Barnett, 1993). These beadlike projections,
besides acting as binding or cementing cells, may serve a more active role in cell
recognition and the successful merging of tissues of the graft partners.
Alternatively, Moore and Walker (1981a,b) examined the relationship between the
structural events associated with graft formation in Crassulacea and no recognition
events were found to be necessary for the initial adhesion of stock and scion, since the
initial adhesion is a passive event that occurs in response to wounding. However, some
form of cellular communication is required during at least the differentiation of
procambium between the stock and scion (Moore and Walker, 1981a). In incompatible
grafts, the failure of this procambial development may be the result of the absence of an
additional and more direct form of cellular communication between the graft partners
(Moore and Walker, 1981b). Therefore, grafting surfaces can be cohered in the absence
4 A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11

of direct cellular contact and protoplasmic continuity, as was postulated by Moore

(1984) in compatible autografts in Sedum telephoides, where the initial cohesion of
stock and scion is mediated by some extracellular interaction between the graft partners.
The cell wall polymers proposed for cellular recognition reaction are abundant in the
graft union. These would be pectic fragments considered as chemical messengers in the
determination of graft compatibility (Jefree and Yeoman, 1983). That cell wall derived
oligassacharides are capable of modulating plant growth and development have been
widely reviewed (for review, see Ridley et al., 2001; Creelman and Mullet, 1997; John
et al., 1997; Fry et al., 1993).
Other works have also found extracellular substances interconnecting adjacent cells at
the surface of intact proliferating callus cells, which most probably represent pectic
material involvement in the establishment of the first mechanical union between cell
surfaces (Moore, 1983; Kollmann and Glockmann, 1991).
Despite the fact that the callus formation occurs as a wound reaction and it is found in
compatible and incompatible grafts, the content and nature of the cells involved in the first
step of graft formation can play an important role in triggering the responses that lead to the
formation of a strong and successful union. In this sense, some differences have been
reported in the callus fusion of Prunus combinations growing in vitro, related to cell
arrangement, stain intensity of cellulose and lipid and phenol content of the cells (Errea
et al., 2001). The changes observed in the callus system are correlated with the changes
observed at a later state of graft systems. The cellular abnormalities observed in callus
tissue seem to be involved in the lack of cambial and vascular formation, avoiding a strong
union in Prunus systems. Some of the theories argued for herbaceous plants, as local
interactions between the opposing cells of the graft union (Yeoman, 1984; Jefree et al.,
1987) could explain the callus differentiation mechanism.
Why a proportion of callus tissue is capable of establishing cambium and vascular
connections, and a large part of the callus formed is not able to differentiate, raises the
question of some type of cellular communication and synthesis of compounds that could be
involved in this differentiation mechanism.

3. Plasmodesmata and its role in cellular communication

Plasmodesmata are diverse and highly dynamic structures that offer a unique pathway
for symplastic cell communication and constitute a potential pathway among cells in the
graft bridge. Studies on the mechanism of plasmodesmata have shown their important role
in the mechanism of cellular communications (Salisbury and Ross, 1991; Lucas et al.,
1993; Schulz, 1999) being subject to discussion the occurrence of symplastic connections
in grafts for a long time. As Jefree and Yeoman (1983) defined, when callus cells come into
contact, the cell walls undergo dissolution, holes in the cell walls appear, plasmalemma
contact and plasmodesmata form. They symplastically connect the grafting partners
(Strasburger, 1901) permitting a mutual metabolic interaction in the interfacing cells. This
requires leaching or diffusion of some compounds from both sides of the union to the other
diffusing into the cell walls, in order to achieve a firm cohesion between rootstock and
scion (Yeoman and Brown, 1976).
A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11 5

