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Acta Physiologiae Plantarum

, 41:163 | Cite as

Photosynthetic apparatus protection and drought effect mitigation in açaí palm seedlings by rhizobacteria

  • Gledson Luiz Salgado de Castro
  • Dalton Dias da Silva Júnior
  • Rafael Gomes Viana
  • Marcela Cristiane Ferreira Rêgo
  • Gisele Barata da SilvaEmail author
Original Article
  • 41 Downloads

Abstract

Water deficit sensitivity decreases the açaí palm seedling production in nurseries. The goal of this study was to evaluate gas exchange, chlorophyll a fluorescence, lipid peroxidation and antioxidant enzymes in açaí palm seedlings inoculated with rhizobacteria. Four rhizobacteria isolates (UFRA-58, UFRA-92, BRM-32111 and BRM-32113) and one control (without inoculation) were inoculated on açaí palm seedlings at field capacity (FC) 100%, 75%, 50% and 25%. Water deficit reduced photosynthetic performance in all açaí palm seedlings, but to a lesser extent in seedlings inoculated with rhizobacteria. At 75% FC, all inoculated seedlings maintained greater water potential, gas exchange and chlorophyll a fluorescence and, at 50% FC, only the seedlings inoculated with BRM-32111 and BRM-32113 were able to maintain these advantages in relation to the control. In 25% FC, no effect was observed for rhizobacteria inoculation. At 50% FC, the increase in catalase (CAT) enzymatic activity was induced by UFRA-58. The ascorbate peroxidase (APX) enzymatic activity was greater for UFRA-92, whereas superoxide dismutase (SOD) enzymatic activity was higher only for BRM-32113. The malonic aldehyde (MDA) content was greater only for control. Rhizobacterial inoculation in açaí palm seedlings attenuates the water deficit effects by photosynthetic performance maintenance and antioxidant enzymes activation, contributing to decrease the seedling mortality rate in nurseries.

Keywords

Antioxidant enzymes Biostimulant Euterpe oleracea Photosynthesis 

Abbreviations

A/E

Water use efficiency

A

Net CO2 assimilation rate

APX

Ascorbate peroxidase EC 1.11.1.11

BRM-32111

Pseudomonas fluorescens

BRM-32113

Burkholderia pyrrocinia

CAT

Catalase EC 1.11.1.6

FC

Field capacity

Ci

Intercellular CO2 concentration

E

Transpiration

ETR

Electron transport rate

Fo

Initial fluorescence

Fm

Maximum fluorescence

Fv’/Fm

Effective photochemical efficiency

Fv/Fo

Photosystem II potential activity

gs

Stomatal conductance

MDA

Malonic aldehyde

PAR

Photosynthetic active radiation

PGPR

Plant growth-promoting rhizobacteria

Ψw

Water potential

qP

Photochemical dissipation coefficient

qN

Non-photochemical dissipation coefficient

UFRA-58

Burkholderia sp.

UFRA-92

Bacillus subtilis

SOD

Superoxide dismutase EC 1.15.1.1

TBA

Thiobarbituric acid

Notes

Acknowledgements

The authors thank the Coordination for Higher Education Staff Development (CAPES) for granting fellowships and to the Plant Protection Laboratory (LPP) of the Federal Rural University of Amazon its logistical support.

