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Scientia Horticulturae 127 (2010) 93–105

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Review

Current status of vegetable grafting: Diffusion, grafting techniques, automation


Jung-Myung Lee a,∗ , C. Kubota b , S.J. Tsao c , Z. Bie d , P. Hoyos Echevarria e , L. Morra f , M. Oda g
a
Honorary Professor, Department of Horticultural Biotechnology, Kyung Hee University, Republic of Korea
b
School of Plant Science, University of Arizona, USA
c
Department of Horticulture, National Taiwan University, Taiwan
d
College of Horticulture and Forestry, Huazhong Agricultural University, China
e
Polytech University of Madrid, Spain
f
Cra-Unita di ricerca per le colture alternative al tabacco, Italy
g
Osaka Prefecture University, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Vegetable production with grafted seedlings was originated in Japan and Korea to avoid the serious crop
Received 11 May 2010 loss caused by infection of soil-borne diseases aggravated by successive cropping. This practice is now
Received in revised form 7 July 2010 rapidly spreading and expanding over the world. Vegetable grafting has been safely adapted for the pro-
Accepted 2 August 2010
duction of organic as well as environmentally friendly produce and minimizes uptake of undesirable
agrochemical residues. The number and size of commercial vegetable seedling producers has increased
Keywords:
markedly reflecting the increase in farmers’ preferences for grafted seedlings of high-quality and better
Vegetable production
performance. In addition to the widely recognized advantages of disease tolerance and high crop yields,
Cucurbitaceae
Solanaceae
grafting technology is also highly effective in ameliorating crop losses caused by adverse environmen-
Organic produce tal conditions such as low soil temperature and high soil salts, especially under protected cultivations
Grafting machines where successive cropping or continuous farming is routinely practiced. Grafted seedlings are much
favored in hydroponics farming systems where the chances of rapid spread of noxious diseases, once
infected, is high. Active research has been focused to develop efficient rootstocks and handy grafting
tools. In addition, researchers are eager to develop grafting machines or robots to reduce the higher
price of grafted seedlings. The quality of grafted transplants is extremely important to maximize high-
quality crop yield. Use of grafted vegetables has increased with the increased use of improved soil mix
or substrate, farmer’s preferences for better seedlings, efficient management of nursery systems, lower
prices of grafted seedlings, and efficient nationwide delivery and/or transportation system. Improved
grafting methods to cut down the labor cost for grafting and subsequent handling of plug-grown grafted
transplants will contribute further to the increased use of grafted vegetables worldwide.
© 2010 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
2. Purpose of vegetable grafting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
2.1. Tolerance to soil-borne diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
2.2. Plant vigor promotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
2.3. Yield increases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
2.4. Tolerances to abiotic stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
2.5. Effect on fruit quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
2.6. Other uses of grafting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3. Current status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1. Rootstock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.2. Grafted plant production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.3. International export . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98

∗ Corresponding author at: Department of Horticultural Biotechnology, College of Life Sciences, Global Campus of Kyung Hee University, Room 509, Seochun-dong
1 Giheung-gu, Yongin, Gyeonggi-do 446-701, Republic of Korea. Tel.: +82 31 201 2618; fax: +82 31 202 1740.
E-mail address: jmlee@khu.ac.kr (J.-M. Lee).

0304-4238/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.scienta.2010.08.003
94 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

4. Grafting methods and acclimatization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99


4.1. Hand grafting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4.1.1. Hole insertion grafting (HIG) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4.1.2. Tongue approach grafting (TAG) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4.1.3. Splice grafting (SG), tube grafting (TG), and one cotyledon splice grafting (OC-SG) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
4.1.4. Cleft grafting (CG) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
4.1.5. Pin grafting (PG) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
4.2. Tools, clips, and grafting aids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
4.3. Grafting machines and robots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
4.4. Acclimatization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
5. Commercial production and quality of grafted seedlings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
6. Conclusions and prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105

1. Introduction Oda, 2003). The increasing awareness and interest in fresh horti-
cultural produce has rapidly expanded among people of all ages
Even though grafting has been practiced in fruit trees for thou- and locations who seek safe, environmentally friendly, and func-
sands of years, vegetable grafting has been only recently widely tional foods. Fast foods are now regarded as dangerous in many
adapted on a commercial scale (Ashita, 1927; Sakata et al., 2007). developed countries and obesity is currently defined as a disease,
Old records on vegetable grafting can be found in Chinese as rather than a symbol of health and prosperity. Many Asian peo-
well as in Korean and Japanese writings. The commercial use ple have been consuming more horticultural crops as compared to
of vegetable grafting is a relatively recent innovation. The wide those living in western countries, especially vegetables. However,
use of plastic films for the production of vegetables in the late because of the very limited total and per capita cultivation area,
1950s provided the momentum for generalized production and intensive use of the land is inevitable to secure food and earnings
use of grafted vegetables. The early use of grafted vegetables was for the majority of farmers. Intensive land use is most frequently
associated with protected cultivation which involves successive performed by multiple or successive cropping even in temperate
cropping. Commercial vegetable grafting originated in Japan and zone areas (Lee et al., 2008). In the southern parts of Korea, it is
Korea and was practiced for about 30 years. It was introduced to not usual to find watermelon growers producing 3–4 crops per
Western countries in the early 1990s and is currently being glob- year in the same greenhouse. The farmers usually apply heavy
ally practiced using local scion cultivars and introduced rootstocks. amount of chemical fertilizers and frequent pesticides treatment
Fortunately, seed companies have been able to select and/or breed to the densely planted vines to obtain high crop yield and earn-
well-adapted scion cultivars for intensive growing. Even though ings. Since the plants are cultivated under the protected structures
the benefits of using grafted seedlings are widely recognized, many year-round, they frequently are subjected to extreme environmen-
other factors must be carefully considered to ensure successful tal conditions in the high tunnels during off-season cultivation
cultivation and satisfactory income with this new technology. For (Lee, 2008). As a result farmers frequently encounter various prob-
example, generous use of chemical fertilizers and synthetic pesti- lems caused by successive as well as off-season cropping such
cides should be minimized for the production of environmentally as heavy infection of soil-borne diseases, low temperatures dur-
friendly produces, in which interest has been exploding in recent ing the winter, high humidity in the high tunnels, insufficient
years (Cushman and Huan, 2008; Davis et al., 2008; Kubota et al., light intensity, and lack of well-balanced fertilization. The plants
2008; Lee and Oda, 2003; Sakata et al., 2007). It has been well- and the fruits grown under these stressful conditions frequently
known that the use of proper rootstocks can minimize the problems suffer from heavy incidence of soil-borne diseases, suboptimal
associated with successive cropping and stress tolerance (Heo, temperature stresses, various physiological disorders, and quality
2000; Hoyos Echeverria, 2010; Lee, 1994; Lee et al., 1998; Lee and deterioration.

Table 1
Major advantages and disadvantages of using grafted vegetable transplants.

