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Why should we investigate vegetable grafting?

Article  in  Acta horticulturae · June 2015

DOI: 10.17660/ActaHortic.2015.1086.1

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Why Should We Investigate Vegetable Grafting?

F. Pérez-Alfoceaa
Department of Plant Nutrition
CEBAS-CSIC
Murcia
Spain

Keywords: food security, sustainable agriculture, fruit quality, new cultivars, R×S×E,
new applications, transgrafting, societal and environmental challenge

Abstract
Agricultural productivity must increase by 60% to feed the expected
population of 9.6 billion people in 2050, and must be achieved through a socio-
environmental sustainability of the natural resources. However, vegetable
production around the world is being increasingly hampered by the unfavourable
soil and environmental conditions that include abiotic constraints such as drought,
extreme temperature, salinity, flooding, low nutrients, organic and heavy metals
contamination, as well as biotic ones assoil and air-borne pests and diseases. This
situation is aggravated by successive cropping, environmental policies, as the phase-
out of the chemical soil disinfectants, and negative impacts of climate change. While
genetic breeding cannot always provide efficient solutions, vegetable grafting has
developed very quickly in the last 50 years, mainly to induce shoot vigor and to
overcome soil borne diseases in susceptible crops, as a surgical alternative to
breeding. However, both the development of new rootstocks and new applications in
agriculture for crop improvement are hampered by the limited knowledge existing
on the physiological and genetic mechanisms underlying rootstock × scion
interactions × environment interactions. A major goal of research in vegetable
grafting should be gaining sound understanding about the physiological and genetic
basis of those interactions and the agronomic performance of rootstock-mediated
traits in order to establish a solid scientific basis for developing efficient rootstocks,
grafting technologies and management practices for different horticultural species
and specific environments. Scientific and technical collaboration will further
contribute to a wider development and exploitation of vegetable grafting towards
socio-economic-environmental sustainable agriculture and food security.

INTRODUCTION
Even though the benefits of using grafted seedlings are now fully recognized
worldwide, it has long been considered as an empirical process and more as a craft secret
than science. The need to understand the scientific basis of grafting-mediated crop
improvement has prompted in the most recent two decades many scientific actions aiming
at filling the gap between empiricism and science. The number of scientific publications
using grafting as an approach has drastically increased since 1992 (see Colla (2010) for
details), in accordance with the number of grafted seedlings produced worldwide.
Nowadays, many scientists employ grafting between different vegetables to (1) improve
understanding of how root-to-shoot signalling alters scion physiology and phenotype; (2)
study specifically how the root system responds to different stresses, and how these
responses affect plant adaptation; (3) gain expertise in using grafting to solve phyto-
pathological and agronomic problems such as soil-borne diseases or abiotic constraints;
and (4) alter positively fruit quality parameters.
Important efforts are being made through different international initiatives to
compile this scattered pre-existing knowledge in order to build-up a global vegetable-
                                                            
a
alfocea@cebas.csic.es

Proc. Ist IS on Vegetable Grafting 21

Eds.: Zhilong Bie et al.
Acta Hort. 1086, ISHS 2015
 

grafting community and to link this knowledge to new genetic, physiological and
agronomic information, thereby contributing to better selection and exploitation of the
available genetic variability in rootstocks, and generation of new variability through
genetic and biotechnological breeding approaches. Several comprehensive reviews on
grafting have compiled existing information about historical aspects and the current state
of the art in herbaceous vegetable and ornamental plants, including practical and
agronomical aspects such as implementation, rootstocks, species and crop performance
(Lee and Oda, 2010). Other studies are partially focused on very specific aspects of root-
to-shoot communication (hydraulics and hormones) in vegetables (Ghanem et al., 2011;
Pérez-Alfocea et al., 2010, 2011), genetics and breeding (King et al., 2010), response of
grafted plants to salinity (Colla et al., 2010), nutrient and heavy metals stresses (Savvas et
al., 2010), thermal stress and organic pollutants (Schwarz et al., 2010), pathogens (Guan
et al., 2012; Louws et al., 2010) and fruit quality (Rouphael et al., 2010). Based on the
available data on the literature, it can be stated that the use of adequate rootstocks is an
efficient strategy to increase the yield stability and sustainability of the intensive
horticulture, and that it has an enormous potential for contributing to food and
environmental security. As American farmers say, “there’s not only a market for it,
there’s a great need for it”, where the ‘need’ not only implies benefits for agriculture, but
indirectly also for the environment and the society.
Rootstocks can contribute to increasing yield stability and sustainability in
vegetable crops through (i) increasing the yield potential of elite cultivars; (ii) filling the
yield gap under biotic (i.e. fungi, bacteria, virus, nematodes) and abiotic (i.e. salinity,
drought, low nutrients, extreme temperatures, soil compaction) stress suboptimal
conditions; (iii) decreasing the use of chemical (pesticides and fertilizers) and
contamination in soil and aquifers; (iv) increasing the efficiency of use of natural (water
and soil) resources; and, therefore, (v) optimizing crop productivity. The socioeconomic
and environmental potential impact of grafting is as broad as the genetic variability able
to cross the barrier between the rootstock and the scion. However, only through
understanding the mechanisms underlying the agronomical phenotypic variability
resulting from rootstock × scion × environment interactions will allow further
development and exploitation of rootstocks for increasing yield stability and sustainability
in horticultural crops. The results obtained so far are very promising, but more research
must be focus on (i) germplasm identification and rootstock breeding; (ii) rootstock-
mediated mechanisms regulating shoot growth; (iii) physiological and genetic
mechanisms involved in (a)biotic stress resistance; (iv) optimization of management
practices; (v) rootstock influence on fruit quality; (vi) generation of new (epi)genetic
variability and understating the mechanisms involved; (vii) use of biotechnological
approaches as transgrafting; and (viii) increasing grafting use efficiency.

