Effect of combination of Azolla microphylla and As(V)-resistant bacterial consortium on growth, oxidative stress and arsenic accumulation in rice plant under As(V) stress

, , , ,


Research Articles | Published:

Print ISSN : 0970-4078.
Online ISSN : 2229-4473.
Website:www.vegetosindia.org
Pub Email: contact@vegetosindia.org
Doi: 10.1007/s42535-022-00345-y
First Page: 796
Last Page: 802
Views: 789


Keywords: Azolla microphylla , Arsenic, Reactive oxygen species, Lipid peroxidation


Abstract


Arsenic (As) pollution in paddy fields is a major environmental threat in many parts of South Asia. In the present study we have explored the role of Azolla microphylla in conjunction with an arsenate [As(V)]-resistant bacterial consortium in modulating the growth and As accumulation in rice plant exposed to 7 mg/l of As(V) stress. The bacterial strains used in consortium show plant growth promoting traits such as siderophore production, phosphate solubilisation and indole acetic acid production. Under As(V) stress, the rice plant exhibited symptoms of phytotoxicity in the form of reduced shoot length or plant height, panicle formation, photosynthetic ability and increased generation of the reactive oxygen species (H2O2) and biological peroxidation of membranes. These effects were alleviated when the rice plant was exposed to As(V) stress in presence of the Azolla microphylla-bacterial consortium combination, causing a marked improvement in physical growth parameters such as shoot length and panicle count, and up to 20.7 and 13% increase in total chlorophyll and carotenoid contents respectively. Oxidative stress was also alleviated, as indicated by 58.5 and 26.7% reduction in endogenous H2O2 content and lipid peroxidation respectively. The residual concentration of As in the soil used for rice paddy cultivation was found to be 25% lesser in the set containing Azolla-bacterial consortium combination than that of the set lacking this combination. The uptake of As in shoot of rice plant was also significantly lesser in the set treated with this Azolla-bacterial consortium and followed the order: leaves > grain. Thus, such a combination of the bio-fertilizer Azolla microphylla and As(V)-resistant plant growth promoting bacterial consortium is capable of alleviating As(V)-induced phytotoxicity in rice plant, with simultaneous reduction in As accumulation in grains, thereby showing potential for use in As-bioremediation in the As-polluted rice paddy fields.



                Azolla microphylla
              , Arsenic, Reactive oxygen species, Lipid peroxidation


*Get Access

(*Only SPR Members can get full access. Click Here to Apply and get access)

Advertisement

References


Abedin J, Cresser M, Meharg AA, Feldmann J, Cotter-Howells J (2002a) Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ Sci Technol 36:962–968


Abedin MJ, Feldmann J, Meharg AA (2002b) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128


Abraham G (2011) Antioxidant enzyme status in Azolla microphylla in relation to salinity and possibilities of environmental monitoring. Thin Solid Films 519:1240–1243


Ames B, Shigenaga M, Hagen T (1993) Oxidants, antioxidants and the degenerative diseases of ageing. Proc Natl Acad Sci 90:7915–7922


Bhowmick S, Pramanik S, Singh P, Mondal P, Chatterjee D, Nriagu J (2018) Arsenic in groundwater of West Bengal, India: a review of human health risks and assessment of possible intervention options. Sci Total Environ 612:148–169


Dai L, Xiong Z, Huang Y, Li M (2006) Cadmium-induced changes in pigments, total phenolics and phenylalanine ammonia-lyase activity in fronds of Azolla imbricata. Environ Toxicol 21:505–512


Dean RT, Gieseg S, Davies M (1993) Reactive species and their accumulation on radical-damaged proteins. Trends Biochem Sci 18:437–441


Dubey RS (2018) Photosynthesis in plants under stressful conditions. Handbook of photosynthesis. CRC Press, Boca Raton, pp 629–649


Edge R, Truscott TG (1999) Carotenoid radicals and the interaction of carotenoids with active oxygen species. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The phytochemistry of carotenoids. Kluwer, Dordrecht, pp 223–234


Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:81–96


Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930


Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: 1. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198


Juhasz AL, Smith E, Weber J, Rees M, Rofe A, Kuchen T, Sansom L, Naidu R (2006) Invivo assessment of arsenic bioavailability in rice and its significance for human health risk assessment. Environ Health Perspect 114:1826–1831


Kalita J, Pradhan AK, Shandilya ZM, Tanti B (2018) Arsenic stress responses and tolerance in rice: physiological, cellular and molecular approaches. Rice Sci 25:235–249


