agronomy Article Effect of Vegetative Propagation Materials on Globe Artichoke Production in Semi-Arid Developing Countries: Agronomic, Marketable and Qualitative Traits JouhainaRiahi1,CarloNicoletto2,* ID,GhaithBouzaein3,PaoloSambo2and KarimaKoukiKhalfallah1 1 DépartementdeProductionVégétale,InstitutNationalAgronomiquedeTunisie,43AvenueCharlesNicolle, Tunis1082,Tunisia;jouhaina_riahi@yahoo.fr(J.R.);karima.koukikhalfallah@gmail.com(K.K.K.) 2 DepartmentofAgriculture,Food,NaturalResources,AnimalsandEnvironment,UniversityofPadova, CampusofAgripolis,Vialedell’Università16,35020Legnaro(PD),Italy;paolo.sambo@unipd.it 3 Stationd’AppuideManouba,GroupementInterprofessionneldesLégumes(SAM),Manouba1120,Tunisia; ghaith_bouzaien@yahoo.fr * Correspondence:carlo.nicoletto@unipd.it;Tel.:+39-049-827-2826 Received:31August2017;Accepted:21September2017;Published:24September2017 Abstract: InTunisia,globeartichokeismainlypropagatedbyundergrounddormantaxillarybuds (ovoli),whichareremovedfromthefieldinAugustduringthequiescenceperiod. Thehighcost ofinvitro-plantsandtheabsenceofspecializednurserieswereamongthereasonsfortheriseof heterogeneity and spread of diseases. The aim was to help farmers to improve artichoke yield andqualitybyamelioratingtheirvegetativepropagationtechniquewithlowcostmethods. Three plant cuttings management methods were tested: summer ovoli (T0); spring offshoots nursery’s cuttingsforcedtopassavegetativerestperiodbystoppingirrigation(T1);andoffshootsnursery’s cuttings not forced (T2). The cuttings management can affect both yield and qualitative traits of artichoke. T1nurseryplantsproducedtheheaviestprimaryheads,7%and23%higherthanT2and T0,respectively. T1plantsexhibitedthehighestyieldduringtheharvestseason,with+17.7%and +12.2%comparedtoT0andT2,respectively. T0andT1showedthehighesttotalantioxidantcapacity andinulincontent;thepropagationmethodalsoaffectedtheshort-chainsugarsratio. T1isaviable andsustainablealternativetothetraditionalonethatdoesnotheavilyimpactongrowingcostsand improvesyieldandqualityofartichoke. Keywords: Cynarascolymus;cuttings;yield;antioxidant;phenolicacids;fructans;sugars 1. Introduction Globeartichoke(CinaracardunculusL.subsp. scolymus(L.)Hegi)isoneofthemostimportant cultivatedspeciesintheMediterraneanBasinandiscontinuingtobeplantedandadaptedinother partsoftheworldduetoitshealthbenefits[1,2]. InTunisia,thecultivationofglobeartichokeismainly concentratedinthelowMadjerdavalley. In2016,thetotalareainvolvedwiththiscropreached3850 hectares, and the total production was approximately 19,000 tons [3]. Around 75% of this area is representedbythecultivar“Violetd’Hyères”whichisthemostappreciatedpurplevarietyinTunisia foritsfastcommercializationinlocalandinternationalmarkets. Inthelastfiveyears,Tunisianglobe artichokeexportationshaveincreasedinaremarkableway,andreached1222tonsin2014[4]. Dueto thelargequantityofpropagationmaterialpresentinaplant,globeartichokesaregenerallypropagated vegetativelybyoffshoots,stumps,ordriedshootsharvestedfromcommercialfieldsattheendofthe growingcycle[5]. Inrecentyears,thepropagationofartichokeshasundergoneconsiderableevolution Agronomy2017,7,65;doi:10.3390/agronomy7040065 www.mdpi.com/journal/agronomy Agronomy2017,7,65 2of18 toavoidsoilbornediseasesfollowingthedevelopmentofmicro-propagationsystems[6,7],grafting techniques[8–10],andbyusinghybridseeds[11]. Alloftheseagronomicinnovationsarecommonly appliedindevelopedcountries, wheretherearenursery techniques andtechnologicalequipment. Inothercontexts,suchasTunisia,vegetativepropagationisthemostwidelyusedtechniquethatcan easilybeadoptedbyproducers. ForTunisianfarmers,earlinessisoneofthemostimportantfactorsfortheproduction,andit is directly linked to the export period which extends from November to January. The absence of specializednurseriesforartichokeplantletproduction,especiallyforthelocalvarieties,hasleadtothe growersproducingtheircuttingsbythemselves,ininappropriateconditions. Asaconsequenceof thisuncontrolledpractice,thenationalaverageyieldofglobeartichokehasneverexceeded7tha−1 duringthelastyears[3].Yet,manyresearchersinsomecountries,suchasItaly[5,12,13],Turkey[14,15], and the US [16], conducted several experiments to improve the vegetative propagation materials andproductiontechniquesofglobeartichoke;however,theydidnotrefertotheavailablevegetative materialofthefarmers,buttheyfocusedtheirattentionontheuseofmicro-propagatedplants. Then, they started to promote the nurseries’ establishment, and to schedule the cuttings’ propagation. This strategy seems to be quite difficult and inadequate in the case of Tunisia, for several