Cloning of a CHS gene of Poncirus trifoliata and its expression in response to soil water deficit and arbuscular mycorrhizal fungi
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
36605949
PubMed Central
PMC9807919
DOI
10.3389/fpls.2022.1101212
Knihovny.cz E-resources
- Keywords
- arbuscular mycorrhiza, chalcone synthase, drought, flavonoid, trifoliate orange,
- Publication type
- Journal Article MeSH
Flavonoids are secondary metabolites widely found in plants with antioxidants, of which chalcone synthase (CHS) is a key enzyme required in flavonoid synthesis pathways. The objective of this study was to clone a CHS gene from trifoliate orange (Poncirus trifoliata) and analyze its biological information and partial functions. A PtCHS gene (NCBI accession: MZ350874) was cloned from the genome-wide of trifoliate orange, which has 1156 bp in length, encoding 391 amino acids, with a predicted protein relative molecular mass of 42640.19, a theoretical isoelectric point of 6.28, and a lipid coefficient of 89.82. The protein is stable, hydrophilic, and high sequence conservation (92.49% sequence homology with CHS gene of other species). PtCHS was highly expressed in stems, leaves and flowers, but very low expression in roots and seeds. Soil water deficit could up-regulate expressions of PtCHS in leaves. An arbuscular mycorrhizal fungus, Funneliformis mosseae, significantly increased plant biomass production, CHS activity, expressions of PtCHS, and total flavonoid content in leaves and roots, independent of soil water status. Total flavonoids were significantly positively correlated with PtCHS expression in leaves only and also positively with root mycorrhizal colonization. Such results provide insight into the important functions of PtCHS in trifoliate orange.
Botany and Microbiology Department College of Science King Saud University Riyadh Saudi Arabia
College of Horticulture and Gardening Yangtze University Jingzhou Hubei China
Department of Chemistry Faculty of Science University of Hradec Kralove Hradec Kralove Czechia
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Abbaspour H., Saeidi-Sar S., Afshari H., Abdel-Wahhab A. M. (2012). Tolerance of mycorrhiza infected pistachio (Pistacia vera l.) seedlings to drought stress under greenhouse conditions. J. Plant Physiol. 169, 704–709. doi: 10.1016/j.jplph.2012.01.014 PubMed DOI
Ahmed U., Rao M. J., Qi C., Xie Q., Noushahi H. A., Yaseen M., et al. . (2021). Expression profiling of flavonoid biosynthesis genes and secondary metabolites accumulation in populus under drought stress. Molecules 26, 5546. doi: 10.3390/molecules26185546 PubMed DOI PMC
Amiri R., Nikbakht A., Rahimmalek M., Hosseini H. (2017). Variation in the essential oil composition, antioxidant capacity, and physiological characteristics of Pelargonium graveolens l. inoculated with two species of mycorrhizal fungi under water deficit conditions. J. Plant Growth Regul. 36, 502–515. doi: 10.1007/s00344-016-9659-1 DOI
Aseel D. G., Rashad Y. M., Hammad S. M. (2019). Arbuscular mycorrhizal fungi trigger transcriptional expression of flavonoid and chlorogenic acid biosynthetic pathways genes in tomato against Tomato mosaic virus . Sci. Rep. 9, 9692. doi: 10.1038/s41598-019-46281-x PubMed DOI PMC
Begum N., Ahanger M. A., Su Y., Lei Y., Mustafa N. S. A., Ahmad P., et al. . (2019). Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants 8, 579. doi: 10.3390/plants8120579 PubMed DOI PMC
