Is winter coming? Impact of the changing climate on plant responses to cold temperature.

biomolecular condensates cold acclimation epigenetics noncoding RNAs plant development regulation of gene expression stress responses thermosensors vernalization

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
11 2023
Historique:
revised: 23 06 2023
received: 03 05 2023
accepted: 03 07 2023
medline: 3 10 2023
pubmed: 13 7 2023
entrez: 13 7 2023
Statut: ppublish

Résumé

Climate change is causing alterations in annual temperature regimes worldwide. Important aspects of this include the reduction of winter chilling temperatures as well as the occurrence of unpredicted frosts, both significantly affecting plant growth and yields. Recent studies advanced the knowledge of the mechanisms underlying cold responses and tolerance in the model plant Arabidopsis thaliana. However, how these cold-responsive pathways will readjust to ongoing seasonal temperature variation caused by global warming remains an open question. In this review, we highlight the plant developmental programmes that depend on cold temperature. We focus on the molecular mechanisms that plants have evolved to adjust their development and stress responses upon exposure to cold. Covering both genetic and epigenetic aspects, we present the latest insights into how alternative splicing, noncoding RNAs and the formation of biomolecular condensates play key roles in the regulation of cold responses. We conclude by commenting on attractive targets to accelerate the breeding of increased cold tolerance, bringing up biotechnological tools that might assist in overcoming current limitations. Our aim is to guide the reflection on the current agricultural challenges imposed by a changing climate and to provide useful information for improving plant resilience to unpredictable cold regimes.

Identifiants

pubmed: 37438895
doi: 10.1111/pce.14669
doi:

Types de publication

Journal Article Review Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3175-3193

