5.9
CiteScore
5.9
Impact Factor
Volume 49 Issue 11
Nov.  2022
Turn off MathJax
Article Contents

Molecular epigenetic mechanisms for the memory of temperature stresses in plants

doi: 10.1016/j.jgg.2022.07.004
Funds:

Research in the He laboratory is supported partly by the National Natural Science Foundation of China (31830049, 31721001, and 31970327) and the Peking-Tsinghua Joint Center for Life Sciences.

  • Received Date: 2022-06-09
  • Accepted Date: 2022-07-13
  • Rev Recd Date: 2022-07-13
  • Publish Date: 2022-07-20
  • The sessile plants encounter various stresses; some are prolonged, whereas some others are recurrent. Temperature is crucial for plant growth and development, and plants often encounter adverse high temperature fluctuations (heat stresses) as well as prolonged cold exposure such as seasonal temperature drops in winter when grown in temperate regions. Many plants can remember past temperature stresses to get adapted to adverse local temperature changes to ensure survival and/or reproductive success. Here, we summarize chromatin-based mechanisms underlying acquired thermotolerance or thermomemory in plants and review recent progresses on molecular epigenetic understanding of ‘remembering of prolonged cold in winter’ or vernalization, a process critical for various over-wintering plants to acquire competence to flower in the coming spring. In addition, perspectives on future study in temperature stress memories of economically-important crops are discussed.
  • loading
  • Abdelrahman, M., Burritt, D.J., Gupta, A., Tsujimoto, H., Tran, L.-S.P., Foyer, C., 2020. Heat stress effects on source-sink relationships and metabolome dynamics in wheat. J. Exp. Bot. 71, 543-554
    Aikawa, S., Kobayashi, M.J., Satake, A., Shimizu, K.K., Kudoh, H., 2010. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc. Natl. Acad. Sci. U S A 107, 11632-11637
    Andres, F., Coupland, G., 2012. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639
    Angel, A., Song, J., Dean, C., Howard, M., 2011. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105-108
    Avvakumov, N., Nourani, A., Cote, J., 2011. Histone chaperones: modulators of chromatin marks. Mol. Cell 41, 502-514
    Baier, M., Bittner, A., Prescher, A., van Buer, J., 2019. Preparing plants for improved cold tolerance by priming. Plant Cell Environ. 42, 782-800
    Banti, V., Mafessoni, F., Loreti, E., Alpi, A., Perata, P., 2010. The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 152, 1471-1483
    Baurle, I., 2016. Plant heat adaptation: priming in response to heat stress. F1000Res 5 (F1000 Faculty Rev), 694
    Blackledge, N.P., Klose, R.J., 2021. The molecular principles of gene regulation by Polycomb repressive complexes. Nat. Rev. Mol. Cell Biol. 22, 815-833
    Borg, M., Jacob, Y., Susaki, D., LeBlanc, C., Buendia, D., Axelsson, E., Kawashima, T., Voigt, P., Boavida, L., Becker, J., et al., 2020. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 22, 621-629
    Bouche, F., Woods, D.P., Amasino, R.M., 2017. Winter memory throughout the plant kingdom: different paths to flowering. Plant Physiol. 173, 27-35
    Brzezinka, K., Altmann, S., Baurle, I., 2019. BRUSHY1/TONSOKU/MGOUN3 is required for heat stress memory. Plant Cell Environ. 42, 771-781
    Brzezinka, K., Altmann, S., Czesnick, H., Nicolas, P., Gorka, M., Benke, E., Kabelitz, T., Jahne, F., Graf, A., Kappel, C., et al., 2016. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. Elife 5, e17061
    Buzas, D.M., Robertson, M., Finnegan, E.J., Helliwell, C.A., 2011. Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis Polycomb target gene FLC. Plant J. 65, 872-881
    Charng, Y.Y., Liu, H.C., Liu, N.Y., Chi, W.T., Wang, C.N., Chang, S.H., Wang, T.T., 2007. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 143, 251-262
