quenching (qP) (by 27% and 24%, respectively) and CO and respectively) 24%, and 27% (by (qP) quenching and K46strainsexhibitedanincreaseofbothphotochemical M9 with Inoculated 0.739). Control: and 0.744 (K46: treatments other to respect with increased (0.784) strain M9 photosystem II(PSII)( that the maximum photochemical quantum yield of showed 0.05) ANOVAThe ≤ evaluated. (P were exchange B. amyloliquefaciens and seeds wereinoculatedwith Jacq.) plantsinoculatedwith the physiologicalparametersofpepper( been poorlystudied. The aimofthisstudywastoevaluate However, theirimpact on photosynthetic metabolismhas used asastudymodelforunderstandingmanyprocesses. Bacillus ABSTRACT CO Key words: sustainable agricultureprograms. straincouldevenbeusedinpromoted bythebacteria.M9 to increased ETRin the thylakoid membranes, which was Promotion of photosyntheticcapacityinpepper was due fluorescence and gas exchange parameters. of thephotosyntheticmechanisminpepperplantstoincrease performance the influenced positively strain M9 with plants characteristics. Ourresults therefore showthat inoculating with theM9strainshowedenhancementsonallgrowth in inoculated plants. However, only plants inoculated PSII (ETR) and PSII operating efficiency ( respect to controls. Likewise, both electron transport rate of with respectively) 57%, and (61% transpiration decreased Furthermore, plantsinoculatedwithM9andK46showed respectively), whencompared with non-inoculated plants. 16%, and 20% (by () rate assimilation doi:10.4067/S0718-58392016000400003 Accepted: 10November2016. Received: 12May2016. Baja León, Nuevo Ejido 21705, California, México. s/n Delta a Carretera Agrícolas, Yucatán, Conkal, 97345, 2 s/n Tecnológico México. Av. Investigación, e 1 photosynthesis inpepper plants photosystem IIefficiencyandenhances Blancka YeseniaSamaniego-Gámez Bacillus Jorge Kantun-Can nvria Atnm d Bj Clfri, nttt d Ciencias de Instituto California, Baja de Autónoma Universidad Posgrado de Estudios de División Conkal, de Tecnológico Instituto 2 CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY assimilationrate,plantgrowthpromotingrhizobacteria. Bacillus * Corresponding author([email protected]). isoneofthemainrhizobacteriatohavebeen

Capsicum chinense Capsicum spp. (M9strain; amixtureof spp.inoculationimproves ), chlorophyllfluorescenceandgas 1 F , Arturo Reyes-Ramírez v / F CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4)OCTOBER m ) inplantsinoculatedwiththe Bacillus cereus Bacillus , chlorophyllfluorescence, spp. strains.Pepper Capsicum chinense Φ B. subtilis PSII (K46strain) 1 , René Garruña ) increased 1 , andLourdes Cervantes-Díaz and 2 - -