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Agarwal, M., Hao, Y., Kapoor, A., Dong, C.-H., Fujii, H., Zheng, X. et al. (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry, 281, 37636-37645. Available from: https://doi.org/10.1074/jbc.M605895200
Angel, A., Song, J., Dean, C. & Howard, M. (2011) A polycomb-based switch underlying quantitative epigenetic memory. Nature, 476, 105-108. Available from: https://doi.org/10.1038/nature10241
Antoniou-Kourounioti, R.L., Hepworth, J., Heckmann, A., Duncan, S., Qüesta, J., Rosa, S. et al. (2018) Temperature sensing is distributed throughout the regulatory network that controls FLC epigenetic silencing in vernalization. Cell Systems, 7, 643-655.e9. Available from: https://doi.org/10.1016/j.cels.2018.10.011
Antoniou-Kourounioti, R.L., Zhao, Y., Dean, C. & Howard, M. (2021) Feeling every bit of winter-distributed temperature sensitivity in vernalization. Frontiers in Plant Science, 12, 628726.
Basso, M.F., Ferreira, P.C.G., Kobayashi, A.K., Harmon, F.G., Nepomuceno, A.L., Molinari, H.B.C. et al. (2019) MicroRNAs and new biotechnological tools for its modulation and improving stress tolerance in plants. Plant Biotechnology Journal, 17, 1482-1500. Available from: https://doi.org/10.1111/pbi.13116
Benedict, C., Skinner, J.S., Meng, R., Chang, Y., Bhalerao, R., Huner, N.P. et al. (2006) The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant, Cell & Environment, 29, 1259-1272. Available from: https://doi.org/10.1111/j.1365-3040.2006.01505.x
Bentsink, L., Jowett, J., Hanhart, C.J. & Koornneef, M. (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences, 103, 17042-17047. Available from: https://doi.org/10.1073/pnas.0607877103
Berry, S., Hartley, M., Olsson, T.S.G., Dean, C. & Howard, M. (2015) Local chromatin environment of a polycomb target gene instructs its own epigenetic inheritance. eLife, 4, e07205. Available from:https://doi.org/10.7554/eLife.07205
Bevilacqua, P.C., Williams, A.M., Chou, H.-L. & Assmann, S.M. (2021) RNA multimerization as an organizing force for liquid-liquid phase separation. RNA, 28, 16-26. Available from: https://doi.org/10.1261/rna.078999.121
Blanco-Pastor, J.L. (2022) Alternative modes of introgression-mediated selection shaped crop adaptation to novel climates. Genome Biology and Evolution, 14, evac107. Available from: https://doi.org/10.1093/gbe/evac107
Bloomer, R.H. & Dean, C. (2017) Fine-tuning timing: natural variation informs the mechanistic basis of the switch to flowering in Arabidopsis thaliana. Journal of Experimental Botany, 68, 5439-5452. Available from: https://doi.org/10.1093/jxb/erx270
Borba, A.R., Serra, T.S., Górska, A., Gouveia, P., Cordeiro, A.M., Reyna-Llorens, I. et al. (2018) Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C4 photosynthesis is based on an ancient code found in the ancestral C3 state. Molecular Biology and Evolution, 35, 1690-1705. Available from: https://doi.org/10.1093/molbev/msy060
Burghardt, L.T., Edwards, B.R. & Donohue, K. (2016) Multiple paths to similar germination behavior in Arabidopsis thaliana. New Phytologist, 209, 1301-1312. Available from: https://doi.org/10.1111/nph.13685
Calderwood, A., Lloyd, A., Hepworth, J., Tudor, E.H., Jones, D.M., Woodhouse, S. et al. (2021) Total FLC transcript dynamics from divergent paralogue expression explains flowering diversity in Brassica napus. New Phytologist, 229, 3534-3548. Available from: https://doi.org/10.1111/nph.17131
Calixto, C.P.G., Guo, W., James, A.B., Tzioutziou, N.A., Entizne, J.C., Panter, P.E. et al. (2018) Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome[CC-BY]. The Plant Cell, 30, 1424-1444. Available from: https://doi.org/10.1105/tpc.18.00177
Calixto, C.P.G., Tzioutziou, N.A., James, A.B., Hornyik, C., Guo, W. & Zhang, R. et al. (2019) Cold-dependent expression and alternative splicing of Arabidopsis long non-coding RNAs. Frontiers in Plant Science, 10, 235.
Cao, Z., Zhao, T., Wang, L., Han, J., Chen, J., Hao, Y. et al. (2021) The lincRNA XH123 is involved in cotton cold-stress regulation. Plant Molecular Biology, 106, 521-531. Available from: https://doi.org/10.1007/s11103-021-01169-1
Capovilla, G., Delhomme, N., Collani, S., Shutava, I., Bezrukov, I., Symeonidi, E. et al. (2018) PORCUPINE regulates development in response to temperature through alternative splicing. Nature Plants, 4, 534-539. Available from: https://doi.org/10.1038/s41477-018-0176-z
Capovilla, G., Pajoro, A., Immink, R.G. & Schmid, M. (2015) Role of alternative pre-mRNA splicing in temperature signaling. Current Opinion in Plant Biology, 27, 97-103. Available from: https://doi.org/10.1016/j.pbi.2015.06.016
Carter, B., Bishop, B., Ho, K.K., Huang, R., Jia, W., Zhang, H. et al. (2018) The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis. The Plant Cell, 30, 1337-1352. Available from: https://doi.org/10.1105/tpc.17.00867
Castaings, L., Bergonzi, S., Albani, M.C., Kemi, U., Savolainen, O. & Coupland, G. (2014) Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives. Nature Communications, 5, 4457. Available from: https://doi.org/10.1038/ncomms5457
Catalá, R., Medina, J. & Salinas, J. (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceedings of the National Academy of Sciences, 108, 16475-16480. Available from: https://doi.org/10.1073/pnas.1107161108
Chahtane, H., Kim, W. & Lopez-Molina, L. (2016) Primary seed dormancy: a temporally multilayered riddle waiting to be unlocked. Journal of Experimental Botany, 68, erw377. Available from: https://doi.org/10.1093/jxb/erw377
Chan, Z., Wang, Y., Cao, M., Gong, Y., Mu, Z., Wang, H. et al. (2016) RDM4 modulates cold stress resistance in Arabidopsis partially through the CBF-mediated pathway. New Phytologist, 209, 1527-1539. Available from: https://doi.org/10.1111/nph.13727
Chekanova, J.A. (2015) Long non-coding RNAs and their functions in plants. Current Opinion in Plant Biology, 27, 207-216. Available from: https://doi.org/10.1016/j.pbi.2015.08.003
Chen, M., MacGregor, D.R., Dave, A., Florance, H., Moore, K., Paszkiewicz, K. et al. (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proceedings of the National Academy of Sciences, 111, 18787-18792. Available from: https://doi.org/10.1073/pnas.1412274111
