Improving Crop Resistance to Abiotic Stress (TUTEJA:PLANT STRESS OMICS O-BK) || Vegetable Crops: Improvement of Tolerance to Adverse Chemical Soil Conditions by Grafting

38Vegetable Crops: Improvement of Tolerance to AdverseChemical Soil Conditions by GraftingGiuseppe Colla, Youssef Rouphael, and Mariateresa Cardarelli

Owing to limited availability of arable land and the high market demand forvegetables around the world, Solanaceae and Cucurbitaceae crops are frequentlycultivated under unfavorable soil conditions. These include salinity, alkalinity, heavymetals, and excessive amount of trace elements. Plants exposed to adverse chemicalsoil conditions exhibit various physiological and biochemical disorders leading tostunted growth and severe yield loss. Oneway to avoid or reduce losses in productioncaused by adverse soil chemical conditions in vegetables would be to graft them ontorootstocks capable of reducing the effect of external stresses on the shoot. Grafting isan integrative reciprocal process and, therefore, both scion and rootstock caninfluence tolerance of grafted plants to adverse soil chemical conditions. Graftedplants grown under adverse soil chemical conditions often exhibited greater growthand yield, higher photosynthesis, better nutritional status, and lower accumulation ofNaþ and/or Cl�, heavymetals, and excessive amount of trace elements in shoots thanungrafted or self-grafted plants. This chapter gives an overview of the recent literatureon the response of grafted plants to adverse soil chemical conditions and themechanisms of tolerance to adverse soil chemical conditions in grafted plants relatedto the morphological root characteristics and the physiological and biochemicalprocesses. The chapter will conclude by identifying several prospects for futureresearch aiming to improve the role of grafting in vegetable crops grown underabiotic stress conditions.

38.1Introduction

Soil chemical factors suchas salinity, alkalinity, heavymetals, andexcessive amountoftraceelementsarecommonabiotic stresses limitingcropproductivity inmanypartsofthe world. At present, a third of irrigated land in the world is affected by salinity andalkalinity problems [1, 2], while many soils are contaminated by heavy metals.

Improving Crop Resistance to Abiotic Stress, First Edition.Edited by Narendra Tuteja, Sarvajeet Singh Gill, Antonio F. Tiburcio, and Renu Tuteja� 2012 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2012 by Wiley-VCH Verlag GmbH & Co. KGaA.

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According to the US Salinity Laboratory, when the electrical conductivity (EC) ofsolution extracted from a soil at its saturation water content is greater than 4 dS m�1

and the exchangeable sodium percentage (ESP) is less than 15, the soil is consideredsaline. Salinity occurs in both nonirrigated and irrigated lands as a result ofevapotranspiration of saline underground water or due to the use of irrigation waterof poor quality. Soil salinization is common especially in arid and semiarid regionswhere the amount of rainfall is insufficient for leaching. The salinization process isparticularly evident under greenhouse conditions where the lack of leaching byrainfall and the high fertilizer application rates result in a dramatic increase in theelectrical conductivity value of soils, especially when poor-quality water is used [3].Although NaCl is usually the most abundant salt in saline soil, other elements (e.g.,Ca2þ , Mg2þ , Kþ , SO4

2�, and NO3�) can be presented in different combinations

depending on the source of salinity and the solubility of the salts [4]. Moreover, thesalinewatermay contain high concentrations of trace elements that can be harmful tomost vegetable crops (e.g., B > 1–2mgL�1). Under saline conditions, crop perfor-mancemay be adversely affected by water deficit arising from the low water potentialof the soil solution (osmotic effect) and by salinity-induced nutritional disordersassociated with excessive ion uptake or nutrient imbalance by nutrient availability,competitive uptake, and transport or partitioning within the plant (ionic effect) [5, 6].The pHof saline soil is usually aroundneutrality or slightly alkaline.However, higherpH values (>8) are observed in saline soils with ESP greater than 15 (saline–sodicsoils) due to the high content of sodium carbonate. Plant growth in sodic soils isdepressed mainly by high pH and bicarbonate, and often by low soil permeability towater, poor aeration, andmechanical impedance.However, alkaline soils areoftennotassociated with salinity, especially when the source of alkalinity is CaCO3 that buffersthe soil in the pH range 7.5–8.5 (calcareous soils). Calcareous soils are generallycharacterized by low bioavailability of plant nutrients, high concentrations of CaCO3

and soil solution HCO3�, high pH, and almost no exchangeable Hþ [7, 8]. Bicar-

bonate ions reduce the plant growth by interfering negatively with the uptake ofmacroelements, in particular P, K, and Mg [9]. For instance, in alkaline soils, P islargely unavailable to plants due to the formation of metal complexes (e.g., Ca–P andMg–P), rendering P only sparingly soluble. Moreover, the concentration of HCO3

�

interacts strongly with the availability of severalmicronutrients, especially Fe2þ , andit is often considered to be the primary factor responsible for chlorosis of plantson calcareous soils [10] leading to serious yield and quality losses. Reduction iniron availability is due to the incapacity of sensitive plants to acquire and totransport iron toward shoots. Iron deficiency reflects upon the physiology andbiochemistry of the whole plant, as iron is an important cofactor of many enzymes,including those involved in the biosynthetic pathway of chlorophylls [7]. Thus, underiron deficiency conditions, the reduction in leaf iron concentration is often accom-panied by amarked reduction of chlorophyll levels [11, 12], by a significant, althoughless intense, decrease in the chlorophyll fluorescence [11, 12] and by a reduction inphotosynthesis [7].

