Advertisement

Açaí palm seedling growth promotion by rhizobacteria inoculation

  • Gledson Luiz Salgado de Castro
  • Marcela Cristiane Ferreira Rêgo
  • Walter Vellasco Duarte Silvestre
  • Telma Fátima Vieira Batista
  • Gisele Barata da SilvaEmail author
Environmental Microbiology - Research Paper
  • 2 Downloads

Abstract

Lower growth rate of the açaí palm seedlings limits the crops’ commercial expansion. The goal was evaluating the biometry, biomass accumulation, nutrient contents, chlorophyll-a fluorescence, and gas exchange in açaí seedlings inoculated with rhizobacteria. The treatments were individual inoculations of the seven rhizobacteria isolates and one control (without inoculation) on the roots. Biometry and biomass data were submitted to cluster analysis to separate the isolates into groups according to the similarity degree, and groups’ means were compared through the SNK test. Three groups were formed; group 1 was composed of the control; group 2 of the UFRA-35, UFRA-38, UFRA-58, UFRA-61, UFRA-92, and BRM-32111 isolates; and group 3 was composed of the BRM-32113 isolate. Group 2 and 3 isolates promoted an increase in growth, biomass accumulation, higher levels of nutrients and chlorophyll, and improvements in the gas exchange and chlorophyll-a fluorescence in comparison with the control. The results evidenced that the rhizobacteria accelerate the growth, increase the photosynthetic efficiency, and induce the leaf nutrient accumulation in açaí palm seedlings. The rhizobacteria inoculation can contribute to the sustainable management of the açaí palm seedling production in nurseries.

Keywords

Euterpe oleracea Biostimulants Biofertilizer Photosynthesis 

Abbreviations

UFRA-35

Burkholderia sp.

UFRA-38

Bacillus safensis

UFRA-58

Burkholderia sp.

UFRA-61

Pseudomonas fluorescens

UFRA-92

Bacillus subtilis

BRM-32111

Pseudomonas fluorescens

BRM-32113

Burkholderia pyrrocinia

N

nitrogen

P

phosphorus

K

potassium

Ca

calcium

Mg

magnesium

A

CO2 net assimilation rate

gs

stomatal conductance to water vapor

E

transpiration rate

Ci

CO2 intercellular concentration

A/E

water use instantaneous efficiency

Chla

chlorophyll-a

Chlb

chlorophyll-b

Chla + b

total chlorophyll

Chla/Chlb

ratio between Chla and Chlb

Fo

initial fluorescence

Fm

maximum fluorescence

Fv/Fo

PSII potential activity

Fv′/Fm′

PSII effective photochemical efficiency

qP

photochemical extinction coefficients

qN

non-photochemical extinction coefficients

ETR

electron transfer rate

Notes

Acknowledgments

The authors thank the Coordination for Higher Education Staff Development (CAPES) for granting fellowships, the Plant Protection Laboratory (PPL) for its logistical support, and Dr. Alessandra Jackeline G. Moraes and Msc. Gleiciane Rodrigues dos Santos of the Universidade Federal Rural da Amazônia for the rhizobacteria molecular identification.

