Research Papers

A Novel Approach for Screening Salinity-Tolerant Rice Germplasm by Exploring Redox-Regulated Cytological Fingerprint

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  • Plant Physiology and Biochemistry Research Laboratory, Centre for Advanced Study, University Grants Commission of India, Department of Botany, University of Burdwan, Burdwan 713104, India

Received date: 2024-05-16

  Accepted date: 2024-11-29

  Online published: 2025-04-14

Abstract

Although metabolic homeostasis disruption, cellular damage, and premature senescence caused by salinity stress are well-documented in the literature, there are few studies investigating cytological changes induced by salinity stress within the altered metabolic landscape of rice, and this study aims to fill that gap. The cytological characterization of root tips (in terms of mitotic index and chromosomal abnormalities such as stickiness, laggards, fragments, bridges, micronuclei, ring chromosomes, and total mitotic abnormalities) was conducted on 10 experimental rice landraces from coastal Bangladesh, grown under post-imbibitional salinity stress (PISS), while correlating these changes with their metabolic status. The results revealed a strong correlation between salinity-induced cytological changes in root cells (mitotic index and chromosomal abnormalities) and the redox interactome status of all experimental rice landraces. The landraces Kutepatnai, Talmugur, Nonakochi, and Benapol, which exhibited a higher ability to mitigate PISS-induced chromosomal abnormalities and improve mitotic index, also showed lower accumulation of oxidative stress markers (protein carbonylation, lipid peroxidation, prooxidant accumulation, oxidative stress index, reactive oxygen species (ROS)-antioxidative stress index, and efficiency of ROS processing via the Halliwell-Asada pathway) compared with more susceptible landraces (Charobalam, Jotaibalam, Kachra, and Lalmota). These findings underscore the role of redox biology in preventing chromotoxic effects under salinity stress. Hierarchical cluster analysis and principal component analysis, used to determine variations and similarities among the experimental rice landraces based on cytological attributes, redox interactome, and physiological phenotypes, classified the landraces according to their salinity tolerance and sensitivity. This study proposes a novel approach for exploring redox-regulated cytological fingerprints as a tool for identifying salinity-tolerant rice landraces.

Cite this article

Uthpal Krishna Roy, Babita Pal, Soumen Bhattacharjee . A Novel Approach for Screening Salinity-Tolerant Rice Germplasm by Exploring Redox-Regulated Cytological Fingerprint[J]. Rice Science, 2025 , 32(2) : 228 -242 . DOI: 10.1016/j.rsci.2025.03.006

