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Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house

Three slow-growing legume trees used for desert reforestation and urban gardening in the Sonoran Desert of Northwestern Mexico and the Southwestern USA were evaluated whether their growth can be promoted by inoculation with plant growth-promoting
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  SHORT COMMUNICATION Responses of native legume desert treesused for reforestation in the Sonoran Desert to plantgrowth-promoting microorganisms in screen house Yoav Bashan  &  Bernardo Salazar  &  Ma. Esther Puente Received: 18 July 2008 /Revised: 24 February 2009 /Accepted: 2 March 2009 /Published online: 18 March 2009 # Springer-Verlag 2009 Abstract  Three slow-growing legume trees used for desert reforestation and urban gardening in the Sonoran Desert of  Northwestern Mexico and the Southwestern USA wereevaluated whether their growth can be promoted by inocula-tion with plant growth-promoting bacteria (  Azospirillumbrasilense  and  Bacillus pumilus ), unidentified arbuscular mycorrhizal (AM) fungi (mainly  Glomus  sp.), and supple-mentation with common compost under regular screen-house cultivation common to these trees in nurseries.Mesquite amargo (  Prosopis articulata ) and yellow paloverde (  Parkinsonia microphylla ) had different positiveresponses to several of the parameters tested while blue palo verde (  Parkinsonia florida ) did not respond. Survivalof all tree species was over 80% and survival of mesquitewas almost 100% after 10 months of cultivation. Inocu-lation with growth-promoting microorganisms inducedsignificant effects on the leaf gas exchange of these trees,measured as transpiration and diffusive resistance, whenthese trees were cultivated without water restrictions. Keywords  Azospirillum .Desert .Mesquite.Paloverde.  Parkinsonia .Plantgrowth-promotingbacteria.PGPB.PGPR .  Prosopis .Reforestation Introduction Desertification is an increasing phenomenon worldwidereducing arable lands and increasing health risks due todust pollution (Mctainsh 1986; Wang et al. 2004). Refor- estation is one of the common solutions to combat encroaching deserts, and projects can be of very large size(Moore and Russell 1990). Trees destined for reforestationare initially grown in greenhouses or screenhouses and later transplanted to the field. Therefore, effective nurserymanagement and proper growth of the trees there is of outmost importance for reforestation practices.Among numerous practices of reforestation for timber  production, inoculation with plant growth-promoting bacteria (PGPB; Bashan and Holguin 1998), and arbus-cular mycorrhizal (AM) fungi is a prospective niche yet toachieve commercial acceptance (Chanway 1997; Perryet al. 1987). Inoculation with PGPB is a contemporarytrend in organic and nonorganic agriculture (Bashan andde-Bashan 2005a; Lucy et al. 2004) that is starting to get a foothold in commercial agricultural applications (Bashanet al. 2004). Growth promotion of numerous crops byPGPB, including fruit trees is well known, while inocu-lation of wild plants is a very recent development.Reforestation with native trees is common (Hooper et al.2002; Miyakawa 1999). Apart from agro-forestry trees like oak, eucalyptus, and pine evaluated for their response to PGPB (Domenech et al.2004; Enebak  2005; Estes et al. 2004; Lucas García et al. 2004; Sastry et al. 2000; Zaady and Perevolotsky 1995), only a handful of wild plants have been inoculated withPGPB; the vast majority were cactus species of the SonoranDesert (Bacilio et al. 2006; Bashan et al. 1999; Carrillo et al. 2002; Carrillo-Garcia et al. 2000; Puente and Bashan Biol Fertil Soils (2009) 45:655  –  662DOI 10.1007/s00374-009-0368-9Y. Bashan ( * ) :  B. Salazar  : M. E. PuenteEnvironmental Microbiology Group, Northwestern Center for Biological Research (CIBNOR),Mar Bermejo 195, Colonia Playa Palo de Santa Rita,La Paz, B.C.S. 23090, Mexicoe-mail: bashan@cals.arizona.eduY. BashanDepartment of Soil, Water and Environmental Science,The University of Arizona,Tucson, AZ, USA  1993; Puente et al. 2004b) and several other shrubby plant  species (Bashan et al. 2000b; Grandlic et al. 2008; Herrera et al. 1993) as well as saltwater mangroves (Bashan andHolguin 2002; Toledo