Abstract

Vegetables are a cornerstone of the human diet, and the importance of vegetables for human health and nutrition cannot be understated. Vegetables are susceptible to a number of biotic and abiotic stressors along with the cumulative pressure of climate change. Climate change is a major driver of the abiotic stress in modern-day vegetable production. Vegetable cropping systems must be resilient to climate change, so that production practices can achieve economic profitability and environmental sustainability. Environmental stressors, such as flooding, drought, and extreme temperatures, pose a severe threat to vegetable crop production, and total crop failures are common. Vegetable grafting, a plant surgical technique that is eco-friendly, rapid, and efficient, is currently the best alternative approach to climate change-resilient plant production that addresses these abiotic stressors. In this review, we document the success of this plant propagation technique using a review of vegetable grafting research results published in the scientific literature.

INTRODUCTION

Global climate change represents the biggest abiotic threat to plant and human health (Costello et al. 2009) and has been given immense consideration worldwide due to its potential impact on agricultural practices (Olesen & Bindi 2002; Baer & Risbey 2008). Increasing agricultural production to meet the dietary preferences of a growing population with limited resources in the face of climate change will require innovative solutions (McMichael et al. 2007). Globally, environmental stressors are the primary cause of crop failures and, on average, result in a 50% yield decrease (Reimers 2000). Importantly, vegetable production is prone to a broad spectrum of these abiotic environmental stresses, such as drought, salinity, flooding, and temperature (both low and high) (Moretti et al. 2010). Predicted impacts of global climate change on crop production have become a primary focus of the agricultural research community, and the environmental factors related to the lost yield potential of vegetable crops are day length (i.e., photoperiod reduction), water availability, and poor vernalization (Sharma et al. 2013).

According to a survey of Kays & Dias (1995), about 392 different vegetables are cultivated globally, representing 70 plant families and 225 genera. Global climate change has a significant impact on vegetable crops due to their succulent nature; vegetables are susceptible to environmental conditions and are affected by both short- and long-term climate changes. Therefore, climate change can impact vegetable crops biochemically, anatomically, morphologically, and physiologically (Fahad et al. 2017; Singh et al. 2017). Some metals like silicon and biochemicals like phenolic acids help in mitigating the stress imposed by the abiotic factors (Kaushik 2019; Kaushik & Saini 2019; Saini & Kaushik 2019). However, increased mean air temperature and humidity under a changing climate scenario may enhance the already presented insect-pest and disease pressure (Chauhan et al. 2014).

Food security is also anticipated to be impacted either directly or indirectly by varying climatic conditions (Schmidhuber & Tubiello 2007). For example, the carbon dioxide (CO2) passing through the leaf stomata at a greater concentration results in the rapid and uniform growth of transplants by affecting the photosynthesis activity (Xu et al. 2016). This CO2 effect could be applied to the healing and acclimatization of grafted transplants in commercial vegetable production. In a study of grafted pepper, transplants were healed and acclimatized following a higher concentration of CO2 (374 or 1,013 μmol·mol−1) over 6 days. This influence of CO2 enrichment resulted in higher CO2 exchange rates of the grafted pepper transplants. Overall, an increase in photosynthesis and the growth of the pepper were reported (Jang et al. 2014).

Climatic vagaries in the form of temperature fluctuations and erratic rainfall affect plant growth and the development of vegetable crops in different ways and cause a drastic reduction in economic yields (Wurr et al. 2004; Rao et al. 2016). Thus, climate change may be more challenging in vegetable production than other grain or food crops. In order to sustain vegetable production under a global climate change scenario, proper strategies are needed to manage such abiotic stresses. Various strategies were tested, such as breeding resistant cultivars and genetic engineering, but the commercialization of these technological advancements was limited due to the genetic and physiological complexity of abiotic stress resistance traits (Colla et al. 2010).

Traditional breeding methods involving large breeding cycles are time-consuming and progress slowly (Atlin et al. 2017). A grafting technique based on rootstock and scion compatibilities requires grafting sensitive or susceptible commercial cultivars onto the resistant or tolerant rootstock to manage various environmental stresses (Edelstein 2004; Altunlu & Gul 2012; Nilsen et al. 2014). Grafting is an environmentally friendly, efficient, rapid, and integrative reciprocal process in which both scion and rootstock influence the grafted plant (Sakata et al. 2007). This technique was first used in watermelon in Japan (He et al. 2009). The first scientific report presented results from grafting watermelon plant scion on pumpkin rootstock to avoid fusarium wilt. However, grafting was widely considered as a technique for woody perennial fruit crops in the 1920s and has only more recently been used in cucurbits to manage soil-borne diseases, specifically Fusarium (Davis et al. 2008; Bhatt et al. 2015).

Currently, many researchers across the world use this grafting technique to improve or increase tolerance to environmental stresses in solanaceous and cucurbitaceous crops (Mohamed et al. 2012; Johnson et al. 2014) and achieve higher yield and fruit quality (Mudge et al. 2009; King et al. 2010). Vegetable grafting is now quite a widespread practice in Asia, Europe, and the USA (Witzel et al. 2015). Indeed, grafting is useful for combating stresses and results in a better plant ideotype (Figure 1).

Figure 1

Illustration of the physiological and morphological benefits of grafted vegetable crops that enable abiotic stress tolerance.

Figure 1

Illustration of the physiological and morphological benefits of grafted vegetable crops that enable abiotic stress tolerance.

However, the latest breeding ‘omics’ technologies have only targeted tomato and potato, while other vegetables are neglected entirely (Liao & Lin 1996; Kato et al. 2001a). In this review article, we discuss the role of vegetable crop grafting for the management of environmental stresses, such as flooding, drought, thermal, and salinity, under a changing climate scenario.

Environmental stress and grafting

Environmental stress, because of a changing global climate, is the primary reason for crop loss or failure. Among the various environmental stressors, extreme temperatures, drought and flooding (due to erratic rainfall), and salinity are the major limiting factors for the sustainable production of agricultural and horticultural crops (Mittler 2006). The severity of these stresses on plants depends on the growth stage, type, and length of exposure to the stress. There are numerous studies describing the use of grafting techniques on different vegetable crops to improve tolerance against a broad spectrum of environmental stresses, and we have summarized the main results in this review article.

Flooding

Excessive moisture due to unpredictable heavy rainfall adversely affects the production of many vegetable crops due to their high sensitivity to flooding, and some vegetables are intolerant of flooded soil conditions throughout their growth and development (Liao & Lin 1996; Kato et al. 2001a). High moisture in the soil causes the reduction of oxygen in the roots of plants by altering photosynthesis and the water potential. It has been documented that grafting has been used by many research groups in various vegetable crops to improve flooding tolerance (Bhatt et al. 2015). Tomato is an example of a globally grown vegetable that is sensitive to flooding (Petran & Hoover 2014). Bhatt et al. (2015) used the interspecific grafting of tomato to improve flooding tolerance. In this experiment, a commercial tomato cultivar, Arka Rakshak, was grafted onto four eggplant rootstocks, such as BPLH-1, Neelkanth, Mattu Gulla, and Arka Keshav. The results of this study showed that grafting significantly affected yield in flooded and non-flooded conditions. After 5 days of flooding, non- and self-grafted plants died, but two combinations Arka Rakshak/Arka Keshav and Arka Rakshak/BPLH-1 exhibited better performance. It can be concluded from this study that eggplant tolerated flooded soil conditions and may be a suitable grafting rootstock to enhance the flooding tolerance of tomato. Likewise, the World Vegetable Center (AVRDC) recommended EG195 and EG203 eggplant accessions as rootstock for the tomato to enhance flooding tolerance (Black et al. 2003).

In a recent study by Bahadur et al. (2015), tomato hybrids (Arka Rakshak and Arka Samrat) were grafted onto eggplant rootstocks (IC-354557, IC-111056, IC-374873, and CHBR-2) and exposed to waterlogged conditions. Observations revealed that there were no symptoms of leaf chlorosis or plant wilting and less of a reduction in chlorophyll at all plant growth stages. In contrast, the ungrafted plants experienced 41–100% reduction in chlorophyll content after 96 h of waterlogged stress, while the plants wilted and died 4–7 days after the stress was removed. However, the grafted plants completely recovered from flooding stress within 7–10 days after exposure. So, eggplant rootstocks, namely IC-354557 and IC-111056, improved waterlogging stress tolerance for 72–96 h for the grafted tomato (Bahadur et al. 2015).

