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Pak. J. Bot., 52(4), DOI: http://dx.doi.org/10.30848/PJB2020-4(10)
GRAFTING IN CONIFERS: A REVIEW
ALBERTO PÉREZ-LUNA1, CHRISTIAN WEHENKEL2, JOSÉ ÁNGEL PRIETO-RUÍZ3,
JAVIER LÓPEZ-UPTON4, SANTIAGO SOLÍS-GONZÁLEZ5,
JORGE ARMANDO CHÁVEZ-SIMENTAL2 AND JOSÉ CIRO HERNÁNDEZ-DÍAZ2*
1Programa Institucional de Doctorado en Ciencias Agropecuarias y Forestales. Universidad Juárez del Estado de
Durango, Km 5.5 Carretera Mazatlán, 34120 Durango, México
2Instituto de Silvicultura e Industria de la Madera, Universidad Juárez del Estado de Durango,
Km 5.5 Carretera Mazatlán, 34120 Durango, México
3Facultad de Ciencias Forestales, Universidad Juárez del Estado de Durango, Río Papaloapan,
Valle del Sur, 34120 Durango, México
4Colegio de Postgraduados, Km. 36.5 Carretera México Texcoco, Montecillo Estado de México C.P. 56230, México.
5 Instituto Tecnológico de El Salto. Mesa del Tecnológico s/n El Salto Durango, 34942 México
*Corresponding author’s email: jciroh@ujed.mx
Abstract
Grafting is one of the vegetative propagation methods most commonly used worldwide to preserve genotypes and
increase germplasm production. The method involves the insertion of a scion from one individual plant into a rootstock from
another individual to form a single plant. It has been widely used in fruit trees and hardwoods, but much less so in conifers.
Grafted trees are used to establish asexual seed orchards for producing forest germplasm and thus yield genetically
improved seed on a large scale. Sprouting processes (callus formation) in the grafted plant are affected by several factors,
the most important of which are the technique used, grafting season, phenological and physiological state of the scion and
the rootstock, taxonomic affinity between the organs, age of buds and rootstocks, microclimatic conditions of the site where
the grafts are maintained, and genetic, anatomical and histological differences between the grafted organs. On the other
hand, graft incompatibility can be caused by extrinsic or intrinsic factors. Grafting is also used to rejuvenate mature trees
(upper buds), and it is possible to shorten the process by applying growth promoting hormones. Good results have been
achieved with conifers in grafting tests conducted in the United States and some parts of Europe and Asia; however,
successful grafting and survival of conifer grafted rootstocks have not yet been achieved in Latin American countries.
Key words: Vegetative propagation, Conifer grafts, Asexual seed orchards, Forest genetic resources, Compatibility-
incompatibility of grafts.
Introduction
Forest genetic resources are socially, scientifically,
environmentally and economically important worldwide.
About 31% of the earth’s surface is covered by forests,
of which 93% are natural and 7% are planted forests.
The total number of tree species in the world is between
80,000 and 100,000, representing 12% of the total
biodiversity on earth (FAO, 2014). The growing demand
for forest products, as well as changes in forest land use
and the effects of climate change have led to forest
degradation (Chidumayo & Gumbo, 2013) and to an
increase in timber deficit in some countries, such as the
US, where wood imports have had to be increased
(Fiedler et al., 2001). The appropriate use of forest
genetic resources will help preserve, improve and
propagate species of high commercial value, providing
the industry with the timber resources it requires (Neale
& Kremer, 2011; Vargas et al., 2013; FAO, 2014;
Burney et al., 2015).
Grafting is the union of two plant organs, a scion,
bud or plectrum (aerial part) and a rootstock (underground
part), which continue to grow, thus generating a single
plant (Gil et al., 1986; Iglesias et al., 1999). Some authors
believe that grafting has been used for more than 3,400
years and that it was practiced by Eurasian peoples
(mainly in Mesopotamia), as well as by the ancient
Hebrews; however, the existing evidence is unclear
(Mudge et al., 2009). Nevertheless, the first documented
evidence of the use of grafting techniques dates back
more than 2,000 years in China, mainly involving species
of importance for producing fruit; a large body of
literature shows that successful grafting was achieved in
some species (González, 2004).