Advantages Disadvantages

Yield increase Additional seeds for rootstocks


Shoot growth promotion Experienced labor needed
Disease tolerance Wise selection of scion/rootstock combinations
Nematode tolerance/resistance Different combinations for cropping season
Low temperature tolerance Different combinations for cropping methods
High temperature tolerance High price of seedlings
Enhanced nutrient uptake Increased infection of seed-borne diseases
Enhanced water uptake Excessive vegetative growth
High salt tolerance Fruit harvesting may be delayed
Wet soil tolerance Inferior fruit quality (taste, color and sugar contents)
Heavy metal and organic pollutant tolerance Increased incidence of physiological disorders
Quality changes Symptoms of incompatibility at later stages
Extended harvest period Different cultural practices should be applied
Multiple and/or successive cropping allowed Higher prices of grafted seedlings
Convenient production of organic wastes
Ornamental values for exhibition and education
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 95

Fig. 1. Adventitious rooting from the melon scion grafted onto squash rootstocks through the hypocotyl cavity of the rootstock, thus counteracting the grafting effect in
some cases (left) and rooting from the scion of the TAG-grafted cucumber onto figleaf gourd (center and right).

2. Purpose of vegetable grafting much more efficiently as compared to non-grafted plants, For
example, in watermelons, it is routinely recommended to reduce
2.1. Tolerance to soil-borne diseases the amount of chemical fertilizers application to about one-half to
two-third as compared to the standard recommendation for the
The vigorous roots of selected rootstock can exhibit excellent non-grafted plants (Lee and Oda, 2003; Salehi-Mohammadi et al.,
tolerance to serious soil-borne diseases, such as those caused by 2009). This is especially true for nitrogen fertilizers during early
Fusarium, Verticillium, Phytophthora, Pseudomonas, Didymella bry- seedling growth and for the safe setting of fruits at the desired
oniae, Monosporascus cannonballus, and nematodes (Edelstein et al., node positions for early fruit set. Early fruit set is crucial for the
1999; Cohen et al., 2000, 2005, 2007; Ioannou, 2001; Trionfetti early harvesting in greenhouses to secure good market prices.
Nisini et al., 2002; Blestos et al., 2003; Morra and Bilotto, 2006; Cytokinin composition in bleeding xylem sap from decapitated,
Crinò et al., 2007) even though the degree of tolerance varies con- grafted, or own-rooted, differs greatly in various cucurbits. Fur-
siderably with the rootstocks. Even the scion infection of certain thermore, the scion is capable of converting the composition of
virus diseases (TMV races) could be markedly influenced by virus cytokinins in the ascending xylem sap (Table 2) in a relative short
resistant rootstocks depending upon the level of resistance in scion period. Thus, the higher cytokinin concentration in the ascending
and rootstocks (Nishi, 2001; Sakata, 1996–97, Vegetable Seed Cat- xylem sap contributes to growth promotion.
alog, p. 176). The mechanism of disease resistance, however, has The frequency of agrochemical application can be significantly
not been intensively investigated. These characteristics are cru- reduced by using vigorous rootstocks. Fungicides application may
cial for the plants grown under protected environments, where also be greatly reduced or totally excluded depending upon the
extended harvesting and higher crop yield are expected. Resis- diseases, thus greatly enhancing the successful production of
tant rootstocks can also effectively counteract the rapid disease organically grown fruits. In cucumber, vigorous root system of the
spread when plants are grown in hydroponics system. The disease rootstock can effectively absorb water so that less frequent irriga-
tolerance in grafted seedlings may be entirely due to the toler- tion may be practiced.
ance of rootstock roots to such diseases (Table 1). However, in
actual planting, adventitious rooting from the scion is common 2.3. Yield increases
(Fig. 1). Plants having the root systems of the scion and rootstock
are expected to be easily infected by soil-borne diseases. How- Grafting is associated with noticeable increases in fruit yield
ever, seedlings having dual root systems occasionally exhibit a in many fruit vegetables regardless of infection with certain soil-
certain degree of disease resistance, thus partially supporting the borne diseases. In oriental melons, fresh fruit weight increase of
previous report that substances associated with Fusarium toler- 25–55% have been reported as compared to own-rooted plants.
ance are synthesized in the root and move to the scion through These yield increase were closely correlated with the maintenance
the xylem. It is generally accepted, however, that the disease- of good plant vigor until late in the growing season in addition to
susceptible characteristics of the scion are not transported to the disease resistance. Virtually no marketable yield was obtained from
rootstock. plants heavily infected with Fusarium. Similar results were obtained
with tomato. Up to 54% increase of marketable yield in tomato was
2.2. Plant vigor promotion obtained with ‘Kagemusia’ and 51% with ‘Helper’ rootstocks (Chung
and Lee, 2007). There was also significant decrease in abnormal
Since the root systems of selected rootstocks are usually much fruits in plant grafted onto most rootstocks as compared with the
larger and more vigorous, they can absorb water and nutrients own-rooted ‘Seokwang’ tomato. Similar yield increase have been

Table 2
Cytokinin composition in xylem sap collected from ungrafted and grafted plants of cucumber, squash, and figleaf gourd plants.

Cytokinin content (ng/ml sap)

Zeatin Zeatin riboside Dihydozeatin riboside Isopentenyl adenine Total

Ungrafted plants
Cucumber (Cucumis sativus L.) 0.08 4.55 0.80 Trace 6.11
Squash A (Cucurbita moschata Duch.) Trace 3.67 0.43 3.63 7.73
Squash B (Cucurbita maxima Duch.) Trace 4.06 0.57 1.84 6.47
Figleaf gourd (Cucurbita ficifolia Bouché) Trace 4.54 1.48 6.18 12.2

Grafted plants
Cucumber/Cucumber 0.55 5.58 0.96 Trace 7.07
Cucumber/Squash A 1.65 4.29 0.20 Trace 6.14
Cucumber/Squash B Trace 5.36 0.19 Trace 5.55
Cucumber/Figleaf gourd 1.49 5.08 0.65 Trace 7.22
96 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

reported by other researchers on watermelon, cucumber (Lee and many growers heat their greenhouse during the winter, there are
Oda, 2003), melon, pepper, and eggplant. more growers who do not have electric or gas-generated heat-
ing systems and depend solely on preservation of solar energy
2.4. Tolerances to abiotic stresses capture during the daytime. These growers find it difficult to main-
tain optimum temperatures in winter greenhouses, especially soil
Grafts were used to induce resistance against low and high tem- temperatures which are far below the optimum thus causing trans-
peratures (Rivero et al., 2003; Venema et al., 2008), to enhance planted plants to suffer during the early stages of cultivation. This
nutrient uptake (Colla et al., 2010a), increase synthesis of endoge- is especially true with crops that require high temperatures for
nous hormones (Dong et al., 2008), improve water use efficiency optimum performance such as watermelon and oriental melon.
(Rouphael et al., 2008a), reduce uptake of persistent organic pollu- Grafting watermelon, melon, cucumber, even summer squash onto
tants from agricultural soils (Otani and Seike, 2006, 2007), improve low temperature tolerant rootstocks such as interspecific hybrid
alkalinity tolerance (Colla et al., 2010b), raise salt and flooding tol- between Cucurbita maxima Duch. × C. moschata Duch. or figleaf
erance (Romero et al., 1997; Colla et al., 2006a,b; Yetisir et al., 2006), gourd can greatly reduce the risk of severe growth inhibition
and limit the negative effect of boron, copper, cadmium, and man- caused by low soil temperatures in winter greenhouses. Cucumber
ganese toxicity (Edelstein et al., 2005, 2007; Rouphael et al., 2008b; grafted onto figleaf gourd (Cucurbita ficifolia Bouché), an excel-
Savvas et al., 2009). lent rootstock even at low soil temperature, grows much faster
Tolerance to extreme temperature is crucial for the produc- than own-rooted cucumber or even summer squash because of
tion of fruiting vegetables under the winter greenhouse conditions. the rootstock’s ability to absorb water and nutrient more effi-
In cucurbits, cropping area under protected structure is sub- ciently at low temperatures (Tachibana, 1982). Many physiological
stantially larger than field cultivation for watermelon, cucumber, disorders can also be minimized effectively by using grafted
and melon in Korea. The transplanting of seedlings for protected plants. Since the resistance to temperature stresses varies with
cultivation is usually done in early to mid-winter and fruit har- the rootstocks, different rootstocks should be used during the hot
vesting is usually finished by spring to early summer. Even though summer season.