References

  1. Alscher R, Erturk N (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341CrossRefGoogle Scholar
  2. Amir HG, Shamsuddin ZH, Halimi MS et al (2005) Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Commun Soil Sci Plant Anal 36:2059–2066.  https://doi.org/10.1080/00103620500194270 CrossRefGoogle Scholar
  3. Astriani M, Mubarik N, Tjahjoleksono A (2016) Selection of bacteria producing indole-3-Acetic acid and its application on oil palm seedlings (Elaeis guineensis Jacq.). Malays J Microbiol 12:147–154.  https://doi.org/10.21161/mjm.74615 CrossRefGoogle Scholar
  4. Baisak R, Rana D, Acharya PBB, Kar M (1994) Alterations in the activities of active oxygen scavenging enzymes of wheat leaves subjected to water stress. Plant Cell Physiol 35(3):489–495Google Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113.  https://doi.org/10.1146/annurev.arplant.59.032607.092759 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Barbosa M, Lobato A, Pereira T et al (2017) Antioxidant system is insufficient to prevent cell damages in Euterpe oleracea exposed to water deficit. Emir J Food Agric 29:206.  https://doi.org/10.9755/ejfa.2016-09-1217 CrossRefGoogle Scholar
  7. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  8. Bresson J, Varoquaux F, Bontpart T et al (2013) The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:558–569.  https://doi.org/10.1111/nph.12383 CrossRefGoogle Scholar
  9. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468.  https://doi.org/10.1111/j.1399-3054.1991.tb00121.x CrossRefGoogle Scholar
  10. Calbo MER, De Moraes JAPV (2000) Efeitos da deficiência de água em plantas de Euterpe oleracea (açaí). Rev Bras Bot 23:225–230.  https://doi.org/10.1590/S0100-84042000000300001 CrossRefGoogle Scholar
  11. Campostrini E (2001) Fluorescência da clorofila a: considerações teóricas e aplicações práticas. uenf.br. UFNF, Rio de JaneiroGoogle Scholar
  12. Cattelan AJ (1999) Métodos Qualitativos para Determinação de Características Bioquímicas e Fisiológicas Associadas com Bactérias Promotoras do Crescimento Vegetal. Embrapa Soja 139:36Google Scholar
  13. Döbereiner J, Day J (1976) Associative symbioses in tropical grasses: characterization of microorganisms and dinitrogen-fixing sites. In: Proceedings of the 1st international symposium on nitrogen fixation. Washington State University Press Pullman, pp 518–538Google Scholar
  14. 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 4:45.  https://doi.org/10.1186/s13568-014-0045-8 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fan X, Hu H, Huang G et al (2015) Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize. Plant Soil 390:337–349.  https://doi.org/10.1007/s11104-015-2410-z CrossRefGoogle Scholar
  16. Filippi MCC, da Silva GB, Silva-Lobo VL et al (2011) Leaf blast (Magnaporthe oryzae) suppression and growth promotion by rhizobacteria on aerobic rice in Brazil. Biol Control 58:160–166.  https://doi.org/10.1016/j.biocontrol.2011.04.016 CrossRefGoogle Scholar
  17. 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
  18. Forni C, Duca D, Glick BR (2016) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 1:5–9.  https://doi.org/10.1007/s11104-016-3007-x CrossRefGoogle Scholar
  19. Gagné-Bourque F, Bertrand A, Claessens A et al (2016) Alleviation of drought stress and metabolic changes in timothy (Phleum pratense L.) colonized with Bacillus subtilis B26. Front Plant Sci 7:1–16.  https://doi.org/10.3389/fpls.2016.00584 CrossRefGoogle Scholar
  20. Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  21. Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Amelioration of drought tolerance in wheat by the interaction of plant growth promoting rhizobacteria. Plant Biol 18:992–1000.  https://doi.org/10.1111/plb.12505 CrossRefGoogle Scholar
  22. Gou W, Tian L, Ruan Z et al (2015) Accumulation of choline and glycinebetaine and drought stress tolerance induced in maize (Zea mays) by three plant growth promoting rhizobacteria (PGPR) strains. Pak J Bot 47:581–586Google Scholar
  23. Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455CrossRefGoogle Scholar