    Charng, Y.Y., Liu, H.C., Liu, N.Y., Hsu, F.C., Ko, S.S., 2006. Arabidopsis HSA32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol. 140, 1297-1305
    Chen, A., Dubcovsky, J., 2012. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 8, e1003134
    Chen, N., Veerappan, V., Abdelmageed, H., Kang, M., Allen, R.D., 2018. HSI2/VAL1 silences AGL15 to regulate the developmental transition from seed maturation to vegetative growth in Arabidopsis. Plant Cell 30, 600-619
    Chen, Z., Galli, M., Gallavotti, A., 2022. Mechanisms of temperature-regulated growth and thermotolerance in crop species. Curr. Opin. Plant Biol. 65, 102134
    Choi, K., Kim, J., Hwang, H.J., Kim, S., Park, C., Kim, S.Y., Lee, I., 2011. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23, 289-303
    Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., Abrams, S.R., 2010. Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679
    De Lucia, F., Crevillen, P., Jones, A.M., Greb, T., Dean, C., 2008. A PHD-Polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. U S A 105, 16831-16836
    Diallo, A.O., Ali-Benali, M.A., Badawi, M., Houde, M., Sarhan, F., 2012. Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation. Mol. Genet. Genomics 287, 575-590
    Filichkin, S.A., Priest, H.D., Givan, S.A., Shen, R., Bryant, D.W., Fox, S.E., Wong, W.K., Mockler, T.C., 2010. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res. 20, 45-58
    Finkelstein, R.R., Lynch, T.J., 2000. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599-609
    Friedrich, T., Faivre, L., Baurle, I., Schubert, D., 2019. Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ. 42, 762-770
    Friedrich, T., Oberkofler, V., Trindade, I., Altmann, S., Brzezinka, K., Lamke, J., Gorka, M., Kappel, C., Sokolowska, E., Skirycz, A., et al., 2021. Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis. Nat. Commun. 12, 3426
    Greenup, A., Peacock, W.J., Dennis, E.S., Trevaskis, B., 2009. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 103, 1165-1172
    Harndahl, U., Hall, R.B., Osteryoung, K.W., Vierling, E., Bornman, J.F., Sundby, C., 1999. The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress Chaperones 4, 129-138
    He, Y., Doyle, M.R., Amasino, R.M., 2004. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18, 2774-2784
    He, Y.H., Chen, T., Zeng, X.L., 2020. Genetic and epigenetic understanding of the seasonal timing of flowering. Plant Commun. 1, 100008
    Heo, J.B., Sung, S., 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79
    Hsu, S.F., Lai, H.C., Jinn, T.L., 2010. Cytosol-localized heat shock factor-binding protein, AtHSBP, functions as a negative regulator of heat shock response by translocation to the nucleus and is required for seed development in Arabidopsis. Plant Physiol. 153, 773-784
    Jiang, D., Berger, F., 2017. DNA replication-coupled histone modification maintains Polycomb gene silencing in plants. Science 357, 1146-1149
    Jiang, D., Kong, N.C., Gu, X., Li, Z., He, Y., 2011. Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet. 7, e1001330
    Jiang, L., Hu, W., Qian, Y., Ren, Q., Zhang, J., 2021. Genome-wide identification, classification and expression analysis of the Hsf and Hsp70 gene families in maize. Gene 770, 145348
    Jo, L., Pelletier, J.M., Harada, J.J., 2019. Central role of the LEAFY COTYLEDON1 transcription factor in seed development. J. Integr. Plant Biol. 61, 564-580
    Kanno, Y., Jikumaru, Y., Hanada, A., Nambara, E., Abrams, S.R., Kamiya, Y., Seo, M., 2010. Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol. 51, 1988-2001