MARCH 2016 DECEMBER 2016 1* , JoséM.Tun-Suárez quantum yield ofphotosystem II(PSII)( drought, salt,UV, andacombinationofhighCO of plantstoattenuatesomedegreethestressfuleffects of Stefan etal.,2013a;Palacios2014). 2010; al., et (Shi unclear remains metabolism photosynthetic theirimpacton known, byrhizobacteriaarewell used mechanisms the Although 2014). Kibret, and (Ahemad effects systemic resistance;andmodulationofenvironmentalstress competition betweenpathogens and non-pathogens; induced production; siderophore lipases; and proteases 1,3-glucanases, include antibiotics;lyticenzymes,suchaschitinases,cellulases, mechanisms that do not involve metabolism. Examples promotes rhizobacteria of presence the Indirectly, 2014). al., et gibberellin, indoleaceticacidandethyleneproduction(Lucas phosphate solubilization,Fesequestration,andcytokinin, fixation, N include Examples metabolism. plant to modifications cause can rhizobacteria of presence the Directly, 2015). al., et (García-Cristobal mechanisms different by fitness plant plant growthpromotion/protectionactivities,whichcanimprove other microbiota, at least for the time needed to express their the rootsurface,surviving,multiplyingandcompetingwith colonizing at proficient are Rhizobacteria 2014). al., et Lucas 2014; Kibret, and (Ahemad roots with association in and surfaces group ofbacteria that can befoundintherhizosphere,onroot Plant growth promoting rhizobacteria (PGPR) are a diverse INTRODUCTION adapted to different conditions and numerous properties of because ithasbeenfoundto possessawidegeneticdiversity been used asa study model forunderstanding many processes, 2015). al., et electron transportrate(ETR) (Lucas etal.,2014;García-Cristobal plants are minimum fluorescence (F fluorescence minimum are plants the ability of the strains to affect the photosynthetic apparatus in main parameters used to sensitively and objectively determine producedbythebacteria. were which acetic acid,IAA) The (indole-3- phytohormones by promoted were increases these beet, leadingtoaconsequentincreasedcarbohydratesynthesis, photosynthetic capacity andtotalchlorophyll contentof sugar the increased species endophytic that showed (2010) al. et Shi Thus, 2014). al., et (Armada photosynthesis in increase an levels indroughtstressedplantsandwerealsocorrelated with that bacterialcapacitytoreducereactiveoxygenspecies(ROS) shown 2015). have al., Actually,studies et some García-Cristobal 2013b; al., et Stefan 2013; al., et (Burlak pressure atmospheric efficiency ( Some studies have reported that PGPR affect the physiology Φ - Bacillus PSII DECEMBER 2016 ), non-photochemical quenching (NPQ), and 2 is one ofthe main rhizobacteria that has 1 , 0 ), maximumphotochemical F v / F m 2 ), PSIIoperating content and low contentandlow

409 RESEARCHRESEARCH Bacillus CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY with physiological parametersof rhizobacteria, the aimofthisstudywasto evaluatethe mechanisms during interactions between plants and order to contribute to the understanding ofphotosynthetic increase inresponsetoplant-rhizobacteriasymbiosis?In inoculation with are the physiological responses of What here: addressed are questions specific two Therefore, spp. onthephotosyntheticmechanismsof 2015), there are noprevious studies onthe effect of Bacillus al., 2014; Valle-Gough et al.,2015). et (Garruña-Hernández stress plant of studies in used been Jacq.) grows in wide temperature range, and has therefore ( pepper Habanero particular, In 2014). adaptation to different agro-climatic regions (Kraft et al., pepper plants are grown around the world because of their economically important genus ofthe Solanaceae family and et al.,2009). acidification thatdirectlymobilizessolubleminerals(Zhang in ironuptakeandtransportaswellinducerhizosphere shown to increase the abundance of transcripts involved levels atthislocation.Inway, accumulation andmaybelinkedwithgreaterchlorophyll by an increase in the photosynthetic rate and biomass that ironaccumulationincassavawasaccompanied showed (2015) al. et Freitas However, 2008). al., et (Zhang with aregulatory role forplantsymbiontsinphotosynthesis signaling, acid(ABA) sugar/abscisic plant endogenous photosynthesis in Arabidopsis throughthemodulationof mL (Niazi et al., 2014). Inoculation with Inoculation 2014). al., et (Niazi interest appliedinindustry, microbiologyandagriculture chamber. The cell concentration was adjusted to 10 to adjusted was concentration cell The chamber. dissolved in2mL salineforcountinginaNeubauer and 0.8% saline sterile with twice washed were which cells, the obtain to °C 29 SOLBAT)at (C-600 centrifuge a in min 15 for rpm 3500 at centrifuged were cultures theSubsequently, °C. 30 at h 96 for rpm 200 at stirring constant under broth nutrient of mL 75 in grown were Strains Yucatán,Mexico. of state the in soils from isolated Bacillus cereus MATERIALS ANDMETHODS with 200 cavities filled with sterile peat moss substrate moss peat sterile with filled cavities 200 with distilled water. Sterile seeds weresowningermination trays sodium hypochlorite2%and washed threetimeswithsterile chinense placed inacentrifugefor1h at 160rpm. a mixture of Although studies have been performed on the effect of ( peppers Furthermore, The H241 genotype of Habanero pepper ( pepper Habanero of genotype H241 The -1 Bacillus in 10 mL saline 8%. Twenty seeds per tube were tube per seeds Twenty8%. saline mL 10 in in Jacq.)wasused,andseeds were disinfectedwith spp.strains andplantmaterial C. chinense spp.strains. B. subtilis (K46strain)and Bacillus (Kanchana et al., 2014; Gan et al., et Gan 2014; al., et (Kanchana and spp. strains? Does photosynthesis Does strains? spp. C. chinense B. amyloliquefaciens Capsicum Bacillus C. chinense B. subtilis B. subtilis Capsicum chinense plantsinoculated spp. (M9strain; spp.) arean spp.) Capsicum Capsicum hasbeen plants to increase - - Bacillus MARCH 2016 DECEMBER 2016 ) were 8 cells spp.

