Growth Response of Different Species of Ziziphus to Inoculation With

Fruits (3), 174–181 | ISSN 0248-1294 print, 1625-967X online | https://doi.org/10.17660/th2017/72.3.7 | © ISHS 2017 Original article Growth response of different species of Ziziphus to inoculation

, S. Mania 7 and with arbuscular1,2,3,6,a 4 mycorrhizal1,2 2 fungi 5 3 1,2 B. Thioye3,6 , A. Kane , C. Ndiaye , A. Ould Soule , D. Fall , R. Duponnois , S.N. Sylla A.M.1 Bâ 2 Département de Biologie Végétale, Université Cheikh Anta Diop, BP 5005, Dakar, Senegal

3 Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, BP 1386, Bel-Air Dakar, Senegal Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR113 INRA/AGRO-M/CIRAD/IRD/UM2-TA10/J, Campus

4 International de Baillarguet, 34398 Montpellier, France

5 Embrapa Agrobiologia, Km 7 BR 465 Seropédica, Rio de Janeiro, Cep 23891 000, Brazil

6 Centre National de Recherches Forestières (CNRF), BP 2312, Dakar-Hann, Senegal 7 Laboratoire de Biologie et Physiologie Végétales, Faculté des Sciences Exactes et Naturelles, Université des Antilles, BP 592, 97159 Pointe-à-Pitre, Guadeloupe, France Ecole Normale Supérieure de Nouakchott, BP 990, Mauritania Summary Significance of this study Introduction – Many of species of Ziziphus are un- What is already known on this subject? derutilized crops despite their potential interests in • agroforestry systems. Except for Ziziphus mauritiana, the effectiveness of arbuscular mycorrhizal fungi mineralThe effectiveness nutrition of arbuscularZ. mauritiana mycorrhizal seedlings. fungi (AMF) on growth and mineral nutrition of Ziziphus (AMF) is well and widely known for the growth and spp. is not known. The aim of our study was to eval- What are the new findings? uate the mycorrhizal dependency (MD) of Ziziphus • R. irregu- spp. in greenhouse conditions. Materials and meth- laris Ziziphus ods – Three isolates of AMF were used: Rhizopha- (includingMycorrhiza Z. inoculation, mauritiana particularly with gus irregularis isolate IR27, Funneliformis mosseae isolate IR27, promoted seven species of isolate DAOM227131 and Rhizoglomus intraradices greenhouse conditions. ) growth by enhancing signifi- isolate DAOM197198, on seven species of Ziziphus: cantly biomass production and nutrient uptake under Z. mauritiana, Z. lotus, Z. spina-christi, Z. mucronata, What is the expected impact on horticulture? Z. amphibia, Z. abyssinica and Z. sphaerocarpa. Plants • Rhizophagus irregularis were grown in nursery receiving 20 g portions of a crude inoculum of AMF. The experiment was set up isolate IR27 constitutes a as a 4×7 factorial design consisting of three AMF, one mancepromising of species tool for of the Ziziphus production of higher quality control (disinfected soil without inoculum) and seven nursery stock with potential improved field perfor- Ziziphus spp. Results and discussion – Inoculation by in agroforestry systems. AMF significantly improved growth and mineral nu- Résumé trition of Ziziphus spp., particularly the P nutrition. Mycorrhizal dependency values of Ziziphus spp. declined with AMF in the following order: R. irregularis de Ziziphus (69.51%), R. intraradices (63.58%) and F. mosseae Réponse à l’inoculation de différentes espèces (52.45%). Total length of AMF hyphae in soil samples Introductionavec – Plusieurs des champignons espèces de Ziziphus mycorhi sont- from inoculated treatments was significantly higher zienssous-utilisées à arbuscules. malgré leur intérêt potentiel dans les in all Ziziphus spp. with R. intraradices combinations. systèmes agroforestiers. L’efficacité des champignons The differences of MD among the tested Ziziphus spp. mycorhiziens à arbuscules (CMA) sur la croissance seem to be due to differences in the development of et la nutrition minérale de Ziziphus spp. n’est pas hyphal length in the soil and in P uptake by the ex- connue à l’exception de Ziziphus mauritiana. L’objec- ternal hyphae. Conclusion – Rhizophagus irregularis tif de notre étude était d’évaluer la dépendance my- constitutes a promising tool for the production of corhizienne (DM) de Ziziphus spp. en serre. Matériel higher quality nursery stock with expected improved et méthodes – Trois souches de CMA ont été utilisées: performance of Ziziphus spp. in agroforestry systems. Rhizophagus irregularis isolat IR27, Funneliformis mosseae isolat DAOM227131 et Rhizoglomus intra- Keywords radices isolat DAOM197198, sur sept espèces de Zi- Senegal, jujube, Ziziphus ziphus: Z. mauritiana, Z. lotus, Z. spina-christi, Z. mu- spp., mycorrhizal dependency, cronata, Z. amphibia, Z. abyssinica et Z. sphaerocarpa. tree nursery, mineral nutrition, hyphal length, Les plants cultivés en pépinière ont reçu une portion agroforestry system de 20 g d’inoculum de CMA. L’expérience a été mise en place suivant un dispositif de type factoriel 4×7 a

Corresponding author: [email protected].

