Skip to main content
SpringerLink
Log in

Chilling tolerance and early vigour-related characteristics evaluated in two Miscanthus genotypes

  • Original papers
  • Published:
Photosynthetica

Abstract

A long growing season, mediated by the ability to grow at low temperatures early in the season, can result in higher yields in biomass of crop Miscanthus. In this paper, the chilling tolerance of two highly productive Miscanthus genotypes, the widely planted Miscanthus × giganteus and the Miscanthus sinensis genotype ‘Goliath’, was studied. Measurements in the field as well as under controlled conditions were combined with the main purpose to create basic comparison tools in order to investigate chilling tolerance in Miscanthus in relation to its field performance. Under field conditions, M. × giganteus was higher yielding and had a faster growth rate early in the growing season. Correspondingly, M. × giganteus displayed a less drastic reduction of the leaf elongation rate and of net photosynthesis under continuous chilling stress conditions in the growth chamber. This was accompanied by higher photochemical quenching and lower nonphotochemical quenching in M. × giganteus than that in M. sinensis ‘Goliath’ when exposed to chilling temperatures. No evidence of impaired stomatal conductance or increased use of alternative electron sinks was observed under chilling stress. Soluble sugar content markedly increased in both genotypes when grown at 12°C compared to 20°C. The concentration of raffinose showed the largest relative increase at 12°C, possibly serving as a protection against chilling stress. Overall, both genotypes showed high chilling tolerance for C4 plants, but M. × giganteus performed better than M. sinensis ‘Goliath’. This was not due to its capacity to resume growth earlier in the season but rather due to a higher growth rate and higher photosynthetic efficiency at low temperatures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll

DOY:

day of year

Fv/Fm :

maximal quantum yield of PSII photochemistry

Fv′/Fm′:

quantum yield of open PSII reaction centers

g s :

stomatal conductance

LED:

leaf elongation duration

LED10–90% :

duration of leaf elongation from 10 to 90% of a final length

LER:

leaf elongation rate

LERmax :

maximum leaf elongation rate

L m :

maximum leaf length

NPQ:

nonphotochemical quenching

P N :

net photosynthetic rate

qP :

photochemical quenching coefficient

Ta :

air temperature

WSC:

water soluble carbohydrates

FCO2 :

quantum yield of photosynthesis

FPSII :

effective quantum yield of PSII photochemistry

References

  • Anderson E., Arundale R., Maughan M. et al.: Growth and agronomy of Miscanthus × giganteus for biomass production. — Biofuels 2: 167–183, 2011.

    Article  CAS  Google Scholar 

  • Arnoult S., Obeuf A., Béthencourt L. et al.: Miscanthus clones for cellulosic bioethanol production: Relationships between biomass production, biomass production components, and biomass chemical composition. — Ind. Crops Prod. 63: 316–328, 2015.

    Article  CAS  Google Scholar 

  • Arredondo J.T., Schnyder H.: Components of leaf elongation rate and their relationship to specific leaf area in contrasting grasses. — New Phytol. 158: 305–314, 2003.

    Article  Google Scholar 

  • Bhosale S.U., Rymen B., Beemster G.T.S. et al.: Chilling tolerance of Central European maize lines and their factorial crosses. — Ann. Bot. 100: 1315–1321, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bultynck L., Ter Steege M.W., Schortemeyer M. et al.: From individual leaf elongation to whole shoot leaf area expansion: a comparison of three Aegilops and two Triticum species. — Ann. Bot. 94: 99–108, 2004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chenu K., Chapman S.C., Hammer G.L. et al.: Short-term responses of leaf growth rate to water deficit scale up to whole-plant and crop levels: an integrated modelling approach in maize. — Plant Cell Environ. 31: 378–391, 2008.

    Article  PubMed  Google Scholar 

  • Clifton-Brown J.C., Jones M.B.: The thermal response of leaf extension rate in genotypes of the C4-grass Miscanthus: an important factor in determining the potential productivity of different genotypes. — J. Exp. Bot. 48: 1573–1581, 1997.

    CAS  Google Scholar 

  • Dohleman F.G., Long S.P.: More productive than maize in the Midwest: How does Miscanthus do it? — Plant Physiol. 150: 2104–2115, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domon J-M., Baldwin L., Acket S. et al.: Cell wall compositional modifications of Miscanthus ecotypes in response to cold acclimation. — Phytochemistry 85: 51–61, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Du Y., Nose A.: Effects of chilling temperature on the activity of enzymes of sucrose synthesis and the accumulation of saccharides in leaves of three sugarcane cultivars differing in cold sensitivity. — Photosynthetica 40: 389–395, 2002.

