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Plant function and evolutionary biology
RESEARCH ARTICLE

Elevated CO2 atmosphere promotes plant growth and inulin production in the cerrado species Vernonia herbacea

Vanessa F. Oliveira A , Lilian B. P. Zaidan A , Márcia R. Braga A , Marcos P. M. Aidar A and Maria Angela M. Carvalho A B
+ Author Affiliations
- Author Affiliations

A Seção de Fisiologia e Bioquímica de Plantas, Instituto de Botânica, C. Postal 3005, 01061-970 – São Paulo, SP, Brasil.

B Corresponding author. Email: mam.carvalho@gmail.com

Functional Plant Biology 37(3) 223-231 https://doi.org/10.1071/FP09164
Submitted: 27 June 2009  Accepted: 22 October 2009   Published: 25 February 2010

Abstract

Carbon allocation in biomass is an important response of plants to the increasing atmospheric [CO2]. The effects of elevated [CO2] are scarcely reported in fructan-accumulating plants and even less in tropical wild species storing this type of carbohydrate. In the present study, the effects of high [CO2] atmosphere was evaluated on growth, biomass allocation and fructan metabolism in Vernonia herbacea (Vell.) Rusby, an Asteraceae from the Brazilian cerrado, which accumulates inulin-type fructans in the underground organs (rhizophores). Plants were cultivated for 120 days in open-top chambers (OTCs) under ambient (~380 μmol mol–1), and elevated (~760 μmol mol–1) [CO2]. Plant growth, photosynthesis, fructan contents, and the activities of fructan metabolising enzymes were analysed in the rhizophores at Time 0 and 15, 30, 60, 90 and 120 days. Plants under elevated [CO2] presented increases in height (40%), photosynthesis (63%) and biomass of aerial (32%) and underground (47%) organs when compared with control plants. Under elevated [CO2] plants also presented higher 1-SST, 1-FFT and invertase activities and lower 1-FEH activity. Although fructan concentration remained unchanged, fructan productivity was higher in plants maintained under elevated [CO2], due to their higher rhizophore biomass. This is the first report on the effects of elevated [CO2] on a plant species bearing underground organs that accumulate fructans. Our results indicate that plants of V. herbacea can benefit from elevated atmospheric [CO2] by increasing growth and carbon allocation for the production of inulin, and may contribute to predict a future scenario for the impact of this atmospheric condition on the herbaceous vegetation of the cerrado.

Additional keywords: carbon partition, fructan active enzymes, non-structural carbohydrates, reserve organs.


Acknowledgements

This work was supported by FAPESP (98/05124–8 and 05/04139–7) and CNPq (474674/2004–5). V.F. Oliveira thanks FAPESP for awarded fellowship (07/59782–7). MAM Carvalho, LBP Zaidan and MR Braga are CNPq research fellows. The authors thank Dr Norio Shiomi (Rakuno Gakuen University, Japan) for kindly providing pure samples of nystose and 1-kestose.


References


Aidar MPM , Martinez CA , Costa AC , Costa PMF , Dietrich SMC , Buckeridge MS (2002) Effect of atmospheric CO2 enrichment on the establishment of seedlings of jatobá, Hymenaea courbaril L. (Leguminosae, Caesalpinioideae). Biota Neotropica 2 BN01602012002 . Available at http://www.biotaneotropica.org.br/v2n1/pt/abstract?article+BN01602012002

Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.
Crossref | GoogleScholarGoogle Scholar | PubMed | [Accessed 10 June 2009]

Edelman J, Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytologist 67, 517–531.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Farrar JF (1996) Sinks – integral parts of a whole plant. Journal of Experimental Botany 47, 1273–1279.
CAS |
open url image1

Högy P, Fangmeier A (2009) Atmospheric CO2 enrichment affects potatoes: 1. Aboveground biomass production and tuber yield. European Journal of Agronomy 30, 78–84.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hunt R (1978) ‘Plant growth analysis.’ (The Camelot Press: London)

IPCC (2007) ‘Climate change 2007: mitigation. Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Eds B Metz, OR Davidson, PR Bosch, R Dave, LA Meyer) (Cambridge University Press: Cambridge)

Isopp H, Frehner M, Almeida JPF, Blum H, Daepp M, Hartwig UA, Lüscher A, Suter D, Nösberger J (2000) Nitrogen plays a major role in leaves when source-sink relations change: C and N metabolism in Lolium perenne growing under free air CO2 enrichment. Australian Journal of Plant Physiology 27, 851–858.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Jermyn MA (1956) A new method for the determination of ketohexoses in presence of aldohexoses. Nature 177, 38–39.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kimball BA (1983) Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agronomy Journal 75, 779–788. open url image1