  24. Kado CI, Heskett MG (1970) Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology 60:969.  https://doi.org/10.1094/Phyto-60-969 CrossRefPubMedGoogle Scholar
  25. Kasim WA, Osman ME, Omar MN et al (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32:122–130.  https://doi.org/10.1007/s00344-012-9283-7 CrossRefGoogle Scholar
  26. 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
  27. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349.  https://doi.org/10.1146/annurev.pp.42.060191.001525 CrossRefGoogle Scholar
  28. Li W, Zhang S, Shan L (2007) Responsibility of non-stomatal limitations for the reduction of photosynthesis-response of photosynthesis and antioxidant enzyme characteristics in alfalfa (Medicago sativa L.) seedlings to water stress and rehydration. Front Agric China 1:255–264.  https://doi.org/10.1007/s11703-007-0044-5 CrossRefGoogle Scholar
  29. Malke H (1991) Z. Klement, K. Rudolph and D. C. Sands (Editors), Methods in Phytobacteriology. XIV + 568 S., 135 Abb., 62 Tab. Budapest 1990. Akadémiai Kaidó. Ft 1520.0 ISBN: 963-05-4955-7. J Basic Microbiol 31:148.  https://doi.org/10.1002/jobm.3620310214 CrossRefGoogle Scholar
  30. Martins BEM (2015) Caracterização morfológica, bioquímica e molecular de isolados bacterianos antagonistas a Magnaporthe oryzae. Diss Univ Fed, Goiás, p 80fGoogle Scholar
  31. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence–a practical guide. J Exp Bot 51:659–668.  https://doi.org/10.1093/jexbot/51.345.659 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Medrano H, Escalona JM, Bota J et al (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89:895–905.  https://doi.org/10.1093/aob/mcf079 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mizuno M, Kamei M, Tsuchida H (1998) Ascorbate peroxidase and catalase cooperate for protection against hydrogen peroxide generated in potato tubers during low-temperature storage. IUBMB Life 44:717–726.  https://doi.org/10.1080/15216549800201762 CrossRefGoogle Scholar
  34. Mohammadi H, Dashi R, Farzaneh M et al (2016) Effects of beneficial root pseudomonas on morphological, physiological, and phytochemical characteristics of Satureja hortensis (Lamiaceae) under water stress. Brazilian J Bot 1:5–9.  https://doi.org/10.1007/s40415-016-0319-2 CrossRefGoogle Scholar
  35. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  36. Nascente AS, de Filippi MCC, Lanna AC et al (2016) Biomass, gas exchange, and nutrient contents in upland rice plants affected by application forms of microorganism growth promoters. Environ Sci Pollut Res 24:2956–2965.  https://doi.org/10.1007/s11356-016-8013-2 CrossRefGoogle Scholar
  37. Naylor D, Coleman-Derr D (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8:1–16.  https://doi.org/10.3389/fpls.2017.02223 CrossRefGoogle Scholar
  38. Oliveira MDSP, Neto JTDF (2004) Cultivar BRS-Pará: açaizeiro para Produção de Frutos em Terra Firme. Embrapa Comun Técnico 114:1–3Google Scholar
  39. Oliveira LC, De Oliveira MDSP, Davide LC, Torres GA (2016) Karyotype and genome size in Euterpe Mart. (Arecaceae) species. Comp Cytogenet 10:17–25.  https://doi.org/10.3897/CompCytogen.v10i1.5522 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 54:135–142.  https://doi.org/10.1023/A:1005936823310 CrossRefGoogle Scholar
  41. Pinheiro HA, Silva JV, Endres L et al (2008) Leaf gas exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus communis L) seedlings subjected to salt stress conditions. Ind Crops Prod 27:385–392.  https://doi.org/10.1016/j.indcrop.2007.10.003 CrossRefGoogle Scholar
  42. Rolli E, Marasco R, Vigani G et al (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331.  https://doi.org/10.1111/1462-2920.12439 CrossRefPubMedGoogle Scholar
  43. Rufino M, Pérez-Jiménez J, Arranz s (2011) Açaí (Euterpe oleraceae) ‘BRS Pará’: a tropical fruit source of antioxidant dietary fiber and high antioxidant capacity oil. Food Res Int 44:2100–2106.  https://doi.org/10.1016/j.foodres.2010.09.011 CrossRefGoogle Scholar
