biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 67:213-223, 2023 | DOI: 10.32615/bp.2023.022

Gene expression and biochemical profiling in the mitigation of heat stress in common bean using Bacillus subtilis

B.C. Lima1, T.R. Cruz2, A.F. RibaS1, T.B. Santos1, V. Cacefo1, F.F. Araujo1, *
1 Plant Production Post Graduate Program, Universidade do Oeste Paulista, CEP 19067-175, Presidente Prudente - SP, Brazil
2 Chemistry Post Graduate Program, Universidade Estadual Paulista "Júlio de Mesquita Filho" CEP 19060-900, Presidente Prudente - SP, Brazil

The present work aimed to evaluate the effect of heat stress on common bean (Phaseolus vulgaris L.) genotypes during the reproductive phase as a function of the inoculation of plants with Bacillus subtilis. The treatments were established by inoculating two strains of B. subtilis (AP-3 and AP-12) and a control. The plants were subjected to heat stress when they reached the reproductive stage, with an increase in temperature to 28/33°C. The duration of the stress period was ten days. Flowering, biochemical, and gene expression evaluations were performed. There was the interaction of B. subtilis AP-3 with the bean cultivar IAC-Imperador, reducing flower abortion, promoting the formation of new flower buds, and increasing the content of proline and guaiacol peroxidase activity in plant tissues. However, there was a reduction of transcription of genes encoding the 1-carboxylic acid-1aminocyclopropane oxidase and ethylene response factors and an increase of the Δ1-pyrroline-5-carboxylate synthetase1 gene. These results suggest that B. subtilis may modulate some metabolic pathways in response to high-temperature stress during the reproductive phase of the common bean. This also confirms that Bacillus strains represent a useful option to moderate abiotic stresses.

Keywords: gene expression, Phaseolus vulgaris L., plant growth-promoting rhizobacteria, stress tolerance.

Received: July 1, 2022; Revised: May 15, 2023; Accepted: May 16, 2023; Published online: August 23, 2023  Show citation

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Lima, B.C., Cruz, T.R., RibaS, A.F., Santos, T.B., Cacefo, V., & Araujo, F.F. (2023). Gene expression and biochemical profiling in the mitigation of heat stress in common bean using Bacillus subtilis. Biologia plantarum67, Article 213-223. https://doi.org/10.32615/bp.2023.022
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References

  1. Abd El-Daim I.A., Bejai S., Meijer J.: Improved heat stress tolerance of wheat seedlings by bacterial seed treatment. - Plant Soil 379: 337-350, 2014.
  2. Abd El-Daim I.A., Bejai S., Meijer J.: Bacillus velezensis 5113 induced metabolic and molecular reprogramming during abiotic stress tolerance in wheat. - Sci. Rep.-UK 9: 16282, 2019.
  3. Adams D.O., Yang S.F.: Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. - PNAS 76: 170-174, 1979. Go to original source...
  4. Andrade C.A., Souza K.R.D., Santos M.O. et al.: Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. - Sci. Hortic.-Amsterdam 232: 40-45, 2018. Go to original source...
  5. Appiah C., Yang Z.F., He J. et al.: Genome-wide identification of Hsp90 gene family in perennial ryegrass and expression analysis under various abiotic stresses. - Plants-Basel 10: 2509, 2021. Go to original source...
  6. Araujo F.F.: [Seed inoculation with Bacillus subtilis, formulated with oyster meal and growth of corn, soybean and cotton.] - Ciênc. Agrotec. 32: 456-462, 2008. [In Portuguese] Go to original source...
  7. Araújo F.F., Henning A.A., Hungria M.: Phytohormones and antibiotics produced by Bacillus subtilis and their effects on seed pathogenic fungi and on soybean root development. - World J. Microb. Biot. 21: 1639-1645, 2005. Go to original source...