174 International Journal of Tropical and Subtropical Horticulture et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi et al et al Rhizophagus composé de trois CMA, un témoin non inoculé et irregularis Glomus aggregatum sept Ziziphus spp. Résultats et discussion – L’inocu- et al., 2012). Guissou . (1998) showed that lation avec les CMA a considérablement amélioré la , isolate IR27 (syn. Z. mauritiana IR27; [Bâ croissance et la nutrition minérale (en particulier le ., 1996]), was one of the AMFZ. providingmauritiana high growth and phosphore) des espèces de Ziziphus. Les valeurs de la Plenchettemineral nutrition et al benefits for seedlings. My- dépendance mycorhizienne des espèces de Ziziphus corrhizal dependency (MD) of et al as defined byet ont diminué suivant l’ordre : R. irregularis (69,51%), al et. al(1983), can reach a maximum of 78%. Simi- R. intraradices (63,58%) et F. mosseae (52,45%). La lar results were found byZ. Guissoumauritiana . (2001) and Sidibé longueur totale des hyphes de CMA dans les échantil- . (2012). Bâ . (2001, 2003) concluded that the absence lons de sol était significativement plus élevée dans les of AM inoculation on seedlings in nursery traitements inoculés avec R. intraradices. Les diffé- could lead to higher mortality of outplanted jujube trees in rences de DM entre Ziziphus spp. semblent être dues betweenthe field. originIt is also and well cultivars known within that responses a single species of AM (Smith inocula et- à des différences au niveau du développement et de la altion vary greatly fromet alone plant species to another and even longueur des hyphes dans le sol et de l’absorption de of considering seed provenance of Z. mauritiana when per P par les hyphes extramatricielles. Conclusion – Rhi- ., 2009). Guissou . (2016) highlighted the importance zophagus irregularis constitue un outil prometteur - pour la production de qualité supérieure de plants forming pre-selection of mycotrophic plant candidates prior en pépinière avec des performances améliorées des to large-scale fruit tree propagation in orchardsZiziphus and is subjected agrofor- espèces de Ziziphus dans les systèmes agroforestiers. estry systems. etThe al complex taxonomy in the genus Mots-clés to debates and could be betweenZ. mauritiana 86 and 170, the species Indian (Azam- jujube Ziziphus orAli ber, and., 2006). Z. jujuba However, the two major cultivated specieset al., in agroforestry systems are Sénégal, jujubier, spp., dépendance mycorhi- Ziziphus are underutilized Mill. the Chinese jujube (Azam-Ali zienne, pépinière, nutrition minérale, longueur d’hyphes, 2006). Many of other species of système agroforestier crops despite their potentialZ. mauritiana interests in, agroforestrythe effectiveness sys- Introduction tems as fruits, firewood, fodder, medicines Ziziphus and live spp. hedge is (Soule, 2011). Except for a combination of approaches including selection and multi importanceof AMF on growth for these and multipurpose mineral nutrition fruit treesof because P is Domestication of fruit trees could be achieved through not known. Arbuscular mycorrhizae may have a particular et al - jective of this work was to investigate the effects of three ofplication the promising of quality approaches planting material, that can befertilization, used in the irrigation, domesti often theRhizophagus limiting nutrient irregularis in agroforestry isolate systems. Funneliformis The ob- pruning, and controlled mycorrhization (Bâ ., 2003). One mosseae Rhizoglomus intraradices - AMF ( IR27, cation of indigenous fruit trees is the arbuscular mycorrhizal mineral nutritionisolate DAOM227131 of seven species and of Ziziphus (Z. mauritiana, (AM) inoculation, since it is established thatet al many of these Zisolate. lotus ,DAOM197198) Z. spina-christi ,on Z. mucronatamycorrhizal, Z dependency. amphibia, Z .(MD) abyssini and- fruitet trees al beneﬁt in terms of growth and mineral nutritionet al., ca and Z. sphaerocarpa) in greenhouse conditions. from this symbiotic association (Guissou ., 1998, 2016; Bâ ., 2000, 2001; Mathur and Vyas, 2000; Sidibé Materials and methods Glomeromycota2012). The AM (Schüßler symbioses et are al associations between roots of terrestrial plants and members of the fungal phylum Soil preparation ., 2001). These are the most The soil used in the experiment was collected from San common and widespread symbioses,et involving al 80% of land plants and at least 250 morphologically defined arbuscular - plantsmycorrhizal for nutrient fungi (AMF)capture (Davison through its network., 2015). of The external AMF galkam (14°46’N, 17°13’W), Senegal. It was a sandy soil with receive plant-synthetized carbon and increase capacity of 88.8% sand, 5.8% silt, 5.4% clay, 0.6% organic matter, 0.3% biofertilizers for sustainable agriculture (Verbruggen et al., total C, 0.02% total N, ratio C/N = 14, 333.5 ppm total K, 41.4 hyphae (Smithet al and Read, 2008). The AMF are promoted as ppm total P, 2.1 ppm P-Bray 1, 1.03 ppm Ca, 0.3 ppm Mg, pH = 6.0 of a soil/water mixture (ratio 1:2, v/v) and pH = 4.6 of a 2013; Hart ., 2015). Nevertheless, they are poorly inves- soil/KCl mixture (ratio 1:2, v/v). The soil was passed through tigated,Ziziphus particularly mauritiana with the indigenous fruit trees from the a 2 mm sieve, sterilized for 4 h in an autoclave oven system at oneSahelian of the and indigenous Sudanian zonesfruit treeof West species Africa. farmers maintain 180 °C to eliminate native AMF, and transferred into plastic on their farms as a source Lam., of commonly food and namedincome jujube,in West is Fungalbags (1.5 inocula kg soil andper plasticinoculation bag). et al Rhizophagus irregularis Glomus aggregatum et al Africareforest (Ouédraogo degraded soils and., 2006). as hedgerows Jujube is to a protect multipurpose crops. FunneliformisThree isolates mosseae of AMF were used: tree providing mainlyZiziphus fruits and fodder. It also planted to isolate IR27 (syn. et al IR27) (BâRhizoglomus ., 1996), intraradices (T.H. Nicolson and Gerd.) C. Walker Nearly every part of plants can be utilized. Due to and A. Schüssler (Redeckeret al ., 2013) and etthe al high dry weight protein Z.content, mauritiana leaves are an important (N.C. Schenck and G.S. Sm.) Sieverd, G.A. Silva and source of protein for cattle (Arndt and Kayser, 2001; Ngwa Oehl (Sieverding ., 2014). The AMF were providedZea mays by the ., 2000). Responses of to AM inoculation LCM laboratory (IRD, Dakar, Senegal, certified ISO 9001, ver- tiondiffer and with morphological respect to functional properties compatibility, of the root (Guissou measured et alas., sion 2000). They were propagated on maize ( L.) for mycorrhizalet al formation, root colonization, nutrient absorp- 3 months on sterilized sandy soil in greenhouse conditions. Mycorrhizal inoculation of the soil was achieved by placing 1998; Bâ ., 2000, 2001; Mathur and Vyas, 2000; Sidibé 20 g portions of a crude inoculum of AMF consisting of sand,

Volume 72 | Issue 3 | May/June 2017 175 Plant materials Ziziphus Z mauritiana Z lotus Z spina-christi Z mucronata Z amphibia . Z abyssinica Z sphaerocarpa Seeds of seven species of ( . Lam., . (L.) Lam., . (L.) Desf., . Willd., . A. Chev , . A. Rich. and . Tul.) (Table 1) were surface-sterilized with 1% NaOCl for 15 min, washed several times and soaked in sterile distilled water for 30 min before being planted in the soil as three per plastic bag (24 cm × 7.5 cm). Plants were grown in the nursery at ISRA/IRD Research Center, Dakar – Bel Air, Senegal (14°44’N, 17°30’W) under natural sunlight (35 °C day, 27 °C night, relative humidity 75% and 14 h photoperiod).Ziziphus After emergence, the seedlings were thinned to one plant per plastic bag. The experiment was set up as a 4×7 factorial design consisting of three AMF and control and seven spp. Experiment was arranged in a completely Quantitativerandomized design evaluation with 15 replicates per treatment combination.

