Abstract
Flowering time is important when adapting crop plants to different environments. While high feeding quality of forage grasses is facilitated by repression of flowering, flowering should also be inducible to facilitate grass seed production. Consequently, the identification and characterization of the genes controlling flowering time in forage grasses, including perennial ryegrass (Lolium perenne L.), is of great interest. In this study, three candidate genes for vernalization response genes in perennial ryegrass were identified based on DNA sequence homology to TmVRN1 and TmVRN2 of diploid wheat (Triticum monococcum), and Hd1 of rice (Oryza sativa). High sequence similarity between LpVRN1 and TmVRN1, co-localization of LpVRN1 with a major quantitative trait loci (QTL) for vernalization response in perennial ryegrass, synteny between map-positions of LpVRN1 and TmVRN1, mRNA expression analysis of LpVRN1 alleles during vernalization, and the correspondence between LpVRN1 mRNA expression levels and flowering time leads us to conclude that LpVRN1 is orthologous to TmVRN1 and that its function is conserved between diploid wheat and perennial ryegrass. Of the remaining two candidate genes, a putative Hd1 orthologue, LpCO, co-localized with a second QTL for vernlization response. LpCO has recently been shown to be involved in the photoperiodic regulation of flowering time. While epistasis, at the level of LpVRN1 transcription, was observed between the LpVRN1 and LpCO genomic regions, no differential expression of LpCO transcripts was observed during vernalization. While orthologous genes controlling flowering time can thus be identified, future allele sequencing efforts will reveal if causative polymorphisms are conserved across the grasses.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
analysis of variance
- AP1 :
-
APETALA1
- BAC:
-
bacterial artificial chromosome
- BLAST:
-
basic local alignment search tool
- CAB:
-
chlorophyll a/b binding protein
- CAPS:
-
cleaved amplified polymorphisms
- CCT:
-
CO, CO-like, TOC1
- EST:
-
expressed sequence tag
- FLC :
-
Flowering locus C
- Hd1 :
-
Heading date 1
- Hd3 :
-
Heading date 3
- LG:
-
linkage group
- LOD:
-
Likelihood of odds
- QTL:
-
quantitative trait loci
- TOC1 :
-
timing of CAB expression 1
- VRN1 :
-
VERNALIZATION1
- VRN2 :
-
VERNALIZATION2
- VIN3 :
-
VERNALIZATION INSENSITIVE 3
- ZCCT:
-
zink-finger/CCT domain transcription factor
References
V. Alm C. Fang C.S. Busso K.M. Devos K. Vollan Z. Grieg O.A. Rognli (2003) ArticleTitleA linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species Theor. Appl. Genet. 108 25–40 Occurrence Handle10.1007/s00122-003-1399-5 Occurrence Handle1:CAS:528:DC%2BD3sXpsVKrtbc%3D Occurrence Handle12923626
S.F. Altschul W. Gish W. Miller E.W. Myers D.J. Lipman (1990) ArticleTitleBasic local alignment search tool J. Mol. Biol. 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712
R. Amasino (2004) ArticleTitleVernalization, competence, and the epigenetic memory of winter Plant Cell 16 2553–2559 Occurrence Handle10.1105/tpc.104.161070 Occurrence Handle1:CAS:528:DC%2BD2cXptVSiu70%3D Occurrence Handle15466409
J.R. Andersen T. Lübberstedt (2003) ArticleTitleFunctional markers in plants Trends Plant Sci. 8 554–560 Occurrence Handle10.1016/j.tplants.2003.09.010 Occurrence Handle1:CAS:528:DC%2BD3sXos1Cnsrc%3D Occurrence Handle14607101
