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Responses of Lotus corniculatus to environmental change 3: The sensitivity of phenolic accumulation to growth temperature and light intensity and effects on tissue digestibility

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Abstract

Main Conclusion

Growth temperature and light intensity are major drivers of phenolic accumulation in Lotus corniculatus resulting in major changes in carbon partitioning which significantly affects tissue digestibility and forage quality.

Abstract

The response of plant growth, phenolic accumulation and tissue digestibility to light and temperature was determined in clonal plants of three genotypes of Lotus corniculatus (birdsfoot trefoil) cv Leo, with low, intermediate or high levels of proanthocyanidins (condensed tannins). Plants were grown from 10 °C to 30 °C, or at light intensities from 20 to 500 µm m−2 s−1. Plants grown at 25 °C had the highest growth rate and highest digestibility, whereas the maximum tannin concentration was found in plants grown at 15 °C. Approximately linear increases in leaf flavonol glycoside levels were found with increasing growth temperature in the low tannin genotype. Tannin hydroxylation increased with increasing growth temperature but decreased with increasing light intensity. The major leaf flavonols were kaempferol glycosides of which kaempferol-3-glucoside and kaempferol-3,7-dirhamnoside were the major components. Increases in both tannin and total flavonol concentrations in leaves were linearly related to light intensity and were preceded by a specific increase in the transcript level of a non-legume type chalcone isomerase. Changes in growth temperature and light intensity, therefore, result in major changes in the partitioning of carbon into phenolics, which significantly affects tissue digestibility and nutritional quality with a high correlation between tannin concentration and leaf digestibility.

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Change history

Abbreviations

BuOH:

n-Butanol

HCA:

Hydroxycinnamic acid

IVDMD:

In-vitro-dry-matter-digestibility

TGA:

Thioglycolic acid

References

  • Abeynayake SW, Panter S, Mouradov A, Spangenberg G (2011) A high-resolution method for the localization of proanthocyanidins in plant tissues. Plant Methods 7:13–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Acuña H, Concha A, Figueroa M (2008) Condensed tannin concentrations of three Lotus species grown in different environments. Chilean J Agric Res 68:31–34

    Article  Google Scholar 

  • Alison MW, Hoveland CS (1989) Birdsfoot trefoil management. 1. Root growth and carbohydrate storage. Agronomy J 81:739–745

    Article  Google Scholar 

  • Anuraga M, Duarsa P, Hill MJ, Lovett JV (1993) Soil moisture and temperature affect condensed tannin concentrations and growth in Lotus corniculatus and Lotus pedunculatus. Australian J Agric Res 44:1667–1681

    Article  Google Scholar 

  • Barahona R, Lascano CE, Narvaez N, Owen E, Morris P, Theodorou MK (2003) In vitro degradability of mature and immature leaves of tropical forage legumes differing in condensed tannin and non-starch polysaccharide concentration and composition. J Food Sci Agric 83:1256–1266

    Article  CAS  Google Scholar 

  • Barry TN, Duncan SJ (1984) The role of condensed tannins in the nutritional-value of Lotus pedunculatus for sheep. 1 Voluntary intake. British J Nutrition 51:485–491

    Article  CAS  Google Scholar 

  • Barry TN, Manley TR (1986) Interrelationships between the concentrations of total condensed tannins, free condensed tannin and lignin in Lotus sp. and their possible consequence in ruminant nutrition. J Sci Food Agric 37:248–254

    Article  CAS  Google Scholar 

  • Bavage AD, Davies IG, Robbins MP, Morris P (1997) Expression of an Antirrhinum dihydroflavonol reductase gene results in changes in condensed tannin structure and accumulation in root cultures of Lotus corniculatus (bird’s foot trefoil). Plant Mol Biol 35:443–458

    Article  CAS  PubMed  Google Scholar 

  • Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. Tansley Review No. 72. New Phytol 127:617–633

    Article  CAS  PubMed  Google Scholar 

  • Boyce PJ, Penaloza E, Volenec JJ (1992) Amylase activity in taproots of Medicago sativa L. and Lotus corniculatus L. following defoliation. J Exp Bot 43:1053–1059

    Article  CAS  Google Scholar 

  • Briggs MA, Schultz JC (1990) Chemical defence production in Lotus corniculatus L. II. Trade-off amongst growth, reproduction and defence. Oecologia 83:32–33