Ziziphus Four months after sowing, plants were harvested to measure height, dry weight of shoots and roots (48 h at 70 °C). The MD of each plant of spp. was calculated using the formula:

�� – �� %� = 100 × �� TDWM TDWNM et al where and are total dry weight of mycorrhizal and non-mycorrhizal plants, et al Ziziphus respectively (Plenchette ., 1983). For mycorrhizal root infection measurement, a part of fresh fine roots was collected from Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungithe root system of each seedling. Root were gently washed under tap water, bleached (KOH, 10%) at 80 °C during 30 min, and stained in 0.05% trypan blue at 80 °C during 35 min R. ir- following the method of Phillips and Hayman (1970). Percentage of root length colonized by spores, fragments of hyphae and maize root segments below and total P content was determined by colorimetry through regularis F. mosseae and R. irregularis was calibrated AMF was assessed at x40 etmagnification al using 100 fragments of lateral roots (approximately the seeds during transplanting. The inoculum density of a spectrophotometer1 cm length)at 660 onnm. microscopic Analyses were slides. performed Mycorrhizal root colonization was evaluated by using IR27, in the Agriculturalthe Chemistry method of Laboratory Trouvelot of Embrapa,. (1986). RioAfter de drying, leaf tissues of each plant were ground, 3 by the most probable number method (Adelman and Mor- samplesJaneiro, Brazil. from eachmineralized treatment through (three heating replicates at 500 per °C, treatdigested in 2 mL HCl (6N) and 10 mL HNO . Total K ton, 1986) as 1,635, 1,023 and 1,347 infective propagules per To measure contentthe length was of determined hyphae of each by the AMF, atomic 2 g of absorbance soil and total P content was determined by 20 g of inoculum, respectively. Controls also received 20 g of colorimetry through a spectrophotometer - at 660 nm. Analyses were performed in the Plantautoclaved materials crude inoculum of AMF. ment) were blendedAgricultural with 500 Chemistry mL distilled Laboratory water, and of Embrapa,30 mL Rio de Janeiro, Brazil. Seeds of seven species of Ziziphus (Z. mauritiana aliquots of this wereTo filtered measure and the stained length with of hyphaetrypan blueof each on AMF, 2 g of soil samples from each treatment Z. lotus Z. spina-christi Z. mucronata Willd., gridded membrane(three filters replicates (1.2 µm) per according treatment) to the were method blended with 500 mL distilled water, and 30 mL Z. amphibia ., Z. abyssinica Z. sphaerocar Lam.,- described by Jakobsenaliquots and of thisRosendahl were filtered (1990). and The stained gridded with trypan blue on gridded membrane filters pa (L.) Lam., (L.) Desf., membrane filters(1.2 were µm) mounted according on to slides the method and hyphae described were by Jakobsen and Rosendahl (1990). The gridded A. Chev A. Rich. and viewed at 100× by using an optical microscope (Olympus membrane filters were mounted on slides and hyphae were viewedGlomeromycota at 100× by using an PlantTul.) materials (Table 1) were surface-sterilized with 1% NaOCl for theBH4). Glomeromycota Many of hyphaeoptical and occurring microscope were attached on (Olympus the membranesto spores BH4). and Manypresent auxil of -hyphae occurring on the membranes presented 15 min, washed several times Ziziphusand soakedZ mauritianain sterile distilledZ lotused a morphologyZ spina-christia similar morphology to those similar produced to those by members produced of by members of the and were water for 30Z mucronata min before beingZ plantedamphibia in the soil. Z asabyssinica three Z sphaerocarpaattached to spores and auxiliary cells. All - intersections between hyphae and a gridded per plasticSeeds ofbag seven (24 speciescm × 7.5 of cm). Plants ( .were grown Lam.,in the . iary(L.) cells. Lam., All intersections. membrane filter between were hyphaecounted and in 20 a griddedfields of view. We used the method of Newman (1966) nursery(L.) Desf., at ISRA/IRD. ResearchWilld., Center,. DakarA. Chev – Bel, Air,. Sen- (H):membraneA. Rich. and filter . to were calculate counted hyphal in 20 length fields (H): of view. We used Tul.) (Table 1) were surface-sterilized with 1% NaOCl for 15 min, washed several times and egal (14°44’N, 17°30’W) under natural sunlight to one (35 plant °C day, per the method of Newman H = (1966) to calculate hyphal length 27soaked °C night, in sterile relative distilled humidity water 75% for and 30 14min h beforephotoperiod). being plant ed in the soil as three per� � � Afterplastic emergence, bag (24 cm the × 7.5seedlings cm). Plants were werethinned grown in theZiziphus nursery atwhere ISRA/IRD N Research Center,� � plasticDakar bag.– Bel The Air, experiment Senegal (14°44’N, was set 17°30’W) up as a 4×7 under factorial natural de- sunlidedght lines,(35 °C A day, 27 °C night,N L is the total line A signrelative consisting humidity of three75% andAMF 14 and h photoperiod). controlZiziphus and seven After emergence,length the seedlings of theis intersections gridded were thinned lines. Lbetween the hyphae and the grid- spp.to one Experimentplant per plasticwas arranged bag. The in experiment a completely was randomized set up as a 4×7 factorial design is thewhere consistingtotal area is intersections of the filter and between the hyphae and the gridded lines, is the total area of the Quantitativedesignof three with AMF 15 evaluationand replicates control per and treatment seven combination. spp. Experiment wasData arranged analysis in aDatafilter completely andanalysis is the total line length of the gridded lines. randomizedQuantitativeFour months design evaluation after with