Contamination of soil and water by heavy metals and excessive amount of traceelements is one of themost troublesome environmental problems faced bymankind

980j 38 Vegetable Crops: Improvement of Tolerance to Adverse Chemical Soil Conditions by Grafting

nowadays. Heavy metals are getting importance for their nondegradable nature andoften accumulate through tropic level causing a deleterious biological effect. Anthro-pogenic activities such as mining, ultimate disposal of treated and untreated wasteeffluents containing toxic metals as well as metal chelates [13] from differentindustries, and the indiscriminate use of heavy metal-containing fertilizers (e.g.,triple superphosphate, animal wastes, and sewage sludge) and pesticides (e.g., Cu-containing fungicides) in agriculture resulted in contamination of soils and indeterioration of water quality, rendering serious environmental problems posingthreat to human beings [14]. Some of the metals such as Cu, Fe, Mn, Ni, and Zn areessential as micronutrients for plants, while many other metals such as Cd, Cr, andPb have no known physiological activity, but they are proved detrimental toplant growth beyond a certain limit, which is very much narrow for some elementssuch as Cd (0.01mg/L), Pb (0.10mg/L), and Cu (0.050mg/L) [15]. Inhibition of rootelongation is in many cases the most sensitive parameter of heavy metal toxicity.Excessive levels of heavy metals in plant tissues can also cause a range of morpho-logical and physiological disorders, such as reduction in shoot growth [16], photo-synthetic activity [17], and uptake ofmineral nutrients [18].Moreover, it may result inchlorosis and necrosis, and damage to plasma membrane permeability that leads toion leakage [19]. Finally, vegetables cultivated in contaminated soils may exhibit highlevels of heavy metals in the edible parts posing serious health risks to humans [20].Numerous attempts have been made to overcome the problems due to adverse soilchemical conditions by traditional breeding programs, but commercial success hasbeen very limited. At present, the major efforts are being directed toward the genetictransformation of plants. Although the expression of a single gene seems to lead insome cases to an improvement in the crop adaptation to some adverse soil chemicalfactors [21], the development of tolerant genotypes normally requires the transfer ofseveral genes due to the multigenic trait of abiotic stress tolerance [22]. As a rapidalternative to the relatively slow breedingmethodology aimed at increasing vegetablecrop tolerance to an abiotic stress, grafting of high-yield genotypes onto selectedrootstocks could be a promising tool.Grafting is commonly applied to vegetable cropsbelong to Solanaceous crops (tomato, eggplant, and pepper) and Cucurbits (water-melon, melon, and cucumber) in Japan, Korea, China, and several European andAmerican countries [23]. The main purpose of grafting is to control soil-bornediseases and nematodes [24]; in addition, grafting may increase the nutrient andwater use efficiency (WUE), enhance plant vigor and yield, and improve tolerance toenvironmental stresses such as high salinity, low and high temperatures, drought,flooding-induced hypoxia, alkalinity, and excessive amount of heavymetals and traceelements [23].

In this chapter, we emphasize the potentiality of vegetable grafting as a tool tomitigate the detrimental effects of adverse soil chemical conditions such as salinity,alkalinity, heavy metals, and excessive amount of trace elements on vegetable cropperformances. The role of grafting in the improvement of growth, yield, and productquality under such soil abiotic stresses is reported. Various mechanisms involved inthe increased tolerance to salinity, alkalinity, heavy metals, and excessive amount oftrace elements are also discussed.