reasons. Thefirstoneislinkedtotheabsenceofnurseriesfortheinvitro-plantproduction. Thesecondreason is related to the harvest time, that starts at the end of February or in March. As a result, Tunisian farmersarenotabletoexporttheirproductionandthisaffectsnegativelytheirincomes. Inadditionto that,headproductionofmicro-propagatedartichokescouldbelowerthantheordinaryplantsand instablefromoneseasontoanother[17,18]. In the last three decades, artichoke breeding programs have produced some hybrids, which started to be considered in the main artichoke producing areas as an alternative to the traditional ones[19]. Yet,hybridsarefreefromthemainendemicdiseaseslikevirusesandfungi,andshowed goodyields[20–22],buttheystarttoproduceheadslaterifcomparedtothestandardcultivars[23] andtheyarestillnotwidelycommercialized. Indeed,thecostofhybridseedsisoftenveryhighand notallfarmerscandealwithit. Consideringthequalitativeaspectsofartichoke,therearemanysourceswhichclearlydescribe thenoticeablehealthpropertiesandqualityofthisvegetable[1,24,25]. Untilnow,themainresearch lines evaluating the effects of agricultural practices on artichoke quality, are concerned with seed propagation[21,26,27],stresseffects[28],differentfertilizationtechniques[29,30],mycorrhizause[31], theapplicationofbio-regulators[32],andtheuseofsustainablefarmingsystems[33]. Regardingthe managementofvegetativepropagationmaterialandartichokequality,thereislittleinformation. Earliness,highyield,andgoodqualityoftheproductionarethemaincriteriatargetedbythe farmers. Theseobjectivescouldbereachedjustbyimprovingthequalityofcuttingsbyupgradingthe rootingofoffshootsinthenursery[12],scalingtheproductionofearlytransplants[34],orconditioning thetransplantstomitigateheat,droughtstress,andbioticstresses[15]. Themainobjectiveofthisworkistoimprovethequalityofartichokecuttingsonthebaseofthe simpletoolsthatTunisianfarmerscanafford. Inthistrial,plantsderivedfromnursery’scuttingswere evaluatedfortheiragronomic,marketable,andqualitativetraits,comparedtothetraditionalplants originatedfromfield’sovoli(undergrounddormantaxillarybuds). 2. Results 2.1. VegetativeGrowthandYieldParameters Following the plants’ vegetative growth 70 to 190 days after planting, nursery transplants of 163 days (T2) showed the lowest elongation rhythm (Figure 1) but the highest extension width comparedtotheplantsderivingfromthetwotypesofovoli: thetraditional,andthenursery’sones (Figure2). Thepre-germinationofovoliwasefficientforT0andT1afterarestperiodfortheactivation oftherootsystemandlateralbuds,obtainingagoodstartforvegetativegrowth. AgronoAmgAryogn2roo0mn1o7ym ,2y70 ,2160751, 77,, 675, 6 5 3 o3f o1f8 1 38o f18 1.41.4 aa T0T0 T1T1 T2T2 aa 1.21.2 aa aa aaaa bb )m( thgieh tn)m( thgieh tn001...680001...680abababab baabaa baabaa baabaa baabaa baabaa baabaa baba baba bb baabaa baabaa alPalP0.40.4 0.20.2 0.00.0 7070 8080 9090 101000 111010 121020 131030 141040 151050 161060 171070 181080 191090 DDayasy asf ateftre pr lpalnatnattaiotinon FigurFeiFg1iug.ruePr e1la . 1nP. tlPahnlaetn ihgt ehhigtehiegtvh eotv leouvltuoioltuinotnioa nac ccacocorcrdodirindnggin gttoo totthh teeh cecu uctuttittnitnginsgg’s st’’y tptyyepp uee suuesdse edfdo rfof otrh rteht hae reatircathricothikcoehk ove kevgeeegvtaeettigavteeitv aet ive proppargpoarptoaipoganagt.iaotWnio. niWt.h Wiitnhitinhth itneh tesh aseam smaeem ppee eprriieoordido,, ddd, adataata twa wewreeer raeen aaannlyaazllyeyzdze edbdy b Ayb yNAONAVONAVO,A aV,n Aadn, dvaa nvluadleusve wasl iwutheit snho wn loiet thlteetnrt eoirn ilne tter incocmocmmommonomnoa nrae raes risegi gsnniigififnicicfaaicnnattnllyyt lydd iidffffieferfreeenrentn tata t atpt p p<< <0 .000.5.00 55a caacccoccroodrridndgiinn gtgo ttoTo uTkTueukyke eyHy SHDHS DSTD eTsetT.s etSs. ttaS.ntaSdntaadrnadrd dear rredorrrose rrasr roaer rse are repreoproterdte. dT. 0T: 0s:u smummemr eorv oovlio; lTi; 1T: 1s:p srpinrgin ogf fosfhfsohootso tns unrusersryer’sy ’csu ctutitntginsg fso rfocercde dto tpo apsas sas va evgeegtaettiavteiv ree sret st reported. T0: summerovoli;T1: springoffshootsnursery’scuttingsforcedtopassavegetativerest peprieordio bdy b syt osptoppipngin igr riirgraigtiaotnio; nT;2 T: 2s:p srpinrgin ogf fosfhfsohootso tnsu nrusersryer’sy ’csu ctutitntginsg nso nt ofto rfocercde. d. periodbystoppingirrigation;T2:springoffshootsnursery’scuttingsnotforced. 