I.P. Armstead L.B. Turner M. Farrell L. Skøt P. Gomez T. Montoya I.S. Donnison I.P. King M.O. Humphreys (2004) ArticleTitleSynteny between a major heading-date QTL in perennial ryegrass (Lolium perenne L.) and the Hd3 heading date locus in rice Theor. Appl. Genet. 108 822–828 Occurrence Handle10.1007/s00122-003-1495-6 Occurrence Handle1:CAS:528:DC%2BD2cXktlals7g%3D Occurrence Handle14634728
I.P. Armstead L. Skot L.B. Turner K. Skot I.S. Donnison M.O. Humphreys I.P. King (2005) ArticleTitleIdentification of perennial ryegrass (Lolium perenne (L.)) and meadow fescue (Festuca pratensis (Huds.)) candidate orthologous sequences to the rice Hd1(Se1) and barley HvCO1 CONSTANS-like genes through comparative mapping and microsynteny New Phytol. 167 239–247 Occurrence Handle10.1111/j.1469-8137.2005.01392.x Occurrence Handle1:CAS:528:DC%2BD2MXmtl2ntrk%3D Occurrence Handle15948846
Asp, T., Didion, T., Holm, P.B., Nielsen, K.K. and Lübberstedt, T. 2005. EST development for nutrient utilization and forage quality of Lolium perenne. In: Plant Biotech Denmark. Annual meeting, 21 January 2005, Copenhagen, Denmark, Plant Biotech Denmark, Copenhagen, p. 15
R. Bastow J.S. Mylne C. Lister Z. Lippman R.A. Martienssen C. Dean (2004) ArticleTitleVernalization requires epigenetic silencing of FLC by histone methylation Nature 427 164–167 Occurrence Handle10.1038/nature02269 Occurrence Handle1:CAS:528:DC%2BD2cXhtFOnug%3D%3D Occurrence Handle14712277
J. Danyluk N.A. Kane G. Breton A.E. Limin D.B. Fowler F. Sarhan (2003) ArticleTitleTaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals Plant Physiol. 132 1849–1860 Occurrence Handle10.1104/pp.103.023523 Occurrence Handle1:CAS:528:DC%2BD3sXmsVant74%3D Occurrence Handle12913142
J. Dubcovsky D. Lijavetzky L. Appendino G. Tranquilli (1998) ArticleTitleComparative RFLP mapping of Triticum monococcum genes controlling vernalization requirements Theor. Appl. Genet. 97 968–975 Occurrence Handle10.1007/s001220050978 Occurrence Handle1:CAS:528:DyaK1cXotVahtb4%3D
M.A. Frohman M.K. Dush G.R. Martin (1988) ArticleTitleRapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer Proc. Natl Acad. Sci. USA 85 8998–9002 Occurrence Handle1:CAS:528:DyaL1MXntVCmtQ%3D%3D Occurrence Handle2461560
D. Fu P. Szücs L. Yan M. Helguera J.S. Skinner J. Zitzewitz Particlevon P.M. Hayes J. Dubcovsky (2005) ArticleTitleLarge deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat Mol. Gen. Genomics 273 54–65 Occurrence Handle10.1007/s00438-004-1095-4 Occurrence Handle1:CAS:528:DC%2BD2MXjvVGlsLw%3D
A.R. Gendall Y.Y. Levy A. Wilson C. Dean (2001) ArticleTitleThe VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis Cell 107 525–535 Occurrence Handle10.1016/S0092-8674(01)00573-6 Occurrence Handle1:CAS:528:DC%2BD3MXovVCnsbk%3D Occurrence Handle11719192
S. Griffiths R.P. Dunford G. Coupland D.A. Laurie (2003) ArticleTitleThe Evolution of CONSTANS-Like Gene Families in Barley, Rice, and Arabidopsis Plant Physiol. 131 1855–1867 Occurrence Handle10.1104/pp.102.016188 Occurrence Handle1:CAS:528:DC%2BD3sXjt1Sqsbc%3D Occurrence Handle12692345
R. Hayama S. Yokoi S. Tamaki M. Yano K. Shimamoto (2003) ArticleTitleAdaptation of photoperiodic control pathways produces short-day flowering in rice Nature 422 719–722 Occurrence Handle10.1038/nature01549 Occurrence Handle1:CAS:528:DC%2BD3sXivFGhsLo%3D Occurrence Handle12700762
Y. He R.M. Amasino (2005) ArticleTitleRole of chromatin modification in flowering-time control Trends Plant Sci. 10 30–35 Occurrence Handle10.1016/j.tplants.2004.11.003 Occurrence Handle1:CAS:528:DC%2BD2MXitFaqsg%3D%3D Occurrence Handle15642521
