Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (12): 2636-2647    DOI: 10.1016/S2095-3119(18)62039-8
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
The role of rhizobacteria in rice plants: Growth and mitigation of toxicity
Marcela C F Rêgo1, Aline F Cardoso1, Thayná da C Ferreira1, Marta C C de Filippi2, Telma F V Batista1, Rafael G Viana1, Gisele B da Silva1
1 Plant Protection Laboratory, Institute of Agrarian Sciences, Federal Rural University of Amazon, Belém 066.077-830, Brazil
2 Phytopathology Laboratory, Brazilian Enterprise for Agricultural Research-Rice and Beans, Goiânia 75375-000, Brazil
Download:  PDF (4500KB) ( )  
Export:  BibTeX | EndNote (RIS)      

Allelopathic compounds reduce the growth and productivity of upland rice plants, especially in consecutive plantations.
The rhizobacteria Pseudomonas fluorescens BRM-32111 and Burkholderia pyrrocinia BRM-32113 have been recorded as
growth promoters in rice. This study was developed to understand the effect of the application of rhizobacteria on upland
rice plants in consecutive plantations. Experiments were conducted in a completely randomized design with four replications
of four treatments: rice seed inoculated with P. fluorescens BRM-32111, rice seed inoculated with B. pyrrocinia BRM-32113
(both sown on soil with rice residue), non-inoculated plants sown on soil with rice residue (control with residue (WR)), and
non-inoculated plants on soil with no residue (NR). Roots and seedling growth were adversely affected by allelopathic
compounds in control WR plants. Plants inoculated with rhizobacteria P. fluorescens BRM-32111 or B. pyrrocinia BRM-32113
induced an increase of 88% in biomass, 3% in the leaf area, 40% in length, 67% in root biomass, 21% in chlorophyll a,
53% in chlorophyll (a+b), 50% in rate of carbon assimilation (A), 227% in A/rubisco carboxylation efficiency (Ci) and 63%
in water use efficiency (WUE) compared to control WR plants. These results indicate that rhizobacteria P. fluorescens
BRM-32111 and B. pyrrocinia BRM-32113 increase the tolerance of rice plants to stress from allelochemicals. There are
possible practical agricultural applications of these results for mitigating the effects of environmental allelochemistry on
upland rice.

Keywords:  allelopathy        B. pyrrocinia        P. fluorescens        rhizobacteria        rice  
Received: 13 January 2017   Accepted:
Fund: The authors thank the National Council for Scientific and Technological Development, Brazil, the Amazon Research Foundation, Brazil, and the Rural Federal University of Amazon, Brazil for the research funding and the Brazilian Federal Agency for the Support and Evaluation of Graduate Education for the grant of a doctorate scholarship.
Corresponding Authors:  Correspondence Marcela C F Rêgo, E-mail:   
About author:  TIAN Zhong-wei, Tel: +86-25-84399623, E-mail:;

Cite this article: 

Marcela C F Rêgo, Aline F Cardoso, Thayná da C Ferreira, Marta C C de Filippi, Telma F V Batista, Rafael G Viana, Gisele B da Silva. 2018. The role of rhizobacteria in rice plants: Growth and mitigation of toxicity. Journal of Integrative Agriculture, 17(12): 2636-2647.

Amb M B, Ahluwalia A S. 2016. Allelopathy: Potential role to achieve new milestones in rice cultivation. Rice Science, 23, 165–183.
Bach E, Seger G D S, Fernandes G C, Lisboa B B, Passaglia L M P. 2016. Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Applied Soil Ecology, 99, 141–149.
Bais H P, Weir T L, Perry L G, Gilroy S, Vivanco J M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233–266. 
Barazani O, Friedman J. 1999. Allelopathic bacteria and their impact on higher plants. Critical Reviews in Plant Sciences, 18, 741–755.
Barto E K, Hilker M, Mueller F, Mohney B K, Weidenhamer J D, Rillig M C. 2011. The fungal fast lane: Common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS ONE, 62, 71–95.
Barto E K, Weidenhamer J D, Cipollini D, Rillig M C. 2012. Fungal superhighways: Do common mycorrhizal networks enhance below ground communication? Trends in Plant Science, 17, 633–637.
Baziramakenga R, Leroux G D, Simard R R. 1995. Effects of benzoic and cinnamic acids on membrane permeability of soybean roots. Journal of Chemical Ecology, 21, 1271–1285.
Bhadoria P. 2011. Allelopathy: A natural way towards weed management. American Journal of Experimental Agriculture, 1, 7–20.