Furthermore, wild species of eggplant are also used as rootstocks of grafted tomato (Petran & Hoover 2014). In another report, Yetisir et al. (2006) found that bitter melon plants grafted onto Luffa rootstocks performed better than ungrafted plants under flooded conditions. Similarly, in watermelon, the commercial cultivar ‘Crimson Tide’ was grafted onto the Lagenaria siceraria SKP (a landrace), and symptoms of chlorosis were observed on both grafted and non-grafted plants, although symptoms were less severe on grafted plants under flooded conditions.

Nevertheless, ungrafted plants accumulated less dry weight than grafted plants under high moisture content; moreover, the decrease in fresh weight of plants was about 180% in ungrafted and 50% in grafted plants compared to the control. Dry weight also decreased by approximately 230 and 80% in non-grafted and grafted plants, respectively. These results suggest that grafted plants exhibited the formation of adventitious roots and aerenchyma tissue after 3 days, but no such observation was made for non-grafted plants under flooded conditions (Liao & Lin 1996; Kato et al. 2001a). Along the same lines as the research of Keatinge et al. (2014), Kato et al. (2001b) conducted a grafting study in waterlogged cucumber and determined that leaf chlorophyll content was enhanced when grafted onto squash rootstocks. However, recently for East Asia, the AVRDC recommended rootstock VI006378 for flood tolerance in tomato, whereas, for eggplant, the recommended rootstocks are VI045276, VI046103, VI034845, VI046104, and VI046101, respectively (Peng et al. 2013). Rootstocks can be banked upon under flooding situations for vegetables and other economically important crops (Cattivelli et al. 2008; Reynolds & Tuberosa 2008). Additional examples are provided in the Table 1.

Table 1

Examples of top-performing rootstock and scion combinations in vegetable crops under induced flooding stress

Sl. no.RootstockScionKey improved characteristicsReference
Flooding stress 
 1 Luffa (Luffa cylindria Roem) cv. Cylinder #2 Bitter melon (Momordia charanthia) cv. New Known You #3 Slight decrease in photosynthetic rate, stomatal conductance, transpiration, and the activity of RuBisCO Liao & Lin (1996)  
 2 Interspecific squash hybrid (Cucurbita maxima Duchesne X C. moschata Duchesne) cv. Shintosa-ichigou Cucumber (Cucumis sativus) cv. Kaga-aonagafushinari Triggering ethylene biosynthesis resulting in reduction in chlorophyll degradation Kato et al. (2001a, 2001b
 3 Lagenaria siceraria (Landrace) Watermelon (Citrullus lanatus (thunb.) Matsum and Nakai) cv. Crimson Tide Formation of aerenchyma tissue and adventitious roots and the reduction in the chlorophyll loss under flooded conditions Yetisir et al. (2006)  
 4 Eggplant (Solanum melongena) cv. Arka Neelkanth, Mattu Gulla, BPLH1 and Arka Keshav Tomato (Solanum lycopersicum) cv. Arka Rakshak 
  • 1.

    Lesser decline in photosynthetic rate and chlorophyll fluorescence

  • 2.

    Stomatal conductance and CO2 concentration

  • 3.

    Enhanced physiological adaptation and better fruit yield

 
Bhatt et al. (2015)  
 5 Eggplant (Solanum melongena) cv. IC-354557, IC-111056, IC-374873, CHBR-2 Tomato (Solanum lycopersicum) Hybrid line cv. Arka Rakshak, Arka Samrat Less reduction in chlorophyll content and chlorophyll fluorescence yield Bahadur et al. (2015)  
Sl. no.RootstockScionKey improved characteristicsReference
Flooding stress 
 1 Luffa (Luffa cylindria Roem) cv. Cylinder #2 Bitter melon (Momordia charanthia) cv. New Known You #3 Slight decrease in photosynthetic rate, stomatal conductance, transpiration, and the activity of RuBisCO Liao & Lin (1996)  
 2 Interspecific squash hybrid (Cucurbita maxima Duchesne X C. moschata Duchesne) cv. Shintosa-ichigou Cucumber (Cucumis sativus) cv. Kaga-aonagafushinari Triggering ethylene biosynthesis resulting in reduction in chlorophyll degradation Kato et al. (2001a, 2001b
 3 Lagenaria siceraria (Landrace) Watermelon (Citrullus lanatus (thunb.) Matsum and Nakai) cv. Crimson Tide Formation of aerenchyma tissue and adventitious roots and the reduction in the chlorophyll loss under flooded conditions Yetisir et al. (2006)  
 4 Eggplant (Solanum melongena) cv. Arka Neelkanth, Mattu Gulla, BPLH1 and Arka Keshav Tomato (Solanum lycopersicum) cv. Arka Rakshak 
  • 1.

    Lesser decline in photosynthetic rate and chlorophyll fluorescence

  • 2.

    Stomatal conductance and CO2 concentration

  • 3.

    Enhanced physiological adaptation and better fruit yield

 
Bhatt et al. (2015)  
 5 Eggplant (Solanum melongena) cv. IC-354557, IC-111056, IC-374873, CHBR-2 Tomato (Solanum lycopersicum) Hybrid line cv. Arka Rakshak, Arka Samrat Less reduction in chlorophyll content and chlorophyll fluorescence yield Bahadur et al. (2015)  

Drought

Drought is another serious water stress problem for sustainable vegetable production worldwide, resulting from water deficit under water-limiting conditions. Although breeding and biotechnological interventions have resulted in some new drought-tolerant crop varieties, these advances have been mostly limited to cereal crops (Potop et al. 2012). Certainly, water availability is highly affected by climate change which influences crop productivity, specifically that of vegetable crops, and total crop failures are common. Decreased precipitation, along with increased mean air temperature, could be the reason for the reduced availability of irrigation water. An upsurge in evapotranspiration would also be anticipated under drought conditions, as vegetables contain about 90% water (Brown et al. 1997; Thomas et al. 2007, 2011).

Under the scenario of global climate change, water availability and drought stress become critical environmental stressors (Schwarz et al. 2010). Therefore, grafting could be used to decrease production losses and increase the water use efficiency (WUE) during water scarcity. This could be accomplished by grafting high yielding susceptible commercial cultivars onto rootstocks capable of reducing the effect of water stress on the shoot. For eggplant, tomato hybrids are popular rootstocks in Europe, including Solanum spp., and interspecific hybrids. Similarly, grafting watermelon (Citrullus lanatus) onto pumpkin (Cucurbita moschata) rootstocks helps reduce the water stress of the watermelon shoots (Davis et al. 2008; King et al. 2010).

To manage or improve drought tolerance, grafting plants onto tolerant rootstock have been practised in vegetable crops, particularly in solanaceous and cucurbitaceous vegetable crops (Sánchez-Rodríguez et al. 2016). For example, a recent study was conducted by Sanchez-Rodriguez and Ruiz (Liu et al. 2016) in tomato using a drought-tolerant cultivar and drought-sensitive cultivar to obtain grafted plants in different combinations. Results of this study showed that the antioxidant enzymes varied in fruits of non-grafted and grafted plants under drought stress. In cucumber, it has been documented that grafting improved the WUE by affecting the ABA biosynthesis pathway (Sakata et al. 2007) which enhanced plant growth and yield. Osmotic manipulations occurred in accordance with the water stress level when sensitive pepper plants were grafted with the relatively tolerant rootstocks (Penella et al. 2014). The parallel study showed that the efficient production of micro- and macronutrients (vitamins and sugars) in the grafted tomato plants resulted in more plant vigor and eventually increased economic yield (Ibrahim et al. 2014).