Research on the mechanism of plasmodesmata formation has shown prominent

differences in the development of interspecific plasmodesmata between graft partners
suggesting that cell recognition and functional coordination may be involved in graft
formation (Kollmann and Glockmann, 1985; Kollmann et al., 1985) with special
attention placed on the establishment and modification of primary plasmodesmata as in
the novo formation or modification of secondary plasmodesmata (Ehlers and Kollmann,
1996, 2001). Regarding to the events leading to the formation of secondary
plasmodesmata begin with the attachment of smooth domains of the ER to the
plasmalemma determining the location and the shape of the developing plasmodesmal
strands. After that, a process of invagination of the plasmalemma occurs around the ER
cisternae, that is interpreted as a consequence of wall material secretion by a
plasmalemma/Golgi vesicle fusion process. The membranes of the fusing Golgi vesicles
form the plasmalemma that lines the plasmodesmal connections (Kollmann and
Glockmann, 1991). Since the thinning and the precise position of the opposite ER-
plasmalema contact occur before any symplasmic cell-to-cell contact is established the
exchange of informational signals across the cell wall might be involved in the
coordination (Jefree and Yeoman, 1983; Moore and Walker, 1981a; Kollmann and
Glockmann, 1991, 1999). Thus, in order to form continuous secondary plasmodesmata
an exact cooperation of both cell partners is required, since insufficient coordination
between adjacent cells leads to the formation of mismatching, half plasmodesmata
through the wall cell only in one cell partner. In graft interfaces of incompatible
heterografts, discontinuous-half plasmodesmata have been observed in the graft unions
between different types of cells, using species-specific cell markers in order to identify
the graft interface (Kollmann et al., 1985). These reports indicate that plasmodesmata
may contribute to graft failure due to a misalignment of the graft partners, although they
may not be unique to graft compatibility.
More recently, advances in studies on caged probes offer experimental approaches to
study the physiological control of plasmodesmata, since the experimental manipulation is
avoided such as the pressure changes or wounded cells introduced by microinjection
(Schulz, 1999; Martens et al., 2004). Recent studies performed using caged fluorescein
have shown the possible existence of plasmodesmal connectivity between in vitro callus
cells in P. munsoniana (Pina et al., data unpublished). We have been encouraged by the
response so far and it is expected that incompatible combinations will not display
widespread uncaged fluorescein indicating the presence of non-functional plasmodesmata.
These studies provide a basis for interpreting earlier responses of callus tissue in apricot on
plum combinations. Its possible role in the mechanism of compatibility needs more
experimental evidence and it is a subject of further researches.

4. Vascular connections in the graft process

In the last step of graft formation, the formation of vascular connections is considered
for most authors the basic requirement for a successful graft (Moore, 1984; Wang and
Kollmann, 1996). The fact that the new vascular connections could be not well
differentiated or weakly established has been postulated as the main reason for
6 A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11

incompatibility in woody plants (Mosse, 1962; Errea et al., 1994a,b). In these cases, an
abnormal process of neocambium differentiation leads to a cambial involution and a lack
of differentiation into new vascular elements, as has been pointed out for pear and
quince grafts (Ermel et al., 1999) and apricot on Prunus grafts (Errea et al., 1994b).
While it appears that the formation of functional vascular connections is essential for
successful grafts in herbaceous plants, in woody plants incompatible grafts can grow for
several years without any external indication of incompatibility, denoting the presence
of functional vascular connections in incompatible grafts (Mosse, 1962; Hartmann et al.,
Studies on phloem regeneration across the graft interface have been the subject of
some herbaceous investigations (Stoddard and Mc Cully, 1979; Tiedemann, 1989;
Kollmann and Glockmann, 1990; Golecki et al., 1998). In the compatible system
Lycopersicon esculentum (L) on Solanum tuberosum (S) as well as in the autografts
(Schöning and Kollmann, 1995, 1997) 14C-labelling techniques revealed that
assimilated transport occurs from the apical callus of the scion, to the basal callus
of the stock. As was expected, a close interrelation between transport and phloem
restitution in the graft union could be demonstrated. On the contrary, in incompatible
system Vicia faba (V) on Helianthus annuus (H), an increase in 14C-transport to the
stock during all stages of graft union development did not occur and no correlation was
found between phloem regeneration and assimilation transport across the graft interface
in this less compatible combination. 5–6 carboxifluorescein (CF) translocation
experiments confirm non-functional phloem connections in V/H-heterograft (Schöning
and Kollmann, 1997).
However, in apricot (Prunus armeniaca) on plum grafts, the formation of new vascular
connections occurs in both compatible and incompatible combinations (Errea et al.,
1994b). The transport of disodium fluorescein across the graft union confirms the
communication and functionality of these connections since fluorescence can be seen in
both partners of the graft. In these combinations, the difference between compatible and
incompatible grafts lies in the presence of a portion of the callus tissue in incompatible
grafts that cannot differentiate into cambium and vascular tissue, resulting in the existence
of wide areas at the union similar to undifferentiated callus cells. This lack of cambial
activity in some areas of the graft union could affect the activity of the new xylem and
phloem formed, causing discontinuities in the cambium and the formation of a
parenchymatous line interrupting the vascular connection (Hartmann et al., 2002),
producing a mechanically weak union.
The majority of studies on herbaceous grafts have been performed with Cucurbits due
to their distinct phloem anatomy and plentiful vascular exudation. As it is known, during
the ontogeny of the sieve element/companion cell complex, synthesis of proteins
coincides with vascular development. Evidence suggests that in the graftage of Cucumis
and Cucurbita, changes in protein banding may be due to polypeptides migrating
symplastically across the graft union via the connecting phloem and not from the
grafting procedure (Tiedemann and Carsens-Behrens, 1994). The urgent need to
reconnect disrupted vascular bundles should result in the expression of essential
proteins, possibly at reduced concentrations owing to abbreviated developmental periods
(Schulz, 1990). The question opened so far is whether in some Prunus grafts, where good
A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11 7

