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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Impact of defoliation frequency on regrowth and carbohydrate metabolism in contrasting varieties of Lolium perenne

Bertrand Lasseur A , Jérémy Lothier A , Annette Morvan-Bertrand A , Abraham Escobar-Guttiérez B , Mervyn O. Humphreys C and Marie-Pascale Prud’homme A D
+ Author Affiliations
- Author Affiliations

A UMR INRA-UCN 950 EVA Ecophysiologie Végétale, Agronomie & Nutritions NCS, Université de Caen, Esplanade de la Paix, F-14032 Caen cedex, France.

B Unité d’Ecophysiologie des Plantes Fourragères, INRA, Route de Saintes, F-86600 Lusignan, France.

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

D Corresponding author. Email: marie-pascale.prudhomme@unicaen.fr

Functional Plant Biology 34(5) 418-430 https://doi.org/10.1071/FP06286
Submitted: 3 November 2006  Accepted: 1 March 2007   Published: 17 May 2007

Abstract

The aims of the study were to gain a better understanding of fructan metabolism regulation during regrowth of Lolium perenne, and to evaluate the role of fructans of remaining tissues as well as carbon assimilation of new leaf tissues in refoliation. Two varieties that contrast for carbohydrate metabolism, Aurora and Perma, were subject to severe and frequent or infrequent defoliations before regrowth. Aurora, which had a greater content of fructans in leaf sheaths than Perma before defoliation, produced more leaf biomass within the 4 days following the first cut. At the end of the regrowth period, Aurora produced more leaf biomass than Perma. Photosynthetic parameters, which were barely affected by defoliation frequency, could not explain these differences. Fructan synthesising activities [sucrose:sucrose 1-fructosyltransferase (1-SST) and fructan:fructan 6G-fructosyltransferase (6G-FFT)], declined after defoliation. In elongating leaf bases, corresponding transcript levels did not decline concomitantly, suggesting a post-transcriptional regulation of expression, while in leaf sheaths the gene expression pattern mostly followed the time-course of the enzyme activities. Regulation of Lp1-SST and Lp6G-FFT gene expression depends, therefore, on the sink–source status of the tissue after defoliation. During the phase of reserve accumulation, fructosyltransferase activities together with corresponding transcripts increased more in frequently defoliated plants than in infrequently defoliated plants.

Additional keywords: carbon assimilation, defoliation, fructans, fructan:fructan 6G-fructosyltransferase, gene expression, Lolium perenne, sucrose:sucrose 1-fructosyltransferase.


Acknowledgements

The authors thank N. Shiomi and N. J. Chatterton for their kind gifts of 1&6G-kestotetraose and 6G-kestotriose, respectively. They acknowledge valuable technical help by A. Bré and P. Beauclair.


References


Amiard V, Morvan-Bertrand A, Billard JP, Huault C, Prud’homme MP (2003a) Fate of fructose supplied to leaf sheaths after defoliation of Lolium perenne L.: assessment by 13C-fructose labelling. Journal of Experimental Botany 54, 1231–1243.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Amiard V, Morvan-Bertrand A, Billard JP, Huault C, Keller F, Prud’homme MP (2003b) Fructans, but not the sucrosyl-galactosides, raffinose and loliose, are affected by drought stress in perennial ryegrass. Plant Physiology 132, 2218–2229.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Amiard V, Mueh KE, Demmig-Adams B, Ebbert V, Turgeon R, Adams WW III (2005) Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proceedings of the National Academy of Sciences USA 102, 12 968–12 973.
Crossref | GoogleScholarGoogle Scholar | open url image1

Asay KH, Nelson CJ, Horst GL (1974) Genetic variability for net photosynthesis in tall fescue. Crop Science 14, 571–574. open url image1

