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Scientia Horticulturae 160 (2013) 189–197

Contents lists available at SciVerse ScienceDirect

Scientia Horticulturae

journa l h om epage: www.elsev ier .com/ locate /sc ihor t i

odeling of water movement trough cherry plant as preselecting toolor prediction of tree vigor

irjana Ljubojevic a,∗, Vladislav Ognjanova, Lana Zoric b, Ivana Maksimovic a,jiljana Merkulovb, Dusica Bosnjakovic a, Goran Barac a

University of Novi Sad, Faculty of Agriculture, Trg Dositeja Obradovica 8, 21000 Novi Sad, SerbiaUniversity of Novi Sad, Faculty of Science, Trg Dositeja Obradovica 2, 21000 Novi Sad, Serbia

r t i c l e i n f o

rticle history:eceived 31 December 2012eceived in revised form 21 May 2013ccepted 24 May 2013

eywords:reedingherryootstockootstock anatomytem anatomyydraulic conductivity

a b s t r a c t

The aim of this study was to predict the rootstock and scion cultivar vigor and rootstock/scion interac-tion on the basis of the knowledge of their morphological and anatomical characteristics and calculatedtheoretical hydraulic conductance. The simulated root system contribution to the plant vigor is numer-ical output of morphological parameter (number of skeletal roots), physiological parameter (active rootsurface area) and root and rootstock stem axial conductance quantified through theoretical hydraulicconductance. Theoretical hydraulic conductance at the graft union included ‘functional’ vessel area ofhipobiont and epibiont. Rootstock stem and scion cross-sections were examined in three zones: inner(the oldest), middle, and outer (the youngest). Calculated functional vessel area and theoretical hydraulicconductance included all three zones of xylem in scion and two rootstock zones (middle and outer), sincethe inner zone of rootstock xylem surface area overlaps with the pith of the scion. Obtained theoreticalhydraulic conductance of scions had values which are in accordance with the natural inherent tree vigor

of the examined varieties.

Graphical models were based on the interaction of the above parameters as a visual simulation ofthe pre-selection method. The lowest vigor was noted in all three examined varieties combined withrootstock ‘Gisela 5’, as well as the combination of European ground cherry and ‘Oblacinska’ sour cherrywith variety ‘Summit’, whereas the most vigorous was ‘Colt’/‘Bigarreau Burlat’, which is in agreementwith in vivo measured parameters on one-year-old fruit trees grown in the nursery.

. Introduction

Expanding sweet and sour cherry production in Europe is incon-eivable without orchard intensification, which requires not onlyhe advanced varieties and technology, but also appropriate dwarfootstocks. Hrotkó (2008) stated that, over the past decades, cherryootstock breeding resulted in 100 rootstock releases from 17ountries. As most of these rootstocks require deep, moist soils,heir cultivation is not possible without intensive irrigation. Con-equently, scientists involved in breeding programs keep searching

or rootstocks with better adaptability to soil and climate con-itions of semi-arid areas. Biodiversity of wild fruit species istill poorly exploited, leaving ample space for selection work

∗ Corresponding author. Tel.: +381 21 4853 373; fax: +381 21 450 123.E-mail addresses: ikrasevm@polj.uns.ac.rs (M. Ljubojevic),

ognjanov@polj.uns.ac.rs (V. Ognjanov), lana.zoric@dbe.uns.ac.rs (L. Zoric),vanam@polj.uns.ac.rs (I. Maksimovic), ljiljana.merkulov@dbe.uns.ac.rsL. Merkulov), dusicab@polj.uns.ac.rs (D. Bosnjakovic), goranb@polj.uns.ac.rsG. Barac).

304-4238/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.scienta.2013.05.032

© 2013 Elsevier B.V. All rights reserved.

(Khadivi-Khub et al., 2011; Bosnjakovic et al., 2012). Breedingprojects in Germany (Weiroot series), Italy (CAB series) andDenmark (DAN series) have shown that intra-specific variationwithin Prunus cerasus can result in non-suckering rootstocks withwide range of vigor and compatibility (Callesen, 1998). Estimatesof molecular variation within species indicated that cherries wereone of the most variable among Prunus species (Aradhya et al.,2004). Nonetheless, the greatest progress in cherry rootstocks hasbeen made with the introduction of numerous wild species andinter-specific hybrids (Hrotkó, 2008).

Every potential new rootstock has to pass through a long-termevaluation process that requires considerable space, time, andknowledge, as well as extensive financial investment. Developmentof a reliable method in rootstock pre-selection would significantlyreduce the extent of those requirements, while increasing the num-ber of evaluated genotypes. Vigor control mechanisms are stillnot well understood and it remains unclear whether the altered

growth is a result of xylem anatomical properties of the rootsystem, graft union and scion, or growth regulators (auxins andcytokinins) in different size-controlling rootstocks (Olmstead et al.,2004; Gonc alves et al., 2007). Numerous investigations have shown

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hat vigor control mechanisms include various aspects, such asnatomical (Atkinson et al., 2003), physiological (Soumelidou et al.,994) and biochemical changes (Errea et al., 1994; Usenik and

ˇtampar, 2001, 2005).Radial water uptake depends on the root system branching pat-

ern and the spatial distribution throughout the soil (root systemrchitecture), as these characteristics are closely related to the abil-ty of root system to access residual moisture deep in the soilrofile (Manske and Vlek, 2002). Once the root-soil connection isstablished, radial water uptake further depends on genetically-ontrolled active surface area—the parameter that reflects rootunction efficiency and shown to be in a significant linear correla-ion with the entire root system hydraulic conductivity (Mu et al.,006). Upon examining the grafted peach trees, Solari et al. (2006)tated that the differences in whole tree hydraulic conductanceay be associated with the differences in the rootstock surface

rea as well as radially absorbed water. According to Steudle andeterson (1998), the exodermis is a substantial barrier to radialater flow. Huang and Eissenstat (2000) emphasized that the dif-

erences in the overall root hydraulic conductivity among citrusootstocks with similar anatomical features were mainly relatedo structural differences in the radial pathway for water move-

ent, suggesting that this is the primary factor determining waterbsorption in citrus rootstocks.