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38.2Salinity

38.2.1Effects on Grafted Plants

38.2.1.1 Growth and YieldIt is well established that crop growth and yield decrease with increasing salinity [25].Reduced yield under saline treatments is attributed to a rapid, osmotic phase thatinhibits growth of young leaves, and a slower, ionic phase that accelerates senescenceof mature leaves [6]. Osmotic stress can also induce premature senescence viastomatal closure and carbohydrate accumulation in source tissues due to decreaseddemand from sink organs. Improvement of growth and yield was observed in manygrafting combinations of fruit vegetables grownunder saline conditions.Moreover, ithas been demonstrated that the level of tolerance of grafting combinations dependson the salt type and concentration, exposure time, and growing conditions. Generally,the positive effect induced by rootstock on shoot saline tolerance increases with thelevel of stress as observed in tomato [26], where grafting �Moneymaker� onto either�Radja� or �Pera� improved tomato fruit yield compared to self-grafted plants of�Moneymaker� when plants were grown at 50mMNaCl, whereas there was no effectof either rootstocks or grafting per se on fruit yield in the absence of or at 25mMNaCl.The yield increase over self-grafted plants was around 40% whereas in the earlierstudy [27] using a different scion (�Jaguar�), the increase was 80% at the same saltconcentration indicating a different salt tolerance of the genotypes. These resultssuggest that the salt tolerance of the shoot depends on the root system, independentof the genotype used as a scion, although the positive effect of rootstock may show adifferent degree depending on the higher or lower exclusion ability of the shootgenotype. Similarly, in eggplant (Solanum melongena L.) grafting cultivar �Suqiqie�onto �Torvum Vigor� (S. torvum Swartz) improved the growth performance undersaline stress conditions [28, 29]. The better crop performance in grafted Solanaceouscrops grown under saline conditions has also been recorded on several Cucurbitssuch as watermelon, melon, and cucumber. Grafting watermelon �Fantasy� cultivaronto plants �Strongtosa� rootstock (Cucurbita maxima Duch.�C. moschata Duch.)reduced the decrease in shootweight and leaf area caused by the increase in salinity incomparison with ungrafted plants [30]. Moreover, other experiments demonstratedthat grafted �Crimson Tide� watermelon onto C. maxima and two Lagenaria sicerariarootstocks had higher plant growth than ungrafted plants under saline conditions(8.0 dSm�1, [31]). In cucumber (Cucumis sativus L.), grafting cultivar �JinchunNo. 2�onto bottle gourd rootstock �Chaofeng 8848� (L. siceraria Standl.) alleviated thenegative effect of salinity on shoot dryweight [32]. In a similar study, cucumber plantscultivar �JinchunNo. 2� grafted ontofigleaf gourd (C. ficifoliaBouch�e) and �ChaofengKangshengwang� had higher fruit number and marketable fruit yield compared tothe self-grafted plants at all salt levels (30 and 60mM NaCl). Similarly, two meloncultivars (C. melo L.) grafted onto three hybrids of squash (C. maxima Duch.�C.moschata Duch.) exhibited higher yield compared to ungrafted ones when grown


under saline conditions (4.6 dS m�1 [33]). However, other researchers [34, 35]recorded that the sensitivity to salinity was similar between grafted and ungraftedmelon plants as a result of the different Cucurbita rootstocks used in these studies.Salt tolerance of grafted plants can vary significantly in relation to the salt compo-sition and growing system. For instance, cucumber plant �Jinchun No. 2� graftedonto �Chaofeng Kangshengwang� (L. siceraria Standl.) was tolerant to salinity whengrown in hydroponics using NaCl as salt source, while �Chaofeng Kangshengwang�failed to increase grafted plant tolerance to salinity when grown in substrate cultureusing macronutrients as salinity source [36].

38.2.1.2 Photosynthesis and Water RelationsUnder saline conditions, the low osmotic potential of soil solution restricts wateravailability and water uptake and thus reduces the root hydraulic conductance andcauses a significant increase in the stomatal resistance and reduction in CO2

photosynthetic assimilation. Stomatal opening and photosynthesis, which areKþ -dependent physiological processes, can also be reduced by NaCl saline condi-tions as a result of the decreased absorption of some nutrients (e.g., K) and theincreased content of the Naþ and Cl� in the leaves. Under saline conditions, salt-tolerant grafted plants exhibit higher photosynthetic rate per unit area and higher leafarea resulting in a greater photosynthetic capacity of the plant than ungrafted or self-grafted plants. For instance, in awatermelon experiment [37], the leaf area and the netassimilation of CO2 under saline conditions were higher in grafted plants of cultivarTex onto Cucurbita hybrid �Ercole� than in ungrafted �Tex� plants. Similarly, it wasdemonstrated [38] that grafted cucumber plants had higher net photosynthesis,stomatal conductance, and intercellular CO2 concentrations under NaCl stress thanself-rooted plants.Moreover, undermoderate and severe salt stresses, tomato-graftedplants of �Hezu903� onto �Zhezhen� rootstock showed higher net CO2 assimilationrate than nongrafted and self-grafted plants [39]. Water use efficiency, calculated asthe ratio of net assimilation of CO2 to transpiration, usually increased in moderatelysalt-stressed plants, owing to the fast decrease in transpiration rate. For instance,grafting tomato �Hezu903� onto �Zhezhen� rootstock increased the WUE undersaline conditions in comparison to the ungrafted and self-grafted plants [39]. ThehigherWUE is important for salt tolerance since a highWUEmay reduce the uptakeof salt and alleviate the water deficiency induced by salinity [40, 41]. Water contentmaintenance and transpiration are crucial to plants under salinity stress. Waterdeficit associated with salinity can increase the leaf water content as a result of thetranspiration rate reduction due to the stomatal closure. For instance, at 100mM ofNaCl, higher leaf water content was observed in grafted tomato plants of �UC-82B�onto �Kyndia� rootstock compared to the self-grafted plants; the better leaf watercontent was associated with a lower shoot growth reduction in grafted plants [42].