Table 3
Rootstocks for cucurbitaceous crops and some related characteristics.

Rootstock Cultivara Major characteristicsb Possible disadvantage

Watermelon
Bottle gourd (Lagenaria siceraria L.) Dongjanggoon, Bulrojangsaeng, VRS, FT, LTT New fusarium race, susceptible to
Sinhwachangjo (Korea), FR Dantos, anthracnose
Renshi, Friend, Super FR Power
(Japan),
Squash (Cucurbita moschata Duch.) Chinkyo, No. 8, Keumkang (Korea) VRS, FT, LTT Inferior fruit shape and quality

Interspecific hybrid squash Shintozwa, Shintozwa #1, VRS, FT, LTT, HTT, SV Reduced fertilizers required. Some
(Cucurbita maxima Duch. × C. Shintozwa #2, Chulgap, (Japan, quality reduction may result.
moschata Duch.) China, Taiwan, Korea)
Pumpkins (Cucurbita pepo L.) Keumsakwa, Unyong, Super VRS, FT, LTT Mostly for cucumbers
Unyong
Wintermelon (Benincasa hispida Lion, Best, Donga GDR Incompatibility
Thunb.)
Watermelon [Citrullus lanatus Kanggang, Res. #1, Tuffnes (Japan), FT Not enough vigor and disease
(Thunb.) Matsum. et Nakai] Ojakkyo(Syngenta) resistance

African horned (AH) cucumber NHRI-1 FT, NMT Medium to poor graft
(Cucumis metuliferus E. Mey. ex Compatibility
Naud)
Cucumber
Figleaf gourd (Cucurbita ficifolia Heukjong (black seeded figleaf LTT, GDT Narrow graft compatibility
Bouché) gourd)
Squash (Cucurbita moschata Duch.) Butternut, Unyong #1, Super FT, FQ Affected by Phytophthora
Unyong
Interspecific hybrid squash Shintozwa, Keumtozwa, Ferro RZ, FT, LTT Slight quality reduction expected
(Cucurbita maxima Duch. × C. 64-05 RZ, Gangryuk Shinwha
moschata Duch.)
Bur cucumber (Sicyos angulatus L.) Andong FT, LTT, SMT, NMT Reduced yield

AH cucumber (Cucumis metuliferus NHRI-1 FT, NMT Weak temperature tolerance


E. Mey. ex Naud)
Melon
Squash (Cucurbita moschata Duch.) Baekkukzwa, No. 8, Keumkang, FT, LTT Phytophthora infection
Hongtozwa
Interspecific hybrid squash Shintozwa, Shintozwa #1, FT, LTT, HTT, SMT Phytophthora infection, poor fruit
(Cucurbita maxima Duch. × C. Shintozwa #2 quality
moschata Duch.)
Pumpkin (Cucurbita pepo L.) Keumsakwa, Unyong, Super FT, LTT and HTT, SMT Phytophthora infection
Unyong
Melon (Cucumis melo L.) Rootstock #1, Kangyoung, FT, FQ Phytophthora problem
Keonkak, Keumgang
AH cucumber(E. Mey. ex Naud) NHRI-1 FT, LTT, SMT, NMT Weak temperature tolerance
a
Cultivars vary greatly depending upon countries, growing types, years, and grafting methods.
b
VRS: vigorous root systems; FT: Fusarium tolerance; LTT: low temperature tolerance; ST: strong vigor; HTT: high temperature tolerance; GDT: good disease tolerance;
GDR: good disease resistance; NMT: nematode tolerance; SMT: high soil moisture tolerance; FQ: fruit quality modification.
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 97

2.5. Effect on fruit quality more commonly practiced for vegetables grown under protected
environment as compared to those under the field condition. Root-
There are several conflicting reports (Proietti et al., 2008; Flores stocks belonging to different species often are preferred where
et al., 2010 and references cited therein) on changes in fruit quality genetic diversity can be exploited. Thus rootstocks of different
due to grafting and whether grafting effects are advantageous or species are widely used in cucurbits (Table 4) and solanaceous crops
deleterious. The differences in reported results may be attributable (Table 5).
in part to different production environments and agricultural prac-
tice, type of rootstock/scion combinations used, and harvest date. 3.2. Grafted plant production
The fruit size of watermelons grafted to rootstock having vig-
orous root systems is often significantly increased compared to Although the possibility and benefits of using grafted plants
the fruit from intact plants, and many growers practice grafting were recognized much earlier, large-scale commercial growing of
mainly for this reason. It is also known that other quality character- grafted vegetables can be traced from the late 1950s to the early
istics, such as fruit shape and skin color, rind thickness, and soluble 1960s in Japan and Korea. Statistics on the current use of grafted
solids concentrations are influenced by rootstock. In cucumbers, plants in Korea and Japan are shown in Table 6. In cucurbitaceous
especially those for export, external color and bloom develop- crops, over 90% of watermelon seedlings are grafted onto various
ment are important quality factors. Even though these are usually rootstocks and about 75% of cucumbers in both countries. Melons
regarded as cultivar-specific hereditary characteristics, they can be show variable grafting percentages depending upon the genotypes.
greatly influenced by the rootstock. However, with the exception For example, virtually all the oriental melons (Cucumis sativus L.
of increasing fruit size, shape, and bloomless-fruit production in var. makuwa Makino) are grafted onto squash in Korea, but other
cucumber, the effects of rootstocks on some fruit quality can be melons are selectively grafted depending on the genotypes using
detrimental such as reduced soluble solids contents, thicker rind, various rootstocks (Ko, 1999, 2008). In solanaceous vegetables,
flavor of rootstocks, and undesirable internal breakdown in mature 20–40% of tomatoes are grafted, 20–40% of eggplants, and 5–10% of
fruit as briefly described in Table 1. Therefore, most newly devised peppers. Since grafting is mostly practiced in cucurbits and solana-
growing recommendations are aimed at minimizing the detrimen- ceous vegetables, the percentages of grafting in all vegetables was
tal effects of rootstock on fruit quality (Cushman and Huan, 2008; only about 5% in 2007. More than 700 million grafted seedlings
Ko, 2008). were estimated to be produced in 2008 in Korea as well as in Japan
(Table 7).
2.6. Other uses of grafting Even though vegetable grafting is actively practiced in other
countries, accurate statistics are unavailable. However, 40–45 mil-
Grafting can be performed for various other reasons. For exam- lion grafted seedlings were distributed in North America in 2005
ple, tomato, eggplant, and pepino can be grafted on potato so that (Kubota et al., 2008). Spain is by far the leading European coun-
4 or more different kind of vegetables could be harvested from a try in using grafted vegetable transplants (129.8 million in 2009)
single plant. Chinese cabbages and cabbages may be grafted on top (Hoyos Echeverria, 2010, pers. commun.), followed by Italy (47.1
of radish. Grafting can be made for some physiological studies such million) (Morra and Bilotto, 2009) and France (about 28 million)
as flower induction and early flowering. Grafting is also commonly (Table 8). It was estimated that about 20% of China’s watermel-
used for bioassays of virus infection (Lee and Oda, 2003; Davis et ons and cucumbers are grafted. For example, over 200 companies
al., 2008). produced grafted seedlings for the farmers with the biggest one
producing 200 million seedlings in 2009 (Bie, 2010, pers. com-
3. Current status mun.). Rapid increases in the use of grafted seedlings are expected
throughout the world for some decades (Davis et al., 2008; Lee
3.1. Rootstock and Oda, 2003; Oda, 2007). Well-known multinational seed com-
panies are now supplying several rootstock seeds which virtually
Various rootstocks have been screened from the existing culti- have little or no negative effects on fruit quality in some vegeta-
vars for use in each crop. Recently, however, seed companies and bles. Even though cucurbits (watermelon, melons, and cucumbers)
various breeders are eager to breed superior rootstocks for veg- and solanaceous crops (tomatoes, eggplants, capsicum peppers) are
etables grown under certain conditions and environments. The routinely grafted, many other vegetables can be grafted for other
growers, therefore, have to make decision on selection of root- purposes (Lee and Oda, 2003).
stocks most suitable for their specific requirements. Some of the The majority of the grafted seedlings are produced by com-
characteristics in cucurbits are summarized in Table 3. Cucurbit mercial growers globally. In Korea, more than 200 seedlings
species and number of registered rootstock cultivars are rapidly growers, excluding individual farmers and farmers’ associations,
increasing mostly due to the increased cultivation of grafted plants are producing plug seedlings and about half of them are produc-
under various cultural as well as environmental conditions (Kato ing grafted seedlings. Hoban Nursery, the largest one in Korea
and Lou, 1989; Ko, 1999; Lee et al., 2008). In general, grafting is located in Chooncheon, Gangweon-do, produced 15.6 million