  44. Samaniego-Gámez BY, Garruña R, Tun-Suárez JM et al (2016) Bacillus spp. inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants. Chil J Agric Res 76:409–416.  https://doi.org/10.4067/S0718-58392016000400003 CrossRefGoogle Scholar
  45. Saravanakumar D, Kavino M, Raguchander T et al (2011) Plant growth promoting bacteria enhance water stress resistance in green gram plants. Acta Physiol Plant 33:203–209.  https://doi.org/10.1007/s11738-010-0539-1 CrossRefGoogle Scholar
  46. Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Ecophysiology of photosynthesis. Springer, Berlin Heidelberg, pp 49–70CrossRefGoogle Scholar
  47. Silva Cravo M, Viégas IJM, Brasil EC (2007) Recomendações de adubação e calagem para o Estado do Pará. EMBRAPA Amazonia Oriental, BélemGoogle Scholar
  48. 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 39:58.  https://doi.org/10.1007/s11738-017-2354-4 CrossRefGoogle Scholar
  49. Silvestre WVD, Pinheiro HA, Souza RORDM, Palheta LF (2016) Revista Brasileira de Engenharia Agrícola e Ambiental Morphological and physiological responses of açaí seedlings subjected to different watering regimes Respostas morfológicas e fisiológicas de mudas de açaizeiros submetidas à diferentes regimes hídricos. 364–371Google Scholar
  50. Silvestre WVD, Silva PA, Palheta LF et al (2017) Differential tolerance to water deficit in two açaí (Euterpe oleracea Mart.) plant materials. Acta Physiol Plant 39:4.  https://doi.org/10.1007/s11738-016-2301-9 CrossRefGoogle Scholar
  51. Stefan M, Munteanu N, Stoleru V (2013) Effects of inoculation with plant growth promoting rhizobacteria on photosynthesis, antioxidant status and yield of runner bean. Rom Biotechnol Lett 18:8132–8143Google Scholar
  52. Steffen KL (1991) Avoidance of photooxidative stress: balancing energy flux within the chloroplast. Curr Top plant Physiol 6:119–130Google Scholar
  53. Sylvester-Bradley R, Asakawa N, La TS et al (1982) Levantamento quantitativo de microrganismos solubilizadores de fosfatos na rizosfera de gramíneas e leguminosas forrageiras na Amazônia. Acta Amaz 12:15–22CrossRefGoogle Scholar
  54. Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43(4):777–780PubMedPubMedCentralGoogle Scholar
  55. Timmusk S, Abd El-Daim IA, Copolovici L et al (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments Enhanced biomass production and reduced emissions of stress volatiles. PLoS One.  https://doi.org/10.1371/journal.pone.0096086 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Wang CJ, Yang W, Wang C et al (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7:1–10.  https://doi.org/10.1371/journal.pone.0052565 CrossRefGoogle Scholar
  57. Wang P, Zhang C, Guo M et al (2014a) Complete genome sequence of Bacillus thuringiensis YBT-1518, a typical strain with high toxicity to nematodes. J Biotechnol 171:1–2.  https://doi.org/10.1016/j.jbiotec.2013.11.023 CrossRefPubMedGoogle Scholar
  58. Wang S, Ouyang L, Ju X et al (2014b) Survey of plant drought-resistance promoting bacteria from populus euphratica tree living in arid area. Indian J Microbiol 54:419–426.  https://doi.org/10.1007/s12088-014-0479-3 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agric Res 56:715–721.  https://doi.org/10.1071/AR04082 CrossRefGoogle Scholar
  60. 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 39:22.  https://doi.org/10.1007/s11738-016-2321-5 CrossRefGoogle Scholar
  61. Zhou C, Ma Z, Zhu L et al (2016) Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int J Mol Sci 17:976.  https://doi.org/10.3390/ijms17060976 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  • Gledson Luiz Salgado de Castro
    • 1
  • Dalton Dias da Silva Júnior
    • 2
  • Rafael Gomes Viana
    • 3
  • Marcela Cristiane Ferreira Rêgo
    • 1
  • Gisele Barata da Silva
    • 1
    Email author
  1. 1.Plant Protection Laboratory (LPP)Federal Rural University of Amazonia (UFRA), Institute of Agricultural SciencesBelémBrazil
  2. 2.Federal University of Amazonas (UFAM), Education, Agriculture and Environment InstituteHumaitáBrazil
  3. 3.Federal Rural University of Amazonia (UFRA), Institute of Agricultural SciencesBelémBrazil

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