38.2.1.3 Fruit QualityIn general, salinity reduces the yield of vegetable crops but in many instancesimproves their quality [43]. Many investigations have shown that increased salinityproduces fruit with a higher content of sugars and organic acids, and higher dry

38.2 Salinity j983

matter, providing a basis for better taste and high nutritional value. Grafting canincrease or decrease the fruit quality depending on the scion–rootstock combination,the salt composition, and the growing conditions [44]. For instance, the dry matter,soluble solid content, and titratable acidity were lower in melon fruits (C. melo L.) ofcultivar �Cyrano� grafted onto �P360� Cucurbita hybrid rootstock than in ungraftedones regardless of the level of salinity [35]. In other experiments on tomato, thesoluble solid content of fruits was similar in both grafted andungrafted tomato plantsand increased with NaCl stress level. On the contrary, it has been reported thatgrafting tomato cultivar �Moneymaker� onto �Radia� rootstock increased both yieldand fruit quality parameters (soluble solids and titratable acidity) in comparison toself-grafted �Moneymaker� grown under saline conditions. Similarly, graftingcucumber cultivar �JinchunNo. 2� onto �Figleaf Gourd� (C. ficifolia Bouch�e) and�Chaofeng Kangshengwang� (L. siceraria Standl.) improved fruit quality under NaClstress owing to an increase in contents of soluble sugar and titratable acidity and adecrease in the percentage of nonmarketable fruits [32]. It is interesting to note that inthe cucumber experiment, the detrimental effects of Cucurbita rootstocks on fruitquality observed in the previous melon experiment was compensated by an increasein soluble sugar under salt stress, which was probably a consequence of a loweraccumulation of saline ions (Naþ and Cl�) that led to a high accumulation of solublesugar involved in the osmotic adjustment.

Since saline stress activates a physiological antioxidative response [45], it has beenreported that ascorbic acid levels increase with salinity, as part of the detoxification offree radicals, and similarlymoderate salt stress enhance the level of other antioxidantssuch as carotenoids (e.g., lycopene and b-carotene), which have been recognized asbeneficial in preventing widespread human diseases, including cancer. Grafting canenhance the content of antioxidants in fruits depending on grafting combinationsand salt concentration as observed in tomato,where the concentration of ascorbic acidin fruit juiceof cultivar �Fanny� remainedunchangedwithgrafting at0mMNaCl [46],whereas when NaCl was increased to 30mM a significant increase was observed forgrafted �Fanny� plants onto tomato rootstock �AR-9704.� Moreover, an increasing incarotenoids (lycopene and b-carotene) was also observed in two tomato cultivars(�Fanny� and �Goldmar�) grafted onto a tomato hybrid rootstock �AR-9704� undersaline conditions. Similarly, vitamin C increased by grafting cucumber cultivar�JinchunNo.� onto �Figleaf Gourd� and �Chaofeng Kangshengwang� in comparisonto self-grafted plants, whether saline-challenged or not. Grafting can improve themineral content of the fruits under saline conditions, which is interesting from anutritional point of view because fruits and vegetables are important source ofminerals in the human diet (e.g., 35, 24, and 11%, respectively, of the total K,Mg, andP dietary intake of humans) [47]. For instance, it has been reported that under salineconditions fruit K content was higher in cucumber cv. �Jinchun No.� grafted onto�Figleaf Gourd� and �Chaofeng Kangshengwang� in comparison to self-graftedplants. Moreover, it has also been observed that salt-tolerant grafting combinationsexhibited a decrease in Na and/or Cl contents in fruits in comparison to the self-grafted plants, which represents a positive quality aspect due to the negative effects ofhigh dietary intake of Na and Cl on human health.


38.2.2Mechanisms of Salt Tolerance in Grafted Plants

38.2.2.1 Root CharacteristicsGenerally, salinity induces a rapid reduction in root growth and an increase in root toshoot dry weight ratio due to a greater reduction in shoot growth; the high root toshoot ratio under saline conditions appears to be an adaptive strategy to increase thenutrient uptake and the ratio of water absorption by water-transpiring organs.Maintaining root growth under saline conditions was correlated with salt tolerancein tomato. Salt-tolerant grafted plants often exhibit a better root growth and higherroot to shoot ratio than ungrafted or self-grafted plants. For example, grafted tomatoplants had a less decrease in root drymass at 100 and 150mMofNaCl than ungraftedplants [39]. Similar results were observed in grafted cucumber plants [32, 48] and ingrafted watermelon plants [31, 37] exposed to salt stress. Therefore, the better growthperformance of grafted vegetable crops could be explained, at least to some extent, interms of root growth under salinity stress.

38.2.2.2 Salt Exclusion and Root RetentionThe main long-term damage caused by salinity in glycophyte crops is the excessiveaccumulation ofNaþ andCl� in leaves that causes awide variety of physiological andbiochemical alterations inhibiting plant growth and production. The increased salttolerance of grafted vegetables has often been associated with lower Naþ and/or Cl�

contents in the shoot. Twomechanisms could explain the decrease in shoot toxic ion(Naþ and/or Cl�) concentrations in grafted plants: toxic ion exclusion by the roots,and toxic ion retention and accumulation within the rootstock. Root retentioninvolves the storage of Naþ and/or Cl� in vacuoles, which can protect cytosolicenzymes from the damaging effects of salt accumulation [49]. The electrochemicalHþ gradients generated by Hþ pumps in the tonoplast (Hþ -ATPase, Hþ -PPase)provide the energy used by tonoplast-bound Naþ /Hþ antiporters (NHX) to couplethe passive movement of Hþ to the active movement of Naþ into the vacuole [50].The Hþ -ATPase and Hþ -PPase activities of root tonoplast membrane are lessinhibited under NaCl stress in salt-tolerant grafted plants than in self-grafted plantsas observed in tomato experiment [51]. Experiments conducted on melon plantgrafted onto different hybrids of squash (C. maxima Duch.�C. moschata Duch.)revealed that the concentrations averaged 11.7 times those in the shoots of plantsgraftedwith pumpkin rootstocks. Quantitative analysis indicated that Na exclusion ofsquash hybrid roots plays amore significant role in its restricted accumulation in theshoot of grafted plants, compared to its retention in the roots: Na exclusion was 69–79%, while the Na root retention was only 37–54% [52].

38.2.2.3 Osmotic AdjustmentSalt tolerance and further growth in a saline soil require a reduction in internal plantwater potential below that of the soil in order tomaintain turgor and water uptake. Infruit vegetables in which salt exclusion (glycophytes) is the principal mechanism ofsalt tolerance, either the synthesis of metabolically compatible solutes (e.g., sucrose,

38.2 Salinity j985

proline, and glycine betaine) or the uptake of inorganic ions (e.g., Kþ , Ca2þ , andNO3

�) must be increased (osmotic adjustment). Unlike Naþ and Cl�, theseosmotically active solutes are not harmful to enzymes and other cellular structureseven at high concentrations (hence �compatible solutes�). Although the biosynthesisof organic compatible solutes is energetically more expensive than the accumulationof Naþ and Cl� take-up from the soil, plants can benefit from the reduction of thedetrimental effects induced by high accumulation of Naþ and Cl�. Moreover,compatible osmolytes may protect plants by scavenging oxygen-free radicals causedby salt stress [53, 54]. It has been reported that salt-tolerant grafted plants of tomatoand cucumber exhibited a better osmotic adjustment under NaCl stress through ahigher accumulation of soluble sugars and proline in leaves than self-graftedplants [32]. Moreover, grafted plants have higher leaf Kþ accumulation, whichseems related to the higher salt tolerance than self-grafted plants [32, 48].

38.2.2.4 Antioxidant Defense SystemSalt stress reduces the photosynthesis rate increasing the formation of reactiveoxygen speciess (ROS) such as superoxide radicals (O2

�) and hydrogen peroxide(H2O2). These ROS are highly reactive and can seriously disrupt normal metabolismthrough oxidative damage to lipids, proteins, and nucleic acids [55]. Plants haveevolved an efficient defense system by which the ROS is scavenged by enzymatic andnonenzymatic antioxidant defense mechanisms.

Enzymatic antioxidants include superoxide dismutase, catalase, ascorbate perox-idase, monodehydroascorbate reductase, dehydroascorbate reductase, and glutathi-one reductase (GR). The most commonly known nonenzymatic antioxidants areglutathione (GSH), ascorbate (AsA), carotenoids, and tocopherols [55, 56]. Anefficient antioxidant system is an important factor for the enhanced salt toleranceof grafted plants. For instance, the increased salt tolerance of cucumber plants graftedonto C. ficifolia was associated with the increased superoxide dismutase andperoxidase activities under saline conditions induced by major nutrients [36].Similarly, the higher antioxidant capacity of grafted plants under salt stress hasbeen observed in other fruit-bearing vegetables such as tomato, eggplant, andwatermelon [39, 48]. Nonenzymatic antioxidants were also found to contribute tothe salinity tolerance in grafted vegetables. The glutathione and ascorbate contents inthe leaves of grafted eggplants are found to be significantly higher than those in self-grafted plants under NaCl stress [28].

38.2.2.5 Phytohormone BiosynthesisChanges in phytohormones or their precursors� concentrations, such as cytokinins(CKs), abscisic acid (ABA), the ethylene precursor 1-aminocyclopropane-1-carboxylicacid (ACC), and auxin indole 3-acetic acid (IAA), are associatedwith a responseof plantsto salinity. It has been suggested that at least part of the growth depression by salinitywas caused by inadequate phytohormone production. Generally, the levels of CKsdecrease while ABA increases in response to salinity. Abscisic acid plays a central roleboth in root to shoot and cellular signaling under salt stress and in the regulation ofstomatal conductance. Under salt stress, a transient loss of leaf turgor stimulates ABA