fluorescence (defined as photochemical quenching (qPphotochemical = ( = ( photons m µmol 1200 radiation active photosynthetic °C, 28 were fluorescence measurement. The greenhouse conditions were performedinthesameleavesusedchlorophyll state. To determine the dark-adapted the in yield fluorescence Chl maximum the sameleavesusedpreviously. in Japan) Osaka, (Minolta, meter chlorophyll portable 502 (8000 µmol photons m photons µmol (8000 calculated accordingtoKalajietal.(2014). México) weekly at a dose of 1 g L g 1 of dose a at weekly México) Constituyentes, Biochem, (UltraFol, fertilized leaf and day second every watered were They °C. 2 ± 20 at room the experimental design. All trays were placed in a growth to according water distilled with capacity field to moistened after darkadaptation,where quantum yieldofPSII when reactioncentersare open parameter The apex. shoot the from leaf third the on h), (05:00 dawn pre- at sowing after d 145 performed were Measurements (PAM Germany). Effeltrich, fluorometer Walz, modulation measured were parameters fluorescence (Chl) chlorophyll The analyses Chlorophyll fluorescence andgasexchange irradiance (PAR) from 0 to 1500 µmol photons m photons µmol 1500 (PAR)to irradiance 0 from a series of nine saturation pulses under increasing actinic fluorescence yield in the dark-adapted state, and fluorescence intensityinthelight-adaptedstate( intensity inthelight-adaptedstate( electron transport rate (ETR = seed sowing(DASS)andplacedinagreenhouse. after d 60 selected randomly were seedlings Ninety above. were watered and fertilized every seconddayasmentioned and °C 2 ± 20 at room growth a in kept were seedlings The substrate. moss peat sterile with filled cups Styrofoam mL 500 to transferred were seedlings germination, d 18 in the light-adapted state ( intensity fluorescence maximum the determine to intervals photons m µmol 420 of light actinic an After,pulse. saturating s 0.6 weak measuring beam. The absorptivity coefficient) and PSIIoperating efficiency ( A as calculated was (WUE) efficiency use WaterUSA). Nebraska, Lincoln, LI-6400, LICOR, (IRGA; analyzer and transpiration(E)weremeasuredusinganinfraredgas ( PSII of activity potential The 2002). al., et (Calatayud non-photochemical quenching (NPQ = non-photochemical quenching(NPQ F N v Total chlorophyll concentration was measured by SPAD-by measured was Totalconcentration chlorophyll CO F /E (Garruña-Hernández et al., 2014). Measurements 2014). al., et (Garruña-Hernández /E / F m 0 ʹ – 2 ) was obtained according to Li et al. (2007). Both (2007). al. et Li to according obtained was ) assimilationrate(A F -2 s F ʹ -2 )/ s in vivo v s F / -1 F m -1 , and65%RH. m ʹ wasswitchedonandsaturatingpulses ) wereobtainedthroughtheapplicationof represents the maximum photochemical with a portable pulse amplitude -2 F s 0 F on excitation of leaf with a N F m -1 F ), stomatalconductance(g - m ) were applied at 10 min 10 at applied were ) m ʹ ), minimum fluorescence F was determinated with a Φ F v F 0 PSII ismaximumvariable ), m -1 ʹ distilled water. After – F × PAR × 0.5 × leaf × 0.5 PAR× × F 0 0 ʹ F is minimum Chl minimum is ) andsteadystate F s )/( m / F F m m ʹ ʹ – – 1) were 1) – -2 s F 0 -1 ʹ F ) and . The Φ m F PSII is is s s ) )

