Arabidopsis’te Vernalizasyon Olgusunda Yer Alan Bazı Genler

Kışlık bitkiler ancak uzun süreli soğuğa maruz kaldıktan sonra çiçek açabilmektedir. Bu olay vernalizasyon olarak bilinmektedir. Vernalizasyon Arabidopsis thaliana model bitkisinde ve monokotillerde geniş çapta incelenmiştir. Vernalizasyon olayı sayesinde çiçek aktivatör genleri baskılanmakta ve kışın çiçeklenme önlenmektedir. Arabidopsis'teki vernalizasyonda Flowering Locus C (FLC) anahtar roldeki baskılayıcıdır. Aynı zamanda FLC homologlarının da monokotil bitkilerde vernalizasyon tepkisinde önemli rol oynadığı bildirilmektedir. Monokotillerde FLC homologlarının varlığı, monokotil ve dikotil bitkilerin vernalizasyon yollarını kıyaslayabilmeye olanak sağlamaktadır. Bu mini derlemede, Arabidopsis bitkisi üzerinde vernalizasyon güdümlü çiçeklenme mekanizmasında rol alan bazı genlerin fonksiyonlarıyla ilgili bilgiler sunulmuştur. Bu sayede soğuk güdümlü çiçeklenmenin Arabidopsis model bitkisi üzerinde daha iyi anlaşılması, ekonomik açıdan önemli bitkilerin vernalizasyon ihtiyaçlarına yönelik ıslah stratejilerinde yol gösterici olacaktır.

The Genes Involved in Vernalization in Arabidopsis

Winter plants can bloom only after prolonged exposure to cold. This phenomenon is known as vernalization. Vernalization has been extensively studied in the model plant Arabidopsis thaliana and monocots. Thanks to the vernalization event, flower activator genes are suppressed and flowering is prevented in winter. Flowering Locus C (FLC) is the key suppressor in vernalization in A. thaliana. It is also reported that FLC homologs play an important role in the vernalization response in monocot plants. The presence of FLC homologs in monocots allows comparing the vernalization pathways of monocot and dicot plants. In this mini-review, information on the functions of some genes involved in the vernalization-driven flowering mechanism on the Arabidopsis sp. plant has been compiled. In this way, a better understanding of cold-driven flowering on the model plant may guide different plant breeding strategies to change the vernalization needs of economically important temperate plants.

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  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES. The molecular basis of vernalization: the centralrole of FLOWERING LOCUS C(FLC). PNAS 2000;97:3753–3758.
  • Amasino R. Vernalization, competence, and theepigenetic memory of winter. Plant Cell 2004; 16: 2553–2559.
  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ. The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 2007;12: 352–357.
  • Kim DH, Doyle MR, Sing S, Amasino RM. Vernalization: winter and the timing of flowering in plants.Annu Rev Cell Dev Biol 2009;25: 277–299
  • Sharma N, Geuten K, Giri BS. Varma A. The molecular mechanism of vernalization in Arabidopsis and cereals: role of Flowering Locus C and its homologs. Physiol Plantarum, 2020; 170: 373-383. https://doi.org/10.1111/ppl.13163
  • Chouard P. Vernalization and its relations to dormancy. Annu Rev Plant Physiol Plant Mol Biol. 1960;11:191–238.
  • Wang Y, Gu X, Yuan W, Schmitz RJ, He Y (2014) Photoperiodic control of the floral transition through a distinct polycomb repressive complex. Dev Cell 28: 727–736.
  • Wollenberg AC, Amasino RM. Natural variation in the temperature range permissive for vernalization in accessions of Arabidopsis thaliana. Plant Cell Environ. 2012;35:2181–2191.
  • Duncan S, Holm S, Questa J, Irwin J, Grant A, Dean C. Seasonal shift in timing of vernalization as an adaptation to extreme winter. Elife 2015;4: e06620.
  • Costa S, Dean C. Storing memories: the distinct phases of Polycomb-mediated silencing of Arabidopsis FLC. Biochem Soc Trans 2019;47:1187–1196.
  • Woodward AW, Bartel B. Biology in Bloom: A Primer on the Arabidopsis thaliana Model System. Genetics Society of America 2018.