synthesis and causes stomatal closures stimulating leaf senescence. CKs are assumedto be synthesized mainly in the roots and transported to the shoots via the xylem. CKsare implicated in controlling both shoot growth and leaf senescence. Some rootstocksexhibited a higher CKs biosynthesis that improved salt tolerance of scion by increasingvegetative and fruit growth and by delaying leaf senescence and maintaining stomatalconductance andPSII efficiency, thereby avoiding or delaying the accumulation of toxicions [57]. Moreover, the ratio between CKs and ACCwas positively correlated with leafgrowth andPSII efficiency in a grafting tomato experiments,where tomato cultivarwasgrafted onto rootstocks from a population of recombinant lines derived fromS. lycopersicum�S. cheemaniae cross and grown under moderate saline conditions(75mM NaCl) [58]. Phytohormones also play an important role in maintaining rootgrowth under salt stress condition and in increasing root to shoot ratio. The greaterpartitioning of assimilates to roots under saline condition has been attributed to adecrease in CK concentrations and an induced basipetal transport of auxin from shootto root with a concomitant change in the activity of the sink-related enzyme cell wallinvertase. Moreover, the increase in root to shoot ratio due to a differential growthresponse of root (maintenance) and shoot (inhibition) under salinity was associatedwith a relative increase and decrease in the auxin IAA concentration, respectively [58].Polyamines [putrescine (Put), spermidine (Spd), and spermine (Spm)] are smallcationic molecules that accumulate in plants under salinity stress. They are involvedin the regulation of many basic cellular processes such as DNA replication andtranscription, cell proliferation, modulation of enzyme activities, membrane rigidity,and stabilization [59]. In grafted tomatoes and eggplants, it has been reported that theABA and total polyamine contents are significantly higher than those of self-graftedplants under NaCl stress [60, 61]. In addition, the Spd and Spm contents, as well as(Spd þ Spm)/Put value, were higher in grafted melon and cucumber plants than inself-grafted plants under NaCl stress [62].

38.3Alkalinity


38.3.1.1 Growth and PhotosynthesisResearchers have demonstrated that plants respond to elevated NaHCO3 concentra-tions in soil or in growing medium solution with decreased shoot and rootgrowth [63–65]. Shoot growth inhibition is associated with a decrease in the numberof leaves, fresh and dry mass, and shoot elongation [66]. For instance, significantdepression in shoot and root biomass production was observed in bicarbonate-treated watermelon plants, and that effect varied as a function of grafting combi-nation [67]. Under alkaline conditions (pH 8.1), shoot and root biomass weightreductions in comparison to control (pH 6.0) were significantly lower in watermeloncultivar Ingrid grafted onto Cucurbita rootstocks �PS1313� and �P360� than that in

38.3 Alkalinity j987

ungrafted watermelon plants, whereas the root to shoot ratio of biomass increased inungrafted plants. The former study showed that the watermelon plants grafted ontoCucurbita rootstocks had less change in root to shoot ratio than those grafted ontobottle gourd rootstocks and the ungrafted plants under alkaline conditions. The lowershoot reductions in grafted plants, especially in those grafted onto pumpkin root-stocks, was related to the capacity of maintaining a higher net CO2 assimilation inresponse to bicarbonate stress compared to ungrafted plants. In addition to reducednet photosynthetic rates, leaf area decreased in response to an increase in alkalinity inthe nutrient solution especially in ungrafted watermelon plants. The restriction ofleaf area may be the result of the suppressed net photosynthetic rates since the lattereffect reduces the available assimilates for leaf growth.

38.3.1.2 Nutrient UptakeAlkaline soils represent a serious concern for iron acquisition by plants since underthese conditions the range of inorganic iron availability is around 0.1–10% of thenormal requirement for optimal plant growth [68]. Colla et al. [67] observed that rootsof grafted and ungrafted watermelon plants accumulated larger amounts of Fe thanleaves, suggesting that the critical process leading to chlorosis in alkaline soils is Feuptake from the root apoplast into the symplast, which can be impaired by thealkaline apoplastic pH due to high bicarbonate concentration [10, 69]. Graftedwatermelon onto pumpkin rootstocks enhanced the uptake and translocation of Fetoward the shoot in comparison with ungrafted plants. The higher uptake andaccumulation of Fe in watermelon plants grafted onto pumpkins was the mainmechanism that reduced the detrimental effect of alkalinity (Fe deficiency) on plantgrowth. Moreover, bicarbonate ions may interfere with the uptake and transport ofother essential nutrients (e.g., P, K, and Mg) and thereby disturbing nutrientcomposition of plants [7]. On the basis of the nutrient composition of plant tissues,it has been demonstrated that watermelon grafted and ungrafted plants respondeddifferently to pH level, as has been observed for growth parameters. For ungraftedplants, the high pH level (8.1) in the nutrient solution caused significant decrease inmacronutrient leaf concentration especially for P compared to plants grafted ontopumpkin rootstocks. Consequently, the improved crop performance of watermelonplants grafted onto pumpkin rootstocks was attributed not only to their strongcapacity to accumulate Fe in the aerial part under alkaline conditions but also to theirability to improve the uptake and transport of P to the shoot [67].

38.3.2Mechanisms of Alkalinity Tolerance in Grafted Plants

38.3.2.1 Root ExudationPlants respond to deficiency of manymacro- andmicronutrients with increased rootexudation, for example, to, P [70], K [71], Zn [72], and Cu [73]. Since organic acidsefficiently solubilize/mobilizemanymetal cations such as Ca, K, andMg [74], Al andFe [74, 75], andMn [76], the purpose of this increased exudation could be to increasethe solubilization of deficient nutrients. Certain rootstocks can improve the uptake of


several macro- and micronutrients under alkaline conditions through a greaterexudation of organic acids. For instance, watermelon plants grafted onto pumpkinrootstocks exuded more citric and malic acids than ungrafted ones especially underbicarbonate-enriched solutions [67]. These results support the hypothesis that uptakeof nutrients (e.g., P and Fe) from the nutrient solution by pumpkin rootstocks wasfacilitated by exudation of organic acids from roots. Similar results were observed inother experiments on Cucurbita plants where the root exudation of organic acids(especially citric acid) increased under P depletion leading to an enhanced P uptakeespecially in C. pepo ssp. ovifera [70].