Cheng H. Q., Giri B., Wu Q. S., Zou Y. N., Kuča K. (2022). Arbuscular mycorrhizal fungi mitigate drought stress in citrus by modulating root microenvironment. Arch. Agron. Soil Sci. 68, 1217–1228. doi: 10.1080/03650340.2021.1878497 DOI
Chen S., Pan X. H., Li Y. T. (2017). Identification and characterization of chalcone synthase gene family members in Nicotiana tabacum . J. Plant Growth Regul. 36, 374–384. doi: 10.1007/s00344-016-9646-6 DOI
Cushnie T. P. T., Lamb A. J. (2011). Recent advances in understanding the antibacterial properties of flavonoids. Int. J. Antimicrobe. Ag. 38, 99–107. doi: 10.1016/j.ijantimicag.2011.02.014 PubMed DOI
Dao T. T. H., Linthorst H. J. M., Verpoorte R. (2011). Chalcone synthase and its functions in plant resistance. Phytochem. Rev. 10, 397–412. doi: 10.1007/s11101-011-9211-7 PubMed DOI PMC
Dias M. C., Pinto D. C., Silva A. M. (2021). Plant flavonoids: Chemical characteristics and biological activity. Molecules 26, 5377. doi: 10.3390/molecules26175377 PubMed DOI PMC
Ding Y. E., Zou Y. N., Wu Q. S., Kuča K. (2022). Mycorrhizal fungi regulate daily rhythm of circadian clock in trifoliate orange under drought stress. Tree Physiol. 42, 616–628. doi: 10.1093/treephys/tpab132 PubMed DOI
Dixon R. A., Paiva N. L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085. doi: 10.1105/tpc.7.7.1085 PubMed DOI PMC
Ferreyra M. L. F., Rius S. P., Casati P. (2012). Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci. 3. doi: 10.3389/fpls.2012.00222 PubMed DOI PMC
Flamini R., Mattivi F., De, Rosso M. D., Arapitsas P., Bavaresco L. (2013). Advanced knowledge of three important classes of grape phenolics: anthocyanins, stilbenes and flavonols. Int. J. Mol. Sci. 14, 19651–19669. doi: 10.3390/ijms141019651 PubMed DOI PMC
Gabriele M., Frassinetti S., Caltavuturo L., Montero L., Dinelli G., Longo V., et al. . (2017). Citrus bergamia powder: Antioxidant, antimicrobial and anti-inflammatory properties. J. Funct. Foods 31, 255–265. doi: 10.1016/j.jff.2017.02.007 DOI
Gao Z., Gao W., Zeng S. L., Li P., Liu E. H. (2018). Chemical structures, bioactivities and molecular mechanisms of citrus polymethoxyflavones. J. Funct. Foods 40, 498–509. doi: 10.1016/j.jff.2017.11.036 DOI
Ghasemi K., Ghasemi Y., Ebrahimzadeh M. A. (2009). Antioxidant activity, phenol and flavonoid contents of 13 citrus species peels and tissues. Pak. J. Pharm. Sci. 22, 277–281. PubMed
Gläßgen W. E., Rose A., Madlung J., Koch W., Gleitz J., Seitz H. U. (1998). Regulation of enzymes involved in anthocyanin biosynthesis in carrot cell cultures in response to treatment with ultraviolet light and fungal elicitors. Planta 204, 490–498. doi: 10.1007/s004250050283 PubMed DOI
Hahlbrock K., Kreuzaler F. (1972). Demonstration of two, up to now, hypothetic enzymes of flavonylglycoside biosynthesis as based on their regulation in plant cell suspension culture. Hoppe–Seylers Z. Physiol. Chem. 353, 1522. PubMed
Han Y., Cao Y., Jiang H., Ding T. (2017). Genome-wide dissection of the chalcone synthase gene family in Oryza sativa . Mol. Breed. 37, 119. doi: 10.1007/s11032-017-0721-x DOI
Han Y. H., Ding T., Su B., Jiang H. Y. (2016). Genome-wide identification, characterization and expression analysis of the chalcone synthase family in maize. Int. J. Mol. Sci. 17, 161. doi: 10.3390/ijms17020161 PubMed DOI PMC
He J. D., Li J. L., Wu Q. S. (2019). Effects of Rhizoglomus intraradices on plant growth and root endogenous hormones of trifoliate orange under salt stress. J. Anim. Plant Sci. 29, 245–250.