et al. 1995). The hypothesis of this study was that native desert-legume trees that do not have commercial timber value but are essential for reforestation of eroded lands to prevent soil erosion and dust pollution respond to inoculation withnative plant growth-promoting microorganisms in asimilar manner as agricultural and agro-forestry trees.Thus, this agricultural technology may be applied also tothe propagation of these trees usually done in screen-houses (Bean et al. 2004). Mesquite amargo and yellowand blue palo verde trees are common native trees of theSonoran desert in the Southwestern USA and NorthwesternMexico. They have extensive deep root systems that enablethem to survive in extremely arid habitats (Shreve 1951),and they are consequently wide spread throughout thedesert (Roberts 1989). Palo verde species have bark  biomass capable of photosynthesis (Adams and Strain1969), hence, their common name (green tree in Spanish).Wild mesquite wood is intensively harvested, legally andillegally, for charcoal and timber industries. The two wild palo verde species are not harvested but are used in urbansettings as ornamental plants that are propagated innurseries. Because of their outstanding topsoil-holdingcapacity, these trees prevent soil erosion in their areas of growth. The three tree species are slow growers under native growth conditions.We attempted to show that the growth of these trees can be enhanced by the use of treatments that previously proved to improve the growth of few desert plants, such ascacti, like inoculation with PGPB (Bashan et al. 1999;Carrillo-Garcia et al. 2000; Carrillo et al. 2002; Puente et al. 2004b), desert AM fungi (Bashan et al. 2000a; Bethlenfalvay et al. 1984; Cui and Nobel 1992; Carrillo- Garcia et al. 1999; Requena et al. 2001;), and the use of  small levels of common compost (Bacilio et al. 2006).This has been done to demonstrate the feasibility of enhanced propagation of these plants under screenhouseconditions that are typical to commercial propagation of these trees for future reforestation of eroded desert lands.We have used two types of native microorganisms asinoculants, AM fungi propagated from resource island soilof the Southern Sonoran Desert (Bashan et al. 2000a;Carrillo-Garcia et al. Carrillo-Garcia et al. 1999) and  Bacillus pumilus , srcinally isolated from cardon roots of this area (Puente et al. 2004a). This bacterium increasedcardon growth in ground rock (Puente et al. 2004b) andalso the growth of the freshwater microalgae  Chlorella  sp.(Hernandez et al. 2009). The nonnative diazotrophic bacterium used was the nonspecific PGPB  Azospirilumbrasilense  Cd (Bashan et al. 2004). Materials and methods OrganismsLegume tree species used were: mesquite amargo (  Prosopisarticulata  (S. Watson)), yellow palo verde or foothill paloverde (  Parkinsonia microphylla  (Torr.)), and blue paloverde or palo junco (  Parkinsonia florida  (Benth. exA. Gray) S. Wats). Microorganisms used were the PGPB  Azospirillum brasilense  Cd (Bashan et al. 2004) and  B. pumilus  strain RIZO1 (EF123224, GenBank of NationalCenter for Biotechnology Information, Bethesda, MDUSA) (Puente et al. 2004a). The AM fungi used were a propagated mixture of   Glomus  sp. and unidentified nativespecies found in resource islands under mesquite trees inthe Southern Sonoran desert (Bashan et al. 2000a; Carrillo-Garcia et al. 1999).Microbial cultivation  A. brasilense  Cd and  B. pumilus  RIZO1 were cultivated ona trypton-yeast extract glucose medium supplemented withmicroelements (TYG) for 24 h at 30°C and 120 rpm(Bashan et al. 2002). The two bacterial species wereformulated into a dry microbead inoculant preparationmade of alginate (Bashan et al. 2002) using specializedequipment (,accessed 15 February 2009).Production of AM inoculumAM fungal inoculum used sorghum plants ( Sorghumbicolor   (L.) Moench) as a trap plant for propagation. Plantswere cultivated in 10-l commercial plastic pots containing poor desert soil (Bashan et al. 2000a; Carrillo-Garcia et al.1999). Resource island soil of high AM-fungal infectivity(Carrillo-Garcia et al. 1999) was the inoculum source.Plants were cultivated in a screenhouse at ambient conditions of the Sonoran desert at light intensitiesapproximately one half of full sunlight (1,000  μ  mole photon