38.3.2.2 Root-Reducing CapacityHigher plants have developed various specific and nonspecific mechanisms toincrease the solubility and uptake of Fe in the rhizosphere. In the root cell plasmamembrane, two different oxidoreductases capable of transferring electrons from thecytosol to several external electron acceptors (ferricyanide or ferric chelates) areinvolved in Fe acquisition. One oxidoreductase reduces only Fe(III) to ferricyanide,and the other is capable of reducing both ferric chelates and ferricyanide. This latterreductase, calledFe(III)-chelate reductase (FeCH-R), is induced or stimulated by iron-deficiency stress and is responsible for generating Fe(II) prior to uptake by dicoty-ledonous andnongraminaceousmonocotyledonous plants [77]. Therefore, Fe uptakeand thus the nutritional status of this micronutrient depends greatly on FeCH-Ractivity. It has been reported that some rootstocks have the potential to improve the Feuptake through ahigherFeCH-Ractivity. For instance, tomato andwatermelonplantsgrafted onto S. lycopersicum variety �TmKnvf2� and C. maxima variety �Dulcemaravilla� rootstocks, respectively, exhibited a higher FeCH-R activity in the rootscompared to ungrafted plants [78]. The higher FeCH-R activity in the roots of graftedwatermelon plants was associated with a higher Fe content in leaves. Increases inFeCH-R activity is frequently observed in dicots cultivated under alkaline conditions,and this has been assumed to arise from an inducible plasma membrane-boundFeCH-Renzyme(s) [79–81].However,nosignificantdifferenceswereobserved in rootFeCH-R activity between grafted and ungrafted watermelon plants grown underalkaline conditions, although the grafted watermelon plants onto Cucurbita hybridrootstocks exhibited a higher leaf Fe concentration than ungrafted plants [67].

38.4Heavy Metals and Excessive Amount of Trace Elements


38.4.1.1 Growth and YieldHeavy metals such as cadmium, nickel, and chrome and excessive amount of traceminerals such as copper manganese and boron in soil and water are toxic to plantseven at very low concentrations, or may accumulate in plant tissues up to a certain

38.4 Heavy Metals and Excessive Amount of Trace Elements j989

level without visible symptoms or yield reduction [19, 82]. Rouphael et al. [19] havedemonstrated that grafting cucumber onto the commercial rootstock �Shintoza� (C.maxima Duch.�C. moschata Duch.) mitigated the adverse effects of excessive Cusupply on plant biomass and fruit yield. In fact, shoot and root biomass weightreductions in control plants were clearly lower in grafted than in ungrafted plants,whereas the root to shoot ratio increased in ungrafted plants as a result of Cu stressconditions. Boron toxicity can also be mitigated by grafting onto suitable rootstocks,as indicated by an experiment with melon (C. melo L.) plants, which were exposed tofive different B concentrations ranging from 0.1 to 10mgL�1 in the irrigationwater [34, 83]. The nongrafted melon plants were more sensitive to excess boronsupply than the grafted ones (C. maxima Duch.�C. moschata Duch.�TZ-148�) interms of fruit yield and dry weight accumulation in shoots and roots [34, 83].

38.4.1.2 Fruit QualityFruit vegetables are characterized by rather low rates of heavymetal and tracemineraltranslocation to the fruit [84]. However, contaminated vegetables are frequent in themarket due to environmental pollution caused by human activities. For instance, asurvey in Japan showed that approximately 7% of eggplant fruits contain cadmiumconcentrations above the international limit for fruiting vegetables. It was suggestedthat grafted plants could be used to prevent the entry of heavy metals and excessiveamount of trace minerals into the supply chains via plants under unfavorableconditions [44]. Arao et al. [85] conducted a study to develop a method to reduceCd concentration in eggplant fruits. They showed that grafting onto S. torvumreduced eggplant fruit Cd concentration by 63–75% in Cd-polluted soil and unpol-luted soil compared to grafting onto S. melongena and S. integrifolium. The accumu-lation of Cu in fruit tissue of cucumber plants grownunderCu-enriched solutionwassignificantly lower in plants grafted onto the �Shintoza�-type rootstock (C. maximaDuch.�C. moschataDuch.) in comparison to that of ungrafted plants [19]. Similarly,the concentrations of B, Zn, Sr,Mn,Cu, Ti, Cr,Ni, andCd in the fruits ofmelonplantsirrigated with marginal water were lower in the grafted plants onto the commercialCucurbita rootstock �TZ-148� than in ungrafted plants [86].

