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Metabolomic approaches for the identification of flavonoids associated with weed suppression in selected Hardseeded annual pasture legumes

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Abstract

Background and aims

Weed suppressive potential of annual pasture legumes has been previously described, the mechanism of interference with weeds has not been clearly elucidated. We, therefore, aimed to delineate the role of secondary metabolites synthesized and released by pasture legumes through a series of studies to: 1) characterize key metabolites present in plant tissues, residue and the rhizosphere and 2) correlate their presence with weed suppressive properties.

Methods

Field and in vitro experimentations coupled with targeted and non-targeted metabolic profiling was performed to evaluate the abundance of key phytotoxic metabolites using UHPLC QTOF-MS. Further, those metabolites strongly correlated with weed suppression and phytotoxicity were predicted by chemometric analyses and their concentration evaluated in field soils collected from the same legume site.

Results

Field experimentation, methanolic extracts and dried residues of Biserrula pelecinus L. and Ornithopus compressus L. exhibited marked phytotoxicity in a series of laboratory experiments. Metabolic profiling revealed that both foliar tissues and rhizosphere soils of pasture legumes possessed a high abundance of flavonoids and their precursors. Chemometric analyses suggested the strong association of quercetin, isoquercetin, kaempferol, and kaempferol-7-O-glucoside with weed suppression under field conditions. Specifically, the abundance of quercetin and kaempferol was significantly higher in soils collected from established stands of biserrula and yellow serradella in contrast to arrowleaf, gland and subterranean clover.

Conclusion

Current study provided an evidence for the role of certain annual legume-produced flavonoids in weed suppression in southern Australia and further insight into their localization and release in the soil rhizosphere.

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References

  • Albuquerque MB, Cavalcanti dos Santos R, Lima LM, de Albuquerque Melo Filho P, Custódio Nogueira RJM, Gomes da Câmara CA, de Rezende RA (2011) Allelopathy, an alternative tool to improve cropping systems. A review. Agron Sustain Dev 31:379–395

    Google Scholar 

  • Bais HP, Walker TS, Kennan AJ, Stermitz FR, Vivanco JM (2003) Structure-dependent phytotoxicity of catechins and other flavonoids: flavonoid conversions by cell-free protein extracts of Centaurea maculosa (spotted knapweed) roots. J Agric Food Chem 51:897–901

    PubMed  CAS  Google Scholar 

  • Barnes JP, Putnam AR, Burke BA, Aasen AJ (1987) Isolation and characterization of allelochemicals in rye herbage. Phytochemistry 26(5):1385–1390

    CAS  Google Scholar 

  • Basile A, Sorbo S, Giordano S, Ricciardi L, Ferrara S, Montesano D, Castaldo Cobianchi R, Vuotto ML, Ferrara L (2000) Antibacterial and allelopathic activity of extract from Castanea sativa leaves. Fitoterapia 71:S110–S116

    PubMed  CAS  Google Scholar 

  • Bertin C, Weston LA, Huang T, Jander G, Owens T, Meinwald J, Schroeder FC (2007) Grass roots chemistry: meta-tyrosine, an herbicidal nonprotein amino acid. Proc Natl Acad Sci 104:16964–16969

    PubMed  CAS  Google Scholar 

  • Bhadoria P (2011) Allelopathy: a natural way towards weed management. Am J Experimental Agr 1:7

    Google Scholar 

  • Breitling R, Ceniceros A, Jankevics A, Takano E (2013) Metabolomics for secondary metabolite research. Metabolites 3:1076–1083

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cao H, Chen X, Jassbi AR, Xiao J (2015) Microbial biotransformation of bioactive flavonoids. Biotech Adv 33:214–223

    CAS  Google Scholar 

  • Carlsen SCK, Fomsgaard IS (2008) Biologically active secondary metabolites in white clover (Trifolium repens L.) – a review focusing on contents in the plant, plant–pest interactions and transformation. Chemoecology 18:129–170

    CAS  Google Scholar 

  • Carlsen SC, Mortensen AG, Oleszek W, Piacente S, Stochmal A, Fomsgaard IS (2008) Variation in flavonoids in leaves, stems and flowers of white clover cultivars. Nat Prod Commun 3:1299–1306

