Abstract
This study may enhance our understanding of AvFLS function in plants under salt stress and may provide a new tool for the improvement of plant salt tolerance in the field. We isolated and identified AvFLS from Apocynum venetum. To further characterize the potential role of AvFLS in salt tolerance and to explore the relationship between FLS and salt resistance, we generated transgenic Arabidopsis lines overexpressing AvFLS. Tissue-specific expression analysis and salt-stress experiments identified AvFLS as a salt-inducible gene that is highly expressed in leaves of A. venetum. Subcellular localization analysis showed that AvFLS was located in the cytoplasm, consistent with other plant FLS proteins.The overexpression of AvFLS in Arabidopsis thaliana significantly improved the salt-stress tolerance of the transgenic plants: under salt stress, transgenic Arabidopsis exhibited improved flavonoid accumulation, seed germination rate, plant growth, chlorophyll content, and fresh weight compared to wild-type plants. Comparison of malonaldehyde (MDA), soluble sugar, and proline contents between the transgenic and wild-type plants indicated that the improved salt tolerance associated with AvFLS overexpression was due to decreased membrane damage. AvFLS overexpression also led to the upregulation of endogenous Arabidopsis genes involved in flavonoid biosynthesis. The results of this study demonstrate the potential utility of the AvFLS gene for molecular crop breeding, both to increase the contents of valuable flavonoids and to improve crop productivity in saline fields.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abubakar AS, Feng X, Gao G, Yu C, Chen J, Chen K et al (2022) Genome wide characterization of R2R3 MYB transcription factor from Apocynum venetum revealed potential stress tolerance and flavonoid biosynthesis genes. Genomics 114:110275. https://doi.org/10.1016/J.YGENO.2022.110275
Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76. https://doi.org/10.1016/j.plantsci.2012.07.014
Akita Y, Kitamura S, Mikami R, Ishizaka H (2018) Identification of functional flavonol synthase genes from fragrant wild cyclamen (Cyclamen purpurascens). J Plant Biochem Biotechnol 27:147–155. https://doi.org/10.1007/s13562-017-0423-9
Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling Behav 6:1720–1731. https://doi.org/10.4161/psb.6.11.17613
An Y, Feng X, Liu L, Xiong L, Wang L (2016) ALA-induced flavonols accumulation in guard cells is involved in scavenging H2O2 and inhibiting stomatal closure in Arabidopsis cotyledons. Front Plant Sci 7:1713. https://doi.org/10.3389/fpls.2016.01713
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93. https://doi.org/10.1016/j.biotechadv.2008.09.003
Baskar, V, Venkatesh, R, Ramalingam, S (2018) Flavonoids (antioxidants systems) in higher plants and their response to stresses. Antioxid Antioxid Enzymes Higher Plants 253–268. https://doi.org/10.1007/978-3-319-75088-0_12
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/bf00018060
Bernal-Vicente A, Cantabella D, Petri C, Hernández JA, Diaz-Vivancos P (2018) The salt-stress response of the transgenic plum line J8–1 and its interaction with the salicylic acid biosynthetic pathway from mandelonitrile. Int J Mol Sci 19:3519. https://doi.org/10.3390/ijms19113519
Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529. https://doi.org/10.1111/j.1469-185X.1968.tb00968.x
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. https://doi.org/10.3389/fpls.2013.00273
Britsch L, Heller W, Grisebach H (1981) Conversion of flavanone to flavone, dihydroflavonol and flavonol with an enzyme system from cell cultures of parsley. Z. Naturforsch., C. J Biosci 36:742–750. https://doi.org/10.1515/znc-1981-9-1009
Chan YJ, Won JL, Hai AT, Cao ST, Suk-Whan H, Hojoung L (2018) AtMybL-O modulates abscisic acid biosynthesis to optimize plant growth and ABA signaling in response to drought stress. Appl Biol Chem 61:473–477. https://doi.org/10.1007/s13765-018-0376-2