410 Control K46 M9 (control). (M9 andK46)notinoculated inoculated withBacillusspp. Table 1.Growth parametersofHabanero pepper plants differences accordingto Tukey test(α=0.05). significant represent columns the in letters Different SE. ± means are Data CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY treatments at above 420 µmol photons m photons µmol 420 above at treatments ANOVA showedsignificantdifferences between in leaves ofplantsinoculated with M9 and K46 strains. control plantsby22%,34%and58%,respectively(Table 1). *Significant between treatmentsat0.05probabilitylevel. NS: nonsignificant,PSII:photosystem II. Data aremeans±SE. inoculated with but stemdiameter, freshweightandrootvolumeofplants All treatmentsweresignificantlysimilarforplantheight, fluorescence parameters Growth parameters andchlorophyll RESULTS ≤ 0.05(StatisticaSix,StatSoft, Tulsa, Oklahoma,USA). ANOVA andmeanswerecomparedusing Tukey’s testatP random design. The results were analyzed with one-way Thirty plants per treatment were used in a completely Experimental design 1150 µmol photons m photons µmol 1150 maximum photochemicalquantumyieldofPSII( The 2). (Figure density flux photon photosynthetic highest in inoculatedplantsthancontrolfromlowestto (Figure 1). PSII operating efficiency ( efficiency operating PSII 1). (Figure 26.8) control: and 40.8 K46: 45.4; (M9: ETR maximum Treatment (control). inoculated with plants pepper Habanero in density flux photon photosynthetic Figure 1. Responsecurves of electron transportrate (ETR) to The electrontransportrate(ETR)ofPSIIincreased Plant height 176 ±7.2 165 ±3.0 180 ±2.3 cm mm Bacillus Bacillus Stem diameter spp. (M9 andK46)notinoculated spp. 21 ±2.1b 20 ±1.1ab 27 ±1.7a -2 sp.M9increasedwithrespectto s -1 all treatments reached the Fresh weight 1093 ±106b 1051 ±64b 1657 ±133a g Φ PSII ) was higher Root volume -2 216 ±60b 483 ±92ab 516 ±96a - - s MARCH 2016 DECEMBER 2016 mL F -1 v . At / F m ) (0.88) (Figure3D). (1.18) increasedtheNPQ26%withrespecttocontrolplants 3C). (Figure respectively) 24%, and (27% plants control to respect qPwith in increase an showed strains K46 and M9 with inoculated Plants 3B). were 20%higher than fornon-inoculated plants (2.9)(Figure (control). inoculated with plants pepper Habanero in density flux photon photosynthetic to Figure 2. Photosystem II (PSII) operating efficiency ( efficiency operating (PSII) II Photosystem 2. Figure our results,inoculating plantswith to According 2007). (Marschner, minerals other and insoluble compoundssuchas calcium di- andtri-phosphates soil- of solubilization and 2014) Kibret, and (Ahemad 2015), regulationofthesynthesis ofplantgrowth-regulators al., et (Ashok fixation N biological via growth plant favor Plant growthpromoting rhizobacteria are knownto (PGPR) DISCUSSION CO the increased K46 and M9 with Inoculation Gas exchange analyses activity of PSII(F potential the hand, other the On 3A). (Figure (0.739) plants control and (0.744) K46 with inoculated plants to respect increasedwith(0.784) strain M9 with inoculated plants of control plants(Figure5). but plants inoculated withthe K46 had lower values than (7%), plants non-inoculated to respect with SPAD values On other hand, plants inoculated with the M9 increased 4D). (Figure respectively 66% and 68% by WUE improved strains two the However, 4C). (Figure respectively) 57% and (61% transpiration and 4B) (Figure respectively) 45% and (56% conductance stomatal both in decreases showed plants (Figure4A).Plantsinoculated with M9andK46also non-inoculated to respectively,compared 16%, and 20% by assimilation rate(photosynthesis)inHabaneropepperplants at 0.05probabilitylevel. treatments between *Significant nonsignificant. NS: SE. ± means are Data F v / F m . Values for plants inoculated with M9 strain (3.6) strain M9 with inoculated plants Valuesfor . Bacillus v /F 0 ) showed a significantly similar trend similar significantly a showed ) spp. (M9 andK46)notinoculated spp.

