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

Hexokinase-dependent sugar signaling represses fructan exohydrolase activity in Lolium perenne1

Jérémy Lothier A , Bertrand Lasseur B , Marie-Pascale Prud’homme C and Annette Morvan-Bertrand C D
+ Author Affiliations
- Author Affiliations

A UMR-462 SAGAH, Université d’Angers, UFR Sciences2, Bd Lavoisier, F-49045 Angers Cedex, France.

B INRA/CNRS-URGV, 2 rue Gaston Crémieux, CP5708, F-91057 Evry cedex, France.

C UMR INRA-UCBN 950 EVA Ecophysiologie Végétale, Agronomie and nutritions NCS, Université de Caen Basse-Normandie, Esplanade de la Paix, F-14032 CAEN cedex, France.

D Corresponding author. Email: annette.bertrand@unicaen.fr

Functional Plant Biology 37(12) 1151-1160 https://doi.org/10.1071/FP10086
Submitted: 16 April 2010  Accepted: 7 September 2010   Published: 17 November 2010

Abstract

Defoliation of perennial ryegrass (Lolium perenne L.) by grazing animals leads to fructan mobilisation via an increase of fructan exohydrolase (FEH) activity. To highlight the regulation of fructan metabolism in perennial ryegrass, the role of sugars as signalling molecules for regulation of FEH activity after defoliation was evaluated. We used an original approach in planta by spraying stubble of defoliated plants (sugar starved plants) during 24 h with metabolisable sugars (glucose, fructose, sucrose) and sugar analogues (3-O-methylglucose, mannose, lactulose, turanose, palatinose). Metabolisable sugar (glucose, fructose, sucrose) supply following defoliation led to the repression of FEH activity increase. The supply of mannose, which is phosphorylated by hexokinase but not further metabolisable, led to the same repressive effect, whereas 3-O-methylglucose, which is not a substrate for hexokinase, had no effect. These results indicate that hexoses could be sensed by hexokinase, triggering a chain of events leading to the repression of FEH activity. By contrast, it was not possible to determine the role of sucrose as a signal since the supply of sucrose analogues (lactulose, turanose and palatinose) enhanced internal hexose content.

Additional keywords: cutting, disaccharides, grassland, sugar starvation, sugar sensing.


References

Amiard V, Morvan-Bertrand A, Billard J, Huault C, Prud’homme MP (2003) 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.
Fate of fructose supplied to leaf sheaths after defoliation of Lolium perenne L.: assessment by 13C-fructose labelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFCju7w%3D&md5=e92e7ef4861fb9680493a7edc4a33d5cCAS | 12654874PubMed |

Atanassova R, Leterrier M, Gaillard C, Agasse A, Sagot E, Coutos-Thevenot P, Delrot S (2003) Sugar-regulated expression of a putative hexose transport gene in grape. Plant Physiology 131, 326–334.
Sugar-regulated expression of a putative hexose transport gene in grape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVGntQ%3D%3D&md5=9ab28e86fd68ec2f9c8ad25ff6e9e952CAS | 12529540PubMed |

Brouquisse R, Evrard A, Rolin D, Raymond P, Roby C (2001) Regulation of protein degradation and protease expression by mannose in maize root tips. Pi sequestration by mannose may hinder the study of its signaling properties. Plant Physiology 125, 1485–1498.
Regulation of protein degradation and protease expression by mannose in maize root tips. Pi sequestration by mannose may hinder the study of its signaling properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFWrtbc%3D&md5=4dbe54f29b128a7b9888f61d98b7f141CAS | 11244127PubMed |

Cortès S, Gromova M, Evrard A, Roby C, Heyraud A, Rolin DB, Raymond P, Brouquisse RM (2003) In plants, 3-O-methylglucose is phosphorylated by hexokinase but not perceived as a sugar. Plant Physiology 131, 824–837.