Chiang, G.C.K., Bartsch, M., Barua, D., Nakabayashi, K., Debieu, M., Kronholm, I. et al. (2011) DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Molecular Ecology, 20, 3336-3349. Available from: https://doi.org/10.1111/j.1365-294X.2011.05181.x
Choi, K., Kim, J., Hwang, H.J., Kim, S., Park, C., Kim, S.Y. et al. (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. The Plant Cell, 23, 289-303. Available from: https://doi.org/10.1105/tpc.110.075911
Ciarmiello, L.F., Woodrow, P., Fuggi, A., Pontecorvo, G. & Carillo, P. (2011) Plant genes for abiotic stress. Abiotic Stress in Plants-Mechanisms and Adaptations, (pp. 283-308).
Coustham, V., Li, P., Strange, A., Lister, C., Song, J. & Dean, C. (2012) Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science, 337, 584-587. Available from: https://doi.org/10.1126/science.1221881
Crevillén, P., Yang, H., Cui, X., Greeff, C., Trick, M., Qiu, Q. et al. (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature, 515, 587-590. Available from: https://doi.org/10.1038/nature13722
Csorba, T., Questa, J.I., Sun, Q. & Dean, C. (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proceedings of the National Academy of Sciences, 111, 16160-16165. Available from: https://doi.org/10.1073/pnas.1419030111
De Lucia, F., Crevillen, P., Jones, A.M.E., Greb, T. & Dean, C. (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proceedings of the National Academy of Sciences, 105, 16831-16836. Available from: https://doi.org/10.1073/pnas.0808687105
Ding, Y., Jia, Y., Shi, Y., Zhang, X., Song, C., Gong, Z. et al. (2018) OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. The EMBO Journal, 37, e98228. Available from: https://doi.org/10.15252/embj.201798228
Ding, Y., Li, H., Zhang, X., Xie, Q., Gong, Z. & Yang, S. (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Developmental Cell, 32, 278-289. Available from: https://doi.org/10.1016/j.devcel.2014.12.023
Ding, Y., Lv, J., Shi, Y., Gao, J., Hua, J. & Song, C. et al. (2019) EGR2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. The EMBO Journal, 38, e99819. Available from:https://doi.org/10.15252/embj.201899819
Ding, Y., Shi, Y. & Yang, S. (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytologist, 222, 1690-1704. Available from: https://doi.org/10.1111/nph.15696
Ding, Y., Shi, Y. & Yang, S. (2020) Molecular regulation of plant responses to environmental temperatures. Molecular Plant, 13, 544-564. Available from: https://doi.org/10.1016/j.molp.2020.02.004
Dixon, L.E., Karsai, I., Kiss, T., Adamski, N.M., Liu, Z., Ding, Y. et al. (2019) VERNALIZATION1 controls developmental responses of winter wheat under high ambient temperatures. Development, 146, dev172684. Available from: https://doi.org/10.1242/dev.172684
Doherty, C.J., Van Buskirk, H.A., Myers, S.J. & Thomashow, M.F. (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. The Plant Cell, 21, 972-984. Available from: https://doi.org/10.1105/tpc.108.063958
Dong, C.-H. & Pei, H. (2014) Over-expression of miR397 improves plant tolerance to cold stress in Arabidopsis thaliana. Journal of Plant Biology, 57, 209-217. Available from: https://doi.org/10.1007/s12374-013-0490-y
Dong, M.A., Farré, E.M. & Thomashow, M.F. (2011) CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis. Proceedings of the National Academy of Sciences, 108, 7241-7246. Available from: https://doi.org/10.1073/pnas.1103741108
Dong, Y., Tang, M., Huang, Z., Song, J., Xu, J., Ahammed, G.J. et al. (2022) The miR164a-NAM3 module confers cold tolerance by inducing ethylene production in tomato. The Plant Journal, 111, 440-456. Available from: https://doi.org/10.1111/tpj.15807
Doğramacı, M., Horvath, D.P. & Anderson, J.V. (2015) Meta-analysis identifies potential molecular markers for endodormancy in crown buds of leafy spurge; a herbaceous perennial. In: Anderson, J.V. (Ed.) Advances in plant dormancy. Cham: Springer International Publishing, pp. 197-219. Available from:https://doi.org/10.1007/978-3-319-14451-1_12
Emenecker, R.J., Holehouse, A.S. & Strader, L.C. (2020) Emerging roles for phase separation in plants. Developmental Cell, 55, 69-83. Available from: https://doi.org/10.1016/j.devcel.2020.09.010
Eriksson, S.K., Kutzer, M., Procek, J., Gröbner, G. & Harryson, P. (2011) Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. The Plant Cell, 23, 2391-2404. Available from: https://doi.org/10.1105/tpc.111.085183
Falavigna, V.daS., Porto, D.D., Silveira, C.P. & Revers, L.F. (2015) Recent advances in genetics and molecular control of bud dormancy in pipfruits. In: Anderson, J.V. (Ed.) Advances in plant dormancy. Cham: Springer International Publishing, pp. 107-122. Available from: https://doi.org/10.1007/978-3-319-14451-1_5
Ferdous, J., Whitford, R., Nguyen, M., Brien, C., Langridge, P. & Tricker, P.J. (2017) Drought-inducible expression of Hv-miR827 enhances drought tolerance in transgenic barley. Functional & Integrative Genomics, 17, 279-292. Available from: https://doi.org/10.1007/s10142-016-0526-8
Finch-Savage, W.E. & Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist, 171, 501-523. Available from: https://doi.org/10.1111/j.1469-8137.2006.01787.x
Fowler, S. & Thomashow, M.F. (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway[W]. The Plant Cell, 14, 1675-1690. Available from: https://doi.org/10.1105/tpc.003483
Franco-Zorrilla, J.M. & Solano, R. (2017) Identification of plant transcription factor target sequences. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1860, 21-30. Available from: https://doi.org/10.1016/j.bbagrm.2016.05.001
Friedrich, T., Faivre, L., Bäurle, I. & Schubert, D. (2019) Chromatin-based mechanisms of temperature memory in plants. Plant, Cell & Environment, 42, 762-770. Available from: https://doi.org/10.1111/pce.13373
Fujii, Y., Tanaka, H., Konno, N., Ogasawara, Y., Hamashima, N., Tamura, S. et al. (2017) Phototropin perceives temperature based on the lifetime of its photoactivated state. Proceedings of the National Academy of Sciences, 114, 9206-9211. Available from: https://doi.org/10.1073/pnas.1704462114
Funes, I., Aranda, X., Biel, C., Carbó, J., Camps, F., Molina, A.J. et al. (2016) Future climate change impacts on apple flowering date in a Mediterranean subbasin. Agricultural Water Management, 164, 19-27. Available from: https://doi.org/10.1016/j.agwat.2015.06.013
