Defense Mechanisms Involved in Disease Resistance of Grafted

HORTSCIENCE 47(2):164–170. 2012. pathogens have been reported in grafted solanaceous and cucurbitaceous crops. Moreover, certain foliar fungal and viral diseases were Defense Mechanisms Involved suppressed when susceptible scions were grafted onto specific rootstocks (Louws et al., in Disease Resistance of 2010). Diseases controlled by grafting in different vegetable crops are listed in Table 1. Grafted Vegetables Soilborne fungal and oomycete diseases. The earliest reported use of vegetable graft- Wenjing Guan and Xin Zhao1 ing for disease control was for management Horticultural Sciences Department, University of Florida, 1301 Fifield Hall, of fusarium wilt in cucurbits (Sakata et al., Gainesville, FL 32611 2005). Commonly used cucurbitaceous rootstocks are non-hosts to most formae speciales Richard Hassell of F. oxysporum, and thus grafting has been Clemson University CREC, 2700 Savannah Highway, Charleston, SC 29414 successfully used to control fusarium wilt in cucurbit production (Louws et al., 2010). Judy Thies Verticillium wilt, primarily caused by Verti- USDA ARS U.S. Vegetable Laboratory, 2700 Savannah Highway, Charleston, cillium dahliae, is another vascular wilt disease that often affects Solanaceae and Cucurbita- SC 29414 ceae. Studies with plants grafted onto com- Additional index words. Cucurbitaceae, induced resistance, microbial community, nutrient mercial rootstocks and subjected to infection uptake, rootstock, Solanaceae with V. dahliae indicated that both scions and rootstocks contributed to disease resistance Abstract. Grafting with resistant rootstocks is an effective strategy to manage a variety of of the grafted combinations in watermelons, soilborne diseases and root-knot nematodes in solanaceous and cucurbitaceous vegeta- melons (Cucumis melo L.), cucumbers bles. In addition, improved resistance to some foliar diseases and viruses has also been (Cucumis sativus L.), and tomatoes (Solanum reported in grafted plants. Hence, grafting technology is considered an important and lycopersicum L.) (Paplomatas et al., 2002). innovative practice of integrated pest management and a promising alternative for soil Monosporascus sudden wilt, caused by fumigants in vegetable production. Inherent resistance within rootstocks and improved Monosporascus cannonballus, is an impor- plant nutrient uptake are generally suggested as the main reasons for improved disease tant soilborne disease of melon and water- control in grafted vegetables. However, increasing evidence indicated that systemic defense melon in hot and semiarid areas. Grafting mechanisms may also play an important role in plant defense as a result of grafting. This scions of susceptible melon cultivars onto C. review analyzes current literature on the use of grafting techniques for disease manage- maxima Duch. and C. maxima · C. moschata ment in vegetable crops, discusses potential mechanisms associated with grafting-conferred rootstocks improved resistance of melon plant defense, and identifies needs for future research to promote more effective and (Edelstein et al., 1999) although Cucurbita efficient use of grafting technology to support sustainable vegetable production. is normally regarded as a host for M. cannonballus (Mertely et al., 1993). However, Grafting, with selected resistant root- A few reviews have been published re- the improved resistance and better yield with stocks, for the purpose of controlling diseases cently, which address the integrated use of grafted plants was inconsistent. The variable and pests is an ancient practice widely used in grafting techniques in vegetable production. results might be attributed to differences in cultivating a variety of woody trees. Some of Among them, a review by Lee and Oda (2003) rootstock–scion combinations and growing the well-known examples include controlling covered topics including grafting methods and conditions. Phytophthora blight, caused by tristeza on citrus, fireblight and collar rot on procedures, grafting physiology, and produc- Phytophthora capsici, is regarded as one of apples, and nematodes on peaches and wal- tion status of grafted vegetables and orna- the most destructive diseases in production of nuts (Mudge et al., 2009). mental crops. Cucurbit grafting including the cucurbits. In P. capsici-infested fields, yields Research on herbaceous vegetable grafting history, current status, and benefits of vege- of cucumbers grafted on bottle gourd [Lage- began in the 1920s with watermelon [Citrullus table grafting were well documented by Davis naria siceraria (Mol.) Standl.], C. moschata lanatus (Thunb.) Matsum. & Nakai] grafted and colleagues (2008). Louws and coauthors Duch., and wax gourd [Benincasa hispida onto squash rootstocks (Cucurbita moschata (2010) summarized current literature on use (Thunb.) Cogn.] rootstocks were significantly Duch.) to overcome yield loss caused by of grafting technology to manage diseases and increased and vegetative growth was more fusarium wilt (Sato and Takamatsu, 