Axial water pathway depends on root, trunk (rootstock stem)nd stem xylem characteristics. As shown by Gonc alves et al.2007), Tombesi et al. (2011) and Zoric et al. (2012), xylem ves-el number and diameter in roots and rootstock stems have strongnfluence on cherry and peach scion vigor. Generally, larger rootnd stem vessels and lower vessel density were associated withree vigor across and within fruit and forest tree species (Castro-iez et al., 1998; Zach et al., 2010). In addition to the rootstocknatomical properties, graft union formation and structure plays

crucial role in cherry tree growth and development. Olmsteadt al. (2004) concluded that vessel diameter and area in theherry graft union increased with rootstock vigor but decreasedhrough the graft union in different rootstock/scion combina-ions, as the proportion of scion tissue increased. This indicateshat the anatomical mechanism of vigor control is determinedy the genetic basis of both grafted constituents, each with itswn specific characteristics and development, which remainsnchanged in the coexistence after grafting. On the other hand,he scion vigor is the inherent vigor of the chosen variety thatas been grafted (Blazkova, 2004). Moreover, rootstock/scion spe-ific interactions may diverge from the average capacity of plantonstituents due to currently insufficiently understood geneticechanisms controlling environmental response (Sansavini and

ugli, 2008). Previous anatomical investigations on Persea amer-cana Mill. (Reyes-Santamaría et al., 2002; Fassio et al., 2009)nd Olea europea L. (Trifilò et al., 2007) rootstocks and vari-ties were performed within a single species. Cherry rootstocksnclude numerous species and inter-specific hybrids, hinderinghe more profound understanding of the mechanisms involved inrowth alterations. Ljubojevic et al. (2012) indicated multiple root-tock/scion interactions within the broad range of cherry geneticiversity, both rootstock and scion manifested in the phenologyf fruit trees, growth, vigor, as well as regularity of yield and fruituality.

The aim of this study was to develop the prediction method ofhe rootstock and scion cultivar vigor and rootstock/scion inter-ction on the basis of the knowledge of their morphological andnatomical characteristics and calculated theoretical hydraulic

onductance. The ultimate goal was to propose pre-selectionimulation model that could be applied in rootstock and scionreeding programs and as a guide for tree spacing in high densitylanting.

ulturae 160 (2013) 189–197

2. Materials and methods

2.1. Plant material

Dwarf cherry rootstock ‘Gisela 5’ , moderately vigorous root-stock ‘Colt’ and vigorous rootstocks Prunus avium L. and Prunusmahaleb L. were chosen as referent rootstocks of different vigor.European ground cherry genotype SV2 (Prunus fruticosa Pall.) wasmapped and collected from its natural habitat, on the eastern sideof Fruska Gora Mountain, in the northern part of Serbia. The firsttest of Prunus fruticosa selection SV2 indicated that this selectionreduces vigor of sweet cherry variety ‘Sylvia’ by 40% compared tothe same variety on rootstock mahaleb (Ognjanov et al., 2012).‘Oblacinska’ sour cherry (P. cerasus L.) accession OV1 was derivedfrom production orchard in village Desilovo, region of Prokuplje.One-year-old scion stems of three varieties that are widely plantedin Serbian orchards were collected from mother trees located in thenursery of the Institute for Fruit science, viticulture, horticultureand landscape architecture. All investigated rootstocks and selec-tions were subsequently propagated in the nursery of the Institute.P. avium and P. mahaleb had been sexually propagated by sowingseeds taken from one individual tree of each type, whereby theformer was open-pollinated and latter self-pollinated. Both root-stock progenies expressed a high level of uniformity in seedlingvigor and plant morphology. ‘Gisela 5’and ‘Colt’ were propagated bysoftwood cuttings taken from 4-year-old virus-free mother trees.‘Bigarreau Burlat’, ‘Summit’ and ‘Hedelfingen’ were used as scionvarieties.

2.2. Total and active root surface area

Ten two-year-old plants were excavated and the roots werewashed and immersed in 0.2 mM methylene blue, as described byMu et al. (2006). Determination of the concentrations was carriedout spectrophotometrically, by measuring the light absorption (thewavelength � = 662 nm). Read values of the light absorption wereconverted to concentrations using a standard curve that was con-structed based on known concentrations of methylene blue and thecorresponding light absorption levels. Finally, active root surfacearea (ARA) was determined by applying the expression:

ARA(m2) = C × 1.05 m2

where C represents the amount of methylene blue absorbed by theroot system in last tub marked as C.

2.3. Anatomical characteristics and measurements

Three two-year-old skeletal, woody roots (4.00–5.90 mm indiameter) from five replicate plants per genotype, were takenfrom different sides of the root system. Samples from two-year-old rootstock stems and one-year-old scion stems were taken fromten replicate plants per genotype, all approximately 10 mm indiameter—the typical rootstock and scion grafting thickness. Plantmaterial was fixed and preserved in 60% ethanol, with addition of10% of glycerin. Cross-sections were obtained using hand micro-tome and cryostat Leica CM 1850 (cutting temperature −20 ◦C;section thickness 60 �m). Cross-sections were examined and mea-sured by light microscope and Image Analyzing System MoticImages Plus. Measurements included both cross-section and xylemcharacteristics on four radial segments, 90◦ apart, on each root andstem cross-section. Root cross-section anatomical measurements

included cross-section area (mm2), diameter (mm), surface areasand proportions of periderm, secondary cortex–phloem and sec-ondary wood–xylem. On stem cross-sections, in addition to theabove parameters, the measurements included secondary cortex,

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econdary wood and pith. In secondary wood of both organs, xylem,otal ray and vessel areas were determined.