Likewise, plantswithM9strain Bacillus spp.strains Φ PSII ) to 2

411 CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY spp. (M9andK46)notinoculated(control). (qP) quenching photochemical (Q transport rateofPSIIsuggeststhatthequinoneacceptor electron the in increase an (1999), Melis to According ETR valuesisaconsequence ofthepositive effect ofPGPR. subjected tostressfulconditions. Therefore, theincreasein by stress. However, theplants in this studywerenot inhibited is PSII of ETR the (2007), al. et Li to According inoculatedwith in leavesofplants control plants(notinoculated). modified thephysiologicalmechanismswithrespectto 3. A) Figure ( photosynthesis ratesandplantgrowth. Inoculating plants therefore has the potential to increase in electrontransport,therebyavoidingphotodamage. as modulators, sensingprimaryandsecondary metabolism, known topossessvolatile organic compoundsthatfunction symbionts inplantenergy acquisition.Some (ABA) signalingandestablish aregulatoryroleforsoil through the modulation of endogenous sugar/abscisic acid elevate photosynthesis in that certainPGPR photosynthetic capacity Bacillus inoculatedwith and Johnson,2000).Habaneropepperplants associated withPSIIthatisusedinphotochemistry(Maxwell measures the proportion of light absorbed by chlorophyll Φ a The electrontransportrate(ETR)ofPSIIincreased Additionally, it is observed that PSII operating efficiency operating PSII that Additionally,observed is it PSII ) is highly oxidized and its excitation energy is utilized ) increased in inoculated plants. This parameter spp.strainsthereforeshowedanincreaseinoverall

Maximum photochemical quantum yield of photosystem II (PSII) ( (PSII) II photosystem of yield quantum photochemical Maximum Data aremeans±SE.Different lettersrepresentsignificantdifferences betweentreatmentsaccordingto Tukey test(α=0.05). Actinic lightintensity:420µmolm in vivo

and D) non-photochemical quenching (NPQ) in Habanero pepper plants inoculated with inoculated plants pepper Habanero in (NPQ) quenching non-photochemical D) and . Zhang et al. (2007) showed (2007) al. et Zhang . Bacillus -2 s -1 . spp. strains. spp. Arabidopsis Bacillus - - MARCH 2016 DECEMBER 2016 are

to Baker (2008), Baker to light absorbedbyPSIIisusedforreductionofQ performance. An is usedasasensitiveindicatorofplantphotosynthetic when usingPGPR. a decrease of 21.7% in F in 21.7% of decrease a Weis, 1991). chemical energy inthePSIIreactioncenter(Krauseand of excitonscapturedbyopen trapsandbeingconvertedto qP with respect to control plants; qP denotes the proportion situations. with PGPRcouldprepare the plant for future abiotic stress and drought.Ourresultsthereforeshowedthatinoculation also elicit so-called ‘induced systemic tolerance’ to salt Medicago sativa of PSII ( et al.,2007). stress responses and hormone regulation in plants (Zhang results (Gururani et al., 2012), with increased with 2012), al., et (Gururani results PSII ininoculated plants, andotherauthorsobtained similar healthy a promoted strain M9 the that suggests This 2000). measurement for mostplantspecies(MaxwellandJohnson, showed asimilartrendto On other hand, the potential activity of PSII (F Plants inoculated with Moreover, the maximum photochemical quantum yield F v / F F m v ) increased in inoculated plants. According / F . Yang et al. (2008) mentioned that PGPR that mentioned (2008) al. Yanget . F F m v ) v / , B)potentialactivityofPSII( / F F m m is the maximum efficiency at which at efficiency maximum the is value of around 0.83 is an optimal an is 0.83 around of value

M9 and K46 had an increase in v /F F v 0 / after 48 h water stress in stress water h 48 after F m . Li et al. (2007) found (2007) al. et Li . F v / F F m v Bacillus / values F A , and 0 v ), C) /F 0 )