    CAS  Google Scholar 

  • Carlsen SCK, Pedersen HA, Spliid NH, Fomsgaard IS (2012) Fate in soil of flavonoids released from white clover (Trifolium repens L.). Appl Environ Soil Sci 2012:1–10

    Google Scholar 

  • Ciegler A, Lindenfelser LA, Nelson GE (1971) Microbial transformation of flavonoids. Appl Microbiol 22:974–979

    PubMed  PubMed Central  CAS  Google Scholar 

  • Clayton G, Rice W, Lupwayi N, Turkington T (1997) Sustainability of legume-based conservation tillage systems. Final Technical Rep on CAESA Project

    Google Scholar 

  • Dayan FE, Duke SO (2014) Natural compounds as next generation herbicides. Plant Physiol: pp 114(239061)

  • Dayan FE, Rimando AM, Pan Z, Baerson SR, Gimsing AL, Duke SO (2010) Sorgoleone. Phytochemistry 71:1032–1039

    PubMed  CAS  Google Scholar 

  • De Martino L, Mencherini T, Mancini E, Aquino RP, De Almeida LFR, De Feo V (2012) In vitro phytotoxicity and antioxidant activity of selected flavonoids. Int J Mol Sci 13:5406–5419

    PubMed  PubMed Central  Google Scholar 

  • Deng S, West BJ, Jensen CJ (2013) UPLC-TOF-MS characterization and identification of bioactive Iridoids in Cornus mas fruit. J Anal Methods Chem 2013:710972

    PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Sumner LW (2003) Legume natural products: understanding and manipulating complex pathways for human and animal health. Plant Physiol 131:878–885

    PubMed  PubMed Central  CAS  Google Scholar 

  • Duke SO (2015) Proving allelopathy in crop–weed interactions. Weed Sci 63:121–132

    Google Scholar 

  • Einhellig FA (1996) Interactions involving allelopathy in cropping systems. Agron J 88:886–893

    CAS  Google Scholar 

  • Einhellig FA (2018) Allelopathy—a natural protection, allelochemicals. Handbook of natural pesticides: methods CRC Press

  • Gholami A, De Geyter N, Pollier J, Goormachtig S, Goossens A (2014) Natural product biosynthesis in Medicago species. Nat Prod Rep 31(3):356–380

    PubMed  CAS  Google Scholar 

  • Gomaa NH, Hassan MO, Fahmy GM, González L, Hammouda O, Atteya AM (2015) Flavonoid profiling and nodulation of some legumes in response to the allelopathic stress of Sonchus oleraceus L. Acta Botanica Brasilica 29:553–560

    Google Scholar 

  • Grata E, Boccard J, Guillarme D, Glauser G, Carrupt P-A, Farmer EE, Wolfender J-L, Rudaz S (2008) UPLC–TOF-MS for plant metabolomics: a sequential approach for wound marker analysis in Arabidopsis thaliana. J Chromatogr B 871:261–270

    CAS  Google Scholar 

  • Griffiths WJ, Wang Y (2009) Mass spectrometry: from proteomics to metabolomics and lipidomics. Chem Soc Rev 38:1882–1896

    PubMed  CAS  Google Scholar 

  • Hale C, Lowther W, Lloyd J (1979) Effect of inoculant formulation on survival of rhizobium trifolii and the establishment of oversown white clover (Trifolium repens). N Z J Exp Agric 7:311–314

    Google Scholar 

  • Hartwig UA, Joseph CM, Phillips DA (1991) Flavonoids released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti. Plant Physiol 95:797–803

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hassan S, Mathesius U (2012) The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444

    PubMed  CAS  Google Scholar 

  • Hiradate S, Ohse K, Furubayashi A, Fujii Y (2010) Quantitative evaluation of allelopathic potentials in soils: total activity approach. Weed Sci 58:258–264

    CAS  Google Scholar 

  • Hoffman ML, Weston LA, Snyder JC, Regnier EE (1996) Allelopathic influence of germinating seeds and seedlings of cover crops on weed species. Weed Sci 579–584