At the genetic level, microRNAs (miRNAs) controlled the growth and development of plants and showed a specific response to various environmental stressors. According to Li et al. (2016), scion of watermelon (Citrullus lanatus) grafted onto bottle gourd (Lagenaria siceraria) or squash (Cucurbita maxima × Cucurbita moschata) rootstock elicited a change in the expression of more than 40 miRNAs. Furthermore, molecular mechanisms of 17 selected miRNAs in grafted plants under drought stress were studied in recent investigations by grafting cucumber plants onto pumpkin (Cucurbita moschata) rootstock. Consequently, the experiment involved mini-watermelon cv. Ingrid, either non-grafted or grafted using rootstock ‘PS 1313’ (Cucurbita maxima × Cucurbita moschata), and results pointed out that grafted plants exhibited higher yield, nutritional, and fruit quality-related parameters than non-grafted plants. Whereas no significant difference was observed between grafted and non-grafted plants in gas exchange and leaf water relations. However, even though sensitivity to water stress was similar between grafted and non-grafted plants, the higher marketable yield was recorded with grafting. The results of this study specifically demonstrated the benefit of rootstock ‘PS 1313’, whereas the use of grafted rootstock plants has been more broadly recommended especially under drought conditions to manage drought stress (Rouphael et al. 2008). Another study which compared drought-tolerant rootstocks for watermelon concluded that wax gourd is a better rootstock than bottle gourd under drought-prone conditions (Muneer et al. 2016). Apart from these examples of the molecular-level physiological response of grafted vegetables to drought stress, other critical physiological responses, such as changes in stomatal conductance, which increased the WUE and photosynthetic activity, have been documented in the stress-prone environment. In the case of sweet pepper grafted on the rootstock Creonte, López-Marín et al. (2017), under a Mediterranean climate, demonstrated that crop total and marketable fruit yield increased by 30 and 50%, respectively. Furthermore, this rootstock maintained 30–60% higher leaf photosynthetic activity and exhibited a significantly higher (10%) WUE. Whereas, for the tomato cultivar Amelia, improved photosynthesis and stomatal conductance were observed when the cultivar Maxifort was used as the rootstock (Chaudhari et al. 2017). Therefore, grafting drought-sensitive commercial cultivars of vegetable crops onto vigorous and tolerant/resistant rootstock would be a viable practice for plants in areas prone to water stress. The benefits of grafting demonstrated in the preceding studies included the maintenance of a high capacity for water and nutrient uptake along with the greater WUE under drought conditions. Additional examples of vegetable grafting studies conducted under drought stress are provided in Table 2.

Table 2

Examples of top-performing rootstock and scion combinations in vegetable crops under induced drought stress

Sl. no.RootstockScionKey improved characteristicsReference
Drought stress 
 1 PS 1313 (Cucurbita maxima Duchesne X Cucurbita moschata DuchesneWatermelon (Citrullus lanatus (thunb.) Matsum and Nakai) cv. Ingrid Enhanced water and nutrient uptake (N, Mg, and K) and increased CO2 assimilation Rouphael et al. (2008)  
 2 Tomato (Solanum lycopersicum) cv. Beaufort Tomato (Solanum lycopersicum) cv.M28 Increased total carotenoid and proline content, less reduction in chlorophyll b concentration, and increased biomass Altunlu & Gul (2012)  
 3 Pepper (Capsicum annum L.) cv. Verset Pepper (Capsicum annum L.) cv. Atlante, PI-15225 and ECU-973 Efficient osmotic adjustment was observed resulting in the optimum function of photosynthetic machinery in water stress conditions Penella et al. (2014)  
 4 Tomato (Solanum lycopersicum) cv. Zarina Tomato (Solanum lycopersicum) cv. Josefina Development of better radicular system and enhanced uptake of micronutrients like Fe, Cu, N, P, and K Sánchez-Rodríguez et al. (2014)  
 5 Tomato (Solanum lycopersicum L.) cv. Faridah Tomato (Solanum lycopersicum L.) cv. Unifort Grafting resulting in more vigorous plants and better fruit quality (increased vitamin C, total soluble salts, and total sugar levels) Ibrahim et al. (2014)  
 6 Tomato (Solanum lycopersicum L.) cv. Jjak Kkung Tomato (Solanum lycopersicum L.) cv. BHN 602 Reduction in aboveground growth and increase in the photosynthetic activity Nilsen et al. (2014)  
 7 Tomato (Solanum lycopersicum L.) cv. Unifort Tomato (Solanum lycopersicum L.) cv. Farida Increased WUE, growth, and yield were observed in grafted plants Wahb-Allah (2014)  
 8 Sweet pepper (Capsicum annum) rootstock lines Atlante, Terrano and Creonte Sweet pepper (Capsicum annum) cv. Herminio High photosynthetic activity, leaf water content, and more stable leaf area and the maintenance of high reproductive/vegetative ratio López-Marín et al. (2017)  
 9 Tomato (Solanum lycopersicum) cv. Beaufort and cv. Maxifort Tomato (Solanum lycopersicum) cv. Amelia Improved photosynthesis and stomatal conductance were observed Chaudhari et al. (2017)  
Sl. no.RootstockScionKey improved characteristicsReference
Drought stress 
 1 PS 1313 (Cucurbita maxima Duchesne X Cucurbita moschata DuchesneWatermelon (Citrullus lanatus (thunb.) Matsum and Nakai) cv. Ingrid Enhanced water and nutrient uptake (N, Mg, and K) and increased CO2 assimilation Rouphael et al. (2008)  
 2 Tomato (Solanum lycopersicum) cv. Beaufort Tomato (Solanum lycopersicum) cv.M28 Increased total carotenoid and proline content, less reduction in chlorophyll b concentration, and increased biomass Altunlu & Gul (2012)  
 3 Pepper (Capsicum annum L.) cv. Verset Pepper (Capsicum annum L.) cv. Atlante, PI-15225 and ECU-973 Efficient osmotic adjustment was observed resulting in the optimum function of photosynthetic machinery in water stress conditions Penella et al. (2014)  
 4 Tomato (Solanum lycopersicum) cv. Zarina Tomato (Solanum lycopersicum) cv. Josefina Development of better radicular system and enhanced uptake of micronutrients like Fe, Cu, N, P, and K Sánchez-Rodríguez et al. (2014)  
 5 Tomato (Solanum lycopersicum L.) cv. Faridah Tomato (Solanum lycopersicum L.) cv. Unifort Grafting resulting in more vigorous plants and better fruit quality (increased vitamin C, total soluble salts, and total sugar levels) Ibrahim et al. (2014)  
 6 Tomato (Solanum lycopersicum L.) cv. Jjak Kkung Tomato (Solanum lycopersicum L.) cv. BHN 602 Reduction in aboveground growth and increase in the photosynthetic activity Nilsen et al. (2014)  
 7 Tomato (Solanum lycopersicum L.) cv. Unifort Tomato (Solanum lycopersicum L.) cv. Farida Increased WUE, growth, and yield were observed in grafted plants Wahb-Allah (2014)  
 8 Sweet pepper (Capsicum annum) rootstock lines Atlante, Terrano and Creonte Sweet pepper (Capsicum annum) cv. Herminio High photosynthetic activity, leaf water content, and more stable leaf area and the maintenance of high reproductive/vegetative ratio López-Marín et al. (2017)  
 9 Tomato (Solanum lycopersicum) cv. Beaufort and cv. Maxifort Tomato (Solanum lycopersicum) cv. Amelia Improved photosynthesis and stomatal conductance were observed Chaudhari et al. (2017)  

Thermal stress

Temperature extremes can result in vegetable production losses by promoting wilt and necrosis, retarding the rate of truss appearance, and impacting the timing of fruit ripening. Grafting can be used to protect plants from thermal shock and help plants perform even better in terms of yield due to the associated physiological changes in the grafted plant (Rivero et al. 2003a). Vegetable crops are highly sensitive to both low and high temperatures. High-temperature conditions are usually seen during the growing season in a tropical environment, while during the winter, spring, and autumn season in the temperate and sub-tropical regions, chilling or low temperature is a serious problem for vegetable production especially for tomato, squash, cucumber, and watermelon.

Furthermore, low temperatures impact seed germination, seedling growth, and plant development resulting in an economic yield loss (Venema et al. 2008). For example, in tomato, high temperatures cause significant losses in crop productivity due to decreased fruit set, small fruit size, and lower fruit quality. Similarly, depending on the intensity and length of exposure, low temperature leads to irreversible dysfunction, cell death, and finally plant death. Early fruit yield and quality characteristics are also influenced by temperature. Efforts were made to develop cultivars with improved thermal stress tolerance using breeding and biotechnology but with limited commercial success since such stresses are genetically complex and plant specific. Therefore, as a rapid and efficient alternative, grafting existing elite commercial cultivars onto selected low-/high-temperature-tolerant rootstocks may be regarded as a viable plant propagation technique.