and functional vascular connections are established, translocation of signalling

molecules, such as polypeptides in the phloem, could be significant in cell recognition
and compatibility between the graft partners (Hartmann et al., 2002).
Due to the importance of the phloem as a nutrient and information transport system,
grafting techniques have been performed to study long-distance translocation of proteins
(Golecki et al., 1998, 1999) and RNA (Ruiz-Medrano et al., 1999; Gómez and Pallás, 2004;
Gómez et al., 2005) via the phloem. It has been shown the P-proteins (PP1, PP2) are
synthesized in companion cells of differentiating sieve element–companion complex
within the phloem transport (Clark et al., 1997), being translocated into sieve elements
(Golecki et al., 1999) when these are established and functionals (Leineweber et al., 2000).
The expression of PP1 and PP2 is developmentally related to defined stages of phloem
differentiation (Dannenhoffer et al., 1997) and they are supposed to be phloem-mobile
(Tiedemann and Carsens-Behrens, 1994). The conservation of the pattern of PP2-gene
expression in the sieve element–companion cell complex in different angyosperm species
suggests that it plays an important role in the development and function of the vascular
system (Dinant et al., 2003). Although it is also known that the majority of the phloem
proteins not only perform sieve tube maintenance, but also can be linked to direct and
indirect stress and defence responses (Walz et al., 2002, 2004). Furthermore, it has been
identified and characterised some melon phloem proteins with RNA-binding activity
(Gómez et al., 2005).
In addition, the relationships between scion and stock are affected by growth regulators,
and it has been postulated that graft incompatibility may also exist. For example, an
important substance involved in the development of compatible unions is auxin, which is
released from vascular strands of the stock and the scion and induces the differentiation of
vascular tissues, functioning as morphogenic substances (Moore, 1984; Aloni, 1987;
Mattsson et al., 2003). Its translocation from the root system has been studied in apples and
has been related to graft incompatibility, since a supra and basipetal movement of auxin can
organize the morphogenetic pattern of the entire plant body (Zajaczowski et al., 1983),
even accelerating the formation of a successful graft (Shimomura and Fujihara, 1977).
Additionally, other compounds, like polyphenols also play a prominent role in graft union
formation by influencing lignification processes and by their protein-precipitating feature
(Haslam, 1979). It has been proposed that stress situations can lead to both the
accumulation of flavanols and their degradation by oxidases (Van Sumere et al., 1985),
which can bring about marked effects on the growth and metabolism of tissues such as an
inhibition of the lignin pathway (Buchloh, 1960). Some papers report observations on the
characterization of monomeric and oligomeric flavan-3-ols in apricot cultivars and
rootstocks (Errea et al., 1994a) and their accumulation in apricot combinations with a
different degree of compatibility (Errea et al., 1992, 2000). Synthesis of flavanones can
determine incompatibility in Prunus, such as prunasin (Moing et al., 1987; Moing and
Carde, 1988), and can be stimulated by ABA and GA (Treutter and Feucht, 1988). The
modulation of prunin levels is affected by growth regulators. All these macromolecules
(phloem proteins, RNA, hormones) that are present in the sap phloem might appear to be
important from our point of view during vascular differentiation in compatibility process.
On the other hand, the involvement of certain enzymes in the cellular behaviour during
the first steps of graft formation have been studied in different species, although the specific
8 A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11

