PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2024.5.893eng

UDC: 631.171

Acknowledgements:
Supported financially by the Russian Science Foundation in accordance with agreement No. 23-26-10050 dated 04.20.2023 (grant No. 23-26-10050) and the St. Petersburg Science Foundation in accordance with agreement dated 05.05.2023 No. 23-26-10050

 

BIOELETROGENESIS IN THE ROOT ENVIRONMENT OF LEAF, FRUIT AND ROOT VEGETABLE CROPS

T.E. Kuleshova, E.M. Ezerina, V.E. Vertebny, Yu.V. Khomyakov, N.G. Sinyavina, G.G. Panova

Agrophysical Research Institute, 14, Grazhdanskii prosp., St. Petersburg, 195220 Russia, e-mail kuleshova@agrophys.ru (✉ corresponding author), lehzerina@yandex.ru, soilchem@yandex.ru, himlabafi@yandex.ru, sinad@inbox.ru, gaiane@inbox.ru

ORCID:
Kuleshova T.E. orcid.org/0000-0003-3802-2494
Khomyakov Yu.V. orcid.org/0000-0002-9149-3247
Ezerina E.M. orcid.org/0009-0008-8243-2435
Sinyavina N.G. orcid.org/0000-0003-0378-7331
Vertebny V.E. orcid.org/0000-0002-2936-5949
Panova G.G. orcid.org/0000-0002-1132-9915

Final revision received May 02, 2024
Accepted July 18, 2024

Bioelectrogenic processes occurring in the root environment of plants associated with the generation of potential difference during oxidation-reduction reactions and ion diffusion that accompany the development of the root system serve as a basis for creating alternative devices for obtaining renewable environmentally friendly resource-saving energy — bioelectrochemical systems (BES). The search for biocompatible, energy-generating, high-performance BES components, including technical elements, root environments and plants is an urgent task, the solution of which will increase the autonomy and efficiency of plant production. At present, there are practically no BES developments based on vegetable crops, or unsuccessful attempts to create them have been reported. In the presented work, for the first time in a comprehensive study of electrogenic processes in original root environment-vegetable plants BES, more stability of electrical properties is shown in lettuce (leaf crop), higher electricity output in small radish (root crop) and longer electricity generation in tomato (fruit vegetable crop). The aim of the work was to measure a set of parameters – electrogenic properties of the root environment, reflectance and fluorescence spectra of leaves, morphometric indicators, biochemical composition, characterizing the efficiency of electricity generation, the ability to convert light energy, yield and quality of plant products obtained when growing various vegetable crops in bioelectrochemical systems. The phytotest objects were lettuce (Lactuca sativa L.) variety Ballet, small radish (Raphanus sativus L.) cultivar Peterburgskiy fioletovyy and dwarf tomato (Solanum lycopersicum L.) variety Natasha. The plants were grown in 2023-2024 under controlled conditions of intensive light culture at the agrobiological testing ground of the FGBNU AFI with controlled microclimate conditions. The light sources were our own AFI-5000 LED lamps simulating sunlight, and the root environment was peat soil. The nutrition was carried out with Knop's solution. The BES was a growing container with a biocompatible corrosion-resistant system of electrodes made of a porous conductive material, providing superficial electrical contact with the root and its environment. The volume of the BES was 440 cm3 for lettuce, 320 cm3 for small radish and 3000 cm3 for tomato. Electrodes of 6½6 cm in size were placed horizontally in the root environment. To form the root crop, the upper electrode was modified by adding a round hole of 3 cm in diameter. The potential difference was recorded automatically every 15 min using an automated voltmeter (Arduino, Arduino Software, China). Polarization curves were recorded at the end of the vegetation period of lettuce and radish and on the 64th day of tomato cultivation. Lettuce and radish plants were harvested on day 28, tomato on 110 day from sowing the seeds. During harvesting, the weight of leaves, fruits and roots, the height of the above-ground part of plants and the yield were taken into account. The biochemical composition (the content of dry matter, nitrates, sugars, vitamin C, pigments, macro- and microelements) was determined by generally accepted methods (thermogravimetric, ionometric, titrimetric, photometric). The photosynthetic activity indices (spectra of radiation reflected from the leaf surface and fluorescence parameters) were estimated non-invasively using a spectrometric system («Ocean Optics», USA) and fluorimeter MINI-PAM-II («Heinz Walz GmbH», Germany). The average potential difference formed in the root environment of lettuce plants was 289±27 mV, the maximum value reached 391 mV. For small radish plants, the potential difference in the root environment averaged 394±50 mV with a maximum value of 532 mV. The average potential difference in the root environment of tomato was 257±123 mV: during the initial development of the aboveground mass and roots, a stable voltage generation of 317±17 mV was observed, but during the fruit filling phase, the potential difference dropped to 120±34 mV, and during the transition to the ripening phase, a reverse increase to 340±74 mV was observed. The overall productivity of the studied crops when grown taking into account the possible number of harvests from one tier per year was similar, 73.5±10.3 kg/m2 for lettuce, 68.6±3.8 kg/m2 for radish and 71.2±9.2 kg/m2 for tomato, and exceeded that when grown in standard systems for lettuce and tomato. The quality of plant products corresponded the sanitary and hygienic requirements of the Russian Federation. Thus, the nitrate content in lettuce leaves was 1597.0±214.7 mg/kg fresh weight (FW) (MPC 2000 mg/kg FW), in radish taproots 1206.0±144.8 mg/kg FW (MPC 1500 mg/kg FW), and in tomato fruits 70.2±9.3 mg/kg FW (MPC 300 mg/kg FW). The sum of sugars reached 13.0±1.2; 29.6±2.9 and 32.1±3.7 % of dry matter (DW), respectively, vitamin C reached 12.9±1.6; 7.7±0.7 and 17.4±2.1 mg/100 g FW. The content of chlorophylls and carotenoids in tomato plant leaves was 98 and 84 % higher than in lettuce leaves and 52 and 61 % higher than in small radish leaves. Of the studied parameters of photosynthetic activity, the light scattering index R800 and the effective quantum yield Y(II) were most closely related to the intensity of electrogenic processes. Thus, leaf crops have the most stable electrical properties, root crops provide a higher output of electrical energy, and fruit crops allow for longer-term generation of electricity. Our findings indicate the possibility of obtaining high yields of high-quality plant products, including commercial root vegetables, when growing plants in a BES.