Fürtauer, L., Weiszmann, J., Weckwerth, W. & Nägele, T. (2019) Dynamics of plant metabolism during cold acclimation. International Journal of Molecular Sciences, 20, 5411. Available from: https://doi.org/10.3390/ijms20215411
Gao, Z., Li, J., Luo, M., Li, H., Chen, Q., Wang, L. et al. (2019) Characterization and cloning of grape circular RNAs identified the cold resistance-related Vv-circATS1. Plant Physiology, 180, 966-985. Available from: https://doi.org/10.1104/pp.18.01331
Gautam, H., Sharma, A. & Trivedi, P.K. (2023) Plant microproteins and miPEPs: small molecules with much bigger roles. Plant Science, 326, 111519. Available from: https://doi.org/10.1016/j.plantsci.2022.111519
Gazzani, S., Gendall, A.R., Lister, C. & Dean, C. (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiology, 132, 1107-1114. Available from: https://doi.org/10.1104/pp.103.021212
Gentile, A., Dias, L.I., Mattos, R.S., Ferreira, T.H. & Menossi, M. (2015) MicroRNAs and drought responses in sugarcane. Frontiers in Plant Science, 6, 58.
Gilmour, S.J., Fowler, S.G. & Thomashow, M.F. (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology, 54, 767-781. Available from: https://doi.org/10.1023/B:PLAN.0000040902.06881.d4
Gilmour, S.J., Hajela, R.K. & Thomashow, M.F. (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiology, 87, 745-750. Available from:https://doi.org/10.1104/pp.87.3.745
Greb, T., Mylne, J.S., Crevillen, P., Geraldo, N., An, H., Gendall, A.R. et al. (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Current Biology, 17, 73-78. Available from: https://doi.org/10.1016/j.cub.2006.11.052
Guan, Q., Wu, J., Zhang, Y., Jiang, C., Liu, R., Chai, C. et al. (2013) A dead box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. The Plant Cell, 25, 342-356. Available from: https://doi.org/10.1105/tpc.112.108340
Hahm, J., Kim, K., Qiu, Y. & Chen, M. (2020) Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nature Communications, 11, 1660. Available from: https://doi.org/10.1038/s41467-020-15526-z
Hawkes, E.J., Hennelly, S.P., Novikova, I.V., Irwin, J.A., Dean, C. & Sanbonmatsu, K.Y. (2016) COOLAIR antisense RNAs form evolutionarily conserved elaborate secondary structures. Cell Reports, 16, 3087-3096. Available from: https://doi.org/10.1016/j.celrep.2016.08.045
Hazarika, T. (2013) Climate change and Indian horticulture: opportunities, challenges and mitigation strategies. Environmental Engineering and Management, 4, 629-630.
He, H., de Souza Vidigal, D., Snoek, L.B., Schnabel, S., Nijveen, H., Hilhorst, H. et al. (2014) Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. Journal of Experimental Botany, 65, 6603-6615. Available from: https://doi.org/10.1093/jxb/eru378
Heo, J.B. & Sung, S. (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science, 331, 76-79. Available from: https://doi.org/10.1126/science.1197349
Hepworth, J., Antoniou-Kourounioti, R.L., Bloomer, R.H., Selga, C., Berggren, K. & Cox, D. et al. (2018) Absence of warmth permits epigenetic memory of winter in Arabidopsis. Nature Communications, 9, 639. Available from: https://doi.org/10.1038/s41467-018-03065-7
Howe, G.T., Horvath, D.P., Dharmawardhana, P., Priest, H.D., Mockler, T.C. & Strauss, S.H. (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Frontiers in Plant Science, 6, 989.
Hyman, A.A., Weber, C.A. & Jülicher, F. (2014) Liquid-liquid phase separation in biology. Annual Review of Cell and Developmental Biology, 30, 39-58. Available from: https://doi.org/10.1146/annurev-cellbio-100913-013325
Irwin, J.A., Soumpourou, E., Lister, C., Ligthart, J.D., Kennedy, S. & Dean, C. (2016) Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas. The Plant Journal, 87, 597-605. Available from: https://doi.org/10.1111/tpj.13221
Jabre, I., Chaudhary, S., Guo, W., Kalyna, M., Reddy, A.S.N., Chen, W. et al. (2021) Differential nucleosome occupancy modulates alternative splicing in Arabidopsis thaliana. New Phytologist, 229, 1937-1945. Available from: https://doi.org/10.1111/nph.17062
Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. & Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science, 280, 104-106. Available from: https://doi.org/10.1126/science.280.5360.104
Jampala, P., Garhewal, A. & Lodha, M. (2021) Functions of long non-coding RNA in Arabidopsis thaliana. Plant Signaling & Behavior, 16, 1925440. Available from: https://doi.org/10.1080/15592324.2021.1925440
Janni, M., Gullì, M., Maestri, E., Marmiroli, M., Valliyodan, B., Nguyen, H.T. et al. (2020) Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity. Journal of Experimental Botany, 71, 3780-3802. Available from: https://doi.org/10.1093/jxb/eraa034
Jeknić, Z., Pillman, K.A., Dhillon, T., Skinner, J.S., Veisz, O., Cuesta-Marcos, A. et al. (2014) Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Molecular Biology, 84, 67-82. Available from: https://doi.org/10.1007/s11103-013-0119-z
Jeon, M., Jeong, G., Yang, Y., Luo, X., Jeong, D., Kyung, J. et al. (2023) Vernalization-triggered expression of the antisense transcript COOLAIR is mediated by CBF genes. eLife, 12, e84594. Available from: https://doi.org/10.7554/eLife.84594
Jia, Y., Ding, Y., Shi, Y., Zhang, X., Gong, Z. & Yang, S. (2016) The CBFs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytologist, 212, 345-353. Available from: https://doi.org/10.1111/nph.14088
Jiang, B., Shi, Y., Peng, Y., Jia, Y., Yan, Y., Dong, X. et al. (2020) Cold-induced CBF-PIF3 interaction enhances freezing tolerance by stabilizing the phyB thermosensor in Arabidopsis. Molecular Plant, 13, 894-906. Available from: https://doi.org/10.1016/j.molp.2020.04.006
Jiang, D. & Berger, F. (2017) DNA replication-coupled histone modification maintains polycomb gene silencing in plants. Science, 357, 1146-1149. Available from: https://doi.org/10.1126/science.aan4965
Jung, J.-H., Barbosa, A.D., Hutin, S., Kumita, J.R., Gao, M., Derwort, D. et al. (2020) A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature, 585, 256-260. Available from: https://doi.org/10.1038/s41586-020-2644-7
Jung, J.-H., Domijan, M., Klose, C., Biswas, S., Ezer, D., Gao, M. et al. (2016) Phytochromes function as thermosensors in Arabidopsis. Science, 354, 886-889. Available from: https://doi.org/10.1126/science.aaf6005
Kendall, S.L., Hellwege, A., Marriot, P., Whalley, C., Graham, I.A. & Penfield, S. (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. The Plant Cell, 23, 2568-2580. Available from: https://doi.org/10.1105/tpc.111.087643
