Abstract
Broussonetia papyrifera is widely found in cadmium (Cd) contaminated areas, with an inherent enhanced flavonoids metabolism and inhibited lignin biosynthesis, colonized by lots of symbiotic fungi, such as arbuscular mycorrhizal fungi (AMF). However, the physiological and molecular mechanisms by which Rhizophagus irregularis, an AM fungus, regulates flavonoids and lignin in B. papyrifera under Cd stress remain unclear. Here, a pot experiment of B. papyrifera inoculated and non-inoculated with R. irregularis under Cd stress was carried out. We determined flavonoids and lignin concentrations in B. papyrifera roots by LC-MS and GC-MS, respectively, and measured the transcriptional levels of flavonoids- or lignin-related genes in B. papyrifera roots, aiming to ascertain the key components of flavonoids or lignin, and key genes regulated by R. irregularis in response to Cd stress. Without R. irregularis, the concentrations of eriodictyol, quercetin and myricetin were significantly increased under Cd stress. The concentrations of eriodictyol and genistein were significantly increased by R. irregularis, while the concentration of rutin was significantly decreased. Total lignin and lignin monomer had no alteration under Cd stress or with R. irregularis inoculation. As for flavonoids- or lignin-related genes, 26 genes were co-regulated by Cd stress and R. irregularis. Among these genes, BpC4H2, BpCHS8 and BpCHI5 were strongly positively associated with eriodictyol, indicating that these three genes participate in eriodictyol biosynthesis and were involved in R. irregularis assisting B. papyrifera to cope with Cd stress. This lays a foundation for further research revealing molecular mechanisms by which R. irregularis regulates flavonoids synthesis to enhance tolerance of B. papyrifera to Cd stress.
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Data availability
Datasets supporting the conclusions of this article are included within the article and its additional files, all gene expression data can be requested from W. H. (hwt@scau.edu.cn).
References
Adolfsson L, Nziengui H, Abreu IN, Simura J, Beebo A, Herdean A, Aboalizadeh J, Siroka J, Moritz T, Novak O, Ljung K, Schoefs B, Spetea C (2017) Enhanced secondary- and hormone metabolism in leaves of Arbuscular Mycorrhizal Medicago truncatula. Plant Physiol 175:392–411. https://doi.org/10.1104/pp.16.01509
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
Akashi T, Aoki T, Ayabe SI (1998) CYP81E1, a cytochrome P450 cDNA of licorice (Glycyrrhiza echinata L.), encodes isoflavone 2′-hydroxylase. Biochem Bioph Res Co 251:67–70. https://doi.org/10.1006/bbrc.1998.9414
Alberti A, Blazics B, Kery A (2008) Evaluation of Sempervivum tectorum L. Flavonoids by LC and LC–MS. Chromatographia 68:107–111. https://doi.org/10.1365/s10337-008-0750-z
Alengebawy A, Abdelkhalek ST, Qureshi SR, Wang MQ (2021) Heavy Metals and Pesticides Toxicity in Agricultural Soil and Plants: Ecological Risks and Human Health Implications. Toxics 9. https://doi.org/ARTN4210.3390/toxics9030042
Ayabe SI, Akashi T (2006) Cytochrome P450s in flavonoid metabolism. Phytochem Rev 5:271–282. https://doi.org/10.1007/s11101-006-9007-3
Baba SA, Ashraf N (2019) Functional characterization of flavonoid 3 ‘-hydroxylase, CsF3 ' H, from Crocus sativus L: Insights into substrate specificity and role in abiotic stress. Arch Biochem Biophys 667:70–78. https://doi.org/10.1016/j.abb.2019.04.012
Barros J, Escamilla-Trevino L, Song LH, Rao XL, Serrani-Yarce JC, Palacios MD, Engle N, Choudhury FK, Tschaplinski TJ, Venables BJ, Mittler R, Dixon RA (2019) 4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase. Nat Commun 10:1994. https://doi.org/ARTN199410.1038/s41467-019-10082-7
Bécard G, Douds DD, Pfeffer PE (1992) Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microb 58:821–825. https://doi.org/10.1128/aem.58.3.821-825.1992
Bhargavan B, Singh D, Gautam AK, Mishra JS, Kumar A, Goel A, Dixit M, Pandey R, Manickavasagam L, Dwivedi SD, Chakravarti B, Jain GK, Ramachandran R, Maurya R, Trivedi A, Chattopadhyay N, Sanyal S (2012) Medicarpin, a legume phytoalexin, stimulates osteoblast differentiation and promotes peak bone mass achievement in rats: evidence for estrogen receptor β-mediated osteogenic action of medicarpin. J Nutr Biochem 23:27–38. https://doi.org/10.1016/j.jnutbio.2010.11.002
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54. https://doi.org/10.1146/annurev.arplant.54.031902.134938. :519 – 546
Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25. https://doi.org/10.1007/s11104-009-0266-9
Chadzinikolau T, Kozlowska M, Mleczek M (2017) Induction of phytochelatins and flavonoids in cadmium polluted Berberis thunbergii. Dendrobiology 77:139–146. https://doi.org/10.12657/denbio.077.011
Chang Q, Diao FW, Wang QF, Pan L, Dang ZH, Guo W (2018) Effects of arbuscular mycorrhizal symbiosis on growth, nutrient and metal uptake by maize seedlings (Zea mays L.) grown in soils spiked with Lanthanum and Cadmium. Environ Pollut 241:607–615. https://doi.org/10.1016/j.envpol.2018.06.003
Chao N, Qi Q, Li S, Ruan B, Jiang X, Gai Y (2021) Characterization and functional analysis of the Hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase (HCT) gene family in poplar. PeerJ 9:e10741. https://doi.org/10.7717/peerj.10741
Chen J, Yuan H, Zhang L, Pan H, Xu R, Zhong Y, Chen J, Nan P (2015) Cloning, expression and purification of isoflavone-2′-hydroxylase from Astragalus membranaceus Bge. Var. mongolicus (Bge.) Hsiao. Protein Expres Purif 107:83–89. https://doi.org/10.1016/j.pep.2014.11.010
Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60:665–671. https://doi.org/10.1016/j.chemosphere.2005.01.029
Chen PL, Hu YM, Tang F, Zhao ML, Peng XJ, Shen SH (2020) Cooperation between Broussonetia papyrifera and its symbiotic fungal community to improve local adaptation of the host. Appl Environ Microb 86: e00464-20. https://doi.org/ARTNe00464-2010.1128/AEM.00464-20
Chen F, Zhuo CL, **ao XR, Pendergast TH, Devos KM (2021a) A rapid thioacidolysis method for biomass lignin composition and tricin analysis. Biotechnol Biofuels 14:1–9. https://doi.org/ARTN1810.1186/s13068-020-01865-y
Chen M, Bruisson S, Bapaume L, Darbon G, Glauser G, Schorderet M, Reinhardt D (2021b) VAPYRIN attenuates defence by repressing PR gene induction and localized lignin accumulation during arbuscular mycorrhizal symbiosis of Petunia hybrida. New Phytol 229:3481–3496. https://doi.org/10.1111/nph.17109
Chen Y, Yi N, Yao SB, Zhuang J, Fu Z, Ma J, Yin S, Jiang X, Liu Y, Gao L, **a T (2021c) CsHCT-Mediated lignin synthesis pathway involved in the response of tea plants to biotic and Abiotic Stresses. J Agric Food Chem 69:10069–10081. https://doi.org/10.1021/acs.jafc.1c02771
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299
Collazo P, Montoliu L, Puigdomènech P, Rigau J (1992) Structure and expression of the lignin O-methyltransferase gene from Zea mays L. Plant Mol Biol 20:857–867. https://doi.org/10.1007/BF00027157
Daly P, McClellan C, Maluk M, Oakey H, Lapierre C, Waugh R, Stephens J, Marshall D, Barakate A, Tsuji Y, Goeminne G, Vanholme R, Boerjan W, Ralph J, Halpin C (2019) RNAi-suppression of barley caffeic acid O-methyltransferase modifies lignin despite redundancy in the gene family. Plant Biotechnol J 17:594–607. https://doi.org/10.1111/pbi.13001
Dastmalchi M, Dhaubhadel S (2015) Soybean chalcone isomerase: evolution of the Fold, and the differential expression and localization of the gene family. Planta 241:507–523. https://doi.org/10.1007/s00425-014-2200-5
Dias MC, Pinto DC, Silva AM (2021) Plant Flavonoids: Chemical Characteristics and Biological Activity. Molecules 26:5377. https://doi.org/ARTN537710.3390/molecules26175377
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
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
Feng SM, Luo ZS, Zhang YB, Zhong Z, Lu BY (2014) Phytochemical contents and antioxidant capacities of different parts of two sugarcane (Saccharum officinarum L.) cultivars. Food Chem 151:452–458. https://doi.org/10.1016/j.foodchem.2013.11.057
Ferreira SS, Antunes MS (2021) Re-engineering Plant Phenylpropanoid Metabolism with the Aid of Synthetic Biosensors. Front Plant Sci 12:701385. https://doi.org/ARTN70138510.3389/fpls.2021.701385
Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711. https://doi.org/10.4161/psb.6.5.15069
Fries LL, Pacovsky RS, Safir GR, Siqueira JO (1997) Plant growth and arbuscular mycorrhizal fungal colonization affected by exogenously applied phenolic compounds. J Chem Ecol 23:1755–1767
Gaddam SR, Sharma A, Trivedi PK (2024) miR397b-LAC2 module regulates cadmium stress response by coordinating root lignification and copper homeostasis in Arabidopsis thaliana. J Hazard Mater 465:133100. https://doi.org/10.1016/j.jhazmat.2023.133100
Gallego-Giraldo L, Jikumaru Y, Kamiya Y, Tang Y, Dixon RA (2011) Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L). New Phytol 190:627–639. https://doi.org/10.1111/j.1469-8137.2010.03621.x