De Coninck B, Van den Ende W, Le Roy K (2007) Fructan exohydrolases (FEHs) in plants: properties, occurrence and 3-D structure. In ‘Recent advances in fructooligosaccharides research’. (Eds N Shiomi, N Benkeblia, S Onodera) pp. 157–179. (Research Signpost: Kerala, India)

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.
Effect of defoliation on fructan pattern and fructan metabolizing enzymes in young chicory plants (Cichorium intybus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVersLs%3D&md5=d306aa15474c0328d5518aad8a218da4CAS |

Fernie AR, Roessner U, Geigenberger P (2001) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers. Plant Physiology 125, 1967–1977.
The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqurw%3D&md5=779f11376d42eb97c100893d727e3d0aCAS | 11299376PubMed |

Gallagher JA, Cairns AJ, Turner LB (2007) Fructan in temperate forage grasses, agronomy, physiology and molecular biology. In ‘Recent advances in fructooligosaccharides research’. (Eds N Shiomi, N Benkeblia, S Onodera) pp. 15–46. (Research Signpost: Kerala, India)

Gonzalez B, Boucaud B, Salette J, Langlois J, Duyme M (1989) Changes in stubble carbohydrate content during regrowth of defoliated ryegrasse (Lolium perenne L.) on two nitrogen levels. Grass and Forage Science 44, 411–415.
Changes in stubble carbohydrate content during regrowth of defoliated ryegrasse (Lolium perenne L.) on two nitrogen levels.Crossref | GoogleScholarGoogle Scholar |

Hendry G (1993) Evolutionary origins and natural functions of fructans: a climatological, biogeographic and mechanistic appraisal. New Phytologist 123, 3–14.

Kato-Noguchi H, Takaoka T, Izumori K (2005) Psicose inhibits lettuce root growth via a hexokinase-independent pathway. Physiologia Plantarum 125, 293–298.
Psicose inhibits lettuce root growth via a hexokinase-independent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1WqsrvI&md5=f6e55e29fa20343574cb402e12c7451cCAS |

Kaufman PB, Ghosheh NS, Lacroix JD, Soni SL, Ikuma H (1973) Regulation of invertase levels in avena stem segments by gibberellic acid, sucrose, glucose, and fructose. Plant Physiology 52, 221–228.
Regulation of invertase levels in avena stem segments by gibberellic acid, sucrose, glucose, and fructose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlt1ahtrg%3D&md5=d070e7491587be576bbbc308c184f728CAS | 16658535PubMed |

Kawakami A, Yoshida M, Van den Ende W (2005) Molecular cloning and functional analysis of a novel 6&1-FEH from wheat (Triticum aestivum L.) preferentially degrading small graminans like bifurcose. Gene 358, 93–101.
Molecular cloning and functional analysis of a novel 6&1-FEH from wheat (Triticum aestivum L.) preferentially degrading small graminans like bifurcose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVShtrnN&md5=276218a6b1ae8d74bdae448674e035eaCAS | 16051449PubMed |

Koops AJ, Jonker HH (1996) Purification and characterization of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus Colombia. II. Purification of sucrose : sucrose 1-fructosyltransferase and reconstitution of fructan synthesis in vitro with purified sucrose : sucrose 1-fructosyltransferase and fructan : fructan 1-fructosyltransferase. Plant Physiology 110, 1167–1175.

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.
Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslGitg%3D%3D&md5=dd2c0344d3497659918a59188965570aCAS |

Loreti E, Alpi A, Perata P (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of alpha amylase in barley embryos. Plant Physiology 123, 939–948.
Glucose and disaccharide-sensing mechanisms modulate the expression of alpha amylase in barley embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1SlsbY%3D&md5=9aa72dd29ec31a9ed1acd9a5600c1ad9CAS | 10889242PubMed |

Lothier J, Lasseur B, Le Roy K, Van Laere A, Prud’homme MP, Barre P, Van den Ende W, Morvan-Bertrand A (2007) Cloning, gene mapping, and functional analysis of a fructan 1-exohydrolase (1-FEH) from Lolium perenne implicated in fructan synthesis rather than in fructan mobilization. Journal of Experimental Botany 58, 1969–1983.
Cloning, gene mapping, and functional analysis of a fructan 1-exohydrolase (1-FEH) from Lolium perenne implicated in fructan synthesis rather than in fructan mobilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFeksLY%3D&md5=e8a5c0f67419ed06ec30fc846ecfdd9eCAS | 17456505PubMed |