Table 4
Rootstock species and number of registered rootstock cultivars for cucurbitaceous crops in China (Bie, 2010, pers. commun.).

Rootstock Crop

Watermelon Cucumber Melon Bitter melon Summer squash Wax gourd Sponge gourd

Lagenaria siceraria L. 6 2 0 0 0 0 0
Cucurbita moschata Duch. 4 5 6 2 0 2 0
C. maxima Duch. × moschata Duch. 4 2 5 0 0 0 0
C. maxima Duch. 1 1 0 0 0 1 0
Citrullus lanatus (Thunb.) Matsum. et Nakai 1 0 0 0 0 0 0
Cucurbita ficifolia Bouché 0 7 1 1 1 1 1
Luffa acutangula (L.) Roxb. 0 0 0 2 0 0 0
Luffa cylindria (L.) M.J. Roem 0 0 0 3 0 0 0
98 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

Table 5
Rootstocks for solanaceous crops (Solanum, Capsicum, and Datura) and their performances.

Rootstock Scion Performance Practical uses or popularity

S. lycopersicum L. Tomato Vigor and virus tolerances Extensive


S. lycopersicum L. Tobacco Nicotine & alkaloid absorption affected Experimental
S. lycopersicum L. Tomato High temperature tolerance Extensive
S. habrochaites S. Knapp & D.M Spooner Tomato Resistant to corky root disease Very limited
Solanum spp. Tomato Resistant to bacterial wilt & nematode Interspecific hybrids
Yield increase
S. sodomaeum L. Tomato Growth & yield reduction Experimental
S. auricularum Ait. Tomato Growth & yield reduction Experimental
S. laciniatum Ait. Tomato Resistant to water-logging Local
S. melongena L. Tomato Growth & yield reduction Moderate
S. integrifolium Poir. Tomato Sugar content increase Local
S. sisymbrifolium Lam. Tomato Disease resistance, no effect on sugar Local
content
S. torvum Sw. Tomato Eggplants Disease resistance, no effect on sugar Nematode tolerant, poor
content seed germination, good
vigor
Extensive
S. toxicarium Lam. Tomato Disease resistance, no effect on sugar
content
S. melongena L. Tomato Multiple disease resistance Local
S. nigrum L. Tomato Fruit size and quality control Selective
S. lycopersicum L. × S. habrochaites S. Tomato Low Fusarium infection Experimental
Knapp & D.M Spooner
S. lycopersicum L. × S. habrochaites S. Tomato Multiple disease resistance Extensive
Knapp & D.M Spooner
S. lycopersicum L. Tomato Resistant to corky root (K), Root knot Extensive
nematode (N), Verticillium wilt (V),
and Fusarium wilt (F)
Yield increase
S. melongena L. Tomato Low & high temperature tolerance Selective
S. lycopersicum L. Tomato Resistance to tomato brown root rot Selective
Solanum torvum Sw. Eggplant Resistant to nematodes Extensive
S. torvum Sw. × S. sanitwongsei Craib. Eggplant Resistance to bacterial wilt Local
S. integrifolium Poir. × S. melongena L. Eggplant High temperature tolerance Experimental
Capsicum spp. Sweet pepper (green) Compatible with Capsicum only Extensive
C. annuum L. × C. chinensis Jacq. Green pepper Superior growth & yield Extensive
Datura tatula Tomato Low yield Experimental

grafted seedlings in 2008 (Table 9). Nongwoo GreenTek produced seeds, rootstock seeds, and labor cost for grafting and post-graft
9.0 million followed by Nosung, Gongju, and Yeoju. Pureun Nurs- care are considered to be the major factors in price determina-
ery produced about 2.8 million seedlings, mostly for export. Yet, tion.
less than 10% of all grafted seedlings are estimated to be produced
by commercial growers in Korea (Ko, 2008). The price of grafted 3.3. International export
seedlings varies with crops and countries, 0.4–1.2$ in the USA and
some Asian countries including Japan and Korea, and 0.6–1.0D in Even though plants growing in pot soil are frequently rejected at
Spain and some European countries (Table 8). The price of scion customs because of strict quarantine regulations, grafted seedlings

Table 6
Vegetable cultivation area, number of total seedlings, and number of grafted seedlings needed in Korea and Japan.

Vegetable Cultivation Cultivation No. of seedlings per ha Maximum no. of % use of grafted Maximum no. of grafted
area-2000 (ha) area-2005 (ha) (×1000) seedlingsa (million) seedlings 2005 seedlings (million)

Republic of Korea
Watermelon 30,451 23,179 6–9 208.6 95 198.2
Melona 13,800 13,000 7–10 130.0 90 117.0
Cucumber 7269 5853 20–30 175.6 75 131.7
Tomato 4916 6749 20–30 202.5 25 50.6
Eggplant 1100 933 10–20 18.6 20 3.7
Pepperb 80,130 67,023 20–40 2681.9 10 268.2
Sub-total 766.3

Japan
Watermelon 16,900 13,400 6–9 120.6 92 111.0
Melona 13,800 10,400 7–10 104.0 30 31.2
Cucumber 15,200 13,400 20–30 402.0 75 301.5
Tomato 13,600 13,000 20–30 390.0 40 156.0
Eggplant 13,300 10,400 10–20 208.0 55 114.4
Pepperb 4110 3620 20–40 144.8 5 7.2
Sub-total 721.3
a
Including net melons, cantaloupes, oriental melons.
b
Including hot peppers for dry and fresh uses.
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 99

Table 7
Current status of the estimated use of grafted vegetables in some Asian and other countries and regions.