    Article  CAS  Google Scholar 

  • Equiza M., Mirave J., Tognetti J.: Differential inhibition of shoot vs. root growth at low temperature and its relationship with carbohydrate accumulation in different wheat cultivars. — Ann. Bot. 80: 657–663, 1997.

    Article  Google Scholar 

  • Farage P.K., Blowers D., Long S.P. et al.: Low growth temperatures modify the efficiency of light use by photosystem II for CO2 assimilation in leaves of two chilling-tolerant C4 species, Cyperus longus L. and Miscanthus × giganteus. — Plant Cell Environ. 29: 720–728, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Farrell A.D., Clifton-Brown J.C., Lewandowski I. et al.: Genotypic variation in cold tolerance influences the yield of Miscanthus. — Ann. Appl. Biol. 149: 337–345, 2006.

    Article  Google Scholar 

  • Fracheboud Y., Haldimann P., Leipner J. et al.: Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). — J. Exp. Bot. 50: 1533–1540, 1999.

    Article  CAS  Google Scholar 

  • Friesen P.C., Peixoto M.M., Busch F. et al.: Chilling and frost tolerance in Miscanthus and Saccharum genotypes bred for cool temperate climates. — J. Exp. Bot. 63: 3749–3758, 2014.

    Article  Google Scholar 

  • Fryer M., Andrews J., Oxborough K. et al: Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. — Plant Physiol. 116: 571–580, 1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genty B., Briantais J.-M., Baker N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochim Biophys Acta 990: 87–92, 1989.

    Article  CAS  Google Scholar 

  • Glowacka K., Adhikari S., Peng J. et al.: Variation in chilling tolerance for photosynthesis and leaf extension growth among genotypes related to the C4 grass Miscanthus × giganteus. — J. Exp. Bot. 65: 5267–5278, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Glowacka K., Jorgensen U., Kjeldsen J.B. et al.: Can the exceptional chilling tolerance of C4 photosynthesis found in Miscanthus × giganteus be exceeded? Screening of a novel Miscanthus Japanese germplasm collection. — Ann. Bot. 115: 981–990, 2015.

    Article  PubMed  Google Scholar 

  • Greef J., Deuter M.: Syntaxonomy of Miscanthus × giganteus Greef et Deu. — Angew. Bot. 67: 87–90, 1993.

    Google Scholar 

  • Heaton E., Voigt T., Long S.P.: A quantitative review comparing the yields of two candidate C4 perennial biomass crops in relation to nitrogen, temperature and water. — Biomass Bioenerg. 27: 21–30, 2004.

    Article  Google Scholar 

  • Hodges D., Andrews C.: Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. — J. Exp. Bot. 48: 1105–1113, 1997.

    Article  CAS  Google Scholar 

  • Janská A., Marsík P., Zelenková S. et al.: Cold stress and acclimation — what is important for metabolic adjustment? — Plant Biol. 12: 395–405, 2010.

    Article  PubMed  Google Scholar 

  • Kao W., Tsai T., Chen W.: A comparative study of Miscanthus floridulus (Labill) Warb and M. transmorrisonensis Hayata: photosynthetic gas exchange, leaf characteristics and growth in controlled environments. — Ann. Bot. 81: 295–299, 1998.

    Article  Google Scholar 

  • Keunen E., Peshev D., Vangronsveld J. et al.: Plant sugars are crucial players in the oxidative challenge during abiotic stress: Extending the traditional concept. — Plant Cell Environ. 36: 1242–1255, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Koster K.L., Lynch D.V.: Solute accumulation and compartmentation during the cold acclimation of Puma Rye. — Plant Physiol. 98: 108–113, 1992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen S.U., Jørgensen U., Kjeldsen J.B. et al.: Long-term Miscanthus yields influenced by location, genotype, row distance, fertilization and harvest season. — BioEnergy Res. 7: 620–635, 2013.

    Article  Google Scholar 

  • Leipner J., Fracheboud Y., Stamp P.: Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. — Environ. Exp. Bot. 42: 129–139, 1999.

