Defense Mechanisms Involved in Disease Resistance of Grafted Vegetables

By W. Guan, Xin Zhao, R. Hassell, J. Thies. 2012

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Grafting with resistant rootstocks is an effective strategy to manage a variety of soilborne diseases and root-knot nematodes in solanaceous and cucurbitaceous vegetables. In addition, improved resistance to some foliar diseases and viruses has also been reported in grafted plants. Hence, grafting technology is considered an important and innovative practice of integrated pest management and a promising alternative for soil fumigants in vegetable production. Inherent resistance within rootstocks and improved plant nutrient uptake are generally suggested as the main reasons for improved disease control in grafted vegetables. However, increasing evidence indicated that systemic defense mechanisms may also play an important role in plant defense as a result of grafting. This review analyzes current literature on the use of grafting techniques for disease management in vegetable crops, discusses potential mechanisms associated with grafting-conferred plant defense, and identifies needs for future research to promote more effective and efficient use of grafting technology to support sustainable vegetable production. Grafting, with selected resistant rootstocks, for the purpose of controlling diseases and pests is an ancient practice widely used in cultivating a variety of woody trees. Some of the well-known examples include controlling tristeza on citrus, fireblight and collar rot on apples, and nematodes on peaches and walnuts (Mudge et al., 2009). Research on herbaceous vegetable grafting began in the 1920s with watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] grafted onto squash rootstocks (Cucurbita moschata Duch.) to overcome yield loss caused by fusarium wilt (Sato and Takamatsu, 1930). Since then, grafting has been widely used in Asia and European countries as an effective tool for managing several soilborne diseases and root-knot nematodes in the Solanaceae and Cucurbitaceae. Interest in vegetable grafting has recently grown in the United States as an alternative to soil fumigants and as an integrated pest management practice in various crop production systems (Kubota et al., 2008). A few reviews have been published recently, which address the integrated use of grafting techniques in vegetable production. Among them, a review by Lee and Oda (2003) covered topics including grafting methods and procedures, grafting physiology, and production status of grafted vegetables and ornamental crops. Cucurbit grafting including the history, current status, and benefits of vegetable grafting were well documented by Davis and colleagues (2008). Louws and coauthors (2010) summarized current literature on use of grafting technology to manage diseases and pests in vegetable production. The review provided up-to-date information on disease cycles, current disease management practices, and effects of rootstocks on controlling different pathotypes. Some important disease resistance mechanisms were mentioned, whereas systematic discussion of this topic was rather limited. Unlike previous work, the current review explores specifically the defense mechanisms in grafted vegetable plants and discusses future research initiatives needed to advance our understanding of the underlying grafting mechanisms and to enhance vegetable rootstock breeding programs. Diseases Controlled by Grafting in Vegetable Production Improved resistances to many soilborne fungal, oomycete, bacterial, and nematode pathogens have been reported in grafted solanaceous and cucurbitaceous crops. Moreover, certain foliar fungal and viral diseases were suppressed when susceptible scions were grafted onto specific rootstocks (Louws et al., 2010). Diseases controlled by grafting in different vegetable crops are listed in Table 1. Soilborne fungal and oomycete diseases. The earliest reported use of vegetable grafting for disease control was for management of fusarium wilt in cucurbits (Sakata et al., 2005). Commonly used cucurbitaceous rootstocks are non-hosts to most formae speciales of F. oxysporum, and thus grafting has been successfully used to control fusarium wilt in cucurbit production (Louws et al., 2010). Verticillium wilt, primarily caused by Verticillium dahliae, is another vascular wilt disease that often affects Solanaceae and Cucurbitaceae. Studies with plants grafted onto commercial rootstocks and subjected to infection with V. dahliae indicated that both scions and rootstocks contributed to disease resistance of the grafted combinations in watermelons, melons (Cucumis melo L.), cucumbers (Cucumis sativus L.), and tomatoes (Solanum lycopersicum L.) (Paplomatas et al., 2002). Monosporascus sudden wilt, caused by Monosporascus cannonballus, is an important soilborne disease of melon and watermelon in hot and semiarid areas. Grafting scions of susceptible melon cultivars onto C. maxima Duch. and C. maxima · C. moschata rootstocks improved resistance of melon (Edelstein et al., 1999) although