    Kyung, J., Jeon, M., Jeong, G., Shin, Y., Seo, E., Yu, J., Kim, H., Park, C.M., Hwang, D., Lee, I., 2022. The two clock proteins CCA1 and LHY activate VIN3 transcription during vernalization through the vernalization-responsive cis-element. Plant Cell 34, 1020-1037
    Lamke, J., Brzezinka, K., Altmann, S., Baurle, I., 2016. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. Embo J. 35, 162-175
    Larkindale, J., Hall, J.D., Knight, M.R., Vierling, E., 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882-897
    Li, C., Gu, L., Gao, L., Chen, C., Wei, C.Q., Qiu, Q., Chien, C.W., Wang, S., Jiang, L., Ai, L.F., et al., 2016. Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat. Genet. 48, 687-693
    Li, Z., Jiang, D., He, Y., 2018. FRIGIDA establishes a local chromosomal environment for FLOWERING LOCUS C mRNA production. Nat. Plants 4, 836-846
    Lin, M.-Y., Chai, K.H., Ko, S.S., Kuang, L.Y., Lur, H.S., Charng, Y.Y., 2014. A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol. 164, 2045-2053
    Ling, Y., Serrano, N., Gao, G., Atia, M., Mokhtar, M., Woo, Y.H., Bazin, J., Veluchamy, A., Benhamed, M., Crespi, M., et al., 2018. Thermopriming triggers splicing memory in Arabidopsis. J. Exp. Bot. 69, 2659-2675
    Liu, C., Lu, F., Cui, X., Cao, X., 2010. Histone methylation in higher plants. Annu. Rev. Plant Biol. 61, 395-420
    Liu, H.C., Liao, H.T., Charng, Y.Y., 2011. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 34, 738-751
    Liu, J., Feng, L., Gu, X., Deng, X., Qiu, Q., Li, Q., Zhang, Y., Wang, M., Deng, Y., Wang, E., et al., 2019. An H3K27me3 demethylase-HSFA2 regulatory loop orchestrates transgenerational thermomemory in Arabidopsis. Cell Res. 29, 379-390
    Liu, J., Feng, L., Li, J., He, Z., 2015. Genetic and epigenetic control of plant heat responses. Front. Plant Sci. 6, 267
    Liu, N.Y., Ko, S.S., Yeh, K.C., Charng, Y.Y., 2006. Isolation and characterization of tomato Hsa32 encoding a novel heat-shock protein. Plant Sci. 170, 976-985
    Luo, C., Sidote, D.J., Zhang, Y., Kerstetter, R.A., Michael, T.P., Lam, E., 2013. Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J. 73, 77-90
    Luo, X., He, Y., 2020. Experiencing winter for spring flowering: A molecular epigenetic perspective on vernalization. J. Integr. Plant Biol. 62, 104-117
    Luo, X., Ou, Y., Li, R.J., He, Y.H., 2020. Maternal transmission of the epigenetic 'memory of winter cold' in Arabidopsis. Nat. Plants 6, 1211-1218
    McKeown, M., Schubert, M., Marcussen, T., Fjellheim, S., Preston, J.C., 2016. Evidence for an early origin of vernalization responsiveness in temperate Pooideae grasses. Plant Physiol. 172, 416-426
    Michaels, S.D., Amasino, R.M., 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956
    Nagaraju, M., Reddy, P.S., Kumar, S.A., Srivastava, R.K., Kishor, P.B.K., Rao, D.M., 2015. Genome-wide scanning and characterization of Sorghum bicolor L. heat shock transcription factors. Curr. Genomics 16, 279-291
    Nakamura, S., Lynch, T.J., Finkelstein, R.R., 2001. Physical interactions between ABA response loci of Arabidopsis. Plant J. 26, 627-635
    Ng, H.H., Robert, F., Young, R.A., Struhl, K., 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709-719
    Nishizawa-Yokoi, A., Nosaka, R., Hayashi, H., Tainaka, H., Maruta, T., Tamoi, M., Ikeda, M., Ohme-Takagi, M., Yoshimura, K., Yabuta, Y., et al., 2011. HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol. 52, 933-945
    Nover, L., Bharti, K., Doring, P., Mishra, S.K., Ganguli, A., Scharf, K.D., 2001. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6, 177-189
    Oberkofler, V., Pratx, L., Baurle, I., 2021. Epigenetic regulation of abiotic stress memory: maintaining the good things while they last. Curr. Opin. Plant Biol 61
