β-Sitosterol differentially regulates key metabolites for growth improvement and stress tolerance in rice plants during prolonged UV-B stress

Shahzad R., Ewas M., Harlina P.W., Khan S.U., Zhenyuan P., Nie X., Nishawy E.

Department of Biotechnology, Faculty of Science and Technology, Universitas Muhammadiyah Bandung, Bandung, West Java 40614, Indonesia; National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China; Department of Plant Genetic Resources, Desert Research Center, Cairo, 11753, Egypt; Department of Food Technology, Faculty of Science and Technology, Universitas Muhammadiyah Bandung, Bandung, West Java 40614, Indonesia; Key Laboratory of Oasis Ecology Agricultural of Xinjiang Bingtuan, Agricultural College, Shihezi University, Shihezi, Xinjiang, 832003, China


Abstract

Background: Elevated ultraviolet-B (UV-B) radiation is potentially deleterious to many organisms specifically crop plants and has become a global challenge. Rice is an exceptionally important staple food which is grown worldwide, and many efforts have been done recently to improve rice varieties against UV-B stress. This current study aims to investigate the effects of exogenous application of β-sitosterol (βSito) on growth improvement and tolerance level of rice plants against prolonged UV-B stress. The physiological and metabolic responses were evaluated in rice plants not supplemented with βSito (Nβ) and those supplemented with βSito (Sβ). Results: The Nβ and Sβ plants were grown under non-stress (ns) and under prolonged UV-B stress (uvs) conditions and termed as Nβns, Sβns and Nβuvs, Sβuvs, respectively. The application of βSito contributes positively under non-stress and specifically to UV-B stress in terms of improving numerous physiological parameters associated with growth and development such as shoot and root length, RWC, whole plant biomass, chlorophyll pigments, and photosynthetic-related parameters (Pn, Gs, Tr, WUEi, Fv/Fm, and NPQ) in Sβ compared with Nβ plants. Moreover, enhanced oxidative stress tolerance of Sβuvs vs. Nβuvs plants under stress was attributed to low levels of ROS and substantial trigger in activities of antioxidant enzymes (SOD, POD, CAT, and APX). Metabolic analysis was performed using GC-TOFMS, which revealed higher accumulation of several key metabolites including organic acids, sugars, amino acids, and others in Sβuvs vs. Nβuvs plants, which were mainly reduced in Nβ plants under stress vs. non-stress conditions. Conclusion: These results provide useful data regarding the important role of βSito on growth maintenance and modulation of several metabolites associated with osmotic and redox adjustments during UV-B stress tolerance in rice plants. Importantly, βSito-regulated plasticity could further be explored specifically in relation to different environmental stresses in other economically useful crop plants. © 2021, The Author(s).

Metabolic analysis; Physiological response; Rice; UV-B stress; β-Sitosterol


Journal

Journal of Genetic Engineering and Biotechnology

Publisher: Springer Science and Business Media Deutschland GmbH

Volume 19, Issue 1, Art No 79, Page – , Page Count


Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85107338050&doi=10.1186%2fs43141-021-00183-6&partnerID=40&md5=529b0360fb661bf563cb28af51091a3c