    CAS  Google Scholar 

  • Howieson JG, O’Hara GW, Carr SJ (2000) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crop Res 65(2–3):107–122

    Google Scholar 

  • Inderjit (1996) Plant phenolics in allelopathy. Bot Rev 62:186–202

    Google Scholar 

  • Inderjit CRM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11

    CAS  Google Scholar 

  • Inderjit WL (2000) Are laboratory bioassays for allelopathy suitable for prediction of field responses? J Chem Ecol 26:2111–2118

    CAS  Google Scholar 

  • Isbell R (1996) The Australian soil classification. Australian soil and land survey handbook, vol 4. CSIRO Publishing, Melbourne, Vic

    Google Scholar 

  • Jabran K (2017) Rye allelopathy for weed control. In: Jabran K (ed) Manipulation of Allelopathic crops for weed control. Springer International Publishing, Cham

    Google Scholar 

  • Jannink J-L, Orf JH, Jordan NR, Shaw RG (2000) Index selection for weed suppressive ability in soybean contribution no. 00-13-0146 of the Minnesota Agric. Exp. Stn., Univ. of Minnesota, St. Paul, MN. 1 mention of any product is for scientific purposes only and does not imply endorsement by the Minnesota agricultural Experiment Station. Crop Sci 40:1087–1094

    Google Scholar 

  • Kalinova J, Vrchotova N (2009) Level of Catechin, Myricetin, quercetin and Isoquercitrin in buckwheat (Fagopyrum esculentum Moench), changes of their levels during vegetation and their effect on the growth of selected weeds. J Agric Food Chem 57:2719–2725

    PubMed  CAS  Google Scholar 

  • Keating KI (1999) Allelopathy: principles, procedures, processes, and promises for biological control. Elsevier, Adv Agron

    Google Scholar 

  • Kim HK, Choi YH, Verpoorte R (2010) NMR-based metabolomic analysis of plants. Nat Protoc 5:536–549

    PubMed  CAS  Google Scholar 

  • Kuang Y, Yang SX, Sampietro DA, Zhang XF, Tan J, Gao QX, Liu HW, Ni QX, Zhang YZ (2017) Phytotoxicity of leaf constituents from bamboo (Shibataea chinensis Nakai) on germination and seedling growth of lettuce and cucumber. Allelopathy J 40:133–142

    Google Scholar 

  • Latif S, Chiapusio G, Weston LA (2017) Chapter two - allelopathy and the role of Allelochemicals in plant Defence. In: Becard G (ed) Adv Bot Res. Academic Press

  • Latif S, Gurusinghe S, Weston PA, Brown B, Quinn J, Piltz J, Weston L (2019a) Performance and weed suppressive potential of selected pasture legumes against annual weeds in southeastern Australia. Crop Pasture Sci

    Google Scholar 

  • Latif S, Gurusinghe S, Weston PA, Brown WB, Quinn JC, Piltz JW, Weston LA (2019b) Performance and weed-suppressive potential of selected pasture legumes against annual weeds in South-Eastern Australia. Crop Pasture Sci 70:147–158

    Google Scholar 

  • Leather GR, Einhellig FA (1988) Bioassay of naturally occurring allelochemicals for phytotoxicity. J Chem Ecol 14:1821–1828

    PubMed  CAS  Google Scholar 

  • Li Z-H, Wang Q, Ruan X, Pan C-D, Jiang D-A (2010) Phenolics and plant allelopathy. Molecules 15:8933–8952

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu H-C, Yang C-A, Liu RH, Lin D-L (2017) Developing a UHPLC–QTOF-MS and automated library search method for screening drugs and toxic compounds in postmortem specimens. J Anal Toxicol 41:421–430

    PubMed  CAS  Google Scholar 

  • Loi A, Howieson JG, Nutt BJ, Carr SJ (2005) A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems. Aust J Exp Agr 45:289–299

    Google Scholar 

  • Macfarlane MJ, Scott D, Jarvis P (1982) Allelopathic Effects of White Clover .2. Field Investigations in Tussock Grasslands. New Zeal J Agr Res 25: 511–518, Allelopathic effects of white clover 2. Field investigations in tussock grasslands