    Article  PubMed  Google Scholar 

  • Carron TR, Robbins MP, Morris P (1994) Genetic modification of condensed tannin biosynthesis in Lotus corniculatus. I. Heterologous antisense dihydroflavonol reductase down-regulates tannin accumulation in ‘hairy root’ cultures. Theor Appl Genet 87:1006–1015

    Article  CAS  PubMed  Google Scholar 

  • Carter EB, Theodorou MK, Morris P (1999) Responses of Lotus corniculatus to environmental change. 2. Effect of elevated CO2, temperature and drought on tissue digestion in relation to tannin and carbohydrate accumulation. J Sci Food Agric 79:1431–1440

    Article  CAS  Google Scholar 

  • Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15:2514–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Paiva N (1995) Stressed induced phenyl-propanoid metabolism. Plant Cell 7:1085–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Xie D-Y, Sharma SB (2005) Tansley review. Proanthocyanins: a final frontier in flavonoid research? New Phytol 165:9–28

    Article  CAS  PubMed  Google Scholar 

  • Ehike NJ, LeGare DG (1993) The effects of temperature and soil stress on the production of tannins in birdsfoot trefoil (Lotus corniculatus L.). Lotus Newslett 24:64–67

    Google Scholar 

  • Escaray FJ, Menendez AB, Gárriz A, Pieckenstain FL, Estrella MJ, Castagno LN, Carrasco P, Sanjuán J, Ruiza OA (2012) Ecological and agronomic importance of the plant genus Lotus. Its application in grassland sustainability and the amelioration of constrained and contaminated soils. Plant Sci 182:121–133

    Article  CAS  PubMed  Google Scholar 

  • Foo LY, Porter LJ (1981) The structure of tannins of some edible fruits. J Sci Food Agric 32:711–716

    Article  CAS  Google Scholar 

  • Foo LY, Newman R, Waghorn G, McNabb WC, Ulyatt MJ (1996) Proanthocyanidins from Lotus corniculatus. Phytochemistry 41:617–624

    Article  CAS  Google Scholar 

  • Foo LY, Lu Y, McNabb WC, Waghorn G, Ulyatta MJ (1997) Proanthocyanidins from Lotus pedunculatus. Phytochemistry 45:1689–1694

    Article  CAS  Google Scholar 

  • Foo LY, Lu Y, Molan AL, Woodfield DR, McNabb WC (2000) The phenols and prodelphinidins of white clover flowers. Phytochemistry 54:539–548

    Article  CAS  PubMed  Google Scholar 

  • Girard M, Dohme-Meier F, Kragten SA, Brinkhaus AG, Arrigo Y, Wyss U, Bee G (2018) Modification of the proportion of extractable and bound condensed tannins in bridsfoot trefoil (Lotus corniculatus) and sanfoin (Onobrychis vicifolia) during wilting, ensilage and pelleting processes. Biotechnol Animal Husb 34:1–19

    Article  Google Scholar 

  • He F, Pan QH, Shi Y, Duan CQ (2008) Biosynthesis and genetic regulation of proanthocyanidins in plants. Molecules 13(10):2674–2703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DI, Hayward MV (1973) A cellulase digestion technique for predicting the dry matter digestibility of grasses. J Sci Food Agric 24:1419–1426

    Article  CAS  PubMed  Google Scholar 

  • Kelman WM, Tanner GJ (1990) Foliar condensed tannin levels in lotus species growing on limed and unlimed soils in South-Eastern Australia. Proc NZ Grassl Assoc 52:51–54

    Google Scholar 

  • Kostopoulou P, Karatassiou M (2017) Lotus corniculatus L. response to carbon dioxide concentration and radiation level variations. Photosynthetica 55:522–531

    Article  CAS  Google Scholar 

  • Kunelius HT, Clark KW (1970) Influence of root temperature on the early growth and symbiotic nitrogen fixation of nodulated Lotus corniculatus plants. Can J Plant Sci 50:569–575

    Article  CAS  Google Scholar 

  • Lanot A (2004) The role of chalcone synthase and chalcone isomerase gene family members in controlling flavonoid and isoflavonoid accumulation in Lotus species. PhD Thesis, Aberystwyth University, UK

  • Lascano CE, Schidt A, Barahona R (2001) Forage quality and the environment. In: International Grassland Congress (19, 2001, Sao Pedro, Sao Paulo, Brazil). Proceedings of Grassland ecosystem: An outlook into the 21st Century. Brazilian Society of Animal Husbandry, Sao Pedro, Sao Paulo, BR, pp 1–19. https://hdl.handle.net/10568/56029