412 CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY Habanero pepper plantsinoculatedwith production ofO minimize to help NPQ and qP Both 2001). al., et (Müller and harmlesslydissipateexcess excitationenergy asheat (Chl) singlet-excited quench that mechanisms already been absorbed,because ofthe non-photochemical better wayofgettingrid excesslightenergy thathad study thereforeshowedthatinoculatedplantshad a between treatmentsaccordingto Tukey test(α=0.05). differences significant represent letters Different SE. ± means are Data with Figure 5.SPAD values ofHabanero pepper plants inoculated Figure 4. A) CO Likewise, NPQwashigherinplantsinoculated. This Bacillus Data aremeans±SE.Different lettersrepresentsignificantdifferences betweentreatmentsaccordingto Tukey test(α=0.05). spp. (M9andK46)notinoculated(control). 2 2 Assimilation rate(A inthePSIIantenna (Mülleretal.,2001). N ), B)stomatalconductance(g Bacillus spp. (M9andK46)notinoculated(control). - - MARCH 2016 DECEMBER 2016 photosynthetic pigments increased when when increased pigments photosynthetic enhance CO H the depend onthestrainusedfor inoculation. effect maytherefore pigments ofPGPRon photosynthetic was combinedwithanarbuscular mycorrhizalfungus. The sativa pigments (chlorophyll and carotenoids) in photosynthetic decreased observed (2008) al. et Aguirre values with respect to non-inoculated plants. Marulanda- by PGPR(LiuandZhang,2015). including theenhancementofplantabioticstresstolerance effects, beneficial mutually promoting soil, the in colonies the formofrootexudatesthatattract and maintain bacterial are knowntoreleasepartoftheirphotosyntheticoutput in role inplantgrowthandtheyieldofvariouscrops.Plants key a play and plant whole the of physiology the influence PGPR (2015), al. et Kumar to tolerance. According drought mention that plants inoculated with PGPRdeveloped 2015) al., et 2011;Armada al., Vardharajulaet 2003; al., et was therefore better, assimilating more CO more assimilating better, therefore was plants inoculated in efficiency Wateruse leaves. by release inoculated with s ), C) transpiration (E), and D) water use efficiency (WUE) of (WUE) efficiency use water D) and (E), transpiration C) ), 2 O moleculereleasedbystomata.Someauthors(Vivas Moreover, itwasobservedthat theinoculationwith SPADincreased M9 with inoculated plants Additionally On theother hand, ourresultstherefore show that plants Bacillus plantsinoculatedwith 2 spp.M9,increasedplantgrowth. Inoculation assimilation (photosynthesis) and reduce water assimilation(photosynthesis)andreducewater Bacillus strainsmodifiedgasexchangeto Bacillus megaterium 2 B. megaterium moleculesper Lactuca , but