Martínez-Noël GMA, Tognetti JA, Salerno GL, Wiemken A, Pontis HG (2009) Protein phosphatase activity and sucrose-mediated induction of fructan synthesis in wheat. Planta 230, 1071–1079.
Protein phosphatase activity and sucrose-mediated induction of fructan synthesis in wheat.Crossref | GoogleScholarGoogle Scholar | 19714360PubMed |

Marx SP, Nösberger J, Frehner M (1997) Hydrolysis of fructan in grasses: a β-(2–6)-linkage specific fructan-β-(2–6)-fructosidase from stubble of Lolium perenne. New Phytologist 135, 279–290.
Hydrolysis of fructan in grasses: a β-(2–6)-linkage specific fructan-β-(2–6)-fructosidase from stubble of Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis12itLs%3D&md5=086d58e1a691111442abface69d5220fCAS |

Michiels A, Van Laere A, Wim Van den Ende W, Tucker M (2004) Expression analysis of a chicory fructan 1-exohydrolase gene reveals complex regulation by cold. Journal of Experimental Botany 55, 1325–1333.
Expression analysis of a chicory fructan 1-exohydrolase gene reveals complex regulation by cold.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVSrtrs%3D&md5=c4979a2c18552171afb61a935ccca6edCAS | 15133058PubMed |

Morvan A, Challe G, Prud’homme M, 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.

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.
Roles of the fructans from leaf sheaths and from the elongating leaf bases in the regrowth following defoliation of Lolium perenne L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1ChsL0%3D&md5=073c092963c37f93fb094848f4b22687CAS | 11523646PubMed |

Müller J, Aeschbacher RA, Sprenger N, Boller T, Wiemken A (2000) Disaccharide-mediated regulation of sucrose: fructan-6-fructosyltransferase, a key enzyme of fructan synthesis in barley leaves. Plant Physiology 123, 265–274.
Disaccharide-mediated regulation of sucrose: fructan-6-fructosyltransferase, a key enzyme of fructan synthesis in barley leaves.Crossref | GoogleScholarGoogle Scholar | 10806243PubMed |

Nagaraj VJ, Altenbach D, Galati V, Lüscher M, Meyer AD, Boller T, Wiemken A (2004) Distinct regulation of sucrose: sucrose-1-fructosyltransferase (1-SST) and sucrose: fructan-6- fructosyltransferase. 6-SFT), the key enzymes of fructan synthesis in barley leaves: 1-sst as the pacemaker. New Phytologist 161, 735–748.
Distinct regulation of sucrose: sucrose-1-fructosyltransferase (1-SST) and sucrose: fructan-6- fructosyltransferase. 6-SFT), the key enzymes of fructan synthesis in barley leaves: 1-sst as the pacemaker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFehsbs%3D&md5=e66251b70995a1ba87f30750e78eed24CAS |

Pego JV, Weisbeek PJ, Smeekens SC (1999) Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiology 119, 1017–1024.
Mannose inhibits Arabidopsis germination via a hexokinase-mediated step.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFymurs%3D&md5=e31ec8fd5712531e50cc011b6eaec398CAS | 10069839PubMed |

Pollock C, Farrar J, Tomos D, Gallagher J, Lu C, Koroleva O (2003) Balancing supply and demand: the spatial distribution of carbon metabolism in grass and cereal leaves. Journal of Experimental Botany 54, 489–494.
Balancing supply and demand: the spatial distribution of carbon metabolism in grass and cereal leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFKgtbw%3D&md5=7269633152566fa716dbe63e4d2a71d4CAS | 12508059PubMed |

Roitsch T, Bittner M, Godt DE (1995) Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink source regulation. Plant Physiology 108, 285–294.
Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink source regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXls1OhsLY%3D&md5=b7ecbcf7eeb89eadf53cb813b6adc76dCAS | 7784506PubMed |

Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675–709.
Sugar sensing and signaling in plants: conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7k%3D&md5=09d490db7f78dc516b719928d061af6bCAS | 16669778PubMed |

Shiomi N (1989) Properties of fructosyltransferases involved in the synthesis of fructan in liliaceous plants. Journal of Plant Physiology 134, 151–155.