role and effects on incompatibility is still not clear (Quesada and Macheix, 1984; Deloire
and Hebant, 1982). Schmid and Feucht (1985) had studied proteins, peroxidases in the
phloem and acid phosphatases in Prunus avium/Prunus cerasus grafting confirming that is
possible to define a good union not only by morphological characters but also by
biochemical methods. Based on biochemical assays, Gulen et al. (2002) concluded that the
absence or presence of peroxidase isozymes profile in the pear-quince graft combination is
an experimental approach to predict incompatibility reaction. More recently, investigations
suggest that increased peroxidase and catalase activities might be involved in graft
development in tomato plants (Fernandez-Garcia et al., 2004).
With regard to grafting process in fruit trees more studies should be performed to obtain
a deeper knowledge about the mechanisms that take place during the graft incompatibility
reactions, which will allow us to make an early rootstock selection, before we observe any
external incompatibility symptoms.

5. Conclusions

The developmental process of the graft union has attracted considerable attention and
much information about it has been gathered. Several investigators have commented on
structural events that may be responsible for the development of cohesion between the stock
and scion during graft ontogeny. These reports study cytological events occurring in response
to grafting with special reference to the possibility that the phenomena of cellular recognition
could be involved in the development of functional vascular connections, since the basis of an
incompatibility response could be determined by local interactions between the opposing
cells of the graft union itself. Contrary to this hypothesis, the cohesion of graft partners has
been explained as resulting from the deposition and subsequent polymerization of cell wall
material that occur in response to the wounding inherent to graft establishment, which is not
related to the compatibility reaction. Despite the fact that callus formation can be considered
as a common wound healing response in plants, recent advances in studying the
plasmodesmata as the highly dynamic structures that offer a pathway for symplastic cell
communication, open the door to its important role in cell recognition, and compatibility and
incompatibility response. Also other lines of research using grafting techniques, revealed the
existence of soluble proteins in phloem exudates that have been developmentally related to
defined stages of phloem differentiation; more experimental proofs will be necessary in order
to fully understand their involvement in phloem function. As the mechanisms involved in all
these processes have been related to herbaceous graft combinations, future studies should
include a much wider range of similarities on woody responses to reach a better
understanding of the mechanism of incompatibility in these graft combinations.


Aloni, R., 1987. Differentiation of vascular tissues. Ann. Rev. Plant Physiol. 38, 179–204.
Barnett, J.R., Weatherhead, I., 1988. Graft formation in Sitka spruce: a scanning electron microscopy study. Ann.
Bot. 61, 581–587.
A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11 9