  8. Ayuso-Calles M., Flores-Félix J.D., Rivas R.: Overview of the role of rhizobacteria in plant salt stress tolerance. - Agronomy 11: 1759, 2021. Go to original source...
  9. Bagdi D.L., Shaw B.P., Sahu B.B., Purohit G.K.: Real time PCR expression analysis of gene encoding p5cs enzyme and proline metabolism under NaCl salinity in rice. - J. Environ. Biol. 36: 955-961, 2015.
  10. Bagheri M., Gholami M., Baninasab B.: Hydrogen peroxide-induced salt tolerance in relation to antioxidant systems in pistachio seedlings. - Sci. Hortic.-Amsterdam 243: 207-213, 2019. Go to original source...
  11. Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
  12. Batool T., Ali S., Seleiman M.F. et al.: Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. - Sci. Rep.-UK 10: 16975, 2020. Go to original source...
  13. Baxter A., Mittler R., Suzuki N.: ROS as key players in plant stress signalling. - J. Exp. Bot. 65: 1229-1240, 2014. Go to original source...
  14. Bhattarai S., Harvey J.T., Djidonou D., Leskovar D.I.: Exploring morpho-physiological variation for heat stress tolerance in tomato. - Plants-Basel 10: 347, 2021. Go to original source...
  15. Bita C.E., Gerats T.: Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. - Front. Plant Sci. 4: 273, 2013. Go to original source...
  16. CGIAR: Developing beans that can beat the heat. Pp. 12. Available at: http://ciat-library.ciat.cgiar.org/articulos_ciat/biblioteca/DEVELOPING_BEANS_THAT_CAN_BEAT_THE_HEAT_lowres%20(2).pdf, 2015.
  17. Chandra D., Srivastava R., Glick B.R., Sharma A.K.: Drought-tolerant Pseudomonas spp. improve the growth performance of finger millet (Eleusine coracana (L.) Gaertn.) under non-stressed and drought-stressed conditions. - Pedosphere 28: 227-240, 2018. Go to original source...
  18. Ding Y., Shi Y., Yang S.: Molecular regulation of plant responses to environmental temperatures. - Mol. Plant 13: 544-564, 2020. Go to original source...
  19. El-Esawi M.A., Alaraidh I.A., Alsahli A.A. et al.: Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. - Plant Physiol. Biochem. 132: 375-384, 2018. Go to original source...
  20. Fan X., Mattheis J.P., Roberts R.G.: Biosynthesis of phytoalexin in carrot root requires ethylene action. - Physiol. Plantarum 110: 450-454, 2000. Go to original source...
  21. Ferreira A.C.: [Physiology and morphology of common bean plants under water deficit.] Thesis. Pp. 63. Universidade de São Paulo, Piracicaba 2017. [In Portuguese]
  22. Furlan A.L., Bianucci E., Giordano W. et al.: Proline metabolic dynamics and implications in drought tolerance of peanut plants. - Plant Physiol. Biochem. 151: 566-578, 2020. Go to original source...
  23. Ghaffari H., Tadayon M.R., Bahador M., Razmjoo J.: Investigation of the proline role in controlling traits related to sugar and root yield of sugar beet under water deficit conditions. - Agr. Water Manage. 243: 106448, 2021. Go to original source...
  24. Ghosh U.K., Islam M.N., Siddiqui M.N., Khan M.A.R.: Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism. - Plant Signal. Behav. 16: 1913306, 2021. Go to original source...
  25. Goswami M., Deka S.: Plant growth-promoting rhizobacteria - alleviators of abiotic stresses in soil: a review. - Pedosphere 30: 40-61, 2020. Go to original source...
  26. Gulen H., Eris A.: Effect of heat stress on peroxidase activity and total protein content in strawberry plants. - Plant Sci. 166: 739-744, 2004. Go to original source...
  27. Guo Q, Li Y., Lou Y et al.: Bacillus amyloliquefaciens Ba13 induces plant systemic resistance and improves rhizosphere micro ecology against tomato yellow leaf curl virus disease. - Appl. Soil Ecol. 137: 154-166, 2019. Go to original source...