Hu B., Yao H., Gao Y. L., Wang R., Li F., Guo J. G., et al. . (2019). Overexpression of chalcone synthase gene improves flavonoid accumulation and drought tolerance in tobacco. Res. Sq. 2019, 1–11. doi: 10.21203/rs.2.18297/v2 DOI
Knogge W., Schmelzer E., Weissenböck G. (1986). The role of chalcone synthase in the regulation of flavonoid biosynthesis in developing oat primary leaves. Arch. Biochem. Biophysiol. 250, 364–372. doi: 10.1016/0003-9861(86)90738-1 PubMed DOI
Koes R. E., Quattrocchio F., Mol J. N. (1994). The flavonoid biosynthetic pathway in plants: Function and evolution. BioEssays 16. doi: 10.3389/fpls.2020.00007 DOI
Kunert K. J., Vorster B. J., Fenta B. A., Kibido T., Dionisio G., Foyer C. H. (2016). Drought stress responses in soybean roots and nodules. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.01015 PubMed DOI PMC
Li D. D., Liang Z. S., Pu B. (2020). Flavonoids contents and flavonoids synthetic key enzyme activities in alfalfa under drought stress. Acta Bot. Boreali–Occidentalia. Sin. 40, 1380–1388. doi: 10.7606/j.issn.1000-4025.2020.08.1380 DOI
Liu X. Q., Cheng S., Aroca R., Zou Y. N., Wu Q. S. (2022). Arbuscular mycorrhizal fungi induce flavonoid synthesis for mitigating oxidative damage of trifoliate orange under water stress. Environ. Exp. Bot. 204, 105089. doi: 10.1016/j.envexpbot.2022.105089 DOI
Liu Y. L., Lou Q., Xu W. R., Xin Y., Bassett C., Wang Y. J. (2011). Characterization of a chalcone synthase (CHS) flower-specific promoter from Lilium orential ‘Sorbonne’. Plant Cell Rep. 30, 2187–2194. doi: 10.1007/s00299-011-1124-9 PubMed DOI
Mahato N., Sharma K., Sinha M., Cho M. H. (2018). Citrus waste derived nutra-/pharmaceuticals for health benefits: Current trends and future perspectives. J. Funct. Foods. 40, 307–316. doi: 10.1016/j.jff.2017.11.015 DOI
Ma D. Y., Sun D. X., Wang C. Y., Li Y. G., Guo T. C. (2014). Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol. Biochem. 80, 60–66. doi: 10.1016/j.plaphy PubMed DOI
Nakabayashi R., Yonekura-Sakakibara K., Urano K., Suzuki M., Yamada Y., Nishizawa T., et al. . (2014). Enhancement of oxidative and drought tolerance in arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77, 367–379. doi: 10.1111/tpj.12388 PubMed DOI PMC
Ouyang J. Y., Wan Y., Xiang D. B., Ma C. R., Liu M., Qin M. L., et al. . (2020). Effects of drought stress on agronomic traits and flavonoid compound contents of tartary buckwheat. J. Anhui Agric. Sci. 48 (16), 35–38. doi: 10.3969/j.issn.0517-6611.2020.16.008 DOI
Pang Y. Z., Shen G. A., Wu W. S., Liu X. F., Lin J. A., Tan F., et al. . (2005). Characterization and expression of chalcone synthase gene from Ginkgo biloba . Plant Sci. 168, 1525–1531. doi: 10.1016/j.plantsci.2005.02.003 DOI
Phillips J. M., Hayman D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc 55, 158–161. doi: 10.1016/s0007-1536(70)80110-3 DOI
Sepiol C. J., Yu J., Dhaubhadel S. (2017). Genome-wide identification of chalcone reductase gene family in soybean: Insight into root-specific GmCHRs and Phytophthora sojae resistance. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.02073 PubMed DOI PMC
Sharma K., Mahato N., Lee Y. R. (2019). Extraction, characterization and biological activity of citrus flavonoids. Rev. Chem. Eng. 35, 265–284. doi: 10.1515/revce-2017-0027 DOI
Shen N., Wang T., Gan Q., Liu S., Wang L., Jin B. (2022). Plant flavonoids: Classification, distribution, biosynthesis, and antioxidant activity. Food Chem. 383, 132531. doi: 10.1016/j.foodchem.2022.132531 PubMed DOI