Bornman J F, Vogelmann T C. 1991. Effect of UV-B radiation on leaf opticalproperties measured with fiber optics. Journal of Experimental Botany, 42, 547–554.
Bueno A C S O, Castro G L S, Silva Junior D D, Pinheiro H A, Filippi M C C, Silva G B. 2017. Response of photosynthesis and chlorophyll a fluorescence in leaf scald-infected rice under influence of rhizobacteria and silicon fertilizer. Plant Pathology (Print), 66, 1487–1495.
Chou C H, Chang F J, Oka H I. 1991. Allelopathic potential of wild rice, Oryza perennis. Taiwania, 36, 201–210.
Chou C H, Lin H J. 1976. Autoinhibition mechanism of Oryza sativa: 1. Phytotoxic effect of decomposing rice residue in soil. Journal of Chemical Ecology, 2, 253–367.
Van Dam N M, Bouwmeester H J. 2016. Metabolomics in the rhizosphere: Tapping into belowground chemical communication. Trends in Plant Sciences, 21, 256–265.
Dwivedi P C, Rao K G. 1972. Electron donor - acceptor complexes of N-phenyl-2-naphthylamine with quinones. Indian Journal of Chemistry, 10, 944–945.
Egerton-Warburton L M, Querejeta J I, Allen M F. 2007. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. Journal of Experimental Botany, 58, 1473–1483.
Einhellig F A. 1996. Interactions involving allelopathy in cropping systems. Agronomy Journal, 88, 886–893.
Fageria N K, Baligar V C. 2003. Upland rice and allelopathy. Communications in Soil Science and Plant Analysis, 34, 1313–1329.
Filippi M C C, Silva G B, Silva-Lobo V, Côrtes M V C B, Moraes A J G, Prabhu A S. 2011. Leaf blast (Magnaporthe oryzae) suppression and growth promotion by rhizobacteria on aerobic rice in Brazil. Biological Control, 58, 160–166.
Galmés J, Flexas J, Savé R, Medrano H. 2007. Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant and Soil, 290, 139–155.
Gimsing A L, Baelum J, Dayan F E, Locke M A, Sejero L H, Jacobsen C S. 2009. Mineralization of the allelochemical sorgoleone in soil. Chemosphere, 76, 1041–1047.
Guckert A, Breisch H, Reisinger O. 1975. Electron-microscopic study on interrelation of mucigel, clay ans microorganisms. Soil Biology & Biochemistry, 7, 241–250.
Hauser S. 1993. Effect of Acioa barteri, Cassia siamea, Flemingia macrophylla and Gmelina arborea leaves on germination and early development of maize and cassava. Agriculture, Ecosystems & Environment, 45, 263–273.
Ihsan M Z, Khaliq A, Mahmood A, Naeem M, El-Nakhalawy F, Alghabari F. 2015. Field evaluation of allelopatic plant extracts alongside herbicides on weed management indices and weed-crop regression analysis in maize. Weed Biology and Management, 15, 78–86.
Inderjit, Wardle D A, Karban R, Cllaway R M. 2011. The ecosystem and evolutionary contexts of allelopathy. Trends in Ecology & Evolution, 26, 655–662.
Khalil Z, Helme T L R D. 1999. Free radicals contribute to the reduction in peripheral vascular responses and the maintenance of thermal hyperalgesia in rats with chronic constriction injury. Pain, 79, 31–37.
Kiers E T, Denison R F. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annual Review of Ecology, Evolution and Systematics, 39, 215–236.
Kloepper J W, Leong J, Teintze M, Schrot M N. 1980. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature, 286, 885–886.
Kremer R J. 2006. The role of allelopathic bacteria in weed management. In: Inderjit X, Mukerji K G, eds., Allelochemicals: Biological Control of Plant Pathogens and Diseases. Springer Netherlands Press, Dordrecht. pp. 143–155.
Lehman M E, Blum U. 1999. Evaluation of ferulic acid uptake as a measurement of allelochemical dose: Effective concentration. Journal of Chemical Ecology, 25, 2585–2600.
Major J, Rondon M, Molina D, Riha S J, Lehmann J. 2010. Maize yield and nutrition during 4 years after biochar application to a Colombian savanna oxisol. Plant and Soil, 333, 117–128.
Marenco R A, Santos A M B. 1999. Crop rotation reduces weed competition and increases chlorophyll concentration and yield of rice. Pesquisa Agropecuaria Brasileira, 34, 1881–1887.
McPherson J K, Chou C H, Muller C H. 1971. Allelopathic constituents of the chaparral shrub (Adenostoma fasciculatum). Phytochemistry, 10, 2925–2933.