GERMPLASM IDENTIFICATION, ROOTSTOCK BREEDING AND

EXPLOITATION
The success of vegetable grafting has been possible thanks to the use of
germplasm existing in other wild relative species through the generation of interspecific
rootstocks, thus providing a direct and efficient surgical alternative to breeding. In the
case of tomato, those rootstocks have been mainly developed by crosses between the
domestic Solanum lycopersicum and accessions from the wild species S. habrochaites and
S. pimpinellifolium. Those species provide vigorous root systems and resistance to soil
borne pathogens (nematodes, fungi, bacteria and viruses), thus allowing a higher
productivity under suboptimal environmental conditions. The interest shown by seed
companies and scientists in developing new rootstocks is increasing by exploring new
exotic germplam into the Solanum genus, such S. pennellii and more recently S. torvum
and S. aethiopicum.
However, the potential impact of rootstocks and grafting in food security is
enormous, since it can be rapidly implemented to enhance productivity and disease
resistance of high-value vegetable crops by exploiting a huge amount of genetic

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variability. Indeed, it is expected that the major development of rootstocks will occur in
Solanaceae, Cucurbitaceae and other annual crops including other families such as
Fabaceae (soybean, peanut), Asteraceae (artichoke) and Euphorbiaceae (cassava). Both
Solanaceae and Cucurbitaceae include 98 and 125 genera and 2700 and 960 species,
respectively, with additional accessions and ecotypes. More than 1000 million tons of
vegetables are produced annually in the world, with around 53 million hectares cultivated
(FAOSTAT, 2010). Many of them are either grafted or can be grafted. Much more well-
performed screening for specific environments, development of hybrid combinations and
graft-compatibility studies are required.

REGULATION OF SHOOT GROWTH AND ADEQUATE CULTIVARS

Altering rootstock cultivar to adjust shoot vigour (by using invigorating and
dwarfing rootstocks in herbaceous and woody species respectively) has been a classic
contribution of grafting to improve crop productivity and sustainability. For example, the
use of dwarfing rootstocks has dramatically increased the profitability of fruit production
by reducing costs and chemical use and by allowing increased planting density (Prassinos
et al., 2009). However, how growth and developmental processes are regulated in the
rootstock-scion interaction and how changes in vigor are transmitted between both
genotypes are open questions. One hypothesis is that rootstock-induced vigor may be
caused by signals such as water, nutrients and especially hormones and nucleic acids that
move through the graft union to affect scion growth. In support of this hypothesis, a
significant number of mobile macromolecules can move through the vascular system, and
more than 800 small organic compounds from different biochemical groups have been
detected in the xylem sap of grafted tomato plants (Albacete et al., 2014, and references
therein cited). Larger signaling molecules such as proteins or RNAs can also move
through the graft union and small differences in the availability of those signals or their
receptors/targets can alter gene expression and shoot growth (Kim et al., 2001; Mallory et
al., 2003). Interestingly, rootstock-induced vigor provokes a transcriptional response in
the scion similar to that of hybrid vigor, suggesting (i) a common genetic/physiological
basis of plant-growth promotion (Cookson and Ollat, 2013) and/or (ii) that the
invigorating signal can be synthesized in the roots and transported to the shoot when the
rootstock is a hybrid. This field provides huge opportunities in basic research with
enormous potential in rootstock breeding for modulating growth/vigour depending on the
cultivars and growing conditions.