Propagating forest species through grafts enables the
preservation of desirable genotypes of high commercial or
ecological value; likewise, forest diversity can be
maintained and loss of genetic variety can be prevented or
reduced (Zobel & Talbert, 1984; Vargas et al., 2004).
Pike et al., (2018) pointed out the importance of
identifying superior individuals that are resistant to attack
by pests and diseases, and of propagating such individuals
by grafting. Once the scions of the superior individuals
are grafted, it is possible to establish asexual seed
orchards (ASOs) (Matziris, 2000; Koskela et al., 2014).
ASOs can be used to preserve genotypes and produce
high quality seed (Wright, 1976; Zobel & Talbert, 1984;
Matziris, 2000; Vargas et al., 2004), thus enhancing the
success of reforestation programs and commercial forest
plantations, as successful establishment of plantations will
help mitigate the degradation of natural forests (Fiedler et
al., 2001; Martínez & Prieto, 2011; Aparicio-Rentería et
al., 2013; Thompson et al., 2014). The first large-scale
study of conifer grafting was carried out in Corsica in
1820 (Jayawickrama et al., 1991). However, the
establishment of ASOs by grafting conifers for breeding
programs did not acquire great importance until the late
1940s in Sweden (Lindgren et al., 2008).
ALBERTO PÉREZ-LUNA ET AL.,
2
Information about the intrinsic and extrinsic factors that
influence graft survival in conifers is scarce (Gil et al., 1986;
Jayawickrama et al., 1991; González, 2004). The objectives
of the present study were therefore to review the
documentary information on the development of grafting
techniques in coniferous species and to report on the current
use of these. The overall aim was thus to contribute to
improving the propagation of clones of desirable conifers,
especially the genus Pinus, which is one of the most
important timber-producing groups worldwide (Martínez &
Prieto, 2011; Vargas et al., 2013; Burney et al., 2015).
The following main topics related to coniferous
grafting are addressed in this review article: grafting
techniques, taxonomic and anatomical affinity of the organs
used for grafting, age of the rootstock and scion, hydric and
hormonal stress, effects of cellular and vascular structures
(parenchyma, meristematic cells, cambial zone, resin
channels, xylem and phloem), effects of temperature,
greenhouse vs. non-greenhouse conditions,
microenvironment of the graft zone, protection of the
grafted area, fungi and possible diseases, prior treatment of
the rootstock and scion, and care of the plants after
grafting. Owing to the scarcity of information on the factors
influencing the compatibility of grafted conifers, the
present review also includes some reports on other
gymnosperm and hardwood species, which may support
future investigations on conifers.
Use of grafting to establish asexual seed orchards
(ASOs) of the genus Pinus: Grafted trees are the main
source of vegetative material used to establish ASOs of
different forest species of interest, in which it is possible
to carry out controlled pollination, with the aim of
generating genetic gains in the progeny obtained through
controlled crosses in the orchard (Nienstaedt, 1965; Zobel
& Talbert, 1984; Jaquish, 2004). Likewise, ASOs can be
used to produce seeds of species that only flower once in
a while (Martín & González, 2000; Prieto & López, 2006;
López et al., 2011).
Establishment of ASOs enables vegetative material
of high genetic quality to be used as scions and thus
produce grafts that may be converted into second
generation orchards, or even more advanced generations
(Medina et al., 2007). Three sources of different
genotypes can be considered: 1) the parent tree from
which the buds are collected for grafting to establish the
first generation ASO; 2) the plants from the first
generation ASO seeds that will be used as the rootstock
and will serve to establish the second generation ASO;
and 3) the bud used as the graft. It is also possible to
reduce the time required for seed generation in second
and later generation ASOs by applying appropriate
methods (Lott et al., 2003; Medina, 2005).
ASOs can potentially be used as sources of seed in
reforestation programs (Byram et al., 2001; Jaquish,
2004). In addition, ASOs are reservoirs of forest genotypes
that can be used to gain greater control over the
information and genetic composition of the clones
included (Jaquish, 2004; Loo, 2004). However, a wide
variation in fertility has been observed in several ASOs,
and in some less than 50% of the clones are seed producers
(Danbury, 1972; Schmidtling, 1983a). Cone production
was observed in 94% of grafted Pinus elliottii Engelm.
trees in an ASO established in Mississippi, during the first
year of establishment (Gooding et al., 1999).