Gill RA, Burke IC (2002) Influence of soil depth on the decomposition of Bouteloua gracilis roots in the shortgrass steppe. Plant Soil 241:233–242. https://doi.org/10.1023/A:1016146805542
Goujon T, Sibout R, Pollet B, Maba B, Nussaume L, Bechtold N, Lu FC, Ralph J, Mila I, Barriere Y, Lapierre C, Jouanin L (2003) A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Mol Biol 51:973–989. https://doi.org/10.1023/A:1023022825098
Guo X, Zhang S, Shan XQ (2008) Adsorption of metal ions on lignin. J Hazard Mater 151:134–142. https://doi.org/10.1016/j.jhazmat.2007.05.065
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Han Y, Zveushe OK, Dong F, Ling Q, Chen Y, Sajid S, Zhou L, Resco de Dios V (2021) Unraveling the effects of arbuscular mycorrhizal fungi on cadmium uptake and detoxification mechanisms in perennial ryegrass (Lolium perenne). Sci Total Environ 798:149222. https://doi.org/10.1016/j.scitotenv.2021.149222
Han X, Zhao Y, Chen Y, Xu J, Jiang C, Wang X, Zhuo R, Lu MZ, Zhang J (2022) Lignin biosynthesis and accumulation in response to abiotic stresses in woody plants. Forestry Res 2:9. https://doi.org/10.48130/FR-2022-0009
He L, He T, Farrar S, Ji LB, Liu TY, Ma X (2017) Antioxidants Maintain Cellular Redox Homeostasis by Elimination of reactive oxygen species. Cell Physiol Biochem 44:532–553. https://doi.org/10.1159/000485089
Heller W, Britsch L, Forkmann G, Grisebach H (1985) Leucoanthocyanidins as intermediates in anthocyanidin biosynthesis in flowers of Matthiola incana R. Br. Planta 163:191–196. https://doi.org/10.1007/BF00393505
Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446–1465. https://doi.org/10.1105/tpc.020297
Hu W, Zhang H, Zhang X, Chen H, Tang M (2017) Characterization of six PHT1 members in Lycium barbarum and their response to arbuscular mycorrhiza and water stress. Tree Physiol 37:351–366. https://doi.org/10.1093/treephys/tpw125
Hu W, Pan L, Chen H, Tang M (2020) VBA–AMF: a VBA program based on the magnified intersections method for quantitative recording of root colonization by Arbuscular Mycorrhizal fungi. Indian J Microbiol 60:374–378. https://doi.org/10.1007/BF00393505
Iiyama K, Wallis AFA (1988) An improved acetyl bromide procedure for determining lignin in woods and wood pulps. Wood Sci Technol 22:271–280. https://doi.org/10.1007/bf00386022
Islam A, Islam MS, Rahman MK, Uddin MN, Akanda MR (2020) The pharmacological and biological roles of eriodictyol. Arch Pharm Res 43:582–592. https://doi.org/10.1007/s12272-020-01243-0
Janczak-Pieniazek M, Cichonski J, Michalik P, Chrzanowski G (2023) Effect of Heavy Metal Stress on Phenolic Compounds Accumulation in Winter Wheat Plants. Molecules 28:241. https://doi.org/ARTN24110.3390/molecules28010241
Jiang D, Tan MT, Wu S, Zheng L, Wang Q, Wang GR, Yan SC (2021a) Defense responses of arbuscular mycorrhizal fungus-colonized poplar seedlings against gypsy moth larvae: a multiomics study. Hortic Res 8. https://doi.org/ARTN24510.1038/s41438-021-00671-3
Jiang LN, Fan ZQ, Tong R, Yin HF, Li JY, Zhou XW (2021b) Flavonoid 3 ‘-hydroxylase of Camellia Nitidissima Chi. Promotes the synthesis of polyphenols better than flavonoids. Mol Biol Rep 48:3903–3912. https://doi.org/10.1007/s11033-021-06345-6
Jiao P, Chaoyang L, Wenhan Z, **gyi D, Yunlin Z, Zhenggang X (2022) Integrative Metabolome and Transcriptome Analysis of Flavonoid Biosynthesis Genes in Broussonetia papyrifera leaves from the perspective of sex differentiation. Front Plant Sci 13:900030. https://doi.org/10.3389/fpls.2022.900030
Jouili H, El Ferjani E (2003) Changes in antioxidant and lignifying enzyme activities in sunflower roots (Helianthus annuus L.) stressed with copper excess. Cr Biol 326:639–644. https://doi.org/10.1016/S1631-0691(03)00157-4
Kamali S, Mehraban A (2020) Nitroxin and arbuscular mycorrhizal fungi alleviate negative effects of drought stress on Sorghum bicolor yield through improving physiological and biochemical characteristics. Plant Signal Behav 15:1813998. https://doi.org/Artn181399810.1080/15592324.2020.1813998
Kidwai M, Ahmad IZ, Chakrabarty D (2020) Class III peroxidase: an indispensable enzyme for biotic/abiotic stress tolerance and a potent candidate for crop improvement. Plant Cell Rep 39:1381–1393. https://doi.org/10.1007/s00299-020-02588-y
Kiselev KV, Suprun AR, Aleynova OA, Ogneva ZV, Kalachev AV, Dubrovina AS (2021) External dsRNA downregulates anthocyanin biosynthesis-related genes and affects anthocyanin Accumulation in Arabidopsis thaliana. Int J Mol Sci 22:6749. https://doi.org/10.3390/ijms22136749