Umemura T, Perata P, Futsuhara Y, Yamaguchi J (1998) Sugar sensing and alpha-amylase gene repression in rice embryos. Planta 204, 420–428.
Sugar sensing and alpha-amylase gene repression in rice embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVOmtro%3D&md5=2d7e381d354ee7beea15f280ba345fb4CAS | 9684366PubMed |

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 1-exohydrolase IIb. Mass fingerprint of the fructan 1-exohydrolase II enzymes. Plant Physiology 126, 1186–1195.
Defoliation induces fructan 1-exohydrolase II in witloof chicory roots. Cloning and purification of two isoforms, fructan 1-exohydrolase IIa and fructan 1-exohydrolase IIb. Mass fingerprint of the fructan 1-exohydrolase II enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFegsLw%3D&md5=a90fe0921a1ec9c3ad2f3c61779fe9caCAS | 11457968PubMed |

Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A, Yoshida M, Kawakami A (2003) Fructan 1-exohydrolases. beta-(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.
Fructan 1-exohydrolases. beta-(2,1)-trimmers during graminan biosynthesis in stems of wheat? Purification, characterization, mass mapping, and cloning of two fructan 1- exohydrolase isoforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjsrY%3D&md5=5c1011fa010d540b63af64c7642e3ad0CAS | 12586886PubMed |

Van den Ende W, De Coninck B, Van Laere A (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends in Plant Science 9, 523–528.
Plant fructan exohydrolases: a role in signaling and defense?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFWrt7g%3D&md5=3cf5c944714ddc276b76188a8d006f30CAS | 15501176PubMed |

Van Riet L, Nagaraj V, Van den Ende W, Clerens S, Wiemken A, Van Laere A (2006) Purification, cloning and functional characterization of a fructan 6-exohydrolase from wheat (Triticum aestivum L.). Journal of Experimental Botany 57, 213–223.
Purification, cloning and functional characterization of a fructan 6-exohydrolase from wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCmsbjP&md5=324062cf6ae4bcfbcca97bf8d8765f18CAS | 16330524PubMed |

Van Riet L, Altenbach D, Vergauwen R, Clerens S, Kawakami A, Yoshida M, Van den Ende W, Wiemken A, Van Laere A (2008) Purification, cloning and functional differences of a third fructan 1-exohydrolase (1-FEHw3) from wheat (Triticum aestivum). Physiologia Plantarum 133, 242–253.
Purification, cloning and functional differences of a third fructan 1-exohydrolase (1-FEHw3) from wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFahtbw%3D&md5=d29abd80c07a95c782abf3425ef6d1a5CAS | 18346083PubMed |

Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiology 120, 351–360.
Fructan: more than a reserve carbohydrate?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFWrurc%3D&md5=0569c1a052a71105d2beadc18d3ddeb6CAS | 10364386PubMed |

Wagner W, Keller F, Wiemken A (1983) Fructan metabolism in cereals: induction in leaves and compartmentation in protoplasts and vacuoles. Zeitschrift für Pflanzenphysiologie 112, 359–372.

Wang N, Nobel PS (1998) Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti. Plant Physiology 116, 709–714.
Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1aisrc%3D&md5=071f6b2892931a4b2e020946a748915eCAS | 9490769PubMed |

Yamamoto S, Mino Y (1987) Effect of sugar level on phleinase induction in stem base of orchardgrass after defoliation. Physiologia Plantarum 69, 456–460.
Effect of sugar level on phleinase induction in stem base of orchardgrass after defoliation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhslejs7s%3D&md5=3e8aa4d780c05fc3f6126004b42059dbCAS |

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