Cucurbita is normally regarded as a host for M. cannonballus (Mertely et al., 1993). However, the improved resistance and better yield with grafted plants was inconsistent. The variable results might be attributed to differences in rootstock–scion combinations and growing conditions. Phytophthora blight, caused by Phytophthora capsici, is regarded as one of the most destructive diseases in production of cucurbits. In P. capsici-infested fields, yields of cucumbers grafted on bottle gourd [Lagenaria siceraria (Mol.) Standl.], C. moschata Duch., and wax gourd [Benincasa hispida (Thunb.) Cogn.] rootstocks were significantly increased and vegetative growth was more vigorous (Wang et al., 2004). Watermelons grafted onto selected bottle gourd rootstocks also exhibited resistance to P. capsici (Kousik and Thies, 2010). Corky root disease caused by Pyrenochaeta lycopersici is a severe problem for Solanaceae. Tomatoes grafted onto ‘Beaufort’ rootstocks (S. lycopersicum · S. habrochaites S. Knapp & D.M. Spooner) had lower disease incidence, higher yield, and larger fruit (Hasna et al., 2009). Similar results were also found in grafted eggplants (S. melongena L.) (Iouannou, 2001). Soilborne bacterial diseases. Tomato bacterial wilt, caused by Ralstonia solanacearum, is one of the most destructive diseases of tomato. Resistance to bacterial wilt in tomatoes is a quantitative trait and is closely associated with small fruit size (Louws et al., 2010). Thus, few resistant tomato cultivars are commercially available (King et al., 2010). Grafting scions of susceptible tomato cultivars onto Received for publication 6 Sept. 2011. Accepted for publication 13 Dec. 2011. We thank Drs. Peter J. Dittmar and Guodong Liu for providing comments before the original manuscript was submitted. To whom reprint requests should be addressed; e-mail zxin@ufl.edu. 164 HORTSCIENCE VOL. 47(2) FEBRUARY 2012 resistant rootstocks has been successful for managing tomato bacterial wilt (Lin et al., 2008; Matsuzoe et al., 1993). The improved resistance in grafted plants may result from limited colonization in the lower stem rather than prevention of bacteria from invading xylem tissues (Grimault and Prior, 1994). Root-knot nematodes. Root galling of susceptible plants is a typical response to root-knot nematode (RKN; Meloidogyne spp.) infection, resulting in poor absorption of water and nutrients. In cucurbits, resistance to M. incognita was identified in Cucumis metuliferus Naud., Cucumis ficifolius A. Rich., and bur cucumber (Sicyos angulatus L.) (Fassuliotis, 1970; Gu et al., 2006). Using C. metuliferus as a rootstock to graft RKNsusceptible melons led to lower levels of root galling and nematode numbers at harvest (Sigüenza et al., 2005). Moreover, C. metuliferus showed high graft compatibility with several melon cultivars (Trionfetti Nisini et al., 2002). Cucumbers grafted on the bur cucumber rootstock exhibited increased RKN resistance (Zhang et al., 2006). Promising progress has also been made in developing M. incognita-resistant germplasm lines of wild watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai var. citroides (L. H. Bailey) Mansf.] for use as rootstocks (Thies et al., 2010). However, at present, cucurbit rootstocks with resistance to RKN are not commercially available (Thies et al., 2010). The Mi gene, which provides effective control against RKN in tomato, has been introgressed into cultivated tomatoes and rootstock cultivars (Louws et al., 2010). Grafting of susceptible tomato cultivars on RKN-resistant rootstocks was effective in controlling RKN in fields naturally infested with RKN (Rivard et al., 2010). However, as a result of temperature sensitivity of the Mi gene, such resistance may not be uniformly stable (Cortada et al., 2009). Pepper (Capsicum annuum L.) cultivars possessing the N gene, which controls resistance to RKNs (M. incognita, M. arenaria, and M. javanica), have been effective as rootstocks to control RKNs in pepper (Oka et al., 2004; Thies and Fery, 1998, 2000). Viral diseases. Vegetable grafting research on resistance to viral diseases yielded mixed results because of the lack of systematic studies in this area. Wang et al. (2002) reported improved antivirus performance in grafted seedless watermelon plants. In Israel, use of resistant rootstocks for controlling the soilborne melon necrotic spot virus in cucurbits was a significant advantage over soil fumigation with methyl bromide, which does not control this viral disease (Cohen et al., 2007). Meanwhile, tomato yellow leaf curl virus, tomato spotted wilt virus, and pepino mosaic virus were also reported to be controlled by grafting (Louws et al., 2010). However, some reports indicated that grafted plants were more vulnerable to viral diseases, possibly as a result of graft incompatibility that weakened the scion plants (Davis et al., 2008). Other diseases. Other fungal diseases that have been controlled by grafting include target leaf spot (caused by Corynespora cassiicola) on cucumbers, black root rot (caused

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