Meharg AA (1994) Relationship between plant phosphorous status and the kinetics of arsenate influx in clones of Deschampsia cespitosa (L.) Beauv. that differ in their tolerance to arsenate. Plant Soil 162:99–106


Meharg AA (2004) Arsenic in rice—understanding a new disaster for South-East Asia. Trends Plant Sci 9:229–234


Meharg AA, Rahman M (2003) Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ Sci Technol 37:229–234


Meharg AA, Witaker MJH (2002) Arsenic uptake and metabolism in arsenic plant species. New Phytol 154:29–43


Montillet JL, Chamnongpol S, Rusterucci C, van de Dat B, Agnel JP, Battesti C, Inze D, van Breusegem F, Triantaphylides C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138:1516–1526


Neill SO, Gould KS (2003) Anthocyanins in leaves: light attenuators or antioxidants. Funct Plant Biol 30:865–873


Nookongbut P, Kantachote D, Megharaj M, Naidu R (2018) Reduction in arsenic toxicity and uptake in rice (Oryza sativa L.) by As-resistant purple nonsulfur bacteria. Environ Sci Pollut Res 25:36530–36544


Panaullah GM, Alam T, Hossain MB, Loeppert RH, Lauren JG, Meisner CA, Ahmed ZU, Duxbury JM (2009) Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh. Plant soil 317:31–39


Pandey C, Gupta M (2015) Selenium and auxin mitigates arsenic stress in rice (Oryza sativa L.) by combining the role of stress indicators, modulators and genotoxicity assay. J Hazard Mater 287:384–391


Pillai PK, Premlatha S, Rajamony S (2002) Azolla—a sustainable feed substitute for livestock, vol 4. LEISA India, p 15


Polle A, Rennenberg H (1993) Significance of antioxidants in plant adaptation to environmental stress. In: Fowden L, Mansfield T, Stoddart J (eds) Plant adaptation to environmental stress. Chapman & Hall, London, p 263


Porra RJ, Thompson WA, Kriedmann 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. Biochem Biophys Acta 975:384–394


Rahman MA, Hasegawa H, Rahman MM, Islam MN, Miah MAM, Tasmen A (2007) Effect of arsenic on growth, photosynthesis and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemos 67:1072–1079


Stone R (2008) Arsenic and paddy rice: a neglected cancer risk? Science 321:184–185


Talukder ASMHM, Meisner CA, Sarkar MAR, Islam MS, Sayre KD (2014) Effects of water management, arsenic and phosphorus levels on rice yield in high-arsenic soil-water system. Rice Sci 21:99–107


Upadhyaya H, Shome S, Roy D, Bhattacharya MK (2014) Arsenic induced changes in growth and physiological responses in Vigna radiata seedling: effect of curcumin interaction. Am J Plant Sci 5:3609


Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain treated bean plants. Plant Sci 151:59–66


Viveros GS, Cerrato RF, Alarcon A (2011) Short-term effects of arsenate-induced toxicity on growth, chlorophyll and carotenoid contents and total content of phenolic compounds in Azolla filliculoides. Water Air Soil Pollut 217:455–462


Wagner G (1997) Azolla: a review of its biology and utilization. Bot Rev 63:1–26


Yadav RK, Abraham G, Singh YV, Singh PK (2014) Advancements in the utilization of Azolla–Anabaena system in relation to sustainable agricultural practices. Proc Indian Natl Sci Acad 80:301–316


Zhang X, Lin AJ, Zhao FJ, Xu GZ, Duan GL, Zhu YG (2008) Arsenic accumulation by the aquatic fern Azolla: comparison of arsenic uptake, speciation and efflux by Azolla caroliniana and Azolla filiculoides. Environ Pollut 156:1149–1155


Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A, Meharg AA, Williams PN (2008a) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42:5008–5013


Zhu YG, Williams PN, Meharg AA (2008b) Exposure to inorganic arsenic from rice: a global health issue? Environ Pollut 154:169–171

 


Acknowledgements


The authors would like to acknowledge the financial aid from West Bengal Department of Science & Technology and Biotechnology.


Author Information


Agnihotri Puja
Department of Microbiology, St. Xavier’s College, Kolkata, India
puja.agnihotri001@gmail.com
Sikdar Suchismita
Department of Microbiology, St. Xavier’s College, Kolkata, India


Maitra Madhumita
Department of Microbiology, St. Xavier’s College, Kolkata, India


Choudhury Sudeshna Shyam
Department of Microbiology, St. Xavier’s College, Kolkata, India


Mitra Arup Kumar
Department of Microbiology, St. Xavier’s College, Kolkata, India