References

[1] Ali Q, Ahmar S, Sohail M A, et al. 2021. Research advances and applications of biosensing technology for the diagnosis of pathogens in sustainable agriculture. Environ Sci Pollut Res, 28(8): 9002-9019.
[2] Badr A. 1986. Effects of the s-triazine herbicide turbutryn on mitosis, chromosomes and nucleic acids in root tips of Vicia faba. Cytologia, 51(3): 571-577.
[3] Baranova E N, Gulevich A A. 2021. Asymmetry of plant cell divisions under salt stress. Symmetry, 13(10): 1811.
[4] Barrôco R M, Van Poucke K, Bergervoet J H W, et al. 2005. The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol, 137(1): 127-140.
[5] Bhattacharjee M. 2014. Studies on mitodepressive effect of Indigocarmine. Int J Innovative Sci Eng Technol, 1: 157-160.
[6] Bhattacharjee S. 2008. Calcium-dependent signaling pathway in the heat-induced oxidative injury in Amaranthus lividus. Biol Plant, 52(1): 137-140.
[7] Bhattacharjee S. 2019. ROS and oxidative stress:Origin and implication. In: Reactive Oxygen Species in Plant Biology. New Delhi, India: Springer: 1-31.
[8] Bose M L, Isa MA, Bayes A, et al. 2001. Impact of modern rice varieties on food security and cultivar diversity: the Bangladesh case. In: Peng S, Hardy B. Rice Research for Food Security and Poverty Alleviation. Manila, the Philippines: IRRI publication: 617-630.
[9] Buege J A, Aust S D. 1978. Microsomal lipid peroxidation. Methods Enzymol, 52: 302-310.
[10] Chaitanya K K, Naithani S C. 1994. Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn. f. New Phytologist, 126(4): 623-627.
[11] Chao B F, Wu Y H, Li Y S. 2008. Impact of artificial reservoir water impoundment on global sea level. Science, 320: 212-214.
[12] Chen H H, Shen Z Y, Li P H. 1982. Adaptability of crop plants to high temperatures Stress. Crop Sci, 22(4): 719-725.
[13] Elsheery N I, Helaly M N, El-Hoseiny H M, et al. 2020. Zinc oxide and silicone nanoparticles to improve the resistance mechanism and annual productivity of salt-stressed mango trees. Agronomy, 10(4): 558.
[14] Farheen J, Mansoor S. 2020. Cytogenetic impact of sodium chloride stress on root cells of Vigna radiata L. seedlings. Turk J Biochem, 45(2): 143-150.
[15] Fick N G, Qualset C D. 1975. Genetic control of plant amylase activity. Proc Natl Acad Sci, 72: 852-862.
[16] Ghosh S, Mistri B. 2020. Drainage induced waterlogging problem and its impact on farming system: A study in Gosaba Island, Sundarban, India. Spatial Inf Res, 28(6): 709-721.
[17] Haque A, Ali M A, Waxuddin M, et al. 1976. Squashmethod for the mitotic chromosomes of grasses. Curr Sci, 43: 382-383.
[18] Hazmana M, Hause B, Eiche E, et al. 2016. Different forms of osmotic stress evokes qualitatively different responses in rice. Plant Physiol, 202: 45-56.
[19] Heath R L, Packer L. 1968. Photo-oxidation in isolated chloroplasts: kinetics and stoichiometry of fatty acid oxidation. Arch Biochem Biophys, 125(1): 189-198.
[20] Hernández J A, Almansa M S. 2002. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. J Plant Physiol, 115(2): 251-257.
[21] Horemans N, Foyer C H, Asard H. 2000. Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci, 5(6): 263-267.
[22] Hossain A, El Sabagh A, Bhatt R, et al. 2021. Consequences of salt and drought stresses in rice and their mitigation strategies through intrinsic biochemical adaptation and applying stress regulators. In: Fahad S, Sönmez O, Saud S, et al. Sustainable Soil and Land Management and Climate Change. Florida, USA: CRC Press: 1-15.
[23] Hossain M A, Ismail M R, Uddin M K, et al. 2013. Efficacy of ascorbate-glutathione cycle for scavenging H2O2 in two contrasting rice genotypes during salinity stress. Aust J Crop Sci, 7(12): 1801-1808.
[24] Hossen M S, Karim M F, Fujita M, et al. 2022. Comparative physiology of indica and Japonica rice under salinity and drought stress: An intrinsic study on osmotic adjustment, oxidative stress, antioxidant defense and methylglyoxal detoxification. Stresses, 2(2): 156-178.