Low-temperature tolerance of the rootstock is one of the most desirable traits for vegetable production in the greenhouse during winter or early spring. den Nijs (1980) conducted a grafting experiment to manage low temperature by taking four advanced breeding lines and Cucurbita ficifolia as the rootstock in the Netherlands. This experiment illustrated that grafted plants performed outstandingly in terms of survival, longevity, and fruit quality compared to non-grafted plants under low-temperature conditions. This study was carried forward by Horvath et al. (1983) with the observation that cucumber plants grafted on C. ficifolia rootstock enhanced trans-hexadecenoic acid in phosphatidyl glycerol, which helps with low-temperature tolerance in plants. In Morocco, C. ficifolia is also the preferred rootstock for cucumbers and is an excellent rootstock for low soil temperature tolerance, particularly for spring production in winter (Besri 2008). The cultivated tomato is highly sensitive to suboptimal and chilling temperature throughout its growth and development stages. To increase tolerance to low-temperature stress in tomato, the grafting of high yielding commercial and susceptible cultivars onto tolerant rootstock is considered as a rapid technique. For instance, the tomato cultivar Moneymaker was grafted onto the Solanum habrochaites accession (LA) 1777 of the wild tomato to study the effect of low temperature by Venema et al. (2008). The authors determined that grafting tomato onto wild tomato rootstock exhibited the high relative growth rate of shoots and higher root mass ratios under low temperature as compared to selfed and non-grafted plants. Therefore, the results of this study document the wild tomato Solanum habrochaites accession (LA) 1777 as another rootstock option when managing suboptimal root zone temperature in tomato and other solanaceous vegetable crops. Additional studies in tomato also revealed the role of resistant rootstock in maintaining an optimal level of hydraulic and stomatal conductance during temperature-related stress (Bloom et al. 2004). Furthermore, such effects are known to be much weaker in grafted compared to non-grafted plants, directly reflected in higher biomass production. The results of this study suggested the practical use of grafted plants under extremely high-temperature conditions. Furthermore, the same research groups in the separate study explained that heat stress in both grafted and non-grafted tomato plants increased phenylalanine ammonia lyase (PAL) activity, increased total phenols, and increased o-diphenols, decreased polyphenol oxidase (PPO), and guaiacol peroxidase (GPX) activities and decreased dry weight. However, the influence of stress was reduced in grafted compared to non-grafted tomato plants (López-Marín et al. 2013). Better performance of grafted plants in thermal stress conditions can also be attributed to better RuBisCO activity and higher photosynthetic efficiency (Zhou et al. 2007). In the case of pepper, studies were conducted to test the behavior of non-grafted and grafted cultivar Herminio plants onto three rootstocks (Atlante, Create, and Terrano) under shaded and non-shaded conditions. The grafted plants performed better than non-grafted under both conditions. About 40% more leaf area was recorded in plants grafted onto Atlante rootstock than the other combinations but found neutral for Atlante. Grafting onto Creonteeli resulted in no significant effect on leaf biomass. However, there was a 30–50% greater total and marketable fruit yield produced by grafted plants under non-shaded and shaded conditions compared to the non-grafted plants. Thus, the rootstock Creontemay is more effective at overcoming thermal stress when grafted to sweet pepper (del Amor et al. 2008). The additional studies conducted by del Amor et al. (2008) and Colla et al. (2008) also documented that sweet pepper-grafted plants produced higher marketable yields under Mediterranean climatic conditions.

For tomato cultivation, high day and night temperatures influence fruit setting, resulting in yield loss. A study associated with high-temperature stress was conducted to test grafted plants of tomato under high-temperature stress. The plants of heat-sensitive tomato cultivar ‘UC 82-B’ were grafted onto the heat-tolerant tomato cultivar rootstock ‘Summerset’ and the eggplant cultivar rootstock ‘Black Beauty’. The results indicated that plants grafted onto the Black Beauty rootstock exhibited significantly more chlorophyll fluorescence at late fruiting stage, greater leaf area, and lower values of electrolyte leakage than non-grafted ‘UC 82-B’ at 37/27 °C (day/night), whereas no positive effect of grafting on total yield was reported by Abdelmageed & Gruda (2009). Recently, Muneer et al. (2016) demonstrated as many as 87 cellular proteins of tomato were responding to temperature fluctuation. Additional studies evaluating the use of vegetable grafting to manage thermal stress are provided in Table 3.

Table 3

Examples of top-performing rootstock and scion combinations in vegetable crops under induced thermal stress

Sl. no.RootstockScionKey improved characteristicsReference
Thermal stress 
 1 Tomato (Solanum lycopersicum) cv. RX-335 Tomato (Solanum lycopersicum) cv. Tmknvf2 
  • 1.

    Increased PAL activity

  • 2.

    Decreased PPO and GPX activity

  • 3.

    Decrease in dry weight

  • 4.

    Increase in total phenols and o-diphenols

 
Rivero et al. (2003b)  
 2 Tomato (Solanum lycopersicum) cv. LA1778 Tomato (Solanum lycopersicum) cv. T5 Root hydraulic conductance and stomatal conductance were maintained in grafted plants Bloom et al. (2004)  
 3 Figleaf Guard (Cucurbita ficifolia BouchéCucumber (Cucumis sativus) cv. Jinyan No. 4 Lesser reduction in the carboxylation activity and RuBisCO activity resulting in comparatively higher CO2 assimilation Zhou et al. (2007)  
 4 Tomato (Solanum habrochaites) breeding line LA1777 Tomato (Solanum lycopersicum) cv. Moneymaker 
  • 1.

    Higher root mass ratio

  • 2.

    High total leaf carbon concentration

 
Venema et al. (2008)  
 5 Tomato (Solanum lycopersicum) cv. Summerset and Eggplant (Solanum melongena) cv. Black Beauty Tomato (Solanum lycopersicum) cv. UC 82-B 
  • 1.

    Larger leaf area, more leaf fresh and dry weight

  • 2.

    Higher chlorophyll fluorescence

  • 3.

    More pollen grains/flower

 
Abdelmageed & Gruda (2009)  
 6 Figleaf Guard (Cucurbita ficifolia) and Luffa (Luffa cylindrica) cv. Xiangfei Cucumber (Cucumis sativus) cv. Jinyan No. 4 
  • 1.

    Higher biomass production and CO2 assimilation capacity

  • 2.

    Decrease in lipid peroxidation and protein oxidation

 
Li et al. (2014)  
Sl. no.RootstockScionKey improved characteristicsReference
Thermal stress 
 1 Tomato (Solanum lycopersicum) cv. RX-335 Tomato (Solanum lycopersicum) cv. Tmknvf2 
  • 1.

    Increased PAL activity

  • 2.

    Decreased PPO and GPX activity

  • 3.

    Decrease in dry weight

  • 4.

    Increase in total phenols and o-diphenols

 
Rivero et al. (2003b)  
 2 Tomato (Solanum lycopersicum) cv. LA1778 Tomato (Solanum lycopersicum) cv. T5 Root hydraulic conductance and stomatal conductance were maintained in grafted plants Bloom et al. (2004)  
 3 Figleaf Guard (Cucurbita ficifolia BouchéCucumber (Cucumis sativus) cv. Jinyan No. 4 Lesser reduction in the carboxylation activity and RuBisCO activity resulting in comparatively higher CO2 assimilation Zhou et al. (2007)  
 4 Tomato (Solanum habrochaites) breeding line LA1777 Tomato (Solanum lycopersicum) cv. Moneymaker 
  • 1.

    Higher root mass ratio

  • 2.

    High total leaf carbon concentration

 
Venema et al. (2008)  
 5 Tomato (Solanum lycopersicum) cv. Summerset and Eggplant (Solanum melongena) cv. Black Beauty Tomato (Solanum lycopersicum) cv. UC 82-B 
  • 1.

    Larger leaf area, more leaf fresh and dry weight

  • 2.

    Higher chlorophyll fluorescence

  • 3.

    More pollen grains/flower

 
Abdelmageed & Gruda (2009)  
 6 Figleaf Guard (Cucurbita ficifolia) and Luffa (Luffa cylindrica) cv. Xiangfei Cucumber (Cucumis sativus) cv. Jinyan No. 4 
  • 1.

    Higher biomass production and CO2 assimilation capacity

  • 2.

    Decrease in lipid peroxidation and protein oxidation

 
Li et al. (2014)  

Salinity stress

About 7% of the world area and close to 20% of the arable irrigated land are affected by soil salinity (Shahid et al. 2018). Climate change stimulates salinization, and therefore, the amount of saline land has been predicted to increase under climate change scenarios (Shrivastava & Kumar 2015). Salinity negatively affects plant production and growth. In order to overcome the impact of salinity and the use of saline soils for vegetable crop production, several strategies have been proposed. Several of the procedures that aim to reclaim saline soils are only a temporary cure and are relatively expensive to implement (Machado & Serralheiro 2017). Similarly, breeding for salt-tolerant vegetable crops has also been considered, but the complex polygenic trait that evokes salt tolerance requires several cycles of plant breeding (Ashraf et al. 2008).