sowing, 15 replicates plants were per harvestedtreatment to combination. mea formed to normalize the distribution of data before statis Ziziphus spp. was calculatedZiziphus using- Mycorrhizal infectionMycorrhizal percentages infection were percentages arcsine trans were- arcsine transformed to normalize the surethe formula: Fourheight, months dry weight after sowing, of shoots plants and were roots harvested (48 h at to70 measure °C). performed height, dry weighton alldistribution data.of shoots Mean of valuesdata before were statisticalcompared analysis. usingP- Two-way analysis of variance (ANOVA) was Theand MDroots of (48each h plantat 70 of°C). The MD of each plant of spp.tical was analysis. calculated Two-wayperformed using the analysis on all data. of variance Mean values (ANOVA) were was compared using Tukey test (Honestly significant formula: Pdifferences, HSD) at the significance level ( < 0.05) with XLSTAT (version 2010, Addinsoft) software. Pearson’s correlation coefficient between dependent variables was performed Tukey test (Honestly significant differences, HSD) at the sig- pendentnificance variables level (using< was 0.05) the performed withsame XLSTAT software. using (version the same 2010, software. Addin- �� – �� 4 �� %� = 100 × soft) software. Pearson’s correlation coefficient between de- �� where TDWTDWMM and TDWTDWNMNM Results and discussion et al et al., where and are are total total dry dry weight weight of ofmycorrhizal mycorrhizal andRoot non-mycorrhizal colonization plants, andrespectively non-mycorrhizal (Plenchette plants, respectively., 1983). (Plenchette 1983).For mycorrhizal root infection measurement, a part of fresh fineffecte roots (P was collected from theFor root mycorrhizal system of each root seedling. infection Root measurement, were gently awashed part of under tapThe water, two factorsbleached (AMF (KOH, and plant species) had a signiﬁcant fresh10%) fine at 80roots °C duringwas collected 30 min, from and the stained root insystem 0.05% of trypaneach blue at 80< °C 0.05) during on all 35 parameters min studied (Table 2). speciesNo AM seedling.following Root the methodwere gently of Phillips washed and under Hayman tap water, (1970). bleached Percentage colonizations of root lengthR. irregularis were colonized observed had by colonized in the non-inoculated better Z. lotus controls, Z. am- (KOH,AMF was 10%) assessed at 80 °C at during x40 etmagnification 30 al min, and stained using 100 in 0.05% fragments try- of la(Tablephibiateral rootsand 2). Mycorrhizal Z.(approximately abyssinica infection varied with plant pan1 cm blue length) at 80 on°C duringmicroscopic 35 min slides. following Mycorrhizal the method root of colonizati Phil- andon wasAMF. evaluated by using R. irregularis and lipsthe andmethod Hayman of Trouvelot (1970). Percentage . (1986). of rootAfter length drying, colonized leaf tissues of each plant were ground, than the other AMF. Mycorrhizal R. intraradices in roots3 seedlings of Z. spina-christi, Z. mucro- bymineralized AMF was throughassessed heating at ×40 atmagnification 500 °C, digested using in 100 2 mL frag HCl- (6Nnata,colonization) and Z. 10 mauritiana mL was HNO signiﬁcantly and. Total Z. sphaerocarpa K higher with than with F. mosseae. mentscontent of waslateral determined roots (approximately by the atomicet al 1 cm absorbance length) on and micro total- P content F.was mosseae determined by scopicleafcolorimetry tissues slides. of through Mycorrhizaleach plant a spectrophotometerwere root ground, colonization mineralized at was 660 evaluated through nm. Analyses were performed in the byAgricultural using the methodChemistry of TrouvelotLaboratory of Embrapa,. (1986). After Rio de drying, Janeiro,. BOverall,razil.The extent of root showed colonization the lowest found AM colonizationin the inoculated com- To measure the length of hyphae of each AMF, 2 g of soil samplepareds tofrom the eachother treatment AMF (Table 3). 3 Z. mauritiana R. irregularis heating(three at replicates 500 °C, digested per treatment) in 2 mL HCl were (6N) blended and 10 withmL HNO 500 mL distilled water, and 30 mL Totalaliquots K content of this was were determined filtered and by stained the atomic with absorbance trypan blue on gridded membraneby filters was 78.20%. These values are Table(1.2 µm) 1. Geographicalaccording to the data method and characteristics described by Jakobsenof seed provenance and Rosendahl locations (1990). and The main gridded uses of the seven Ziziphus spp. membrane filters were mounted on slides and hyphae were viewed at 100× by using an Country of seed Seed collection Glomeromycota opticalZiziphus microscope spp. (Olympus BH4). Many of hyphae occurring on theLongitude membranes presentedLatitude Main uses provenance site a morphology similar to those produced by members of the and were attachedZ. mauritiana to spores and auxiliaryMauritania cells. All intersectionsBouguedra between 08°97’W hyphae and a gridded32°25’N Fruit, forage membraneZ. lotus filter were countedMauritania in 20 fields of view. WeAtar used the method13°05’W of Newman (1966)20°50’N Fruit, live hedge toZ. calculatespina-christi hyphal length (H):Mauritania Maghama 12°85’W 15°54’N Fruit, timber Z. mucronataH = Mauritania Maghama 12°85’W 15°54’N Forage, firewood � � � Z. amphibia Mauritania Bouguedra 08°97’W 32°25’N Fruit, medicine � � Z. abyssinicaN Burkina Faso Dindéresso A04°25’W 11°13’N Fruit, medicine Z. sphaerocarpaL France (Guadeloupe) Bois Jolan 61°36’W 16°23’N Fruit where is intersections between the hyphae and the gridded lines, is the total area of the Datafilter andanalysis is the total line length of the gridded lines.