doi: 10.1186/s43141-021-00183-6

Issn: 1687157X

Type: All Open Access, Gold, Green


References

Bais, A.F., Lucas, R.M., Bornman, J.F., Williamson, C.E., Sulzberger, B., Austin, A.T., Wilson, S.R., Heikkilä, A.M., Environmental effects of ozone depletion, UV radiation and interactions with climate change: UNEP Environmental Effects Assessment Panel, update 2017 (2018) Photochem Photobiol Sci, 17 (2), pp. 127-179; Fina, J., Casadevall, R., AbdElgawad, H., Prinsen, E., Markakis, M.N., Beemster, G.T.S., Casati, P., UV-B inhibits leaf growth through changes in growth regulating factors and gibberellin levels (2017) Plant Physiol, 174 (2), pp. 1110-1126; Biever, J.J., Brinkman, D., Gardner, G., UV-B inhibition of hypocotyl growth in etiolated Arabidopsis thaliana seedlings is a consequence of cell cycle arrest initiated by photodimer accumulation (2014) J Exp Bot, 65 (11), pp. 2949-2961; Robson, T.M., Aphalo, P.J., Species-specific effect of UV-B radiation on the temporal pattern of leaf growth (2012) Physiol Plant, 144 (2), pp. 146-160; González-Villagra, J., Marjorie, R.-D., Alberdi, M., Acevedo, P., Loyola, R., Tighe-Neira, R., Arce-Johnson, P., Inostroza-Blancheteau, C., Solar UV irradiation effects on photosynthetic performance, biochemical markers, and gene expression in highbush blueberry (Vaccinium corymbosum L.) cultivars (2020) Sci Hortic, 259, p. 108816; Mosadegh, H., Trivellini, A., Lucchesini, M., Ferrante, A., Maggini, R., Vernieri, P., Mensuali Sodi, A., UV-B physiological changes under conditions of distress and eustress in sweet basil (2019) Plants, 8 (10), p. 396; Robson, T.M., Klem, K., Urban, O., Jansen, M.A., Re-interpreting plant morphological responses to UV-B radiation (2015) Plant Cell Environ, 38 (5), pp. 856-866; Huang, H., Ullah, F., Zhou, D.-X., Yi, M., Zhao, Y., Mechanisms of ROS regulation of plant development and stress responses (2019) Front Plant Sci, 10 (800). , https://doi.org/10.3389/fpls.2019.00800; Mittler, R., ROS are good (2017) Trends Plant Sci, 22 (1), pp. 11-19; Ighodaro, O.M., Akinloye, O.A., First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid (2018) Alexandria J Med, 54 (4), pp. 287-293; Liu, Y., Liu, J., Abozeid, A., Wu, K.-X., Guo, X.-R., Mu, L.-Q., Tang, Z.-H., UV-B radiation largely promoted the transformation of primary metabolites to phenols in Astragalus mongholicus seedlings (2020) Biomolecules, 10 (4), p. 504; Peng, M., Shahzad, R., Gul, A., Subthain, H., Shen, S., Lei, L., Zheng, Z., Luo, J., Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance (2017) Nat Commun, 8 (1), p. 1975; Li, Z., Cheng, B., Yong, B., Liu, T., Peng, Y., Zhang, X., Ma, X., Nie, G., Metabolomics and physiological analyses reveal β-sitosterol as an important plant growth regulator inducing tolerance to water stress in white clover (2019) Planta, 250 (6), pp. 2033-2046; Bueno, P.C.P., Lopes, N.P., Metabolomics to characterize adaptive and signaling responses in legume crops under abiotic stresses (2020) ACS Omega, 5 (4), pp. 1752-1763; Rogowska, A., Szakiel, A., The role of sterols in plant response to abiotic stress (2020) Phytochem Rev, 19 (6), pp. 1525-1538; Elkeilsh, A., Awad, Y.M., Soliman, M.H., Abu-Elsaoud, A., Abdelhamid, M.T., El-Metwally, I.M., Exogenous application of β-sitosterol mediated growth and yield improvement in water-stressed wheat (Triticum aestivum) involves up-regulated antioxidant system (2019) J Plant Res, 132 (6), pp. 881-901; Salama, K.H.A., Mansour, M.M.F., Choline priming-induced plasma membrane lipid alterations contributed to improved wheat salt tolerance (2015) Acta Physiol Plant, 37 (8), p. 170; Griebel, T., Zeier, J., A role for β-sitosterol to stigmasterol conversion in plant–pathogen interactions (2010) Plant J, 63 (2), pp. 254-268; Piccini, C., Cai, G., Dias, M.C., Romi, M., Longo, R., Cantini, C., UV-B radiation affects photosynthesis-related processes