Crop Item Japan Korea China Taiwan USA


a
Watermelon Area (ha) 13,000 20,756 2,162, 456 13,431 50,810
Graft (%)b 92 95 20 35 NAc
Grafting methodd HIG,S HIG, TAG HIG, TAG, SG HIG,TAG,SG –
Rootstockse Ls, Cl Ls, Cmm Ls, Cl Cmm, Ls –

Cucumber Area (ha)a 12,800 5,630 1,702, 777 2,666 59,480


Graft (%)b 75 75 30 11 NAc
Grafting methodd TAG,SG SG, TAG HIG, TAG TAG –
Rootstockse Cmm, Cf Cmm, Cf Cm, Sa, Cf A –

Melons Area (ha)a 10,500 6,607 570,874 6,441 35,790


Graft (%)b 30 90 5 0.1 NAc
Grafting methodd TAG,SG SG, TAG HIG – –
Rootstockse Cmm, Cm Cmm Cm, Cmm, Cl – –

Bitter melon Area (ha)a NAc NAc 200,000 1,802 NAc


Graft (%)b – – 2 30 –
Grafting methodd – – HIG, TAG TAG,CG –
Rootstockse – – Lc La, Cm –

Pickling melon Area (ha)a 232 NAc NAc NAc NAc


Graft (%)b – – – – –
Grafting methodd TAG – – – –
Rootstockse – – – – –

Tomato Area (ha)a 12,700 6,144 1454, 533 4235 330f


Graft (%)b 40 25 1 25 70f
Grafting methodd SG, TAG SG SG HIG, SG SG
Rootstockse Sl, St Sl, Ss Sl Ss, Sl Ss

Eggplant Area (ha)a 10,800 325 1051, 537 1503 2200


Graft (%)b 55 20 1 1.3 NAc
Grafting methodd SG, TAG SG SG – –
Rootstockse Ss Ss St – –

Pepper Area (ha)a 3620 61,023 16,625 2405 32,140


Graft (%)b 5 10 1 2.5 NAc
Grafting methodd SG, TAG SG SG – –
Rootstockse Ca Ca,Cs Cf – –

Data supplied by M. Oda J.M. Lee Z. Bie and Y. Huang S.J. Tsao C. Kubota and M. Bausher
a
Cultivation area was obtained from FAO Statistics 2008 except Taiwan. Other countries actively using grafted vegetable seedlings include Vietnam (6000 ha out of
20,000 ha tomato production area is planted with grafted plants in Vietnam) and possibly many others.
b
Percentage of cultivation area with grafted plants.
c
Data not available (NA).
d
Major grafting methods are: TAG, tongue approach grafting; SG, splice grafting; HIG: hole insertion grafting; and CG, cleft grafting, respectively.
e
Rootstocks are: Cf, Cucurbita ficifolia; Cm, Cucurbita moschata; Cmm, Cucurbita maxima × C. moschata; Cl, Citrullus lanatus; La, Luffa aegyptiaca; Lc, Luffa cylindrica; Sl,
Solanum lycopersicum; Ls, Lagernaria siceraria; Sa, Sicyos angulatus; Sm, Solanum melongena; Ss, Solanum species including interspecific hybrids; and St: Solanum torvum,
respectively.
f
Greenhouse hydroponic tomato cultivation area only. Little or no grafting had been reported for field tomatoes of 162,580 ha in the USA.

produced by export-oriented nurseries easily pass through the reg- ulation, (3) healing of the union, and (4) acclimation of the grafted
ulation. One of the reasons for this easy pass is the use of sterile plant. In fruit species, pruning is often an essential part of the
substrates rather than contaminated soils which are believed to grafting process. Grafting methods vary greatly and considerably
be fully contaminated with numerous diseases and even other depending upon the kind of crops, farmers’ experiences and pref-
microorganisms. Furthermore the growing period is very short, erences, facilities and machines available, numbers of grafting, and
usually less than 30 days in most cases except eggplants. Trans- even by the purpose of grafting such as grafting for their own
portation and shipping are also easy with plug seedlings grown in uses or for sales only by commercial growers. In case of Japan
cell trays. Tomato is the major grafted vegetable for export, fol- (Table 10), hole insertion grafting is by far the most popular grafting
lowed by watermelon and eggplant. It is worthwhile to note that method in watermelon. However, in cucumbers, tongue insertion
seedling growers in Agadir, Morocco, exported 12 million grafted grafting is most popular among the individual growers producing
seedlings to southern Europe countries in 2007 and it is expected transplants for their own use. In contrast, the commercial grow-
that this kind of export will be markedly increased in coming years. ers prefer splice grafting. In eggplant, individual farmers prefer
In North America, Canada is the major source of grafted seedlings, split grafting where as the commercial growers definitely prefer
exporting more than 10 million grafted plants to the USA and splice grafting. In summary, less experienced, small-scale farmers
northern Mexico. Active export of grafted transplant from Korea select tongue approach grafting for most vegetables whereas large-
to Japan had been taken place for several years via several nurs- scaled experienced professional seedling producers like to adapt
eries. splice grafting. It is generally accepted that the quality of seedlings
grafted by splice grafting is much better than those grafted by
4. Grafting methods and acclimatization tongue approach grafting. Manual or hand grafting is by far the
major grafting method even though several grafting machines and
Grafting is a process that involves: (1) the choice of rootstock semi-automatic machines or robots have been developed and com-
and scion species, (2) creation of a graft union by physical manip- mercially available.
100 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

Table 8
Current statusa of the estimated use of grafted vegetables in some European and other countries as of April 30, 2009.

Crop Item Spain Italy France Netherlands

Watermelon Area (ha) 16,100 11,091 186 NAb


No. grafts (million) 48.2 10.0 NA NA
Rootstocksc RS-841 Shintoza Strongtosa Macis RS-841 Shintoza NA NA

Melons Area (ha) 38,600 28,199 14,747 3086


No. grafts (million) 2.5 8.2 NA NA
Rootstocksc RH-841 Shintoza Strongtosa Shintoza Camelforce Dinero RS-841 TZ-148 Dinero NA

Cucumber Area (ha) 7000 2065 631 NA


No. grafts (million) 0.5 0.8 NA NA
Rootstocksc Azman Hercules Titan NA NA NA

Tomato Area (ha) 55,300 115,477 4122 1800


No. grafts (million) 72.8 15.1 50% 75%
Rootstocksc Maxifort Beaufort Beaufort Maxifort He-Man Maxifort Beaufort NA

Eggplant Area (ha) 3500 10,862 417 115


No. grafts (million) 1.8 11.8 65% 75%
Rootstocksc Torvum Vigor Beaufort Espina Salutum STT3 Beaufort Brigeor Maxifort NA

Pepper Area (ha) 24,100 11,721 NA 41


No. grafts (million) 4.0 1.2 NA NA
Rootstocksc Atlante Tresor Rocal Atlante Tresor Galaxy Snooker NA

Price and planting densitiesd,e


a
Information in this table was obtained by contacting seed companies, related horticultural agencies, seedling producing nurseries, and personal communications. Acreage
was obtained from FAO Statistics 2008.
b
Data not available as of April 2010 are marked “NA” in the cell. Other countries actively using grafted vegetable seedlings include Turkey (50% of watermelons), Belgium
(mostly tomatoes), Germany, Switzerland, Denmark, and UK (50% or higher), and Morocco (also for export).
c
Seed companies supplying the rootstocks seeds are Seminis, Syngenta, Nunhems, Clause/Tezier, De Ruiter, Rijk Zwaan, Ramiro Arnedo, and others.
d
The price of grafted seedlings varies from 0.6 to 1.0 euro depending upon the crops (Hoyos Echeverria, 2010).
e
Number of seedlings planted per hectare varies from 15,000 to 30,000 depending upon the kind of crops and planting densities. Use of double-stemmed tomato grafted
transplants may cut down the purchasing expense by half (Hoyos Echeverria, 2010).