Chen, C, Wang, C, Liu, Z, Cai, Z, Hua, Y, Mei, Y, et al. (2020) iTRAQ-based proteomic technique provides insights into salt stress responsive proteins in Apocyni Veneti Folium (Apocynum venetum L.). Environ Exp Bot 180. https://doi.org/10.1016/j.envexpbot.2020.104247
Davies KM, Schwinn KE, Deroles SC, Manson DG, Lewis DH, Bloor SJ et al (2003) Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase. Euphytica 131:259–268. https://doi.org/10.1023/A:1024018729349
Delgado-Pertı́ñez M, Gómez-Cabrera A, Garrido A (2000) Predicting the nutritive value of the olive leaf (Olea europaea): digestibility and chemical composition and in vitro studies. Anim Feed Sci Technol 87:187–201. https://doi.org/10.1016/S0377-8401(00)00195-4
Djeridane A, Yousfi M, Nadjemi B, Boutassouna D, Stocker P, Vidal N (2006) Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem 97:654–660. https://doi.org/10.1016/j.foodchem.2005.04.028
Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J Integr Plant Biol 63:180–209. https://doi.org/10.1111/jipb.13054
Eghbaliferiz S, Iranshahi M (2016) Prooxidant activity of polyphenols, flavonoids, anthocyanins and carotenoids: updated review of mechanisms and catalyzing metals. Phytother Res 30:1379–1391. https://doi.org/10.1002/ptr.5643
Ellis RH, Covell S, Roberts EH, Summerfield RJ (1986) The Influence of Temperature on Seed Germination Rate in Grain Legumes II. Intraspecific variation in chickpea (Cicer arietinum L.) At constant temperatures. J Exp Bot 37:1503–1515. https://doi.org/10.1093/jxb/37.10.1503
Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52:29–66. https://doi.org/10.1146/annurev.arplant.52.1.29
Falcone Ferreyra ML, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K et al (2010) Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J 62:77–91. https://doi.org/10.1111/j.1365-313X.2010.04133.x
Falcone Ferreyra ML, Rius SP, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222. https://doi.org/10.3389/fpls.2012.00222
Fang Y, Deng X, Lu X, Zheng J, Jiang H, Rao Y et al (2019) Differential phosphoproteome study of the response to cadmium stress in rice. Ecotoxicol Environ Saf 180:780–788. https://doi.org/10.1016/j.ecoenv.2019.05.068
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustainable Dev 29:185–212. https://doi.org/10.1051/agro:2008021
Flowers, TJ, Muscolo, A (2015) Introduction to the special issue: halophytes in a changing world. AoB Plants 7. https://doi.org/10.1093/aobpla/plv020
Froemel S, De Vlaming P, Stotz G, Wiering H, Forkmann G, Schram AW (1985) Genetic and biochemical studies on the conversion of flavanones to dihydroflavonols in flowers of Petunia hybrida. Theor Appl Genet 70:561–568. https://doi.org/10.1007/BF00305991
Fujino N, Tenma N, Waki T, Ito K, Komatsuzaki Y, Sugiyama K et al (2018) Physical interactions among flavonoid enzymes in snapdragon and torenia reveal the diversity in the flavonoid metabolon organization of different plant species. Plant J 94:372–392. https://doi.org/10.1111/tpj.13864
Fujita A, Goto-Yamamoto N, Aramaki I, Hashizume K (2006) Organ-specific transcription of putative flavonol synthase genes of grapevine and effects of plant hormones and shading on flavonol biosynthesis in grape berry skins. Biosci., Biotechnol. Biochem 70:632–638. https://doi.org/10.1271/bbb.70.632
Gao Y, Liu J, Chen Y, Tang H, Wang Y, He Y et al (2018) Tomato SlAN11 regulates flavonoid biosynthesis and seed dormancy by interaction with bHLH proteins but not with MYB proteins. Hortic Res 5:1–18. https://doi.org/10.1038/s41438-018-0032-3
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Goyal S, Lambert C, Cluzet S, Mérillon JM, Ramawat KG (2012) Secondary metabolites and plant defence. In Plant Defence: Biol Control 12:109–138. https://doi.org/10.1007/978-94-007-1933-0_5
Gratani L (1992) A non-destructive method to determine chlorophyll content of leaves. Photosynthetica 26:469–473. https://doi.org/10.1007/BF00049537