Knogge W, Schmelzer E, Weissenbock G (1986) The role of chalcone synthase in the regulation of flavonoid biosynthesis in develo** oat primary leaves. Arch Biochem Biophys 250:364–372. https://doi.org/10.1016/0003-9861(86)90738-1
Kuang Y, Li X, Wang Z, Wang X, Wei H, Chen H, Hu W, Tang M (2023) Effects of Arbuscular Mycorrhizal Fungi on the growth and Root Cell Ultrastructure of Eucalyptus grandis under cadmium stress. J Fungi 9:140. https://doi.org/10.3390/jof9020140
Lachman J, Dudjak J, Miholova D, Kolihova D, Pivec V (2005) Effect of cadmium on flavonoid content in young barley (Hordeum sativum L.) plants. Plant Soil Environ 51:513–516. https://doi.org/10.17221/3625-Pse
Lan HN, Liu RY, Liu ZH, Li X, Li BZ, Yuan YJ (2023) Biological valorization of lignin to flavonoids. Biotechnol Adv 64:108107. https://doi.org/ARTN10810710.1016/j.biotechadv.2023.108107
Lao R, Guo Y, Hao W, Fang W, Li H, Zhao Z, Li T (2023) The role of lignin in the compartmentalization of Cadmium in Maize roots is enhanced by Mycorrhiza. J Fungi 9:852. https://doi.org/10.3390/jof9080852
Li Y, Kim JI, Pysh L, Chapple C (2015) Four isoforms of Arabidopsis 4-Coumarate: CoA ligase have overlap** yet distinct roles in Phenylpropanoid Metabolism. Plant Physiol 169:2409–2421. https://doi.org/10.1104/pp.15.00838
Li H, Liang J, Chen H, Ding G, Ma B, He N (2016a) Evolutionary and functional analysis of mulberry type III polyketide synthases. BMC Genomics 17:540. https://doi.org/10.1186/s12864-016-2843-7
Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH (2016b) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190. https://doi.org/10.1016/j.scitotenv.2016.07.124
Li Y, Liu X, Cai X, Shan X, Gao R, Yang S, Han T, Wang S, Wang L, Gao X (2017) Dihydroflavonol 4-Reductase genes from Freesia Hybrida Play important and partially overlap** roles in the biosynthesis of flavonoids. Front Plant Sci 8:428. https://doi.org/10.3389/fpls.2017.00428
Li J, Zhao AC, Yu MD, Li YF, Liu XQ, Chen XY (2018) Function analysis of anthocyanidin synthase from Morus alba L. by expression in bacteria and tobacco. Electron J Biotechn 36:9–14. https://doi.org/10.1016/j.ejbt.2018.09.001
Li L, Yan XY, Li J, Tian YS (2022) Physiological and gene expression responses to PEG-Simulated Drought and Cadmium stresses in Tartary Buckwheat seedlings. J Plant Growth Regul 41:3518–3529. https://doi.org/10.1007/s00344-021-10530-z
Liang JW, Wang ZH, Ren Y, Jiang ZJ, Chen H, Hu WT, Tang M (2023) The alleviation mechanisms of cadmium toxicity in Broussonetia papyrifera by arbuscular mycorrhizal symbiosis varied with different levels of cadmium stress. J Hazard Mater 459:132076. https://doi.org/ARTN13207610.1016/j.jhazmat.2023.132076
Lin CC, Chen LM, Liu ZH (2005) Rapid effect of copper on lignin biosynthesis in soybean roots. Plant Sci 168:855–861. https://doi.org/10.1016/j.plantsci.2004.10.023
Liu Q, Zheng L, He F, Zhao FJ, Shen Z, Zheng L (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387:323–336. https://doi.org/10.1007/s11104-014-2290-7
Liu TT, Yao RL, Zhao YC, Xu S, Huang CL, Luo J, Kong LY (2017) Cloning, Functional Characterization and Site-Directed Mutagenesis of 4-Coumarate: Coenzyme A Ligase (4CL) Involved in Coumarin Biosynthesis in Dunn. Front Plant Sci 8:4. https://doi.org/ARTN410.3389/fpls.2017.00004
Liu LW, Li W, Song WP, Guo MX (2018a) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219. https://doi.org/10.1016/j.scitotenv.2018.03.161
Liu QQ, Luo L, Zheng LQ (2018b) Lignins: Biosynthesis and Biological Functions in Plants. Int J Mol Sci 19:335. https://doi.org/ARTN33510.3390/ijms19020335
Liu HL, Su BB, Zhang H, Gong JX, Zhang BX, Liu YL, Du LJ (2019) Identification and Functional Analysis of a Flavonol Synthase Gene from Grape Hyacinth. Molecules 24:1579. https://doi.org/ARTN157910.3390/molecules24081579
Liu W, Feng Y, Yu S, Fan Z, Li X, Li J, Yin H (2021) The flavonoid biosynthesis network in plants. Int J Mol Sci 22:12824. https://doi.org/10.3390/ijms222312824
Liu D, Zheng K, Wang Y, Zhang Y, Lao R, Qin Z, Li T, Zhao Z (2022a) Harnessing an arbuscular mycorrhizal fungus to improve the adaptability of a facultative metallophytic poplar (Populus yunnanensis) to cadmium stress: physiological and molecular responses. J Hazard Mater 424:127430. https://doi.org/10.1016/j.jhazmat.2021.127430