In addition to the above, it is important to establish
ASOs in high quality sites, as it has been observed that
Pinus pinaster Ait. seed produced in ASOs established in
high quality sites in Spain was more likely to germinate
than seed from poorer quality sites (Cendán et al., 2013).
Establishing ASOs of Pinus caribaea var.
hondurensis (Sénéclauze) Barret and Golfari., Pinus
oocarpa Schiede ex Schltdl. and Pinus patula Schiede ex
Schltdl. et Cham. acquired great importance in the 1980s
and 1990s in countries such as Brazil, Zimbabwe,
Australia and Venezuela (Valera et al., 1992; Pottinger,
1994; Valera et al., 1997). Clones of Pinus radiata D.
Don grown in ASOs established in Spain, New Zealand
and Australia have shown great potential for genetic gain,
as well as substantially increased seed production
(Pascual et al., 2000; Baltunis & Brawner, 2010).
Flowering was observed to be more intense in clones
produced by heteroplastic (interspecific) grafts than in
those produced by homoplastic (intraspecific) grafts in an
ASO in Guadalajara (Spain) (Climent et al., 1997).
However, flowering was much lower in clones of Pinus
contorta var. latifolia Dougl. in an ASO than in trees of
the species in natural stands (Wheeler et al., 1982). It has
been suggested that for some pine species, the
establishment of 20 ASO clones should be considered to
optimize genetic gain and decrease the risk of self-
fertilization (Lindgren & Prescher, 2005).
In Turkey, pollen production was lower in a Pinus
brutia Ten. ASO than in Pinus nigra J.F. Arnold and
Pinus sylvestris L. ASOs, and age was found to be an
important factor in the variable pollen production, as the
P. brutia ASO was the youngest ASO in the country
(Bilir et al., 2002). On the other hand, seed production
was higher in a P. sylvestris ASO in Turkey than in
orchards of the same species established in Sweden
(Sivacioğlu, 2010).
In several progeny trials with seed produced in a
Pinus halepensis Mill. ASO in Greece, significant
differences in the genetic gain between the different
families involved in the germplasm production were
observed (Matziris, 1998; Matziris, 2000). However, in
Norway, plants produced with seed from an ASO were
more susceptible to cold, and the mortality rate was
higher than that of the plant produced with seed from
natural stands (Johnsen, 1989).
Due to the low growth yields of plants produced from
seed obtained in natural stands of Pinus armandii Franch.,
a genetic improvement program was implemented in
China to establish ASOs by grafting (Wang, 2004).
Furthermore, Pinus koraiensis Siebold & Zuccarini ASOs
were successfully established in the north of China, North
Korea and South Korea (Wang et al., 2000; Wang, 2004).
In Mexico, ASOs of the main commercial species,
including Pinus douglasiana Martínez, P. greggii var.
australis, P. patula, P. arizonica Engelm., P.
pseudostrobus Lindl., P. teocote Schiede ex Schltdl.,
Cedrela odorata L., Cupressus lusitanica Mill.,
Eucalyptus camaldulensis Dehnh., Hevea brasiliensis
(Willd. ex A. Juss.) Müll. Arg., Jatropha platyphylla
Müll. Arg. and Swietenia macrophylla King., have been
established (López et al., 2011; Rodríguez, 2013).
However, despite attempts to establish dense ASOs with
diverse families, the planting density of these orchards is
GRAFTING IN CONIFERS. A REVIEW
3
often low due to high mortality during the grafting stage
(Aparicio-Rentería et al., 2013); likewise, in general, it
has not been possible to carry out the massive
reproduction of improved forest germplasm (Aparicio-
Rentería et al., 2013; Rodríguez, 2013).
In forest genetic improvement programs that involve
establishing ASOs, action plans must be designed to
mitigate any damage that may be caused by natural
phenomena and to minimize loss of seed production. It is
also necessary to design strategies to prevent, as far as
possible, economic losses such as those incurred in
Mississippi in 2005, when hurricane Katrina affected 12
ASOs in the region (Byram et al., 2005).
Grafting in conifers: Grafts and cuttings can be used to
propagate superior conifer trees (Cuevas-Cruz et al.,
2015). However, it is difficult to propagate conifers using
shoots from superior mature trees selected in the field
(Medina et al., 2007), and it is therefore preferable to use
grafting techniques in breeding programs (Holst et al.,
1956; Barnes, 1974).