Guo X, Chai W, Bai J, Ma ZR (2019) Cloning and bioinformatics analysis of AvFLS gene from Apocynum venetum. Mol Plant Breed 17:4978–4985. https://doi.org/10.13271/j.mpb.017.004978
Guo Y, Gao C, Wang M, Fu FF, El-Kassaby YA, Wang T et al (2020) Metabolome and transcriptome analyses reveal flavonoids biosynthesis differences in Ginkgo biloba associated with environmental conditions. Ind Crops Prod 158:112963. https://doi.org/10.1016/j.indcrop.2020.112963
Guo X, Wang Z, Cai D, Song L, Bai JL (2022) The chloroplast genome sequence and phylogenetic analysis of Apocynum venetum L. PLoS ONE 17:e0261710. https://doi.org/10.1371/journal.pone.0261710
Hao S, Wang Y, Yan Y, Liu Y, Wang J, Chen S (2021) A review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae 7:132. https://doi.org/10.3390/HORTICULTURAE7060132
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102. https://doi.org/10.1023/A:1005703923347
Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846. https://doi.org/10.1016/j.phytochem.2007.09.017
Heath RL, Packer L (1968) Photoperoxidation in Isolated Chloroplasts: I. Kinetics and Stoichiometry of Fatty Acid Peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083. https://doi.org/10.1105/tpc.7.7.1071
Holton TA, Brugliera F, Tanaka Y (1993) Cloning and expression of flavonol synthase from Petunia hybrida. Plant J 4:1003–1010. https://doi.org/10.1046/j.1365-313x.1993.04061003.x
Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136. https://doi.org/10.1104/pp.122.4.1129
Hou M, Zhang Y, Mu G, Cui S, Yang X, Liu L (2020) Molecular cloning and expression characterization of flavonol synthase genes in peanut (Arachis hypogaea). Sci Rep 10:17717. https://doi.org/10.1038/s41598-020-74763-w
Jeyaraj A, Liu S, Zhang X, Zhang R, Shangguan M, Wei C (2017) Genome-wide identification of microRNAs responsive to Ectropis oblique feeding in tea plant (Camellia sinensis L.). Sci Rep 7:1–16. https://doi.org/10.1038/s41598-017-13692-7
Jiang X, Shi Y, Fu Z, Li WW, Lai S, Wu Y et al (2020) Functional characterization of three flavonol synthase genes from Camellia sinensis: Roles in flavonol accumulation. Plant Sci 300:110632. https://doi.org/10.1016/j.plantsci.2020.110632
Jiang L, Wu X, Zhao Z, Zhang K, Tanveer M, Wang L et al (2021) Luobuma (Apocynum)–Cash crops for saline lands. Ind Crops Prod 173:114146. https://doi.org/10.1016/j.indcrop.2021.114146
Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant, Cell Environ 37:300–311. https://doi.org/10.1111/pce.12157
Kawai Y, Ono E, Mizutani M (2014) Evolution and diversity of the 2–oxoglutarate-dependent dioxygenase superfamily in plants. Plant J 78:328–343. https://doi.org/10.1111/tpj.12479
Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9:2732. https://doi.org/10.3389/fmicb.2018.02732
Kim BG, Kim JH, Kim J, Lee C, Ahn J (2008) Accumulation of flavonols in response to ultraviolet-B irradiation in soybean is related to induction of flavanone 3-beta-hydroxylase and flavonol synthase. Mol Cells 25:247–252. https://doi.org/10.1016/j.febslet.2008.03.057
Kim YB, Kim K, Kim Y, Tuan PA, Kim HH, Cho JW et al (2014) Cloning and characterization of a flavonol synthase gene from Scutellaria baicalensis. Sci World J 2014:980740. https://doi.org/10.1155/2014/980740
Koes RE, Quattrocchio F, Mol JN (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16:123–132. https://doi.org/10.1002/bies.950160209
Kuhn BM, Geisler M, Bigler L, Ringli C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 156:585–595. https://doi.org/10.1104/pp.111.175976
Lee J, Koo N, Min DB (2004) Reactive oxygen species, aging, and antioxidative nutraceuticals. Compr Rev Food Sci Food Saf 3:21–33. https://doi.org/10.1111/j.1541-4337.2004.tb00058.x
Li C, Bai Y, Li S, Chen H, Han X, Zhao H et al (2012) Cloning, characterization, and activity analysis of a flavonol synthase gene FtFLS1 and its association with flavonoid content in tartary buckwheat. J Agric Food Chem 60:5161–5168. https://doi.org/10.1021/jf205192q