The use of resistant genotypes as the rootstocks was deemed to be an easy and efficient technique for improving crop tolerance to salt stress (Koevoets et al. 2016). In the past decade, studies have investigated the salt tolerance of grafted vegetable crops and most of the studies have concluded that grafting is a highly efficient way to improve salt tolerance (Colla et al. 2010). Interspecific hybrid rootstock has improved the salt tolerance of the grafted tomato plants (Di Gioia et al. 2013). When bottle gourd was used as a rootstock, the salt tolerance capacity of watermelon plants improved several-fold (Yang et al. 2013). In the case of muskmelon, Orsini et al. (2013) found that interspecific squash rootstock (Cucurbita maxima×Cucurbita moschata Duch.) increased salt tolerance, along with plant biomass and leaf area, in the grafted muskmelon compared to non-grafted control plants. Additional studies evaluating vegetable grafting to manipulate salt tolerance are provided in Table 4.

Table 4

Examples of top-performing rootstock and scion combinations in vegetable crops under induced salinity stress

Sl. no.RootstockScionKey improved characteristicsReference
Salinity stress 
 1 
  • a)

    Macis (Lagenaria siceraria Standl., Nunhems Zaden, The Netherlands)

  • b)

    Ercole (Cucurbita maxima Duchesne X Cucurbita moschata Duchesne, Nunhems Zaden, The Netherlands)

 
Watermelon (Citrullus lanatus) cv. Tex Increased total soluble solid content, dry matter, and sugar content Colla et al. (2006)  
 2 
  • a)

    Black seeded figleaf gourd (Cucurbita ficifolia Bouché)

  • b)

    Chaofeng Kangshengwang (Lagenaria siceraria Standl.)

 
Cucumber plant (Cucumis sativus L.) cv. Jinchun No. 2 Grafted plants possessed significantly higher scion dry weight, more soluble sugars and micronutrient content Huang et al. (2010)  
 3 Cucurbita hybrid rootstocks (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘P360’ and ‘PS13132’ 
  • a)

    Melon (Cucumis melo L.) cv. Cyrano

  • b)

    Cucumber (Cucumis sativus L.) cv. Akito

 
  • 1.

    Lesser reduction in the leaf area index in grafted plants.

  • 2.

    Smaller effect of salinity on the net photosynthetic rate (PN) and stomatal conductance (gs) in grafted individuals

 
Rouphael et al. (2012)  
 4 Cucurbita hybrid rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘PS1313’ Cucumber (Cucumis sativus L.) cv. Akito Relatively higher chlorophyll content (SPAD index), better net assimilation rate, and higher nutritional value Colla et al. (2012)  
 5 
  • a)

    Cucumber (Cucumis sativus L.) cv. Affyne

  • b)

    Cucurbita hybrid rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘P360’

 
Cucumber (Cucumis sativus L.) cv. Ekron 
  • 1.

    Higher PSII photochemical activity

  • 2.

    Lesser reduction in chlorophyll content (SPAD index)

    Better GPX activity resulting in the enhanced antioxidant system

 
Colla et al. (2013)  
 6 Interspecific tomato hybrid rootstocks (Solanum lycopersicum X S. habrochaites) ‘Maxifort’. ‘Arnold’ & ‘Armstrong’ Tomato (S. lycopersicum L.) cv. Cuore di Bue Higher fruit juice Na+ content Di Gioia et al. (2013)  
 7 Chaofeng Kangshengwang (Lagenaria siceraria Standl.) Watermelon (Citrullus lanatus) cv. Xiuli Increase in the total biomass and NO3 Yang et al. (2013)  
 8 Interspecific squash rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘RS841 improved’ Melon (Cucumis melo L.) cv. Brennus and London 
  • 1.

    Improved plant biomass and leaf area

  • 2.

    Enhanced ion partitioning resulting in the selective uptake of K+

  • 3.

    Better stomatal regulation under salt stress conditions

 
Orsini et al. (2013)  
 9 Pumpkin (Cucurbita moschata Duch.) cv. Chaojiquanwang Cucumber (Cucumis sativus L.) cv. Jinchun No. 2 1. Relatively higher activities of dehydroascorbate reductase, ascorbate peroxidase, and glutathione reductase were observed in the chloroplasts of grafted plants providing better H2O2-scavenging capacity
4. Enhanced net CO2 assimilation and transpiration rates 
Zhen et al. (2011)  
 10 a) Capsicum chinense Jacq. ‘ECU-973’
Capsicum baccatum L. var. pendulum ‘BOL-58’ 
Pepper (Capsicum annum) cv. Adige 2. Lesser negative impact on the nitrate reductase activity, photosynthetic rate, and lipid peroxidation Penella et al. (2014)  
Sl. no.RootstockScionKey improved characteristicsReference
Salinity stress 
 1 
  • a)

    Macis (Lagenaria siceraria Standl., Nunhems Zaden, The Netherlands)

  • b)

    Ercole (Cucurbita maxima Duchesne X Cucurbita moschata Duchesne, Nunhems Zaden, The Netherlands)

 
Watermelon (Citrullus lanatus) cv. Tex Increased total soluble solid content, dry matter, and sugar content Colla et al. (2006)  
 2 
  • a)

    Black seeded figleaf gourd (Cucurbita ficifolia Bouché)

  • b)

    Chaofeng Kangshengwang (Lagenaria siceraria Standl.)

 
Cucumber plant (Cucumis sativus L.) cv. Jinchun No. 2 Grafted plants possessed significantly higher scion dry weight, more soluble sugars and micronutrient content Huang et al. (2010)  
 3 Cucurbita hybrid rootstocks (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘P360’ and ‘PS13132’ 
  • a)

    Melon (Cucumis melo L.) cv. Cyrano

  • b)

    Cucumber (Cucumis sativus L.) cv. Akito

 
  • 1.

    Lesser reduction in the leaf area index in grafted plants.

  • 2.

    Smaller effect of salinity on the net photosynthetic rate (PN) and stomatal conductance (gs) in grafted individuals

 
Rouphael et al. (2012)  
 4 Cucurbita hybrid rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘PS1313’ Cucumber (Cucumis sativus L.) cv. Akito Relatively higher chlorophyll content (SPAD index), better net assimilation rate, and higher nutritional value Colla et al. (2012)  
 5 
  • a)

    Cucumber (Cucumis sativus L.) cv. Affyne

  • b)

    Cucurbita hybrid rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘P360’

 
Cucumber (Cucumis sativus L.) cv. Ekron 
  • 1.

    Higher PSII photochemical activity

  • 2.

    Lesser reduction in chlorophyll content (SPAD index)

    Better GPX activity resulting in the enhanced antioxidant system

 
Colla et al. (2013)  
 6 Interspecific tomato hybrid rootstocks (Solanum lycopersicum X S. habrochaites) ‘Maxifort’. ‘Arnold’ & ‘Armstrong’ Tomato (S. lycopersicum L.) cv. Cuore di Bue Higher fruit juice Na+ content Di Gioia et al. (2013)  
 7 Chaofeng Kangshengwang (Lagenaria siceraria Standl.) Watermelon (Citrullus lanatus) cv. Xiuli Increase in the total biomass and NO3 Yang et al. (2013)  
 8 Interspecific squash rootstock (Cucurbita maxima Duch. X Cucurbita moschata Duch.) ‘RS841 improved’ Melon (Cucumis melo L.) cv. Brennus and London 
  • 1.

    Improved plant biomass and leaf area

  • 2.

    Enhanced ion partitioning resulting in the selective uptake of K+

  • 3.