Vessel frequency, average vessel area and their affiliation to dif-erent size classes were also determined. All vessels in the fieldf vision were included in the analysis and divided according toheir area. For roots, they were grouped into three classes, namely

– <700 �m2, II – 700 ÷ 2000 �m2, and III – >2000 �m2. Similarly,lasses I – <300 �m2, II – 300 ÷ 700 �m2 and III – >700 �m2 werereated for stems. Since rootstock and scion stem thickness enablednalysis of a greater number of visual fields on one radius, xylemurface area was divided into three zones (rings): inner (the oldest),iddle and outer (the youngest).Based on the anatomical measurements, theoretical axial

ydraulic conductance (kh) of root, rootstock stem and scion stemer visual field, as well as for total cross-section area, were calcu-

ated according to the expression given by Tyree and Ewers (1991),ased on Hagen-Poisseuille’s law:

h = ��

128�

n∑

i=1

d4i

here d was the diameter of the vessels in meters, � was the fluidensity (assumed to be 103 kg m−3 for water at 20 ◦C) and � washe viscosity (assumed to be 1.002 10−9 MPa s for water at 20 ◦C).

Based on number of visual fields on cross-sections, single rootnd stem theoretical hydraulic conductance was calculated. Rootystem hydraulic conductivity Kh(R) was derived from the singlekeletal root hydraulic conductivity (Kh), according to the followingxpression:

Kh(R) = Kh × number of skeletal roots. Further, calculated Kh(R)s a determinant of axial water path was corrected by applyinghe coefficient for reduced water uptake (Cwu), where the P. aviumctive root surface area was adopted as a reference and given valuef 1, in relation to which all the others were calculated and con-erted into coefficients.

.4. Statistical analysis

The observed data were statistically processed using STATISTICA0.0 (StatSoft, Inc., Tulsa, OK, USA). The significance of differences

n measured and calculated parameters between the samples wereetermined by Duncan’s multiple range tests with the confidencef p ≤ 0.05.

. Results

.1. Morphological and anatomical characteristics of roots

Root system total and active surface area showed signifi-ant differences, thus reducing the genotype grouping potential.omparable values of total root surface area were measured for

Oblacinska’ sour cherry selection OV1 and ‘Gisela 5’ , while P. fru-icosa selection SV2 and ‘Gisela 5’ had similar values of active rooturface area. Rootstocks P. mahaleb and ‘Colt’ formed homogenousroups according to both total and active root surface area (Table 1).

Root cross-section area of investigated rootstocks varied signifi-antly. The greatest value was recorded in P. fruticosa selection SV2,nd the lowest in ‘Oblacinska’ sour cherry selection OV1; however,his variation did not imply greater or lesser portion of secondaryood and secondary cortex in the named selections (Table 1). P.

vium and P. mahaleb rootstocks were characterized by greater sec-ndary wood and lower secondary phloem tissue and thus had the

ighest secondary wood/cortex ratio (2.2 and 1.9, respectively).imilar values of xylem portion were found in P. avium and P.ahaleb rootstocks, and were higher than those measured for P.

ruticosa selection SV2, ‘Gisela 5’ and ‘Colt’, while ‘Oblacinska’ sour

ulturae 160 (2013) 189–197 191

cherry selection OV1 had the lowest value. Percentages of rays weresimilar among P. avium, P. mahaleb and ‘Colt’ and among P. fruticosaselection SV2 and ‘Gisela 5’ , while ‘Oblacinska’ sour cherry selec-tion OV1 differed from other rootstocks once again. Based on theportion of total vessel area on cross-sections, rootstocks were sep-arated into two groups, with invigorating P. avium, P. mahaleb and‘Colt’ with 6.1–7.2% at one side, and dwarfing ‘Gisela 5’ , P. fruti-cosa selection SV2, and ‘Oblacinska’ sour cherry selection OV1 with3.9–4.4% at the other.

The lowest number of vessels at the cross-section was deter-mined for P. mahaleb and ‘Oblacinska’ sour cherry selection OV1,while significant number was found in P. avium and ‘Colt’; how-ever, all genotypes were characterized by large average vesselarea. Although P. fruticosa selection SV2 and rootstock ‘Gisela 5’were characterized by the greatest number of vessels at the cross-sections, their average area was considerably smaller. In P. avium,P. mahaleb and ‘Oblacinska’ sour cherry selection OV1, most of themeasured vessels belonged to group II (surface area between 700and 2000 �m2), followed by vessels from group III (surface areagreater than 2000 �m2). In ‘Colt’, the greatest number of vesselswas found in group II, followed by group I and group III. P. fruticosaselection SV2 and ‘Gisela 5’ differed in percentages of vessels ingroups I and II; however, vessels from group III were not identifiedin either rootstock.

3.2. Anatomical characteristics of rootstock stems

A significant number of rootstock stem anatomical parameterswere investigated in detail, since this part of the plant is a graftingpoint and presents a potential barrier in the conductance of watersolution derived from the root system (Table 2).

Anatomical characteristics of total cross-section areas revealedno significant differences in secondary cortex areas and secondarywood/cortex ratio of the investigated rootstock stems. Pith areaswere small, not exceeding 1.34%, irrespective of the rootstockgenotype. However, rootstock stem secondary wood anatomicalcharacteristics strongly differed. Very low total vessel area wasrecorded in P. fruticosa selection SV2, with 4.9%, compared to 8.62%and 9.07% in ‘Colt’ and ‘Oblacinska’ sour cherry selection OV1,respectively. Significant clustering of rootstocks into homogenousgroups could not be observed based on the portion of vessels ofarea less than 300 �m2 (on total secondary wood); however, someregularities in vessels with area between 300 and 700 �m2 andlarger than 700 �m2 were recorded. Homogenous groups accord-ing to portion of large vessels (from 23.98% to 46.48%) comprisedrootstocks P. avium, ‘Colt’, P. mahaleb and ‘Oblacinska’ sour cherryselection OV1 at one side, and rootstock ‘Gisela 5’ and P. fruticosaselection SV2 at the other side with less than 5%.