  28. Haase M., Fitze G.: HSP90AB1: Helping the good and the bad. - Gene 575: 171-186, 2016. Go to original source...
  29. Hahn A., Bublak D., Schleiff E., Scharf K.-D.: Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. - Plant Cell 23: 741-755, 2011. Go to original source...
  30. Haider S., Iqbal J., Naseer S. et al.: Unfolding molecular switches in plant heat stress resistance: a comprehensive review. - Plant Cell Rep. 41: 775-798, 2022. Go to original source...
  31. Hassan M.K., McInroy J.A., Kloepper J.W.: The interactions of rhizodeposits with plant growth-promoting rhizobacteria in the rhizosphere: a review. - Agriculture 9: 142, 2019. Go to original source...
  32. Hoffmann L., Ribeiro N.D., Rosa S.S. et al.: [Response of beans cultivars to high air temperature in the reproductive period.] - Ciênc. Rural 37: 1543-1548, 2007. [In Portuguese] Go to original source...
  33. Huang B.: Plant-Environment Interactions. 3rd Edition. Pp. 387. CRC Press, Boca Raton-London-New York 2006.
  34. Husain T., Fatima A., Suhel M. et al.: A brief appraisal of ethylene signaling under abiotic stress in plants. - Plant Signal. Behav. 15: 178205, 2020. Go to original source...
  35. Ibarra-Villarreal A.L., Gándara-Ledezma A., Godoy-Flores A.D. et al.: Salt-tolerant Bacillus species as a promising strategy to mitigate the salinity stress in wheat (Triticum turgidum subsp. durum). - J. Arid Environ. 186: 104399, 2021. Go to original source...
  36. Izquierdo J.A., Hosfield G.L.: A collection receptacle for field abscission studies in common bean. - Crop Sci. 21: 622-625, 1981. Go to original source...
  37. Jabborova D.P., Narimanov A.A., Enakiev Y.I., Davranov K.D.: Effect of Bacillus subtilis 1 strain on the growth and development of wheat (Triticum aestivum L.) under saline condition. - Bulg. J. Agric. Sci. 26: 744-747, 2020.
  38. Khan M.A., Asaf S., Khan A.L. et al.: Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1. - Ann. Microbiol. 69: 797-808, 2019. Go to original source...
  39. Khan M.A., Asaf S., Khan A.L. et al.: Thermotolerance effect of plant growth promoting Bacillus cereus SA1 on soybean during heat stress. - BMC Microbiol. 20: 175, 2020. Go to original source...
  40. Kozeko L.Y.: The role of HSP90 chaperones in stability and plasticity of ontogenesis of plants under normal and stressful conditions (Arabidopsis thaliana). - Cytol. Genet. 53: 143-161, 2019. Go to original source...
  41. Kumar A., Prakash A., Johri B.N.: Bacillus as PGPR in crop ecosystem. - In: Maheshwari D. (ed.): Bacteria in Agrobiology: Crop Ecosystems. Pp. 37-59. Springer, Berlin-Heidelberg 2011. Go to original source...
  42. Lastochkina O.: Bacillus subtilis-mediated abiotic stress tolerance in plants. - In: Islam M., Rahman M., Pandey P. et al. (ed.): Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol. Bacilli in Climate Resilient Agriculture and Bioprospecting. Pp. 97-133. Springer, Cham 2019. Go to original source...
  43. Lima B.C., Moro A.L., Pacheco A.C.P. et al.: Bacillus subtilis ameliorates water stress tolerance in maize and common bean. - J. Plant Interact. 14: 432-439, 2019. Go to original source...
  44. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
  45. Lucon C.M.M., Akamatsu M.A., Harakava R.: [Growth promotion and damping-off control of cucumber seedling by rhizobacteria.] - Pesqui. Agropecu. Bras. 43: 691-697, 2008. [In Portuguese] Go to original source...