    Better stomatal regulation under salt stress conditions

 
Orsini et al. (2013)  
 9 Pumpkin (Cucurbita moschata Duch.) cv. Chaojiquanwang Cucumber (Cucumis sativus L.) cv. Jinchun No. 2 1. Relatively higher activities of dehydroascorbate reductase, ascorbate peroxidase, and glutathione reductase were observed in the chloroplasts of grafted plants providing better H2O2-scavenging capacity
4. Enhanced net CO2 assimilation and transpiration rates 
Zhen et al. (2011)  
 10 a) Capsicum chinense Jacq. ‘ECU-973’
Capsicum baccatum L. var. pendulum ‘BOL-58’ 
Pepper (Capsicum annum) cv. Adige 2. Lesser negative impact on the nitrate reductase activity, photosynthetic rate, and lipid peroxidation Penella et al. (2014)  

CONCLUSION AND FUTURE RECOMMENDATIONS

In summary, grafting scion and rootstock of genetically diverse vegetable crops with the goal of mitigating environmental stressors predicted under a changing global climate scenario have been documented in the scientific literature as a promising technique. New research should be conducted to evaluate and test elite diverse germplasm as a source of the viable rootstock. However, realizing the full potential of the grafting methodology is based on several factors, such as the appropriate selection of scion and rootstock, the geographical location, scion–rootstock communication, and the reciprocal effect of the shoot and root system. Additional research is needed to develop automated grafting platforms which scale-up this technique, so that grafting can become an integral component of modern vegetable crop production. Only then can progress in modern simulation and automated grafting techniques for the production of grafted plant material become more economically accessible to vegetable farmers. Moreover, vegetable grafting is followed in the developed parts of the world owing to the updated knowledge of the farmers regarding the modern vegetable production technology.

Vegetable grafting will help growers to deal with climate change and to overcome the unsustainable vegetable production practices which result in soil degradation and the rapid depletion of natural resources. In the future, research involving the development of grafting technologies ideal for the stable, year-round, and economical production of seedlings is required, so that this technology becomes more accessible to farmers in every part of the world.