    Article  CAS  Google Scholar 

  • Lesur C., Jeuffroy M-H., Makowski D. et al.: Modeling longterm yield trends of Miscanthus × giganteus using experimental data from across Europe. — F. Crop Res. 149: 252–260, 2013.

    Article  Google Scholar 

  • Lewandowski I., Clifton-Brown J.C., Scurlock J.M. et al.: Miscanthus: European experience with a novel energy crop. — Biomass Bioenerg. 19: 209–227, 2000.

    Article  CAS  Google Scholar 

  • Lewandowski I., Scurlock J., Lindvall E. et al.: The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. — Biomass Bioenerg. 25: 335–361, 2003.

    Article  Google Scholar 

  • Long S.P., Spence A.K.: Toward cool C(4) crops. — Annu. Rev. Plant Biol. 64: 701–722, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Lootens P., Van Waes J., Carlier L.: Effect of a short photoinhibition stress on photosynthesis, chlorophyll a fluorescence, and pigment contents of different maize cultivars. Can a rapid and objective stress indicator be found? — Photosynthetica 42: 187–192, 2004.

    Article  CAS  Google Scholar 

  • Matros A., Peshev D., Peukert M. et al.: Sugars as hydroxyl radical scavengers. Proof-of-concept by studying the fate of sucralose in Arabidopsis. — Plant J. 82: 822–839, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Miguez F.E., Villamil M.B., Long S.P. et al.: Meta-analysis of the effects of management factors on Miscanthus × giganteus growth and biomass production. — Agric. For. Meteorol. 148: 1280–1292, 2008.

    Article  Google Scholar 

  • Morsy M.R., Jouve L., Hausman J-F. et al.: Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. — J. Plant Physiol. 164: 157–167, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. — J. Exp. Bot. 64: 3983–3998, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Muylle H., Van Hulle S., De Vliegher A. et al.: Dry matter yield and energy balance of annual and perennial lignocellulosic crops for bio-refinery use: a four-year field experiment in Belgium. — Eur. J. Agron. 63: 62–70, 2015.

    Article  Google Scholar 

  • Nägele T., Heyer A.G.: Approximating subcellular organisation of carbohydrate metabolism during cold acclimation in different natural accessions of Arabidopsis thaliana. — New Phytol. 198: 777–787, 2013.

    Article  PubMed  Google Scholar 

  • Nägele T., Stutz S., Hörmiller I. et al.: Identification of a metabolic bottleneck for cold acclimation in Arabidopsis thaliana. — Plant J. 72: 102–114, 2012.

    Article  PubMed  Google Scholar 

  • Naidu S.L., Long S.P.: Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus × giganteus: an in vivo analysis. — Planta 220: 145–155, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A., Yabuta Y., Shigeoka S.: Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. — Plant Physiol. 147: 1251–1263, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peter R., Eschholz T.W., Stamp P. et al.: Swiss Flint maize landraces. — A rich pool of variability for early vigour in cool environments. — F. Crop Res. 110: 157–166, 2009.

    Google Scholar 

  • Purdy S.J., Maddison A.L., Jones L.E. et al.: Characterization of chilling-shock responses in four genotypes of Miscanthus reveals the superior tolerance of M. × giganteus compared with M. sinensis and M. sacchariflorus. — Ann. Bot. 111: 999–1013, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robson P., Jensen E., Hawkins S. et al.: Accelerating the domestication of a bioenergy crop: identifying and modelling morphological targets for sustainable yield increase in Miscanthus. — J. Exp. Bot. 64: 4143–55, 2013a.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robson P., Mos M., Clifton-Brown J. et al.: Phenotypic variation in senescence in Miscanthus: towards optimising biomass quality and quantity. — BioEnergy Res. 5: 95–105, 2011.

    Article  Google Scholar 

  • Robson P.R.H., Farrar K., Gay A.P. et al.: Variation in canopy duration in the perennial biofuel crop Miscanthus reveals complex associations with yield. — J. Exp. Bot. 64: 2373–83, 2013b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rymen B., Fiorani F., Kartal F. et al.: Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. — Plant Physiol. 143: 1429–1438, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadok W., Naudin P., Boussuge B. et al.: Leaf growth rate per unit thermal time follows QTL-dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions. — Plant Cell Environ. 30: 135–146, 2007.