1.81.8 aa 1.61.6 T0T0 T1T1 T2T2 aa aaaa aaaaaa aaaa )m( htdiw tnalP )m( htdiw tnalP011...1824011...1824bacbac bacbac bacbac abababab aaaaaa bbabba aaaaaa abababab abababab abbabb aa 0.60.6 0.40.4 7070 8080 9090 101000 111010 121020 131030 141040 151050 161060 171070 181080 191090 DDayasy asf ateftre pr lpalnatnattaiotinon FigurFeiFg2iug.ruePr e2l .a 2nP. ltPawnlatn idwt tiwhditdehvt heo vleouvltuoiltouiontnioa nac ccacoocrcrdodriindnggin gttoo totth hteeh eccu uctuttittnitnginsgg stsy tptyyepp eue suuesdse edfdo rfof otrh rteh thea reatircathricothikcoehk oev kevgeeegvtaeettgiavteeitv aet ive proppargpoarptoaipoganagt.iaoWtnio.i ntWh. Wiinthititnhh ienth steah smea smeaemp eper epiroieodrdi,o, ddd,a adttaaa twwa ewerreee raean naanalyalyzlyezzdee ddby bb yAy NAAONNVOOAVV AaAn adan ndvda vluavleausle uwse iwsthiwt hni otn hloe ntlteoetrtl eeirnt tine rin cocmommomno na rae rsei gsnigifniicfaicnatnlyt lyd idffiefrfeenretn at t apt p< <0 .005.0 5a caccocrodridngin gto toT uTkuekye yH SHDS DT eTset.s tS. taSntadnadradr der reorrros ras rae re common are significantly different at p < 0.05 according to Tukey HSD Test. Standard errors are repreoproterdte. dT. 0T: 0s:u smummemr eorv oovlio; lTi; 1T: 1s:p srpinrgin ogf fosfhfsohootso tns unrusersryer’sy ’csu ctutitntginsg fso rfocercde dto tpo apsas sas va evgeegtaettiavteiv ree sret st reported. T0: summerovoli;T1: springoffshootsnursery’scuttingsforcedtopassavegetativerest peprieordio bdy b syt osptoppipngin igr riirgraigtiaotnio; nT;2 T: 2s:p srpinrgin ogf fosfhfsohootso tnsu nrusersryer’sy ’csu ctutitntginsg nso nt ofto rfocercde. d. periodbystoppingirrigation;T2:springoffshootsnursery’scuttingsnotforced. ThTeh me monointoitroinrign go fo of fofsfhfsohooto fto fromrmataiotino nre rveevaeleadle dsi gsinginfiicfaicnatn dt idffieffreernecnecse bs ebtewtweeene nth teh ter etraetamtmenetns.t s. AThtA etth tmeh eeon nedni tdoo fro iJfna Jngaunoaurfayor y(f1f (5s1h05 o0do adtyasfy oasr fmateftrae ptri lopannlatnarettaivoteinoa)n,l e)t,hd teh seeim genmisisfisiiocsianon not fo dnf ienfwfeew roe fonfsfchfesohsootbose tsstt wastreateertdne.d tT.h 1Te 1at nraden adTt 0mT 0e nts. Atthweweerneedr feao fifraliJyral yncl uoclsaoers,y ea,(n 1adn5 0dsh dsohawoywesdea dtfht etehr hep ihglaihgnehtsaet stnito unnmu)m,btebhre eor feo mof fofissfhfssiohooontoso twsf wintheitw han ao naffv asehvreoargoaetgs oesf ot aafl rmatlemodso.t sT5t 1s5h asonhoodtosT tas0t a wt ere thteh een edn do fo tfh teh he ahravrevsetisntign gse saesaosno n(F (iFgiugruer 3e) 3. )T. 2T d2 idspislpaylaeyde dth teh leo lwowere or fofsfhfsohootos tps rpordoudcuticotino,n 1,4 1.74%.7% le sless s fairlyclose,andshowedthehighestnumberofoffshootswithanaverageofalmost5shootsattheend thtahna nT 1T. 1. oftheharvestingseason(Figure3). T2displayedtheloweroffshootsproduction,14.7%lessthanT1. Agronomy 2017, 7, 65 4 of 18 Agronomy2017,7,65 4of18 a a ab 6 a b t n T0 T1 T2 a a b lp 5 ab r e b p s 4 a t ab o oh 3 b s f fo a fo 2 a re a b 1 m u N 0 January February March April May Harevst time FiguFreig3u.reN 3u. mNubmerboerf ooff fosfhfsohootostsf oformrmeedd aaccccoorrddiinngg ttoo ththe ecuctutitntignsg tsyptye pueseuds feodr tfhoer athrteicahrotkiceh voekgeetvateigvee tative proppargoaptaigoant.ioWn.i Wthiitnhitnh ethsea smameep peerrioiodd,, ddaattaa wweerree aannaalylzyezde dbyb AyNAONVOAV, Aan,da nvadluveasl uweitshw niot hletnteor lient terin commcoomnmaorne asrieg nsiigfinciafincatlnytlyd idffifefreernentta att pp << 00..0055,, aaccccoordrdinign gtot oTuTkuekye HySHDS TDesTt.e Sstta.nSdtaarndd earrrdorse rarroer s are reporretpedor.teTd0.: Ts0u: msummemreor voovloi;liT; T11::s spprriinngg ooffffsshhooootst snnuursresreyr’ys ’csucttuinttgisn gfosrcfeodr cteod ptaossp aa svsegaevtaetgiveet aretisvt erest periopderbioyds btoyp sptoipnpginirgr iigrraigtiaotnio;nT; 2T:2s: psprriningg ooffffsshhoooottss nnuurrseseryr’ys’ scuctutitntgins gnsont footrcfoedrc. ed. First heads were harvested on 14 January 2016, and their height, diameter, and fresh weight were mFierasstuhreedad (Tsawbleer e1)h. aTr1v neustresedryo npl1a4ntJsa pnruoadruyc2ed01 t6h,ea hnedavtiheesitr phriemigahryt, hdeiaadmse wteirth,a an mdefarens whewigehigt hoft were meas2u69r egd, 7(T%a balned1 2)3.