176 Mycorrhizal infectionInternational percentages were Journal arcsine of transformed Tropical to nandormalize Subtropical the Horticulture distribution of data before statistical analysis.P Two-way analysis of variance (ANOVA) was performed on all data. Mean values were compared using Tukey test (Honestly significant differences, HSD) at the significance level ( < 0.05) with XLSTAT (version 2010, Addinsoft) software. Pearson’s correlation coefficient between dependent variables was performed using the same software. 4

et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi Table 2. Ziziphus spp. level on growth

Significance level obtained from two-way ANOVA testing the effects of AMF and Total dry Mycorrhizal Hyphal Mycorrhizal parameters, mycorrhizalHeight dependency,SDW hyphal RDW length andRoot/shoot mycorrhizal infection after four months under greenhouse conditions. Factors tested biomass dependency length infection (cm) (g) (g) ratios (g) (%) (cm g-1) (%) AMF *** *** *** ** *** *** *** *** Ziziphus spp. *** ** * * ** *** *** ** AMF×Ziziphus spp. *** *** ** NS *** *** *** *** Significant values are indicated: *P < 0.05; **P < 0.01; ***P < 0.001; NS: not significant to Tukey’s HSD; RDW: root dry weight; SDW: shoot dry weight. indicators of the effectiveness of inoculation (Guissou et al., similar to thoseet presented al by other authorset al as being good creasedwell as plant-plantaccording to interactions species in the (Smith following and Read, order: 2008). R. intra- In et al radicesour study,, R. irregularisthe production and F. of mosseae hyphal. R.length intraradices significantly who pro de- 1998,et al 2016; Bâ ., 2000, 2001; Sidibé ., 2012; Guissou, 2009).could have Moreover, a detrimental Bâ . (2000),effect on Guissou the growth (2009) of Z.and mauriti Sidibé- - ana . (2012) found that the absence of the AM inoculation duced the highest hyphalP length also mobilized more P than Pthe concentrations other AMF. Hence, in shoots there of was Ziziphus a significant positive cor- in unsterileR. irregularis nursery soils., R. intraradices Here, we have and extended F. mosseae these) on inrelation accordance (r = 0.908, with works< 0.0001) of Smith between et al hyphal length and sevenfindings Ziziphus by reporting spp. (including for the first Z. mauritiana time, the )effectiveness in greenhouse of that Medicago trunculata with Scutellospora spp. Ourcalospora results grew are three AMF ( Ziziphus spp. were colo better than plants growing with Gigaspora. (2000) caledonium who found. This nized better with R. irregularis R. intraradices conditions. All analyzedF. mosseae seedlings of - (67.10%) and Plantwas due growth to the development of external hyphae. (65.30%)Hyphal length than (59.96%). The growth advantages resulting from inoculation with There were some variations in the production of external Ziziphus spp. in Ziziphus spp. rhizospheric soil samples from inoculated treatments was AMF isolates were not the same for each hyphae by AMF (TableZiziphus 3). The spp.total associated length of hyphae with R. inintra- the the P-deficient soil (Table 3). Non-inoculated radices than R. irregularis and F. mosseae, except for Z. abyssi- ofdisplayed Ziziphus the lowest growth compared to the inoculated significantlynica higher in Ziziphus spp., the production of exceptplants. forInoculation Z. lotus. There with wasAMF a enhancedpositive effect significantly of R. irregularis height F. mosseae, in the production spp. as of compared biomass of with Ziziphus non-inoculated spp. when compared controls, R. irregularis (Table 3). and Irrespective R. intraradices of Z. mucro- external hyphae increased in the following order: nata. Rhizophagus intraradices increased biomass produc increased according to fungal species (Table in 3). the following order: to the non-inoculatedZ. mauritiana controls,, Z. amphibia except in andthe caseZ. sphaerocarpa of R. intraradicesIn our study,, R.the irregularis production and of hyphal F. mosseae length. Hence, significantly there - P masstion only production, on F. mosseae Zin. mauritianacomparison, Z to. mucronata non-inoculated, Z. amphibia ones. ,With and Z respect. sphaerocarpa to bio- was a significant positive correlation (r = 0.902, < 0.0001) showed higher values only on betweenet al development of external hyphae and MD.Triticum The re- Ziziphus spp. was aestivumsults of the present study are in agreement with those of observedas compared with with F. mosseae non-inoculated except forplants. Z. mucronata-R. The lowest effect irregu of- Yao . (2001) who found that the MD of three AMFlaris inoculationZiziphus on biomass sphaerocarpa production showed of the highest cultivars was determined by hyphalZ. development.sphaerocarpa R. irregularis irrespective Theand Zmycorrhizal. spina christi inoculation induced a significant decrease (Table 3). ofMoreover, the root/shoot there were ratios negative particularly correlations for the between root/ SDW values when inoculated with Z. ab- - compared with non-mycorrhizalP plants. yssinicaof plant-fungusR. irregularis combinations. RDW varied with plant spe- P cies and AMF and its highest values wereZiziphus observed spp. in were shoot ratiosP and hyphal length (r = -0.300, < 0.014), my- similar, -except in the casescombination of Z. spina-christi (Table 3). Theand root/shootZ. sphaero- corrhizal colonization (r = -0.236, < 0.184) and MD (r = carparatios of inoculated and non-inoculated -0.236, < 0.184). These results already occurred with argan Z. amphibia inoculated with R. irregularis and F. mosseae tree (Nouaim and Chaussod, 1994), and can be explained by . There was a significant increase in this ratio only in the higher efficiency of a mycorrhizal root system due to the R. irregularis developmentet al of external hyphae. The production of external of(Table Z. amphibia 3). This could probably be explained by the factet that al. hyphae could play a key role for uptake and transport of P positivelyAcaulospora influence spinosa RDW, Glomus and SDW manihotis production and (Jakobsen ., 1992). Our findings indicateR .that intraradices total length. Glomus aggregatum. Similar. trends were found by Guissou of hyphae in soil samples from inoculated treatments was (1998) and with R. irregularis and R. intraradices significantly higher in the associationP with There was a significant positive correlation between Of the AMF tested, only Z. mauritiana seedlings ofMD one and fungus hyphal depended length (r on = 0.822, the associated < 0.0001). Ziziphus Our measure spp. The- giveled to the increase best responses all parameters in terms measured. of biomass Our production findings conpar- ments of hyphal length clearly showed that the effectiveness firm previous R.studies irregularis indicating (Guissou that et al kobsen et al et al et al - hyphal length differed between AMF in previous studies (Ja- ticularly with ., 1998, 2009, 2016; ., 1992; Pearson and Jakobsen, 1993) and in the Bâ ., 2000, 2001; Sidibé ., 2012). present study. The underground hyphal networks formed The mycorrhizal dependency (MD) differed between by AMF can influence plant growth, nutrient acquisition as plant species according to the AMF (Table 3). Irrespective

Volume 72 | Issue 3 | May/June 2017 177 et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi

------Mycorrhizal infection (%) 62.50±8.60 de 64.33±9.90 d 66.89±10.31 cd 56.20±4.94 ef 43.69±8.63 i 67.46±6.96 cd 46.93±11.86 ghi 46.93±11.86 44.02±3.76 hi 79.84±14.45 ab 74.37±6.02 bc 51.67±5.47 fgh 76.95±4.50 b 84.96±4.87 a 73.55±2.42 bc 85.49±8.52 a 53.40±8.96 fg 49.12±9.67 fghi 67.05±15.26 cd 73.78±18.15 bc 46.09±14.46 ghi 78.20±16.29 ab ) -1 Hyphal ------length (cm g 53.60±2.31 bc 47.55±0.90 de 51.40±1.54 cd 52.29±1.92 c 40.38±1.09 i 56.83±0.65 b 54.28±0.74 bc 40.38±0.59 gh 32.81±2.05 i 61.37±1.13 a 44.25±1.14 efg 52.78±0.47 bc 61.80±1.25 a 42.54±0.49 fg 40.38±3.29 hi 55.46±1.06 bc 40.38±2.70 hi 41.94±1.79 g 63.14±1.94 a 34.10±1.51 i 46.62±0.77 ef