References

  1. 1.
    Yamaguchi KKDL, Pereira LFR, Lamarão CV, Lima ES, da Veiga-Junior VF (2015) Amazon acai: chemistry and biological activities: a review. Food Chem 179:137–151.  https://doi.org/10.1016/j.foodchem.2015.01.055 CrossRefPubMedGoogle Scholar
  2. 2.
    Cantu-Jungles TM, Iacomini M, Cipriani TR, Cordeiro LMC (2017) Extraction and characterization of pectins from primary cell walls of edible açaí (Euterpe oleraceae) berries, fruits of a monocotyledon palm. Carbohydr Polym 158:37–43.  https://doi.org/10.1016/j.carbpol.2016.11.090 CrossRefPubMedGoogle Scholar
  3. 3.
    Oliveira MDSP, Neto JTDF (2004) Cultivar BRS-Pará: Açaizeiro para Produção de Frutos em Terra Firme. Embrapa Comun Técnico 114(1):1–3Google Scholar
  4. 4.
    Costa MR, De Oliveira MDSP, Ohaze MMM (2004) Divergência Genética No Açaizeiro Com Base Em Marcadores Rapd. Rev Ciênc Agrár 41:89–95Google Scholar
  5. 5.
    Om AC, Ghazali AHA, Keng CL, Ishak Z (2009) Microbial inoculation improves growth of oil palm plants (Elaeis guineensis Jacq.). Trop Life Sci Res 20(2):71–77PubMedPubMedCentralGoogle Scholar
  6. 6.
    George P, Gupta A, Gopal M, Thomas L, Thomas GV (2013) Multifarious beneficial traits and plant growth promoting potential of Serratia marcescens KiSII and Enterobacter sp. RNF 267 isolated from the rhizosphere of coconut palms (Cocos nucifera L.). World J Microbiol Biotechnol 29(1):109–117.  https://doi.org/10.1007/s11274-012-1163-6 CrossRefPubMedGoogle Scholar
  7. 7.
    Haldar S, Sengupta S (2015) Plant-microbe cross-talk in the rhizosphere: insight and biotechnological potential. Open Microbiol J 9(iii):1–7.  https://doi.org/10.2174/1874285801509010001 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Chaudhary SR, Sindhu SS (2016) Growth stimulation of clusterbean (Cyamopsis tetragonoloba) by coinoculation with rhizosphere bacteria and Rhizobium. Legum Res - An Int J 39(OF):1003–1012.  https://doi.org/10.18805/lr.v0iOF.8605 CrossRefGoogle Scholar
  9. 9.
    Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119(3):243–254.  https://doi.org/10.1007/s10658-007-9165-1 CrossRefGoogle Scholar
  10. 10.
    Astriani M, Mubarik NR, Tjahjoleksono A (2016) Selection of bacteria producing indole-3-acetic acid and its application on oil palm seedlings (Elaeis guineensis Jacq.). Malays J Microbiol 12(2):147–154.  https://doi.org/10.21161/mjm.74615 CrossRefGoogle Scholar
  11. 11.
    Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15.  https://doi.org/10.6064/2012/963401 CrossRefGoogle Scholar
  12. 12.
    Aslantaş R, Çakmakçi R, Şahin F (2007) Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Sci Hortic (Amsterdam) 111(4):371–377.  https://doi.org/10.1016/j.scienta.2006.12.016 CrossRefGoogle Scholar
  13. 13.
    Asari S, Tarkowská D, Rolčík J et al (2016) Analysis of plant growth-promoting properties of Bacillus amyloliquefaciens UCMB5113 using Arabidopsis thaliana as host plant. Planta.:15–30.  https://doi.org/10.1007/s00425-016-2580-9 CrossRefGoogle Scholar
  14. 14.
    Amir HG, Shamsuddin ZH, Halimi MS, Marziah M, Ramlan MF (2005) Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Commun Soil Sci Plant Anal 36(15–16):2059–2066.  https://doi.org/10.1080/00103620500194270 CrossRefGoogle Scholar
  15. 15.
    Noor Ai’shah O, Tharek M, Keyeo F et al (2013) Influence of indole-3-acetic acid (IAA) produced by diazotrophic bacteria on root development and growth of in vitro oil palm shoots (Elaeis guineensis Jacq.). J Oil Palm Res 25(APR):100–107Google Scholar