The need to establish precise protocols has been
highlighted in relation to achieving successful grafting in
conifer species (Mencuccini et al., 2007). These authors
identified several variables that affect graft survival of
these species in the short term (less than two years),
although the influence of these variables disappeared in the
medium and long term (more than two years). The
following variables are most commonly considered: quality
of the rootstock, environmental conditions during grafting,
post-graft cultural activities, hormonal conditions of the
organs to be grafted before and after grafting, and the
taxonomic and anatomical affinity between the scion and
the rootstock (Holst, 1956; Ahlgren & Wilderness, 1972;
Jayawickrama et al., 1991; Valdés et al., 2003a).
Grafting techniques: The grafting techniques most
commonly used in conifer species are terminal fissuring
and lateral plating (Staubach & Fins, 1988; Muñoz et al.,
2013). Lateral plating consists of maintaining the
complete rootstock and making a longitudinal cut where
the scion is inserted (Fig. 1(a)). In the scion, a long cut (3
to 5 cm) is made at the end to be inserted (Fig. 1(b)); a
smaller cut (approximately 0.5 cm) is subsequently made
opposite to the first cut. The length of the cut on the
rootstock should coincide with the length of the long cut
of the bud being grafted. To make the graft union, both
cuts are joined, so that the scion is held firmly on the
rootstock. Once both parts are joined (Fig. 1(c)), the graft
union is tied up with a rubber band and the area is then
sealed with fungicide mixed with vinyl paint. In some
studies, resin-based healing wax is used to seal the graft
union (Fig. 1(d)) (Staubach & Fins, 1988; Muñoz et al.,
2013; Pérez, 2016).
The terminal fissure technique, described by
Staubach & Fins (1988), Muñoz et al., (2013) and Pérez
(2016), involves making two longitudinal cuts parallel to
the cambium on the opposite side of the scion (Fig. 2(a)).
For preparation of the rootstock, a transverse cut is made
in the cambium, eliminating the upper part of the stem,
and a longitudinal (3 to 4 cm) is then made in the in the
middle of the rootstock stem (Fig. 2(b)). As in the lateral
plating graft, the graft union is secured with a rubber
band, and sealed with vinyl and fungicide paint, to
prevent contamination and attack by fungi in the grafted
area (Fig. 2(c)). In some cases, the mooring is covered
with Campeche wax during the grafting.
In some species of the genera Pinus and Larix, good
results have been obtained with the terminal fissure
grafting (Staubach & Fins, 1988; Gallardo & Gallardo,
1991; Ávila & Pompa, 2008). However, the lateral plating
technique seems to be more successful with caespitose
species of the genus Pinus (Pérez, 2016). In an
experiment carried out in Scotland the lateral plating
technique was successfully applied in homoplastic
grafting (see section 4) of Pinus sylvestris (Vanderklein et
al., 2007). In China, in trials with Pinus koraiensis, lateral
plating was successfully used in homoplastic grafting,
whereas the terminal fissure technique yielded better
results in heteroplastic grafting of Pinus ponderosa
Douglas Ex C. Lawson buds on Pinus tabuliformis Carr.
rootstocks (Zhang & Tang, 2005; De-li et al., 2007).
Fig. 1. Lateral plating grafting process. (a) Preparation of the
rootstock for grafting; (b) the cut bud used for grafting; (c)
lateral plating graft assembly; (d) mooring of the graft and
application of fungicide. Photos: Alberto Pérez Luna (2016).
Fig. 2. Terminal fissure graft process. (a) Preparation of bud for
grafting; (b) preparation of rootstock for grafting; (c)
assembling, tying and sealing the terminal fissure graft. Photos:
Alberto Pérez Luna (2016).
ALBERTO PÉREZ-LUNA ET AL.,
4
Grafting adventitious buds has recently been used in
Sweden with the genera Abies and Pinus. This technique
involves grafting small buds of less than two years of
age onto rootstocks of smaller diameter than necessary
in grafts of lateral plating and terminal fissure (Hajek,
2008; Mahunu et al., 2010). Grafting adventitious buds
enables multiple shoots to be inserted in the same
rootstock, thus reducing the time until seed production
in clones established in ASOs (Khattak et al., 2002;
Pomper et al., 2009).