  • Lees GL, Hinks CF, Suttill NH (1994) Effect of high temperature on condensed tannin accumulation in leaf tissues of big trefoil (Lotus uliginosus Schkuhr). J Sci Food Agric 65:415–422

    Article  CAS  Google Scholar 

  • Li YG, Tanner GJ, Larkin PJ (1996a) The DMACA-HCl protocol and the threshold proanthocyanidin concentration for bloat safety in forage legumes. J Sci Food Agric 70:89–101

    Article  CAS  Google Scholar 

  • Li R, Volenec JJ, Joern BC, Cunningham SM (1996b) Seasonal changes in non-structural carbohydrates, protein, and macronutrients in roots of Alfalfa, Red clover, Sweet clover, and Birdsfoot-trefoil. Crop Sci 36:617–662

    Article  CAS  Google Scholar 

  • MacAdam JW, Villalba JJ (2015) Beneficial effects of temperate forage legumes that contain condensed tannins. Agriculture 5:475–491

    Article  Google Scholar 

  • Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+ -antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMahon LR, McAllister TA, Berg BP, Majak W, Acharya SN, Popp JD, Coulman BE, Wang Y, Cheng K-J (2000) A review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattle. Can J Plant Sci 80:469–485

    Article  CAS  Google Scholar 

  • McSweeney CS, Palmer B, McNeill DM, Krause DO (2001) Microbial interactions with tannins: nutritional consequences for ruminants. Anim Feed Sci Technol 91:83–93

    Article  CAS  Google Scholar 

  • Meagher LP, Widdup K, Sivakumaran S, Lucas R, Rumball W (2006) Floral Trifolium proanthocyanidins: polyphenol formation and compositional diversity. J Agric Food Chem 54:5482–5488

    Article  CAS  PubMed  Google Scholar 

  • Miller PR, Ehlke NJ (1996) Condensed tannins in birdsfoot trefoil: genetic relationships with forage yield and quality in NC-83 germplasm. Euphytica 92:383–391

    Article  CAS  Google Scholar 

  • Mithöfer A, Bola W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    Article  PubMed  Google Scholar 

  • Morris P, Robbins MP (1992) Condensed tannin formation by Agrobacterium rhizogenes transformed root and shoot organ cultures of Lotus corniculatus. J Exp Bot 43:221–247

    Article  CAS  Google Scholar 

  • Nelson CJ, Smith D (1968) Growth of birdsfoot trefoil and alfalfa. 4. Carbohydrate reserve levels and growth analysis under two temperature regimes. Crop Sci 9:589–591

    Article  Google Scholar 

  • Pang Y, Peel GJ, Wright E, Wang Z, Dixon RA (2007) Early steps in proanthocyanidin biosynthesis in the model legume Medicago truncatula. Plant Physiol 145:601–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paolocci F, Capucci R, Arcioni S, Damiani F (1999) Birdsfoot trefoil, a model for studying the synthesis of condensed tannins. In: Gross GG, Hemingway RW, Yoshida T (eds) Plant polyphenols 2. Chemistry, biology, pharmacology, ecology. Kluwer Academic/Plenum Press, New York 343–356

  • Paolocci F, Bovone T, Tosti N, Arcioni S, Damiani F (2005) Light and an exogenous transcription factor qualitatively and quantitatively affect the biosynthetic pathway of condensed tannins in Lotus corniculatus leaves. J Exp Bot 56:1093–1103

    Article  CAS  PubMed  Google Scholar 

  • Paolocci F, Robbins MP, Madeo L, Arcioni S, Martens S, Damiani F (2007) Ectopic expression of a basic Helix-Loop-Helix gene transactivates parallel pathways of proanthocyanidin biosynthesis. Structure, expression analysis, and genetic control of leucoanthocyanidin 4-reductase and anthocyanidin reductase genes in Lotus corniculatus. Plant Physiol 143:504–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramakrishna A, Ravishankar GA (2013) Role of plant metabolites in abiotic stress tolerance under changing climatic conditions with special reference to secondary compounds. In: Tutejy N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley-VCH Verlag, Weinheim, Germany 705–726. https://doi.org/10.1002/9783527675265.ch26