Buchloh, G., 1960. The lignification in stock-scion junctions and its relation to compatibility. In: Pidham, J.B.
(Ed.), Phenolics in Plants in Health and Disease. Pergamon Press, p. 67.
Clark, A.M., Jacobsen, K.R., Bostwick, D.E., Dannenhoffer, J.M., Skaggs, M.I., Thompson, G.A., 1997.
Molecular characterization of a phloem-specific gene encoding the filament protein, phloem protein 1
(PP1) from Curcubita maxima. Plant J. 12, 49–61.
Creelman, R.A., Mullet, J.E., 1997. Oligosaccharins, brassinolides, and jasmonates: nontraditional regulators of
plant growth, development, and gene expression. Plant Cell 9 (7), 1211–1223.
Dannenhoffer, J.M., Schulz, A., Skaggs, M.I., Bostwick, D.E., Thompson, G.A., 1997. Expression of the phloem
lectin is developmentally linked to vascular differentiation in cucurbits. Planta 201, 405–414.
Deloire, A., Hebant, C., 1982. Peroxidase activity and lignification at the interface between stock and scion of
compatible and incompatible grafts of Capsicum on Lycopersicum. Ann. Bot. 49, 887–891.
Dinant, S., Clark, A.M., Zhu, Y., Vilaine, F., Palauqui, J.Ch., Kusiak, Ch., Thompson, G.A., 2003. Diversity of the
superfamily of phloem Lectins (phloem protein 2) in angyosperms. Plant Physiol. 131, 114–128.
Ehlers, K., Kollmann, R., 2001. Primary and secondary plasmodesmata: structure, origin, and functioning.
Protoplasma 216 (1–2), 1–30.
Ehlers, K., Kollmann, R., 1996. Formation of branched plasmodesmata in regenerating Solanum nigrum-
protoplasts. Planta 1999, 126–138.
Ermel, F.F., Kervella, J., Catesson, A.M., Poessel, J.L., 1999. Localized graft incompatibility in pear/quince (Pyrus
communis/Cydonia oblonga) combinations: multivariate analysis of histological data from 5-month-old
grafts. Tree Physiol. 19 (10), 645–654.
Errea, P., Garay, L., Marı́n, J.A., 2001. Early detection of graft incompatibility in apricot (Prunus armeniaca)
using in vitro techniques. Physiol. Plant 112, 135–141.
Errea, P., Gutmann, M., Feucht, W., 2000. Physiological implications of falvan-3-ols in apricot-rootstock
combinations. Adv. Hort. Sci. 14 (3), 126–134.
Errea, P., Treutter, D., Feucht, W., 1994a. Characterization of flavanol-type polyphenols in apricot cultivar and
rootstocks. Adv. Hort. Sci. 3, 165–169.
Errea, P., Felipe, A., Herrero, M., 1994b. Graft establishment between compatible and incompatible Prunus spp. J.
Exp. Bot. 45, 393–401.
Errea, P., Treutter, D., Feucht, W., 1992. Specificity of individual flavan 3-ols interfering with the grafting stress of
apricots. Angewandte Botanik 66, 21–24.
Fernandez-Garcia, N., Carvajal, M., Olmos, E., 2004. Graft union formation in tomato plants: peroxidase and
catalase involvement. Ann. Bot. 93 (1), 53–60.
Fry, S.C., Aldington, S., Hetherington, P.R., Aitken, J., 1993. Oligosaccharides as signals and substrates in the
plant-cell wall. Plant Physiol. 103 (1), 1–5.
Golecki, B., Schulz, A., Thompson, G.A., 1999. Translocation of structural P proteins in the phloem. Plant Cell 11,
Golecki, B., Schulz, A., Carstens-Behrens, U., Kollmann, R., 1998. Evidence for graft transmission of structural
phloem proteins or their precursors in heterografts of Cucurbitaceae. Planta 206, 630–640.
Gómez, G., Pallás, V., 2004. A long-distance translocatable phloem protein from cucumber forms a ribonucleo-
protein complex in vivo with Hop stunt viroid RNA. J. Virol. 78 (18), 10104–10110.
Gómez, G., Torres, H., Pallás, V., 2005. Identification of translocatable RNA-binding phloem proteins from melon,
potential components of the long-distance RNA transport system. Plant J. 41 (1), 107–116.
Gulen, H., Arora, R., Kuden, A., Krebs, S.L., Postman, J., 2002. Peroxidase isozyme profiles in compatible and
incompatible pear-quince graft combinations. J. Am. Soc. Hort. Sci. 127 (2), 152–157.
Hartmann, H.T., Kester, D.E., Davies, F.T., Geneve, R.L., 1997. Plant Propagation. Principles and Practices, sixth
ed. Prentice Hall, Upper Saddle River, NJ, 757 pp. ISBN 0-13-206103-1.
Hartmann, H.T., Kester, D.E., Davies, F.T., Geneve, R.L., 2002. Plant Propagation. Principles and Practices,
seventh ed. Prentice Hall, Upper Saddle River, NJ, 849 pp. ISBN 0-13-679235-9.
Haslam, E., 1979. Vegetable tannins. In: Swain, T., Harborne, B., van Sumere, F. (Eds.), Biochemistry of Plant
Phenolics, vol. 12. Plenum Press, New York, London, pp. 475–523.
Jefree, C.E., Yeoman, M.M., Parkinson, M., Holden, M.A., 1987. The chemical basis of cell to cell contact and its
possible role in differentiation. British Plant Growth Regulator Group, Monograph 16. Advances in the
Chemical Manipulation of Plant Tissue Cultures, pp. 73–86.
10 A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11