Keywords: Lactuca sativa L., Raphanus sativus L., Solanum lycopersicum L., bioelectrochemical systems, biocompatible electrodes, fluorescence, reflectance indices, productivity, biochemical composition.

 

REFERENCES

  1. Kuleshova T.E., Galushko A.S., Panova G.G., Volkova E.N., Apollon W., Shuang Ch., Sevda S. Bioelectrochemical systems based on the electroactivity of plants and microorganisms in the root environment (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2022, 57(3): 425-440 CrossRef
  2. Winaikij P., Sreearunothai P., Sombatmankhong K. Probing mechanisms for microbial extracellular electron transfer (EET) using electrochemical and microscopic characterisations. Solid State Ionics, 2018, 320: 283-291 CrossRef
  3. Tongphanpharn N., Guan C.Y., Chen W.S., Chang C.C., Yu C.P. Evaluation of long-term performance of plant microbial fuel cells using agricultural plants under the controlled environment. Clean Technologies and Environmental Policy, 2023, 25(2): 633-644 CrossRef
  4. Guan C.Y., Yu C.P. Evaluation of plant microbial fuel cells for urban green roofs in a subtropical metropolis. Science of the Total Environment, 2021, 765: 142786 CrossRef
  5. Regmi R., Nitisoravut R., Charoenroongtavee S., Yimkhaophong W., Phanthurat O. Earthen pot—plant microbial fuel cell powered by Vetiver for bioelectricity production and wastewater treatment. CLEAN Soil, Air, Water, 2018, 46(3): 1700193 CrossRef
  6. Arulmani S.R.B., Gnanamuthu H.L., Kandasamy S., Govindarajan G., Alsehli M., Elfasakhany A., Zhang H. Sustainable bioelectricity production from Amaranthus viridis and Triticum aestivum mediated plant microbial fuel cells with efficient electrogenic bacteria selections. Process Biochemistry, 2021, 107: 27-37 CrossRef
  7. Sarma P.J., Mohanty K. Epipremnum aureum and Dracaena braunii as indoor plants for enhanced bio-electricity generation in a plant microbial fuel cell with electrochemically modified carbon fiber brush anode. Journal of Bioscience and Bioengineering, 2018, 126(3): 404-410 CrossRef
  8. Bhattacharya R., Parthasarthy V., Bose D., Gulia K., Srivastava S., Roshan K.R., Shankar R. Overview of the advances in plant microbial fuel cell technology for sustainable energy recovery from rhizodeposition. Biotechnology and Bioengineering, 2023, 120(6): 1455-1464 CrossRef
  9. Sophia A.C., Sreeja S. Green energy generation from plant microbial fuel cells (PMFC) using compost and a novel clay separator. Sustainable Energy Technologies and Assessments, 2017, 21: 59-66 CrossRef
  10. Hu J., Yang Z., Huang Z., Li H., Wu Z., Zhang X., Qin X., Li C., Ruan M., Zhou K., Wu, X., Zhang Y., Xiang Y., Huang J. Co-composting of sewage sludge and Phragmites australis using different insulating strategies. Waste Management, 2020, 108: 1-12 CrossRef
  11. Di L., Li Y., Nie L., Wang S., Kong F. Influence of plant radial oxygen loss in constructed wetland combined with microbial fuel cell on nitrobenzene removal from aqueous solution. Journal of Hazardous Materials, 2020, 394: 122542 CrossRef
  12. Sato C., Apollon W., Luna-Maldonado A. I., Paucar N. E., Hibbert M., Dudgeon J. Integrating microbial fuel cell and hydroponic technologies using a ceramic membrane separator to develop an energy—water—food supply system. Membranes, 2023, 13(9): 803-824 CrossRef
  13. Lepikash R., Lavrova D., Stom D., Meshalkin V., Ponamoreva O., Alferov S. State of the art and environmental aspects of plant microbial fuel cells’ application. Energies, 2024, 17(3): 752 CrossRef