Differences among genotypes were even greater when totalsecondary wood surface area was divided into three radiallyoutward-extending zones—last year’s wood, early (spring) woodand late wood—whereby their total vessel area ratios in the totalsecondary wood area were less than 20%, 40% and 45%, respec-tively. Total vessel area showed that P. fruticosa selection SV2 and‘Gisela 5’ , as well as ‘Colt’ and P. avium, formed homogenousgroups in all three zones. Average vessel area in the early (spring)wood was characterized by the highest values, except in P. mahaleband ‘Oblacinska’ sour cherry selection OV1, where the followingorder was observed: last year’s wood > early (spring) wood > latewood. In ‘Oblacinska’ sour cherry selection OV1, percentage of largevessels increases from outer to inner xylem zone, together with

the decrease of the percentage of the medium-sized and small-sized vessels. ‘Gisela 5’ rootstock was characterized by the oppositetrend, whereby the percentage of small vessels increases from theouter to the inner ring.

192 M. Ljubojevic et al. / Scientia Horticulturae 160 (2013) 189–197

Table 1Root system morphological and anatomical characteristics of studied cherry rootstocks.

P. fruticosa SV2 P. cerasus ‘Oblacinska’ OV1 ‘Gisela 5’ ‘Colt’ P. mahaleb P. avium

Morphological characteristics of root systemRoot system total surface area (m2) 0.57c 0.41d 0.46d 0.69b 0.75b 0.95a

Root system active surface area (m2) 0.19c 0.15d 0.21c 0.27b 0.28b 0.31a

Coefficient for reduced water uptake (Cwu) 0.60c 0.49d 0.68c 0.89b 0.91b 1.00a

Number of skeletal roots 4.33ab 3.67b 3.0b 5.67a 5.67a 5.67a

Cross-section anatomical characteristicsCross-section area (mm2) 27.9 (100)a 14.7 (100)c 15.0 (100)c 24.3 (100)ab 20.4 (100)b 21.3 (100)b

Periderm area (mm2) 1.0 (3.7)c 1.1 (7.5)b 1.3 (8.8)ab 24.3 (6.6)b 2.0 (10.0)a 2.3 (10.9)a

Phloem area (mm2) 12.2 (43.8)b 8.3 (56.5)a 5.7 (37.7)b 1.6 (40.3)b 6.4 (31.5)c 6.2 (28.9)c

Wood/phloem ratio 1.2c 0.6d 1.4bc 9.8bc 1.9ab 2.2a

Anatomical characteristics of total wood surface areaWood area (%) 14.7 (52.5)b 5.3 (35.9)c 8.0 (53.5)ab 12.9 (53.0)ab 11.9 (58.3)a 12.8 (60.1)a

Xylem area (%) 11.2 (40.0)ab 4.4 (30.1)c 6.3 (41.9)ab 9.4 (38.9)b 9.1 (44.5)a 10.0 (46.9)a

Total ray area (%) 3.5 (12.5)a 0.9 (5.8)b 1.7 (11.5)a 3.5 (14.3)a 2.8 (13.8)a 2.8 (13.0)a

Total vessel area (%) 1.2 (4.4)b 0.9 (4.4)b 0.6 (3.9)b 1.5 (6.1)a 0.8 (6.5)a 1.5 (7.2)a

Average vessel area (�m2) 926b 1481a 522c 1355a 1446a 1358a

Number of vessels 1274 (100)a 565 (100)b 1218 (100)a 1155 (100)a 756 (100)b 1135 (100)a

No. of vessels <700 �m2 318 (25.0)b 111 (19.6)b 967 (79.4)a 255 (22.1)b 139 (18.3)b 158 (13.9)b

No. of vessels 700–2000 �m2 956 (75.0)a 314 (55.6)b 251 (20.6)c 717 (62.1)ab 439 (57.6)b 770 (67.8)ab

No. of vessels > 2000 �m2 0 (0)b 140 (24.8)a 0 (0)b 182 (15.8)a 182 (24.1)a 207 (18.3)a

Table 2Two-year old rootstock stem anatomical characteristics of four cherry rootstocks and two cherry rootstock selections.

P. fruticosa SV2 P. cerasus ‘Oblacinska’ OV1 ‘Gisela 5’ ‘Colt’ P. mahaleb P. avium

Cross-section area (mm2) 51.7 (100)d 74.0 (100)b 61.2 (100)cd 66.6 (100)bc 78.1 (100)b 100.9 (100)a

Periderm area (mm2) 2.1 (4.0)a 2.3 (3.2)a 2.4 (4.0)a 2.4 (3.6)a 2.6 (3.4)a 2.6 (2.6)a

Phloem area (mm2) 13.3 (25.6)ab 23.4 (31.6)a 18.0 (29.4)ab 17.0 (25.6)ab 17.2 (22.1)b 28.0 (28.0)ab

Wood/phloem ratio 2.7b 2.0c 2.24c 2.7b 3.34a 2.5bc

Pith area (mm2) 0.7 (1.3)a 1.0 (1.3)a 0.6 (1.0)a 0.8 (1.2)a 0.4 (0.6)b 0.3 (0.4)b

Anatomical characteristics of total wood surface areaWood area (mm2) 35.7 (69.1)a 47.2 (63.8)a 40.3 (65.8)a 46.4 (69.7)a 57.9 (74.0)a 69.9 (69.0)a

Xylem area (mm2) 32.3 (62.5)a 41.9 (56.6)a 36.5 (59.7)a 41.0 (61.5)a 49.6 (63.6)a 60.0 (59.5)a