1930). pests in vegetable production. The review pro- vigorous (Wang et al., 2004). Watermelons Since then, grafting has been widely used in vided up-to-date information on disease cy- grafted onto selected bottle gourd rootstocks Asia and European countries as an effective cles, current disease management practices, and also exhibited resistance to P. capsici (Kousik tool for managing several soilborne diseases effects of rootstocks on controlling different and Thies, 2010). Corky root disease caused and root-knot nematodes in the Solanaceae pathotypes. Some important disease resistance by Pyrenochaeta lycopersici is a severe prob- and Cucurbitaceae. Interest in vegetable graft- mechanisms were mentioned, whereas system- lem for Solanaceae. Tomatoes grafted onto ing has recently grown in the United States as atic discussion of this topic was rather limited. ‘Beaufort’ rootstocks (S. lycopersicum · S. an alternative to soil fumigants and as an Unlike previous work, the current review habrochaites S. Knapp & D.M. Spooner) had integrated pest management practice in var- explores specifically the defense mechanisms lower disease incidence, higher yield, and ious crop production systems (Kubota et al., in grafted vegetable plants and discusses fu- larger fruit (Hasna et al., 2009). Similar re- 2008). ture research initiatives needed to advance sults were also found in grafted eggplants our understanding of the underlying grafting (S. melongena L.) (Iouannou, 2001). mechanisms and to enhance vegetable root- Soilborne bacterial diseases. Tomato bac- stock breeding programs. terial wilt, caused by Ralstonia solanacearum, is one of the most destructive diseases of Received for publication 6 Sept. 2011. Accepted tomato. Resistance to bacterial wilt in toma- for publication 13 Dec. 2011. We thank Drs. Peter J. Dittmar and Guodong Liu Diseases Controlled by Grafting toes is a quantitative trait and is closely associ- for providing comments before the original manu- in Vegetable Production ated with small fruit size (Louws et al., 2010). script was submitted. Thus, few resistant tomato cultivars are com- 1To whom reprint requests should be addressed; Improved resistances to many soilborne mercially available (King et al., 2010). Grafting e-mail zxin@ufl.edu. fungal, oomycete, bacterial, and nematode scions of susceptible tomato cultivars onto

164 HORTSCIENCE VOL. 47(2) FEBRUARY 2012 REVIEW

Table 1. Diseases reported to be controlled by grafting in different vegetable crops. Colletotrichum coccodes) on tomatoes and Disease and pest Pathogen Crops eggplants, and Rhizoctonia damping off Fungal and oomycete diseases (caused by Rhizoctonia solani) on tomatoes Fusarium wilt Fusarium oxysporum Tomato, pepper, watermelon, (King et al., 2008; Louws et al., 2010) (Table melon, cucumber 1). Grafting has also been reported to im- Fusarium crown and root rot Fusarium oxysporum; Tomato, pepper, watermelon prove crop resistance to the foliar fungal Fusarium solani diseases such as powdery mildew (caused Verticillium wilt Verticillium dahliae Tomato, eggplant, watermelon, by Podosphaera xanthii) and downy mildew melon, cucumber (caused by Pseudoperonospora cubensis)on Monosporascus sudden wilt Monosporascus cannonballus Watermelon, melon Phytophthora blight Phytophthora capsici Tomato, pepper, watermelon, cucumbers, when certain rootstocks were cucumber used (Louws et al., 2010; Sakata et al., 2006). Corky root Pyrenochaeta lycopersici Tomato, eggplant Target leaf spot Corynespora cassiicola Cucumber Inherent Resistance within Rootstocks Black root rot Phomopsis sclerotioides Cucumber, melon as the First Line of Defense Gummy stem blight Didymella bryoniae Melon Southern blight Sclerotium rolfsii Tomato Because grafting is used primarily for con- Brown root rot Colletotrichum coccodes Tomato, eggplant trolling soilborne diseases, the defense mech- Rhizoctonia damping off Rhizoctonia solani Tomato anisms are generally associated with inherent Powdery mildew Podosphaera xanthii Cucumber Downy mildew Pseudoperonospora cubensis Cucumber resistance within rootstocks (King et al., Bacterial diseases 2008). Rootstock selection and breeding has Bacterial wilt Ralstonia solanacearum Tomato, pepper, eggplant targeted both non-host and host resistance. Nematodes Using non-host resistance. Non-host dis- Root-knot Meloidogyne spp. Cucumber, melon, watermelon, ease resistance refers to the resistance pro- tomato, eggplant, pepper vided by all members of a plant species Viral diseases against all races of a certain pathogen and it Melon necrotic spot virus Melon necrotic spot virus (MNSV) Watermelon is often considered the most common and Tomato yellow leaf curl Tomato yellow leaf curl virus Tomato durable plant disease resistance (Mysore (TYLCV) Tomato spotted wilt Tomato spotted wilt virus (TSWV) Tomato and Ryu, 2004). Solanaceous vegetables Pepino mosaic virus Pepino mosaic virus (PepMV) Tomato and cucurbits are often grafted onto root- Information was adapted from published reviews (King et al., 2008; Louws et al., 2010). stocks that, although