Millar K D L, Johnson C M, Edelmann, Kiss J K. 2011. An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology, 11, 787–797.
Minnocci A, Panicucci A, Sebastiani L, Lorenzini G, Vitagliano C. 1999. Physiological and morphological responses of olive plants to ozone exposure during a growing season. Tree Physiology, 19, 391–397.
Mishra S, Nautiyal C S. 2012. Reducing the allelopathic effect of Parthenium hysterophorus L. on wheat (Triticum aestivum L.) by Pseudomonas putida. Plant Growth Regulation, 66, 155–165.
Mishra S, Upadhyay R S, Nautiyal C S. 2013. Unravelling the beneficial role of microbial contributors in reducing the allelopathic effects of weeds. Applied Microbiology and Biotechnology, 97, 5659–5668.
Nascente A S, Filippi M C C, Lanna A C, Souza A C A, Silva Lobo V L, Silva G B. 2016. Biomass, gas exchange, and nutrient contents in upland rice plants affected by application forms of microorganism growth promoters. Environmental Science and Pollution Research International, 24, 2956–2965.
Niinemets Ü. 2001. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 82, 453–469.
Pinheiro B S, Castro E M, Guimaraes C M. 2006. Sustainability and profitability of aerobic rice production in Brazil. Field Crops Research, 97, 34–42.
Porra R J, Thompson W A, Kriedemann P E. 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. Biochem Biophys Acta, 975, 384–394.
Putnam A R. 1988. Allelochemicals from plants as herbicides. Weed Technology, 2, 510–518.
Qian H F, Xu X Y, Chen W, Jiang H, Jin Y X, Liu W P, Fu Z W. 2009. Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere, 75, 368–375.
Ranagalage A S, Jayakody T S D, Wathugala D L. 2014. Allelopathic potential of rice residues of selected rice varieties (Oryza sativa L.) against echinochloa crus-galli. Journal of Tropical Forestry and Environment, 4, 24–30.
Rêgo M C F, Ilkiu-Borges F, Filippi M C C, Gonçalves L A, Silva G B. 2014. Morphoanatomical and biochemical changes in the roots of rice plants induced by plant growth-promoting microorganisms. Journal of Botany, 2014, 1–10.
Rice E L. 1984. Allelopathy. 2nd ed. Academic Press Inc., Orlando, Florida. p. 422.
Sack L, Grubb P J, Marañón T. 2003. The functional morphology of juvenile plants tolerant of strong summer drought in shaded forest understories in southern Spain. Plant Ecology, 68, 139–163.
Shibu J, Andrew R G. 1998. Allelopathy in black walnut (Juglans nigra L.) alley cropping. II. Effects of juglone on hydroponically grown corn (Zea mays L.) and soybean (Glycine max L. Merr.) growth and physiology. Plant and Soil, 203, 199–205.
Torres A, Olivia R M, Castellano D, Cross P. 1996. A science of the future. In: Proceedings of the 1st World Congress on Allelopathy. University of Cadiz, Cadiz, Spain. p. 278.
Uddin M R, Park S U, Dayan F E, Pyon J Y. 2014. Herbicidal activity offormulated sorgoleone, a natural product of sorghum root exudate. Pest Management Science, 70, 252–257.
Venturi V, Keel C. 2016. Signaling in the rhizosphere. Trends in Plant Sciences, 21, 187–198.
Wathugala D L, Ranagalage A S. 2015. Comparison of allelopathic potential of Sri Lankan varieties (Oryza sativa L.) as an indicator plant. International Journal of Agriculture Innovations and Research, 3, 1473–2319.
Weir C J, Ling A T, Belelli D, Wildsmith J A, Peters J A, Lambert J J. 2004. The interaction of anaesthetic steroids with recombinant glycine and GABAA receptors. British Journal of Anaesthesia, 92, 704–711.
Wright I J, Westoby M. 2002. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist, 155, 403–416.
Wu H, Pratley J, Lemerled D, Haig T. 1999. Crop cultivars with allelopathic capability. Weed Research, 39, 171–180.
Wu Z, Yang L, Wang R, Zhang Y, Shang Q, Wang L. 2015. In vitro study of the growth, development and pathogenicity responses of Fusarium oxysporum to phthalic acid, an autotoxin from Lanzhou lily. World Journal of Microbiology & Biotechnology, 31, 1227–1234.
Yu G R, Kobayashi T, Zhuang J. Wang Q F, Qu L Q. 2003. A coupled model of photosynthesis-transpiration based on the stomatal behavior for maize (Zea mays L.) grown in the field. Plant and Soil, 249, 401–415.