Livingston DP, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences ,
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annual Review of Plant Biology 55, 591–628.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Martinoia E (1992) Transport processes in vacuoles of higher plants. Botanica Acta 105, 232–245.
CAS |
open url image1

Marx SP, Nosberger J, Frehner M (1997) Seasonal variation of fructan-β-fructosidase (FEH) activity and characterization of a β-(2,1)-linkage specific FEH from tubers of Jerusalem artichoke (Helianthus tuberosus). New Phytologist 135, 267–277.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Miglietta F, Magliulo V, Bindi M, Cerio L, Vaccari FP, Luduca V, Peressotti A (1998) Free air CO2 enrichment of potato (Solanum tuberosum L.): development, growth and yield. Global Change Biology 4, 163–172.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant, Cell & Environment 22, 659–682.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annual Review of Plant Physiology and Plant Molecular Biology 42, 77–101.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Poorter H , Garnier E (2007) Ecological significance of inherent variation in relative growth rate. In ‘Functional plant ecology’. (Eds F Pugnaire, F Valladares) pp. 67–100. (CRC Press: Boca Raton, FL)

Portes MT, Carvalho MAM (2006) Spatial distribution of fructans and fructan metabolizing enzymes in rhizophores of Vernonia herbacea (Vell.) Rusby in different developmental phases. Plant Science 170, 624–633.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Portes MT, Figueiredo-Ribeiro RCL, Carvalho MAM (2008) Low temperature and defoliation affect fructan-metabolizing enzymes in different regions of the rhizophores of Vernonia herbacea. Journal of Plant Physiology 165, 1572–1581.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Global Change Biology 5, 807–837.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ritsema T, Smeekens S (2003) Fructans: beneficial for plants and humans. Current Opinion in Plant Biology 6, 223–230.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Roberfroid MB (2005) Introducing inulin-type fructans. British Journal of Nutrition 93, S13–S25.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rogers A, Allen DJ, Davey PA, Morgan PB, Ainsworth EA , et al . (2004) Leaf photosynthesis and carbohydrate dynamics of soybeans growth throughout their life-cycle under free-air carbon dioxide enrichment. Plant, Cell & Environment 27, 449–458.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Shipley B (2006) Net assimilation rate, specific leaf area and leaf mass ratio: which is most closely correlated with relative growth rate? A meta-analysis. Functional Ecology 20, 565–574.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sild E, Younis S, Pleijel H, Selldén G (1999) Effect of CO2 enrichment on non-structural carbohydrates in leaves, stems and ears of spring wheat. Physiologia Plantarum 107, 60–67.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Smart DR, Chatterton NJ, Bugbee B (1994) The influence of elevated CO2 on non-structural carbohydrate distribution and fructan accumulation in wheat canopies. Plant, Cell & Environment 17, 435–442.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Somogyi M (1945) A new reagent for the determination of sugars. The Journal of Biological Chemistry 160, 61–63.
CAS |
open url image1

Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosyntetic cells. Plant, Cell & Environment 14, 741–762.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tertuliano MF, Figueiredo-Ribeiro RCL (1993) Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phytologist 123, 741–749.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Updegraff UM (1969) Semimicro determination of cellulose in biological materials. Analytical Biochemistry 32, 420–424.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Van den Ende W, Michiels A, De Roover J, Van Laere A (2002) Fructan biosynthetic and breakdown enzymes in dicots evolved from different invertases. Expression of fructan genes throughout chicory development. The Scientific World Journal 2, 1281–1295.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A, Yoshida M, Kawakami A (2003) Fructan 1-exohydrolases: β-(2,1) trimmers during graminan biosynthesis in stems of wheat? Purification, characterization, mass mapping and cloning of two fructan 1-exohydrolase isoforms. Plant Physiology 131, 621–631.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wang C, Tillberg JE (1996) Effects of nitrogen deficiency on accumulation of fructan and fructan metabolizing enzyme activities in sink and source leaves of barley (Hordeum vulgare). Physiologia Plantarum 97, 339–345.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wheeler TR, Morison JLL, Ellis RH, Hadley P (1994) The effect of CO2, temperature and their interation on the growth and yield of carrot (Daucus carota L.). Plant, Cell & Environment 17, 1275–1284.
Crossref | GoogleScholarGoogle Scholar | open url image1