  • Olivas NHD, Frago E, Thoen MPM., Kloth KJ, Becker KFM, van Loon JJA, Gort G, Keurentjes JJB, van Heerwaarden J, Dicke M. Natural variation in life history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds. Wiley Online Library 2017. https://doi.org/10.1111/mec.14100
  • Szymanski D. Arabidopsis thaliana: The Premier Model Plant. Brenner's Encyclopedia of Genetics 2013. https://doi.org/10.1016/B978-0-12- 374984-0.00088-7
  • Johnson X, Bouchez D. The Model Species, Arabidopsis thaliana. Science Publishers 2007. https://doi.org/10.1201/10.1201/b1 0760-23
  • Song J, Angel A, Howard M, Dean C. Vernalization: a cold induced epigenetic switch. J Cell Sci 2012;125:3723–373.
  • Bouché F, Detry N, Périlleux C. Heat can erase epigenetic marks of vernalization in Arabidopsis. Plant Signal Behav. 2015;10(3):e990799. doi: 10.4161/15592324.2014.990799. Erratum for: doi: 10.1111/tpj.12208. PMID: 25648822; PMCID: PMC4622702.
  • Preston JC, Fjellheim S. Flowering time runs hot and cold. Plant Physiol. 2022;190(1):5-18. doi: 10.1093/plphys/kiac111. PMID: 35274728; PMCID: PMC9434294.
  • Kerbler SM, Wigge PA. Temperature Sensing in Plants. Annu. Rev. Plant Biol. 2023;74:20.1-20.26.
  • Xu S, Chong K. Remembering winter through vernalisation. Nat. Plants 2018;4(12):997–1009.
  • Lee I, Bleecker A, Amasino R. Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol GenGenet 1993;237:171–176.
  • Clarke JH, Dean C. Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet 1994;242: 81–89.
  • Koornneef M, Vries BH, Hanhart C, Soppe W, Peeters T. The phenotype of some late-flowering mutants isenhanced by a locus on chromosome 5 that is not effective in the Landsbergerect a wildtype. Plant J 1994;6:911–919.
  • Whittaker C, Dean C. The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev CellDev Biol 2017;33: 555–575.
  • Choi K, Kim J, Hwang HJ, Kim S, Park C. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 2011;23(1):289–303.
  • Michaels SD, Amasino RM. Loss of FLOWERINGLOCUS C activity eliminates the late-flowering phenotypeof FRIGIDA and autonomous pathway mutations but notresponsiveness to vernalization. Plant Cell 2001;13: 935–941.
  • Jiang D, Gu X, He Y. Establishment of the winter-annual growth habit via FRIGIDA-mediated histonemethylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 2009;21:1733–1746.
  • Turck F, Fornara F, Coupland G. Regulation andidentity offlorigen: FLOWERING LOCUS T moves centerstage. Annu Rev Plant Biol 2008;59: 573–594.
  • Lee J, Oh M, Park H, Lee I. SOC1 translocated to thenucleus by interaction with AGL24 directly regulatesleafy. Plant J 2008;55: 832–843.
  • Alexandre CM, Hennig L. FLC or not FLC: the other side of vernalization. J. Exp. Bot. 2008;59(6):1127– 35.
  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 2004;427(6970):164–67.
  • Michaels SD, Amasino RM. FLOWERING LOCUS Cencodes a novel MADS domain protein that acts as arepressor of flowering. Plant Cell 1999;11: 949–956.
  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards J. A, Peacock W. J, Dennis ES. The FLF MADS box gene: arepressor offlowering inArabidopsisregulated byvernalization and methylation. Plant Cell. 1999;11: 445–458
  • Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM. Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 2005;137(1):149–56
  • Sheldon CC, Finnegan EJ, Dennis ES, Peacock WJ. 2006. Quantitative effects of vernalization on FLC and SOC1 expression. Plant J. 45(6):871–83.
  • Helliwell CA, Wood CC, Roberston M, Peacock JW,Dennis ES. The Arabidopsis FLC protein interactsdirectly in vivo with SOC1 and FT chromatin and is part ofa high-molecular-weight protein complex. Plant J 2006;46:183–192.
  • Searle I, He Y, Turck F, Vincent C, Fornara F, Krober S,Amasino RA, Coupland G. The transcription factorFLC confers aflowering response to vernalization byrepressing meristem competence and systemic signalingin Arabidopsis. Genes Dev 2006;20:898–912.
  • Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ,Dennis ES. FLOWERING LOCUS C (FLC) regulates development pathways throughout the lifecycle ofArabidopsis. Proc Natl Acad Sci USA 2011;108:6680–6685.
  • Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C. Multiple roles of Arabidopsis VRN1 in vernalization andflowering time control. Science 2002;297:243–246.
  • Gendall AR, Levy YY, Wilson A, Dean C. TheVERNALIZATION 2 gene mediates the epigeneticregulation of vernalization inArabidopsis. Cell 2001;107:525–535.
  • Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES,Helliwell CA. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 2006;103: 14631–14636.