Liu JY, Ahmad N, Hong YQ, Zhu MH, Zaman S, Wang N, Yao N, Liu XM (2022b) Molecular Characterization of an Isoflavone 2′-Hydroxylase Gene Revealed Positive Insights into Flavonoid Accumulation and Abiotic Stress Tolerance in Safflower. Molecules 27:8001. https://doi.org/ARTN800110.3390/molecules27228001
Liu XQ, Cheng S, Aroca R, Zou YN, Wu QS (2022c) Arbuscular mycorrhizal fungi induce flavonoid synthesis for mitigating oxidative damage of trifoliate orange under water stress. Environ Exp Bot 204:105089. https://doi.org/10.1016/j.envexpbot.2022.105089
Lorenzo M, Moldes D, Sanromán MÁ (2006) Effect of heavy metals on the production of several laccase isoenzymes by Trametes Versicolor and on their ability to decolourise dyes. Chemosphere 63:912–917. https://doi.org/10.1016/j.envexpbot.2022.105089
Luo J, Li X, ** Y, Traore I, Dong L, Yang G, Wang Y (2021) Effects of Arbuscular Mycorrhizal Fungi Glomus mosseae on the growth and Medicinal Components of Dysosma Versipellis under copper stress. Bull Environ Contam Toxicol 107:924–930. https://doi.org/10.1007/s00128-019-02780-1
Ma QH, Xu Y (2008) Characterization of a caffeic acid 3-O-methyltransferase from wheat and its function in lignin biosynthesis. Biochimie 90:515–524. https://doi.org/10.1016/j.biochi.2007.09.016
Mechri B, Tekaya M, Attia F, Hammami M, Chehab H (2020) Drought stress improved the capacity of Rhizophagus Irregularis for inducing the accumulation of oleuropein and mannitol in olive (Olea europaea) roots. Plant Physiol Bioch 156:178–191. https://doi.org/10.1016/j.plaphy.2020.09.011
Mei X, Zhou C, Zhang W, Rothenberg DO, Wan S, Zhang L (2019) Comprehensive analysis of putative dihydroflavonol 4-reductase gene family in tea plant. PLoS ONE 14:e0227225. https://doi.org/10.1371/journal.pone.0227225
Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29:645–653. https://doi.org/10.1016/j.biotechadv.2011.04.006
Miransari M (2017) Arbuscular mycorrhizal fungi and heavy metal tolerance in plants. Arbuscular mycorrhizas and stress tolerance of plants. Singapore Springer, Singapore, pp 147–161. https://doi.org/10.1007/978-981-10-4115-0_7
Mollavali M, Perner H, Rohn S, Riehle P, Hanschen FS, Schwarz D (2018) Nitrogen form and mycorrhizal inoculation amount and timing affect flavonol biosynthesis in onion (Allium cepa L). Mycorrhiza 28:59–70. https://doi.org/10.1007/s00572-017-0799-3
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Map** and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628. https://doi.org/10.1038/nmeth.1226
Moura JCMS, Bonine CAV, Viana JDF, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the Lignin content and composition in plants. J Integr Plant Biol 52:360–376. https://doi.org/10.1111/j.1744-7909.2010.00892.x
Niu EL, Hu WJ, Ding J, Wang W, Romero A, Shen GX, Zhu SL (2022) GC-MS/LC-MS and transcriptome analyses revealed the metabolisms of fatty acid and flavonoid in olive fruits (Olea europaea L.). Sci Hortic-Amsterdam 299:111017. https://doi.org/ARTN11101710.1016/j.scienta.2022.111017
Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible WR, Stitt M (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49:463–491. https://doi.org/10.1111/j.1365-313X.2006.02979.x
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
Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci 5:e47. https://doi.org/10.1017/jns.2016.41
Park SI, Park HL, Bhoo SH, Lee SW, Cho MH (2021) Biochemical and molecular characterization of the Rice Chalcone Isomerase Family. Plants (Basel) 10:2064. https://doi.org/10.3390/plants10102064
Pawlak-Sprada S, Stobiecki M, Deckert J (2011) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part II. Profiling of isoflavonoids and their glycoconjugates induced in roots of lupine (Lupinus luteus) seedlings treated with cadmium and lead. Acta Biochim Pol 58:217–223
Penailillo J, Olivares G, Moncada X, Payacan C, Chang CS, Chung KF, Matthews PJ, Seelenfreund A, Seelenfreund D (2016) Sex distribution of Paper Mulberry (Broussonetia papyrifera) in the Pacific. PLoS ONE 11:e0161148. https://doi.org/10.1371/journal.pone.0161148
Peng XJ, Liu H, Chen PL, Tang F, Hu YM, Wang FF, Pi Z, Zhao ML, Chen NZ, Chen H, Zhang XK, Yan XQ, Liu M, Fu XJ, Zhao GF, Yao P, Wang LL, Dai H, Li XM, **ong W, Xu WC, Zheng HK, Yu HY, Shen SH (2019) A Chromosome-Scale Genome Assembly of Paper Mulberry (Broussonetia papyrifera) provides New insights into its forage and papermaking usage. Mol Plant 12:661–677. https://doi.org/10.1016/j.molp.2019.01.021