Kerbler, S.M. & Wigge, P.A. (2022) Temperature sensing in plants. Annual Review of Plant Biology, 74, 341-366.
Kidokoro, S., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2022) Transcriptional regulatory network of plant cold-stress responses. Trends in Plant Science, 27, 922-935. Available from: https://doi.org/10.1016/j.tplants.2022.01.008
Kidokoro, S., Yoneda, K., Takasaki, H., Takahashi, F., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2017) Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. The Plant Cell, 29, 760-774. Available from: https://doi.org/10.1105/tpc.16.00669
Kim, J.Y., Kwak, K.J., Jung, H.J., Lee, H.J. & Kang, H. (2010) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA. Plant and Cell Physiology, 51, 1079-1083. Available from: https://doi.org/10.1093/pcp/pcq072
Kim, Y., Park, S., Gilmour, S.J. & Thomashow, M.F. (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. The Plant Journal, 75, 364-376. Available from: https://doi.org/10.1111/tpj.12205
Kim, D.H. & Sung, S. (2017) Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Developmental Cell, 40, 302-312e4. Available from: https://doi.org/10.1016/j.devcel.2016.12.021
Kindgren, P., Ard, R., Ivanov, M. & Marquardt, S. (2018) Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nature Communications, 9, 4561. Available from: https://doi.org/10.1038/s41467-018-07010-6
Kindgren, P., Ivanov, M. & Marquardt, S. (2019) Native elongation transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis. Nucleic Acids Research, 48, 2332-2347. Available from: https://doi.org/10.1093/nar/gkz1189
King, M., Altdorff, D., Li, P., Galagedara, L., Holden, J. & Unc, A. (2018) Northward shift of the agricultural climate zone under 21st-century global climate change. Scientific Reports, 8, 7904. Available from: https://doi.org/10.1038/s41598-018-26321-8
Kurikesu, I., Anuja, T.J., Gangaprasad, A. & Nair, A.J. (2018) Regulation of micrornas during biotic and abiotic stress. Bulletin of Pure & Applied Sciences- Botany, 37b, 49. Available from: https://doi.org/10.5958/2320-3196.2018.00007.1
Kwon, C.S., Lee, D., Choi, G. & Chung, W.-I. (2009) Histone occupancy-dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. The Plant Journal, 60, 112-121. Available from: https://doi.org/10.1111/j.1365-313X.2009.03938.x
Lamichhane, J.R. (2021) Rising risks of late-spring frosts in a changing climate. Nature Climate Change, 11, 554-555. Available from: https://doi.org/10.1038/s41558-021-01090-x
Lämke, J., Brzezinka, K., Altmann, S. & Bäurle, I. (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. The EMBO Journal, 35, 162-175. Available from: https://doi.org/10.15252/embj.201592593
Landry, M.P. & Mitter, N. (2019) How nanocarriers delivering cargos in plants can change the GMO landscape. Nature Nanotechnology, 14, 512-514. Available from: https://doi.org/10.1038/s41565-019-0463-5
Lee, B., Kapoor, A., Zhu, J. & Zhu, J.K. (2006) Stabilized1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. The Plant Cell, 18, 1736-1749. Available from: https://doi.org/10.1105/tpc.106.042184
Legris, M., Klose, C., Burgie, E.S., Rojas, C.C.R., Neme, M., Hiltbrunner, A. et al. (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science, 354, 897-900. Available from: https://doi.org/10.1126/science.aaf5656
Leviatan, N., Alkan, N., Leshkowitz, D. & Fluhr, R. (2013) Genome-wide survey of cold stress regulated alternative splicing in Arabidopsis thaliana with tiling microarray. PLoS ONE, 8, e66511. Available from: https://doi.org/10.1371/journal.pone.0066511
Li, F., Hu, Q., Chen, F. & Jiang, J.F. (2021) Transcriptome analysis reveals vernalization is independent of cold acclimation in Arabidopsis. BMC Genomics, 22, 462. Available from: https://doi.org/10.1186/s12864-021-07763-3
Li, H., Ding, Y., Shi, Y., Zhang, X., Zhang, S., Gong, Z. et al. (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Developmental Cell, 43, 630-642.e4. Available from: https://doi.org/10.1016/j.devcel.2017.09.025
Li, J., Kinoshita, T., Pandey, S., Ng, C.K.-Y., Gygi, S.P., Shimazaki, K. et al. (2002) Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature, 418, 793-797. Available from: https://doi.org/10.1038/nature00936
Li, P., Filiault, D., Box, M.S., Kerdaffrec, E., van Oosterhout, C., Wilczek, A.M. et al. (2014) Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes & Development, 28, 1635-1640. Available from: https://doi.org/10.1101/gad.245993.114
Li, S., Cheng, Z., Dong, S., Li, Z., Zou, L., Zhao, P. et al. (2022) Global identification of full-length cassava lncRNAs unveils the role of cold-responsive intergenic lncRNA 1 in cold stress response. Plant, Cell & Environment, 45, 412-426. Available from: https://doi.org/10.1111/pce.14236
Li, S., Yu, X., Lei, N., Cheng, Z., Zhao, P., He, Y. et al. (2017) Genome-wide identification and functional prediction of cold and/or drought-responsive lncRNAs in cassava. Scientific Reports, 7, 45981. Available from: https://doi.org/10.1038/srep45981
Liu, G., Liu, F., Wang, Y. & Liu, X. (2022) A novel long noncoding RNA CIL1 enhances cold stress tolerance in Arabidopsis. Plant Science, 323, 111370. Available from: https://doi.org/10.1016/j.plantsci.2022.111370
Liu, H.-H., Tian, X., Li, Y.-J., Wu, C.-A. & Zheng, C.-C. (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836-843. Available from: https://doi.org/10.1261/rna.895308
Liu, J., Shi, Y. & Yang, S. (2018) Insights into the regulation of C-repeat binding factors in plant cold signaling. Journal of Integrative Plant Biology, 60, 780-795. Available from: https://doi.org/10.1111/jipb.12657
Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. et al. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell, 10, 1391-1406. Available from: https://doi.org/10.1105/tpc.10.8.1391
Liu, W., Cheng, C., Lin, Y., XuHan, X. & Lai, Z. (2018) Genome-wide identification and characterization of mRNAs and lncRNAs involved in cold stress in the wild banana (Musa itinerans). PLoS ONE, 13, e0200002. Available from: https://doi.org/10.1371/journal.pone.0200002
Liu, Y., Cai, Y., Li, Y., Zhang, X., Shi, N. & Zhao, J. et al. (2022) Dynamic changes in the transcriptome landscape of Arabidopsis thaliana in response to cold stress. Frontiers in Plant Science, 13, 983460.