    Article  PubMed  Google Scholar 

  • Schneider T., Keller F.: Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. — Plant Cell Physiol. 50: 2174–2182, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Spence A.K., Boddu J., Wang D. et al.: Transcriptional responses indicate maintenance of photosynthetic proteins as key to the exceptional chilling tolerance of C4 photosynthesis in Miscanthus × giganteus. — J. Exp. Bot. 65: 3737–3747, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tarkowski L.P., Van den Ende W.: Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. — Front Plant Sci. 6: 203, doi: 10.3389/fpls.2015.00203, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  • Valluru R., Van den Ende W.: Plant fructans in stress environments: emerging concepts and future prospects. — J. Exp. Bot. 59: 2905–16, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Van den Ende W., El-Esawe S.K.: Sucrose signaling pathways leading to fructan and anthocyanin accumulation: A dual function in abiotic and biotic stress responses? — Environ. Exp. Bot. 108: 4–13, 2013.

    Article  Google Scholar 

  • Van Hulle S., Van Waes C., De Vliegher A. et al.: Comparison of dry matter yield of lignocellulosic perennial energy crops in a longterm Belgian field experiment. — In: 24th General Meeting of the European Grassland Federation, Lublin 2012.

    Google Scholar 

  • Vargas L.A., Andersen M.N., Jensen C.R. et al.: Estimation of leaf area index, light interception and biomass accumulation of Miscanthus sinensis “Goliath” from radiation measurements. — Biomass Bioenerg. 22: 1–14, 2002.

    Article  Google Scholar 

  • Voorend W., Lootens P., Nelissen H. et al.: LEAF-E: a tool to analyze grass leaf growth using function fitting. — Plant Methods 10: doi: 10.1186/1746-4811-10-37 37, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang D., Portis A.R., Moose S.P. et al.: Cool C4 photosynthesis: pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus × giganteus. — Plant Physiol. 148: 557–67, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J., Chen W., Luo F. et al.: Variability and adaptability of Miscanthus species evaluated for energy crop domestication. — GCB Bioenergy 4: 49–60, 2011.

    Article  Google Scholar 

  • Zhang J., Xu Y., Chen W., Dell B. et al.: A wheat 1-FEH w3 variant underlies enzyme activity for stem WSC remobilization to grain under drought. — New Phytol. 205: 293–305, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Zub H.W., Arnoult S., Brancourt-Hulmel M.: Key traits for biomass production identified in different Miscanthus species at two harvest dates. — Biomass Bioenerg. 35: 637–651, 2011.

    Article  Google Scholar 

  • Zub H.W., Arnoult S., Younous J. et al.: The frost tolerance of Miscanthus at the juvenile stage: Differences between clones are influenced by leaf-stage and acclimation. — Eur. J. Agron. 36: 32–40, 2012b.

    Article  Google Scholar 

  • Zub H.W., Brancourt-Hulmel M.: Agronomic and physiological performances of different species of Miscanthus, a major energy crop. A review. — Agron. Sustain. Dev. 30: 201–214, 2010.

    Article  Google Scholar 

  • Zub H.W., Rambaud C., Bethencourt L. et al.: Late emergence and rapid growth maximize the plant development of Miscanthus clones. — BioEnergy Res. 5: 841–854, 2012a.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), 9090, Melle, Belgium

    S. Fonteyne, P. Lootens, H. Muylle, T. de Swaef & I. Roldan-Ruiz

  2. Department of Plant Production, Ghent University, 9000, Ghent, Belgium

    S. Fonteyne & D. Reheul

  3. Laboratory of Molecular Plant Biology, Katholic University Leuven, 3000, Leuven, Belgium

    W. van den Ende

Authors
  1. S. Fonteyne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Lootens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Muylle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W. van den Ende
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. de Swaef
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. Reheul
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. Roldan-Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Lootens.

Additional information

Acknowlegdements: The research reported in this article was funded by the European Union's 7th framework project OPTIMISC (289159). The authors wish to thank Rudy Vergauwen, Robbrecht Cardon, Ellen De Sutter, and Evelien Mortaignie for their help with the measurements and the ILVO technical staff for their help with setting up the experiments.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fonteyne, S., Lootens, P., Muylle, H. et al. Chilling tolerance and early vigour-related characteristics evaluated in two Miscanthus genotypes. Photosynthetica 54, 295–306 (2016). https://doi.org/10.1007/s11099-016-0193-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-016-0193-y

Additional key words

Search

Navigation