Li X, Kim YB, Kim Y, Zhao S, Kim HH, Chung E et al (2013) Differential stress-response expression of two flavonol synthase genes and accumulation of flavonols in tartary buckwheat. J Plant Physiol 170:1630–1636. https://doi.org/10.1016/j.jplph.2013.06.010
Li Q, Yu HM, Meng XF, Lin JS, Li YJ, Hou BK (2018) Ectopic expression of glycosyltransferase UGT 76E11 increases flavonoid accumulation and enhances abiotic stress tolerance in Arabidopsis. Plant Biol 20:10–19. https://doi.org/10.1111/plb.12627
Li P, Xu Y, Zhang Y, Fu J, Yu S, Guo H et al (2020) Metabolite profiling and transcriptome analysis revealed the chemical contributions of tea trichomes to tea flavors and tea plant defenses. J Agric Food Chem 68:11389–11401. https://doi.org/10.1021/acs.jafc.0c04075
Li P, Lei K, Liu L, Zhang G, Ge H, Zheng C et al (2021) Identification and functional characterization of a new flavonoid synthase gene MdFLS1 from apple. Planta 253:1–15. https://doi.org/10.1007/S00425-021-03615-2
Liu W, Xiao Z, Fan C, Jiang N, Meng X, Xiang X (2018) Cloning and characterization of a flavonol synthase gene from Litchi chinensis and its variation among litchi cultivars with different fruit maturation periods. Front Plant Sci 9:567. https://doi.org/10.3389/fpls.2018.00567
Liu W, Feng Y, Yu S, Fan Z, Li X, Li J et al (2021) The flavonoid biosynthesis network in plants. Int J Mol Sci 22:12824. https://doi.org/10.3390/IJMS222312824
Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell Environ 29:315–330. https://doi.org/10.1111/j.1365-3040.2005.01493.x
Lou Q, Liu Y, Qi Y, Jiao S, Tian F, Jiang L et al (2014) Transcriptome sequencing and metabolite analysis reveals the role of delphinidin metabolism in flower color in grape hyacinth. J Exp Bot 65:3157–3164. https://doi.org/10.1093/jxb/eru168
Luo P, Ning G, Wang Z, Shen Y, Jin H, Li P et al (2016) Disequilibrium of flavonol synthase and dihydroflavonol-4-reductase expression associated tightly to white vs. red color flower formation in plants. Front Plant Sci 6:1257. https://doi.org/10.3389/fpls.2015.01257
Ma D, Sun D, Wang C, Li Y, Guo T (2014) Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol Biochem 80:60–66. https://doi.org/10.1016/j.plaphy.2014.03.024
Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B et al (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712. https://doi.org/10.1046/j.1365-313X.2002.01389.x
Mahajan M, Ahuja PS, Yadav SK (2011) Post-transcriptional silencing of flavonol synthase mRNA in tobacco leads to fruits with arrested seed set. PLoS ONE 6:e28315. https://doi.org/10.1371/journal.pone.0028315
Martens S, Preuß A, Matern U (2010) Multifunctional flavonoid dioxygenases: flavonol and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry 71:1040–1049. https://doi.org/10.1016/j.phytochem.2010.04.016
Morimoto T, Tao R (2016) Functional characterization of Prunus SLFLs in transgenic Petunia. Acta Hortic 1231:85–90. https://doi.org/10.17660/actahortic.2019.1231.15
Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, Ric De Vos CH et al (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474. https://doi.org/10.1038/88150
Mukami A, Ngetich A, Mweu C, Oduor RO, Muthangya M, Mbinda WM (2019) Differential characterization of physiological and biochemical responses during drought stress in finger millet varieties. Physiol Mol Biol Plants 25:837–846. https://doi.org/10.1007/s12298-019-00679-z
Nguyen HN, Kim JH, Hyun WY, Nguyen NT, Hong SW, Lee H (2013) TTG1-mediated flavonols biosynthesis alleviates root growth inhibition in response to ABA. Plant Cell Rep 32:503–514. https://doi.org/10.1007/s00299-012-1382-1
Nguyen NH, Kim JH, Kwon J, Jeong CY, Lee W, Lee D et al (2016) Characterization of Arabidopsis thaliana FLAVONOL SYNTHASE 1 (FLS1)-overexpression plants in response to abiotic stress. Plant Physiol Biochem 103:133–142. https://doi.org/10.1016/j.plaphy.2016.03.010