[25] Hussain S, Zhang J H, Zhong C, et al. 2017. Effects of salt stress on rice growth, development characteristics, and the regulating ways: A review. J Integr Agric, 16(11): 2357-2374.
[26] Ismail A M, Heuer S, Thomson M J, et al. 2007. Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol, 65(4): 547-570.
[27] Jiang M Y, Zhang J H. 2001. Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol, 42(11): 1265-1273.
[28] Jiang W, Liu D. 2000. Effects of Pb2+ on root growth, cell division, and nucleolus of Zea mays L. Bull Environ Contam Toxicol, 65(6): 786-793.
[29] Kato T A, Haskins J S. 2023. Mitotic index analysis. Methods Mol Biol, 2519: 17-26.
[30] Kesawat M S, Satheesh N, Kherawat B S, et al. 2023. Regulation of reactive oxygen species during salt stress in plants and their crosstalk with other signaling molecules-current perspectives and future directions. Plants, 12(4): 864.
[31] Kiełkowska A. 2017. Cytogenetic effect of prolonged in vitro exposure of Allium cepa L. root meristem cells to salt stress. Cytol Genet, 51(6): 478-484.
[32] Kitsios G, Doonan J H. 2011. Cyclin dependent protein kinases and stress responses in plants. Plant Signal Behav, 6(2): 204-209.
[33] Kononenko N V, Dilovarova T A, Kanavsky R V, et al. 2019. Evaluation of morphological and biochemical resistance parameters to chloride salination in different wheat genotypes. RUDN J Agron Anim Ind, 14(1): 18-39.
[34] Li J Y, Jiang A L, Zhang W. 2007. Salt stress-induced programmed cell death in rice root tip cells. J Integr Plant Biol, 49(4): 481-486.
[35] Lim C B, Prêle C M, Baltic S, et al. 2015. Mitochondria- derived reactive oxygen species drive GANT61-induced mesothelioma cell apoptosis. Oncotarget, 6(3):1519-1530.
[36] Lisa L A, Seraj Z I, Fazle Elahi C M, et al. 2004. Genetic variation in microsatellite DNA, physiology and morphology of coastal saline rice (Oryza sativa L.) landraces of Bangladesh. Plant Soil, 263(1): 213-228.
[37] Lubini G, Fachinetto J M, Laughinghouse H D, et al. 2008. Extracts affecting mitotic division in root-tip meristematic cells. Biologia, 63(5): 647-651.
[38] Luo L Z, Werner K M, Gollin S M, et al, 2004. Cigarette smoke induces anaphase bridges and genomic imbalances in normal cells. Mutat Res Fundam Mol Mech Mutagen, 554(1/2): 375-385.
[39] MacNevin W M, Urone P F. 1953. Separation of hydrogen peroxide from organic hydroperoxides. Anal Chem, 25(11): 1760-1761.
[40] Mensor L L, Menezes F S, Leitão G G, et al. 2001. Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytother Res, 15(2): 127-130.
[41] Miller G, Suzuki N, Ciftci-Yilmaz S, et al. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ, 33(4): 453-467.
[42] Moradi F, Ismail A M. 2007. Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot, 99(6): 1161-1173.
[43] Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol, 22(5): 867-880.
[44] Nefic H, Musanovic J, Metovic A, et al. 2013. Chromosomal and nuclear alterations in root tip cells of Allium cepa L. induced by alprazolam. Med Arch, 67(6): 388-392.
[45] Noctor G, Reichheld J P, Foyer C H. 2018. ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol, 80: 3-12.
[46] Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolff S P. 1994. Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenylphosphine. Anal Biochem, 220(2): 403-409.
[47] Palmer R G, Heer H. 1973. A root tip squash technique for soybean Chromosomes. Crop Sci, 13(3): 389-391.
[48] Park H J, Kim W Y, Yun D J. 2016. A new insight of salt stress signaling in plant. Mol Cells, 39(6): 447-459.
[49] Patterson J C, Joughin B A, van de Kooij B, et al. 2019. ROS and ooxidative stress are eelevated in mitosis during aasynchronous ccell cycle pprogression and aare eexacerbated by mitotic aarrest, Cell Systems, 8(02): 163-167.e2.
[50] Peterman T K, Siedow J N. 1985. Immunological comparison of lipoxygenase isozymes-1 and -2 with soybean seedling lipoxygenases. Arch Biochem Biophys, 238(2): 476-483.
[51] Qin J, Dong W Y, He K N, et al. 2010. NaCl salinity-induced changes in water status, ion contents and photosynthetic properties of Shepherdia argentea (Pursh) Nutt. seedlings. Plant Soil Environ, 56(7): 325-332.