    Olas, J.J., Apelt, F., Annunziata, M.G., John, S., Richard, S.I., Gupta, S., Kragler, F., Balazadeh, S., Mueller-Roeber, B., 2021. Primary carbohydrate metabolism genes participate in heat-stress memory at the shoot apical meristem of Arabidopsis thaliana. Mol. Plant 14, 1508-1524
    Oliver, S.N., Finnegan, E.J., Dennis, E.S., Peacock, W.J., Trevaskis, B., 2009. Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl. Acad. Sci. U S A 106, 8386-8391
    Pandey, S.P., Benstein, R.M., Wang, Y., Schmid, M., van Zanten, M., 2021. Epigenetic regulation of temperature responses: past successes and future challenges. J. Exp. Bot. 21, 7482-7497
    Perrella, G., Baurle, I., Zanten, M., 2022. Epigenetic regulation of thermomorphogenesis and heat stress tolerance. New Phytol. 234, 1144-1160
    Richter, K., Haslbeck, M., Buchner, J., 2010. The heat shock response: Life on the verge of death. Mol. Cell 40, 253-266
    Sakata, Y., Nakamura, I., Taji, T., Tanaka, S., Quatrano, R.S., 2010. Regulation of the ABA-responsive Em promoter by ABI3 in the moss Physcomitrella patens: role of the ABA response element and the RY element. Plant Signal. Behav. 5, 1061-1066
    Scharf, K.D., Berberich, T., Ebersberger, I., Nover, L., 2012. The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochim. Biophys. Acta. 1819, 104-119
    Schlenkera, W., Roberts, M.J., 2009. Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change. Proc. Natl. Acad. Sci. U S A 106, 15594-15598
    Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R.A., Coupland, G., 2006. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898-912
    Sedaghatmehr, M., Mueller-Roeber, B., Balazadeh, S., 2016. The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis. Nat. Commun. 7, 12439
    Sharma, N., Ruelens, P., D'Hauw, M., Maggen, T., Dochy, N., Torfs, S., Kaufmann, K., Rohde, A., Geuten, K., 2017. A FLOWERING LOCUS C homolog is a vernalization-regulated repressor in Brachypodium and is cold regulated in wheat. Plant Physiol. 173, 1301-1315
    Shilatifard, A., 2012. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95
    Shindo, C., Aranzana, M.J., Lister, C., Baxter, C., Nicholls, C., Nordborg, M., Dean, C., 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol. 138, 1163-1173
    Shvedunova, M., Akhtar, A., 2022. Modulation of cellular processes by histone and non-histone protein acetylation. Nat. Rev. Mol. Cell Biol. 23, 329-349
    Stief, A., Altmann, S., Hoffmann, K., Pant, B.D., Scheible, W.R., Baurle, I., 2014. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26, 1792-1807
    Sung, S., Amasino, R.M., 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164
    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. Nat. Plants 5, 424-435
    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
    Urrea Castellanos, R., Friedrich, T., Petrovic, N., Altmann, S., Brzezinka, K., Gorka, M., Graf, A., Baurle, I., 2020. FORGETTER2 protein phosphatase and phospholipase D modulate heat stress memory in Arabidopsis. Plant J. 104, 7-17
    Wang, C., Zhang, Q., Shou, H.X., 2009a. Identification and expression analysis of OsHsfs in rice. J. Zhejiang Univ. Sci. B 10, 291-300
    Wang, J.-W., Czech, B., Weigel, D., 2009b. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749
    Wang, J.W., 2014. Regulation of flowering time by the miR156-mediated age pathway. J. Exp. Bot. 65, 4723-4730
    Wang, Y.P., Li, L., Ye, T.T., Lu, Y.M., Chen, X., Wu, Y., 2013. The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J. Exp. Bot. 64, 675-684
    Weng, M., Yang, Y.U.E., Feng, H., Pan, Z., Shen, W.-H., Zhu, Y.A.N., Dong, A., 2014. Histone chaperone ASF1 is involved in gene transcription activation in response to heat stress in Arabidopsis thaliana. Plant Cell Environ. 37, 2128-2138