related, are different species or hybrids of different species. Tak- ing advantage of the non-host resistance in resistant rootstocks has been successful for naturally infested with RKN (Rivard et al., these rootstocks is a convenient approach to managing tomato bacterial wilt (Lin et al., 2010). However, as a result of temperature battling specific pathogens that infect the 2008; Matsuzoe et al., 1993). The improved sensitivity of the Mi gene, such resistance may cultivated scion species but not the rootstock resistance in grafted plants may result from not be uniformly stable (Cortada et al., 2009). species. For example, F. oxysporum f. sp. limited colonization in the lower stem rather Pepper (Capsicum annuum L.) cultivars pos- niveum causes disease specifically on water- than prevention of bacteria from invading sessing the N gene, which controls resistance melon and F. oxysporum f. sp. lagenaria xylem tissues (Grimault and Prior, 1994). to RKNs (M. incognita, M. arenaria,andM. typically infects bottle gourd (Namiki et al., Root-knot nematodes. Root galling of javanica), have been effective as rootstocks to 1994). Because all of the bottle gourd geno- susceptible plants is a typical response to control RKNs in pepper (Oka et al., 2004; types offer resistance to all races of F. oxy- root-knot nematode (RKN; Meloidogyne Thies and Fery, 1998, 2000). sporum f. sp. niveum (race 0, 1, 2), non-host spp.) infection, resulting in poor absorption Viral diseases. Vegetable grafting re- resistance has been proven to be a viable of water and nutrients. In cucurbits, resis- search on resistance to viral diseases yielded mechanism to control fusarium wilt in wa- tance to M. incognita was identified in Cucu- mixed results because of the lack of system- termelons when they are grafted onto bottle mis metuliferus Naud., Cucumis ficifolius atic studies in this area. Wang et al. (2002) gourd rootstocks (Yetisir et al., 2007). A. Rich., and bur cucumber (Sicyos angulatus reported improved antivirus performance in Breeding host-resistant rootstocks. Al- L.) (Fassuliotis, 1970; Gu et al., 2006). Using grafted seedless watermelon plants. In Israel, though interspecific grafting, i.e., grafting C. metuliferus as a rootstock to graft RKN- use of resistant rootstocks for controlling the between scion and rootstock that are not from susceptible melons led to lower levels of soilborne melon necrotic spot virus in cucur- the same species, is often conducted to use root galling and nematode numbers at harvest bits was a significant advantage over soil the non-host resistance in the rootstock, in- (Siguënza et al., 2005). Moreover, C. metu- fumigation with methyl bromide, which does traspecific grafting, i.e., grafting between liferus showed high graft compatibility with not control this viral disease (Cohen et al., scion and rootstock that are from the same several melon cultivars (Trionfetti Nisini 2007). Meanwhile, tomato yellow leaf curl species, is also commonly performed, es- et al., 2002). Cucumbers grafted on the bur virus, tomato spotted wilt virus, and pepino pecially when host-resistant rootstocks are cucumber rootstock exhibited increased RKN mosaic virus were also reported to be con- available. Sometimes intraspecific grafting resistance (Zhang et al., 2006). Promising trolled by grafting (Louws et al., 2010). may be preferred because it helps enhance progress has also been made in developing However, some reports indicated that grafted graft compatibility and reduce potential det- M. incognita-resistant germplasm lines of plants were more vulnerable to viral diseases, rimental effects on fruit quality in compari- wild watermelon [Citrullus lanatus (Thunb.) possibly as a result of graft incompatibility son with interspecific grafting. Matsum. & Nakai var. citroides (L. H. that weakened the scion plants (Davis et al., Host resistance can be generally classified Bailey) Mansf.] for use as rootstocks (Thies 2008). into two categories: vertical resistance and et al., 2010). However, at present, cucurbit Other diseases. Other fungal diseases that horizontal resistance. Vertical resistance is rootstocks with resistance to RKN are not have been controlled by grafting include governed by single genes that lead to large commercially available (Thies et al., 2010). target leaf spot (caused by Corynespora and differential effects, whereas horizontal The Mi gene, which provides effective control cassiicola) on cucumbers, black root rot resistance is controlled by multiple genes against RKN in tomato, has been introgressed (caused by Phomopsis sclerotioides) on cu- with small and nondifferential effects (Fry, into cultivated tomatoes and rootstock cultivars cumbers and melons, gummy stem blight 1982). Oftentimes, the horizontal resistance (Louws et al., 2010). Grafting of susceptible (caused by Didymella bryoniae) on melons, can be unintentionally lost by continuous tomato cultivars on RKN-resistant rootstocks southern blight (caused by Sclerotium rolfsii) selection for horticultural characteristics. Many was effective in controlling RKN in fields on tomatoes, brown root rot (caused by cucurbitaceous and solanaceous rootstocks are