Total ray area (mm2) 3.4 (6.6)c 5.4 (7.3)b 3.8 (6.1)c 5.5 (8.2)b 8.3 (10.6)a 9.9 (9.8)a

Total vessel area (mm2) 2.5 (4.9)c 6.7 (9.1)a 3.5 (5.7)c 5.7 (8.6)b 5.4 (6.9)b 6.6 (6.5)a

Average vessel area (�m2) 421c 690a 388d 710a 572b 667a

No. of vessels 5598 (100)c 9465 (100)a 9915 (100)a 8083 (100)b 9825 (100)a 9668 (100)a

No. of vessels < 300 �m2 1771 (31.6)a 919 (9.7)b 3248 (32.8)a 254 (3.0)c 980 (10.0)b 344 (3.6)c

No. of vessels 300–700 �m2 3585 (64.0)a 6164 (65.1)a 6364 (64.2)a 4076 (50.5)b 6489 (66.1)a 4955 (51.3)b

No. of vessels > 700 �m2 242 (4.4)c 2382 (25.2)b 303 (3.0)c 3753 (46.5)a 2356 (23.9)b 4369 (45.1)a

Anatomical characteristics of wood outer zone–late woodWood area (mm2) 18.1 (34.9)a 23.8 (32.2)a 20.5 (33.4)a 23.5 (35.3)a 30.2 (38.5)a 36.9 (36.3)a

Xylem area (mm2) 16.3 (31.6)a 21.1 (28.5)a 18.5 (30.3)a 20.7 (31.0)a 25.8 (29.3)a 31.5 (31.2)a

Total ray area (mm2) 1.7 (3.3)c 2.7 (3.6)b 1.9 (3.1)c 2.8 (4.3)b 4.4 (5.6)a 5.4 (5.3)a

Total vessel area (mm2) 1.0 (1.9)c 3.1 (4.2)a 1.5 (2.5)c 2.6 (3.8)ab 2.4 (3.1)b 3.3 (3.2)b

Average vessel area (�m2) 362c 500b 373c 737a 493b 704a

No. of vessels 2593 (100)e 5689 (100)a 4180 (100)c 3609 (100)d 4820 (100)b 4733 (100)b

No. of vessels < 300 �m2 1302 (50.2)a 827 (14.5)bc 1149 (27.5)ab 144 (4.0)d 664 (13.8)c 122 (2.6)d

No. of vessels 300–700 �m2 1252 (48.3)b 4127 (72.5)a 3008 (72.0)a 1835 (50.9)b 3308 (68.6)a 2336 (49.4)b

No. of vessels > 700 �m2 39 (1.5)c 735 (13.0)b 23 (0.5)c 1630 (45.2)a 848 (17.6)b 2275 (48.1)a

Anatomical characteristics of wood middle zone–early woodWood area (mm2) 11.9 (23.1)a 15.7 (21.3)a 13.5 (22.1)a 15.7 (23.6)a 19.3 (24.7)a 23.4 (23.1)a

Xylem area (mm2) 10.8 (20.9)a 13.9 (18.8)a 12.2 (20.0)a 13.9 (20.9)a 16.6 (21.2) a 20.0 (19.9)a

Total ray area (mm2) 1.1 (2.2)c 1.8 (2.5)b 1.3 (2.1)c 1.9 (2.8)b 2.8 (3.5)a 3.4 (3.4)a

Total vessel area (mm2) 1.1 (2.1)c 2.5 (3.4)a 1.4 (2.3)bc 2.3 (3.4)a 2.0 (2.5)b 2.4 (2.3)bc

Average vessel area (�m2) 484c 779a 435c 758a 607b 721a

No. of vessels 2021 (100)c 2404 (100)c 4080 (100)a 3024 (100)b 3318 (100)b 3272 (100)b

No. of vessels < 300 �m2 262 (13.0)b 79 (3.3)b 1487 (36.4)a 86 (2.8)b 265 (8.0)b 77 (2.4)b

No. of vessels 300–700 �m2 1582 (78.3)a 1422 (59.2)b 2341 (57.4)b 1274 (42.1)c 2032 (61.2)b 1520 (46.4)c

No. of vessels > 700 �m2 177 (8.8)c 903 (37.5)b 252 (6.2)c 1664 (55.1)a 1021 (30.8)b 1675 (51.2)a

Anatomical characteristics of wood inner zone–last year’s woodWood area (mm2) 5.8 (11.2)a 7.8 (10.5)a 6.3 (10.4)a 7.2 (10.8)a 8. 4 (10.8)a 9.7 (9.7)a

Xylem area (mm2) 5.2 (10.0)a 6.9 (9.4)a 5.8 (9.5)a 6.4 (9.6)a 7.2 (9.3)a 8.5 (8.4)a

Total ray area (mm2) 0.6 (1.1)a 0.9 (1.2)a 0.6 (0.9)a 0.8 (1.2)a 1.2 (1.5)a 1.2 (1.2)a

Total vessel area (mm2) 0.4 (0.9)b 1.0 (1.4)a 0.6 (1.0)b 0.9 (1.4)a 1.0 (1.3)a 0.9 (0.9)b

Average vessel area (�m2) 418c 792a 355c 636b 616b 577b

No. of vessels 984 (100)c 1372 (100)b 1655 (100)a 1450 (100)b 1687 (100)a 1663 (100)a

No. of vessels < 300 �m2 207 (21.1)b 13 (1.0)d 612 (37.0)a 24 (1.7)d 51 (3.0)d 145 (8.7)c

No. of vessels 300–700 �m2 751 (76.3)a 615 (44.8)c 1015 (61.3)b 967 (66.7)b 1149 (68.1)b 1099 (66.1)b

No. of vessels > 700 �m2 26 (2.6)c 744 (54.2)a 28 (1.7)c 459 (31.6)b 487 (28.9)b 419 (25.2)b

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.3. Anatomical characteristics of scion stems

The investigated varieties did not differ significantly accordingo their total stem cross-section characteristics (pith, secondaryood, secondary cortex, and periderm area), while xylem char-

cteristics showed differences. Xylem area in ‘Hedelfingen’ waslightly greater than that in ‘Bigarreau Burlat’ and ‘Summit’. Thereatest total vessel cross-section area and the greatest averageessel area was determined for ‘Bigarreau Burlat’ variety, withignificantly lower values for ‘Summit’, and the values related toHedelfingen’ between the two extremes. Increasing number ofmall vessels (vessels smaller than 300 �m2) and decreasing num-er of large vessels (vessels larger than 700 �m2) were noted in theame variety order, from ‘Bigarreau Burlat’ to ‘Summit’ (Table 3).