Jefree, C.E., Yeoman, M.M., 1983. Development of intercellular connections between opposing cells in a graft
union. New Phytol. 93, 491–509.
John, M., Rohrig, H., Schmidt, J., Walden, R., Schell, J., 1997. Cell signalling by oligosaccharides. Trends Plant
Sci. 2 (3), 111–115.
Kollmann, R., Glockmann, C., 1999. Multimorphology and nomenclature of plasmodesmata in higher plants. In:
van Bel, A.J.E.,van Kesterenm, W.J.P. (Eds.),Plasmodesmata: structure, function, role in cell communication.
Springer, Berlin Heidelberg, New York, Tokio, pp. 149–172.
Kollmann, R., Glockmann, C., 1991. Studies on graft unions. III. On the mechanism of secondary formation of
plasmodesmata at the graft interface. Protoplasma 165, 71–85.
Kollmann, R., Glockmann, C., 1990. Sieve elements of graft unions. In: Behnke, H.-D., Sjolund, R.D. (Eds.), The
Sieve Element—Comparative Structure, Induction, Development. Springer Verlag, Berlin, Heidelberg, New
York, pp. 219–237.
Kollmann, R., Glockmann, C., 1985. Studies on graft unions. I. Plasmodesmata between cells of plants belonging
to different unrelated taxa. Protoplasma 124, 224–235.
Kollmann, R., Yang, S., Glockmann, C., 1985. Studies on graft unions. II. Continuous and half plasmodesmata in
different regions of the graft interface. Protoplasma 126, 19–29.
Leineweber, K., Schulz, A., Thompson, G.A., 2000. Dynamic transitions in the translocated phloem filament
protein. Aust. J. Plant Physiol. 27, 733–741.
Lucas, W.J., Ding, B., Van der Schoot, C., 1993. Plasmodesmata and the supracellular nature of plants. New
Phytol. 125, 435–476.
Martens, J., Hansen, M., Schulz, A., 2004. Caged probes—a novel tool in studying symplasmic transport in plant
tissues. Protoplasma 223 (1), 63–66.
Mattsson, J., Ckurshumova, W., Berleth, T., 2003. Auxin signaling in Arabidopsis leaf vascular development.
Plant Physiol. 131 (3), 1327–1339.
Miller, H., Barnett, J.R., 1993. The structure and composition of bead-like projections on Sitka spruce callus cells
formed during grafting and in culture. Ann. Bot. 72, 441–448.
Moing, A., Salesses, G., Saglio, P.H., 1987. Growth and the composition and transport of carbohydrate in
compatible and incompatible peach plum grafts. Tree Physiol. 3 (4), 345–353.
Moing, A., Carde, J.P., 1988. Growth, cambial activity and phloem structure in compatible and incompatible peach
plum grafts. Tree Physiol. 4 (4), 347–359.
Moore, R., 1984. A model for graft compatibility-incompatibility in higher plants. Am. J. Bot. 71, 751–758.
Moore, R., 1983. Studies of vegetative compatibility-incompatibility in higher-plants. 4. The Development of
Tensile-Strength in a Compatible and an Incompatible Graft. Am. J. Bot. 70 (2), 226–231.
Moore, R., Walker, D.B., 1981a. Studies on vegetative compatibility-incompatibility in higher plants. I. A
structural study of a compatible autograph in Sedum telephoides (Crassulaceae) Am. J. Bot. 68, 820–
Moore, R., Walker, D.B., 1981b. Studies on vegetative compatibility-incompatibility in higher plants. II. A
structural study of an incompatible heterograft between Sedum telephoides (Crassulaceae) and Solanum
pennelli (Solanaceae) Am. J. Bot. 68, 831–842.
Mosse, B., 1962. Graft incompatibility in fruit trees. Technical Communication of the Commonwealth Bureau of
Horticultural Plant Crops 28, 1–36.
Quesada, M.P., Macheix, J.J., 1984. Caractérisation d’une peroxydase impliquée spécifiquement dans la
lignification, en relation avec I’incompatibilité au greffage chez I’abricotier. Phys. Veg. 22, 533–540.
Ridley, B.L., O’Neill, M.A., Mohnen, D.A., 2001. Pectins: structure, biosynthesis, and oligogalacturonide-related
signaling. Phytochemistry 57 (6), 929–967.
Ruiz-Medrano, R., Xoconostle-Cazares, B., Lucas, W.J., 1999. Phloem long-distance transport of CmNACP
mRNA: implications for supracellular regulation in plants. Development 126 (20), 4405–4419.
Salisbury, F.B., Ross, C.W., 1991. In: Plant Physiology, fourth ed. Wadsworth Publishing Company. Belmont
California. A division of Wadsworth Inc. ISBN 0-534-15162-0. Sections 1.4 and 7.3.
Schöning, U., Kollmann, R., 1995. The function of phloem connections in regenerating in vitro-grafts. Bot. Acta
108, 56–62.
Schöning, U., Kollmann, R., 1997. Phloem translocation in regenerating in vitro-heterografts of different
compatibility. J. Exp. Bot. 48, 289–295.
A. Pina, P. Errea / Scientia Horticulturae 106 (2005) 1–11 11