HORTSCIENCE VOL. 47(2) FEBRUARY 2012 165 selected from wild germplasm, and thus they respectively. Susceptible scions grafted onto a group of soil microorganisms with great are more likely to maintain nondifferential transgenic rootstocks exhibited high resis- potential to protect plants against pathogens resistance to a wide range of pathogens. tance against viral pathogens (Gal-On et al., (Doumbou et al., 2001). Although it is still During the past decades, considerable efforts 2005; Park et al., 2005; Yi et al., 2009). uncertain about the extent to which acti- have been directed into breeding plants with Future prospects. Using rootstocks with nomycetes contribute to plant disease control, resistance (R) genes against distinct patho- non-host resistance has been shown as an higher populations of actinomycetes detected gens. However, combining a complete set of effective tactic in controlling fusarium wilt in the rhizosphere of grafted plants could pos- desirable traits including horticultural char- in cucurbits. However, this method may in- sibly play a role in disease suppression when acteristics and resistance to multiple diseases crease risk of graft incompatibility if root- susceptible scions are grafted onto certain re- into a single variety is rather challenging and stocks and scions are not from the same sistant rootstocks. sometimes can be contradictory. The close species or genus. For example, figleaf gourd Future prospects. Microbial communities linkage between resistance against bacterial (Cucurbita ficifolia Bouche´) is incompati- in the rhizosphere are highly diversified and wilt in the Solanaceae and small fruit size ble with oriental melons and watermelons, influenced by several factors including plant is such an example (Louws et al., 2010). whereas wax gourd is incompatible with species, soil types, management practices, Through the use of grafting, the breeding oriental melons (Lee and Oda, 2003). and environmental conditions (Garbeva et al., programs can become more efficient and Considering the variation of graft compat- 2004). Although microbial shifts in rhizo- effective by focusing on above- and below- ibility between even closely related spe- spheres of grafted plants have been observed ground traits separately and combining dis- cies, it is always suggested to test graft in some studies and remain an intriguing area ease resistance and other horticultural traits compatibility before considering the use of for study, little is known about how these into a so-called ‘‘graft hybrid’’ (Mudge et al., non-host-resistant rootstocks for soilborne shifts are related to the intrinsic resistance of 2009). disease control. the rootstock and what processes directly Vertical resistance is often governed by Regardless of the advancement in root- cause such shifts. Some of the grafting re- cascade reactions initiated by interactions of stock resistance research, many fundamental search has focused on comparison of grafted R genes of plants with avirulence (avr) genes areas are still poorly understood, including plants to self-rooted scion plants without of pathogens, which is known as a gene-for- the effects of grafting and scion feedback on including non-grafted rootstock plants as a gene hypothesis (Flor, 1971). Identification the inherent resistance of rootstocks. Jiang positive control. To better understand effects of R genes as well as its downstream signal et al. (2010a) observed that grafted peppers of grafting on rhizosphere microbial diver- transduction is always the key to understand- had a lower incidence of fusarium root rot sity, non-grafted rootstock plants as well as ing host resistance. R genes have been iden- than self-rooted scion plants, whereas non- non-grafted and self-grafted scion control tified in many cucurbitaceous and solanaceous grafted rootstock plants showed the lowest plants should all be evaluated. Furthermore, rootstocks. One of the examples is the Mi disease incidence. It indicated that scion long-term grafting studies with different re- gene, which confers resistance to M. incognita, feedback may potentially influence rootstock sistant rootstocks, soil types, and management M. javanica, and M. arenaria in tomato. This resistance. As a result of the lack of in-depth practices are warranted to clearly elucidate the resistance involves hypersensitive responses studies on rootstock defense mechanisms, it influence of grafting on soil microbial diver- and reactive oxygen production at the feeding is even more challenging to determine the sity as related to soilborne disease control. site, restricting the establishment of the RKN effect of various scion cultivars on rootstock juveniles (Fuller et al., 2008). In the case of resistance. Elucidating the interactions of scions Contributions of Vigorous Root Systems combating fusarium wilt of melons caused by and rootstocks would greatly enhance our of Grafted Vegetables to Plant Defense four races (0, 1, 2, and 1.2) of