4.1. Hand grafting pith cavity of the rootstock (Fig. 1). Some growers insert young
watermelon seedlings (usually somewhat etiolated seedlings with
There are a number of grafting methods applicable for herba- cotyledons still in folded position) into the hypocotyl (Fig. 2A and
ceous grafting. Some of the most frequently used methods are B). HIG had been favorably practiced for tomato and eggplant for
diagrammed in Fig. 2. a while, but splice grafting is definitely much favored even among
the farmers for their own uses.
4.1.1. Hole insertion grafting (HIG)
Grafting methods vary with the kind of crops being grafted, 4.1.2. Tongue approach grafting (TAG)
preferences and experience of the growers, and the kind of graft- Tongue approach grafting (Fig. 2C) is usually favored by less
ing machines or robots available. For watermelons, hole insertion experienced farmers and those who do not have a greenhouse with
hypocotyl grafting (Fig. 2A) is favored by many farmers in many good microclimate control system. Even though this method needs
areas because of the smaller seedling size of watermelon as com- more space and labor as compared to other methods, a higher rate
pared to the size of the rootstock, which is usually squash or bottle of seedling survival is possible even for beginners. Furthermore, no
gourd. Watermelon seeds are sown 7–8 days after the sowing of special facilities and machines are needed for this grafting tech-
gourd seeds (rootstock) or 3–4 days after sowing squash rootstock nique. Since the grafting operation would be much more efficient
seeds. Grafting is made 7–8 days after the sowing of watermelon with both scion and rootstock seedlings having similar height, the
seeds. Both the scion and rootstock should be uniform and strong seeds of scion (usually watermelons, cucumbers, and melons) are
enough to undergo the grafting operation. The true leaf including sown 5–7 days earlier than the rootstock seeds. The growing point
the growing point should be carefully and thoroughly removed and of the rootstocks should be carefully removed before grafting to
a hole is made with a bamboo or plastic gimlet or drill at a slant reduce the unnecessary loss of nutrient for the bud growth and to
angle to the longitudinal direction. The hypocotyl portion of the promote the rapid union of graft interface. Occasionally one cotyle-
watermelon is prepared by slant cutting to have tapered end for don may also be removed when removing the growing point to
easy insertion. Care should be given to avoid the insertion into the ensure complete removal of the growing point and to avoid over-
hypocotyl cavity since this greatly interferes with formation of a crowding in limited space on the greenhouse bench. The grafting
rapid union and facilitates later protrusion of watermelon adven- cut for rootstock should be made in a downward direction and the
titious roots into the soil after downward elongation through the scion cut in an upward direction at an angle, usually 30◦ –40◦ to the

Table 9
Number of grafted seedlings produced by some major nurseries in Korea in 2008 (×1000).

Nursery Watermelon Cucumber Melon Pumpkin Tomato Pepper Eggplant Total

GreenTek 2500 3000 – – 500 3000 – 9000


Nosung 4000 300 – 700 300 – – 5300
Gongju 1500 1000 500 – 1000 – – 400
Yeoju 600 1000 – – 1200 200 1000 4000
Pureuna 300 500 – – 1000 1000 – 2800
a
Major exporter in Korea.
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 101

Table 10
Grafting seedlings produced by different grafting methods in Japan (revised from the survey data of Yoshioka, 2001).

Crop Area surveyed (ha) Percent share of grafting methods (%)

Tongue approach Split Hole insertion Root-removed & insertion Splice Others & unknown

Grafted seedlings produced by farmers for their own use


Watermelon 9244 7 1 53 38 – –
Cucumber 6648 89 1 5 4 1 0
Melonsa 1715 56 16 27 1 – –
Tomato 2412 36 13 6 – 45 0
Eggplant 2034 3 79 7 – 10 1

Grafted seedlings produced by commercial nurseries for sale


Watermelon 4455 1 5 35 55 3 1
Cucumber 3171 14 2 18 26 39 1
Melonsa 236 8 14 38 39 2 –
Tomato 2081 4 4 1 – 90 1
Eggplant 3436 2 18 8 – 71 1

Sub-total (own use + commercial)


Watermelon 13,699 5 3 47 44 1 0
Cucumber 9819 65 1 9 11 13 1
a
Melons 1951 50 16 28 6 0 –
Tomato 4493 21 9 4 – 66 0
Eggplant 5470 2 41 8 – 48 1
a
Only the field melon data was listed (house melons and greenhouse melons were not listed).

perpendicular axis, and deep enough to allow the fusion of as many ceous crops. In spite of the simple and easy grafting operation
vascular bundles as possible. After the graft is completed, specially and higher rate of survival, this method is not extensively used
designed clips are placed to fix the graft position. Grafted plants are by commercial seedling growers mainly because (1) labor required
then planted together in a 9–12 cm diameter container. for grafting, (2) labor needed for cutting the rootstock again, (3)
The grafted plants are partially shaded for 1 or 2 days before needs for removal of clips after union, (4) larger space is needed
placing them under normal greenhouse growing conditions. The for growing grafted plants as compared to other methods, and (5)
lower hypocotyl of the scion of several test plants is cut to examine frequent rooting from the scion after transplanting if the seedlings
the degree of graft-take 10–12 days after grafting and based upon are transplanted too deep (Lee, 1994, see Fig. 1).
the results the remaining plants can be handled as described below.
The root and lower hypocotyl of the scion are removed from the 4.1.3. Splice grafting (SG), tube grafting (TG), and one cotyledon
grafted plant by simply cutting off at the desired position, prefer- splice grafting (OC-SG)
ably at the closer position to the grafted position held by the clip. Splice grafting (Fig. 2D, E and J) is very popular among expe-
The clips are usually removed at later stages, shortly before trans- rienced growers and commercial plug seedling nurseries. Splice
planting. An experienced person can graft about 800 plants per day, grafting can be done by hand, machine, or robot and can be applied
but grafting machines and robots specifically designed for this kind to most vegetables. The major advantage is the production of strong
of grafting are also available at varying prices. and healthy grafted seedlings since all the vascular bundles of the
TAG is the oldest and perhaps the most convenient grafting scion are fused with those of rootstock and the graft union is strong
method for herbaceous plants. The method can be used for basi- enough to take all the rough post-graft handling. Intact or excised
cally any kind of plants such as cucurbits, solanaceous plants, and (root-removed) rootstock seedlings may be used depending upon
many other types. Grafting is performed with very young seedlings the growers and farmers’ preference. For the cucurbit rootstocks,
and preferably at the hypocotyl portion of the rootstock and scion of 1 cotyledon and the growing point are removed for grafting. After
cucurbitaceous plants and at the lower epicotyl portion in solana- placing the scion on the rootstock (Fig. 2D and E), ordinary graft-

Fig. 2. Major grafting methods in cucurbits and solanaceous vegetables: (A and B) hole insertion grafting; (C) tongue approach grafting; (D, E and J) splice grafting; (F, G)
cleft grafting; (H and I) pin grafting.
102 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

ing clips as in tongue approach grafting are used to fix the grafted


position tightly together. This is the most common methods for
cucurbits and also called as one cotyledon splice grafting (OC-SG).
For solanaceous crops, grafting is usually made at lower epicotyl
and fixed (Fig. 2J) with ordinary clips, elastic tube-shaped clip with
side slit, or ceramic pins (see Section 4.1.5) developed specifically
for this type of grafting. Tube grafting is performed by holding the
grafted position together in a slit elastic tube rather than using the
usual grafting clips. The tube may be used several times depending
upon the materials.