IDENTIFICATION OF RESISTANCES AND TOLERANCES

The management of soil-borne pathogens is becoming more and more complicated
due to the increasing restrictive policies in the use of fumigants since the Montreal
Protocol established the phase-out dates for the production and use of methyl bromide by
2005 for developed countries and 2015 for developing countries (Batchelor, 2004; Savvas
et al., 2011). Grafting susceptible cultivars onto resistant rootstocks to important soil-
borne pathogens and using this technique into integrated crop management systems has
proven to be an environment-friendly alternative to soil fumigation with methyl bromide
(Davis et al., 2008; Rivard and Louws, 2008). Nowadays, grafting is an important
integrated pest management strategy able to control about thirty different pests and
pathogens of Solanaceous and Cucurbitaceous crops (see Guan et al., 2012; Louws et al.,
2010); for reviews). Important pathogens managed by grafting include fungal pathogens
such as Verticillium, Fusarium, Pyrenochaeta and Monosporascus; oomycete pathogens
such as Phytophthora; bacterial pathogens, particularly Ralstonia; root knot nematodes
(RKN) and several virus diseases (Louws et al., 2010). Grafting has also been
documented to impact foliar pests including pathogens, arthropods and viruses (Guan et
al., 2012). However, grafting onto resistant rootstock is more successful when it is
developed on the basis of an understanding of the complex nature of diverse biotic agents,
integrated pest management programs, farming systems research, local capacity for
transplant production, and legal regulations that may limit certain species as rootstock

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sources, but requires much more extensive and intensive work. Indeed, it is difficult to
separate the rootstock-mediated vigor and resistance effects. For instance, the 25-55%
yield increases in grafted melons affected by Fusarium were not only due to the disease
resistance but also especially to plant vigor maintenance during the late growing season
(Lee et al., 2010).
Besides the vigor or genetic resistance, the rootstocks have also the capacity to
provoke changes in the rhizosphere that can positively (association with beneficial
microorganisms) or negatively (changes in pathogenic variation of existing
microorganism and/or re-emergence of new ones) affect plant performance and crop
productivity (Gilardi et al., 2013; Pérez-Alfocea et al., 2011). It should be expected that
understanding the physiological and genetic mechanisms underlying this root × beneficial
microorganism interaction will contribute to incorporate new interesting traits to the
commercial rootstocks aiming at a better yield stability and soil sustainability.

CROP MANAGEMENT: USE OF FUMIGANTS, FERTILIZERS AND

IRRIGATION
A major problem of intensive farming practices with limited crop rotations is that
multiple cropping (3-4 crops per year) in the same greenhouse can lead to a build-up of
soil-borne pathogens and other deleterious factors to the plants, such as heavy infection,
increased salinity, extreme temperatures, humidity and radiation during the winter-
summer seasons, and lack of balanced fertilization (King et al., 2010). Indeed, a common
farming practice is the frequent application of a heavy amount of chemical fertilizers and
pesticides treatment to the high density plantations to obtain high crop yield and benefits,
which implies strong economic and environmental constraints.
Since grafted vegetables may alleviate some soil-borne pathogens and provide
more vigorous vegetative growth, crop management is also an important point to consider
in relation to improve fumigant, water and fertilizer use efficiency, in addition to
productivity. In the case of fumigants, the treatment must be considered not only in
relation to the yield between fumigated and non-fumigated fields, but also taking into
account the evolution of pathogen populations in the soil in order to make the appropriate
decision in the context of integrated practices. Rootstocks can also have useful properties
to absorb more water and nutrients through more efficient uptake systems and/or its
capacity to explore wider and deeper soil volumes. However, if those properties can be
transferred to increased yields or improved efficiencies in the use of those resources, this
requires well-designed studies on yield responses vs. a gradient of nutrient/water
application to the plant. For example, the accumulation of a given nutrient in the leaves
during vegetative growth is not an indicator of nutrient use efficiency, but should be
rather considered in relation to the total nutrient absorbed by the plant and the yield
produced.
Additionally, the vigour provided by the rootstock can be also managed in order to
optimize the use of water and nutrients as well as to balance the economic investment in
the grafted seedling, and it can be done through the control of the number of fruiting
stems or leaders. For example, a reduction in plant density may help to compensate for
the higher prices of grafted seedlings compared to non-grafted transplants. In Southeast
Spain the cost of grafted plants (including seeds of conventional cultivars) is about 0.62-
0.70 €, compared to 0.26-0.30 € of non-grafted seedlings. Therefore, the 2-fold increase
in seedling costs can be overcome by adequate crop management, as for instance
increasing the numbers of leaders per plant, as long as it is supported by the vigor of the
root system. The impact of the reduced plant density on the use of water and fertilizers
must be also properly addressed in many crops and in different cropping systems by
optimizing the vegetative/reproductive growth.