    Wu, T.Y., Juan, Y.T., Hsu, Y.H., Wu, S.H., Liao, H.T., Fung, R., Charng, Y.Y., 2013. Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis. Plant Physiol. 161, 2075-2084
    Xiao, J., Xu, S.J., Li, C.H., Xu, Y.U., Xing, L.J., Niu, Y.D., Huan, Q., Tang, Y.M., Zhao, C.P., Wagner, D., et al., 2014. O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat. Nat. Commun. 5, 4572
    Xie, L., Zhang, Y., Wang, K., Luo, X., Xu, D., Tian, X., Li, L., Ye, X., Xia, X., Li, W., et al., 2021. TaVrt2, an SVP-like gene, cooperates with TaVrn1 to regulate vernalization-induced flowering in wheat. New Phytol. 231, 834-848
    Xin, M., Wang, Y., Yao, Y., Xie, C., Peng, H., Ni, Z., Sun, Q., 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol. 10, 123
    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. Plant Cell 34, 2205-2221
    Xu, S., Chong, K., 2018. Remembering winter through vernalisation. Nat. Plants 4, 997-1009
    Xu, S., Dong, Q., Deng, M., Lin, D., Xiao, J., Cheng, P., Xing, L., Niu, Y., Gao, C., Zhang, W., et al., 2021. The vernalization-induced long non-coding RNA VAS functions with the transcription factor TaRF2b to promote TaVRN1 expression for flowering in hexaploid wheat. Mol. Plant 14, 1525-1538
    Yamaguchi, N., Matsubara, S., Yoshimizu, K., Seki, M., Hamada, K., Kamitani, M., Kurita, Y., Nomura, Y., Nagashima, K., Inagaki, S., et al., 2021. H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis. Nat. Commun. 12, 3480
    Yan, L.L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., SanMiguel, P., Bennetzen, J.L., Echenique, V., Dubcovsky, J., 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640-1644
    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
    Yeh, C.H., Kaplinsky, N.J., Hu, C., Charng, Y.Y., 2012. Some like it hot, some like it warm: Phenotyping to explore thermotolerance diversity. Plant Sci. 195, 10-23
    Yu, X., Wang, H., Lu, Y., de Ruiter, M., Cariaso, M., Prins, M., van Tunen, A., He, Y., 2012. Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J. Exp. Bot. 63, 1025-1038
    Yuan, W., Luo, X., Li, Z., Yang, W., Wang, Y., Liu, R., Du, J., He, Y., 2016. A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nat. Genet. 48, 1527-1534
    Zeng, X., Gao, Z., Jiang, C., Yang, Y., Liu, R., He, Y., 2020. HISTONE DEACETYLASE 9 functions with Polycomb silencing to repress FLOWERING LOCUS C expression. Plant Physiol. 182, 555-565
    Zhao, C., Liu, B., Piao, S., Wang, X., Lobell, D.B., Huang, Y., Huang, M., Yao, Y., Bassu, S., Ciais, P., et al., 2017. Temperature increase reduces global yields of major crops in four independent estimates. Proc. Natl. Acad. Sci. U S A 114, 9326-9331
    Zhao, L., Wang, S., Cao, Z., Ouyang, W., Zhang, Q., Xie, L., Zheng, R., Guo, M., Ma, M., Hu, Z., et al., 2019. Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation. Nat. Commun. 10, 3640
    Zhao, Y.S., Antoniou-Kourounioti, R.L., Calder, G., Dean, C., Howard, M., 2020. Temperature-dependent growth contributes to long-term cold sensing. Nature 583, 825-829
    Zhong, L., Zhou, W., Wang, H., Ding, S., Lu, Q., Wen, X., Peng, L., Zhang, L., Lu, C., 2013. Chloroplast small heat shock protein HSP21 interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. Plant Cell 25, 2925-2943
    Zhou, C.M., Zhang, T.Q., Wang, X., Yu, S., Lian, H., Tang, H., Feng, Z.Y., Zozomova-Lihova, J., Wang, J.W., 2013. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340, 1097-1100
    Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324
    Zhu, P., Lister, C., Dean, C., 2021. Cold-induced Arabidopsis FRIGIDA nuclear condensates for FLC repression. Nature 599, 657-661
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (596) PDF downloads (87) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return