  14. Bataillou G., Ondel O., Haddour N. 900-Days long term study of plant microbial fuel cells and complete application for powering wireless sensors, Journal of Power Sources, 2024, 593: 233965  CrossRef
  15. Lu Z., Yin D., Chen P., Wang H., Yang Y., Huang G., Cai L., Zhang L. Power-generating trees: Direct bioelectricity production from plants with microbial fuel cells. Applied Energy, 2020, 268: 115040 CrossRef
  16. Osorio-de-la-Rosa E., Valdez-Hernández M., Vázquez-Castillo J., Franco-de-la-Cruz A., Woo-García R., Castillo-Atoche A., La-Rosa R. Plant microbial fuel cells as a bioenergy source used in precision beekeeping. Sustainable Energy Technologies and Assessments, 2023, 60: 103499 CrossRef
  17. Maddalwar S., Nayak K.K., Singh L. Evaluation of power generation in plant microbial fuel cell using vegetable plants. Bioresource Technology Reports, 2023, 22: 101447 CrossRef
  18. Sinyavina N.G., Kochetov A.A., Kocherina N.V., Egorova K.V., Kurina A.B., Panova G.G., Chesnokov Y.V. Breeding approaches for controlled conditions of artificial light culture for small radish and radish (Raphanus sativus L.). Horticulturae, 2023, 9(6): 678 CrossRef
  19. Kochetov A.A., Sinyavina N.G. Patent na selektsionnoe dostizhenie 11518 RF. Redis Raphanus sativus var. sativus Peterburgskiy fioletovyy. FGBNU Agrofizicheskiy nauchno-issledovatel’skiy institut. Zayavka № 8058521. Data prioriteta. 28.11.2019. Vydan 25.03.2021 [Patent for selection achievement 11518 RF. Radish Raphanus sativus var. sativus Petersburg purple. FGBNU Agrophysical Research Institute. Appl. 8058521. Priority date. 11/28/2019. Issued 03/25/2021](in Russ.).
  20. Panova G.G., Udalova O.R., Kanash E.V., Galushko A.S., Kochetov A.A., Priyatkin N.S., Arkhipov M.V., Chernousov I.N. Fundamentals of physical modeling of “ideal” agroecosystems. Technical Physics, 2020, 65: 1563-1569 CrossRef
  21. Kuleshova T.E., Gall’ N.R. Pochvovedenie, 2021, 3: 338-346 CrossRef (in Russ.).
  22. Ermakov A.I., Arasimovich V.V., Yarosh N.P., Peruanskiy Yu.V., Lukovnikova G.A., Smirnova-Ikonnikova M.I. Metody biokhimicheskogo issledovaniya rasteniy [Methods of biochemical research of plants].Leningrad, 1987 (in Russ.).
  23. Rukovodstvo po metodam analiza kachestva i bezopasnosti pishchevykh produktov /Pod redaktsiey Skurikhina I.M., Tutel’yana V.A. [Guide to methods of analysis of food quality and safety. Skurikhin I.M., Tutel’yan V.A. (eds.)]. Moscow, 1998 (in Russ.).
  24. MINI-PAM Photosynthesis Yield Analyzer. Manual. Edition 3. Heinz Walz GmbH, Effeltrich, Germany, 2018.
  25. Wang S., Gariepy Y., Adekunle A., Raghavan V. External resistance as a potential tool for bioelectricity and methane emission control from rice plants in hydroponic microbial fuel cell. Fuel, 2024, 368: 131431 CrossRef
  26. Holland B.L., Monk N.A.M., Clayton R.H., Osborne C.P. A theoretical analysis of how plant growth is limited by carbon allocation strategies and respiration. In Silico Plants, 2019, 1(1): diz004 CrossRef
  27. Apal’ko A.D., Kondrat’ev V.M., Osipova G.S. Vestnik Studencheskogo nauchnogo obshchestva, 2017, 8(1): 91-92 (in Russ.).
  28. Balashova I.T., Sirota S.M., Pinchuk E.V., Vershinina N.P., Sivochenko S.P. Ovoshchi Rossii, 2020, 1: 29-34 CrossRef (in Russ.).
  29. SanPiN 2.3.2.1078-01. Gigienicheskie trebovaniya k bezopasnosti i pishchevoy tsennosti pishchevykh produktov. 06.11.2001 [SanPiN 2.3.2.1078-01. Hygienic requirements for the safety and nutritional value of food products. 11/06/2001].