    Google Scholar 

  • Mahmood K, Khan MB, Song YY, Ijaz M, Luo SM, Zeng RS (2013) UV-irradiation enhances rice allelopathic potential in rhizosphere soil. Plant Growth Regul 71:21–29

    CAS  Google Scholar 

  • Mathesius U (2018) Flavonoid Functions in Plants and Their Interactions with Other Organisms. Plants 7(2):30

    PubMed Central  Google Scholar 

  • Munzuroglu O, Geckil H (2002) Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Arch Environ Contam Toxicol 43:203–213

    PubMed  CAS  Google Scholar 

  • Mwangi H, Kihurani A, Wesonga J, Ariga E, Kanampiu F (2015) Effect of Lablab purpureus L. cover crop and imidazolinone resistant (IR) maize on weeds in drought prone areas, Kenya. Crop Prot 72:36–40

    Google Scholar 

  • Nakabayashi R, Saito K (2015) Integrated metabolomics for abiotic stress responses in plants. Curr Opin Plant Biol 24:10–16

    PubMed  CAS  Google Scholar 

  • Nichols PGH, Revell CK, Humphries AW, Howie JH, Hall EJ, Sandral GA, Ghamkhar K, Harris CA (2012) Temperate pasture legumes in Australia—their history, current use, and future prospects. Crop Pasture Sci 63(9):691–725

  • Okada S, Iwasaki A, Kataoka I, Suenaga K, Kato-Noguchi H (2018) Isolation and identification of a phytotoxic substance in kiwifruit leaves. 1218 edn. International Society for Horticultural Science (ISHS), Leuven, Belgium

  • Pandya SM, Pota KB (1978) Allelopathic potentials of root exudates from different ages of celosia-Argentea Linn - weed. National Academy Science Letters-India 1:56–58

    Google Scholar 

  • Parker C (1966) The importance of shoot entry in the action of herbicides applied to the soil. Weeds 14(2):117–121

    CAS  Google Scholar 

  • Patel D, Kumbhar B (2016) Weed and its management: a major threats to crop economy. Journal of Pharmaceutical Sciences and Bioscientific Research 6:453–758

    Google Scholar 

  • Powles SB, Yu Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347

    PubMed  CAS  Google Scholar 

  • Razzaq A, Cheema Z, Jabran K, Hussain M, Farooq M, Zafar M (2012) Reduced herbicide doses used together with allelopathic sorghum and sunflower water extracts for weed control in wheat. J Plant Prot Res 52:281–285

    CAS  Google Scholar 

  • Seal AN, Pratley JE, Haig T (2008) Can results from a laboratory bioassay be used as an indicator of field performance of rice cultivars with allelopathic potential against Damasonium minus (starfruit)? Aust J Agric Res 59:183–188

    Google Scholar 

  • Shah SMM, Sadiq A, Shah SMH, Khan S (2014) Extraction of saponins and toxicological profile of Teucrium stocksianum boiss extracts collected from district swat, Pakistan. Biol Res 47:65–65

    PubMed  PubMed Central  Google Scholar 

  • Siddiqui S, Yadav R, Yadav K, Wani FA, Meghvansi MK, Sharma S, Jabeen F (2009) Allelopathic potentialities of different concentration of aqueous leaf extracts of some arable trees on germination and radicle growth of Cicer arietinum Var.–C-235. G J M S 4:91–95

    Google Scholar 

  • Singh HP, Batish DR, Kaur S, Arora K, Kohli RK (2006) Alpha-Pinene inhibits growth and induces oxidative stress in roots. Ann Bot 98:1261–1269

    PubMed  PubMed Central  CAS  Google Scholar 

  • Teasdale JR, Rice CP, Cai G, Mangum RW (2012) Expression of allelopathy in the soil environment: soil concentration and activity of benzoxazinoid compounds released by rye cover crop residue. Plant Ecol 213:1893–1905

    Google Scholar 

  • Uddin M, Won O-J, Pyon J-Y (2010) Herbicidal effects and crop selectivity of sorgoleone, a sorghum root exudate under greenhouse and field conditions. Korean Journal of Weed Science 30:412–420