of two Italian Olea europaea (L.) varieties differently (2020) Plants (Basel), 9 (12), p. 1712; Mmbando, G.S., Teranishi, M., Hidema, J., Very high sensitivity of African rice to artificial ultraviolet-B radiation caused by genotype and quantity of cyclobutane pyrimidine dimer photolyase (2020) Sci Rep, 10 (1), p. 3158; Zhang, F., Guo, H., Huang, J., Yang, C., Li, Y., Wang, X., Qu, L., Luo, J., A UV-B-responsive glycosyltransferase, OsUGT706C2, modulates flavonoid metabolism in rice (2020) Sci China Life Sci, 63 (7), pp. 1037-1052; Fang, C., Li, L., Zhang, P., Wang, D., Yang, L., Reza, B.M., Lin, W., Lsi1 modulates the antioxidant capacity of rice and protects against ultraviolet-B radiation (2019) Plant Sci, 278, pp. 96-106; Yun, H., Lim, S., Kim, Y.X., Lee, Y., Lee, S., Lee, D., Park, K., Sung, J., Diurnal changes in CN metabolism and response of rice seedlings to UV-B radiation (2018) J Plant Physiol, 228, pp. 66-74; Song, Y., Chen, Q., Ci, D., Shao, X., Zhang, D., Effects of high temperature on photosynthesis and related gene expression in poplar (2014) BMC Plant Biol, 14 (1), p. 111; Shahzad, R., Ahmed, F., Wang, Z., Harlina, P.W., Nishawy, E., Ayaad, M., Manan, A., Ewas, M., Comparative analysis of two phytochrome mutants of tomato (Micro-Tom cv.) reveals specific physiological, biochemical, and molecular responses under chilling stress (2020) J Genet Eng Biotechnol, 18 (1), p. 77; Rivero, R.M., Mestre, T.C., Mittler, R., Rubio, F., Garcia-Sanchez, F., Martinez, V., The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants (2014) Plant Cell Environ, 37 (5), pp. 1059-1073; Gururani, M.A., Ganesan, M., Song, I.-J., Han, Y., Kim, J.-I., Lee, H.-Y., Song, P.-S., Transgenic turfgrasses expressing hyperactive Ser599Ala phytochrome A mutant exhibit abiotic stress tolerance (2016) J Plant Growth Regul, 35 (1), pp. 11-21; Zhao, H., Ye, L., Wang, Y., Zhou, X., Yang, J., Wang, J., Cao, K., Zou, Z., Melatonin increases the chilling tolerance of chloroplast in cucumber seedlings by regulating photosynthetic electron flux and the ascorbate-glutathione cycle (2016) Front Plant Sci, 7 (1814). , https://doi.org/10.3389/fpls.2016.01814; Jadamba, C., Kang, K., Paek, N.-C., Lee, S.I., Yoo, S.-C., Overexpression of rice expansin7 (Osexpa7) confers enhanced tolerance to salt stress in rice (2020) Int J Mol Sci, 21 (2), p. 454; Poli, Y., Nallamothu, V., Balakrishnan, D., Ramesh, P., Desiraju, S., Mangrauthia, S.K., Voleti, S.R., Neelamraju, S., Increased catalase activity and maintenance of photosystem II distinguishes high-yield mutants from low-yield mutants of rice var. Nagina22 under low-phosphorus stress (2018) Front Plant Sci, 9, p. 1543; Soares, A.M.S., Oliveira, J.T.A., Gondim, D.M.F., Domingues, D.P., Machado, O.L.T., Jacinto, T., Assessment of stress-related enzymes in response to either exogenous salicylic acid or methyl jasmonate in Jatropha curcas L. leaves, an attractive plant to produce biofuel (2016) S Afr J Bot, 105, pp. 163-168; Soda, N., Gupta, B.K., Anwar, K., Sharan, A., Govindjee, S.-P.S.L., Pareek, A., Rice intermediate filament, OsIF, stabilizes photosynthetic machinery and yield under salinity and heat stress (2018) Sci Rep, 8 (1), p. 4072; Faseela, P., Puthur, J.T., Intraspecific variation in sensitivity of high yielding rice varieties towards UV-B radiation (2019) Physiol Mol Biol Plants, 25 (3), pp. 727-740; Hidema, J., Kumagai, T., Sensitivity of rice to ultraviolet-B radiation (2006) Ann Bot, 97 (6), pp. 933-942; Valitova, J., Renkova, A., Mukhitova, F., Dmitrieva, S., Beckett, R.P., Minibayeva, F.V., Membrane sterols and genes of sterol biosynthesis are involved in the response of Triticum aestivum seedlings to cold stress (2019) Plant Physiol Biochem, 142, pp. 452-459; Kumar, M.S.S., Ali, K., Dahuja, A., Tyagi, A., Role of phytosterols in drought stress tolerance in rice (2015) Plant Physiol Biochem, 