%T 1hniguhresre trhyanp lTa2n tasnpd rTo0d, urceespdetchtievehlye.a Ivni etsetrmpsr iomf ahreyighhet aadnsd wdiiathmeatemr,e parnimwaeryig htof 269gh,e7a%dsa pnrdod2u3c%edh ibgyh pelratnhtas ndeTr2ivainngd fTro0m,r ensuprescetriyv’es loyv.oInli taenrdm tsraodfihtieoingahl tfiaenldd’sd oiavmolei twere,rpe rsiimmailrayr.h eads prodTuhcee dflobwyepr liannittisatdioenri ovfi nTg1 fprloamntsn buergsuenry e’asrolivero tlhiaann dthter aodthietiro pnlaalntfise’ ltdre’satomveonltisw, aenrde tshimis irleasru.lTt hweasfl ower initiaptrioovnedo fbTy1 thpel aensttismbaetigoun nofe tahreli perertcheanntatghee oof tehaerlry pyliaenldt,s s’otr tehaet mpreimntasr,ya hnedadths iwserrees uadltvwanatasgperoouvs edby to grow and to gain more weight before the first time of harvest. theestimationofthepercentageofearlyyield,sotheprimaryheadswereadvantageoustogrowand togainmoreweightbeforethefirsttimeofharvest. Table 1. Characterization of primary harvested heads according to the cutting type used for the artichoke vegetative propagation. Table 1. Characterization of primary harvested heads according to the cutting type used for the Treatment Height (mm) Diameter (mm) Weight (g) artichokevegetativepropagation. T0 95.3 ± 1.5 a 92.5 ± 0.6 ab 208 ± 8 c T1 96.9 ± 1.9 a 94.8 ± 0.7 a 269 ± 11 a Treatment Height(mm) Diameter(mm) Weight(g) T2 89.9 ± 2.2 b 89.2 ± 0.4 b 249 ± 6 b T0 95.3±1.5a 92.5±0.6ab 208±8c Within each parameter, data were analyzed by ANOVA and different letters indicate significant T1 96.9±1.9a 94.8±0.7a 269±11a differences according to the Tukey’s HSD test at p < 0.05. Standard errors are reported. T0: summer T2 89.9±2.2b 89.2±0.4b 249±6b ovoli; T1: spring offshoots nursery’s cuttings forced to pass a vegetative rest period by stopping Withineachparameter,datawereanalyzedbyANOVAanddifferentlettersindicatesignificantdifferencesaccording irrigation; T2: spring offshoots nursery’s cuttings not forced. totheTukey’sHSDtestatp<0.05.Standarderrorsarereported.T0:summerovoli;T1:springoffshootsnursery’s cuttingsforcedtopassavegetativerestperiodbystoppingirrigation;T2: springoffshootsnursery’scuttings notfoTrhceed .yield of the local cultivar “Violet d’Hyères” was evaluated progressively through the measurement of heads weight per plant in each harvest for all treatments. As a consequence, cumulative yield per hectare (Figure 4) was monthly estimated along the growing cycle, from 14 The yield of the local cultivar “Violet d’Hyères” was evaluated progressively through the January to 15 May 2016. T1 plants, deriving from nursery’s ovoli, exhibited the highest head measurementofheadsweightperplantineachharvestforalltreatments.Asaconsequence,cumulative production during the harvest season, with a final cumulative yield of 29.21 t ha−1 against 24.03 t ha−1 yield per hectare (Figure 4) was monthly estimated along the growing cycle, from 14 January to (−17.7%) and 25.65 t ha−1 (−12.2%), respectively, for T0 and T2. 15May2016. T1plants,derivingfromnursery’sovoli,exhibitedthehighestheadproductionduring theharvestseason,withafinalcumulativeyieldof29.21tha−1 against24.03tha−1 (−17.7%)and 25.65tha−1(−12.2%),respectively,forT0andT2. AgronoAmgryon2o0m17y ,270,1675, 7, 65 5 of 18 5of18 a ab a 35 b T0 T1 T2 a b 1) 30 b b -a b h t 25 a ( d b le 20 iy e a b vit 15 b a lu 10 b m u C 5 0 January February March April May Harvest time Figure4.Cumulativeyieldevolutionaccordingtothecuttingstypeusedfortheartichokevegetati ve propFaiggautrieo n4.. CWumithuilnatitvhee ysiealmd eevpoelurtiioodn, adccaotardwinegr teo athnea lcyuztteindgbs ytyApeN uOseVdA foar nthde varatliucheoskwe vitehgentoatilveett erin commproonpaagraetisoing. nWifiitchainn ttlhye dsiafmfeer epnetriaotd,p dldM(aJra 2n0–1M5)a r2015) 11.8101 .±6 30.1±9 b0 .23b49.14 8.4 141.134.5 ±5 0±.170 a.2 9a48.4 46.412.5132 ±. 102.1±6 c0 .314c8.8 47.3 LateToytiaell dyie(>ldM ar2015) 24.1013±.8 00.1±5 b0 .19b1004 9.1 291.421.1±4 0±.150 a.1 7a100 48.425.6152±. 503.15± c 0.161c00 48.8 Totalyield 24.03±0.15b 100 29.21±0.15a 100 25.65±0.15c 100 Within the same period, data were analyzed by ANOVA and values with no letter in common are Withisnigtnhiefiscaamntelyp derififoedr,endta taat wp Mar2015) 260±3b 277±5a 247±3c Meanheaddiameter(mm) Earlyyield(Mar2015) 69±1ab 74±2a 62±2b Withinthesameperiod,datawereanalyzedbyANOVA,andvalueswithnoletterincommonaresignificantly differentatp<0.05,accordingtoTukey’sHSDTest.Standarderrorsarereported.T0:summerovoli;T1:spring offshootsnursery’scuttingsforcedtopassavegetativerestperiodbystoppingirrigation;T2: springoffshoots nursery’scuttingsnotforced. Thebiggestheadsizewasobtainedintheearlyharvestseason,withamaximumof109mmof diameterinthetreatmentT1,andthesmalleroneinthelateharvest,withanaverageof62mmfound inthetreatmentT2. AccordingtoTable4,morethan65%ofharvestedheadswereclassifiedbetween thetwosizes75mmand110mmofdiameterinalltreatments. T2wasthemostadvantageous,witha rateof71%,followedbyT0(69%)andT1(68%)ofheads. Forthesmallestsize,T2presentedabout 4.10tha−1withthehighestrateoftheproduction(16%). AccordingtoUNECEstandardclassification ofcommercialqualityartichokes(Table5),morethan50%oftheproductionwasclassifiedasanextra qualityonlyforplantsderivingfromnurseryandtraditionalovoli. T1wasthemostadvantageous