38.4.2Mechanisms of Tolerance in Grafted Plants

The enhanced tolerance of grafted vegetables to heavymetals and excessive amount oftrace element has often been associated with root exclusion and/or to the restrictedtranslocation from roots to shoots. Arao et al. [85] observed that grafting S. melongenaplants onto S. torvum reduced the leaf and stem Cd concentrations by 67–73% incomparison to self-grafting or grafting onto S. integrifolium, in both Cd-polluted andunpolluted soils. The Cd concentration in xylem sap collected from stems of S. torvumwas 22%of that in stems ofS.melongena, indicating an appreciable restriction of theCdtranslocation fromroot to shoot in the former.However, the concentrations ofCd in theroots of S. melongena and S. torvum were similar when the plants were exposed toidentical external Cd levels [20]. These results indicate that S. torvum restricts


specifically the translocation of Cd to the shoot and not the Cd uptake by the roots.Genotypic differences in the ability of the root to prevent Cd translocation to the shoothave been reported also for soybean bymeans of grafting experiments [87]. AccordingtoMori et al. [20], the restriction of Cd translocation to the fruit of eggplant grafted ontoS. torvum in comparison to self-grafted S. melongena seems to be related to the processof xylem loading. Yamaguchi et al. [88] attempted to elucidate the molecular mechan-isms governing the reducedCd uptake byS. torvum and found that dehydration-relatedtranscription factors and aquaporin isoforms are potential constituents of Cd-inducedbiochemical impediments. Other results have shown that the rootstock significantlyaffects gene expression in the scion, thereby indicating that some signals transportedfrom the root to the shoot may also influence the Cd uptake and translocation [89].Edelstein et al. [83] recorded that grafting melon onto the commercial C. maximaDuch.�C.moschataDuch. rootstock �TZ-148� reduced the boron concentration in theleaves of grafted plants in comparison to ungrafted plants. The lower boron concen-tration could be the result ofmainly the differences in the properties of the root systemsof the two plant types. Boron could accumulate and bind in the root system, whichwould limit its movement toward the shoot, as reported for some fruit trees [90, 91]. Itshould be noted, however, that in the current study boron concentrations in the rootsystems of both grafted and ungraftedmelon plants were relatively low and,moreover,the boron concentrations in the roots of the ungrafted plants were similar to or higherthan those in the roots of the grafted ones. Thus, it can be concluded that the lowerboron concentrations in the leaves of the grafted plants than in those of the ungraftedones were not the result of greater boron accumulation and attachment in the roots ofthe grafted plants than in those of the ungrafted ones [83]. Grafting cucumber cv.�Akito� onto the commercial rootstock �Shintoza� restricted the uptake and translo-cation of Cu to the shoot [19]. The leaf Cu concentration in grafted plants treatedwith anutrient solution containing 47 and 94mMCu increased by 138 and181%, respectively,in comparison toplants suppliedwith0.3mMCu,while inungraftedplants the increasein the leaf Cu level was 235 and 392%, respectively. Rouphael et al. [19] attributed theimproved crop performance of grafted cucumber plants to the ability of the squashrootstock to restrict the accumulation of Cu in the shoot. These results indicate that Cutoxicity in cucumber cultivated inenvironmentswith toohighCu levels in the root zonemay be partly mitigated by grafting onto the rootstock �Shintoza.� Similarly, Savvaset al. [92, 93] found that the transport of Cu to the leaves of tomato �Belladona� was alsorestricted when the plants were grafted onto the �He-Man� rootstock (S. lycopersicumL.�S. habrochaites S. Knapp & D.M. Spooner). However, the concentration of Cu wassignificantly lower not only in the leaves but also in the roots of plants grafted onto �He-Man� in comparison to self-grafted �Belladona� plants.

38.5Concluding Remarks and Future Perspectives

For decades, vegetable grafting has been successfully practiced in many Asiancountries, and it is becoming increasingly popular in Europe as well. This chapter

38.5 Concluding Remarks and Future Perspectives j991

concludes that grafting is an effective way to mitigate the detrimental effects ofadverse soil chemical conditions such as salinity, alkalinity, heavy metals, andexcessive amount of trace elements on vegetable crop performances particularly inCucurbitaceae and Solanaceae. The increased tolerance of grafted plant to adversesoil chemical conditions was due to the use of tolerant rootstocks. Several effectiverootstocks arementioned and already in practical use, or used in breeding programs.The mechanisms involved in the advantageous response of specific stress-tolerantrootstocks are manifold and partly still unknown. Augmentation of this knowledgemay help to select and breed appropriate rootstocks that improve the adaptability offruit vegetable crops to salinity, alkalinity, heavymetals, and excessive amount of traceelements. The agronomical and physiological processes implicated in the toleranceof grafted plants to adverse soil chemical conditions have received much attention,but the biochemical and molecular processes involved remain relatively unknown.So, a thorough investigation should be conducted with the aim of providingbiochemical and molecular knowledge on the metabolism of grafted plants grownunder adverse soil chemical conditions. Finally, researchers, extension specialists,and seed companies need to work together to integrate this modernized technologyas an effective tool for producing high-quality vegetables under adverse soil chemicalconditions.

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