Asega AF, Carvalho MAM (2004) Fructan metabolising enzymes in rhizophores of Vernonia herbacea upon excision of aerial organs. Plant Physiology and Biochemistry 42, 313–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Broadley MR, Escobar-Gutiérrez AJ, Burns A, Burns I (2001) Nitrogen-limited growth of lettuce is associated with lower stomatal conductance. New Phytologist 152, 97–106.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldwell MM, Richards JH, Johnson DA, Nowak RS, Dzurec RS (1981) Coping with herbivory: photosynthetic capacity and resource allocation in two semiarid Agropyron bunchgrasses. Oecologia 50, 14–24.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unpredicted proteins. The Plant Cell 16, 3285–3303.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chalmers J, Johnson X, Lidgett A, Spangenberg G (2003) Isolation and characterisation of a sucrose:sucrose 1-fructosyltransferase gene from perennial ryegrass (Lolium perenne). Journal of Plant Physiology 160, 1385–1391.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chalmers J, Lidgett A, Cummings N, Cao Y, Forster J, Spangenberg G (2005) Molecular genetics of fructan metabolism in perennial ryegrass. Plant Biotechnology Journal 3, 459–474.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Darwen CWE, John P (1989) Localization of the enzymes of fructan metabolism in vacuoles isolated in by a mechanical method from tubers of Jerusalem artichoke (Helianthus tuberosus L.). Plant Physiology 89, 658–663.
PubMed |
open url image1

Davidson JL, Milthorpe FL (1966) The effect of defoliation on the carbon balance in Dactylis glomerata. Annals of Botany 30, 185–198. open url image1

Davies A (1965) Carbohydrate levels and regrowth in perennial ryegrass. Journal of Agricultural Science 65, 213–221. open url image1

Davies A (1966) The regrowth of swards of S24 perennial ryegrass subjected to different pre-treatments. Journal of Agricultural Science 67, 139–144. open url image1

Demel RA, Dorrepaal E, Ebskamp MJM, Smeekens JCM, de Kruijff B (1998) Fructans interact strongly with model membranes. Biochimica et Biophysica Acta 1375, 36–42.
Crossref | PubMed |
open url image1

De Roover J, Van Laere A, Van den Ende W (1999) Effect of defoliation on fructan pattern and fructan metabolizing enzymes in young chicory plants (Cichorium intybus). Physiologia Plantarum 106, 158–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Roover J, Van den Branden K, Van Laere A, Van den Ende W (2000) Drought induces fructan synthesis and 1-SST (sucrose:sucrose fructosyltransferase) in roots and leaves of chicory seedlings (Cichorium intybus L.). Planta 210, 808–814.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

De Visser R, Vianden H, Schnyder H (1997) Kinetics and relative significance of remobilized and current C and N incorporation in leaf and root growth zones of Lolium perenne after defoliation: assessment by 13C and 15N steady-state labelling. Plant, Cell & Environment 20, 37–46.
Crossref | GoogleScholarGoogle Scholar | open url image1

Donaghy DJ, Fulkerson WJ (1997) The importance of water-soluble carbohydrate reserves on regrowth and root growth of Lolium perenne (L.). Grass and Forage Science 52, 401–407.
Crossref | GoogleScholarGoogle Scholar | open url image1

Donaghy DJ, Fulkerson WJ (1998) Priority of allocation of water-soluble carbohydrate reserves during regrowth of Lolium perenne. Grass and Forage Science 53, 211–218.
Crossref | GoogleScholarGoogle Scholar | open url image1

Duchateau N, Bortlik K, Simmen U, Wiemken A, Bancal P (1995) Sucrose:fructan 6-fructosyltransferase, a key enzyme for diverting sucrose to fructan in barley leaves. Plant Physiology 107, 1249–1255.
PubMed |
open url image1

Fujishima M, Sakai H, Ueno K, Takahashi N, Onodera S, Benkeblia N, Shiomi N (2005) Purification and characterization of a fructosyltransferase from onion bulbs and its key role in the synthesis of fructo-oligosaccharides in vivo. New Phytologist 165, 513–524.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fulkerson WJ, Slack K (1994) Leaf number as a criterion for determining defoliation time for Lolium perenne: 1. The effect of water-soluble carbohydrates and senescence. Grass and Forage Science 49, 373–377.
Crossref | GoogleScholarGoogle Scholar | open url image1