4.1.4. Cleft grafting (CG)


Cleft grafting (Fig. 2F and G) in herbaceous plants may be some-
what different from those of woody plants. Usually a portion of the
stem is cut longitudinally. The rootstock seedlings are decapitated
and longitudinal cut is made in a downward direction, 1–1.5 cm
long and 3/4 depth of the stem diameter. The scion is pruned to
have 1–3 true leaves and the lower stem is cut to slant angle to
make a tapered wedge. After placing the scion into the split made
on the rootstock, a clip is placed to hold in position until the union.
Various types of grafting clips, differing in material, size, shape,
and others, have been developed for cleft grafting. Cleft grafting
had been used in cucurbits for a while in several countries, but the
use is usually confined to solanaceous crops these days.

4.1.5. Pin grafting (PG)


Pin grafting (Fig. 2H and I) is basically the same as the splice
grafting. However, instead of placing grafting clips to hold the Fig. 3. HIG grafted watermelon seedlings ready for transplanting.
grafted position, specially designed pins are used to hold the grafted
position in place. The ceramic pin developed by Takii Seed Co., in ers in different parts of the world. A special knife with self-feeding
Japan is about 15 mm long and 0.5 mm in diagonal width of the connection of skimmed milk or alcohol to inactivate some potent
hexagonal cross-section. The pins are made of natural ceramic so it viruses has been developed in The Netherlands and in Korea. A
can be left on the plant without any problem. The price of ceramic hand held grafting device constructed with changeable stainless
pin is fairly high so that alternative methods are being sought. steel, single-edge razor blades, makes it possible to simultaneously
Experimental results revealed that bamboo pins, rectangular in create a uniform wedge and a receptacle in the stem of Phaseolus
cross-sectional shape, could successfully replace the expensive vulgaris. Rapid changes have been taking place recently and it is evi-
ceramic pins at much lower price. Watermelon seedlings grafted by dent that marked progress will be made on these devices with the
HIG described above are shown in Fig. 3 and a solanaceous grafted improvement of grafting technology and introduction of new and
plant near maturity is shown in Fig. 4. efficient grafting robots. Uniformly small seedlings are definitely
favored for grafting, especially for machine grafting, so that experi-
4.2. Tools, clips, and grafting aids

A number of grafting tools to perform automated grafting and to


hold the graft union together have been developed by various agri-
cultural companies (Lee and Oda, 2003). Unfortunately, however,
most of them have not been widely used by the commercial grow-
ers. Simple grafting aids, such as grafting clips, tubes, tapes, and
pins have been selectively but widely used for grafting (Fig. 5). The
ordinary grafting clips consisting of a round spring made out of plas-
tic (Fig. 5A) have been most extensively used for tongue approach
grafting in cucurbits and other crops. The clips, although slightly
different in size and shape depending upon manufacturer, are inex-
pensive, ease to operate and handle for various stem sizes, and can
be used many times. Various other clips, especially elastic tube-
shaped clips with or without attachment for supporting pole for
the grafted seedlings (Fig. 5B and C), are also widely used by many
commercial growers for manual grafting as well as for machine
or robot grafting. Much smaller elastic slit-tubes are being used in
many countries including Israel and The Netherlands (Fig. 5E) for
tomato and pepper grafting. Ceramic pin (Fig. 5D) is a very handy
and efficient aid to fix the grafted interface, and highly suitable for
machine or robot grafting. It can be used with naked hands, with
simple pencil-shaped device, or with machine or robots. Adhesive
tape or glue, or sometimes aluminum foil, is another means of hold-
ing the grafted counterparts in place. Specially designed knives and
gimlets for grafting have been manufactured and are used by grow- Fig. 4. Tomato grafted onto potato plants near harvest time.
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 103

tively reasonable prices. Three grafting robots have been developed


in Korea, 2 in 1998 and 1 in 1999, and one was commercialized
in 2001. The pin grafting robot developed by Rural Development
Administration for solanaceous crops can graft 1200 seedlings per
hour. The simple and economic grafting machine was developed
by Yupoong and has been very popular in Korea. This machine
by Yupoong, priced about US $500, has been exported for more
than 10 years to many Asian countries and some European coun-
tries. This machine can graft up to 600 seedlings per hour by
tongue approach grafting, mostly in cucurbitaceous crop. However,
an experienced operator is needed to run this machine effec-
tively and efficiently. Recently a multiuse semi-automatic grafting
machine has been developed by a private company in Korea (Helper
RoboTech) and many growers purchased this machine to graft
tomato and pepper plug seedlings. This machine (Fig. 6) has also
been actively exported to many foreign countries in recent years
because of the reasonable price, multiple functions (can be used
Fig. 5. Grafting clips, tubes, pins, and other aids. for both cucurbit and solanaceous crops), and convenient handling.
More recently, a fully automated grafting robot (1000 grafts per
hour) has been developed and used commercially for tomato in
enced growers are eager to produce uniform healthy seedlings for The Netherlands (ISO GROEP). With increasing demand of grafted
efficient grafting by using better quality seeds preferably primed plants, faster, more reliable, and more flexible automation of graft-
seeds. ing operations is one of the key technologies need to develop in the
future.
4.3. Grafting machines and robots
4.4. Acclimatization
The first robot, the “One Cotyledon Splice Grafting” system was
developed in 1980s by Iam Brain in Japan to graft cucurbit veg- Proper acclimatization is critical for grafted plants to survive.
etables (similar to the latest Korean version shown in Fig. 6). The Acclimatization involves healing of the cut surface and hardening
robot took into account variation of seedling shape, location of for field or greenhouse survival (Lee and Oda, 2003). Maintenance
cutting and gripping, cutting, and attachment. Seedlings were cut of proper moisture content before and after grafting is critical for
at the point of attachment of the cotyledon to the hypocotyl at the production of uniform grafted seedlings. Acclimatization may
an angle of 20◦ –30◦ for the scion and the rootstock, respectively. be achieved simply by enclosing the rootstock and scion in a black
The prototype grafting robot was constructed in 1987 and the plastic bag (to avoid heat buildup) until the union is formed. Grow-
second in 1989 (Ito, 1992; Kubota et al., 2008). It took 4.5 s to ers usually achieve acclimatization by use of plastic film coverings.
make a grafted plant with 95% survival. The demonstration model In many commercial nurseries, the grafted plants, usually in cell
robot was deemed practical and the results were transferred to trays of 32–72 cells, are placed on a greenhouse bench and the trays
an agricultural machinery company that developed machines for are sealed with a single layer of semi-transparent high-density
the market. Prototype semi-automatic grafting system was also polyethylene film (0.01 mm or thinner) to reduce the moisture loss
developed in Korea. Several grafting robots have been manufac- and kept sealed for 5–7 days without additional irrigation. Par-
tured by the Rural Development Administration (RDA), Korea, and tial shading may be needed during the daytime to avoid excessive
will be distributed to the commercial plug seedling growers at rela- heat build-up. Several types of acclimatization chambers have been
developed and widely used by commercial plug seedling growers
in Japan and Korea (Lee et al., 2008).