413 CHILEAN JOURNAL OF AGRICULTURALCHILEAN JOURNAL OF AGRICULTURAL RESEARCH 76(4) OCTOBER RESEARCH 76(1)JANUARY Calvin cycle,andimproving plant growth. the in assimilation C for employed production, NADPH and energy isutilized inelectrontransport,leadinghigher ATP reported that CO that reported (2002) Quick and Hibberd photosynthesis. increase CO Moreover, 2014). Kibret, and (Ahemad pool auxin plant bychangingthepigment formationandphotosynthesis acetic acid/IAA). The IAA affects plant cell division, acid/indole (indole-3-acetic auxins synthesize rhizosphere microorganismsfrom the isolated (1996) Glick and Patten 2014). to al., According et (Nadeem nutrients solubilizing hormonal balance,producingplantgrowthregulatorsand promote plantgrowthbyregulatingnutritional and tocontrolplants. respect with The microorganisms can improved inpepperplantsinoculatedwithM9strain increase biomass. However, all plant growth parameters and itsincreaseinphotosynthesiswasnotenoughto strain has not an excellent synergy with pepper plants, species ofplantsandmicroorganisms, probablyK46 exudates is dependent upon the physiological status and are influenced byrootexudates,compositionof these interactions symbiotic plant-beneficial the (2014) Kibret from those of controls. According with Ahemad and with K46strain, plant growth parameters were similar root system(Vessey, 2003). developing orstressedplants,inducingelongationofthe the of content ethylene in decrease a and 2014); Kibret, uptake of water and minerals from the soil (Ahemad and root growthandproliferationofhairs,enhancingthe synthesis ofplantgrowth-regulators,whichcanpromote Biological Nfixation(Ashoketal.,2015);regulationofthe favorplantgrowth: PGPR explaininghow mechanisms inbiomass. anincrease observed There aredifferent pepper plantsinoculatedwith evaluated (2013) al. et Luna yield. and weight fruit fruits, increased growthcharacteristicssuchastotalnumberof plants withstrainsof pepper of inoculation the that found (2011) al. et Datta respectively.41.5%, and 73.9% by weight fresh root promoted significant growth of peppers, enhancing their used (2007) al. et Kang plants, pepper on studies previous with PGPRwasfoundtoimproveplantgrowthin quinone acceptor (Q more reaction centers and higher light harvesting; thus, the parameters andtotalchlorophyllconcentration,suggesting increased lightharvestingandphotosynthesisefficiency. changes initsphotosyntheticapparatus,leading to that upon endophyte colonization, host plant undergoes suggest (2015) al. et Rozpadek way, this In stomata. photosynthesis fromthevascularsystemandnot for C with supplied are tobacco in cells stem shoot; the Although some physiological parameters increased Here, M9strain improved chlorophyll fluorescence 2 resultingfromrespirationofbacteriacanhelpto Pseudomonas rhodesiaePseudomonas 2 producedinrootscanbetransportedto a ) is highly oxidized and its excitation Bacillus and spp. and Bacillus Pantoea ananatis Streptomyces spp. strainsand - - MARCH 2016 DECEMBER 2016 and spp. sustainable agricultureprograms. couldbeusedin M9strain characteristics. all growth inoculated with the M9 strain showed enhancements on mechanism in Habanero pepper plants. However, plants photosynthetic the of performance the influenced positively with Inoculation rate. transpiration decreasing and (WUE), efficiency use water and (photosynthesis) rate assimilation remarkably improved gas exchange, increasing both the net In addition,plantsinoculatedwithM9andK46showed PSII. of activity potential and (fluorescence) yield quantum photochemical quenching (NPQ), maximum photochemical M9 increasedphotochemicalquenching(qP),non- operating efficiency ( efficiency operating increase boththeelectrontransportrate(ETR)andPSII improved theefficiency ofphotosystem II (PSII)to on all parameters evaluated. Both strains (M9 and K46) spp.) usedinthisstudydemonstratedastriking influence strain ( Based onourresults,weconcludedthatM9 CONCLUSION Calatayud, A., J.W. Ramirez, D.J. Iglesias, and E. Barreno. 2002. Barreno. E. and Iglesias, D.J. J.W.Ramirez, A., Calatayud, Kozyrovska.Vera,O.P., J.P.V.de N.O. Burlak, Yatsenko, and of probe a fluorescence: Chlorophyll 2008. Baker, N.R. Ashok, K.A.,I.Bahadur, B.R.Maurya,R.Raghuwanshi, V.S. Armada, E.,G.Portela, A. Roldán,andR. Azcón. 2014.Combined Azcón. R. and Roldán, A. P. Castillo, Barea, J.M. E., Armada, applications and Mechanisms 2014. Kibret. M. and M., Ahemad, REFERENCES #334212 toJ.Kantun-Can. grant master’s for and B.Y.Samaniego-Gámez by studies doctoral for #253611 scholarship the for (CONACYT) Tecnologíay Ciencia de Nacional Consejo to Thank ACKNOWLEDGEMENTS Physiologia Plantarum116:308-316. a fluorescenceandantioxidant systemsinlettuceleaves. Effects of ozone on photosynthetic CO photosynthetic on ozone of Effects photosystem understress.Biopolymers andCell29:3-10. plant on effects bacterial of mechanisms Putative 2013. 59:89-113. photosynthesis invivo. Annual Review ofPlantBiology Pure and Applied Microbiology9:715-724. rhizobacteria enhanceagriculturalsustainability?Journalof promoting growth plant a Does 2015. al. et Singh, D.K. 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