O.M. Heide (1994) ArticleTitleControl of flowering and reproduction in temperate grasses New Phytol. 128 347–362 Occurrence Handle1:CAS:528:DyaK2MXitFahsr8%3D
I.R. Henderson C. Dean (2004) ArticleTitleControl of Arabidopsis flowering: the chill before the bloom Development 131 3829–3838 Occurrence Handle10.1242/dev.01294 Occurrence Handle1:CAS:528:DC%2BD2cXns1SntL0%3D Occurrence Handle15289433
C.S. Jensen K. Salchert C. Gao C.H. Andersen T. Didion K.K. Nielsen (2004) ArticleTitleFloral inhibition in red fescue (Festuca rubra L.) through expression of a heterologous flowering repressor from Lolium Mol. Breed. 13 37–48 Occurrence Handle1:CAS:528:DC%2BD2cXkt1Krtg%3D%3D
L.B. Jensen J.R. Andersen U. Frei Y. Xing C. Taylor P.B. Holm T. Lübberstedt (2005a) ArticleTitleQTL mapping of vernalization response in perennial ryegrass (Lolium perenne L.) reveals co-location with an orthologue of wheat VRN1 Theor. Appl. Genet. 110 527–536 Occurrence Handle10.1007/s00122-004-1865-8 Occurrence Handle1:CAS:528:DC%2BD2MXhsVymsrc%3D
Jensen, L.B., Muylle, H., Arens, P., Andersen, C.H., Holm, P.B., Ghesquiére, M., Julier, B., Lübberstedt, T., Nielsen, K.K., de Riek, J., Roldán-Ruiz, I., Roulund, N., Taylor, C., Vosman, B. and Barre, P., 2005b. Development and mapping of a public reference set of SSR markers in Lolium perenne L. Mol Ecol Notes doi:10.1111/j.1471–8286.2005.01043.x
V. Lauvergeat P. Barre M. Bonnet M. Ghesquiére (2005) ArticleTitleSixty simple sequence repeat markers for use in the Festuca-Lolium complex in grasses Mol. Ecol. Notes 5 401–405 Occurrence Handle10.1111/j.1471-8286.2005.00941.x Occurrence Handle1:CAS:528:DC%2BD2MXlslKltrs%3D
Y.Y. Levy S. Mesnage J.S. Mylne A.R. Gendall C. Dean (2002) ArticleTitleMultiple roles of Arabidopsis VRN1 in vernalization and flowering time control Science 297 243–246 Occurrence Handle10.1126/science.1072147 Occurrence Handle1:CAS:528:DC%2BD38XlsVCnsL0%3D Occurrence Handle12114624
K.J. Livak T.D. Schmittgen (2001) ArticleTitleAnalysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method Methods 25 402–408 Occurrence Handle10.1006/meth.2001.1262 Occurrence Handle1:CAS:528:DC%2BD38XhtFelt7s%3D Occurrence Handle11846609
J. Martin M. Storgaard C.H. Andersen K.K. Nielsen (2004) ArticleTitlePhotoperiodic regulation of flowering in perennial ryegrass involving a CONSTANS-like homolog Plant Mol. Biol. 56 159–169 Occurrence Handle10.1007/s11103-004-2647-z Occurrence Handle1:CAS:528:DC%2BD2MXhtVerug%3D%3D Occurrence Handle15604735
S.D. Michaels R.M. Amasino (1999) ArticleTitleFLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering Plant Cell 11 949–956 Occurrence Handle10.1105/tpc.11.5.949 Occurrence Handle1:CAS:528:DyaK1MXjvVajsLc%3D Occurrence Handle10330478
K. Murai M. Miyamae H. Kato S. Takumi Y. Ogihara (2003) ArticleTitleWAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth Plant Cell Physiol. 44 1255–1265 Occurrence Handle10.1093/pcp/pcg171 Occurrence Handle1:CAS:528:DC%2BD2cXhsFKqsg%3D%3D Occurrence Handle14701921
A. Nepveu (2001) ArticleTitleRole of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development Gene 270 1–15 Occurrence Handle10.1016/S0378-1119(01)00485-1 Occurrence Handle1:CAS:528:DC%2BD3MXkt1KltLg%3D Occurrence Handle11403998
R.L. Ott (1993) An Introduction to Statistical Methods and Data Analysis Wadsworth Publishing Company Belmont, Ca 822–824
K. Petersen T. Didion C.H. Andersen K.K. Nielsen (2004) ArticleTitleMADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth J. Plant Phys. 161 439–447 Occurrence Handle1:CAS:528:DC%2BD2cXktlCksbc%3D