  • Robbins MP, Bavage AD, Strudwicke C, Morris P (1998) Genetic manipulation of condensed tannins in higher plants II. Analysis of birdsfoot trefoil plants harboring antisense dihydroflavonol reductase constructs. Plant Physiol 116:1133–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robbins MP, Paolocci F, Hughes J-W, Turchetti V, Arcioni S, Morris P, Damiani F (2002) Sn, a maize bHLH gene, transactivates anthocyanin and condensed tannin pathways in Lotus corniculatus. J Exp Bot 54:239–248

    Article  Google Scholar 

  • Sivakumaran S, Rumball W, Lane GA, Fraser K, Foo LY, Yu M, Meagher LP (2006) Variation of proanthocyanidins in Lotus species. J Chem Ecol 32:1797–1816

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Sasaki R, Ogata Y, Nakamura Y, Sakurai N, Kitajima M, Takayama H, Kanaya S, Aoki K, Shibata D, Saito K (2008) Metabolic profiling of flavonoids in Lotus japonicus using liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry. Phytochemistry 69:99–111

    Article  CAS  PubMed  Google Scholar 

  • Swain T (1977) Secondary compounds as protective agents. Annu Rev Plant Physiol 28:479–501

    Article  CAS  Google Scholar 

  • Terrill TH, Rowan AM, Douglas GB, Barry TW (1992) Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentration meals and cereal grains. J Sci Food Agric 58:321–329

    Article  CAS  Google Scholar 

  • Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anil Feed Sci Technol 48:185–197

    Article  Google Scholar 

  • Van Handell E (1968) Direct micro-determination of sucrose. Annals. Biochem 22(280–632):283

    Google Scholar 

  • Volenec JJ, Boyce PJ, Hendershot KL (1991) Carbohydrate metabolism in taproots of Medicago sativa L. during winter adaptation and spring regrowth. Plant Physiol 96:786–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waghorn GC, Ulyatt MJ, John A, Fisher MJ (1987) The effect of condensed tannins on the site of digestion of amino acids and other nutrients in sheep fed on Lotus corniculatus L. British J Nutrition 57:115–126

    Article  CAS  Google Scholar 

  • Waghorn GC, Jones WT, Shelton ID, McNabb WC (1990) Condensed tannins and the nutritive value of herbage. Proc NZ Grassl Assoc 51:171–176

    Google Scholar 

  • Wang Y, Waghorn GC, Barry TN, Shelton ID (1994) The effect of condensed tannins in Lotus corniculatus on plasma metabolism of methionine, cysteine and inorganic sulphate by sheep. British J Nutrition 72:923–935

    Article  CAS  Google Scholar 

  • Whitmore FW (1978) Lignin-carbohydrate complex formed in isolated cell walls of callus. Phytochemistry 17:421–425

    Article  CAS  Google Scholar 

  • Zhao J, Pang Y, Dixon RA (2010) The mysteries of proanthocyanidin transport and polymerization. Plant Physiol 153:437–443

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Acknowledgements

We would like to thank Julie Downsborough, Delma Jones and Alison Brooks for technical and analytical help. This research was supported by the BBSRC under the Global Environment Response Programme, (GERP grant number PG230/526), and BBSRC strategic grants to IGER (BBS/E/G/00003307,3120, 3390 and PU15), and the authors have no conflict of interest to declare.

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Authors and Affiliations

  1. Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, SY23 3EB, UK

    Phillip Morris, Eunice B. Carter, Barbara Hauck, Alexandra Lanot, Michael K. Theodorou & Gordon Allison

  2. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Plas Gogerddan, Aberystwyth, Ceredigion, SY23 3EB, Wales, UK

    Eunice B. Carter, Barbara Hauck & Gordon Allison

  3. Department of Biology, University of York, Heslington, York, YO10 5DD, UK

    Alexandra Lanot

  4. Department of Agriculture and Environment, Agriculture Centre for Sustainable Energy Systems, Harper Adams University, Newport, Shropshire, TF10 8NB, UK

    Michael K. Theodorou

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  1. Phillip Morris
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Correspondence to Phillip Morris.

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The original online version of this article was revised: The co-author Michael K Theodorou was not listed among the authors or in the author contribution statement and an additional person was missed from the acknowledgments section. The original article has been corrected.

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Morris, P., Carter, E.B., Hauck, B. et al. Responses of Lotus corniculatus to environmental change 3: The sensitivity of phenolic accumulation to growth temperature and light intensity and effects on tissue digestibility. Planta 253, 35 (2021). https://doi.org/10.1007/s00425-020-03524-w

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