96, pp. 83-89; Sieprawska, A., Filek, M., Tobiasz, A., Walas, S., Dudek-Adamska, D., Grygo-Szymanko, E., Trace elements’ uptake and antioxidant response to excess of manganese in in vitro cells of sensitive and tolerant wheat (2016) Acta Physiol Plant, 38 (2), p. 55; Cheng, Y., Chen, Y., Li, J., Qu, H., Zhao, Y., Wen, C., Zhou, Y., Dietary β-sitosterol improves growth performance, meat quality, antioxidant status, and mitochondrial biogenesis of breast muscle in broilers (2019) Animals, 9 (3), p. 71; Itam, M., Mega, R., Tadano, S., Abdelrahman, M., Matsunaga, S., Yamasaki, Y., Akashi, K., Tsujimoto, H., Metabolic and physiological responses to progressive drought stress in bread wheat (2020) Sci Rep, 10 (1), p. 17189; Darko, E., Végh, B., Khalil, R., Marček, T., Szalai, G., Pál, M., Janda, T., Metabolic responses of wheat seedlings to osmotic stress induced by various osmolytes under iso-osmotic conditions (2019) PLoS One, 14 (12); Neugart, S., Hideg, É., Czégény, G., Schreiner, M., Strid, Å., Ultraviolet-B radiation exposure lowers the antioxidant capacity in the Arabidopsis thaliana pdx1.3-1 mutant and leads to glucosinolate biosynthesis alteration in both wild type and mutant (2020) Photochem Photobiol Sci, 19 (2), pp. 217-228; Drincovich, M.F., Voll, L.M., Maurino, V.G., Editorial: On the diversity of roles of organic acids (2016) Front Plant Sci, 7 (1592). , https://doi.org/10.3389/fpls.2016.01592; Zhao, L., Huang, Y., Hu, J., Zhou, H., Adeleye, A.S., Keller, A.A., 1H NMR and GC-MS based metabolomics reveal defense and detoxification mechanism of cucumber plant under mano-Cu stress (2016) Environ Sci Technol, 50 (4), pp. 2000-2010; Khan, M.I.R., Asgher, M., Khan, N.A., Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.) (2014) Plant Physiol Biochem, 80, pp. 67-74; Panchal, P., Miller, A.J., Giri, J., Organic acids: versatile stress response roles in plants (2021) J Exp Bot, 20, p. erab019; Yu, J., Li, R., Fan, N., Yang, Z., Huang, B., Metabolic pathways involved in carbon dioxide enhanced heat tolerance in bermudagrass (2017) Front Plant Sci, 8 (1506). , https://doi.org/10.3389/fpls.2017.01506; Cho, H.Y., Loreti, E., Shih, M.C., Perata, P., Energy and sugar signaling during hypoxia (2021) New Phytol, 229 (1), pp. 57-63; Yang, L., Zhao, X., Zhu, H., Paul, M., Zu, Y., Tang, Z., Exogenous trehalose largely alleviates ionic unbalance, ROS burst, and PCD occurrence induced by high salinity in Arabidopsis seedlings (2014) Front Plant Sci, 5 (570). , https://doi.org/10.3389/fpls.2014.00570; Megguer, C.A., Fugate, K.K., Lafta, A.M., Ferrareze, J.P., Deckard, E.L., Campbell, L.G., Lulai, E.C., Finger, F.L., Glycolysis is dynamic and relates closely to respiration rate in stored sugarbeet roots (2017) Front Plant Sci, 8, p. 861; Kaur, G., Asthir, B., Proline: a key player in plant abiotic stress tolerance (2015) Biol Plant, 59 (4), pp. 609-619; Kaur, H., Mukherjee, S., Baluska, F., Bhatla, S.C., Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants (2015) Plant Signal Behav, 10 (11), pp. e1049788-e1104978; Pott, D.M., Osorio, S., Vallarino, J.G., From central to specialized metabolism: An overview of some secondary compounds derived from the primary metabolism for their role in conferring nutritional and organoleptic characteristics to fruit (2019) Front Plant Sci, 10 (835). , https://doi.org/10.3389/fpls.2019.00835; Zhuang, L., Yang, Z., Fan, N., Yu, J., Huang, B., Metabolomic changes associated with elevated CO2-regulation of salt tolerance in Kentucky bluegrass (2019) Environ Exp Bot, 165, pp. 129-138; Nocchi, N., Duarte, H.M., Pereira, R.C., Konno, T.U.P., Soares, A.R., Effects of UV-B radiation on secondary metabolite production, antioxidant activity, photosynthesis and herbivory interactions in Nymphoides humboldtiana (Menyanthaceae) (2020) J Photochem Photobiol B, 212, p. 112021

Indexed by Scopus

Leave a Comment