ROOTSTOCK INFLUENCE ON FRUIT QUALITY

The incidence of such ‘new roots’ on the fruit composition have been addressed in
terms of classical quality parameters such as minerals, °Brix, common sugars and organic

24
 

acids, pigments like lycopene and other carotenoids and some vitamins (Rouphael et al.,
2010). However, no attention has been paid so far to other minor organic compounds that
can be specifically produced by the new roots and transported to the fruits, which can
influence the nutritional, nutraceutical and toxicological properties of the fruits, being an
important factor to be considered in terms of food security, in addition to yield stability
under a changing environment.
A specially promising rootstock for tomato interspecific grafting is Solanum
torvum, a species native to the western tropics and India that tolerates the climatic
pressures of tropical regions (floods, drought, high temperature) and a wide range of soil
borne pathogens, including Verticillium dahlia, Ralstonia solanacearum, Fusarium
oxysporum and Meloidogyne spp. root-knot nematodes (Petran and Hoover, 2014).
However, even if S. torvum has been selected as rootstock of interest against other tomato
rootstocks of known high compatibility, this species is currently classified as ‘‘noxious
weed’’ which prohibits, without permit, its movement ‘‘into or through the United States,
or interstate’’ (ECFR, 2008), in addition to other additional restrictions that have been
placed by several US states (Smith et al., 2008).
Intoxication outbreaks have been detected by consuming 20-30 mg eq
solanine/100 g fruit of S. torvum (Smith et al., 2008). Toxic effects appear to be mediated
by several steroideal glycoalkaloids (SGAs) including solasonine and solamargine,
isomers of a chacotriosyl hydroxysolanidine and possibly other compounds which
produce gastrointestinal and neurological effects (Rangan, 2008; Smith et al., 2008).
Those toxic compounds are derived from cholesterol and can act synergistically in the
plant resistance to insects, fungi, and nematode (Morris and Lee, 1984). Although toxic
SGAs are not usually detectable in the fruit, tomato leaves and vines contain SGAs
similar to solanine, and the fruits may be poisonous under certain circumstances and it has
been speculated that pre- and post-harvest stresses, fruit maturity, cultivar differences,
and growth environment can contribute to substantial changes in final concentration into
the fruit (Smith et al., 2008). Therefore, the existence of a transport from the S. torvum-
derived rootstock to the scion cannot be ruled out and should be investigated.
Except for some chlorophyll and photosynthesis-related compounds, it is believed
that roots are able to produce every type of compounds that exist in plants (Gregory,
2006; Uren, 2001). Special attention has been paid to the study of the organic compounds
released from plant roots into the rhizosphere in relation to the soil and biota interaction,
where metabolites from major chemical groups from primary and secondary metabolism
(sugars and polysaccharides, amino acids, fatty acids, sterols, vitamins, enzymes,
flavonones, carotenoids, hormones) have been identified (Gregory, 2006; Uren, 2001).
Whether or not those compounds are present in the root-xylem sap and can be transported
and accumulated into the fruit remains an open question that need to be addressed.

NEW GENETIC VARIABILITY

Perhaps the major contribution of grafting to plant breeding has been the creation
of new cultivars by asexual hybridization inducing heritable changes by grafting, which is
known as ‘graft hybridization’. Graft hybridization is not only a simple and powerful
means of plant breeding, but also plays a crucial role in revealing the mystery of non-
Mendelian inheritance in grafted fruit trees, which limits the success of breeding through
crossing grafted fruit cultivars (Liu, 2006). Importantly, graft hybridization may affect
multigenic quantitative characters either alone or in combination with qualitative
characters and may reduce the time needed to produce new cultivars by breaking down
linkage relationships and allowing selective transfer of desirable genes from relatively
distantly related species (Liu, 2000, 2006; Liu et al., 2004). Although practical results
may be rare, some graft hybrids can boost food production, such as has been reported in
cassava (Bomfim and Nassar, 2014). This capacity to generate new genetic variability and
its genetic or epigenetic basis must be addressed in vegetables, not only through the
generation of graft hybrids, but also through the study of the rootstock effect on seed
formation.