Ohno S, Hosokawa M, Kojima M, Kitamura Y, Hoshino A, Tatsuzawa F et al (2011) Simultaneous post-transcriptional gene silencing of two different chalcone synthase genes resulting in pure white flowers in the octoploid dahlia. Planta 234:945–958. https://doi.org/10.1007/s00425-011-1456-2
Owens DK, Alerding AB, Crosby KC, Bandara AB, Westwood JH, Winkel BS (2008) Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiol 147:1046–1061. https://doi.org/10.1104/pp.108.117457
Park YK, Koo MH, Ikegaki M, Contado JL (1997) Comparison of the flavonoid aglycone contents of Apis mellifera propolis from various regions of Brazil. Arq Biol Tecnol 40:97–106. https://doi.org/10.1007/s002849900274
Park S, Kim DH, Park BR, Lee JY, Lim SH (2019) Molecular and functional characterization of Oryza sativa flavonol synthase (OsFLS), a bifunctional dioxygenase. J Agric Food Chem 67:7399–7409. https://doi.org/10.1021/acs.jafc.9b02142
Parvanova D, Ivanov S, Konstantinova T, Karanov E, Atanassov A, Tsvetkov T et al (2004) Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol Biochem 42:57–63. https://doi.org/10.1016/j.plaphy.2003.10.007
Preuß A, Stracke R, Weisshaar B, Hillebrecht A, Matern U, Martens S (2009) Arabidopsis thaliana expresses a second functional flavonol synthase. FEBS Lett 583:1981–1986. https://doi.org/10.1016/j.febslet.2009.05.006
Quick WP, Chaves MM, Wendler R, David M, Rodrigues ML, Passaharinho JA et al (1992) The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions. Plant, Cell Environ 15:25–35. https://doi.org/10.1111/j.1365-3040.1992.tb01455.x
Reginato MA, Castagna A, Furlán A, Castro S, Ranieri A, Luna V (2014) Physiological responses of a halophytic shrub to salt stress by Na2SO4 and NaCl: oxidative damage and the role of polyphenols in antioxidant protection. AoB Plants 6:plu042. https://doi.org/10.1093/aobpla/plu042
Richards RA (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J Exp Bot 51:447–458. https://doi.org/10.1093/jexbot/51.suppl_1.447
Sánchez-Rodríguez E, Moreno DA, Ferreres F, del Mar Rubio-Wilhelmi M, Ruiz JM (2011) Differential responses of five cherry tomato varieties to water stress: changes on phenolic metabolites and related enzymes. Phytochemistry 72:723–729. https://doi.org/10.1016/j.phytochem.2011.02.011
Saslowsky DE, Warek U, Winkel BS (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740. https://doi.org/10.1074/jbc.M413506200
Shah A, Smith DL (2020) Flavonoids in agriculture: Chemistry and roles in, biotic and abiotic stress responses, and microbial associations. Agronomy 10:1209. https://doi.org/10.3390/agronomy10081209
Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Mol Online 24:2452. https://doi.org/10.3390/molecules24132452
Shi J, Li W, Gao Y, Wang B, Li Y, Song Z (2017) Enhanced rutin accumulation in tobacco leaves by overexpressing the NtFLS2 gene. Biosci Biotechnol Biochem 81:1721–1725. https://doi.org/10.1080/09168451.2017.1353401
Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353. https://doi.org/10.1007/s11738-013-1279-9
Stracke R, De Vos RC, Bartelniewoehner L, Ishihara H, Sagasser M, Martens S et al (2009) Metabolomic and genetic analyses of flavonol synthesis in Arabidopsis thaliana support the in vivo involvement of leucoanthocyanidin dioxygenase. Planta 229:427–445. https://doi.org/10.1007/s00425-008-0841-y
Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749. https://doi.org/10.1111/j.1365-313X.2008.03447.x
Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G (2004) Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol 163:547–561. https://doi.org/10.1111/J.1469-8137.2004.01126.X
Thakur M, Bhattacharya S, Khosla PK, Puri S (2019) Improving production of plant secondary metabolites through biotic and abiotic elicitation. J Appl Res Med Aromat Plants 12:1–12. https://doi.org/10.1016/j.jarmap.2018.11.004
Toh HC, Wang SY, Chang ST, Chu FH (2013) Molecular cloning and characterization of flavonol synthase in Acacia confusa. Tree Genet Genomes 9:85–92. https://doi.org/10.1007/s11295-012-0536-1
Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, De Vos CHR et al (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106. https://doi.org/10.1093/jxb/erf044
Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291. https://doi.org/10.1038/nchembio.158
Vu TT, Jeong CY, Nguyen HN, Lee D, Lee SA, Kim JH et al (2015) Characterization of Brassica napus flavonol synthase involved in flavonol biosynthesis in Brassica napus L. J Agric Food Chem 63(35):7819–7829. https://doi.org/10.1021/acs.jafc.5b02994
Wang M, Qin L, Xie C, Li W, Yuan J, Kong L et al (2014) Induced and constitutive DNA methylation in a salinity-tolerant wheat introgression line. Plant Cell Physiol 55:1354–1365. https://doi.org/10.1093/pcp/pcu059
Wang F, Kong W, Wong G, Fu L, Peng R, Li Z et al (2016) AtMYB12 regulates flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Genet Genomics 291:1545–1559. https://doi.org/10.1007/s00438-016-1203-2
Wang M, Ren T, Huang R, Li Y, Zhang C, Xu Z (2021a) Overexpression of an Apocynum venetum flavonols synthetase gene confers salinity stress tolerance to transgenic tobacco plants. Plant Physiol Biochem 162:667–676. https://doi.org/10.1016/j.plaphy.2021.03.034
Wang M, Zhang Y, Zhu C, Yao X, Zheng Z, Tian Z et al (2021b) EkFLS overexpression promotes flavonoid accumulation and abiotic stress tolerance in plant. Physiol Plant 172:1966–1982. https://doi.org/10.1111/ppl.13407
Wang Y, Shi Y, Li K, Yang D, Liu N, Zhang L et al (2021c) Roles of the 2-Oxoglutarate-Dependent Dioxygenase Superfamily in the Flavonoid Pathway: A Review of the Functional Diversity of F3H, FNS I, FLS, and LDOX/ANS. Mol Online 26:6745. https://doi.org/10.3390/molecules26216745
Wang Y, Zhou LJ, Wang Y, Liu S, Geng Z, Song A et al (2021d) Functional identification of a flavone synthase and a flavonol synthase genes affecting flower color formation in Chrysanthemum morifolium. Plant Physiol Biochem 166:1109–1120. https://doi.org/10.1016/j.plaphy.2021.07.019
Wang D, Dong W, Murray J, Wang E (2022a) Innovation and appropriation in mycorrhizal and rhizobial symbioses. Plant Cell 34:1573–1599. https://doi.org/10.1093/plcell/koac039
Wang Z, Liu A, Liu J, Huang X, Xiao F, Tian M et al (2022b) Substrates and Loaded Iron Ions Relative Position Influence the Catalytic Characteristics of the Metalloenzymes Angelica archangelica Flavone Synthase I and Camellia sinensis Flavonol Synthase. Front Pharmacol 13:902672. https://doi.org/10.3389/FPHAR.2022.902672
Xie W, Zhang X, Wang T, Hu J (2012) Botany, traditional uses, phytochemistry and pharmacology of Apocynum venetum L. (Luobuma): A review. J Ethnopharmacol 141:1–8. https://doi.org/10.1016/j.jep.2012.02.003
Xu F, Li L, Zhang W, Cheng H, Sun N, Cheng S et al (2012) Isolation, characterization, and function analysis of a flavonol synthase gene from Ginkgo biloba. Mol Biol Rep 39:2285–2296. https://doi.org/10.1007/s11033-011-0978-9
Xu N, Liu S, Lu Z, Pang S, Wang L, Wang L et al (2020a) Gene expression profiles and flavonoid accumulation during salt stress in Ginkgo biloba seedlings. Plants 9:1162. https://doi.org/10.3390/plants9091162
Xu X, Gong J, Zhang T, Li Z, Zhang J, Wang L et al (2020b) Insights into antibacterial mechanism of Apocynum venetum L. fiber: Evolution of bioactive natural substances in bast during chemical degumming process. Ind Crops Prod 151:112419. https://doi.org/10.1016/j.indcrop.2020.112419
Xu Z, Wang M, Ren T, Li K, Li Y, Marowa P et al (2021) Comparative transcriptome analysis reveals the molecular mechanism of salt tolerance in Apocynum venetum. Plant Physiol Biochem 167:816–830. https://doi.org/10.1016/j.plaphy.2021.08.043
Yadav B, Jogawat A, Rahman MS, Narayan OP (2021) Secondary metabolites in the drought stress tolerance of crop plants: A review. Gene Rep 23:101040. https://doi.org/10.1016/j.genrep.2021.101040