treatment,withmorethan18tha−1fortheclassExtra,followedbyT0with12.25tha−1,andsofar, T2with3.09tha−1. FortheclassI,34%oftheT2totalproductionwasthehighestratecomparedto T0andT1. Concerningthelowestqualityclass,T1expressedthelowesttotalyieldwith4.38tha−1 converselytoT2,thatshowedthehighestportionofthetotalyieldwithanaverageof13.84tha−1. Table4.Yielddistribution(tha−1)anditspercentageclassifiedbydiameteraccordingtothecutting typeusedfortheartichokevegetativepropagation. Treatment T0 T1 T2 HeadDiameter tha−1 % tha−1 % tha−1 % D≥130m 1.44±0.01a 6 0.51±0.05c 2 0.77±0.01b 3 110m≤D<130mm 3.84±0.07ab 16 4.62±0.30a 18 2.57±0.31b 10 90mm≤D<110mm 8.65±0.18c 36 11.39±0.23a 39 9.49±0.07b 37 75mm≤D<90mm 7.93±0.28b 33 8.47±0.23c 29 8.72±0.15a 34 6mm≤D<75mm 2.16±0.08b 9 3.51±0.05b 12 4.10±0.06a 16 Withinthesamediameter,datawereanalyzedbyANOVAandvalueswithnoletterincommonaresignificantly differentatp<0.05accordingtoTukey’sHSDTest.Standarderrorsarereported.T0:summerovoli;T1:spring offshootsnursery’scuttingsforcedtopassavegetativerestperiodbystoppingirrigation;T2: springoffshoots nursery’scuttingsnotforced. Table5.Totalyielddistribution(tha−1)anditspercentageaccordingtothecuttingtypeusedforthe artichokevegetativepropagationinrelationtoUNECEclassification. Treatment T0 T1 T2 MarketableClasses tha−1 % tha−1 % tha−1 % ClassExtra 12.25±0.06b 51 18.11±0.24a 62 3.09±0.17c 12 ClassI 7.68±0.03b 32 6.72±0.14c 23 8.72±0.17a 34 ClassII 4.09±0.02b 17 4.38±0.04c 15 13.84±0.17a 54 Withinthesamemarketableclass, datawereanalyzedbyANOVAandvalueswithnoletterincommonare significantlydifferentatp<0.05accordingtoTukey’sHSDTest.Standarderrorsarereported.T0:summerovoli; T1:springoffshootsnursery’scuttingsforcedtopassavegetativerestperiodbystoppingirrigation;T2:spring offshootsnursery’scuttingsnotforced. Agronomy2017,7,65 7of18 2.2. QualitativeTraits Duringtheintermediateperiod(mid-early)ofheadharvest,thequalitativetraitsofmarketable product and leaves were evaluated for each treatment, in order to highlight any changes in the nutritionalprofileoftheplant. Thedataobtaineddemonstratethattheplantpropagationmethodcan significantlyaffectqualitativeaspects. Regardingpigmentcontent(Table6),T1andT2hadsignificantlyhighervaluesthanthecontrol treatment. In particular, the content of chlorophyll a, b and xanthophyll + carotenoids in T1 was higherof24.5%, 24.7%, and18.0%, respectively, ifcomparedtoT0. T0andT1showedthehighest totalantioxidantcapacityvaluesincontrasttoT2thatalsopresentedthelowestlevelsoftotalphenols. Regardingthephenolicacidcontent,thechemicalanalysesidentifiedthepresenceofchlorogenicacid andcaffeicacid. Forthefirstone,thehighestvalueswererecordedinT0andT1,respectively29.6% and30.2%greaterthanT2. Nosignificantdifferenceswerefoundwithcaffeicacid. Thequalitative parameters so far reported were also assessed in the plant leaves (data not reported), however, nosignificantdifferenceswereobserved,withtheexceptionofthechlorogenicacidcontent. Thelatter washigherinT0(91.2mgkg−1dw)andT2(89.0mgkg−1dw),whereasT1presentedthelowervalues (53.6mgkg−1dw). Thechlorogenicacidcontentintheleaveswasmuchlowerthanthatofthehead (−97.7%onaverage). Table 6. Effect of cutting type used for the artichoke vegetative propagation on pigments and antioxidantcompounds. Xanthofills+ Chlorogenic Chlorophylla Chlorophyllb TP TAC CaffeicAcid Carotenoids Acid µgg−1dw µgg−1dw µgg−1dw k(mg−g1GdAwE) k(mg−g1Fdew2+) (mgkg−1dw) (mgkg−1dw) artichokehead T0 221±3b 92.5±2b 29.5±1.5b 8361±56a 7636±43a 3873±25a 79.4 T1 293±4a 122±5a 37.4±2.4a 9068±78a 6827±72ab 3905±48a 69.2 T2 293±6a 124±7a 35.4±2.1a 6569±29b 6033±37b 2724±32b 54.3 ** * * *** * *** n.s. Withinthesametrait,datawereanalyzedbyANOVAandvalueswithnoletterincommonaresignificantlydifferent atp<0.05accordingtoTukey’sHSDTest.Standarderrorsarereported.T0:summerovoli;T1:springoffshoots nursery’scuttingsforcedtopassavegetativerestperiodbystoppingirrigation;T2: springoffshootsnursery’s cuttingsnotforced;TP:totalphenols;TAC:totalantioxidantactivity.n.s.:notsignificant;*:significantatp<0.05; **:significantatp<0.01;***:significantatp<0.001. Also,sugarcontentwasaffectedbytheplant’spropagationmode.Ingeneral,inulinconcentration was significantly higher than the other sugars considered (Figure 5), and was found only in the marketableproduct. Concerningthemarketableheads(Figure5A),thesucroseandinulincontentswereconditioned bythetreatmentsevaluatedinthisexperiment. T0andT1showedinulinvalueshigherthan180gkg−1 dw,whereasT2significantlydifferedfromT0,presenting12.8%less. Alwaysinthemarketablehead, eventhesucrosecontentwasaffectedbypropagationmethod,andT1andT2showedthehighest