Liu, Y., Dang, P., Liu, L. & He, C. (2019) Cold acclimation by the CBF-COR pathway in a changing climate: lessons from Arabidopsis thaliana. Plant Cell Reports, 38, 511-519. Available from: https://doi.org/10.1007/s00299-019-02376-3
Liu, Y., Wang, K., Li, D., Yan, J. & Zhang, W. (2017) Enhanced cold tolerance and tillering in switchgrass (Panicum virgatum L.) by heterologous expression of Osa-miR393a. Plant and Cell Physiology, 58, 2226-2240. Available from: https://doi.org/10.1093/pcp/pcx157
Liu, Z., Jia, Y., Ding, Y., Shi, Y., Li, Z., Guo, Y. et al. (2017) Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Molecular Cell, 66, 117-128.e5. Available from: https://doi.org/10.1016/j.molcel.2017.02.016
Luedeling, E. (2012) Climate change impacts on winter chill for temperate fruit and nut production: a review. Scientia Horticulturae, 144, 218-229. Available from: https://doi.org/10.1016/j.scienta.2012.07.011
Ma, Y., Dai, X., Xu, Y., Luo, W., Zheng, X., Zeng, D. et al. (2015) COLD1 confers chilling tolerance in rice. Cell, 160, 1209-1221. Available from: https://doi.org/10.1016/j.cell.2015.01.046
Martínez-Berdeja, A., Stitzer, M.C., Taylor, M.A., Okada, M., Ezcurra, E., Runcie, D.E. et al. (2020) Functional variants of DOG1 control seed chilling responses and variation in seasonal life-history strategies in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 117, 2526-2534. Available from: https://doi.org/10.1073/pnas.1912451117
Michaels, S.D., Bezerra, I.C. & Amasino, R.M. (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proceedings of the National Academy of Sciences, 101, 3281-3285. Available from: https://doi.org/10.1073/pnas.0306778101
Mikulski, P., Wolff, P., Lu, T., Nielsen, M., Echevarria, E.F. & Zhu, D. et al. (2022) VAL1 acts as an assembly platform co-ordinating co-transcriptional repression and chromatin regulation at Arabidopsis FLC. Nature Communications, 13, 5542. Available from: https://doi.org/10.1038/s41467-022-32897-7
Miura, K., Jin, J.B., Lee, J., Yoo, C.Y., Stirm, V., Miura, T. et al. (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. The Plant Cell, 19, 1403-1414. Available from: https://doi.org/10.1105/tpc.106.048397
Moison, M., Pacheco, J.M., Lucero, L., Fonouni-Farde, C., Rodríguez-Melo, J., Mansilla, N. et al. (2021) The lncRNA APOLO interacts with the transcription factor WRKY42 to trigger root hair cell expansion in response to cold. Molecular Plant, 14, 937-948. Available from: https://doi.org/10.1016/j.molp.2021.03.008
Nakamichi, N., Kusano, M., Fukushima, A., Kita, M., Ito, S., Yamashino, T. et al. (2009) Transcript profiling of an Arabidopsis pseudo response regulator arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant and Cell Physiology, 50, 447-462. Available from: https://doi.org/10.1093/pcp/pcp004
Nambara, E., Keith, K., McCourt, P. & Naito, S. (1994) Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 gene. Plant and Cell Physiology, 35, 509-513. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a078623
Novillo, F., Medina, J. & Salinas, J. (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proceedings of the National Academy of Sciences, 104, 21002-21007. Available from: https://doi.org/10.1073/pnas.0705639105
Oberkofler, V., Pratx, L. & Bäurle, I. (2021) Epigenetic regulation of abiotic stress memory: maintaining the good things while they last. Current Opinion in Plant Biology, 61, 102007. Available from: https://doi.org/10.1016/j.pbi.2021.102007
Ohama, N., Sato, H., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2017) Transcriptional regulatory network of plant heat stress response. Trends in Plant Science, 22, 53-65. Available from: https://doi.org/10.1016/j.tplants.2016.08.015
Olate, E., Jiménez-Gómez, J.M., Holuigue, L. & Salinas, J. (2018) NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nature Plants, 4, 811-823. Available from: https://doi.org/10.1038/s41477-018-0254-2
O'Neill, C.M., Lu, X., Calderwood, A., Tudor, E.H., Robinson, P., Wells, R. et al. (2019) Vernalization and floral transition in autumn drive winter annual life history in oilseed rape. Current Biology, 29, 4300-4306.e2. Available from: https://doi.org/10.1016/j.cub.2019.10.051
Osterlund, M.T., Hardtke, C.S., Wei, N. & Deng, X.W. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature, 405, 462-466. Available from: https://doi.org/10.1038/35013076
Pajoro, A., Severing, E., Angenent, G.C. & Immink, R.G.H. (2017) Histone H3 lysine 36 methylation affects temperature-induced alternative splicing and flowering in plants. Genome Biology, 18, 102. Available from: https://doi.org/10.1186/s13059-017-1235-x
Park, J., Lim, C.J., Khan, I.U., Jan, M., Khan, H.A., Park, H.J. et al. (2018) Identification and molecular characterization of HOS15-interacting proteins in Arabidopsis thaliana. Journal of Plant Biology, 61, 336-345. Available from: https://doi.org/10.1007/s12374-018-0313-2
Park, S., Lee, C.-M., Doherty, C.J., Gilmour, S.J., Kim, Y. & Thomashow, M.F. (2015) Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. The Plant Journal, 82, 193-207. Available from: https://doi.org/10.1111/tpj.12796
Patop, I.L., Wüst, S. & Kadener, S. (2019) Past, present, and future of circRNAs. The EMBO Journal, 38, e100836. Available from: https://doi.org/10.15252/embj.2018100836
Pino, M.-T., Skinner, J.S., Jeknić, Z., Hayes, P.M., Soeldner, A.H., Thomashow, M.F. et al. (2008) Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant, Cell & Environment, 31, 393-406. Available from: https://doi.org/10.1111/j.1365-3040.2008.01776.x
Polisensky, D.H. & Braam, J. (1996) Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiology, 111, 1271-1279. Available from: https://doi.org/10.1104/pp.111.4.1271
Postma, F.M. & Ågren, J. (2022) Effects of primary seed dormancy on lifetime fitness of Arabidopsis thaliana in the field. Annals of Botany, 129, 795-808. Available from: https://doi.org/10.1093/aob/mcac010
Qüesta, J.I., Antoniou-Kourounioti, R.L., Rosa, S., Li, P., Duncan, S., Whittaker, C. et al. (2020) Noncoding SNPs influence a distinct phase of polycomb silencing to destabilize long-term epigenetic memory at Arabidopsis FLC. Genes & Development, 34, 446-461. Available from: https://doi.org/10.1101/gad.333245.119