m − 2 s − 1 ) for 6 months and irrigated with tap water when necessary to prevent desiccation. They were fertilizedonce with 1.5% NPK commercial garden fertilizer but withlow P content (0.1%) to enhance AM fungal growth(R. Linderman, personal communication). The plants weresenescent at harvest. At harvest, analysis of the roots for thenumber of spores and AM fungal infection, presence, andfrequency was done by the method of measurement of length in random arrangements of lines (Marsh 1971) and by root staining (Vierheilig et al. 1998). Upon excising thestems, the rooted soil clumps were air-dried for 2 weeks before being crumbed for spore counts. Spore numberswere determined by wet-sieving (45-, 75-, 100-, and 656 Biol Fertil Soils (2009) 45:655  –  662  200- μ  m sieve openings), decanting, and sucrose-gradient centrifugation (Brundrett et al. 1994) of the soil samples.Colonization of root fragments used in the inoculum was54.5%.Compost The common dairy-wheat compost used was produced for cultivation of cardon cactus and its composition wasdescribed earlier (Bacilio et al. 2006). It was applied at the rate of 1:8 (compost/soil,  v  /  v  ).Preparation of inoculantsBacterial inoculant made of alginate microbead wasattached to the seeds of wild trees as described for wheat  plants (Bashan et al. 2002) in the screenhouse experiment at a level of 1.2×10 6 cfu g − 1 soil of   B. pumilus  and 1×10 6 cfug − 1 soil of   A. brasilense . AM inoculant was prepared asfollows: after propagation of AM fungi in sorghum roots,roots were separated from the soil. The soil was saved, andthe roots were cut into small pieces (<0.5 cm). Then theroot pieces were mixed again with the same soil. A mixtureof soil and root (213 g) was used to inoculate each pot of the legume trees. The inoculant was placed around the root system of the plants, and the rest of the pot volumes werefilled with field soil.Collection of seedsSeeds of mesquite amargo, yellow palo verde, and blue paloverde were collected from ten native trees (200 g plant  -1 )located in fields surrounding the settlements of ElCentenario and El Comitan, 15 km from La Paz, BajaCalifornia Sur, Mexico (24°07 ′ 36 ″  N, 110°25 ′ 48 ″  W) inJuly 2003 and kept in hermetically sealed boxes at ambient temperature until use (Puente and Bashan 1993).Screenhouse cultivationLegume trees were grown in black plastic commercial tubeswith drainage for growing plants (50×10 cm in diameter)each containing 2.5 kg soil. Dead mineral soil was collectedfrom desert sites bare of vegetation to minimize itsmicrobial content. It was not autoclaved to avoid possibledeleterious effects, such as Mn toxicity. The soil was usedsieved to 1 mm (Tyler equivalent 16 mesh No.18 USAstandard testing sieve). Seeds were washed with 2% Tween20 (Polyoxyethylene-sorbitan-monolaurate; Sigma, St.Louis MO, USA) under constant agitation for 5 min,thoroughly washed with tap water, disinfected in 1% (thetwo palo verde species) and 3% (mesquite) commercial NaOCl under constant agitation for 5 min, thoroughlyrewashed with sterile tap water, and soaked in water in asteel strainer at 55°C for 2 min (mesquite) and boilingwater for 1 min for the two species of palo verde (Scott 2006). Seeds were germinated on large Petri dishes withmoist, sterile filter-paper towels about 1 cm apart andincubated in the dark at 33°C in a growth chamber (Conviron, Model 125L, Manitoba, Canada). Defectiveseedlings were discarded. Healthy seedlings were trans-ferred to large test tubes (12.5 cm long, 1.5 cm in diameter)containing 10 ml of sterile distilled water for 14 days untilthey were about 10 cm tall. Seedlings of similar size were planted in pots. All other seedlings were discarded.Each pot contained initially five seedlings. After 1 month, the pots were thinned to one plant per pot intending to obtain similar sized seedlings in naturallyvariable native plants. A total of 50 pots per plant specieswere used (ten per treatment in a completely randomizedlayout). All plants were grown in a screenhouse on elevatedmetal net beds at the ambient temperature (15  –  35°C, night/ day) irrigated with tap water twice a week (small plants)and later three times a week. No water stress was imposedon these plants to avoid wilting throughout the experiment and a single fertilization (commercial 