Peng XP, Bian J, Yao SQ, Ma CY, Wen JL (2021) Effects of P-Coumarate 3-Hydroxylase Downregulation on the Compositional and Structural Characteristics of Lignin and Hemicelluloses in Poplar Wood (Populus alba× Populus glandulosa). Front Bioeng Biotech 9:790539. https://doi.org/ARTN79053910.3389/fbioe.2021.790539
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 55:158–IN18. https://doi.org/10.1016/S0007-1536(70)80110-3
Phillips DA, Tsai SM (1992) Flavonoids as plant signals to rhizosphere microbes. Mycorrhiza 1:55–58. https://doi.org/10.1007/BF00206136
Qi X, Shuai Q, Chen H, Fan L, Zeng Q, He N (2014) Cloning and expression analyses of the anthocyanin biosynthetic genes in mulberry plants. Mol Genet Genomics 289:783–793. https://doi.org/10.1007/s00438-014-0851-3
Qin JC, Zhang YM, Lang CY, Yao YH, Pan HY, Li X (2012) Cloning and functional characterization of a caffeic acid O-methyltransferase from Trigonella foenum-graecum L. Mol Biol Rep 39:1601–1608. https://doi.org/10.1007/s11033-011-0899-7
Quan L, Zhang J, Wei Q, Wang Y, Qin C, Hu F, Chen Y, Shen Z, **a Y (2021) Promotion of Zinc Tolerance, Acquisition and translocation of Phosphorus in Mimosa pudica L. mediated by Arbuscular Mycorrhizal Fungi. Bull Environ Contam Toxicol 106:507–515. https://doi.org/10.1007/s00128-021-03113-x
Rashad Y, Aseel D, Hammad S, Elkelish A (2020) Rhizophagus Irregularis and Rhizoctonia solani differentially elicit systemic transcriptional expression of Polyphenol Biosynthetic pathways genes in sunflower. Biomolecules 10:379. https://doi.org/10.3390/biom10030379
Ren L, Zhang N, Wu P, Huo H, Xu G, Wu G (2015) Arbuscular mycorrhizal colonization alleviates Fusarium wilt in watermelon and modulates the composition of root exudates. Plant Growth Regul 77:77–85. https://doi.org/10.1007/s10725-015-0038-x
Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y, Zhou Y, Anastopoulos I, Wang X (2021) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J Hazard Mater 402:123919. https://doi.org/10.1016/j.jhazmat.2020.123919
Rivera-Becerril F, van Tuinen D, Martin-Laurent F, Metwally A, Dietz KJ, Gianinazzi S, Gianinazzi-Pearson V (2005) Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16:51–60. https://doi.org/10.1007/s00572-005-0016-7
Riyazuddin R, Nisha N, Ejaz B, Khan MIR, Kumar M, Ramteke PWW, Gupta R (2022) A Comprehensive Review on the Heavy Metal Toxicity and Sequestration in Plants. Biomolecules 12:43. https://doi.org/ARTN4310.3390/biom12010043
Rodrigues JL, Rodrigues LR (2022) Microbial production of caffeic acid. Microbial Production of Food Bioactive compounds. Springer, Cham, pp 1–34. https://doi.org/10.1007/978-3-030-81403-8_9-1
Ruan H, Shi X, Gao L, Rashid A, Li Y, Lei T, Dai X, **a T, Wang Y (2022) Functional analysis of the dihydroflavonol 4-reductase family of Camellia sinensis: exploiting key amino acids to reconstruct reduction activity. Hortic Res 9:098. https://doi.org/10.1093/hr/uhac098
Saito K, Linquist B, Keobualapha B, Shiraiwa T, Horie T (2009) Broussonetia papyrifera (paper mulberry): its growth, yield and potential as a fallow crop in slash-and-burn upland rice system of northern Laos. Agroforest Syst 76:525–532. https://doi.org/10.1007/s10457-009-9206-1
Sävenstrand H, Strid Å (2004) Six genes strongly regulated by mercury in Pisum sativum roots. Plant Physiol Bioch 42:135–142. https://doi.org/10.1016/j.plaphy.2003.11.005
Scervino JM, Ponce MA, Erra-Bassells R, Bompadre J, Vierheilig H, Ocampo JA, Godeas A (2007) The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Can J Microbiol 53:702–709. https://doi.org/10.1139/W07-036
Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633. https://doi.org/10.1016/j.jplph.2004.08.010
Schilmiller AL, Stout J, Weng JK, Humphreys J, Ruegger MO, Chapple C (2009) Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J 60:771–782. https://doi.org/10.1111/j.1365-313X.2009.03996.x
Selvaraj A, Thangavel K, Uthandi S (2020) Arbuscular mycorrhizal fungi (Glomus intraradices) and diazotrophic bacterium (Rhizobium BMBS) primed defense in blackgram against herbivorous insect (Spodoptera litura) infestation. Microbiol Res 231:126355. https://doi.org/10.1016/j.micres.2019.126355
Sheteiwy MS, Abd Elgawad H, **ong YC, Macovei A, Brestic M, Skalicky M, Shaghaleh H, Hamoud YA, El-Sawah AM (2021) Inoculation with Bacillus amyloliquefaciens and mycorrhiza confers tolerance to drought stress and improve seed yield and quality of soybean plant. Physiol Plant 172:2153–2169. https://doi.org/10.1111/ppl.13454