F. oxysporum f. understanding of disease resistance of grafted sp. melonis (FOM), commercial melon culti- vegetables. Many rootstocks developed for vegetable vars containing two R genes (Fom-1 and grafting were selected or bred from wild Fom-2) provide resistance to FOM 0, 1, and Shift of Rhizosphere Microbial genotypes. In addition to specific disease re- 2 but fail to control FOM 1.2. With resistance Diversity as a Result of Grafting sistance, they are characterized by large and to FOM 1.2 identified in new breeding lines vigorous root systems (Davis et al., 2008; and indigenous cultivars of C. melo (Herman Rhizosphere microorganisms can play Lee, 1994). Soilborne pathogens often infect and Perl-Treves, 2007; Hirai et al., 2002), critical roles in suppressing soilborne dis- and damage plant roots, and, as a result, plant grafting susceptible cultivars onto resistant eases through a variety of mechanisms such nutrient and water uptake can be affected. rootstocks can be an effective and efficient as nutrient competition, antagonism, and par- Therefore, root system size and vigor may be method to control FOM 1.2 given that FOM asitism. Exploring rhizosphere microbial di- associated with resistance to soilborne dis- 1.2 resistance is polygenically inherited. versity related to plant species and genotypes, eases. Moreover, vigorous roots help improve Proteins encoded by R genes may play therefore, is another approach to understand- nutritional status and thus the overall health of a direct role in detoxification of toxins or ing soilborne disease incidence and severity plants, which may augment resistance against activation of plant defense by initiating signal (Broeckling et al., 2008; Garbeva et al., 2004; foliar diseases. transduction. Interestingly, several common Yao and Wu, 2010). Improved nutrient uptake in grafted veg- features have been identified among R gene- Studies on cucumbers grafted onto C. etables. Efficiency of nitrogen uptake and use encoded proteins from different species such moschata indicated that grafting increased can be improved by grafting vegetables onto as the leucine zipper region, nucleotide bind- the population of bacteria and actinomycetes vigorous rootstocks (Colla et al., 2010a). ing site, and leucine-rich repeats, suggesting while reducing the total number of fungi in Melon grafted onto C. maxima · C. moschata a common pathway of plant defense against the rhizosphere (Dong et al., 2010). Research rootstocks exhibited higher nitrate concen- a variety of pathogens (Hammond-Kosack and on grafted peppers also showed that acti- tration in xylem sap than that of self-rooted Jones, 1997). nomycete populations in the rhizosphere melon plants (Salehi et al., 2010). In addition, Developing transgenic rootstocks. In ad- were higher in the resistant rootstock and foliar nitrate concentrations were lower in dition to use of non-host-resistant rootstocks grafted plants compared with the self-rooted grafted watermelons and melons accompa- as well as selection and breeding for host scion control when plants were inoculated nied by higher nitrate reductase activities in resistance from a wide range of germplasm, with F. solani (Jiang et al., 2010a). Incidence comparison with self-rooted plants, which transgenic rootstocks with specific disease of verticillium wilt was reduced when a sus- suggests an elevated level of nitrogen assim- resistances have been developed. For exam- ceptible eggplant scion was grafted onto ilation in grafted plants (Pulgar et al., 2000; ple, a cucumber green mottle mosaic virus coat Solanum torvum rootstock accompanied by Ruiz and Romero, 1999). Phosphorus is a protein gene and a cucumber fruit mottle mosaic enhanced ratios of bacteria and actinomycetes macronutrient that often limits plant growth tobamovirus replicasegenewereintroduced to fungi in the rhizosphere of grafted plants as a result of its low mobility in the soil. into watermelon and cucumber rootstocks, (Yin et al., 2008). Actinomycetes represent Phosphorus uptake can be enhanced by

166 HORTSCIENCE VOL. 47(2) FEBRUARY 2012 grafting with vigorous rootstocks as con- onstrated the influence of mineral nutrients Moreover, systemic defense responses may firmed by analyzing phosphorus concentra- on plant disease development. Several min- be triggered by localized tissue damage in tions in plant tissues of grafted eggplants eral elements, including silicon, have been plants (Schilmiller and Howe, 2005). (Leonardi and Giuffrida, 2006), melons suggested to play critical roles in plant de- Does grafting with rootstocks induce (Salehi et al., 2010), and watermelons (Colla fense (Savant et al., 1996). Hasama et al. systemic defense? A proteomics study of et al., 2010b). However, variable results were (1993) showed that the increase of suscepti- leaves from cucumber plants grafted onto obtained when different rootstocks and root- bility to target leaf spot in grafted cucumbers C. moschata and leaves from self-rooted stock/scion combinations were used. In ad- with a tested rootstock might be related to cucumbers