REFERENCES

Abdelmageed
A. H. A.
Gruda
N.
2009
Influence of grafting on growth, development, and some physiological parameters of tomatoes under controlled heat stress conditions
.
European Journal of Horticultural Science
74
(
1
),
16
20
.
Altunlu
H.
Gul
A.
2012
Increasing drought tolerance of tomato plants by grafting
.
Acta Horticulturae
960
,
183
190
.
Ashraf
M.
Athar
H. R.
Harris
P. J. C.
Kwon
T. R.
2008
Some prospective strategies for improving crop salt tolerance
.
Advances in Agronomy
97
,
45
110
.
Bahadur
A.
Rai
N.
Kumar
R.
Tiwari
S. K.
Singh
A. K.
Rai
A. K.
Singh
U.
Patel
P. K.
Tiwari
V.
Rai
A. B.
Singh
M.
Singh
B.
2015
Grafting tomato on eggplant as a potential tool to improve waterlogging tolerance in hybrid tomato
.
Vegetable Science
42
(
2
),
82
87
.
Besri
M.
2008
Cucurbits grafting as alternative to Methyl Bromide for cucurbits production in Morocco
. In:
Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions
,
November 2008
,
Orlando, Florida
, pp.
11
14
.
Bhatt
R.
Upreti
K.
Divya
M. H.
Bhat
S.
Pavithra
C. B.
Sadashiva
A. T.
2015
Interspecific grafting to enhance physiological resilience to flooding stress in tomato (Solanum lycopersicum L.)
.
Scientia Horticulturae
182
,
8
17
.
https://doi.org/10.1016/j.scienta.2014.10.043
.
Black
L. L.
Wu
D. L.
Wang
J. F.
Kalb
T.
Abbass
D.
Chen
J. H.
2003
Grafting Tomatoes for Production in the Hot-Wet Season
.
AVRDC Publication #03-551
.
Bloom
A. J.
Zwieniecki
M. A.
Passioura
J. B.
Randall
L. B.
Holbrook
N. M.
St. Clair
D. A.
2004
Water relations under root chilling in a sensitive and tolerant tomato species
.
Plant, Cell & Environment
27
(
8
),
971
979
.
Brown
J. H.
Valone
T. J.
Curtin
C. G.
1997
Reorganization of an arid ecosystem in response to recent climate change
.
Proceedings of the National Academy of Sciences
94
(
18
),
9729
9733
.
https://doi.org/10.1073/pnas.94.18.9729
.
Cattivelli
L.
Rizza
F.
Badeck
F.-W.
Mazzucotelli
E.
Mastrangelo
A.
Francia
E.
Marè
C.
Tondelli
A.
Stanca
M.
2008
Drought tolerance improvement in crop plants: an integrated view from breeding to genomics
.
Field Crops Research
105
(
1–2
),
1
14
.
https://doi.org/10.1016/j.fcr.2007.07.004
.
Chaudhari
S.
Jennings
K. M.
Monks
D. W.
Jordan
D. L.
Gunter
C. C.
Louws
F. J.
2017
Response of drought-stressed grafted and nongrafted tomato to postemergence metribuzin
.
Weed Technology
31
(
3
),
447
454
.
Chauhan
B. S.
Kaur
P.
Mahajan
G.
Randhawa
R. K.
Singh
H.
Kang
M. S.
2014
Global warming and its possible impact on agriculture in India
. In:
Advances in Agronomy
(
Sparks
D.
, ed.).
Elsevier
, pp.
65
121
.
https://doi.org/10.1016/B978-0-12-420225-2.00002-9
Colla
G.
Roupahel
Y.
Cardarelli
M.
Rea
E.
2006
Effect of salinity on yield, fruit quality, leaf gas exchange, and mineral composition of grafted watermelon plants
.
HortScience
41
(
3
),
622
627
.
https://doi.org/10.21273/HORTSCI.41.3.622
.
Colla
G.
Rouphael
Y.
Cardarelli
M.
Temperini
O.
Rea
E.
Salerno
A.
Pierandrei
F.
2008
Influence of grafting on yield and fruit quality of pepper (Capsicum annuum L.) grown under greenhouse conditions
.
Acta Horticulturae
359
364
.
https://doi.org/10.17660/ActaHortic.2008.782.45
.
Colla
G.
Rouphael
Y.
Leonardi
C.
Bie
Z.
2010
Role of grafting in vegetable crops grown under saline conditions
.
Scientia Horticulturae
127
(
2
),
147
155
.
https://doi.org/10.1016/j.scienta.2010.08.004
.
Colla
G.
Rouphael
Y.
Rea
E.
Cardarelli
M.
2012
Grafting cucumber plants enhance tolerance to sodium chloride and sulfate salinization
.
Scientia Horticulturae
135
,
177
185
.
https://doi.org/10.1016/j.scienta.2011.11.023
.
Colla
G.
Rouphael
Y.
Jawad
R.
Kumar
P.
Rea
E.
Cardarelli
M.
2013
The effectiveness of grafting to improve NaCl and CaCl2 tolerance in cucumber
.
Scientia Horticulturae
164
,
380
391
.
https://doi.org/10.1016/j.scienta.2013.09.023
.
Costello
A.
Abbas
M.
Allen
A.
Ball
S.
Bell
S.
Bellamy
R.
Friel
S.
Groce
N.
Johnson
A.
Kett
M.
Lee
M.
Levy
C.
Maslin
M.
McCoy
D.
McGuire
B.
Montgomery
H.
Napier
D.
Pagel
C.
Patel
J.
Antonio
J.
de Oliveira
P.
Redclift
N.
Rees
H.
Rogger
D.
Scott
J.
Stephenson
J.
Twigg
J.
Wolff
J.
Patterson
C.
2009
Managing the health effects of climate change
.
The Lancet
373
,
1693
1733
. .
Davis
A.
Perkins-Veazie
P.
Sakata
Y.
López-Galarza
S.
Maroto
J.
Lee
S.-G.
Huh
Y.-C.
Sun
Z.
Miguel
A.
King
S.
Cohen
R.
Lee
J.-M.
2008
Cucurbit grafting
.
Critical Reviews in Plant Sciences
27
(
1
),
50
74
.
https://doi.org/10.1080/07352680802053940
.
del Amor
F. M.
López-Marín
J.
González
A.
2008
Effect of photoselective sheet and grafting technique on growth, yield, and mineral composition of sweet pepper plants
.
Journal of Plant Nutrition
31
(
6
),
1108
1120
.
https://doi.org/10.1080/01904160802115557
.
den Nijs
A. P. M.
1980
The Effect of Grafting on Growth and Early Production of Cucumbers at Low Temperature
.
ISHS Acta Horticulturae 118: Working-party on Greenhouse Cucumber
, pp.
57
64
.
Di Gioia
F.
Signore
A.
Serio
F.
Santamaria
P.
2013
Grafting improves tomato salinity tolerance through sodium partitioning within the shoot
.
HortScience
48
(
7
),
855
862
.
https://doi.org/10.21273/HORTSCI.48.7.855
.
Edelstein
M.
2004
Grafting vegetable-crop: pros and cons
.
Acta Horticulturae
235
238
.
https://doi.org/10.17660/ActaHortic.2004.659.29
.
Fahad
S.
Bajwa
A. A.
Nazir
U.
Anjum
S. A.
Farooq
A.
Zohaib
A.
Sadia
S.
Nasim
W.
Adkins
S.
Saud
S.
Ihsan
M. Z.
Alharby
H.
Wu
C.
Wang
D.
Huang
J.
2017
Crop production under drought and heat stress: plant responses and management options
.
Frontiers in Plant Science
8
,
1147
1162
.
https://doi.org/10.3389/fpls.2017.01147
.
He
Y.
Zhu
Z.
Yang
J.
Ni
X.
Zhu
B.
2009
Grafting increases the salt tolerance of tomato by improvement of photosynthesis and enhancement of antioxidant enzymes activity
.
Environmental and Experimental Botany
66
(
2
),
270
278
.
https://doi.org/10.1016/j.envexpbot.2009.02.007
.
Horvath
I.
Vigh
L.
Hasselt
P. R.
Woltjes
J.
Kuiper
P. J. C.
1983
Lipid composition in leaves of cucumber genotypes as affected by different temperature regimes and grafting
.
Physiologia Plantarum
57
(
4
),
532
536
.
Huang
Y.
Bie
Z.
He
S.
Hua
B.
Zhen
A.
Liu
Z.
2010
Improving cucumber tolerance to major nutrients induced salinity by grafting onto Cucurbita ficifolia
.
Environmental and Experimental Botany
69
(
1
),
32
38
.
https://doi.org/10.1016/j.envexpbot.2010.02.002
.
Ibrahim
A.
Wahb-Allah
M.
Abdel-Razzak
H.
Alsadon
A.
2014
Growth, yield, quality and water use efficiency of grafted tomato plants grown in greenhouse under different irrigation levels
.
Life Science Journal
11
(
2
),
118
126
.
Jang
Y.
Mun
B.
Do
K.
Um
Y.
Chun
C.
2014
Effects of photosynthetic photon flux and carbon dioxide concentration on the photosynthesis and growth of grafted pepper transplants during healing and acclimatization
.
Horticulture, Environment, and Biotechnology
55
,
387
396
.
doi:10.1007/s13580-014-0221-4
.
Johnson
S.
Inglis
D.
Miles
C.
2014
Grafting effects on eggplant growth, yield, and verticillium wilt incidence
.
International Journal of Vegetable Science
20
(
1
),
3
20
.
https://doi.org/10.1080/19315260.2012.751473
.
Kato
C.
Ohshima
N.
Kamada
H.
Satoh
S.
2001a
Enhancement of the inhibitory activity for greening in xylem sap of squash root with waterlogging
.
Plant Physiology and Biochemistry
39
(
6
),
513
519
.
https://doi.org/10.1016/S0981-9428(01)01262-1
.
Kato
C.
Ohshima
N.
Kamada
H.
Satoh
S.
2001b
Enhancement of the inhibitory activity for greening in xylem sap of squash root with waterlogging
.
Plant Physiology and Biochemistry
513
519
.
https://doi.org/10.1016/S0981-9428(01)01262-1 (Its same as paper a)
.
Kaushik
P.
2019
Genetic analysis for fruit phenolics content, flesh color, and browning related traits in eggplant (Solanum melongena)
.
International Journal of Molecular Sciences
20
,
2990
.
https://doi.org/10.3390/ijms20122990
.
Kaushik
P.
Saini
D. K.
2019
Silicon as a vegetable crops modulator – a review
.
Plants
8
,
148
.
https://doi.org/10.3390/plants8060148
.
Kays
S. J.
Dias
J. C. S.
1995
Common names of commercially cultivated vegetables of the world in 15 languages
.
Economic Botany
49
(
2
),
115
152
.
https://doi.org/10.1007/BF02862917
.
Keatinge
J. D. H.
Lin
L. J.
Ebert
A. W.
Chen
W. Y.
Hughes
J. d.
Luther
G. C.
Wang
J.-F.
Ravishankar
2014
Overcoming biotic and abiotic stresses in the Solanaceae through grafting: current status and future perspectives
.
Biological Agriculture & Horticulture
30
(
4
),
272
287
.
https://doi.org/10.1080/01448765.2014.964317
.
King
S. R.
Davis
A. R.
Zhang
X.
Crosby
K.
2010
Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae
.
Scientia Horticulturae
127
(
2
),
106
111
.
https://doi.org/10.1016/j.scienta.2010.08.001
.
Koevoets
I. T.
Venema
J. H.
Elzenga
J. T. M.
Testerink
C.
2016
Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance
.
Front Plant Science
7
.
doi:10.3389/fpls.2016.01335
.
Li
H.
Wang
F.
Chen
X. J.
Shi
K.
Xia
X. J.
Considine
M. J.
Yu
J. Q.
Zhou
Y. H.
2014
The sub/supra-optimal temperature-induced inhibition of photosynthesis and oxidative damage in cucumber leaves are alleviated by grafting onto figleaf gourd/luffa rootstocks
.
Physiologia Plantarum
152
(
3
),
571
584
.
Liao
C.
Lin
C.
1996
Photosynthetic responses of grafted bitter melon seedlings to flood stress