Shi JW, Yan X, Sun TT, Shen YX, Shi Q, Wang W, Bao MZ, Luo H, Nian FZ, Ning GG (2022) Homeostatic regulation of flavonoid and lignin biosynthesis in phenylpropanoid pathway of transgenic tobacco. Gene 809:146017. https://doi.org/ARTN14601710.1016/j.gene.2021.146017
Shimada N, Akashi T, Aoki T, Ayabe SI (2000) Induction of isoflavonoid pathway in the model legume Lotus japonicus: molecular characterization of enzymes involved in phytoalexin biosynthesis. Plant Sci 160:37–47. https://doi.org/10.1016/S0168-9452(00)00355-1
Su N, Ling F, **ng A, Zhao H, Zhu Y, Wang Y, Deng X, Wang C, Xu X, Cui J, Shen Z, **a Y (2020) Lignin synthesis mediated by CCoAOMT enzymes is required for the tolerance against excess Cu in Oryza sativa. Environ Exp Bot 175:104059. https://doi.org/10.1016/j.envexpbot.2020.104059
Sun SC, **ong XP, Zhang XL, Feng HJ, Zhu QH, Sun J, Li YJ (2020) Characterization of the Gh4CL gene family reveals a role of Gh4CL7 in drought tolerance. Bmc Plant Biol 20: 1–15. https://doi.org/ARTN6510.1186/s12870-021-02834-9
Sychta K, Slomka A, Kuta E (2021) Insights into Plant Programmed Cell Death Induced by Heavy Metals-Discovering a terra incognita. Cells 10:65. https://doi.org/ARTN6510.3390/cells10010065
Symonowicz M, Kolanek M (2012) Flavonoids and their properties to form chelate complexes. Food Sci Biotechnol 76:35–41
Tan Z, Liu R, Hu Y, Lin Z (2012) Production of isoflavone genistein in transgenic IFS tobacco roots and its role in stimulating the development of arbuscular mycorrhiza. Acta Physiol Plant 34:1863–1871. https://doi.org/10.1007/s11738-012-0984-0
Tian BL, Pei YC, Huang W, Ding JQ, Siemann E (2021) Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant. Isme J 15:1919–1930. https://doi.org/10.1038/s41396-021-00894-1
Volpin H, Phillips DA, Okon Y, Kapulnik Y (1995) Suppression of an Isoflavonoid Phytoalexin Defense Response in Mycorrhizal Alfalfa roots. Plant Physiol 108:1449–1454. https://doi.org/10.1104/pp.108.4.1449
Wang CH, Yu J, Cai YX, Zhu PP, Liu CY, Zhao AC, Lu RH, Li MJ, Xu FX, Yu MD (2016) Correction: characterization and functional analysis of 4-Coumarate: CoA ligase genes in Mulberry. PLoS ONE 11:e0157414. https://doi.org/10.1371/journal.pone.0157414
Wang X, Liang J, Liu Z, Kuang Y, Han L, Chen H, **e X, Hu W, Tang M (2022) Transcriptional regulation of metal metabolism-and nutrient absorption-related genes in Eucalyptus grandis by arbuscular mycorrhizal fungi at different zinc concentrations. BMC Plant Biol 22:76. https://doi.org/10.1186/s12870-022-03456-5
Westfall A, Sigurdson GT, Giusti MM (2019) Antioxidant, UV Protection, and Antiphotoaging properties of anthocyanin-pigmented lipstick formulations. J Cosmet Sci 70:63–76
Wu QS (2017) Arbuscular mycorrhizas and stress tolerance of plants. Springer Berlin Heidelberg, New York. https://doi.org/10.1007/978-981-10-4115-0
Wu JT, Wang L, Zhao L, Huang XC, Ma F (2020) Arbuscular mycorrhizal fungi effect growth and photosynthesis of Phragmites australis (Cav.) Trin ex. Steudel under copper stress. Plant Biol 22:62–69. https://doi.org/10.1111/plb.13039
**e DY, Jackson LA, Cooper JD, Ferreira D, Paiva NL (2004) Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol-4-reductase from Medicago truncatula. Plant Physiol 134:979–994. https://doi.org/10.1104/pp.103.030221
**e G, Meng X, Wang F, Bao Y, Huo J (2017) Eriodictyol attenuates arsenic trioxide-induced liver injury by activation of Nrf2. Oncotarget 8:68668. https://doi.org/10.18632/oncotarget.19822
Xu F, Li L, Zhang W, Cheng H, Sun N, Cheng S, Wang Y (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 CG, Tang TX, Chen R, Liang CH, Liu XY, Wu CL, Yang YS, Yang DP, Wu H (2014) A comparative study of bioactive secondary metabolite production in diploid and tetraploid Echinacea purpurea (L.) Moench. Plant Cell Tiss Org 116:323–332. https://doi.org/10.1007/s11240-013-0406-z
Yan Q, Si JR, Cui XX, Peng H, Chen X, **ng H, Dou DL (2019) The soybean cinnamate 4-hydroxylase gene GmC4H1 contributes positively to plant defense via increasing lignin content. Plant Growth Regul 88:139–149. https://doi.org/10.1007/s10725-019-00494-2
Yang YJ, Cheng LM, Liu ZH (2007) Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci 172:632–639. https://doi.org/10.1016/j.plantsci.2006.11.018
Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of Arbuscular Mycorrhizal Fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE 10:e0145726. https://doi.org/10.1371/journal.pone.0145726