  16. 16.
    Zhang K, Liu Z, Shan X et al (2017) Physiological properties and chlorophyll biosynthesis in a Pak-choi (Brassica rapa L. ssp. chinensis) yellow leaf mutant, pylm. Acta Physiol Plant 39(1):22.  https://doi.org/10.1007/s11738-016-2321-5 CrossRefGoogle Scholar
  17. 17.
    Nascente AS, de Filippi MCC, Lanna AC, de Souza ACA, da Silva Lobo VL, da Silva GB (2016) Biomass, gas exchange, and nutrient contents in upland rice plants affected by application forms of microorganism growth promoters. Environ Sci Pollut Res 24(3):2956–2965.  https://doi.org/10.1007/s11356-016-8013-2 CrossRefGoogle Scholar
  18. 18.
    Maxwell K, Johnson GN (2000) Chlorophyll fluorescence--a practical guide. J Exp Bot 51(345):659–668.  https://doi.org/10.1093/jexbot/51.345.659 CrossRefGoogle Scholar
  19. 19.
    Silva Cravo M, Viégas IJM, Brasil EC (2007) Recomendações de Adubação e Calagem Para o Estado Do Pará. EMBRAPA Amazonia Oriental, BélemGoogle Scholar
  20. 20.
    Klar AE, Villa Nova NA, Marcos ZZ, Cervéllini A (1966) Determinação da umidade do solo pelo método das pesagens. An da Esc Super Agric Luiz Queiroz 23:15–30.  https://doi.org/10.1590/S0071-12761966000100003 CrossRefGoogle Scholar
  21. 21.
    Filippi MCC, da Silva GB, Silva-Lobo VL, Côrtes MVCB, Moraes AJG, Prabhu AS (2011) Leaf blast (Magnaporthe oryzae) suppression and growth promotion by rhizobacteria on aerobic rice in Brazil. Biol Control 58(2):160–166.  https://doi.org/10.1016/j.biocontrol.2011.04.016 CrossRefGoogle Scholar
  22. 22.
    Martins BEM (2015) Caracterização morfológica, bioquímica e molecular de isolados bacterianos antagonistas a Magnaporthe oryzae. 80 f (Doctoral dissertation, Dissertação, Universidade Federal de Goiás).Google Scholar
  23. 23.
    Kado CI, Heskett MG (1970) Selective Media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology. 60(6):969.  https://doi.org/10.1094/Phyto-60-969 CrossRefPubMedGoogle Scholar
  24. 24.
    Xiang L, de Boer SH (1995) Selection of polymerase chain reaction primers from an RNA intergenic spacer region for specific detection of <i xmlns=. Phytopathology. 85:837–842.  https://doi.org/10.1094/Phyto-85-837 CrossRefGoogle Scholar
  25. 25.
    Silvestre WVD, Pinheiro HA, Souza RORDM, Palheta LF (2016) Morphological and physiological responses of açaí seedlings subjected to different watering regimes. Revista Brasileira de Engenharia Agrícola e Ambiental. 20(4):364–371CrossRefGoogle Scholar
  26. 26.
    Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components - calculation of qP and Fv’/Fm’ without measuring Fo’. Photosynth Res 54(2):135–142.  https://doi.org/10.1023/A:1005936823310 CrossRefGoogle Scholar
  27. 27.
    De Jesus SV, Marenco RA (2008) O SPAD-502 como alternativa para a determinação dos teores de clorofila em espécies frutíferas. Acta Amaz 38(4):815–818.  https://doi.org/10.1590/S0044-59672008000400029 CrossRefGoogle Scholar
  28. 28.
    Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA-Bioenergetics 975(3):384–394.  https://doi.org/10.1016/S0005-2728(89)80347-0 CrossRefGoogle Scholar
  29. 29.
    Silva F (2009) Manual de Análises Químicas de Solos, Plantas e Fertilizantes. Brasília, Embrapa Informação TecnológicaGoogle Scholar
  30. 30.
    Benincasa MMP (1988) Análise de Crescimento de Plantas: Noções Básicas. Jaboticabal, FUNEPGoogle Scholar
  31. 31.