[52] Radić S, Prolić M, Pavlica M, et al. 2005. Cytogenetic effects of osmotic stress on the root meristem cells of Centaurea ragusina L. Environ Exp Bot, 54(3): 213-218.
[53] Rahman M A, Thomson M J, Shah-E-Alam M, et al. 2016. Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization. Ann Bot, 117(6): 1083-1097.
[54] Rank J, Lopez L C, Nielsen M H, et al. 2002. Genotoxicity of maleic hydrazide, acridine and DEHP in Allium cepa root cells performed by two different laboratories. Hereditas, 136(1): 13-18.
[55] Rubio-Casal A E, Castillo J M, Luque C J, et al. 2003. Influence of salinity on germination and seeds viability of two primary colonizers of Mediterranean salt pans. J Arid Environ, 53(2): 145-154.
[56] Ryu H, Cho Y G. 2015. Plant hormones in salt stress tolerance. J Plant Biol, 58(3): 147-155.
[57] Saleem M H, Ali S, Hussain S, et al. 2020. Flax (Linum usitatissimum L.): A potential candidate for phytoremediation? Biological and economical points of view. Plants, 9(4): 496.
[58] Saleh A K, Shaban A S, Diab M A, et al. 2023. Green synthesis and characterization of aluminum oxide nanoparticles using Phoenix dactylifera seed extract along with antimicrobial activity, phytotoxicity, and cytological effects on Vicia faba seeds. Biomass Conv Bioref, 14: 31859-31875.
[59] Sapkota A. 2002. Chromosomal mutation: Causes, mechanism, types, examples. In: Russel P J. Genetics. San Francisco, USA: Pearson Education Inc: 595-621.
[60] Schaedle M, Bassham J A. 1977. Chloroplast glutathione reductase. Plant Physiol, 59(5): 1011-1012.
[61] Shaban A S, Safhi F A, Fakhr M A, et al. 2023. Comparison of the Morpho-physiological and molecular responses to salinity and alkalinity stresses in rice. Plants, 13(1): 60.
[62] Simontacchi M, Caro A, Fraga C G, et al. 1993. Oxidative stress affects α-tocopherol content in soybean embryonic axes upon imbibition and following germination. Plant Physiol, 103(3): 949-953.
[63] Singh D, Roy B K. 2016. Salt stress affects mitotic activity and modulates antioxidant systems in onion roots. Braz J Bot, 39(1): 67-76.
[64] Tajbakhsh M, Zhou M X, Chen Z H, et al. 2006. Physiological and cytological response of salt-tolerant and non-tolerant barley to salinity during germination and early growth. Aust J Exp Agric, 46(4): 555-562.
[65] Teixeira S B, Pires S N, Ávila G E, et al. 2018. Cytogenetic activity of root meristems of rice in response to conditioning in carrot extract and salinity. J Exp Agric Int, 24(5): 1-12.
[66] Tobe K, Zhang L P, Omasa K. 2003. Alleviatory effects of calcium on the toxicity of sodium, potassium and magnesium chlorides to seed germination in three non-halophytes. Seed Sci Res, 13(1): 47-54.
[67] Türkoğlu S. 2008. Evaluation of genotoxic effects of sodium propionate, calcium propionate and potassium propionate on the root meristem cells of Allium cepa. Food Chem Toxicol, 46(6): 2035-2041.
[68] Vázquez-Ramos J M,de la Paz Sánchez M. 2003. The cell cycle and seed germination. Seed Sci Res, 13(2): 113-130.
[69] Wang W D, Sheng X Y, Shu Z F, et al. 2016. Combined cytological and transcriptomic analysis reveals a nitric oxide signaling pathway involved in cold-inhibited Camellia sinensis pollen tube growth. Front Plant Sci, 7: 456.
[70] Xu Y M, Bu W C, Xu Y C, et al. 2024. Effects of salt stress on physiological and agronomic traits of rice genotypes with contrasting salt tolerance. Plants, 13(8): 1157.
[71] Yildiz M, Ciğerci I H, Konuk M, et al. 2009. Determination of genotoxic effects of copper sulphate and cobalt chloride in Allium cepa root cells by chromosome aberration and comet assays. Chemosphere, 75(7): 934-938.
[72] Zhang X, Yin H B, Chen S H, et al. 2014. Changes in antioxidant enzyme activity and transcript levels of related genes in Limonium sinense Kuntze seedlings under NaCl stress. J Chem, 2014: 749047.
[73] Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167(2): 313-324.
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