.
Environmental and Experimental Botany
36
(
2
),
167
172
.
https://doi.org/10.1016/0098-8472(96)01009-X
.
Liu
S.
Li
H.
Lv
X.
Ahammed
G.
Xia
X.
Zhou
J.
Shi
K.
Asami
T.
Yu
J.
Zhou
Y.
2016
Grafting cucumber onto luffa improves drought tolerance by increasing ABA biosynthesis and sensitivity
.
Scientific Reports
6
,
20212
.
https://doi.org/10.1038/srep20212
.
López-Marín
J.
González
A.
Pérez-Alfocea
F.
Egea-Gilabert
C.
Fernández
J. A.
2013
Grafting is an efficient alternative to shading screens to alleviate thermal stress in greenhouse-grown sweet pepper
.
Scientia Horticulturae
149
,
39
46
.
https://doi.org/10.1016/j.scienta.2012.02.034
.
López-Marín
J.
Gálvez
A.
del Amor
F. M.
Albacete
A.
Fernández
J. A.
Egea-Gilabert
C.
Pérez-Alfocea
F.
2017
Selecting vegetative/generative/dwarfing rootstocks for improving fruit yield and quality in water stressed sweet peppers
.
Scientia Horticulturae
214
,
9
17
.
McMichael
A. J.
Powles
J. W.
Butler
C. D.
Uauy
R.
2007
Food, livestock production, energy, climate change, and health
.
The Lancet
370
(
9594
),
1253
1263
.
https://doi.org/10.1016/S0140-6736(07)61256-2
.
Mittler
R.
2006
Abiotic stress, the field environment and stress combination
.
Trends in Plant Science
11
(
1
),
15
19
.
Mohamed
F.
El-Hamed
K.
Elwan
M.
Hussien
M. A.
2012
Impact of grafting on watermelon growth, fruit yield and quality
.
Vegetable Crops Research Bulletin
76
,
99
118
.
https://doi.org/10.2478/v10032-012-0007-0
.
Moretti
C. L.
Mattos
L. M.
Calbo
A. G.
Sargent
S. A.
2010
Climate changes and potential impacts on postharvest quality of fruit and vegetable crops: a review
.
Food Research International
43
(
7
),
1824
1832
.
Mudge
K.
Janick
J.
Scofield
S.
Goldschmidt
E. E.
2009
A history of grafting
.
Horticultural Reviews
35
(
9
),
437
493
.
https://doi.org/10.1002/9780470593776.ch9
.
Muneer
S.
Ko
C. H.
Wei
H.
Chen
Y.
Jeong
B. R.
2016
Physiological and proteomic investigations to study the response of tomato graft unions under temperature stress
.
PLoS One
11
(
6
),
e0157439
.
https://doi.org/10.1371/journal.pone.0157439
.
Olesen
J. E.
Bindi
M.
2002
Consequences of climate change for European agricultural productivity, land use and policy
.
European Journal of Agronomy
16
(
4
),
239
262
.
https://doi.org/10.1016/S1161-0301(02)00004-7
.
Orsini
F.
Sanoubar
R.
Oztekin
G. B.
Kappel
N.
Tepecik
M.
Quacquarelli
C.
Tuzel
Y.
Bona
S.
Gianquinto
G.
2013
Improved stomatal regulation and ion partitioning boosts salt tolerance in grafted melon
.
Functional Plant Biology
40
(
6
),
628
636
.
https://doi.org/10.1071/FP12350
.
Penella
C.
Nebauer
S. G.
San Bautista
A.
López-Galarza
S.
Calatayud
Á
.
2014
Rootstock alleviates PEG-induced water stress in grafted pepper seedlings: physiological responses
.
Journal of Plant Physiology
171
(
10
),
842
885
.
Peng
Y.
Dong
Y.
Tu
B.
Zhou
Z.
Zheng
B.
Luo
L.
Shi
C.
Du
K.
2013
Roots play a vital role in flood-tolerance of poplar demonstrated by reciprocal grafting
.
Flora – Morphology, Distribution, Functional Ecology of Plants
208
(
8–9
),
479
487
.
https://doi.org/10.1016/j.flora.2013.08.001
.
Petran
A.
Hoover
E.
2014
Solanum torvum as a compatible rootstock in interspecific tomato grafting
.
Journal of Horticulture
103
(
1
).
https://doi.org/10.4172/2376-0354.1000103
.
Potop
V.
Možný
M.
Soukup
J.
2012
Drought evolution at various time scales in the lowland regions and their impact on vegetable crops in the Czech Republic
.
Agricultural and Forest Meteorology
156
,
121
133
.
https://doi.org/10.1016/j.agrformet.2012.01.002
.
Rao
C. S.
Gopinath
K. A.
Prasad
J. V. N. S.
Singh
A. K.
2016
Climate resilient villages for sustainable food security in tropical India: concept, process, technologies, institutions, and impacts
. In:
Advances in Agronomy
(
Sparks
D.
, ed.).
Elsevier
, pp.
101
214
.
https://doi.org/10.1016/bs.agron.2016.06.003
.
Reimers
H.
2000
Climate change and global crop productivity
.
Agriculture, Ecosystems & Environment
3
(
81
),
232
233
.
https://doi.org/10.1016/S0167-8809(00)00208-5
.
Reynolds
M.
Tuberosa
R.
2008
Translational research impacting on crop productivity in drought-prone environments
.
Current Opinion in Plant Biology
11
(
2
),
171
179
.
https://doi.org/10.1016/j.pbi.2008.02.005
.
Rivero
R. M.
Ruiz
J. M.
Romero
L.
2003a
Can grafting in tomato plants strengthen resistance to thermal stress?
Journal of the Science of Food and Agriculture
83
(
13
),
1315
1319
.
https://doi.org/10.1002/jsfa.1541
.
Rivero
R. M.
Ruiz
J. M.
Sánchez
E.
Romero
L.
2003b
Does grafting provide tomato plants an advantage against H2O2 production under conditions of thermal shock?
Physiologia Plantarum
117
(
1
),
44
50
.
https://doi.org/10.1034/j.1399-3054.2003.1170105.x
.
Saini
D. K.
Kaushik
P.
2019
Visiting eggplant from a biotechnological perspective: a review
.
Scientia Horticulturae
253
,
327
340
.
https://doi.org/10.1016/j.scienta.2019.04.042
.
Sakata
Y.
Ohara
T.
Sugiyama
M.
2007
The history and present state of the grafting of cucurbitaceous vegetables in Japan
.
Acta Horticulturae
731
,
159
170
.
https://doi.org/10.17660/ActaHortic.2007.731.22
.
Sánchez-Rodríguez
E.
Leyva
R.
Constán-Aguilar
C.
Romero
L.
Ruiz
J. M.
2014
How does grafting affect the ionome of cherry tomato plants under water stress?
Soil Science and Plant Nutrition
60
(
2
),
145
155
.
Sánchez-Rodríguez
E.
Romero
L.
Ruiz
J. M.
2016
Accumulation on free polyamines enhanced antioxidant response in fruit of grafting tomato plants under water stress
.
Journal of Plant Physiology
190
,
72
78
.
https://doi.org/10.1016/j.jplph.2015.10.010
.
Schmidhuber
J.
Tubiello
F. N.
2007
Global food security under climate change
.
Proceedings of the National Academy of Sciences
104
(
50
),
19703
19708
.
https://doi.org/10.1073/pnas.0701976104
.
Schwarz
D.
Rouphael
Y.
Colla
G.
Venema
J. H.
2010
Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants
.
Scientia Horticulturae
127
(
2
),
162
171
.
https://doi.org/10.1016/j.scienta.2010.09.016
.
Shahid
S. A.
Zaman
M.
Heng
L.
2018
Soil salinity: historical perspectives and a world overview of the problem
. In:
Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques
(
Zaman
M.
Shahid
S. A.
Heng
L.
, eds).
Springer International Publishing
,
Cham
, pp.
43
53
.
doi:10.1007/978-3-319-96190-3_2
.
Sharma
J.
Upadhyay
A. K.
Adsule
P. G.
Sawant
S. D.
Sharma
A. K.
Satisha
J.
Yadav
D. S.
Ramteke
S. D.
2013
Effect of Climate Change on Grape and its Value-added Products
;
Climate-Resilient Horticulture: Adaptation and Mitigation Strategies. https://doi.org/10.1007/978-81-322-0974-4_7
.
Shrivastava
P.
Kumar
R.
2015
Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation
.
Saudi Journal of Biological Sciences
22
,
123
131
.
doi:10.1016/j.sjbs.2014.12.001
.
Singh
H.
Kumar
P.
Chaudhari
S.
Edelstein
M.
2017
Tomato grafting: a global perspective
.
HortScience
52
,
1328
1336
.
doi:10.21273/HORTSCI11996-17
.
Thomas
D.
Twyman
C.
Osbahr
H.
Hewitson
B.
2007
Adaptation to climate change and variability: farmer responses to intra-seasonal precipitation trends in South Africa
.
Climatic Change
83
,
301
322
.
https://doi.org/10.1007/s10584-006-9205-4
.
Thomas
D. S.
Twyman
C.
Osbahr
H.
Hewitson
B.
2011
Adaptation to climate change and variability: farmer responses to intra-seasonal precipitation trends in South Africa
. In:
African Climate and Climate Change
,
Vol. 43
(
Williams
C.
Kniveton
D.
, eds).
Springer
,
Dordrecht
, pp.
155
178
.
https://doi.org/10.1007/978-90-481-3842-5_7
.
Venema
J. H.
Dijk
B. E.
Bax
J. M.
Van Hasselt
P. R.
Elzenga
J. T. M.
2008
Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance
.
Environmental and Experimental Botany
63
(
1–3
),
359
367
.
https://doi.org/10.1016/j.envexpbot.2007.12.015
.
Witzel
K.
Neugart
S.
Ruppel
S.
Schreiner
M.
Wiesner
M.
Baldermann
S.
2015
Recent progress in the use of ‘omics’ technologies in brassicaceous vegetables
.
Frontiers in Plant Science
6
,
244
.
https://doi.org/10.3389/fpls.2015.00244
.
Wurr
D. C. E.
Fellows
J.
Fuller
M. P.
2004
Simulated effects of climate change on the production pattern of winter cauliflower in the UK
.
Scientia Horticulturae
101
(
4
),
359
372
.
https://doi.org/10.1016/j.scienta.2003.11.011
.
Xu
Z.
Jiang
Y.
Jia
B.
Zhou
G.
2016
Elevated-CO2 response of stomata and Its dependence on environmental factors
.
Front Plant Science
7
.
doi:10.3389/fpls.2016.00657
.
Yang
Y.
Lu
X.
Yan
B.
Li
B.
Sun
J.
Guo
S.
Tezuka
T.
2013
Bottle gourd rootstock-grafting affects nitrogen metabolism in NaCl-stressed watermelon leaves and enhances short-term salt tolerance
.
Journal of Plant Physiology
170
(
7
),
653
661
.
https://doi.org/10.1016/j.jplph.2012.12.013
.
Yetisir
H.
Çaliskan
M. E.
Soylu
S.
Sakar
M.
2006
Some physiological and growth responses of watermelon [Citrullus lanatus (Thunb.) Matsum. and Nakai] grafted onto Lagenaria siceraria to flooding
.
Environmental and Experimental Botany
58
(
1–3
),
1
8
.
https://doi.org/10.1016/j.envexpbot.2005.06.010
.
Zhen
A.
Bie
Z.
Huang
Y.
Liu
Z.
Lei
B.
2011
Effects of salt-tolerant rootstock grafting on ultrastructure, photosynthetic capacity, and H2O2-scavenging system in chloroplasts of cucumber seedlings under NaCl stress
.
Acta Physiologiae Plantarum
33
(
6
),
2311
.
https://doi.org/10.1007/s11738-011-0771-3
.