showed that the expression of dition, enhanced absorption of potassium, reduced uptake of silicon because grafted two types of proteins was significantly higher calcium, and magnesium was also observed cucumber plants with the other rootstock in grafted plants compared with self-rooted in grafted vegetables (Fernańdez-Garcıá demonstrated improved disease resistance plants. The first protein type was related to et al., 2004; Leonardi and Giuffrida, 2006). and a higher level of silicon absorption. plant defense responses, and the second type A recent review by Savvas et al. (2010) Whether vigorous rootstocks could poten- included photosynthesis-related proteins (Li summarized the research findings on mineral tially improve the uptake of silicon and other et al., 2009). Gene expressions of ‘Gala’ nutrient uptake in fruit vegetables as a result mineral elements is unknown. Exploring these apple trees (Malus pumila Mill.) grafted onto of grafting with specific rootstocks. questions in future research would be an two rootstocks, one with moderate resistance Nutrient uptake in relation to disease intriguing topic not only for vegetable graft- to fireblight (caused by Erwinia amylovora) development. Plant nutrients, in addition to ing, but also for plant pathology and nutrition and the other susceptible to fireblight, were their essential roles in plant growth and studies. examined using cDNA amplified fragment development, can be directly involved in length polymorphism. Interestingly, scions plant defense pathways. For example, foliar Grafting-induced Systemic Defense grafted onto the resistant rootstock showed application of phosphate salts can induce increased expression of stress-related genes, systemic protection against anthracnose in Plant defense to pathogen attack takes whereas scions grafted onto the susceptible cucumbers (Gottstein and Kuc´, 1989), and place primarily at two levels. The first level rootstock did not (Jensen et al., 2003). A phosphate-mediated resistance induction has involves the production of physical barriers, similar study of eggplants grafted onto to- been associated with localized cell death e.g., trichomes, to prevent or restrict patho- mato rootstocks indicated altered expression (Walters and Murray, 1992). Nitrogen de- gen invasions. The second level is derived of diverse functional genes. Functions of ficiency can compromise elicitor-induced re- from systemic plant defense mechanisms. A these genes ranged from metabolism, signal sistance to pathogen infection (Dietrich et al., diverse range of defense responses are acti- transduction, and stress response to cell cycle 2004), whereas excessive nitrogen increases vated by plant–pathogen recognition. Among and transcription/translation (Zhang et al., disease incidence by promoting growth of these responses are accumulation of reactive 2008). large plant canopies (Simoń et al., 2003). In oxygen species (ROS), production of antimi- Defense-related enzymes are often induced addition, many other mineral nutrients such crobial compounds, expression of pathogenesis- by a variety of abiotic and biotic stresses. as potassium, calcium, sulfur, and micro- related genes, synthesis of nitric oxide, and Studies have shown that plants grafted on nutrients also play significant roles in plant hypersensitive responses (Buchanan et al. certain rootstocks generally exhibit a higher defense mechanisms (Walters and Bingham, 2000). Defense responses are vital for plants; activity of defense-related enzymes com- 2007). however, these responses are also meta- pared with self-rooted plants under certain Future prospects. Although improved nu- bolically expensive. Several pre-condition- stressful conditions (Table 2). trient uptake of grafted vegetable plants ing stimuli have been investigated, including Phenylpropanoids are compounds in- might be related to grafting-conferred disease pathogen attack, in which infection by a spe- duced by various biotic and abiotic stresses. control, direct evidence is missing at present. cific type of pathogen may induce long- In response to pathogen infection, phenyl- Most currently reported grafting experiments lasting and broad-spectrum disease resistance propanoids can increase markedly to levels on nutrient uptake were conducted under to subsequent infections; such resistance is that are toxic to pathogens (Dixon and Paiva, growing conditions without disease pres- known as systemic acquired resistance (Durrant 1995). Phenylalanine ammonia-lyase (PAL) sure. It would be interesting to use disease- and Dong, 2004). In addition, pre-conditioning plays a key role in the synthesis of phenyl- resistant and vigorous rootstocks to study can include plant growth-promoting rhizo- propanoids and this enzyme activity often is absorption and functions of critical nutrients bacteria, which can reduce diseases in above- considered an indicator of plant defense in the context of plant defense against spe- ground plant parts through the induction against pathogen attack. In response to V. cific pathogens. Previous research has dem- of systemic resistance (van Loon, 2007). dahliae infection, shoots and roots of grafted