  • Bond DM, Dennis ES, Finnegan EJ. Hypoxia: a novelfunction for VIN3. Plant Signal Behav 2009;4:773–776.
  • Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR,Dean C. The PHDfinger protein VRN5 functions inthe epigenetic silencing of Arabidopsis FLC. Curr Biol 2007;17:73–78.
  • Hepworth J, Antoniou-Kourounioti RL, Bloomer RH,Selga C, Berggren K, Cox D, Harris BRC, Irwin JA, Holm S,Sall T, Howard M, Dean C. Absence of warmthpermits epigenetic memory of winter in Arabidopsis. NatCommun 2018;9: 639.
  • De Lucia F, Crevillen P, Jones AM, Greb T, Dean C. APHD-polycomb repressive complex 2 triggers theepigenetic silencing of FLC during vernalization. ProcNatl Acad Sci USA 2008; 105:16831–16836.
  • Angel A, Song J, Dean C, Howard M. A Polycomb-based switch underlying quantitative epigenetic memory.Nature 2011;476:105–108.
  • Sung S, Amasino RM. Vernalization and epigenetics:how plants remember winter. Curr Opin Plant Biol 2004;7: 4–10.
  • Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L,Bernatavichute YV, Jacobsen SE, Fransz P, Dean C. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required forepigenetic silencing of FLC. Proc Natl Acad Sci USA 2006;103:5012–5017.
  • Zhang Y, Sikes ML, Beyer AL, Schnneider DA. The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc Natl Acad Sci USA 2009;106:2153–2158.
  • Pien S, Fleury D, Mylne JS, Crevillen P, Inzé D, Avramova Z, Dean C, Grossniklaus U. ARABIDOPSIS TRITHORAX 1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 2008;20:580–588.
  • Xiao J, Xiao J, Jin R, Yu X, Shen M, Wagner JD. Cis and trans determinants of epigenetic silencing byPolycomb repressive complex 2 in Arabidopsis. NatGenet 2017;49: 1546–1552.
  • Zhou Y, Wang Y, Krause K, Yang T, Dongus JA, Zhang Y, Turck F. Telobox motifs recruit CLF/SWN-PRC2 forH3K27me3 deposition via TRB factors in Arabidopsis. NatGenet 2018;50: 638–644.
  • Zhu D, Rosa S, Dean C (2015) Nuclear organization changesand the epigenetic silencing ofFLCduring vernalization.J Mol Biol 427: 659–669Edited by T. GrebPhysiol. Plant. 170, 2020
  • Wu Z, Fang X, Zhu D, Dean C. Autonomous pathway: FLOWERING LOCUS C repression through an antisense-mediated chromatin-silencing mechanism. Plant Physiol 2020;182:27–37.
  • Heo JB, Sung S. Vernalization-mediated epigeneticsilencing by a long intronic noncoding RNA. Science 2011;331:76–79.
  • Qüesta JI, Antoniou-Kourounioti RL, Rosa S, Li P, Duncan S,Whittaker C, Howard M, Dean C. Noncoding SNPsinfluence a distinct phase of Polycomb silencing todestabilize long-term epigenetic memory at Arabidopsis FLC. Genes Dev 2020;34: 446–461.
  • Çalışkan M. Horasan buğdayının (Triticum turanicum) farklı ekim zamanlarına ve ekim sıklıklarına tepkisinin belirlenmesi. (Yüksek lisans tezi). 2007. Kahramanmaraş Sütçü İmam Üniversitesi, Fen Bilimleri Enstitüsü, Kahramanmaraş.
  • Arabacı O, Konak C, Yılmaz R. Ekmeklik (Triticum aestivum L. Em. Thell) ve makarnalık (T. durum Desf.) buğdayda sulama ve ekim zamanının verim ve verim öğelerine etkisi. Ege Tarımsal Araştırma Dergisi, 2002;12(2), İzmir.
  • Fowler DB, Limin AE, Wang SY, Ward RW. Relationship between low-temperature tolerance and vernalization response in wheat and rye. Canadian J. Plant Sci. 1996;76(1), 37-42. DOI: 10.4141/cjps96-007.
  • Yıldırım T, Yakışır E, Eser C, Türköz M, Çeri S, Özer E, Kara İ, Yaşar M, Cerit Ş. Ekmeklik Buğday Çeşit ve Hatlarında Kışlık ve Yazlık Ekimlerin Morfolojik ve Fenolojik Özellikler Üzerine Etkisinin Belirlenmesi. Bahri Dağdaş Bitkisel Araştırma Dergisi, 2020; 9(2), 122-133.