Qüesta, J.I., Song, J., Geraldo, N., An, H. & Dean, C. (2016) Arabidopsis transcriptional repressor VAL1 triggers polycomb silencing at FLC during vernalization. Science, 353, 485-488. Available from: https://doi.org/10.1126/science.aaf7354
Quint, M., Delker, C., Franklin, K.A., Wigge, P.A., Halliday, K.J. & Van Zanten, M. (2016) Molecular and genetic control of plant thermomorphogenesis. Nature Plants, 2, 15190. Available from: https://doi.org/10.1038/nplants.2015.190
Rihan, H.Z., Al-Issawi, M. & Fuller, M.P. (2017) Upregulation of CBF/DREB1 and cold tolerance in artificial seeds of cauliflower (Brassica oleracea var. botrytis). Scientia Horticulturae, 225, 299-309. Available from: https://doi.org/10.1016/j.scienta.2017.07.017
Rinne, P.L.H., Welling, A., Vahala, J., Ripel, L., Ruonala, R., Kangasjärvi, J. et al. (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-Inducible 1,3-β-glucanases to reopen signal conduits and release dormancy in Populus. The Plant Cell, 23, 130-146. Available from: https://doi.org/10.1105/tpc.110.081307
Ronald, J. & Davis, S.J. (2019) Focusing on the nuclear and subnuclear dynamics of light and circadian signalling. Plant, Cell & Environment, 42, 2871-2884. Available from: https://doi.org/10.1111/pce.13634
Saeed, S., Usman, B., Shim, S.-H., Khan, S.U., Nizamuddin, S., Saeed, S. et al. (2022) CRISPR/Cas-mediated editing of cis-regulatory elements for crop improvement. Plant Science, 324, 111435. Available from: https://doi.org/10.1016/j.plantsci.2022.111435
Schranz, M.E., Quijada, P., Sung, S.-B., Lukens, L., Amasino, R. & Osborn, T.C. (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics, 162, 1457-1468. Available from: https://doi.org/10.1093/genetics/162.3.1457
Seo, P.J., Park, M.-J., Lim, M.-H., Kim, S.-G., Lee, M., Baldwin, I.T. et al. (2012) A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. The Plant Cell, 24, 2427-2442. Available from: https://doi.org/10.1105/tpc.112.098723
Shi, Y., Ding, Y. & Yang, S. (2018) Molecular regulation of CBF signaling in cold acclimation. Trends in Plant Science, 23, 623-637. Available from: https://doi.org/10.1016/j.tplants.2018.04.002
Shin, Y. & Brangwynne, C.P. (2017) Liquid phase condensation in cell physiology and disease. Science, 357, eaaf4382. Available from: https://doi.org/10.1126/science.aaf4382
Soltész, A., Smedley, M., Vashegyi, I., Galiba, G., Harwood, W. & Vágújfalvi, A. (2013) Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. Journal of Experimental Botany, 64, 1849-1862. Available from: https://doi.org/10.1093/jxb/ert050
Stockinger, E.J., Gilmour, S.J. & Thomashow, M.F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences, 94, 1035-1040. Available from: https://doi.org/10.1073/pnas.94.3.1035
Sung, S. & Amasino, R.M. (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature, 427, 159-164. Available from: https://doi.org/10.1038/nature02195
Sunkar, R. & Zhu, J.-K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis[W]. The Plant Cell, 16, 2001-2019. Available from: https://doi.org/10.1105/tpc.104.022830
Swiezewski, S., Liu, F., Magusin, A. & Dean, C. (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature, 462, 799-802. Available from: https://doi.org/10.1038/nature08618
Tähtiharju, S., Sangwan, V., Monroy, A.F., Dhindsa, R.S. & Borg, M. (1997) The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta, 203, 442-447.
Tao, Z., Hu, H., Luo, X., Jia, B., Du, J. & He, Y. (2019) Embryonic resetting of the parental vernalized state by two B3 domain transcription factors in Arabidopsis. Nature Plants, 5, 424-435. Available from: https://doi.org/10.1038/s41477-019-0402-3
Tao, Z., Shen, L., Gu, X., Wang, Y., Yu, H. & He, Y. (2017) Embryonic epigenetic reprogramming by a pioneer transcription factor in plants. Nature, 551, 124-128. Available from: https://doi.org/10.1038/nature24300
Thomashow, M.F. (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 571-599. Available from: https://doi.org/10.1146/annurev.arplant.50.1.571
Tondelli, A., Francia, E., Barabaschi, D., Pasquariello, M. & Pecchioni, N. (2011) Inside the CBF locus in Poaceae. Plant Science, 180, 39-45. Available from: https://doi.org/10.1016/j.plantsci.2010.08.012
Tylewicz, S., Petterle, A., Marttila, S., Miskolczi, P., Azeez, A., Singh, R.K. et al. (2018) Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science, 360, 212-215. Available from: https://doi.org/10.1126/science.aan8576
Unterberger, C., Brunner, L., Nabernegg, S., Steininger, K.W., Steiner, A.K., Stabentheiner, E. et al. (2018) Spring frost risk for regional apple production under a warmer climate. PLoS ONE, 13, e0200201. Available from: https://doi.org/10.1371/journal.pone.0200201
Vitasse, Y. & Rebetez, M. (2018) Unprecedented risk of spring frost damage in Switzerland and Germany in 2017. Climatic Change, 149, 233-246. Available from: https://doi.org/10.1007/s10584-018-2234-y
Vu, L.D., Xu, X., Gevaert, K. & De Smet, I. (2019) Developmental plasticity at high temperature. Plant Physiology, 181, 399-411. Available from: https://doi.org/10.1104/pp.19.00652
Wang, X., Ding, Y., Li, Z., Shi, Y., Wang, J., Hua, J. et al. (2019) PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Developmental Cell, 51, 222-235.e5. Available from: https://doi.org/10.1016/j.devcel.2019.08.008
Wang, Y., Gao, L., Zhu, B., Zhu, H., Luo, Y., Wang, Q. et al. (2018) Integrative analysis of long non-coding RNA acting as ceRNAs involved in chilling injury in tomato fruit. Gene, 667, 25-33. Available from: https://doi.org/10.1016/j.gene.2018.05.030
Waseem, M., Yang, X., Aslam, M.M., Li, M., Zhu, L., Chen, S. et al. (2022) Genome-wide identification of long non-coding RNAs in two contrasting rapeseed (Brassica napus L.) genotypes subjected to cold stress. Environmental and Experimental Botany, 201, 104969. Available from: https://doi.org/10.1016/j.envexpbot.2022.104969
Webb, M.S., Uemura, M. & Steponkus, P.L. (1994) A comparison of freezing injury in oat and Rye: two cereals at the extremes of freezing tolerance. Plant Physiology, 104, 467-478. Available from: https://doi.org/10.1104/pp.104.2.467
Wierzbicki, A.T., Blevins, T. & Swiezewski, S. (2021) Long noncoding RNAs in plants. Annual Review of Plant Biology, 72, 245-271. Available from: https://doi.org/10.1146/annurev-arplant-093020-035446
Wisniewski, M., Norelli, J., Bassett, C., Artlip, T. & Macarisin, D. (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta, 233, 971-983. Available from: https://doi.org/10.1007/s00425-011-1358-3