Table 2. Enzymes reported with higher activities in grafted vegetables compared with self-rooted plants. Enzymes Scion Rootstock Plant tissue Stress condition Reference Phenylalanine ammonia-lyase (PAL) Eggplant Solanum torvum Roots and Inoculation of Zhou et al., 1998 leaves V. dahliae Pepper Pepper Roots and Inoculation of Jiang et al., 2010b leaves F. solani Eggplant Solanum torvum Leaves NaCl Zhou et al., 2010 Antioxidant enzymes Peroxidase (POD), Superoxide dismutase (SOD), Eggplant Solanum torvum Leaves NaCl Li et al., 2006 Catalase (CAT) SOD, CAT Cucumber Cucurbita ficifolia Leaves NaCl Gao et al., 2008 SOD, POD, Ascorbate peroxidase (APX), Eggplant Solanum torvum Leaves Excess of Wei et al., 2009 Glutathione reductase (GR) Ca(NO3)2 SOD, POD, CAT Watermelon Lagenaria siceraria Leaves NaCl Zhu et al., 2008 CAT, dehydroascorbate reductase (DHAR), GR Tomato Tomato Leaves NaCl He et al., 2009 DHAR, GR, SOD Cucumber Cucurbita ficifolia Leaves Low temperature Gao et al., 2009a, 2009b Polyamine synthesis-related enzymes Arginine decarboxylase (ADC), ornithine Cucumber Cucurbita ficifolia Roots Copper Zhang et al., 2010 decarboxylase (ODC), S-adenosylmethionine decarboxylase (SAMDC)

HORTSCIENCE VOL. 47(2) FEBRUARY 2012 167 eggplant had higher PAL activity than self- systemic acquired resistance and activates need to be elucidated to gain a complete rooted plants (Zhou et al., 1998). Similarly, plant defense mechanisms against biotrophic understanding of rootstock–scion interactions PAL activity in roots of grafted pepper was and hemibiotrophic pathogens, whereas JA is in induced systemic defense. higher in comparison with the self-rooted usually involved in defense pathways against control both before and after inoculation with necrotrophic pathogens and herbivorous in- Concluding Remarks F. solani. Phenolic and lignin contents in sects (Bari and Jones, 2009). Although graft- leaves and roots of grafted plants were also ing could possibly induce systemic defense, Grafting technology has evolved into higher than that of self-rooted plants after few studies have explored the link between a unique component in the production of inoculation with F. solani (Jiang et al., grafting and defense-related phytohormones. several solanaceous and cucurbitaceous veg- 2010b). Rivard and Louws (2007) showed that the etables for pest management and for im- During host–pathogen interactions, ROS expression of PinII, a JA pathway-mediated provement of crop productivity. The ready can accumulate quickly and may function as proteinase inhibitor, was induced in tomato availability of disease-resistant rootstocks antimicrobial agents that are directly toxic to plants grafted on certain rootstocks. and development of highly efficient grafting pathogens or are involved in signaling to Cytokinins are a group of plant hormones techniques has led to expansion in the use of initiate plant defense cascades (Lamb and produced in the roots. It has been reported grafted plants worldwide. Previous studies Dixon, 1997). A variety of antioxidant en- that more cytokinins could be released into have provided an enhanced understanding of zymes are associated with ROS production xylem sap of cucumber scions grafted on grafting-conferred defense mechanisms from after pathogen attacks. Among them, perox- figleaf gourd rootstocks than in the xylem sap inherent resistance within rootstocks to in- idase, superoxide dismutase, and catalase are of self-rooted cucumber plants (Lee et al., duced systemic resistance. However, there is directly involved in ROS detoxification. 2010). Aloni and coworkers (2010) pointed still a lack of in-depth research on rootstock– Grafted plants had higher antioxidant en- out that the increased level of cytokinins in scion interactions and long-distance signal- zyme activities than self-rooted plants when xylem exudates of scions grafted onto certain ing as related to improved resistance in subjected to abiotic stresses such as salinity vigorous rootstocks was closely linked to the grafted plants. In addition to resistance to and low temperature (Gao et al., 2008, 2009a, improved growth and fruit yield of grafted soilborne diseases and nematodes, foliar and 2009b; He et al., 2009; Wei et al., 2009) plants. However, it is not well recognized that virus disease resistances of grafted plants (Table 2). cytokinins are also involved in the regulation warrant more studies. To differentiate the Potential signals associated with grafting- of plant defense responses against some grafting effect per se from rootstock–scion induced systemic defense. Long-distance sig- pathogens. Global gene expression analysis interactions, well-designed studies should in- naling is a central aspect of induced systemic of Arabidopsis infected by Plasmodiophora clude a complete set of non-grafted and self- resistance. Because grafting allows physical brassicae indicated a downregulation of genes grafted rootstock and scion treatments in union of root and