Zou S P, Li X W, Ma Y Q, Yang S Y. 2014. Soil microbes are linked to the allelopathic potential of different wheat genotypes. Plant and Soil, 378, 49–58.
[1] GAO Peng, ZHANG Tuo, LEI Xing-yu, CUI Xin-wei, LU Yao-xiong, FAN Peng-fei, LONG Shi-ping, HUANG Jing, GAO Ju-sheng, ZHANG Zhen-hua, ZHANG Hui-min. Improvement of soil fertility and rice yield after long-term application of cow manure combined with inorganic fertilizers[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2221-2232.
[2] GAO Zhi-ping, XU Min-li, ZHANG Hai-zi, LÜ Chuan-gen, CHEN Guo-xiang. Photosynthetic properties of the mid-vein and leaf lamina of field-grown, high-yield hybrid rice during senescence[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1913-1926.
[3] TIAN Chang, SUN Ming-xue, ZHOU Xuan, LI Juan, XIE Gui-xian, YANG Xiang-dong, PENG Jian-wei. Increase in yield and nitrogen use efficiency of double rice with long-term application of controlled-release urea[J]. >Journal of Integrative Agriculture, 2022, 21(7): 2106-2118.
[4] ZHOU Tian-yang, LI Zhi-kang, LI En-peng, WANG Wei-lu, YUAN Li-min, ZHANG Hao, LIU Li-jun, WANG Zhi-qin, GU Jun-fei, YANG Jian-chang. Optimization of nitrogen fertilization improves rice quality by affecting the structure and physicochemical properties of starch at high yield levels[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1576-1592.
[5] Christian Adler PHARES, Selorm AKABA. Co-application of compost or inorganic NPK fertilizer with biochar influenced soil quality, grain yield and net income of rice[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3600-3610.
[6] Muhammad Amjad BASHIR, ZHAI Li-mei, WANG Hong-yuan, LIU Jian, Qurat-Ul-Ain RAZA, GENG Yu-cong, Abdur REHIM, LIU Hong-bin. Apparent variations in nitrogen runoff and its uptake in paddy rice under straw incorporation[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3356-3367.
[7] HUANG Li-ying, Li Xiao-xiao, ZHANG Yun-bo, Shah FAHAD, WANG Fei. dep1 improves rice grain yield and nitrogen use efficiency simultaneously by enhancing nitrogen and dry matter translocation[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3185-3198.
[8] CHEN Zhong-du, LI Feng-bo, XU Chun-chun, JI Long, FENG Jin-fei, FANG Fu-ping. Spatial and temporal changes of paddy rice ecosystem services in China during the period 1980–2014[J]. >Journal of Integrative Agriculture, 2022, 21(10): 3082-3093.
[9] CHEN Yun-feng, XIA Xian-ge, HU Cheng, LIU Dong-hai, QIAO Yan, LI Shuang-lai, FAN Xian-peng. Effects of long-term straw incorporation on nematode community composition and metabolic footprint in a rice–wheat cropping system[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2265-2276.
[10] LIN Fa-ming, LI Shen, WANG Ke, TIAN Hao-ran, GAO Jun-feng, DU Chang-qing. Receptor-like kinase OsASLRK regulates methylglyoxal response and content in rice[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1731-1742.
[11] SHI Min, Krishna P. PAUDEL, CHEN Feng-bo. Mechanization and efficiency in rice production in China[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1996-2008.
[12] ZHANG Jing, ZHANG Yan-yan, SONG Ning-yuan, CHEN Qiu-li, SUN Hong-zheng, PENG Ting, HUANG Song, ZHAO Quan-zhi. Response of grain-filling rate and grain quality of mid-season indica rice to nitrogen application[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1465-1473.
[13] WU Qiong, WANG Yu-hui, DING Yan-feng, TAO Wei-ke, GAO Shen, LI Quan-xin, LI Wei-wei, LIU Zheng-hui, LI Gang-hua. Effects of different types of slow- and controlled-release fertilizers on rice yield[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1503-1514.
[14] QU Xue, Daizo KOJIMA, Yukinaga NISHIHARA, WU La-ping, Mitsuyoshi ANDO. Can harvest outsourcing services reduce field harvest losses of rice in China?[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1396-1406.
[15] ZHANG Chuan-hong, Wandella Amos BENJAMIN, WANG Miao. The contribution of cooperative irrigation scheme to poverty reduction in Tanzania[J]. >Journal of Integrative Agriculture, 2021, 20(4): 953-963.
No Suggested Reading articles found!