Guerrand D, Prud’homme MP, Boucaud J (1996) Fructan metabolism in expanding leaves, mature leaf sheaths and mature leaf blades of Lolium perenne: fructan synthesis, fructosyltransferase and invertase activities. New Phytologist 134, 205–214.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hendry GAF , Wallace RK (1993) The origin, distribution and evolutionary significance of fructans. In ‘Science and technology of fructans’. (Eds M Suzuki, NJ Chatterton) pp. 119–139. (CRC Press: Boca Raton, FL)

Hincha DK, Hellwege EM, Heyer AG, Crowe JH (2000) Plant fructans stabilize phosphatidylcholine liposomes during freeze-drying. European Journal of Biochemistry 267, 535–540.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Humphreys MO (1989) Water-soluble carbohydrates in perennial ryegrass breeding. I. Genetic differences among cultivars and hybrid progeny grown as spaced plants. Grass and Forage Science 44, 231–236.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jafari A, Conolly V, Walsh EJ (2003) Genetic analysis of yield and quality in full-sib families of perennial ryegrass (Lolium perenne L.) under two cutting managements. Irish Journal of Agricultural and Food Research 42, 275–292. open url image1

Jones MGK, Outlaw WH, Lowry OH (1977) Enzymatic assay of 10−7 to 10−14 moles of sucrose in plant tissues. Plant Physiology 60, 379–383.
PubMed |
open url image1

Lasseur B, Lothier J, Djoumad A, De Coninck B, Smeekens S, Van Laere A, Morvan-Bertrand A, Van den Ende W, Prud’homme MP (2006) Molecular and functional characterization of a cDNA encoding fructan:fructan 6G-fructosyltransferase (6G-FFT)/1-fructan:fructan fructosyltransferase (1-FFT) from perennial ryegrass (Lolium perenne L.). Journal of Experimental Botany 57, 2719–2734.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Livingston DP, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat, responses to second-phase cold hardening. Plant Physiology 116, 403–408.
Crossref | GoogleScholarGoogle Scholar | open url image1

Louahlia S, Macduff JH, Ourry A, Humphreys M, Boucaud J (1999) Nitrogen reserve status affects the dynamics of nitrogen remobilization and mineral nitrogen uptake during recovery of contrasting cultivars of Lolium perenne from defoliation. New Phytologist 142, 451–462.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marx SP, Nösberger J, Frehner M (1997) Hydrolysis of fructan in grasses: a β-(2-6)-linkage specific fructan-β-fructosidase from stubble of Lolium perenne. New Phytologist 135, 279–280.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miller LA, Moorby JM, Davies DR, Humphreys MO, Scollan ND, Macrae JC, Theodorou MK (2001) Increased concentration of water-soluble carbohydrate in perennial ryegrass (Lolium perenne L.). Milk production from late-lactation dairy cows. Grass and Forage Science 56, 383–394.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mino Y, Shimada A, Yamamoto S (1978) Effect of cutting height on the carbohydrate metabolism in haplocorm of timothy (Phleum pratense L.). Journal of the Japanese Society of Grass Sciences 24, 34–39. open url image1