Physiological characteristics of the grafted organs
Taxonomic affinity: Grafting can be homoplastic or
heteroplastic. In homoplastic grafting, the buds and
rootstock used are from the same species and variety,
while in heteroplastic grafting, they are from different
species or even genera. The taxonomic affinity of the
species used in heteroplastic grafting is an important
factor to take into consideration, as the yield from this
method tends to be lower than in homoplastic grafting
(Ahlgren & Wilderness, 1972; Gil et al., 1986; Climent et
al., 1997). Variable results have been obtained with
heteroplastic grafting, with compatibility, semi-
compatibility and incompatibility observed (Ahlgren &
Wilderness, 1972; Climent et al., 1997), as with grafting
buds of the genus Pinus onto rootstocks of Abies
balsamea (L.) Mill. (Ahlgren & Wilderness, 1972). In a
trial of grafts of Pinus pinea L. rootstocks with buds of
Cedrus libani A. Rich., carried out in winter, survival was
more than 50% (Barnes, 2005).
Good results were obtained for buds of Cedrus
atlantica (Endl.) Manetti ex Carrière grafted on Pinus
strobus L. rootstocks, thus compensating for the difficulty
in using Cedrus rootstocks due to the deficient formation
of root systems in this genus (Barnes, 2008). In a grafting
study carried out in Guadalajara (Spain), Pinus nigra
material was used as rootstock for heteroplastic and
homoplastic grafting of Pinus nigra and Pinus brutia;
homoplastic grafting yielded the best results (Climent et
al., 1997). Mutke et al., (2003) reported the existence of a
clone bank of homoplastic grafts of Pinus pinea in
Valladolid (Spain). Scions of Pinus patula were
successfully grafted on Pinus douglasiana and Pinus
pseudostrobus rootstocks in Mexico, with better results
than the P. patula / P. douglasiana combination
(Villaseñor & Carrera, 1980).
Vigour and asepsis: An important factor to consider in
grafting is the sanitary state and vigour of the buds used,
because the grafted plants are more likely to survive if the
material used is in optimal condition (Gil et al., 1986;
Upchurch, 2009). Similarly, it is essential to use
rootstocks with healthy and robust roots (Holst et al.,
1956; White et al., 1983). The characteristics of the scion
and the rootstock are important for grafting success, and it
is therefore necessary to use vegetative material of good
phenotypic quality (White et al., 1983; Melchior, 1984).
Age and origin of scion and rootstock: The age of the
buds and rootstock plants are important for grafting
success. For Pinus radiata and P. arizonica, better
sprouting and survival results were obtained with
rootstocks of less than two years of age (Moncaleán et al.,
2006; Ávila & Pompa, 2008). On the other hand,
Staubach & Fins (1988) successfully grafted buds of trees
of a Larix species of approximate age 50 years.
Furthermore, no significant differences in grafting success
were observed with buds obtained from P. sylvestris trees
of ages ranging from 36 to 269 years (Vanderklein et al.,
2007). Good results have been obtained with buds from 6
to 12-year-old Abies fraseri (Pursh) Poir. trees (Hinesley
et al., 2018) and with buds from 33-year-old Araucaria
angustifolia (Bertol.) Kuntze trees (Gaspar et al., 2017).
The buds used for grafting must be obtained from
superior trees, so that the grafted trees inherit high genetic
gain in the future production of seeds in ASOs (Lott et al.,
2003; Venturini & Lopez, 2010). Superior conifer trees
are considered to be those of dominant height, straight
stem, desirable natural pruning, small crown occupying
less than one third of the total height, insertion of
branches at an angle close to 90°, and with no damage
caused by pests and diseases (Prieto & López, 2006).
These types of characteristics are detected when the trees
reach maturity, once the stems and branches clearly show
their definitive physiognomy (Castellanos-Bolaños et al.,
2008; EUROPARC-Spain, 2015).
Coniferous graft yield in different environmental and
protection conditions
Environmental effects: In the processes of grafting
specimens of the genus Pinus, some environmental factors
cause low rates of sprouting and survival, and some
intrinsic factors in the species can lead to incompatibility
between the grafted organs (Cuevas, 2014).
Grafting can be carried out in winter, when the scion
is dormant; this has the advantage that the scion remains
turgid for a longer time after it is extracted from the
parent tree. Grafting can also be carried out in summer,
when the scion has resumed its vegetative activity;
however, in some species the results are usually less
effective than those obtained in winter (Gil et al., 1986;
Salvo et al., 2013). For grafting Araucaria angustifolia,
the best results were obtained with dormant scions
(Gaspar et al., 2017).