25
 

TRANSGRAFTING
Transgrafting can be defined as the use of a genetically engineered rootstock to
support a WT scion, or vice versa, and it might be very useful to protect horticultural
crops from biotic and abiotic stresses (Lemgo et al., 2013) and can be considered as a
promising biotechnological tool to address food security, beyond conventional breeding
technologies (Lusser et al., 2012). Creating new transgenic rootstocks to resist biotic (e.g.
(fungi and viruses) and abiotic stresses (salinity, drought, soil deficiencies,
temperature,…), especially those for which resistance genes are rare in the plant genome,
is a promising development (Lusser et al., 2012). Although the presence of the trans-
genetic material in the shoot tissues may be a concern since both mRNAs and siRNAs can
cross a graft junction, the use of RNA signaling technology in modified roots represents
an excellent opportunity to induce virus resistance(s) but still maintaining production of
non-transgenic fruits. However, transgrafting might help to minimise consumer concerns
of transgene flow, since the non-transgenic scion would only produce non-transgenic
pollen (COGEM, 2006; Lev-Yadun and Sederoff, 2001). The potential of
biotechnological approaches addressed to the rootstock are obvious.

GRAFTING USE EFFICIENCY

The benefits of using grafting should be first considered at the level of individual
farmer and secondly, on the socio-economic-environmental balance of agriculture. The
cost of producing grafted seedling has been always considered as a major concern in the
implementation of this technology. Even though the high price of the seedlings is still a
major problem, the important reduction in producing costs during the last years, together
with the needs imposed by international environmental policies, has allowed a rapid
development of vegetable grafting in developed countries that accounts for 5% of the
world vegetable production with only 3% of the cultivated area (FAOSTAT, 2010). In
order to allow further development, especially in underdeveloped countries, important
research efforts must be made to improve grafting use efficiency through decreasing costs
(both grafting process and seeds), crop management optimization (plant, nutrients, water,
fumigants, energy) and training farmers.

CONCLUSION AND PERSPECTIVES

We should investigate vegetable grafting because it is regarded as a quick and
efficient alternative to breeding to secure food production through a socio-economic-
environmentally sustainable agriculture. Another important reason is that its potentiality
is as broad as the genetic variability able to cross the barriers between rootstocks and
scions. While empirical research and craft secrets have been dominating the current state
of the art, future developments and applications should be based on cutting-edge scientific
advances gaining further insights into the physiological and genetic determinants of
rootstock-scion interactions and communication and specially those underlying
favourable rootstock × scion × environment combinations. Moreover, the favourable
phenotypes must be optimized for specific environments by developing adequate crop
management practices. This new knowledge can open new possibilities for breeding,
biotechnological and management manipulations. Sharing knowledge and enhancing
scientific and technical collaboration will surely fill knowledge gaps in the area of
vegetable grafting. This will ultimately be used to help vegetable growers and breeders
deal with the predicted impacts of climate change and to overcome the consequences of
unsustainable agricultural practices that are causing soil degradation and depleting natural
resources.

ACKNOWLEDGEMENTS
We thank the European Commission (ROOTOPOWER Contract # 289365), the
EU COST office (FA1204 Action on Vegetable Grafting), and the Spanish MICINN-
FEDER (AGL2011-27996) for support grafting research in my laboratory.

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yield, and quality of salinized tomato. J. Plant Nutr. Soil Sci. 174:154-162.
Schwarz, D., Rouphael, Y., Colla, G. and Venema, J.H. 2010. Grafting as a tool to
improve tolerance of vegetables to abiotic stresses: Thermal stress, water stress and
organic pollutants. Scientia Horticulturae 127:162-171.
Smith, S.W., Giesbrecht, E., Thompson, M., Nelson, L.S. and Hoffman, R.S. 2008.
Solanaceous steroidal glycoalkaloids and poisoning by Solanum torvum, the normally
edible susumber berry. Toxicon. 52:667-676.
Uren, N.C. 2001. Types, amounts, and possible functions of compounds released into the
rhizosphere by soilgrown plants. p.19-34. In: R. Pinton, Z. Varanini and P. Nannipieri
(eds.), The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant
Interface. Marcel Dekker, New York.

28
 

Figures
50 1000
Korea
South-Eastern Spain
40 Number of publications 800

Million seedlings
30 600
Number

20 400

10 200

0 0
2000 2002 2004 2006 2008 2010 2012

Year  

Fig. 1. Number of articles on vegetable grafting published in international journals during

the last decade. (replotted from Colla (2010) and completed from
www.scopus.com) and the evolution of the number of grafted seedlings produced
in two major grafting-producing regions such as Korea (replotted from Lee et al.
(2010)) and South-Eastern Spain comprising Almeria, Murcia and la Comunidad
Valenciana, where some official information exists (replotted from Hoyos (2007)
and F. Pérez-Alfocea, unpublished).

Fig. 2. Future challenges and prospects in vegetable grafting that should be addressed by
current and future research initiatives.

29
  

 
 
 
 
 

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