  46. Maghsoudi K., Emam Y., Niazi A. et al.: P5CS expression level and proline accumulation in the sensitive and tolerant wheat cultivars under control and drought stress conditions in the presence/absence of silicon and salicylic acid. - J. Plant Interact. 13: 461-471, 2018. Go to original source...
  47. Makky M., Paschalidis K.A., Soni P. et al.: A new rapid gas chromatographic method for ethylene, respirational, and senescent gaseous production of climacteric fruits stored in prolonged low temperature. - In: International Conference on Agricultural, Environmental and Biological Sciences (AEBS-2014), April 24-25, 2014, Phuket, Thailand. Pp. 11-16. International Institute of Chemical, Biological and Environmental Engineering, Phuket 2014.
  48. Mendis H.C., Thomas V.P., Schwientek P. et al.: Strain-specific quantification of root colonization by plant growth promoting rhizobacteria Bacillus firmus I-1582 and Bacillus amyloliquefaciens QST713 in non-sterile soil and field conditions. - PLoS ONE 13: e0193119, 2018. Go to original source...
  49. Misra S., Chauhan P.S.: ACC deaminase-producing rhizosphere competent Bacillus spp. mitigate salt stress and promote Zea mays growth by modulating ethylene metabolism. - 3 Biotech 10: 119, 2020. Go to original source...
  50. Mittler R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  51. Morgan P.W., He C.J., De Greef J.A., De Proft M.P.: Does water deficit stress promote ethylene synthesis by intact plants? - Plant Physiol. 94: 1616-1624, 1990. Go to original source...
  52. Mukhtar T., Rehman S., Smith D. et al.: Mitigation of heat stress in Solanum lycopersicum L. by ACC-deaminase and exopolysaccharide producing Bacillus cereus: effects on biochemical profiling. - Sustainability 12: 2159, 2020. Go to original source...
  53. Nazir S., Jan H., Tungmunnithum D. et al.: Callus culture of basil is an effective biological system for the production of antioxidants. - Molecules 25: 4859, 2020. Go to original source...
  54. Peksen E.: Non-destructive leaf area estimation model for faba bean (Vicia faba L.). - Sci. Hortic.-Amsterdam 113: 322-328, 2007. Go to original source...
  55. Poveda J., González-Andrés F.: Bacillus as a source of phytohormones for use in agriculture. - Appl. Microbiol. Biot. 105: 8629-8645, 2021. Go to original source...
  56. Rainey K.M., Griffiths P.D.: Diallel analysis of yield components of snap beans exposed to two temperature stress environments. - Euphytica 142: 43-53, 2005. Go to original source...
  57. Saini N., Nikalje G.C., Zargar S.M., Suprasanna P.: Molecular insights into sensing, regulation and improving of heat tolerance in plants. - Plant Cell Rep. 41: 799-813, 2022. Go to original source...
  58. Samakovli D., Tichá T., ©amaj J.: HSP90 chaperones regulate stomatal differentiation under normal and heat stress conditions. - Plant Signal. Behav. 15: 1789817, 2020. Go to original source...
  59. Sharma A., Shahzad B., Rehman A. et al.: Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. - Molecules 24: 2452, 2019. Go to original source...
  60. Silva D.A., Pinto-Maglio C.A.F., Oliveira É.C.: Influence of high temperature on the reproductive biology of dry edible bean (Phaseolus vulgaris L.). - Sci. Agric. 77: e20180233, 2020. Go to original source...
  61. Silveira P.M., Braz A.J.B.P., Didonet A.D.: [Chlorophyll meter to evaluate the necessity of nitrogen in dry beans.] - Pesqui. Agropecu. Bras. 38: 1083-1087, 2003. [In Portuguese] Go to original source...