Singh N., Kumaria S. (2020). Molecular cloning and characterization of chalcone synthase gene from Coelogyne ovalis lindl. and its stress-dependent expression. Gene 762, 145104. doi: 10.1016/j.gene.2020.145104 PubMed DOI
Song M. Y., Wu X., Charoensinphon N., Wang M., Zheng J. K., Gao Z., et al. . (2017). Dietary 5-demethylnobiletin inhibits cigarette carcinogen NNK-induced lung tumorigenesis in mice. Food Funct. 8, 954–963. doi: 10.1039/c6fo01367h PubMed DOI PMC
Tian B., Pei Y., Huang W., Ding J., Siemann E. (2021). Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant. ISME J. 15, 1919–1930. doi: 10.1038/s41396-021-00894-1 PubMed DOI PMC
Tripoli E., La G. M., Giammanco S., Mijo D. D., Giammanco M. (2007). Citrus flavonoids: Molecular structure, biological activity and nutritional properties: A review. Food Chem. 104, 466–479. doi: 10.1016/j.foodchem.2006.11.054 DOI
Vadivel A. K. A., Krysiak K., Tian G., Dhaubhadel S. (2018). Genome-wide identification and localization of chalcone synthase family in soybean (Glycine max [L] merr). BMC Plant Biol. 18, 325. doi: 10.1186/s12870-018-1569-x PubMed DOI PMC
Wang Y., Li J., Xia R. X. (2010). Expression of chalcone synthase and chalcone isomerase genes and accumulation of corresponding flavonoids during fruit maturation of guoqing no. 4 satsuma mandarin (Citrus unshiu marcow). Sci. Hortic. 125, 110–116. doi: 10.1016/j.scienta.2010.02.001 DOI
Wang Z. B., Yu Q. B., Shen W. X., Mohtar C. A. E., Zhao X. Z., Gmitter ,. F. G., Jr (2018). Functional study of CHS gene family members in citrus revealed a novel CHS gene affecting the production of flavonoids. BMC Plant Biol. 18, 189. doi: 10.1186/s12870-018-1418-y PubMed DOI PMC
Wang C. H., Zhi S., Liu C. Y., Xu F. X., Zhao A., Wang X. L., et al. . (2017). Isolation and characterization of a novel chalcone synthase gene family from mulberry. Plant Physiol. Bioch. 115, 107–118. doi: 10.1016/j.plaphy.2017.03.014 PubMed DOI
Wu Q. S., Srivastava A. K., Zou Y. N. (2013). AMF-induced tolerance to drought stress in citrus. Sci. Hortic. 164, 77–87. doi: 10.1016/j.scienta.2013.09.010 DOI
Wu Q. S., Zou Y. N., Liu W., Ye X. F., Zai H. F., Zhao L. J. (2010). Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: Changes in leaf antioxidant defense systems. Plant Soil Environ. 56, 470–475. doi: 10.1016/j.jplph.2013.06.006 DOI
Yahyaa M., Ali S., Rikanati R. D., Ibdah M., Shachtier A., Eyal Y., et al. . (2017). Characterization of three chalcone synthase-like genes from apple (Malus x domestica borkh.). Phytochemistry 140, 125–133. doi: 10.1016/j.phytochem.2017.04.022 PubMed DOI
Yin Y. C., Hou J. M., Tian S. K., Yang L., Zhang Z. X., Li W. D., et al. . (2020). Overexpressing chalcone synthase (CHS) gene enhanced flavonoids accumulation in Glycyrrhiza uralensis hairy roots. Bot. Lett. 167, 219–231. doi: 10.1080/23818107.2019.1702896 DOI
Yonekura S. K., Higashi Y., Nakabayashi R. (2019). The origin and evolution of plant flavonoid metabolism. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00943 PubMed DOI PMC
Zhang F., Zou Y. N., Wu Q. S., Kuča K. (2020). Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environ. Exp. Bot. 171, 103962. doi: 10.1016/j.envexpbot.2019.103926 DOI
Zou Y. N., Wang P., Liu C. Y., Ni Q. D., Zhang D. J., Wu Q. S. (2017). Mycorrhizal trifoliate orange has greater root adaptation of morphology and phytohormones in response to drought stress. Sci. Rep. 7, 41134. doi: 10.1038/srep41134 PubMed DOI PMC