At mean temperatures below 12°C, graft survival was
35% in Pinus patula (Aparicio-Rentería et al., 2013) and
less than 5% in P. leiophylla Schiede ex Schltdl. et Cham.
(Cuevas, 2014) and P. durangensis Martínez (Pérez,
2016). It is therefore advisable to carry out grafting trials
at different times, to determine the optimum climatic
conditions for each species (Aparicio-Rentería et al.,
2013; Cuevas, 2014; Pérez, 2016). In the UK,
experimental grafting of Pinus sylvestris was carried out
by maintaining controlled conditions in the greenhouse,
yielding good results (Mencuccini et al., 2005).
Grafting when daytime temperatures are below 24°C
(and preferably when the night-time temperature is
around 8°C) has been recommended to avoid breaking the
dormancy state in the buds (Upchurch, 2009). In an early
study, it was suggested that in the northern hemisphere
grafting conifers was possible at any time of the year,
although it was recognised that survival rates are highest
in winter and spring (Nienstaedt, 1965).
GRAFTING IN CONIFERS. A REVIEW
5
In a grafting trial with Pinus patula in Mexico,
better sprouting results and higher survival were
obtained in the nursery than in the greenhouse, because
of difficulties in maintaining a constant temperature
inside the greenhouse (Villaseñor & Carrera, 1980).
Unfortunately, no further information regarding the
environmental effects was provided.
Protection of the graft union: In a grafting trial of Pinus
resinosa Sol. Ex Aiton, four graft protection treatments
were evaluated, along with a control (no protection):
microclimate induced by polyethylene bags; protection
with kraft paper bags; a combination of polyethylene
microclimate and kraft paper bag; and protection with
cardboard cylinders (Holst, 1956). The best results for
grafting and graft survival were obtained with the
combination of polyethylene bag microclimate and kraft
paper protection, while protection with cardboard
cylinders and control (no protection) yielded the lowest
percentage of sprouting and survival. In an experimental
grafting trial with Pinus taeda L., in Alabama (US), in
which the graft (scion plus graft union) was entirely
covered with paraffin as the only means of protection, the
graft survival rate was 90%, and the technique was
reported to be very economical (White et al., 1983).
Due to the high temperature generated inside the
polythene bags used to protect the graft, contact between
water and the regenerating area of the graft should be
prevented when the plants are watered. Use of
fungicides is also recommended to prevent proliferation
of fungi in the grafted area (Ávila & Pompa, 2008;
Bioforest, 2011; Muñoz et al., 2013). In addition to
optimizing the grafting process, acclimatization of the
grafted plants should also be optimized before the
planting out, to help maximise survival of the clones in
the final plantation site (Salvo et al., 2013).
Graft compatibility-incompatibility: In several studies,
the clones died two to three years after grafting and even
after establishment in the field. The genetic, technical and
cultivation factors that cause this apparent late
incompatibility in grafts must be determined (Valera et
al., 1997; Güçlü, 2019). Graft incompatibility can be
divided into localized and translocated incompatibility
(Mosse, 1962). Localized incompatibility refers to the
lack of coincidence (in size or taxonomy) between the
grafted organs, while translocated incompatibility
depends on factors not related to the characteristics of the
scion or the rootstock and that are mainly caused by
inadequate application of the grafting techniques.
Localized incompatibility in Pinus radiata grafts in New
Zealand was observed, with no coincidence between the
cambium of the scion and the cambium of the rootstock
during grafting, thus hindering graft healing (Sweet &
Thulin, 1973). On the other hand, translocated
incompatibility has been observed in several trials, due to
phloem damage when the grafted organs are cut, causing
their degeneration and short- and long-term graft
mortality (Sweet & Thulin, 1973; Hartmann et al., 2002).
In a study carried out on eight-year-old Pinus taeda L.
grafts, the number of strobili, number of cones produced
and the height and normal diameter of the clones were
related to variables such as the collection site of the buds,
tree of origin and the trees used as rootstocks, and it was
found that the yield of the grafts depended to a great extent
on the site and tree of origin, while the rootstock was not as
important for adaptation of the grafts (Jayawickrama et al.,
1997). Genetic incompatibility between the buds and the
rootstocks used for grafting Araucaria cunninghamii Aiton
ex D. Don. was observed as the parent trees of the seed
with which the rootstocks were produced and the donor
trees of the buds to be grafted had different genetic loads
(Dieters & Haines, 1991).