0.5% NPK 18:4:18)was given after 10 days. Each experiment (using one treespecies) was conducted separately. The three experimentswere maintained for 10 months each. Chemicals used for foliar pest control were nonsystemic to avoid influencingthe treatments by translocation to the roots. Their use wasnecessary in these long-term experiments to control thesweet potato whitefly  Bemisia tabaci  (Gennadius), and ants(Hormiga Arriera;  Atta mexicana  Smith). This was doneafter 3 months of cultivation using a concentration of 1 mll − 1 of each of the following insecticides:  “  Naturales-L ” (Troy Biosciences, USA) then with a mixture of Previcur N(Bayer CropScience, Chile) and Derosal (Bayer, Mexico).Second and third applications were given at 10 and 25 dayslater, respectively. Fumigation was done directly to theleaves avoiding contact with the soil after covering the soilsurface with black plastic film. Cover was removed onlyafter insecticides dried out. Fumigations were of lowvolume and were restricted to the foliage.Measurement of plant parametersThe plant parameters measured were plant height, trunk diameter (0.5 to 1 cm above soil level; Bowers and Turner 2001), number of developing branches, and survival after 150 days and additional measurement after 300 days. At theend of the experiments after 10 months, dry weight (40°C,72 h) of foliage was determined (Bashan and de-Bashan2005b). After 270 days of cultivation, the following gas-exchange parameters were measured using a portablePorometer LI-1600 (LI-Cor, Lincoln, Nebraska, USA): Biol Fertil Soils (2009) 45:655  –  662 657  diffusive resistance (seconds per centimeter), and transpi-ration (microgram per square centimeter per second). Thesemeasurements were done only on mesquite amargo andyellow palo verde because the leaf structure of blue paloverde (needles) was incompatible with the equipment used.Experimental design and statistical analysisScreenhouse experiments were conducted in a completelyrandomized design, one tree per pot and a total of ten trees per treatment and 50 trees per experiment. The treatmentswere: inoculation with AM fungi, inoculation with PGPB,soil supplement with compost, all the three treatmentscombined, and nontreated control trees. A wooden con-struction ensured equal distance between the pots to provide similar competition for space and light when thetrees grew larger.All experiments were analyzed statistically and wererepeated. After normalization of the data, results of allexperiments were analyzed by one-way ANOVA and then by Tukey ’ s HSD post hoc analysis at the significance levelof   P  ≤ 0.05. Data in percentage were converted to arcsin before analysis. All statistics use Statistica software(Statsoft  ™ , Tulsa, OK, USA). Results Effect of inoculation with PGPB and AM fungi on plant form and functionThe height of trees was not promoted in the three treespecies apart from a small but significant (  P  ≤ 0.05) increasein mesquite amargo treated with AM fungi. Addition of compost reduced plant height in all species (Fig. 1a).Mesquite amargo responded positively to all treatments byincreasing the number of branches per tree. Yellow paloverde responded positively only to addition of compost or the combined treatment, while blue palo verde did not respond positively to any treatment (Fig. 1 b). Only thecompost treatment affected stem thickness of the two paloverde species as did the combined treatment for yellow paloverde (Fig. 1c). Survival of all mesquite amargo trees,untreated control trees included, was almost 100%. Similar survival occurred with control trees of blue palo verde or those treated with AM fungi. Untreated yellow palo verdesurvived less well (about 80%); therefore, application of compost, AM fungi, and all the treatments combinedsignificantly enhanced survival (Fig. 1d). When all thetrees were harvested, only the dry weights of mesquiteamargo (in all treatments) and yellow palo verde (incombined treatment) were significantly increased(Fig. 1e). Several of the treatments had small negative but significant (  P  ≤ 0.05) effects on plant growth and none of the treatments, except those of AM fungi on trunk thickness, had a positive effect of blue palo verde trees.When another identical evaluation of these parameters wasdone after 300 days of