Morvan A, Challe G, Prud’homme MP, Le Saos J, Boucaud J (1997) Rise of fructan exohydrolase activity in stubble of Lolium perenne after defoliation is decreased by uniconazole, an inhibitor of the biosynthesis of gibberellins. New Phytologist 136, 81–88.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morvan-Bertrand A, Pavis N, Boucaud J, Prud’homme MP (1999a) Partitioning of reserve and newly assimilated carbon in roots and leaf tissues of Lolium perenne during regrowth after defoliation: assessment by 13C steady-state labelling and carbohydrate analysis. Plant, Cell & Environment 22, 1097–1108.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morvan-Bertrand A, Boucaud J, Prud’homme MP (1999b) Influence of initial levels of carbohydrates, fructans, nitrogen, and soluble proteins on regrowth of Lolium perenne L. cv. Bravo following defoliation. Journal of Experimental Botany 50, 1817–1826.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morvan-Bertrand A, Boucaud J, Le Saos J, Prud’homme MP (2001) Roles of the fructans from leaf sheaths and from the elongating leaf bases in the regrowth following defoliation of Lolium perenne L. Planta 213, 109–120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Müller J, Aeschbacher RA, Sprenger N, Boller T, Wiemken A (2000) Disaccharide-mediated regulation of sucrose:fructan-6-fructosytransferase, a key enzyme of fructan synthesis in barley leaves. Plant Physiology 123, 265–273.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nowak RS, Caldwell MM (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61, 311–318.
Crossref | GoogleScholarGoogle Scholar | open url image1

Obenland DM, Simmen U, Boller T, Wiemken A (1991) Regulation of sucrose-sucrose-fructosyltransferase in barley leaves. Plant Physiology 97, 811–813.
PubMed |
open url image1

Ourry A, Bigot J, Boucaud J (1989) Protein mobilization from stubble and roots, and proteolytic activities during post-clipping regrowth of perennial ryegrass. Journal of Plant Physiology 134, 298–303. open url image1

Pavis N, Chatterton NJ, Harrison PA, Baumgartner S, Praznik W, Boucaud J, Prud’homme MP (2001a) Structure of fructans in roots and leaf tissues of Lolium perenne. New Phytologist 150, 83–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pavis N, Boucaud J, Prud’homme MP (2001b) Fructans and fructan-metabolizing enzymes in leaves of Lolium perenne. New Phytologist 150, 97–109.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pollock CJ , Eagles CF (1988) Low temperature and the growth of plants. In ‘Plants and temperature. Symposium of Society of Experimental Biology 42’. (Eds SP Long, FI Woodward) pp. 157–180. (Company of Biologists: Cambridge)

Pilon-Smits EAH, Ebskamp MJM, Paul MJ, Jeuken JW, Weisbeek PJ, Smeekens SCM (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiology 107, 127–130. open url image1

Prud’homme MP, Gonzalez B, Billard JP, Boucaud J (1992) Carbohydrate content, fructan and sucrose enzyme activities in roots, stubble and leaves of ryegrass (Lolium perenne L.) as affected by source/sink modification after cutting. Journal of Plant Physiology 140, 282–291. open url image1

Radojevic I, Simpson RJ, St John JA, Humphreys MO (1994) Chemical composition and in vivo digestibility of lines of Lolium perenne selected for high concentration of water-soluble carbohydrate. Australian Journal of Agricultural Research 45, 901–912.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. Biochimica et Biophysica Acta 1696, 253–261.
PubMed |
open url image1

Richards JH (1993) Physiology of plants recovering from defoliation. In ‘Grasslands for our world’. (Ed. MJ Bakes) pp. 46–54. (SIR Publishing: Wellington)

Roegiers P, Reheul D, Van Bogaert G (1988) The persistence of tetraploid perennial ryegrass in a mixture with diploid perennial ryegrass. Journal Agronomy & Crop Science 161, 40–44. open url image1

Rogers A, Fischer BU, Bryant J, Frehner M, Blum H, Raines CA, Long SP (1998) Acclimation of photosynthesis to elevated CO2 under low-nitrogen nutrition is affected by the capacity for assimilate utilization. Perennial ryegrass under free-air CO2 enrichment. Plant Physiology 118, 683–689.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Roth A, Lüscher M, Sprenger N, Boller T, Wiemken A (1997) Fructan and fructan-metabolizing enzymes in the growth zone of barley leaves. New Phytologist 136, 73–79.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryle GJA, Powell CE (1975) Defoliation and regrowth in the graminaceous plants: the role of current assimilate. Annals of Botany 39, 297–310. open url image1