Wood, C.C., Robertson, M., Tanner, G., Peacock, W.J., Dennis, E.S. & Helliwell, C.A. (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proceedings of the National Academy of Sciences, 103, 14631-14636. Available from: https://doi.org/10.1073/pnas.0606385103
Xi, Y., Park, S.-R., Kim, D.-H., Kim, E.-D. & Sung, S. (2020) Transcriptome and epigenome analyses of vernalization in Arabidopsis thaliana. The Plant Journal, 103, 1490-1502. Available from: https://doi.org/10.1111/tpj.14817
Xu, G., Tao, Z. & He, Y. (2022) Embryonic reactivation of FLOWERING LOCUS C by ABSCISIC ACID-INSENSITIVE 3 establishes the vernalization requirement in each Arabidopsis generation. The Plant Cell, 34, 2205-2221. Available from: https://doi.org/10.1093/plcell/koac077
Yamauchi, Y., Ogawa, M., Kuwahara, A., Hanada, A., Kamiya, Y. & Yamaguchi, S. (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds[W]. The Plant Cell, 16, 367-378. Available from: https://doi.org/10.1105/tpc.018143
Yang, C., Li, D., Mao, D., Liu, X., Ji, C., Li, X. et al. (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant, Cell & Environment, 36, 2207-2218. Available from: https://doi.org/10.1111/pce.12130
Yang, H., Berry, S., Olsson, T.S.G., Hartley, M., Howard, M. & Dean, C. (2017) Distinct phases of polycomb silencing to hold epigenetic memory of cold in Arabidopsis. Science, 357, 1142-1145. Available from: https://doi.org/10.1126/science.aan1121
Yang, H., Howard, M. & Dean, C. (2014) Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Current Biology, 24, 1793-1797. Available from: https://doi.org/10.1016/j.cub.2014.06.047
Yang, M., Zhu, P., Cheema, J., Bloomer, R., Mikulski, P., Liu, Q. et al. (2022) In vivo single-molecule analysis reveals COOLAIR RNA structural diversity. Nature, 609, 394-399. Available from: https://doi.org/10.1038/s41586-022-05135-9
Yang, R., Hong, Y., Ren, Z., Tang, K., Zhang, H. & Zhu, J.-K. et al. (2019) A role for PICKLE in the regulation of cold and salt stress tolerance in Arabidopsis. Frontiers in Plant Science, 10, 900.
Ye, C.-Y., Chen, L., Liu, C., Zhu, Q.-H. & Fan, L. (2015) Widespread noncoding circular RNAs in plants. New Phytologist, 208, 88-95. Available from: https://doi.org/10.1111/nph.13585
Ye, K., Li, H., Ding, Y., Shi, Y., Song, C.-P. & Gong, Z. et al. (2019) BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. The Plant Cell, 31(11), 2682-2696. Available from: https://doi.org/10.1105/tpc.19.00058
Yoo, H., Triandafillou, C. & Drummond, D.A. (2019) Cellular sensing by phase separation: using the process, not just the products. Journal of Biological Chemistry, 294, 7151-7159. Available from: https://doi.org/10.1074/jbc.TM118.001191
Yuan, W., Luo, X., Li, Z., Yang, W., Wang, Y., Liu, R. et al. (2016) A cis cold memory element and a trans epigenome reader mediate polycomb silencing of FLC by vernalization in Arabidopsis. Nature Genetics, 48, 1527-1534. Available from: https://doi.org/10.1038/ng.3712
Zacharaki, V., Meena, S.K. & Kindgren, P. (2023) The non-coding RNA SVALKA locus produces a cis-natural antisense transcript that negatively regulates the expression of CBF1 and biomass production at normal temperatures. Plant Communications, 4, 100551. Available from: https://doi.org/10.1016/j.xplc.2023.100551
Zhang, D., Guo, X., Xu, Y., Li, H., Ma, L., Yao, X. et al. (2019) OsCIPK7 point-mutation leads to conformation and kinase-activity change for sensing cold response. Journal of Integrative Plant Biology, 61, 1194-1200. Available from: https://doi.org/10.1111/jipb.12800
Zhang, Z., Li, J., Li, F., Liu, H., Yang, W., Chong, K. et al. (2017) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Developmental Cell, 43, 731-743.e5. Available from: https://doi.org/10.1016/j.devcel.2017.11.016
Zhao, C., Wang, P., Si, T., Hsu, C.-C., Wang, L., Zayed, O. et al. (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Developmental Cell, 43, 618-629.e5. Available from: https://doi.org/10.1016/j.devcel.2017.09.024
Zhao, C., Zhang, Z., Xie, S., Si, T., Li, Y. & Zhu, J.-K. (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiology, 171, 2744-2759. Available from: https://doi.org/10.1104/pp.16.00533
Zhao, X., Li, J., Lian, B., Gu, H., Li, Y. & Qi, Y. (2018) Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nature Communications, 9, 5056 Available from: https://doi.org/10.1038/s41467-018-07500-7
Zhao, Y., Antoniou-Kourounioti, R.L., Calder, G., Dean, C. & Howard, M. (2020) Temperature-dependent growth contributes to long-term cold sensing. Nature, 583, 825-829. Available from: https://doi.org/10.1038/s41586-020-2485-4
Zhao, Y., Zhu, P., Hepworth, J., Bloomer, R., Antoniou-Kourounioti, R.L., Doughty, J. et al. (2021) Natural temperature fluctuations promote COOLAIR regulation of FLC. Genes & Development, 35, 888-898. Available from: https://doi.org/10.1101/gad.348362.121
Zhen, Y. & Ungerer, M.C. (2008) Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana. Molecular Biology and Evolution, 25, 2547-2555. Available from: https://doi.org/10.1093/molbev/msn196
Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M. & Luo, L. (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany, 61, 4157-4168. Available from: https://doi.org/10.1093/jxb/erq237
Zhou, M. & Luo, H. (2013) MicroRNA-mediated gene regulation: potential applications for plant genetic engineering. Plant Molecular Biology, 83, 59-75. Available from: https://doi.org/10.1007/s11103-013-0089-1
Zhu, P., Lister, C. & Dean, C. (2021) Cold-induced Arabidopsis FRIGIDA nuclear condensates for FLC repression. Nature, 599, 657-661. Available from: https://doi.org/10.1038/s41586-021-04062-5
Zuo, J., Wang, Q., Zhu, B., Luo, Y. & Gao, L. (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochemical and Biophysical Research Communications, 479, 132-138. Available from: https://doi.org/10.1016/j.bbrc.2016.07.032

Auteurs

Alvaro Santiago Larran (AS)

Centre for Research in Agricultural Genomics (CRAG) IRTA-CSIC-UAB-UB, Campus UAB, Barcelona, Spain.

Alice Pajoro (A)

National Research Council, Institute of Molecular Biology and Pathology, Rome, Italy.

Julia I Qüesta (JI)

Centre for Research in Agricultural Genomics (CRAG) IRTA-CSIC-UAB-UB, Campus UAB, Barcelona, Spain.

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