Schulz, A., 1990. Wound-sieve elements. In: Behnke, H.D., Sjolund, R.D. (Eds.), Sieve Elements: Comparative
Structure, Induction and Development. Springer, Berlin, pp. 199–217.
Schulz, A., 1999. Physiological control of plasmodesmal gating. In: van Bel, A.J.E., van Kesteren, W.J.P. (Eds.),
Plasmodesmata: Structure, Function, Role in Cell Communication. Springer Verlag, Berlin, Heidelberg, New
York, pp. 173–204.
Schmid, P.P.S., Feucht, W., 1985. Compatibility in Prunus avium/Prunus cerasus graftings during the initial phase.
III. Isoelectrofocusing of proteins, peroxidases and acid phosphatases during union formation. J. Hort. Sci. 60
(3), 311–318.
Shimomura, T., Fujihara, K., 1977. Physiological study of graft union formation in Cactus. II. Role of auxin on
vascular connection between stock and scion I. Jpn. Soc. Hort. Sci. 45, 397–406.
Stoddard, F.L., Mc Cully, M.E., 1979. Histology of the development of the graft union in pea roots. Can. J. Bot. 57,
Strasburger, E., 1901. Über Plasmaverbindungen pflanzlicher Zellen. Jahrb Wiss Bot 36, 493–610.
Tiedemann, R., Carsens-Behrens, U., 1994. Influence of grafting on the phloem protein patterns in Cucurbitaceae.
I. Additional phloem exudate proteins in Cucumis sativus grafted on two Curcubita species. J. Plant Physiol.
143, 189–194.
Tiedemann, R., 1989. Graft union development and symplastic phloem contact in the heterograft Cucumis sativus
on Curcubita ficifolia. J. Plant Physiol. 134, 427–440.
Treutter, D., Feucht, W., 1988. Accumulation of the flavonoid prunin in P. avium/P. cerasus grafts and its possible
involvement in the process of compatibility. Acta Hort. 227, 74–78.
Van Sumere, C.F., Vande Casteele, K., de Loose, R., Heursel, J., 1985. Reverse phase-HPLC analysis of flavonoids
and the biochemical identification of cultivars of evergreen Azaela. The Biochemistry of Plant Phenolics, 25.
Clarendon Press, Oxford, pp. 17–44.
Walz, C., Giavalisco, P., Schad, M., Juenger, M., Klose, J., Kehr, J., 2004. Proteomics of curcurbit phloem exudate
reveals a network of defence proteins. Phytochemistry 65 (12), 1795–1804.
Walz, C., Juenger, M., Schad, M., Kehr, J., 2002. Evidence for the presence and activity of a complete antioxidant
defence system in mature sieve tubes. Plant J. 31 (2), 189–197.
Wang, Y., Kollmann, R., 1996. Vascular differentiation in the graft union of in vitro-grafts with different
compatibility. Structural and functional aspects. J. Plant Physiol. 147, 521–533.
Weatherhead, I., 1986. Causes of graft failure in Sitka spruce (Picea sitchensis-Bomg.-Carr.). Ph.D. thesis,
University of Reading.
Yeoman, M.M., 1984. Cellular recognition systems in grafting. In: Linkskens, H.F., Heslop-Harrison, I. (Eds.),
Cellular Interaction, Encyclopaedia of Plant Physiology, New Series, vol. 17. Springer-Verlag, Berlin, pp.
Yeoman, M.M., Kilpatrick, D.C., Miedzybrodzka, M.B., Gould, A.R., 1978. Cellular interactions during graft
formation in plants, a recognition phenomenon? Symposia of the Society for Experimental Biology XXXII,
Yeoman, M.M., Brown, R., 1976. Implications of the formation of the graft union for organization in the intact
plant. Ann. Bot. 40, 1265–1276.
Zajaczowski, S., Wodzicki, T.j., Bruinsma, J., 1983. A possible mechanism for whole plant morphogenesis.
Physiol. Plant 57, 306–310.