F. Robson M.M. Costa S.R. Hepworth I. Vizir M. Pineiro P.H. Reeves J. Putterill G. Coupland (2001) ArticleTitleFunctional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants Plant J. 28 619–631 Occurrence Handle10.1046/j.1365-313x.2001.01163.x Occurrence Handle1:CAS:528:DC%2BD38XhtV2kt7o%3D Occurrence Handle11851908
J. Schmitz R. Franzen T.H. Ngyuen F. Garcia-Maroto C. Pozzi F. Salamini W. Rohde (2000) ArticleTitleCloning, mapping and expression analysis of barley MADS-box genes Plant Mol. Biol. 42 899–913 Occurrence Handle10.1023/A:1006425619953 Occurrence Handle1:CAS:528:DC%2BD3cXks12jsLc%3D Occurrence Handle10890536
C.C. Sheldon J.E. Burn P.P. Perez J. Metzger J.A. Edwards W.J. Peacock E.S. Dennis (1999) ArticleTitleThe FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation Plant Cell 11 445–458 Occurrence Handle10.1105/tpc.11.3.445 Occurrence Handle1:CAS:528:DyaK1MXitlehsL4%3D Occurrence Handle10072403
J.D. Sherman L. Yan L. Talbert J. Dubcovsky (2004) ArticleTitleA PCR marker for growth habit in common wheat based on allelic variation at the VRN-A1 gene Crop Sci. 44 1832–1838 Occurrence Handle1:CAS:528:DC%2BD2cXotVCgu70%3D
S. Sung R.M. Amasino (2004) ArticleTitleVernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 Nature 427 159–164 Occurrence Handle10.1038/nature02195 Occurrence Handle1:CAS:528:DC%2BD2cXhtFOnsA%3D%3D Occurrence Handle14712276
G. Tranquilli J. Dubcovsky (1999) ArticleTitleEpistatic interaction between vernalization genes Vrn-Am1 and Vrn-Am2 in diploid wheat J. Hered. 91 304–306
B. Trevaskis D.J. Bagnall M.H. Ellis W.J. Peacock E.S. Dennis (2003) ArticleTitleMADS box genes control vernalization-induced flowering in cereals Proc. Natl Acad. Sci. USA 100 13099–13104 Occurrence Handle10.1073/pnas.1635053100 Occurrence Handle1:CAS:528:DC%2BD3sXoslKmsLY%3D Occurrence Handle14557548
J.W. Ooijen ParticleVan M.P. Boer R.C. Jansen C. Maliepaard (2002) MapQTL 4.0, Software for the Calculation of QTL Positions on Genetic Maps Plant Research International Wageningen
L. Yan A. Loukoianov G. Tranquilli M. Helguera T. Fahima J. Dubcovsky (2003) ArticleTitlePositional cloning of the wheat vernalization gene VRN1 Proc. Natl Acad. Sci. USA 100 6263–6268 Occurrence Handle1:CAS:528:DC%2BD3sXjvFOksr4%3D Occurrence Handle12730378
L. Yan A. Loukoianov A. Blechl G. Tranquilli W. Ramakrishna P. SanMiguel J.L. Bennetzen V. Echenique J. Dubcovsky (2004a) ArticleTitleThe wheat VRN2 gene is a flowering repressor down-regulated by vernalization Science 303 1640–1644 Occurrence Handle1:CAS:528:DC%2BD2cXhvFCnsb0%3D
L. Yan M. Helguera K. Kato S. Fukuyama J. Sherman J. Dubcovsky (2004b) ArticleTitleAllelic variation at the VRN-1 promoter region in polyploid wheat Theor. Appl. Genet. 109 1677–1686 Occurrence Handle10.1007/s00122-004-1796-4 Occurrence Handle1:CAS:528:DC%2BD2cXps1Ons7c%3D
M. Yano Y. Katayose M. Ashikari U. Yamanouchi L. Monna T. Fuse T. Baba K. Yamamoto Y. Umehara Y. Nagamura T. Sasaki (2000) ArticleTitleHd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS Plant Cell 12 2473–2484 Occurrence Handle10.1105/tpc.12.12.2473 Occurrence Handle1:CAS:528:DC%2BD3MXns1SgsQ%3D%3D Occurrence Handle11148291
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Andersen, J.R., Jensen, L.B., Asp, T. et al. Vernalization Response in Perennial Ryegrass (Lolium perenne L.) Involves Orthologues of Diploid Wheat (Triticum monococcum) VRN1 and Rice (Oryza sativa) Hd1. Plant Mol Biol 60, 481–494 (2006). https://doi.org/10.1007/s11103-005-4815-1
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-005-4815-1