------Mycorrhizal 74.96±1.99 ab 68.81±1.66 de 78.65±1.65 a 68.15±2.25 de 44.14±1.26 g 70.55±1.30 cde 67.21±2.16 e 30.50±0.75 h 74.57±2.65 abc 55.02±1.43 f 45.40±0.90 g 68.88±1.43 de 46.14±1.55 g 57.52±1.38 f 69.66±1.06 de 55.74±1.46 f 68.22±1.58 de 45.29±1.80 g 70.30±1.22 de 69.33±0.66 de 71.73±1.07 bcd dependency (%) Total dry Total biomass (g) 0.82±0.45 f-i 1.79±0.32 ab 1.53±0.14 a-d 1.99±0.33 a 1.20±0.38 c-f 1.58±0.21 a-d 1.42±0.44 bcd 1.84±0.31 ab 0.37±0.04 ijk 1.55±0.12 a-d 1.30±0.23 cde 1.87±0.15 ab 0.20±0.03 k 0.63±0.17 h-k 0.84±0.09 e-i 0.29±0.04 jk 0.85±0.06 e-h 1.12±0.24 d-g 1.25±0.54 c-f 1.64±0.40 abc 0.21±0.03 k 0.73±0.24 g-j 0.46±0.15 h-k 0.71±0.25 g-j 0.45±0.16 h-k 1.56±0.14 a-d 1.48±0.24 bcd 1.64±0.31 abc ratios Root/shoot 2.37±1.10 a-d 1.32±0.27 e-i 1.05±0.23 f-j 1.01±0.41 f-j 2.33±0.40 a-d 2.43±0.65 ab 2.83±0.40 a 2.46±0.80 ab 0.48±0.13 j 1.20±0.14 e-j 1.40±0.30 e-h 1.63±0.13 c-g 1.39±0.21 e-i 0.85±0.45 g-j 0.50±0.07 j 1.62±0.18 c-g 2.98±0.45 a 1.57±0.40 d-g 1.96±0.67 b-e 1.85±0.29 b-f 1.61±0.31 c-g 0.67±0.41 h-j 0.50±0.32 j 1.18±0.26 e-j 2.24±0.62 a-d 1.85±0.38 b-f 1.59±0.29 d-g 1.85±0.72 b-f (g) < shoot dry weight. root dry weight; SDW: HSD; RDW: Tukey’s 0.05) according to RDW = 15). n 0.55±0.20 g-j 1.02±0.20 a-e 0.78±0.15 c-g 1.00±0.20 a-e 0.84±0.29 b-g 1.12±0.21 abc 1.05±0.36 a-d 1.31±0.30 a 0.12±0.03 k 0.84±0.03 b-g 0.76±0.15 d-g 1.16±0.06 ab 0.11±0.01 k 0.11±0.01 0.26±0.15 jk 0.28±0.05 jk 0.11±0.03 k 0.11±0.03 0.63±0.03 f-i 0.68±0.22 e-h 0.83±0.17 b-g 1.06±0.26 a-d 0.13±0.03 k 0.30±0.08 ijk 0.15±0.04 k 0.38±0.12 h-k 0.31±0.14 ijk 1.01±0.10 a-e 0.91±0.19 b-f 1.06±0.31 a-d ferent ( P (g) SDW 0.27±0.03 i-m 0.77±0.15 b 0.74±0.07 bc 0.99±0.19 a 0.36±0.11 g-k 0.36±0.11 0.46±0.08 e-i 0.37±0.10 f-k 0.53±0.03 d-h 0.25±0.02 j-m 0.70±0.10 bcd 0.54±0.14 c-g 0.71±0.09 bcd 0.08±0.01 m 0.36±0.07 g-k 0.56±0.05 c-g 0.17±0.02 klm 0.21±0.03 klm 0.44±0.07 e-j 0.42±0.08 e-j 0.57±0.15 b-f 0.08±0.01 m 0.43±0.20 e-j 0.31±0.13 i-l 0.33±0.14 h-l 0.14±0.02 lm 0.55±0.08 c-g 0.57±0.06 b-f 0.58±0.03 b-e (cm) Height 11.44±1.81 i 11.44±1.81 11.77±1.39 i 11.77±1.39 11.55±1.93 i 11.55±1.93 11.00±1.22 i 11.00±1.22 13.88±2.80 hi 29.22±3.52 abc 24.55±3.53 b-f 29.66±1.58 ab 12.88±1.76 hi 20.33±3.04 efg 20.33±2.29 efg 20.22±3.52 fg 28.00±4.18 a-d 24.22±3.64 b-f 29.22±3.10 abc 20.66±4.55 efg 23.00±4.59 d-g 18.11±2.52 gh 18.11±2.52 23.66±4.49 c-g 25.00±4.10 b-f 24.11±6.16 b-f 24.11±6.16 14.00±1.87 hi 13.55±1.13 hi 12.44±1.50 hi 13.33±1.13 hi 28.00±4.06 a-d 26.11±4.63 a-e 26.11±4.63 31.66±3.34 a Effect of inoculation with arbuscular mycorrhizal fungi (AMF) on growth parameters, mycorrhizal dependency, hyphal length infection hyphal after four months and under mycorrhizal Effect of inoculation fungi with dependency, (AMF) arbuscular mycorrhizal on mycorrhizal parameters, growth

spp. with or 3. Control R. intraradices F. mosseae F. Z. sphaerocarpa R. irregularis Control R. intraradices F. mosseae F. Z. abyssinica R. irregularis Control R. intraradices F. mosseae F. Z. amphibia R. irregularis Control R. intraradices F. mosseae F. Z. mucronata R. irregularis Control R. intraradices F. mosseae F. Z. spina-christi R. irregularis Control R. intraradices F. mosseae F. Z. lotus R. irregularis Control R. intraradices Ziziphus without AMF F. mosseae F. Z. mauritiana R. irregularis Means in the same column followed by letter are not significantly dif greenhouse conditions. Data values represent means represent conditions. Data values greenhouse ± ( errors standard Table

178 International Journal of Tropical and Subtropical Horticulture et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi Z. sphaerocarpa showed the Table 4. R. irregularis. These Ziziphus spp. level on shoot of plant-fungus combinations, Z. amphibia phosphorus Significance (P) and levelpotassium obtained (K) from contents two-way after ANOVA four highestbiosis with MD F. values mosseae when inoculated with monthstesting theunder effects greenhouse of AMF conditions.and MD values ranged from 68.81Ziziphus to 78.65%. spp. declined according in sym to- K P showedR. the irregularis lowest MD, R. intraradicesvalues of 30.5%. and Factors tested (%) (%) However,F. mosseae MD values of AMF in the following order: P AMF *** *** (Table 3). There was a significant positiveP correla- Ziziphus spp. ** *** tion between MD and hyphal length (r = 0.902, < 0.0001), AMF × Ziziphus spp. *** *** and MD and mycorrhizal infection (r = 0.908,

, since they showed the

Volume 72 | Issue 3 | May/June 2017 179 et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi Table 6. and nutritional parameters of Ziziphus spp. seedlings. Correlation coefficients between hyphal length, mycorrhizal infection, mycorrhizal dependency, root/shoot ratio K P HL MI MD Root/shoot ratios K 1 P 0.365 NS 1 HL 0.268 NS 0.908* 1 MI 0.145 NS 0.841* 0.938* 1 MD 0.166 NS 0.822* 0.902* 0.908* 1 Root/shoot ratios -0.051 NS -0.256 NS -0.300 NS -0.236 NS -0.236 NS 1 HL: hyphal length; MI: mycorrhizal infection; MD: mycorrhizal dependency; NS: not significant; *P < 0.0001 using Pearson’s correlation coefficients.