Outer, middle and inner secondary wood anatomical character-stics of the investigated varieties followed the trend identified forhe total secondary wood area, with two exceptions. The middleing total vessel area was the highest for ‘Hedelfingen’ (0.99 mm2),

ollowed by ‘Bigarreau Burlat’ (0.96 mm2), and ‘Summit’ with theowest value (0.75 mm2). The inner ring average vessel area washe greatest for ‘Bigarreau Burlat’ (694 �m2), followed by ‘Summit’572 �m2) and ‘Hedelfingen’ (452 �m2).

able 3ne-year old scion stem anatomical characteristics of three cherry varieties.

‘Bigarreau Burlat’

Cross-section area (mm2) 52.3 (100)a

Periderm area (mm2) 2.2 (4.2)ab

Phloem area (mm2) 19.7 (37.6)a

Wood/phloem ratio 1.3a

Pith area (mm2) 4.9 (9.4)a

Anatomical characteristics of total wood surface areaWood area (mm2) 25.5 (48.7)a

Xylem area (mm2) 21.7 (41.5)a

Total ray area (mm2) 3.8 (7.2)a

Total vessel area (mm2) 2.7 (5.2)a

Average vessel area (�m2) 589a

No. of vessels 4576 (100)b

No.of vessels < 300 �m2 616 (13.5)c

No.of vessels 300–700 �m2 2986 (65.3)a

No.of vessels > 700 �m2 974 (21.2)a

Anatomical characteristics of wood outer zoneWood area (mm2) 10.9 (20.9)a

Xylem area (mm2) 9.7 (18.4)a

Total ray area (mm2) 1.3 (2.5)a

Total vessel area (mm2) 0.9 (1.8)a

Average vessel area (�m2) 484a

No. of vessels 1943 (100)a

No.of vessels < 300 �m2 475 (24.5)b

No.of vessels 300–700 �m2 1351 (69.5)a

No.of vessels > 700 �m2 117 (6.0)a

Anatomical characteristics of wood middle zoneWood area (mm2) 8.6 (16.3)a

Xylem area (mm2) 7.7 (14.7)a

Total ray area (mm2) 0.9 (1.6)a

Total vessel area (mm2) 1.0 (1.9)a

Average vessel area (�m2) 648a

No. of vessels 1481 (100)a

No.of vessels < 300 �m2 60 (4.1)a

No.of vessels 300–700 �m2 964 (65.1)a

No.of vessels > 700 �m2 457 (30.8)a

Anatomical characteristics of wood inner zoneWood area (mm2) 6.0 (11.5)a

Xylem area (mm2) 5.4 (10.4)a

Total ray area (mm2) 0.6 (1.1)a

Total vessel area (mm2) 0.8 (1.5)a

Average vessel area (�m2) 694b

No. of vessels 1152 (100)b

No.of vessels < 300 �m2 81 (7.0)b

No.of vessels 300–700 �m2 671 (58.3) b

No.of vessels > 700 �m2 400 (34.7)a

ulturae 160 (2013) 189–197 193

3.4. Simulation of grafted cherry tree vigor based on theoreticalhydraulic conductance

The simulation of grafted cherry tree included hydraulic con-ductivity of root system (Kh(R)), rootstock stem (Kh(RSt)) and scionstem (Kh(SSt)), with all specificities of single plant organ, the resultsof which are shown in Table 4. Single root Kh, total root systemKh(R) and functional root system hydraulic conductivity Kh(Rc) var-ied significantly and showed the greatest differences, since noneof the investigated rootstocks could be grouped. The highest totalrootstock stem hydraulic conductivity Kh(RSt) values were deter-mined for ‘Colt’ and ‘Oblacinska’ sour cherry selection OV1, withup to 25% lower values associated with P. avium and P. mahaleb.The values corresponding to the same trait in low vigor rootstocks‘Gisela 5’ and P. fruticosa selection SV2 were two to three timeslower than in ‘Colt’. Because of the overlap between the scion pitharea/rootstock secondary wood inner ring tissue, anatomical char-acteristics and closely related hydraulic conductivity of functional

xylem of all three rings in scion stems and two rings (middle andouter) of rootstock stems were included in the model of scion stemvigor contribution. When functional xylem area and functional ves-sel area of rootstock stems were considered, similar theoretical

‘Summit’ ‘Hedelfingen’