concentrations;nosignificantdifferenceswereobservedinglucoseandfructoseload. Interestingly, thepropagationmodealsoaffectedtheshort-chainsugarsratio. Thesucrose/glucoseratioranged from0.35to0.44,respectively,forT0andT1,whereasfructose/glucoseratio(0.7)wasratherconstant. Theleafbiomass(Figure5B)presentedsignificantlyhigherconcentrationsofglucosethanfructose andsucrose;moreover,treatmentssignificantlyinfluencedtheglucosecontent. T2suppliedthehigher responses,with19.7%and25.0%morethanT0andT1,respectively. Agronomy 2017, 7, 65 8 of 18 than fructose and sucrose; moreover, treatments significantly influenced the glucose content. T2 Agronomy2017,7,65 8of18 supplied the higher responses, with 19.7% and 25.0% more than T0 and T1, respectively. 220 220 A B 200 aab 200 180 b 180 T0 T1 T2 T0 T1 T2 160 160 )w140 )w140 d120 d120 1-g100 1-g100 a k g( 80 k g( 80 b b a a a 60 a a a 60 40 a a a 40 b a a 20 20 a a a 0 0 sucrose glucose fructose inulin sucrose glucose fructose FiguFreig5u.reE 5ff.e Ecftfeocft couf tctuinttgintgy tpyepeu useseddf foorr tthhee vveeggeettaatitvivee pprorpoapgaagtiaotnio onno snugsaurg caorntceonnt tienn atritnichaortkiec hhoeakde head (A)a(nAd) alenadv leeasv(eBs) (.BW). iWthiitnhitnh tehes asmameet rtraaiitt,, ddaattaa wweerree aannalaylzyezde dbyb AyNAONVOAV, aAn,da vnadluveas lwueitsh wnoit hletnteor letter incoimn cmomonmaorne asrieg sniigfincifaincatnlytlyd idffifefreerenntta att pp << 00..0055, ,aaccccoordrdinign gtot TouTkueky’esy H’sSHD STDestT. eSstta.nSdtaarndd earrrodrse rarroe rsare reporretpedor.teTd0.: Ts0u: msummemreor voovloi;liT; T11::s spprriinngg ooffffsshhooootsts nnuursresreyr’ys ’csucttuinttgisn gfosrcfeodrc teod ptaossp aa svsegaevtaetgiveet arteisvt erest period by stopping irrigation; T2: spring offshoots nursery’s cuttings not forced. periodbystoppingirrigation;T2:springoffshootsnursery’scuttingsnotforced. The mineral profile of the plant is another parameter that was affected by the propagation mode oTfh eartmicihnoekrea. lRpergoafirdleinog fmthaerkpetlaabnlte isheaando t(hTearblpe a7ra),m cehtleorridthesa,t pwhaosspahfafetecst,e dsublfyateths,e spordoiupmag, ation modpeootafsasirutimch, oaknde. cRalecgiuamrd iwnegrem saigrnkiefticaabnltelyh edaifdfer(eTnatb. lTe07 )e,xcphrelossreidd etsh,ep hhiogshperh arteessu,ltssu flofar taelsl ,tshoed ium, potascosimupmo,neanntds lcisatelcdi uambovwe,e Tre1 swigasn infiocta dnitflfyerednitf fferroemn tT.0 Te0xceepxtp rfoers scehdlortihdeesh aigndh esrodreiusmul tcsonfoternta, ll the compwohneerenatss Tli2s taendd aTb0o svheo,wTe1d wthaes sanmote dcoifnfteernetn otff rpohmospTh0ateexs.c eAps tpfaorrt ocfh ltohrei dleeasveasn, dthes ocdoniutemnt coofn tent, wherseoadsiuTm2, apnodtasTsi0umsh, oawnde dmtahgenessaiumme nciotrnattee nwtaos fspighnoifsicpahnatltye slo.wAers inp aTr2t. oRfetghaerdlinega vneistr,attehse, Tco0 ntent presented the highest concentration. of sodium, potassium, and magnesium nitrate was significantly lower in T2. Regarding nitrates, T0presentedthehighestconcentration. Table 7. Effect of cuttings type used for the vegetative propagation on mineral content in artichoke head and leaves. Table7. Effectofcuttingstypeusedforthevegetativepropagationonmineralcontentinartichoke hea dandClela− ves. PO43− SO42− Na2+ NH4+ K+ Mg2+ Ca2+ NO3− (g kg−1 dw) T0 12.4 aC l− 6.8P7 Oa 43− 2.6S9O a4 2− 2.N58a Aa2 +rticho0Nk.3eH3 h14e +ad 30K.2+ a M1.g821+ C3.a422+ a NOn3d− T1 12.3 a 5.41 b 2.16 b 2.67 a (g0.k34g7− 1dw2)8.3 b 1.75 2.78 b nd T2 10.6 b 6.69 a 2.28 b 2.03 b 0.385 29.2 ab 1.85 2.39 b nd Artichokehead *** *** *** *** n.s. * n.s. *** T0 12.4a 6.87a 2.69a 2.58Aarticho0k.e3 3le1af 30.2a 1.81 3.42a nd T0 T1 61.91 2.3a 3.352. 41b 4.23.01 6b 192..06 7a a 10..3304 7 4228..13 ab 21.9.785 a 2.788.52b n7d.34 a T1 T2 57.11 0.6b 3.260. 69a 5.20.02 8b 127..80 3a b 10..2398 5 4219..02 aabb 2.19.78 5ab 2.399.61b n5d.72 b T2 49.2 *** 3.45 *** 4.30** * 15.7** b* 1n.2.3s . 39.1* b 2n.5.3s .b *8*.*22 5.22 b n.s. n.s. n.s. *** Artichonk.se. leaf * * n.s. *** Within the same trait, data were analyzed by ANOVA, and values with no letter in common are T0 61.9 3.32 4.30 19.0a 1.30 42.1a 2.98a 8.52 7.34a significantly different at p < 0.05, according to Tukey’s HSD Test. T0: summer ovoli; T1: spring T1 57.1 3.20 5.00 17.8a 1.29 41.0ab 2.97ab 9.61 5.72b offshoots nursery’s cuttings forced to pass a vegetative rest period by stopping irrigation; T2: spring T2 49.2 3.45 4.30 15.7b 1.23 39.1b 2.53b 8.22 5.22b offshoots nursery’s cuttings not forced. nd: not detected; n.s.: not significant; *: significant at p < 0.05; n.s. n.s. n.s. *** n.s. * * n.s. *** **: significant at p < 0.01; ***: significant at p < 