5. Commercial production and quality of grafted seedlings

High-quality grafted seedlings are usually produced by profes-


sional seedling growers rather than individual farmers. The overall
quality as well as the price of those grafted seedlings produced
by large commercial growers is much higher than those produced
by smaller growers or farmers’ associations. However, the sale of
these grafted seedlings grown in cell trays has been grown explo-
sively during the last decades. Even though there are considerable
differences in quality of plug-grown seedlings depending upon the
growers as well as the substrate, farmers would like to order their
seedlings grafted on preferred combinations from the industrial
growers. Most of the seedlings are grown in trays of different num-
ber of cells. The cell trays in Korea are the same in size and the
seedlings are easy to handle for grafting and transport including
export and also can be efficiently transplanted by machine. Even
though problems arising from the use of grafted seedlings are rather
common especially with respect to seedling health and quality of
Fig. 6. Semi-automatic grafting machine developed by Helper Robotech Co., in
produces, more farmers are purchasing grafted seedlings rather
Korea. than grafting their own seedlings.
104 J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105

Since more and more farmers are purchasing grafted trans- 6. Conclusions and prospects
plants from professional nurseries, the quality has become one of
the keen concerns among the farmers. The quality of transplant For decades, vegetable grafting has been successfully practiced
varies greatly depending upon the growers and also by substrates. in many Asian countries, and is becoming increasingly popu-
The definition of high-quality seedling would be very complicated lar worldwide. Many multinational seed companies are eager to
task because so many factors are associated with quality evalua- develop and distribute rootstock seeds through their commercial
tion. Seedlings are in the first place normal and abnormal seedlings seed catalogs. Identification of compatible multi-disease resistant
based upon the external appearance. Various factors influence the rootstocks with tolerance to abiotic stresses is a basic require-
outcome of abnormal seedlings. Uniformity in terms of genetic ment for continued success. Watermelon and tomato are the 2
quality and cultural and/or physiological quality are the 2 major major vegetables for grafting and worldwide distribution. Grafting
factors influencing seedling quality (Lee, 2007). Mineral deficiency in herbaceous plants is also practiced in cucumber, melon, orien-
in the soil or substrate, frost damage, heating, mechanical dam- tal melon, greenhouse squash, eggplant, and peppers. Introduction
age, insect damage, chemical treatment injury, declining vigor, of excellent rootstocks possessing multiple disease resistance and
pathogen infections, water and temperature stresses, and many efficient grafting machines including grafting robots will greatly
others. In vegetable seedlings, the quality of seedling also varied encourage the extended use of grafted vegetables over the world.
greatly depending upon the kind of crops and types of seedling There are many problems commonly associated with vegetable
distribution such as seedlings without soil or substrate, seedlings grafting and cultivating grafted seedlings as seen in Table 1. These
grown in conventional pots, or seedlings grafted or non-grafted, include the additional cost for rootstock seeds, labor required
or seedlings grown in cell trays. The performance check of the for the grafting and raising grafted seedlings, lack of experience
seedlings would be the best way to evaluate the seedling qual- and technique for grafting and cultivation of grafted plants, and
ity, but this is almost impossible, because so many other factors incidence of possible physiological disorders associated with graft-
also influence the seedling performance after the transplanting. ing. However, there are enormous benefits from using grafted
Therefore, the quality of seedlings is mostly evaluated at the time of seedlings. These include income increase by high yield and off-
transplanting or seedling purchase at the commercial nurseries. On season growing, lower input of fertilizers and irrigation water
the basis of this concept, the high-quality seedlings should be uni- due to the wide root systems of the rootstocks, considerable sav-
form in size and traits, proper size or height with thick healthy stem ing in agrochemicals due to high resistance of the rootstocks,
with large thick leaves. The seedling should have well-developed extension of the harvest period, efficient maintenance of popu-
root systems and show good shoot/root ratio. Seedlings for fruit lar cultivars against diseases and other physiological disorders, no
production should have large number of flowers in good vigor. need for long-term crop rotations, overcoming problems due to
Those seedlings for leaf such as lettuces and cabbages should not saline soils and thermal stress, ease of producing organically grown
bolt after transplanting. The seedlings should not be exposed to vegetables. Partial or full take of these benefits will depend upon
extreme water and/or temperature stresses during their growth various factors such as farm size and degree of mechanization,
stage. cultivation practices such as crop rotation and transplanting, tech-
One of the conveniently used parameters to evaluate the nology level, understanding the full benefits and risks of grafted
seedling quality is the ratio of shoot dry weight divided by shoot seedlings, and the uses of protected cultivation and hydropon-
length. This may be appropriate for tomatoes, peppers, and egg- ics.
plants. However, in cabbages and Chinese cabbages, different Growers can now purchase grafted seedlings of any specific
criteria should be adapted and so are the cucurbits. Perhaps, the combination from many commercial plug seedling growers rather
critical factor involved in seedling quality is the infection of serious than doing the tedious grafting themselves although growers
bacterial and viral diseases which may not be easily recognized at need to place orders in advance in most cases. This is especially
the time of seedling purchase. Serious outbreaks of tomato bacte- true in Japan, Korea, and The Netherlands. With the invention
rial canker had been reported in Mexico caused by infected seeds, of more efficient grafting robots and acclimatization facilities,
causing closure of a commercial propagation in Mexico who was a the price of grafted seedlings could be considerably reduced in
main supplier of grafted seedlings (Kubota et al., 2008, pers. com- the future to meet grower expectations. Grafted seedlings can
mun.). Serious outbreaks of cucumber green mottle mosaic virus solve much of the problems arising from conventional cultiva-
(CGMMV), a strain of tobacco mosaic virus (TMV), in many parts tion such as use of methyl bromide for soil sterilization, incidence
of the world, causing tremendous damage to the farmers as well as well as the rapid spread of diseases caused by successive
as the seed companies who supplied the virus-infected rootstock cropping, low soil temperature damage during the early stages,
seeds for watermelon seedling production. Since the spread of these heavy use of pesticides and chemical fertilizers, and economic
diseases is phenomenal, the presence of a single infected plant can use of irrigation water. For organic produces, the seeds of both
destroy the entire field. Two large seed companies in Korea were scion and rootstock may be treated with dry heat to eliminate
bankrupted after serious outbreaks in 1997 and 2000. seed-borne diseases such as Fusarium and viruses. Effective dry
CGMMV can be transmitted by seeds, contact, grafting, and heat treatment method has been developed and rapid detection
some other means such as soil and water. Dry heat treatment is technique on the inactivation of some seed-borne virus, such
the only practical way of eliminating this virus from infected or as cucumber green mottle mosaic virus, has also been estab-
infection-suspected seeds and has been used routinely for all the lished. Even though the benefits of using grafted seedlings are
cucurbits seeds in Japan and Korea (Kim and Lee, 2000). Production now fully recognized over the world, production of uniform,
of organic vegetables using pesticide-free seeds can only be per- healthy grafted seedlings at reasonable prices is the key point
formed by using dry heat treatment in various vegetables including for wider use, especially in those countries with limited experi-
lettuce and Brassica crops. However, production, supply, and use ence.
of healthy seeds should be the first choice for the production of
healthy seedlings, especially in cucurbits and solanaceous crops.
Overuse or misuse of bioregulators or chemical inhibitors to sup- Acknowledgements
press the overgrowth of seedlings grown in high-density cell trays
is another problem to be minimized and replaced by other physical Critical reading of this manuscript by Dr. Jules Janick of the USA
means. is deeply appreciated.
J.-M. Lee et al. / Scientia Horticulturae 127 (2010) 93–105 105

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