    Google Scholar 

  • Wang CM, Jhan YL, Yen LS, Su YH, Chang CC, Wu YY, Chang CI, Tsai SY, Chou CH (2013) The allelochemicals of litchi leaf and its potential as natural herbicide in weed control. Allelopathy J 32:157–173

    CAS  Google Scholar 

  • Wang R, Yang X, Song Y, Zhang M, Hu L, Su Y, Zeng R (2011) Allelopathic potential of Tephrosia vogelii Hook. F.: laboratory and field evaluation. Allelopathy J 28:53–62

    Google Scholar 

  • Wang X, Sun C, Gao S, Wang L, Shuokui H (2001) Validation of germination rate and root elongation as indicator to assess phytotoxicity with Cucumis sativus. Chemosphere 44:1711–1721

    PubMed  CAS  Google Scholar 

  • Weston LA, Burke B, Putnam A (1987) Isolation, characterization and activity of phytotoxic compounds from quackgrass [Agropyron repens (L.)Beauv.]. J Chem Ecol 13:403–421

    PubMed  CAS  Google Scholar 

  • Weston LA, Duke SO (2003) Weed and crop allelopathy. Crit Rev Plant Sci 22:367–389

    CAS  Google Scholar 

  • Weston LA, Harmon R, Mueller S (1989) Allelopathic potential of sorghum-sudangrass hybrid (sudex). J Chem Ecol 15:1855–1865

    PubMed  CAS  Google Scholar 

  • Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

    PubMed  CAS  Google Scholar 

  • Weston LA, Skoneczny D, Weston PA, Weidenhamer JD (2015) Metabolic profiling: an overview—new approaches for the detection and functional analysis of biologically active secondary plant products. Journal of Allelochemical Interactions 1:15–27

    Google Scholar 

  • Weston PA, Gurusinghe S, Birckhead E, Skoneczny D, Quinn JC, Weston LA (2019) Chemometric analysis of Amaranthus retroflexus in relation to livestock toxicity in southern Australia. Phytochemistry 161:1–10

    PubMed  CAS  Google Scholar 

  • Zhu Z-j, Schultz AW, Wang J, Johnson CH, Yannone SM, Patti GJ, Siuzdak G (2013) Liquid chromatography quadrupole time-of-flight mass spectrometry characterization of metabolites guided by the METLIN database. Nat Protoc 8:451–460

    PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge funding support from Meat and Livestock Australia (MLA) (Grant: B.WEE.0146 awarded to L.A. Weston and J. Piltz) for field trial research and the Australian Centre for International Agricultural Research (ACIAR) for sponsoring the PhD fellowship awarded to S. Latif for his studies associated with the project. The authors also wish to acknowledge Ulrike Mathesius of The Australian National University (Acton, ACT, Australia) for providing analytical standards of numerous flavonoids, Douglas Rutledge from AgroParis Tech (Paris, France) for his support in chemometric analysis, Dr. Russell Barrow for reviewing the manuscript and Dr. Willian Brown, Vincent West, Graeme Heath, Simon Flinn and Agasthya Thotagamuwa for their support in data collection and bioassay performance.

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Authors and Affiliations

  1. Graham Centre for Agricultural Innovation (NSW Department of Primary Industries), Locked Bag 588, Wagga Wagga, NSW, 2678, Australia

    Sajid Latif, Saliya Gurusinghe, Paul A. Weston, Jane C. Quinn, John W Piltz & Leslie A Weston

  2. School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW, 2678, Australia

    Sajid Latif & Jane C. Quinn

  3. School of Agriculture and Wine Sciences, Charles Sturt University, Wagga Wagga, NSW, 2678, Australia

    Paul A. Weston & Leslie A Weston

  4. NSW Department of Primary Industries, Agricultural Institute, Wagga Wagga, NSW, 2650, Australia

    John W Piltz

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  1. Sajid Latif
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  2. Saliya Gurusinghe
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  3. Paul A. Weston
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Correspondence to Sajid Latif.

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Latif, S., Gurusinghe, S., Weston, P.A. et al. Metabolomic approaches for the identification of flavonoids associated with weed suppression in selected Hardseeded annual pasture legumes. Plant Soil 447, 199–218 (2020). https://doi.org/10.1007/s11104-019-04225-4

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