  62. Singh P., Pandey S.S., Dubey B.K. et al.: Salt and drought stress tolerance with increased biomass in transgenic Pelargonium graveolens through heterologous expression of ACC deaminase gene from Achromobacter xylosoxidans. - Plant Cell Tiss. Org. Cult. 147: 297-311, 2021. Go to original source...
  63. Singh R., Pandey N., Naskar J., Shirke P.A.: Physiological performance and differential expression profiling of genes associated with drought tolerance in contrasting varieties of two Gossypium species. - Protoplasma 252: 423-438, 2015. Go to original source...
  64. Song Z., Pan F., Yang C. et al.: Genome-wide identification and expression analysis of HSP90 gene family in Nicotiana tabacum. - BMC Genet. 20: 35, 2019. Go to original source...
  65. Subramanian P., Krishnamoorthy R., Chanratana M. et al.: Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in psychrotolerant bacteria modulates ethylene metabolism and cold induced genes in tomato under chilling stress. - Plant Physiol. Biochem. 89: 18-23, 2015. Go to original source...
  66. Suzuki K., Takeda H., Tsukaguchi T., Egawa Y.: Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress. - Sex. Plant Reprod. 13: 293-299, 2001. Go to original source...
  67. Theocharis A., Bordiec S., Fernandez O. et al.: Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. - Mol. Plant Microbe Interact. 25: 241-249, 2012. Go to original source...
  68. Tittabutr P., Piromyou P., Longtonglang A. et al.: Alleviation of the effect of environmental stresses using co-inoculation of mungbean by Bradyrhizobium and rhizobacteria containing stress-induced ACC deaminase enzyme. - Soil Sci. Plant Nutr. 59: 559-571, 2013. Go to original source...
  69. Tiwari S., Prasad V., Chauhan P.S., Lata C.: Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. - Front. Plant Sci. 8: 1510, 2017. Go to original source...
  70. Tsukaguchi T., Kawamitsu Y., Takeda H. et al.: Water status of flower buds and leaves as affected by high temperature in heat-tolerant and heat-sensitive cultivars of snap bean (Phaseolus vulgaris L.). - Plant Prod. Sci. 6: 24-27, 2003. Go to original source...
  71. Vilas Boas E.V.B.: Frutos climatéricos e não climatéricos: implicações na pós colheita. [Climacteric and non-climacteric fruits: postharvest implications.] - In: Simpósio de controle de doenças de plantas 2. [Disease control symposium of plants 2.] Pp. 9-23. UFLA, Lavras 2002. [In Portuguese]
  72. Wang W., Wu Z., He Y. et al.: Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. - Ecotox. Environ. Safe. 164: 520-529, 2018. Go to original source...
  73. Woo O.-G., Kim H., Kim J.-S. et al.: Bacillus subtilis strain GOT9 confers enhanced tolerance to drought and salt stresses in Arabidopsis thaliana and Brassica campestris. - Plant Physiol. Biochem. 148: 359-367, 2020. Go to original source...
  74. Yuan L., Tang L., Zhu S. et al.: Influence of heat stress on leaf morphology and nitrogen-carbohydrate metabolisms in two wucai (Brassica campestris L.) genotypes. - Acta Soc. Bot. Pol. 86: 3554, 2017. Go to original source...
  75. Zhang X.L., Wu Q., Tao Y. et al.: ANACO044 is associated with P reutilization in P deficient Arabidopsis thaliana root cell wall in an ethylene dependent manner. - Environ. Exp. Bot. 185: 104386, 2021. Go to original source...
  76. Zhou Y., Xu F., Shao Y., He J.: Regulatory mechanisms of heat stress response and thermomorphogenesis in plants. - Plants-Basel 11: 3410, 2022. Go to original source...
  77. Zhu T., Deng X., Zhou X. et al.: Ethylene and hydrogen peroxide are involved in brassinosteroid-induced salt tolerance in tomato. - Sci. Rep.-UK 6: 35392, 2016. Go to original source...