For grafting Pinus taeda with rootstocks of Abies
spp. and P. taeda, the rootstock condition influenced the
height growth and fecundity of the clones obtained, with
better sprouting and survival obtained when the first
genus was used as rootstock (Schmidtling & Scarbrough,
1970; Schmidtling, 1983b).
Compatibility due to the anatomy and histology of
grafts: The anatomical and histological affinity of the
organs to be grafted is an important factor that determines
the compatibility or incompatibility of grafts (Barnett &
Miller, 1994; Kankaya et al., 1999; Castro-Garibay et al.,
2017; Pérez-Luna et al., 2019). The effect of the resin on
the graft union has been analyzed in some studies, and
various authors have stated that it only functions as a
means of temporary fusion, which may protect against
fungal attack and moisture loss (Noel, 1968; Tiedeman,
1989; Mahunu et al., 2012). The meristematic activity of
the cambium (between the scion and the rootstock) has
been considered an important factor in the success of
grafting, and it has been suggested that the graft
incompatibility may be due to deficient contact between
the cambium of the grafted organs (Yeoman, 1984;
Tiedemann, 1989; Hartmann et al., 2002). Parenchymal
cells are formed at the moment of contact between the
cambial zones of the rootstock tissues and the grafted bud,
which is important for photosynthesis, nutrient reserve
and protection of the xylem and phloem (Hartmann et al.,
2010). Likewise, during callus formation, new xylem and
phloem are formed, thus enabling the formation of
vascular tissue that completely connects the grafted
organs (Moore & Walker, 1981a, 1981b; Pina & Errea,
2005). Unfortunately, little is known about the effect of
meristematic cell activity on grafts of conifer species
(Jayawickrama et al., 1991; Hartmann et al., 2010).
During the fusion of the cambial areas of the scion
and the rootstock, three important stages are recognized
in grafting: callus formation, cambial differentiation and
cambial continuity (formation of vascular tissues)
(Moore, 1984; Tekintas, 1991; Polat & Kaska, 1992;
Tekintas & Dolgun, 1996). In Prunus domestica subsp.
insititia (L.) C.K. Schneid., cambium cells joined 60
days after grafting, in the process of callus formation,
giving rise to the process called “cambial continuity”
(Dolgun et al., 2008). By contrast, in heteroplastic
grafting of Prunus domestica subsp. insititia and Prunus
dulcis (Mill.) D.A. Webb, the cambial zone merged
within 45 to 60 days after grafting (Tekintas & Dolgun,
1996). However, some studies of woody species have
shown that incompatibility can develop over several
years, indicating the possible presence of vascular tissue
that helps the survival and growth of incompatible grafts
(Mosse, 1962; Pina & Errea, 2005).
ALBERTO PÉREZ-LUNA ET AL.,
6
Some theories about the activity in the cambial zone
during the grafting process have been proposed. Thus, it
has been suggested, on the basis of anatomical studies,
that the cell walls of grafted organs are diluted during
callus formation, allowing contact between plasma
membranes and the subsequent secretion of proteins,
generating an effect called "catalytic complex". It has also
been suggested that graft compatibility depends on the
formation of this complex and that incompatibility occurs
in its absence (Yeoman & Brown, 1976; Yeoman et al.,
1978; Jeffree & Yeoman, 1983). However, other authors
have argued that it is impossible to determine how the
catalytic complex is formed due to the poor visibility of
the cell walls during callus formation (McCully, 1983;
Moore, 1983).
Effect of concentration and application of hormones in
grafting: For grafting in conifers, incompatibility has
been found to be mainly caused by the difference in the
concentration of growth hormones in the grafted organs
(Coenen & Lomax, 1997; Valdés et al., 2003a, 2003b).
The most important growth hormones in plants are
auxins, gibberellins and cytokinins (Peng & Harberd,
2002; Rashotte et al., 2003).
Cytokinins have an important effect on the grafting
and / or graft incompatibility in coniferous species, as
they are of great importance in cell division and
regeneration, promoting sprouting and activation of
axillary buds (Kato et al., 2000; Valdés et al., 2003a;
Jordán & Casaretto, 2006).