  30. Osipova G.S., Apal’ko A.D., Kondrat’ev V.M. Nauchnyy vklad molodykh issledovateley v sokhranenie traditsiy i razvitie APK, 2016: 73-74 (in Russ.).
  31. Sinyavina N.G., Kochetov A.A., Khomyakov Yu.V., Kononchuk P.Yu., Vertebnyy V.E., Dubovitskaya V.I., Tkacheva A.Yu. Ovoshchi Rossii, 2019, 3: 35-39 CrossRef (in Russ.).
  32. Balashova I.T., Sirota S.M., Pinchuk E.V., Udalova O.R., Anikina L.M., Panova G.G. Materialy II Mezhdunarodnoy nauchnoy konferentsii posvyashchennoy pamyati akademika E.I. Ermakova «Tendentsii razvitiya agrofiziki: ot aktual’nykh problem zemledeliya i rastenievodstva k tekhnologiyam budushchego» [Proc. II Int. Conf. dedicated to the memory of Academician E.I. Ermakov «Trends in the development of agrophysics: from current problems of agriculture and plant growing to technologies of the future»]. St. Petersburg, 2019: 180-189 (in Russ.).
  33. Kuleshova T.E., Zhelnina A.I., Udalova O.R., Panova G.G., Gall’ N.R. Aktual’nye voprosy biologicheskoy fiziki i khimii, 2020, 5(3): 379-385 (in Russ.).
  34. Sims D.A., Gamon J.A. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing of Environment, 2002, 81(2-3): 337-354 CrossRef
  35. Peñuelas J., Filella I., Biel C., Serrano L., Save R. The reflectance at the 950-970 nm region as an indicator of plant water status. International Journal of Remote Sensing, 1993, 14(10): 1887-1905 CrossRef
  36. Gamon J.A., Serrano L., Surfus J.S. The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia, 1997, 112: 492-501 CrossRef
  37. Kitajima M., Butler W.L. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1975, 376(1): 105-115 CrossRef
  38. Genty B., Briantais J.-M., Baker N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) - General Subjects, 1989, 990(1): 87-92 CrossRef
  39. Bilger W., Björkman O. Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research, 1990, 25: 173-185 CrossRef
  40. Genty B., Harbinson J., Cailly A.L., Rizza F. Fate of excitation at PS II in leaves: the non-photochemical side. Proc. 3rd BBSRC Robert Hill Symposium on photosynthesis. B. Genty, J. Harbinson, A.L. Cailly, F. Rizza. University of Sheffield, Department of Molecular Biology and Biotechnology, Western Bank, Sheffield, UK, 1996: 28.
  41. Kanash E.V., Osipov Yu.A. Diagnostika fiziologicheskogo sostoyaniya i ustoychivosti rasteniy k deystviyu stressovykh faktorov sredy (na primere UF-V radiatsii). Metodicheskie rekomendatsii [Diagnostics of the physiological state and resistance of plants to the effects of environmental stress factors (using UV-B radiation as an example). Methodological recommendations]. St. Petersburg, 2008 (in Russ.).
  42. Fincheira P., Quiroz A., Tortella G., Diez M.C., Rubilar O. Current advances in plant-microbe communication via volatile organic compounds as an innovative strategy to improve plant growth. Microbiological Research, 2021, 247: 126726 CrossRef
  43. Kwon K.J., Park B.J. Efficiency of Spathiphyllum spp. as a plant-microbial fuel cell. Ornamental Horticulture, 2021, 27: 173-182 CrossRef
  44. Aulakh M., Wassmann R., Bueno C., Kreuzwieser J., Rennenberg H. Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biology, 2001, 3(2): 139-148 CrossRef
  45. Pamintuan K.R.S., Katipunana A.M.C., Palaganasa P.A.O., Caparangaa A.R. An analysis of the stacking potential and efficiency of plant-microbial fuel cells growing green beans (Vigna ungiculata ssp. sesquipedalis). International Journal of Renewable Energy Development, 2020, 9(3): 439-447 CrossRef

 

back

 


CONTENTS

 

Full article PDF (Eng)