50.9 (100)a 53.9 (100)a

2.1 (4.3)ab 2.0 (3.7)b

18.3 (36.3)a 19.7 (36.7)a

1.3a 1.3a

6.2 (12.3)a 6.1 (11.4)a

24.2 (47.1)a 26.1 (48.3)a

21.4 (42.1)a 23.1 (42.8)a

2.8 (5.6)b 3.1 (5.7)b

2.1 (4.0)b 2.6 (4.8)ab

421b 442b

4875 (100)b 5819 (100)a

1593 (32.7)a 1320 (22.7)b

2684 (55.1)a 3840 (66.0)a

598 (12.2)b 659 (11.3)b

10.0 (19.5)a 11.0 (20.3)a

9.0 (17.6)a 9.7 (17.9)a

1.1 (2.1)a 1.4 (2.2)a

0.6 (1.2)b 0.9 (1.6)a

289b 352b

2075 (100)a 2418 (100)a

1167 (56.2)a 935 (38.7)a

908 (43.8)a 1459 (60.3)a

0 (0)b 24 (1.0)b

8.1 (15.7)a 8.7 (16.1)a

7.1 (14.0)b 7.7 (14.3)a

0.9 (1.9)a 1.0 (1.9)a

0.8 (1.5)a 1.0 (1.8)a

495b 555ab

1576 (100)a 1785 (100)a

259 (16.4)b 144 (8.1)ab

1089 (69.1)a 1257 (70.4)a

228 (14.5)a 384 (21.5)a

6.0 (11.7)a 6.4 (11.8)a

5.3 (10.4)a 5.7 (10.6)a

0.7 (1.4)b 0.7 (1.2)ab

0.7 (1.4)b 0.7 (1.4)b

572b 452a

1224 (100)b 1616 (100)a

167 (13.6)a 241 (14.9)a

687 (56.1)b 1124 (69.6)a

370 (30.3)a 251 (15.5)b

194 M. Ljubojevic et al. / Scientia Horticulturae 160 (2013) 189–197

Table 4Root system, rootstock stem and scion stem hydraulic conductivity (10−5 kg m/MPa s).

P. fruticosa SV2 P. cerasus‘Oblacinska’ OV1

‘Gisela 5’ ‘Colt’ P. mahaleb P. avuim

Single skeletal root hydraulic conductivity Kh 4.29d 3.77e 1.37f 10.37b 9.59c 11.02a

Average number of skeletal roots 4.33a 3.67a 3.30a 5.67a 5.67a 5.67a

Root system hydraulic conductivity Kh(R) 18.58d 13.84e 4.52f 58.80b 54.38c 62.48a

Functional root system hydraulic conductivity Kh(Rc) = (Kh(R) × Cwu) 11.14d 6.74e 3.07f 52.45b 49.38c 62.48a

Rootstock stem total hydraulic conductivity Kh(RSt) 7.12c 19.27a 7.89c 20.60a 14.01b 15.42b

Rootstock stem inner zone hydraulic conductivity Kh(RSt-ir) 1.45c 3.79a 1.19c 2.86a 2.30b 2.15b

Rootstock stem middle zone hydraulic conductivity Kh(RSt-mr) 3.59c 8.72a 3.54c 8.99a 6.27b 5.55b

Rootstock stem outer zone hydraulic conductivity Kh(RSt-or) 2.08c 6.76b 3.16c 8.75a 5.44b 7.72a

Functional rootstock stem hydraulic conductivity Kh(RStf) = Kh(RSt) − Kh(RSt-ir) 5.67d 15.48b 6.70d 17.74a 11.71c 13.27c

‘Bigarreau Burlat’ ‘Summit’ ‘Hedelfingen’

Functional scion stem hydraulic conductivity Kh(SSt) (all three wood zones) (10−5 kg m/MPa s) 10.29c 6.96d 7.70d

Fig. 1. Functional hydraulic conductance of root system, rootstock stem and scion stem of six cherry rootstocks and three sweet cherry varieties (A – P. avium; B – P. mahaleb;C – ‘Colt’; D – P. cerasus ‘Oblacinska’ selection OV1; E – P. fruticosa selection SV2; F – ‘Gisela 5’.

M. Ljubojevic et al. / Scientia Horticulturae 160 (2013) 189–197 195

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ig. 2. Model of plant vigor based on the limiting theoretical hydraulic conductancV1; E – P. fruticosa selection SV2; F – ‘Gisela 5’).

ydraulic conductance (Kh(RStf)) was determined again in P. aviumnd P. mahaleb, as well as in ‘Gisela 5’ and selection P. fruticosaelection SV2 (Table 4).

Graphically simulated water conductivity of the root system,ootstock stem and scion stem are presented in Fig. 1. Accordingo these results, four different water regulation patterns could beetermined. Root system of vigorous rootstock P. avium, P. mahalebnd ‘Colt’ can send much higher amounts of water than rootstocknd scion stems can receive and forward to leaves. In this series,cion stem anatomy, and consequently its hydraulic conductivity,s the limiting factor in the water flow, but is still sufficient to

eet maximum crown conductance of the scion. In contrast to theforementioned pattern, root system of ‘Oblacinska’ sour cherryelection OV1 can send much lower quantity of moisture thanootstock and scion stem can conduct. In this water regulation pat-ern, root system hydraulic conductivity is the lowest and thus theimiting factor. Root system of P. fruticosa selection SV2 is character-

zed by medium hydraulic conductivity that nonetheless exceededootstock stem water conductivity. Since scion stem hydraulic con-uctivities of the investigated varieties are higher than those of the. fruticosa selection SV2 rootstock stem, in this pattern, rootstock

otstock (A – P.avium; B – P. mahaleb; C – ‘Colt’; D – P. cerasus ‘Oblacinska’ selection

stem conductivity determines the plant water conductance. Wateruptake by root system of ‘Gisela 5’ is the lowest and well belowthe rootstock stem and scion stem conductive capacity. Root sys-tem can send much lower amounts of water than rootstock stemcan receive; however, in this line, rootstock stems also had lowerhydraulic conductivity than that in scion stems. Consequently,based on the functional hydraulic conductivity of root system androotstock stem and inherent scion stem hydraulic conductivity,vigor simulation model for each rootstock/scion interaction hasbeen developed (Fig. 2).