0.001. Withinthesametrait,datawereanalyzedbyANOVA,andvalueswithnoletterincommonaresignificantly differentatp<0.05,accordingtoTukey’sHSDTest. T0: summerovoli;T1: springoffshootsnursery’scuttings 3. Discussion forcedtopassavegetativerestperiodbystoppingirrigation;T2:springoffshootsnursery’scuttingsnotforced.nd: notdetected;n.s.:notsignificant;*:significantatp<0.05;**:significantatp<0.01;***:significantatp<0.001. Vegetative propagation methods on globe artichoke significantly affected the yield, and the marketable and qualitative characteristics of the product. Under the production point of view, the 3. Discussion Vegetative propagation methods on globe artichoke significantly affected the yield, and the marketable and qualitative characteristics of the product. Under the production point of view, thelowestgrowthrhythm,registeredinT2,couldbeduetothetransplantage[27]. Thiscaninfluence thevegetativedevelopmentofartichokeplants,modifyingthedevelopmentstageoftheauxiliarybuds thatwereactivatedduringthenurseryphaseandtheaerialpartofT2cuttingsgrewuplaterallyusing Agronomy2017,7,65 9of18 theaccumulatedreserves. TheheightdevelopmentofT2plantswasaffectedbytheslowemission ofnewadventitiousroots,andthedamageoftheexistedrootsduringthenurseryphase,afterthe removalofplantsfromthenurserytothefield. Infact,tissueagecanaffecttheabilityofcuttingsto formnewadventitiousroots,anditisalsolinkedtoontogeneticphases;thesemarkthedifferentiation of the tissue from meristem that is getting physiologically older and more mature [35]. The slow growthrateofT2plantalsoaffectedthereproductivephaseofthecrop,andthisresultisconfirmed byT1, whichproducedtheearliestandtheheaviestprimaryheadscomparedtoothertreatments. Theseresultsprovethatovolitypologycaninfluencethenumberofearlyharvestedheadsandhead weight,asreportedinliterature[36]. Overall,T1providedthehighestyieldresults,withmorethan 29tha−1,whichareinlinewiththoseobtainedfromotherexperiments. In2013,anexperimental essaywasconductedinKaâlatElAndalousinArianagovernateinthenorthofTunisia(37◦ N,10◦ E, altitude238m). Assuggestedinotherstudies[37],thebiggestheadsizewasobtainedintheearly harvestseason. Inaddition,theharvestperiodsignificantlyinfluencedthephysicalqualityofheads. Thelowestmeanweightandmeandiameterofheadswereobtainedinthelateharvestingperiod. Similarresultswerepresentedbyanotherexperiment[38],wherethehighestheadweight(253g)and headdiameter(74mm)wereobtainedon15January,whereasthelowestvalues(179gforheadweight and67mmforheaddiameter)wereregisteredon15March. Asreportedforagronomicandmarketableparameters,thequalitativeoneswereinfluencedby thevegetativepropagationmethods. Takingintoconsiderationheadcolorcharacteristics,different pigmentcontentswereobserved. Asknown,pigmentcontentdependsonthephotosyntheticcapacity ofleavesandleafarea[39]. Thisinformationcanbelinkedtoourexperiment,whereleavesofT1and T2plantswerewiderthanT0, infact, significantdifferenceswereobservedinplantwidthduring thevegetativephase. Thevaluesmeasuredforantioxidantcapacityweregenerallylowerthanthose observed for other artichoke varieties, like “Violetto di Chioggia” and “Violetto di S. Erasmo” [2]; ifweconsider“ViolettodiToscana”,instead“Violetd’Hyères”,thetotalantioxidantcapacity(TAC) valuesareonaverage50%higher. Thisvariabilityintheconcentrationofantioxidantcompoundsis mainlyduetogeneticaspects,agronomicpractices,andenvironmentalconditions[1,40]. Furthermore, the high content of antioxidants and total phenols in T0 and T1 may also be connected to more stressfulconditionsthattheplantcuttingshaveexperiencedbeforetransplantingintheexperimental field. The drought stress, that was induced for 60 days, at least for T0 and T1 plants to obtain cuttingswithquiescentbuds,hasinfluencedthequalityofproducedheadsduringthegrowingcycle. As previously reported [36], ovoli management has an important impact on the head production. Asknown,astressexperiencedbytheplantduringthegrowingseasoncansignificantlyinfluencethe antioxidantamount. Infact,plantstresstolerancemaybeimprovedbytheenhancementofinvivo levelsofantioxidant[41,42]. Thelowerorslowerrootsystemdevelopmentreduced,forsomeperiods, the nutrient and water availability to the plant, by inducing such responses. The low antioxidant content in T2 is probably due to the lower stress condition that the plant has suffered during the cropcycle. Asaresult,theconcentrationofchlorogenicacid(caffeoylquinicacid)waslowerinT2by 29.6%and30.2%comparedtoT0andT1. Basedontotalcaffeoylquinicacidcontents,caffeoylquinic acidisthemostabundantsinglecomponent(39%),followedby1,5-O-dicaffeoylquinicacid(21%), and3,4-O-dicaffeoylquinicacid(11%). Cynarin(1,3-O-dicaffeoylquinicacid)contentisusuallyvery