    Team RC (2017) R: A language and environment for statistical computing. R Found Stat Comput Vienna, Austria https://www.R-project.org. Accessed 3 Dec 2018
  32. 32.
    Rais A, Shakeel M, Hafeez FY, Hassan MN (2016) Plant growth promoting rhizobacteria suppress blast disease caused by Pyricularia oryzae and increase grain yield of rice. BioControl. 61(6):769–780.  https://doi.org/10.1007/s10526-016-9763-y CrossRefGoogle Scholar
  33. 33.
    Gu A, Ozaktan H, Yolageldi L (2017) Rhizobacteria promoted growth and yield of tomato plants and control of Fusarium oxysporum f. sp. Acta Hortic:345–352.  https://doi.org/10.17660/ActaHortic.2017.1164.44
  34. 34.
    Prasad AA, Babu S (2017) In growth promotion of groundnut ( Arachis hypogea L.). An Acad Bras Cienc 89(2):1027–1040CrossRefGoogle Scholar
  35. 35.
    De Sousa TP, Carlos A, De Souza A et al (2018) Bioagents and silicon promoting fast early upland rice growth. Environ Sci Pollut Res 25:3657–3668.  https://doi.org/10.1007/s11356-017-0753-0 CrossRefGoogle Scholar
  36. 36.
    Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350CrossRefGoogle Scholar
  37. 37.
    Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84(3):603–615.  https://doi.org/10.1007/s10725-017-0365-1 CrossRefGoogle Scholar
  38. 38.
    Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57(1):233–266.  https://doi.org/10.1146/annurev.arplant.57.032905.105159 CrossRefPubMedGoogle Scholar
  39. 39.
    Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34Google Scholar
  40. 40.
    Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157(3):361–379.  https://doi.org/10.1111/j.1744-7348.2010.00439.x CrossRefGoogle Scholar
  41. 41.
    Kang SM, Khan AL, You YH, Kim JG, Kamran M, Lee IJ (2014) Gibberellin production by newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J Microbiol Biotechnol 24(1):106–112.  https://doi.org/10.4014/jmb.1304.04015 CrossRefPubMedGoogle Scholar
  42. 42.
    Kang SM, Khan AL, Hamayun M et al (2012) Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J Microbiol 50(6):902–909.  https://doi.org/10.1007/s12275-012-2273-4 CrossRefPubMedGoogle Scholar
  43. 43.
    Silva PA, Cosme VS, Rodrigues KCB et al (2017) Drought tolerance in two oil palm hybrids as related to adjustments in carbon metabolism and vegetative growth. Acta Physiol Plant 39(2):58.  https://doi.org/10.1007/s11738-017-2354-4 CrossRefGoogle Scholar
  44. 44.
    Flexas J, Barbour MM, Brendel O et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84.  https://doi.org/10.1016/j.plantsci.2012.05.009 CrossRefPubMedGoogle Scholar
  45. 45.
    Fan X, Hu H, Huang G, Huang F, Li Y, Palta J (2015) Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize. Plant Soil 390(1–2):337–349.  https://doi.org/10.1007/s11104-015-2410-z CrossRefGoogle Scholar
  46. 46.
    Doni F, Isahak A, Che Mohd Zain CR, Wan Yusoff WM (2014) Physiological and growth response of rice plants (Oryza sativa L.) to Trichoderma spp. inoculants. AMB Express 4(1):45.  https://doi.org/10.1186/s13568-014-0045-8 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Shi Y, Lou K, Li C (2010) Growth and photosynthetic efficiency promotion of sugar beet (Beta vulgaris L.) by endophytic bacteria. Photosynth Res 105(1):5–13.  https://doi.org/10.1007/s11120-010-9547-7 CrossRefPubMedGoogle Scholar
  48. 48.
    Alam S, Cui Z-J, Yamagishi T, Ishii R (2001) Grain yield and related physiological characteristics of rice plants (Oryza sativa L.) inoculated with free-living rhizobacteria. Plant Prod Sci 4(2):126–130.  https://doi.org/10.1626/pps.4.126 CrossRefGoogle Scholar