shoot systems from different governing cytokinin homeostasis, whereas addition to the scion–rootstock grafts. Be- genetic backgrounds, long-distance signals transgenic Arabidopsis overexpressing cyto- cause crosstalk may exist among pathways may be involved in activating systemic de- kinin oxidase/dehydrogenase genes showed that cope with biotic and abiotic stresses, a fense in grafted plants. resistance to the disease (Siemens et al., 2006). comprehensive understanding of the defense In grafted cucumber studies, analysis of The uni-1D mutant in Arabidopsis that in- mechanisms in grafted plants will greatly phloem exudates collected from both the duced the expression of pathogenesis-related assist with the effective development of cucumber scions and squash rootstocks pro- genes also caused the accumulation of cyto- desirable rootstocks to serve sustainable vided direct evidence that some of the phloem kinins in Arabidopsis (Igari et al., 2008). agriculture. proteins can move across graft unions (Golecki These studies provided evidence for the et al., 1998; Tiedemann and Carstens-Behrens, possible involvement of cytokinins in plant 1994). Large-scale mass spectrometry has defense responses. Nevertheless, it is still Literature Cited been used to identify individual proteins with unclear whether and how the cytokinin pro- Aloni, B., R. Cohen, L. Karni, H. Aktas, and M. diverse functions, including structural production is directly related to disease resis- Edelstein. 2010. Hormonal signaling in root- teins, antioxidant defense compounds, pro- tance of grafted plants. stock–scion interactions. Sci. Hort. 127:119–126. teinase inhibitors, and RNA-binding proteins Future prospects. Grafting-induced sys- Bari, R. and J.D.G. Jones. 2009. Role of plant (Walz et al., 2004). It is likely that some of temic defense is an exciting field for future hormones in plant defence responses. Plant these mobile proteins might participate in study. To achieve a comprehensive under- Mol. Biol. 69:473–488. signaling cascades associated with grafting- standing of its potential roles in grafting- Broeckling, C.D., A.K. Broz, J. Bergelson, D.K. Manter, and J.M. Vivanco. 2008. Root exudates induced systemic defense. conferred disease control, it will be critical regulate soil fungal community composition Long-distance signals also may involve to identify potential signals involved in the and diversity. Appl. Environ. Microbiol. 74:738– mRNAs and small RNAs (Kehr and Buhtz, process. Studies on phloem long-distance 744. 2008). RNA transcripts, which have been macromolecular trafficking indicated that the Buchanan, B.B., W. Gruissem, and R.L. Jones. identified in the phloem, include transcrip- key signals may include proteins, mRNAs, 2000. Biochemistry and molecular biology of tional regulators, genes controlling cell fate small RNAs, and plant secondary metabolites. plants. American Society of Plant Biologists, and cell cycle, phytohormone responsive However, the individual roles of these signals John Wiley & Sons, Inc., Somerset, NJ. genes, and metabolic genes (Lough and Lucas, in plant defense are not well understood. Thus, Cohen, R., Y. Burger, C. Horev, A. Koren, and M. 2006; Omid et al., 2007). Small interfering new information regarding defense related Edelstein. 2007. Introducing grafted cucurbits to modern agriculture: The Israeli experience. RNAs (siRNAs) mediate post-transcriptional long-distance signals is needed to extend Plant Dis. 91:916–923. gene silencing, a gene expression regulation our knowledge of grafting-induced systemic Colla, G., C.M. Cardona Sua´rez, M. Cardarelli, and mechanism involved in different layers of defense. Y. Rouphael. 2010a. Improving nitrogen use plant innate immunity (Padmanabhan et al., The distinction between the grafting pro- efficiency in melon by grafting. HortScience 2009). Given that siRNAs are transmissible cess and signal transduction between rootstock 45:559–565. across grafting unions, this would be an and scion also should be closely examined. Colla, G., Y. Rouphael, M. Cardarelli, A. Salerno, intriguing field in which to explore specific Grafting can result in wounding responses that and E. Rea. 2010b. The effectiveness of graft- roles of siRNAs in grafting-induced systemic trigger changes in enzyme activities and hor- ing to improve alkalinity tolerance in water- defense. monal status, and such changes may attenuate melon. Environ. Exp. Bot. 68:283–291. Cortada, L., F.J. Sorribas, C. Ornat, M.F. Andre´s, Defense-related phytohormones, particu- with healing of the graft union. In future and S. Verdejo-Lucas. 2009. Response of larly salicylic acid (SA) and jasmonic acid research, it will be important to distinguish tomato rootstocks carrying the Mi-resistance (JA), have been widely studied with respect between the effects of the grafting process gene to populations of Meloidogyne arenaria, to their involvement in plant defense re- and rootstock–scion interactions. Changes in M. incognita and M. javanica. Eur. J. Plant sponses. 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