Simpson RJ, Bonnett GD (1993) Fructan exohydrolase from grasses. New Phytologist 123, 453–469.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sprenger N, Bortlik K, Brandt A, Boller T, Wiemken A (1995) Purification, cloning, and functional expression of sucrose:fructan 6-fructosyltransferase, a key enzyme of fructan synthesis in barley. Proceedings of the National Academy of Sciences USA 92, 11#652–11#656.
Crossref | GoogleScholarGoogle Scholar | open url image1

Steel RGD , Torrie JA (1980) ‘Principles and procedures of statistics, 2nd edn.’ (McGraw-Hill: New York)

Szponarski W, Sommerer N, Boyer JC, Rossignol M, Gibart R (2004) Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by two-dimensional liquid chromatography. Proteomics 4, 397–406.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thornton B, Millard P (1997) Increased defoliation frequency depletes mobilization of nitrogen for leaf growth in grasses. Annals of Botany 80, 89–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turner LB, Cairns AJ, Armstead IP, Ashton J, Skøt K, Whittaker D, Humphreys MO (2006) Dissecting the regulation of fructan metabolism in perennial ryegrass (Lolium perenne) with quantitative trait locus mapping. New Phytologist 169, 45–58.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Turner LB, Humphreys MO, Cairns AJ, Pollock CJ (2001a) Comparison of growth and carbohydrate accumulation in seedlings of two varieties of Lolium perenne. Journal of Plant Physiology 158, 891–897.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turner LB, Humphreys MO, Cairns AJ, Pollock CJ (2001b) Carbon assimilation and partitioning into non-structural carbohydrate in contrasting varieties of Lolium perenne. Journal of Plant Physiology 158, 891–897.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van den Ende W, Michiels A, Van Wonterghem D, Clerens SP, De Roover J, Van Laere AJ (2001) Defoliation induces fructan 1-exohydrolase II in witloof chicory roots. Cloning and purification of two isoforms, fructan 1-exohydrolase IIa and fructan exohydrolase IIb. Mass fingerprint of the fructan 1-exohydrolase II enzymes. Plant Physiology 126, 1186–1195.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Van Huylenbroeck JM, Lootens P, Van Bockstaele E (1999) Photosynthetic characteristics of perennial ryegrass and red fescue turf-grass cultivars. Grass and Forage Science 54, 267–274.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vereyken IJ, Chupin V, Islamov A, Kuklin A, Hincha D, de Kruijff B (2003) The effect of fructan on the phospholipids organization in the dry state. Biophysical Journal 85, 3058–3065.
PubMed |
open url image1

Vijn I, Van Dijken A, Sprenger N, Van Dun K, Weisbeek P, Wiemken A, Smeekens S (1997) Fructan of the inulin neoseries is synthesized in transgenic chicory plants (Cichorium intybus L.) harbouring onion (Allium cepa L.) fructan:fructan 6G-fructosyltransferase. The Plant Journal 11, 387–398.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vitale A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends in Plant Science 4, 149–155.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Volenec JJ (1986) Nonstructural carbohydrates in stem base components of tall fescue during regrowth. Crop Science 26, 122–127. open url image1

Wiemken A, Frehner M, Keller F, Wagner W (1986) Fructan metabolism, enzymology and compartmentation. Current Topics in Plant Biochemistry and Physiology 5, 17–31. open url image1

Wilkins PW, Lovatt JA, Jones ML (2003) Improving annual yields of sugars and crude protein by recurrent selection within diploid ryegrass breeding populations, followed by chromosome doubling and hybridisation. Czech Journal of Genetics and Plant Breeding 39, 96–99. open url image1

Woledge J (1977) The effects of shading and cutting treatments on the photosynthetic rates of ryegrass leaves. Annals of Botany 41, 1279–1286. open url image1

Yamamoto S, Mino Y (1989) Mechanism of phleinase induction in the stem base of orchardgrass after defoliation. Journal of Plant Physiology 134, 258–260. open url image1