growth, no difference in survival andthe number of branches was detected with only minimalincrease in plant height (data not shown).Effect of inoculation with PGPB and AM fungi on leaf gasexchange of mesquite amargo and yellow palo verde treesTreatments with PGPB, AM fungi, and compost-affectedleaf gas exchange in these two tree species. In yellow paloverde, inoculation with AM fungi reduced transpiration andincreased diffusive resistance over untreated control trees(Fig. 2). PGPB and compost amendment had the oppositeeffect; they reduced diffusive resistance and increasedtranspiration (Fig. 2). The combined treatment had noeffect on gas exchange.A different pattern was observed in mesquite amargowhere compost increased diffusive resistance and had noeffect on transpiration. This effect was opposite to that inyellow palo verde. AM fungi increased transpiration andreduced diffusive resistance (also opposite to what wasobserved in yellow palo verde). Inoculation with PGPB hadno effect, and combined inoculation created similar effectsas inoculation with AM fungi (Fig. 3). It was noted that transpiration rates in yellow palo verde were much higher than those in mesquite amargo. Discussion Reforestation of severely degraded areas of the SonoranDesert with shrubs, trees, and cacti is always difficult and,in many cases, unsuccessful (Bashan et al. 1999; Bean et al.2004). This happens because the nurse tree systemgoverning natural revegetation in deserts is often destroyed;the topsoil together with its beneficial microorganisms iseroded by wind and water; organic matter is scarce; andwater, by default, is usually in short supply. Therefore, anyattempt to restore a desert with trees and long-lived cactishould also consider to restore the beneficial microfloraassociated with these plants and to provide some source of organic matter (Bacilio et al. 2006; Grandlic et al. 2008). Although all trees share the same habitat, they respondeddifferently to the various treatments. Because height wasnot a good parameter for evaluation for any of the species,an increase in stem diameter is an indication of the goodhealth of these trees (Bowers and Turner  2001) as wasdemonstrated for some treatments of mesquite amargo andyellow palo verde. On the other hand, the other two speciesshowed growth-promotion effects such as an increase in the 658 Biol Fertil Soils (2009) 45:655  –  662  number of branches and dry weight in response to different treatments, while survival was relatively high (>80%) for all trees. Mesquite amargo was the most robust plant tested;almost all plant survived the growing season. It alsoresponded better to inoculation and compost treatments.Therefore, it should be considered as a candidate for reforestation trials in the field even if it is considered a pest in rangeland by cattle ranchers in the southern USA but not in Mexico. Because both species of palo verde havehigh ornamental value and public acceptance, albeit onespecies responded less than mesquite and the other did not respond at all, they nevertheless merit further long-termevaluation upon transplanting to the field. This studydemonstrated that native desert trees respond to inoculationwith growth promoting microorganisms in a manner resembling agricultural crops and cacti (Bashan and    T   h   i  c   k  n  e  s  s  o   f  s   t  e  m   (  m  m   ) 253035404550 AABABAABBBCBAABBAA c    N  u  m   b  e  r  o   f   b  r  a  n  c   h  e  s  p  e  r   t  r  e  e 05101520253035    H  e   i  g   h   t   (  c  m   ) 406080100120140 BABCBBABBBDCAAB a BBBDBABABCBABABBA b Non - treated controlCompostAM fungiPGPBCombined treatments    S  u  r  v   i  v  a   l   (   %   ) 60708090100 BBBABBACCCBBAA d Tree species MesquiteYellow palo verdeBlue palo verde    D   W    (  g   ) 0246810121416 ACBABBBABCCBCCAB e B Fig. 1  Effect of inoculation withPGPB and AM fungi and sup- plementation of compost ongrowth parameters of three nativelegume trees in a screenhouse.Each group of   columns sepa-rately denoted by different letters differ significantly at   P  ≤ 0.05using one-way ANOVA.  Bars represent standard errors.  a Height.  b  Number of branches per tree.  c  Thickness of stem. d  Survival.  e  Dry weight Biol Fertil Soils (2009) 45:655  –  662 659
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