  49. 49.
    Samaniego-Gámez BY, Garruña R, Tun-Suárez JM, Kantun-Can J, Reyes-Ramírez A, Cervantes-Díaz L (2016) Bacillus spp. inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants. Chil J Agric Res 76(4):409–416.  https://doi.org/10.4067/S0718-58392016000400003 CrossRefGoogle Scholar
  50. 50.
    Lucas JA, García-Cristobal J, Bonilla A, Ramos B, Gutierrez-Mañero J (2014) Beneficial rhizobacteria from rice rhizosphere confers high protection against biotic and abiotic stress inducing systemic resistance in rice seedlings. Plant Physiol Biochem 82:44–53.  https://doi.org/10.1016/j.plaphy.2014.05.007 CrossRefPubMedGoogle Scholar
  51. 51.
    Suresh K, Nagamani C, Kantha DL, Kumar MK (2012) Changes in photosynthetic activity in five common hybrids of oil palm (Elaeis guineensis Jacq.) seedlings under water deficit. Photosynthetica. 50(4):549–556.  https://doi.org/10.1007/s11099-012-0062-2 CrossRefGoogle Scholar
  52. 52.
    Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42(1):313–349.  https://doi.org/10.1146/annurev.pp.42.060191.001525 CrossRefGoogle Scholar
  53. 53.
    Wolff WM, Floss EL (2008) Correlação entre teores de nitrogênio e de clorofila na folha com o rendimento de grãos de aveia branca. Ciência Rural 38(6):1510–1515.  https://doi.org/10.1590/S0103-84782008000600003 CrossRefGoogle Scholar
  54. 54.
    Amir HG, Shamsuddin ZH, Halimi MS, Ramlan MF, Marziah M (2003) N2 fixation, nutrient accumulation and plant growth promotion by rhizobacteria in association with oil palm seedlings. Pak J Biol Sci 6(14):1269–1272CrossRefGoogle Scholar
  55. 55.
    Acevedo E, Galindo-Castañeda T, Prada F, Navia M, Romero HM (2014) Phosphate-solubilizing microorganisms associated with the rhizosphere of oil palm (Elaeis guineensis Jacq.) in Colombia. Appl Soil Ecol 80(August):26–33.  https://doi.org/10.1016/j.apsoil.2014.03.011 CrossRefGoogle Scholar
  56. 56.
    Velásquez E, Rodríguez-Barrueco C (2007) In: Velázquez E, Rodríguez-Barrueco C (eds) First International Meeting on Microbial Phosphate Solubilization. Springer Netherlands, Dordrecht.  https://doi.org/10.1007/978-1-4020-5765-6 CrossRefGoogle Scholar
  57. 57.
    Pan Y, Lu Z, Lu J, Li X, Cong R, Ren T (2017) Effects of low sink demand on leaf photosynthesis under potassium deficiency. Plant Physiol Biochem 113:110–121.  https://doi.org/10.1016/j.plaphy.2017.01.027 CrossRefPubMedGoogle Scholar
  58. 58.
    Hu X, Chen J, Guo J (2006) Two phosphate- and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22(9):983–990.  https://doi.org/10.1007/s11274-006-9144-2 CrossRefGoogle Scholar
  59. 59.
    Duarah I, Deka M, Saikia N, Deka Boruah HP (2011) Phosphate solubilizers enhance NPK fertilizer use efficiency in rice and legume cultivation. 3 Biotech 1(4):227–238.  https://doi.org/10.1007/s13205-011-0028-2 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Gledson Luiz Salgado de Castro
    • 1
  • Marcela Cristiane Ferreira Rêgo
    • 1
  • Walter Vellasco Duarte Silvestre
    • 2
  • Telma Fátima Vieira Batista
    • 1
  • Gisele Barata da Silva
    • 1
    Email author
  1. 1.Institute of Agricultural Sciences, Plant Protection Laboratory (LPP)Federal Rural University of Amazonia (UFRA)BelémBrazil
  2. 2.Institute of Agricultural SciencesFederal Rural University of Amazonia (UFRA)BelémBrazil

Personalised recommendations