Acacia ho- accumulated more P and K with R. intraradices and R. irregu- losericea Acacia mangium Bâ, A.M., Dalpé, Y., and Guissou, T. (1996). Les Glomales d’ highestlaris mycorrhizal colonization with the both AMF, and it A. Cunn. ex G. Don. et d’ Willd.: Diversité more than the absorption of K (Guissou et al et abondance relative des champignons mycorhiziens à arbuscules , respectively. P absorption probably contributed to this kina Faso. Bois For. Trop. 250 dans deux types de sols de la zone Nord et Sud Soudanienne du Bur- who found that there is an evident relationship., between 1998). Ourthe , 5–18. results supported the findings of Koide and Mosse (2004) Bâ, A.M., Plenchette, C., Danthu, P., Duponnois,50 R., and Guissou, T. degree to which a root system of a plant is colonized by AM (2000). Functional compatibility of two arbuscular mycorrhizae with fungi and the potential for the plant to benefit significantly thirteen fruit trees in Senegal. Agrofor. Syst. , 95–105. https://doi. org/10.1023/A:1006482904452. from the symbiosis. P is critical for plantet al growth and makes up about 0.2% of dry weight, but it is one of the most difficult Bâ, A.M., Guissou, T., Duponnois, R., Plenchette, C., Danthu, P., Sacko, Conclusionnutrients for plants to acquire (Smith ., 2011). jubier.O., Sidibé, Fruits D., 56Sylla, K., and Windou, B. (2001). Mycorhization contrô- lée et fertilisation phosphatée: Application à la domestication du ju- , 261–269. https://doi.org/10.1051/fruits:2001128. promoted Ziziphus cation of jujube fruit trees (Zizyphus mauritiana The present study clearly showed that AM inoculation Bâ, A.M., Danthu, P., Duponnois, R., and Soleviev, P. (2003). Domesti- spp. growth by enhancing Ziziphus significantly spp. Lam.). In Crop Man- testedbiomass seem production to be due and to nutrientdifferences uptake, in the particularly development P up of- agement and Postharvest Handling of Horticultural Crops, R. Dris, R. take. The differences of MD among the various Niskanen, and S.M. Jain, eds. (Science Publishers, Inc.), p. 255–279. Rhizophagus irregularis seems to be an Davison, J., Moora, M., Öpik, M., Adholeya, A., Ainsaar, L., Bâ, A.M., hyphal length in the soil andZiziphus in the spp.P uptake tested. by From the external a prac Burla, S., Diédhiou, A.G., Hiiesalu, I., Jairus, T., Johnson, N.C., Kane, A., hyphae. Moreover, Koorem, K., Kochar, M., Ndiaye, C., Pärtel, M., Reier, Ü., Saks, Ü., Singh, efficient fungus for all the - 349R., Vasar, M., and Zobel, M. (2015). Global assessment of arbuscular tical point of view, this AMF constitutesZiziphus a promising tool for mycorrhizal fungus diversity reveals very low endemism. Science the production of higher quality nursery stock with potential , 970–973. https://doi.org/10.1126/science.aab1161. improved field performance of spp. in agroforestry Guissou, T. (2009). Contribution of arbuscular mycorrhizal3 fungi to systems.Acknowledgments growth and nutrient uptake by jujube and tamarind seedlings in a phosphate (P)-deﬁcient soil. Afr. J. Microbiol. Res. (5), 297–304. Parkia biglobosa Tamarindus in- The authors are thankful to Dr. Kadidia Sanon for pro- dicaGuissou, T.,Ziziphus Bâ, A.M., mauritiana Ouadba, J.M., Guinko, S., and Duponnois, R. (1998). Responses of (Jacq.) Benth., viding seed materials. Babacar Thioye received grants from 26 L. and Lam. to arbuscular mycorrhizal fungi the Institut de Recherche pour le Développement (IRD) and in a phosphorus-deficient sandy soil. Biol. Fertil. Soils , 194–198. the Institut Sénégalais de Recherches Agricoles (ISRA). This https://doi.org/10.1007/s003740050367. work was funded under the Africa-Brazil-France tripartite research program entitled “Fight against desertification in Guissou, T., Bâ, A.M., Plenchette, C., Guinko,Balanites S., and aegyptiaca Duponnois, R. Africa”. (2001).Parkia Effets biglobosa des mycorhizes à arbusculesTamarindus sur indica la toléranceZiziphus à un References mauritianastress hydrique chez quatre arbres12 fruitiers (L.) Del., (Jacq.) Benth., L. et Lam. Sécheresse , 121–127. Adelman, M.J., and Morton, J.B. (1986). Infectivity of vesicular-arbus- Guissou, T., Sanon, K.B., Babana, A., and Bâ, A.M. (2016). Effect of 18cular mycorrhizal fungi: Influence of host-soil diluent combinations house propagated fruit trees from diverse geographic provenances. on MPN estimates and percentage colonization. Soil. Biol. Biochem. arbuscular mycorrhizae on 20growth and mineral nutrition of green- , 7–13. https://doi.org/10.1016/0038-0717(86)90106-9.Ziziphus, a medicinal plant genus 22 Biotech. Agro. Soc. Environ. , 417–426. Arndt,man). S.K., and Kayser, O. (2001). with tradition and future potential. Z. fur Phytother. , 91 (in Ger- Hart, M., Ehret, D.L., Krumbein, A., Leung, C., Murch, S.,25 Turi, C., and Franken, P. (2015). Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza , 359–376. Azam-Ali, S., Bonkoungou, E., Bowe, C., deKock, C., Godara, A., and https://doi.org/10.1007/s00572-014-0617-0. Williams, J.T. (2006). Ber and other jujubes. In Ber and Other Jujubes, Jakobsen, I., and Rosendahl, L. (1990). Carbon flow into soil and Southampton).J.T. Williams, R.W. Smith, N. Haq, and Z. Dunsiger, eds. (Southamp- 115 ton, UK: International Centre for Underutilised Crops, University of external hyphae from roots of mycorrhizal cucumber plants. New Phytol. , 77–83. https://doi.org/10.1111/j.1469-8137.1990. tb00924.x.

