Responses of Lotus Corniculatus to Environmental Change 3: the Sensitivity of Phenolic Accumulation to Growth Temperature and Li
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Aberystwyth University Responses of Lotus corniculatus to environmental change 3 Morris, Phillip; Carter, Eunice; Hauck, Barbara; Lanot, Alexandra; Allison, Gordon Published in: Planta DOI: 10.1007/s00425-020-03524-w Publication date: 2021 Citation for published version (APA): Morris, P., Carter, E., Hauck, B., Lanot, A., & Allison, G. (2021). 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(2), 35. 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Sep. 2021 Planta (2021) 253:35 https://doi.org/10.1007/s00425-020-03524-w ORIGINAL ARTICLE Responses of Lotus corniculatus to environmental change 3: The sensitivity of phenolic accumulation to growth temperature and light intensity and efects on tissue digestibility Phillip Morris1 · Eunice B. Carter1,2 · Barbara Hauck1,2 · Alexandra Lanot1,3 · Michael K. Theodorou1,4 · Gordon Allison1,2 Received: 17 July 2020 / Accepted: 2 December 2020 © The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021, corrected publication 2021 Abstract Main Conclusion Growth temperature and light intensity are major drivers of phenolic accumulation in Lotus cor- niculatus resulting in major changes in carbon partitioning which signifcantly afects tissue digestibility and forage quality. Abstract The response of plant growth, phenolic accumulation and tissue digestibility to light and temperature was deter- mined 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 favonol 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 favonols were kaempferol glycosides of which kaempferol-3-glucoside and kaempferol-3,7-dirhamnoside were the major components. Increases in both tannin and total favonol concentrations in leaves were linearly related to light intensity and were preceded by a specifc 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 signifcantly afects tissue digestibility and nutritional quality with a high correlation between tannin concentration and leaf digestibility. Keywords Condensed tannins · Climate change · Flavonoids · Lignins · Nutritional quality Abbreviations Communicated by Dorothea Bartels. BuOH n-Butanol HCA Hydroxycinnamic acid Supplementary Information The online version contains supplemen- IVDMD In-vitro-dry-matter-digestibility tary material available at https://doi. org/ 10. 1007/ s00425- 020- 03524-w . TGA Thioglycolic acid * Phillip Morris [email protected] Introduction 1 Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, UK It is well established that the accumulation of secondary 2 Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Plas Gogerddan, Aberystwyth, metabolites can be affected by external abiotic factors Ceredigion SY23 3EB, Wales, UK (Dixon and Paiva 1995; Ramakrishna and Ravishankar 3 Department of Biology, University of York, Heslington, 2013), as well as by biotic stress such as fungal attack and York YO10 5DD, UK herbivore predation (Swain 1977; Bennett and Wallsgrove 4 Department of Agriculture and Environment, Agriculture 1994; Mithöfer and Bola 2012). Response to climate change Centre for Sustainable Energy Systems, Harper Adams could include both increases in plant secondary metabo- University, Newport, Shropshire TF10 8NB, UK lites to deleterious levels, or decreases in levels resulting Vol.:(0123456789)1 3 35 Page 2 of 15 Planta (2021) 253:35 in reduced plant pathogen defence responses. To evaluate include lignin, cell wall hydroxycinnamic acids, favones, plant breeding strategies aimed at ameliorating such poten- favonols, induced isofavans, anthocyanins and condensed tial threats to crop productivity, herbivory or survival ftness, tannins (Fig. 1). we need a better understanding of how changes in growth Condensed tannin concentrations of diferent cultivars of conditions afect the accumulation of plant metabolites with both Lotus corniculatus and Lotus pedunculatus (syn: uligi- potentially toxic, anti-nutritional or plant defence properties. nosus), grown in diferent environments are highly variabil- Secondary metabolism gives rise to an enormous vari- ity, ranging of 4.7–8.7% dry weight in Lotus corniculatus ety of functionally important end products with those of and 6.3–11.0% dry weight in Lotus pedunculatus (Kelman the polyphenol biosynthetic pathway being agronomically and Tanner 1990; Acuña et al. 2008), and while the structure and economically important in a range of forage and crop of Lotus corniculatus tannin is suitable for improving the plant species depending upon crop usage. These include efciency of protein use without reducing consumption or phenylpropanoid compounds that have roles in plant sup- digestibility, the levels and structure of Lotus pedunculatus port (lignin), UV protection (favones and favonols) and tannins are often suboptimal for animal production (Wag- plant defence (isofavonoid phytoalexins and condensed horn et al. 1990). tannins), (Dixon and Paiva 1995). Condensed tannins can Increases in the accumulation of condensed tannins under have both positive and negative efects on animal nutrition controlled high temperature conditions were found in Lotus often through interactions with proteins and bacteria in the pedunculatus (Lees et al. 1994), but not in L. corniculatus rumen (McSweeney et al. 2001). As well as contributing by- (Ehike and LeGare 1993; Carter et al. 1999). Temperature pass proteins in ruminants, they can also be antinutritional efects on condensed tannins are also signifcantly larger depending on their concentration and structure (reviewed by in combination with other environmental factors such as McMahon et al. 2000). drought (Anuraga, et al. 1993; Carter et al. 1999), high Because they reduce both digestibility and palatability CO2 levels (Carter et al. 1999) and soil nutrient defciencies condensed tannins are considered anti-nutritional at high (Barry and Manley 1986). concentrations (above 4–5% dry weight) (Barry and Duncan Large variations in the levels of total tannins and in the 1984). In contrast, at low concentrations (2–3% dry weight) ratio of free and bound tannins were also found with increas- some condensed tannins are considered benefcial to rumi- ing soil nutrient and climatic stress with levels of condensed nants as they bind to plant proteins and protect them from tannins above 9% dry matter being freely extractable (Barry deamination by rumen microbes, increasing the amount of and Manley 1986). protein available for post-ruminal digestion and absorption Low temperatures have been reported to elevate con- and reducing the possibility of bloat (Barry and Manley densed tannin concentrations in L corniculatus (Carter et al. 1986; Waghorn et al. 1987). 1999), while high temperature and drought stress increased These phenolic and polyphenolic end products are of condensed tannin levels in L uliginosus indicating species critical value in higher plants and in forage species their diferences in condensed tannin biosynthesis in response to tissue-specifc accumulation particularly afects feed intake, temperature (Anuraga et al. 1993). digestibility and crop quality (MacAdam and Villalba 2015). However, few studies have determined growth and phe- However, despite considerable worldwide eforts, the full nolic accumulation over a wide range of temperatures or impact of condensed tannins on the nutritional value of for- light intensities, or considered the subsequent efects of envi- age has not yet provided unequivocal results. This may be ronmentally induced changes in phenolics on the nutritional partially related to the high levels of variation in the amount quality of Lotus corniculatus. and structure (molecular weight and monomeric composi- tion) (Sivakumaran et al. 2006), as