Cytokinin levels measured in Pinus radiata were
higher in individuals younger than 30 years and the
concentration was highest in 9-year-old specimens
(Valdés et al., 2003a). Axillary buds from individuals
with high concentrations of cytokinins favoured graft
adaptation and survival (Valdés et al., 2003a).
In a later study using molecular markers to identify
juvenile genotypes with a high level of maturation in
Pinus radiata trees, the cytokinin levels decreased
considerably with maturation (Valdés et al., 2003b).
The cytokinin concentration was much higher when
grafting organs originated from old trees, indicating
that rejuvenation was achieved at physiological level
and of the endogenous hormonal content (Valdés et al.,
2003a, 2003b).
Several authors have pointed out that cambial
differentiation between the scion and the rootstock, giving
rise to cambial continuity subsequent to grafting, is due to
the secretion of auxins present in the vascular tissues
(Sachs, 1981; Moore, 1984).
The application of gibberellins in grafts with low
production of male and female strobili promotes
flowering (Ross, 1976; Chalupka, 1981; Wheeler et al.,
1982; Hare, 1984; Ross, 1990). In a study in which
gibberellins GA4/7 and auxins were applied in the form of
naphthaleneacetic acid (NAA) to grafts of Picea
engelmannii Carr., more female strobili were produced
when concentrations of 125 to 625 μg / spray of GA4/7 and
without NAA were used, with cone production reaching
48% of the individuals included in the treatment (Ross,
1990); in addition, a dose of NAA of 5 μg/spray was toxic
for the female structures, but male flowering was
favoured by the application of GA4/7 and NAA at the
doses indicated above (Ross, 1990).
When GA4/7 and GA5 were applied at a dose of 100-
200 μg/spray to grafts of Pseudotsuga menziesii (Mirb.)
Franco, flowering of male strobili increased by 80 and
65%, respectively; however, production of female strobili
was only significantly affected by application of GA4/7,
reaching 55% (Ross, 1976). Flowering was more intense
in Pinus taeda and Pinus elliottii var. elliotti Engelm.
when GA4/7 was applied at a dose of 200 μg in 0.1 mL of
50% ethanol than when no NAA was applied; flowering
was 69 and 62% for P. taeda and P. elliottii, respectively
(Hare, 1984). Likewise, flowering in grafted Pinus
sylvestris trees was superior when 400 mg/mL in 50%
ethanol was applied without NAA, with female and male
strobili produced in almost 40% of the treated grafts
(Luukkanen & Johansson, 1980).
In an ASO with five- to seven-year-old grafted trees of
Pinus strobus, only 7.5% of the individuals developed male
strobili, and none of the clones produced female strobili.
Gibberellins were applied, accelerating the sprouting of
strobili within a year, with 38% of the clones producing
female strobili, and 47% male strobili (Pijut, 2002).
Further studies are needed to determine the effect of
hormonal concentrations in grafted conifers, thus helping
to improve the propagation of superior forest genotypes
(Coenen & Lomax, 1997; Valdés et al., 2003a, 2003b).
Final considerations: Advances in grafting as a means of
vegetative propagation have been widely reported, mainly
for fruit trees, vegetables and some hardwood forest
species; however, studies of grafting in conifers are
scarce. Researchers in the areas of plant physiology and
forest genetic resources should give priority to vegetative
propagation, by grafting economically, ecologically and
socially important conifer species, thereby also helping to
reduce the risk of loss of genetic diversity. Studies of
graft compatibility and incompatibility in conifers due to
genetic, anatomical and histological factors are also
necessary. Furthermore, the characteristics of the
rootstocks used for grafting diverse species of interest
must be identified, considering the following aspects:
seed origin for the production of rootstocks, volume and
type of substrate used in root production, as well as age,
height and rootstock diameter at the time of grafting.
Research should focus on defining methods that guarantee
grafting success, taking into account both favourable
factors and the limitations of the sites where actions for
the conservation and propagation of forest genetic
resources are intended to be carried out, through the
establishment of ASOs.
Funding: This work was financially supported by the
Consejo Nacional de Ciencia y Tecnología [CONACYT,
441054]; and Consejo de Ciencia y Tecnología del Estado
de Durango [COCYTED-12/02/18/265].
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(Received for publication 24 September 2018)