180 International Journal of Tropical and Subtropical Horticulture et al Ziziphus

Thioye . | Growth response of to inoculation with arbuscular mycorrhizal fungi Rhizo- glomus, a new genus of the Glomeraceae 129 TrifoliumJakobsen, subterraneum I., Abbott, L.K., and Robson, A.D. (1992). External hy- Sieverding, E., da Silva, G.A., Berndt, R., and Oehl, F. (2014). phae of vesicular–arbuscular mycorrhizal120 fungi associated with . Mycotaxon , 373–386. L. 1. Spread of hyphae and phospho- https://doi.org/10.5248/129.373. rus inﬂow into roots. New Phytol. , 371–380. https://doi. org/10.1111/j.1469-8137.1992.tb01077.x. Smith, S.E., and Read, D.J. (2008). Mycorrhizal Symbiosis (London: 84 Academic Press). Klironomos, J.N. (2003). Variation in plant response to native and ex- otic arbuscular mycorrhizal fungi. Ecology , 2292–2301. https:// giaSmith, 104 S.E., and Smith, F.A. (2012). Fresh perspectives on the roles of doi.org/10.1890/02-0413. arbuscular mycorrhizal fungi in plant nutrition and growth. Mycolo- 14 , 1–13. https://doi.org/10.3852/11-229. Koide, R.T., and Mosse, B. (2004). A history of research on arbuscular mycorrhiza. Mycorrhiza , 145–163. https://doi.org/10.1007/ Smith, F.A., Jakobsen, I., and MedicagoSmith, S.E. truncatula (2000). Spatial differences147, s00572-004-0307-4. in acquisition of soil phosphate between two arbuscular mycorrhi- trient uptake and establishment of in vitro raised Ziziphus mauriti- zal fungi in symbiosis with , New Phytol. Mathur,ana N., and Vyas, A. (1999). Improved155 biomass production, nu- 357–366. https://doi.org/10.1046/j.1469-8137.2000.00695.x. mance in stressful environments: interpreting new and established by VA mycorrhiza. J. Plant. Physiol. , 129–132. https://doi. Smith, S.E., Facelli, E., Pope, S., and Smith, F.A. (2009). Plant perfor326-, org/10.1016/S0176-1617(99)80153-9. knowledge of the roles of arbuscular mycorrhizas. Plant Soil inMathur, Ziziphus N., andmauritiana Vyas, A. (2000). Influence of arbuscular mycorrhizae45, 3−20. https://doi.org/10.1007/s11104-009-9981-5. on biomass production, nutrient uptake and physiological changes Lam. under water stress. J. Arid Environ. Smith, S.E., Jakobsen, I., Grønlund, M., and Smith, F.A. (2011). Roles of 191–195. https://doi.org/10.1006/jare.2000.0644. rootsarbuscular have mycorrhizasimportant implications in plant phosphorus for understanding nutrition: and interactions manipu 3 between pathways of phosphorus uptake in arbuscular156 mycorrhizal Newman, E.I. (1966). A method of estimating the total length - of a root in a sample. J. Appl. Ecol. , 139–145. https://doi.org/ lating plant phosphorus acquisition. Plant. Physiol. , 1050–1057. 10.2307/2401670. https://doi.org/10.1104/pp.111.174581.

Ngwa, A.T., Pone, D.K., and Mafeni, J.M. (2000). Feed selection and88, Soule, A. (2011). Plantes Ligneuses de Mauritanie: Caractéristiques dietary preferences of forage by small ruminants grazing natural et Usages (Fondation MON-3). pastures in the Sahelian zone of Cameroon. An. Feed Sci. Tech. 49 253–266. https://doi.org/10.1016/S0377-8401(00)00215-7. Tawaraya, K. (2003). Arbuscular mycorrhizal dependency of dif- cropropagated argan tree (Argania spinosa): I. Growth and biomass ferent plant species and cultivars. Soil Sci. Plant. Nut. , 655–668. Nouaim, R., and Chaussod, R. (1994).27 Mycorrhizal dependency of mi- https://doi.org/10.1080/00380768.2003.10410323. production. Agroforest Syst. , 53–65. https://doi.org/10.1007/ Trouvelot, A., Kough, J.L., and Gianinazzi-Pearson, V. (1986). Mesure BF00704834. du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In Ouédraogo,ca: response S.J., of introducedBayala, J., Dembélé, and local C., cultivars Kaboré, to A., rock Kaya, phosphate B., Niang, and A., Physiology and Genetic Aspects of Mycorrhizae, V. Gianinazzi-Pear- and Somé, A.N. (2006). Establishing jujube trees in sub-Saharan68 Afri- son, and S. Gianinazzi, eds. (Paris: INRA), p. 217–221. water supply in Burkina Faso, West Africa. Agrofor. Syst. , 69–80. Verbruggen, E., Van der Heijden, M.G.A., Rillig, M.C.,197 and Kiers, E.T. https://doi.org/10.1007/s10457-006-6843-5. (2013). Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol. , 1104–1109. Pearson, J.N., and Jakobsen, I. (1993). The relative contribution124 of, https://doi.org/10.1111/j.1469-8137.2012.04348.x. hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants measured by dual labelling with 32P and 33P. New Phytol. Yao, Q., Li, X.L., Feng, G., and32 Christie, P. (2001). Influence of extramat- 489–494. https://doi.org/10.1111/j.1469-8137.1993.tb03840.x. rical hyphae on mycorrhizal dependency of wheat genotypes. Com- mun. Soil. Sci. Plant. Anal. , 3307–3317. https://doi.org/10.1081/ Phillips, J.M., and Hayman, D.S. (1970). Improved procedures for CSS-120001122. Soc.clearing 55 roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. , 158–161. https://doi.org/10.1016/S0007-1536(70)80110- Received: Oct. 19, 2016 3. Accepted: Apr. 6, 2017

Plenchette, C., Fortin, J.A., and Furlan, V. (1983). Growth responses70, of several plant species to mycorrhizae in a soil of moderate P-fertil- ity. I: Mycorrhizal dependency under field conditions. Plant Soil 199–209. https://doi.org/10.1007/BF02374780.

Redecker, D., Schüβler, A., Stockinger, H.,Glomeromycota Stürmer, S., Morton, J., and 23Walker, C. (2013). An evidence-based consensus for the classifica- tion of arbuscular mycorrhizal fungi ( ). Mycorrhiza , 515–531. https://doi.org/10.1007/s00572-013-0486-y. lum, the Glomeromycota 105, Schüßler, A., Schwarzott, D., and Walker, C. (2001). A new fungal phy- : phylogeny and evolution. Mycol. Res. 1413–1421. https://doi.org/10.1017/S0953756201005196.

ZiziphusSidibé, D., mauritiana Sanou, H., andTeklehaimanot, Tamarindus Z., indica Mahamadi, D., and Kone, S. (2012). The use85 of mycorrhizal inoculation in the domestication of in Mali (West Africa). Agrofor. Syst. , 519–528. https://doi.org/10.1007/s10457-012- 9486-8.

Volume 72 | Issue 3 | May/June 2017 181