4. Discussion and conclusions

Since there are several plant organs participating in cherry treewater conductance, it is necessary to identify the limiting one, asit determines the quantity of water reaching the scion. Vercambreet al. (2002) showed that there was no reduction in axial conduc-

tance due to branching pattern of the Prunus root system, and thatthe main roots had at least 10% higher axial conductance than thesum of the axial conductance of the branches. Thus, we assumedthat number of large skeletal roots and their hydraulic conductivity

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96 M. Ljubojevic et al. / Scientia

Kh) fully determined the root system hydraulic conductivity Kh(R).here is no significant relationship between whole root surface areand root system hydraulic conductivity because some parts of theoot system do not participate in the water uptake. Rieger and Litvin1999) found that root system hydraulic conductivity is inverselyelated to root cortical thickness and the presence of a suberizedxodermis. As reported by Mu et al. (2006), active root surfacerea truly reflects the level of radial root functional efficiency andas thus adopted as the correcting coefficient of the whole root

ystem hydraulic conductivity in our vigor simulation modeling.ased on such methodology, this paper is introducing functionaloot system hydraulic conductivity Kh(Rc) as an improved approacho quantifying the rootstock contribution to the cherry tree vigor.

It was shown that total and active root surface area regularlyecreased with a reduction in rootstock vigor and correspondedo the size-controlling capacities of these rootstocks in relation to. avium. Active root surface area accurately reflects root systemhysiological activity and can be reliable pre-selection parameter

n size-controlling cherry rootstock breeding. The main advantagef the investigated method is that methylene blue solution is notarmful to plants; thus, after examination, root system can beinsed and planted in a container, where the plant resumes normalrowth and development. Furthermore, root system can be succes-ively monitored and evaluated from early stages of rhyzogenesisntil the optimal time for the pre-selection of future rootstocks.

Rootstock stem plays considerable role in water transport, sincet represents the point of graft symbiosis between hipobiont andpibiont. In the cherry plant vigor model for P. avium, P. mahaleb,

Colt’ and P. fruticosa selection SV2, the calculated rootstock con-ribution is represented by functional rootstock stem hydrauliconductivity Kh(RStf). In contrast, functional root system hydrauliconductivity Kh(Rc) is the limiting factor in ‘Oblacinska’ sour cherryelection OV1 and ‘Gisela 5’, since hydraulic conductivity of root-tock stem and scion is not the anatomical barrier for the waterransport to the scion. This indicates that there is more thanne size-controlling mechanism and that root and rootstock stemydraulic conductivities are both valid pre-selection parameters.ydraulic conductivity of the scion varieties was in agreement with

heir hereditary controlled plant growth. Functional rootstock stemydraulic conductivity (Kh(RStf)) in vigorous rootstocks P. avium, P.ahaleb and ‘Colt’ exceeded that of the investigated scion varieties.

n all three investigated low-vigor rootstocks—‘Oblacinska’ sourherry selection OV1, P. fruticosa selection SV2 and ‘Gisela 5’—theater solution conductance was below that of the scion.

Despite the similar and low theoretical hydraulic conductancealues, vessel size and pathway of water solution through the ‘cap-llary tubes’ of investigated rootstocks differs significantly. Themallest average vessel size accompanied by high proportion ofmall vessels was determined in both ‘Gisela 5’ roots and stem,mplying that much more energy is required to supply scion with

ater solution. According to Godini et al. (2008) and Végvárit al. (2008), ‘Gisela 5’ lacks the ability to overcome drought andeating of the rhizosphere; thus, rootstocks with such anatom-

cal traits should be favored in northern climatic regions, whereummers are short, rainy and cool. These results are in agreementith those reported by Hajagos and Végvári (2013), who hypoth-

sized that stem anatomical characteristics in cherry rootstocksight contribute to water stress sensitivity. Much more reliable

ootstock stem anatomical parameters could be obtained in two-ear-old rootstock stems taken prior to the grafting in early springLjubojevic, 2012), rather than on one-year-old shoots, as proposedy Hajagos and Végvári (2013). Slightly greater average vessel area

n roots of P. fruticosa selection SV2 and almost equal number of ves-els per cross-section favor this selection as a future better-adaptedow-vigor cherry rootstock for hot and dry summers. Low numberf large vessels in roots and rootstock stem, as in ‘Oblacinska’ sour

ulturae 160 (2013) 189–197

cherry selection OV1, are desirable only if such traits are associatedwith small amount of radially adopted water, resulting in suc-cessful low vigorous growth and development of grafted cherries.This leads to low vessel resistance to water conductivity, whichis ideal for semi-arid climate conditions. This supposition is sup-ported by empirical evidence, whereby 20-year-old sweet cherrytrees grafted on non-selected ‘Oblacinska’ sour cherry rootstocksare successfully grown in semi-arid conditions without irrigationin a hilly region of Prokuplje, Southern Serbia. Moreover, the resultsof Georgiev et al. (1997)—where ‘Oblacinska’ sour cherry is declaredas up to 50% less vigorous rootstock than P. mahaleb, and thus welladapted to arid Macedonian climate—indicate that this pattern isappropriate for semi-arid climatic conditions.

The model predicts the rootstock and scion cultivar vigorand rootstock/scion interaction based on the knowledge of theirmorphological and anatomical characteristics and calculated the-oretical hydraulic conductance. Application of the proposed vigorsimulation model is a result of multiple trait interactions and stronginterdependence among active root surface area, root systemhydraulic conductivity, rootstock stem and scion stem anatomicalcharacteristics and their hydraulic conductivity. The methodol-ogy could thus be an effective pre-selection simulation tool forestimating rootstock dwarfing capacity, scion cultivar vigor andspecific rootstock/scion interactions in rootstock and scion breed-ing programs and serve as a guide for spacing trees in high densityplanting. Its output is in full agreement with subsequent in vivomeasurements during three years following the planting. Based onthe stated model, P. fruticosa selection SV2 and ‘Oblacinska’ sourcherry selection OV1 are expected to be low-vigor cherry rootstockcandidates.

Acknowledgements

This research was supported and funded by the Serbian Ministryof Education and Science as one of the research topics in the project“Selection of sweet and sour cherry dwarfing rootstocks and devel-opment of intensive cultivation technology based on sustainableagriculture principles,” evidence number TR 31038, for the grantperiod 2011–2014.

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