Yang CX, Zhao WN, Wang YN, Zhang L, Huang SC, Lin JX (2020) Metabolomics Analysis Reveals the Alkali Tolerance Mechanism in Puccinellia tenuiflora Plants Inoculated with Arbuscular Mycorrhizal Fungi. Microorganisms 8:327. https://doi.org/ARTN32710.3390/microorganisms8030327
Yao K, Wang Y, Wu Y (2022) Competition and niche differentiation of Water and nutrients between Broussonetia papyrifera and Platycladus orientalis under prolonged Drought stress. Agronomy 12:1489. https://doi.org/10.3390/agronomy12071489
Yin YC, Zhang XD, Gao ZQ, Hu T, Liu Y (2019) The Research Progress of Chalcone isomerase (CHI) in plants. Mol Biotechnol 61:32–52. https://doi.org/10.1007/s12033-018-0130-3
Zamora P, Pardo A, Fierro A, Prieto H, Zuniga GE (2013) Molecular characterization of the chalcone isomerase gene family in Deschampsia antarctica. Polar Biol 36:1269–1280. https://doi.org/10.1007/s00300-013-1346-0
Zeng P, Guo ZH, **ao XY, Peng C, Huang B, **n LQ (2018) Effect of phytoremediation with Broussonetia papyrifera on the biological quality in soil contaminated with heavy metals. China Environ Sci 38:2639–2645
Zhang M, Fang YM, Ji YH, Jiang ZP, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot 85:1–9. https://doi.org/10.1016/j.sajb.2012.11.005
Zhang H, Du C, Wang Y, Wang J, Zheng L, Wang Y (2016) The Reaumuria trigyna leucoanthocyanidin dioxygenase (RtLDOX) gene complements anthocyanidin synthesis and increases the salt tolerance potential of a transgenic Arabidopsis LDOX mutant. Plant Physiol Bioch 106:278–287. https://doi.org/10.1007/s10265-021-01315-2
Zhang JR, Trossat-Magnin C, Bathany K, Delrot S, Chaudiere J (2019a) Oxidative Transformation of Leucocyanidin by Anthocyanidin synthase from Vitis vinifera leads only to Quercetin. J Agric Food Chem 67:3595–3604. https://doi.org/10.1021/acs.jafc.8b06968
Zhang XF, Hu ZH, Yan TX, Lu RR, Peng CL, Li SS, **g YX (2019b) Arbuscular mycorrhizal fungi alleviate cd phytotoxicity by altering Cd subcellular distribution and chemical forms in Zea mays. Ecotox Environ Safe 171:352–360. https://doi.org/10.1016/j.ecoenv.2018.12.097
Zhao HY, Guan JL, Liang Q, Zhang XY, Hu HL, Zhang J (2021) Effects of cadmium stress on growth and physiological characteristics of sassafras seedlings. Sci Rep 11:9913. https://doi.org/ARTN991310.1038/s41598-021-89322-0
Zhao XY, Li PP, Li C, **a T (2022) The Key Regulators and Metabolic Intermediates of Lignin Response to Low Temperatures Revealed by Transcript and Targeted Metabolic Profiling Analysis in Poplar. Agronomy 12:2506. https://doi.org/ARTN250610.3390/agronomy12102506
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 HH, Zhang RQ, Chen WL, Gu ZH, **e XL, Zhao HQ, Yao Q (2015) The possible involvement of salicylic acid and hydrogen peroxide in the systemic promotion of phenolic biosynthesis in clover roots colonized by arbuscular mycorrhizal fungus. J Plant Physiol 178:27–34. https://doi.org/10.1016/j.jplph.2015.01.016
Zhu Y, Peng Q, Li K, **e DY (2018) Molecular cloning and functional characterization of a dihydroflavonol 4-Reductase from Vitis bellula. Molecules 23:861. https://doi.org/10.3390/molecules23040861
Zhuang WB, Li YH, Shu XC, Pu YT, Wang XJ, Wang T, Wang Z (2023) The Classification, Molecular Structure and Biological Biosynthesis of Flavonoids, and Their Roles in Biotic and Abiotic Stresses. Molecules 28:3599. https://doi.org/ARTN359910.3390/molecules28083599
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The authors are grateful to Prof. David Janos, Editor-in-Chief of this journal, and to the two reviewers for their instructive advice and useful suggestions on both language and academic aspects.
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This study was financially supported by the National Natural Science Foundation of China (32001289), and the Laboratory of Lingnan Modern Agriculture Project, grant number (NZ2021025).
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Conceptualization, W.H., L.P. and S.D.; Data collection and analysis, S.D., T.K. and J.L.; Project administration, W.H. and M.T.; Supervision, W.H.; Writing—original draft, S.D. and L.P.; Writing—review and editing, M.T., W.H., L.P., R.Z., and H.C.
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Deng, S., Pan, L., Ke, T. et al. Rhizophagus Irregularis regulates flavonoids metabolism in paper mulberry roots under cadmium stress. Mycorrhiza (2024). https://doi.org/10.1007/s00572-024-01155-7
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DOI: https://doi.org/10.1007/s00572-024-01155-7