low(about1.5%)inmethanolicextractsofartichoke[1]. Thechlorogenicacidcontentintheleaves was much lower than that of the head. This result is similar to what reported for the “Violetto di Toscana”artichokevariety(−82.9%)[43]. Moreover,itshouldberememberedthatthecaffeoylquinic derivatives content in artichoke tissues highly depends on the physiological stages of the plant. The total caffeoylquinic acid content can range from about 8% in young tissues to less than 1% in senescenttissuesondrymatterbasis[44]. Asknown,theartichokeisaspeciescharacterizedbyahighamountoflongandshortchainof sugars. Inadditiontosimplesugars, thefructangroupisofgrowinginterestasafunctionalfood ingredient,becauseoftheirpotentialbenefitsforhumanhealth[45–47]. Ashumanenzymescannot Agronomy2017,7,65 10of18 digestfructans,theyreachthecolonandserveasasubstrateforenterobacterialgrowth[1]. Fructan containing diets selectively stimulate bifidobacteria and make them the predominant species [48]. Consequently,anincreasedfecalcontentofshort-chainfattyacidsandadecreasedconcentrationof tumor-promotingsubstances,suchasammonia,wereobserved[49]. Theinulinvaluesmeasuredfor “Violetd’Hyères”artichoke,commonlygrowninTunisia,areinlinewiththoseobtainedforother varietiesofartichoke(LeCastelandGreenGlobe)[47]. Thesugarratioisalsogreatlyinfluencedbythe varietalcharacteristics. Thesucrose/glucoseratiorangesfrom0.46to2.29forthevarietiesPoivrade andBuette,respectively[47]. Otherauthors,instead,foundlowersucrose/glucoseratios(0.07–0.1), respectively, for“ViolettodiS.Erasmo”and“ViolettodiChioggia”[2]. Thehighconcentrationof glucose,comparedtofructoseandsucroseinleafbiomass,weresignificant. Treatmentsremarkably influencedtheglucosecontent,andT2suppliedthehighestoutcomes. Thisresultismainlylinkedto thebiggersizeoftheleavesinT2inthefirstpartofthecropcycle,thuspromotingthephotosynthetic activity.Thisconfirmsthatthehighartichokeleafareapositivelyinfluencedthephotosynthesisactivity, asalreadyreported[50]. Themineralprofilewasalsoaffectedbytheplantpropagationmode. Ingeneral,mostofresults areattributabletothedifferentabilityofoffshootsandovolitoformnewroots,andtotheirability toexplorethesoil. Somesignificantchangeshavebeenrecordedforpotassiumandsodium. Infact, thesemineralsarethemainindicatorsforplanttolerancetomitigatedroughtstress[51,52]. During thenurseryphase,thecuttingsofT2werecontinuouslyirrigateduntiltheirtransplantationinthe experimentalfield,whereascuttingsofT1andT0wereforcedtoenterinavegetativerestperiodby causingdroughtstressthroughstoppingofirrigationformorethan2months. After80daysfromfield transplantation,T2plantsemittednewsecondaryroots,mainlyinthe0.25mofthetopsoil,whereas T0andT1plantsdevelopeddeepersecondaryroots. Thiscouldexplainwhytheabsorptionofmineral nutrientswaslowerinT2thantheothertreatments. Ingeneral,themineralcontentwassignificantly higherintheleavescomparedtothemarketableyield. Sucharesponseisinagreementwithother findings[43]. Inthehead,themostabundantelementwaspotassium,withvaluescloseto30gkg−1 dwandto40gkg−1dwintheleaves. Ontheotherhand,thecontentofchloridesisparticularlyhigh, probablyduetotheirpersistenceinthesoil,becauseoftheuseofpotassiumchlorideasafertilizerfor previouscultures. Comparedtothemineralcompositionofothervegetablesreportedintheliterature, theglobeartichokerepresentsagoodsourceofK[53]. Inaddition,theNa/Kratioofglobeartichoke isoneofthelowestratios,followingpotato. Thisparameterisveryimportant,sinceahighlevelis involvedinincreasingbloodpressureandcardiovasculardiseases[54]. Therefore,theconsumptionof globeartichokemightalsobesuggestedtoovercomethesediseases. Moreover,theincreasedmineral contentintheleavescanbeexplainedbythecapacityofglobeartichoketocompartmentalizeexcess ionsinthevegetative,ratherthanthereproductive,partsoftheplant[55]. 4. MaterialsandMethods 4.1. ExperimentalSite TheexperimentwasconductedintheSupportStationofManouba(SAM),whichisunderthe supervision of the Inter-professional Group of Vegetables (GIL). It is located in Manouba region, situatedinthenorthofTunisia(36◦48(cid:48) N;10◦03(cid:48) E,altitude469m). Thelocalclimateofthisareais characterizedbyanuppersemi-aridstage,withanaveragedailytemperaturerangingfrom9◦Cas minimuminJanuary,to25◦CasmaximuminAugust. Therainfallisirregular,withanaverageof 450mmperyear. MeteorologicaldatarecordedduringthetrialperiodarereportedinFigure6.

Effect of Vegetative Propagation Materials on Globe Artichoke Production in Semi-Arid Developing

Similar Effect of Vegetative Propagation Materials on Globe Artichoke Production in Semi-Arid Developing