Yang J, Zhang L, Jiang L, Zhan YG, Fan GZ (2021) Quercetin alleviates seed germination and growth inhibition in Apocynum venetum and Apocynum pictum under mannitol-induced osmotic stress. Plant Physiol Biochem 159:268–276. https://doi.org/10.1016/j.plaphy.2020.12.025
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.1042/bj0570508
Yonekura-Sakakibara K, Higashi Y, Nakabayashi R (2019) The origin and evolution of plant flavonoid metabolism. Front Plant Sci 10:943. https://doi.org/10.3389/fpls.2019.00943
Yu D, Huang T, Tian B, Zhan J (2020) Advances in biosynthesis and biological functions of proanthocyanidins in horticultural plants. Foods 9:1774. https://doi.org/10.3390/foods9121774
Yu Z, Dong W, Teixeira da Silva JA, He C, Si C, Duan J (2021) Ectopic expression of DoFLS1 from Dendrobium officinale enhances flavonol accumulation and abiotic stress tolerance in Arabidopsis thaliana. Protoplasma 258:803–815. https://doi.org/10.1007/s00709-020-01599-6
Yuan Y, Qi L, Yang J, Wu C, Liu Y, Huang L (2015) A Scutellaria baicalensis R2R3-MYB gene, SbMYB8, regulates flavonoid biosynthesis and improves drought stress tolerance in transgenic tobacco. Plant Cell, Tissue Organ Cult 120:961–972. https://doi.org/10.1007/s11240-014-0650-x
Zahra R, Fatemeh N, Ali AM (2018) Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio ( Pistacia vera L.) rootstocks. J Plant Interact 13:73–82. https://doi.org/10.1080/17429145.2018.1424355
Zhang C, Liu H, Jia C, Liu Y, Wang F, Wang J (2016a) Cloning, characterization and functional analysis of a flavonol synthase from Vaccinium corymbosum. Trees 30:1595–1605. https://doi.org/10.1007/s00468-016-1393-6
Zhang X, Henriques R, Lin S, Niu Q, Chua N (2016b) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646. https://doi.org/10.1038/nprot.2006.97
Zhang C, Li X, Zhan Z, Cao L, Zeng A, Chang G et al (2018) Transcriptome sequencing and metabolism analysis reveals the role of cyanidin metabolism in dark-red onion (Allium cepa L.) bulbs. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-32472-5
Zhao D, Jiang Y, Ning C, Meng J, Lin S, Ding W et al (2014) Transcriptome sequencing of a chimaera reveals coordinated expression of anthocyanin biosynthetic genes mediating yellow formation in herbaceous peony (Paeonia lactiflora Pall.). BMC Genomics 15:689. https://doi.org/10.1186/1471-2164-15-689
Zhou XW, Fan ZQ, Chen Y, Zhu YL, Li JY, Yin HF (2013) Functional analyses of a flavonol synthase–like gene from Camellia nitidissima reveal its roles in flavonoid metabolism during floral pigmentation. J Biosci 38:593–604. https://doi.org/10.1007/s12038-013-9339-2
Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159. https://doi.org/10.1016/j.copbio.2008.02.004
Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261. https://doi.org/10.1146/annurev-arplant-042809-112206
Acknowledgements
We thank LetPub for linguistic assistance and pre-submission expert review.
Funding
This research was supported by the Fundamental Research Funds for the Central Universities(31920220138) and the National Natural Science Foundation of China (Grant No. 31760242).
Author information
Authors and Affiliations
Contributions
XG and DC contributed substantially to the experimental design, conceived the study, and approved the final manuscript. XG contributed to funding, interpreted the data, authored or reviewed the draft, and revised the manuscript. JL and DC carried out mainly experiments, finished the draft of the manuscript, and comprehensively analyzed the data from all experimental results. All authors contributed to the article and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of Interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Guo, X., Li, J. & Cai, D. Overexpression of a Flavonol Synthase Gene from Apocynum venetum Improves the Salinity Stress Tolerance of Transgenic Arabidopsis thaliana. J Soil Sci Plant Nutr (2023). https://doi.org/10.1007/s42729-023-01590-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42729-023-01590-z