植物学报 ›› 2017, Vol. 52 ›› Issue (6): 689-698.doi: 10.11983/CBB17132

• 特邀综述 • 上一篇    下一篇

CBF: 平衡植物低温应答与生长发育的关键

刘静妍, 施怡婷, 杨淑华*()   

  1. 中国农业大学植物生理学与生物化学国家重点实验室, 北京 100193
  • 收稿日期:2017-07-13 接受日期:2017-09-12 出版日期:2017-11-01 发布日期:2018-12-10
  • 通讯作者: 杨淑华 E-mail:yangshuhua@cau.edu.cn
  • 基金资助:
    国家自然科学基金青年科学基金(No.31700214)和中国博士后科学基金(No.2016M601174)

CBF: A Key Factor Balancing Plant Cold Stress Responses and Growth

Liu Jingyan, Shi Yiting, Yang Shuhua*()   

  1. State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University, Beijing 100193, China
  • Received:2017-07-13 Accepted:2017-09-12 Online:2017-11-01 Published:2018-12-10
  • Contact: Yang Shuhua E-mail:yangshuhua@cau.edu.cn

摘要:

低温是影响植物生长发育以及植被分布的重要环境因子。目前, 低温信号研究中比较清楚的是CBF依赖的低温信号途径。该文总结了近年来有关CBF的研究成果, 详细介绍了CBF家族成员在植物耐寒性中的重要作用, 着重分析与讨论CBF介导的低温调控网络及一系列复杂调控机制。理解CBF的复杂作用机制有助于了解植物中CBF介导的冷信号如何平衡耐寒性与生长发育, 进而有助于耐寒作物的培育。

关键词: CBF转录因子, 低温胁迫, 抗冻性, 生长发育

Abstract:

Cold stress is an important environmental factor that affects plant growth and development as well as plant distribution. The CBF-dependent cold signaling pathway has been extensively studied. In this review, we summarize the latest advances in research of CBF genes, revealing the important role of CBFs in freezing tolerance and in chilling resistance of plants. The understanding of the CBF regulatory mechanism network at multiple levels will provide new insights into how CBF-mediated cold signaling balances tolerance and growth in plants, which may help to improve cold- stress tolerance in crops.

Key words: CBF transcription factors, cold stress, freezing tolerance, growth and development

图1

CBF依赖的低温信号途径实线代表直接调控, 虚线代表间接调控。箭头代表正调控, T型箭头代表负调控。"

[1] Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008). The cold-inducible CBF1 factor: dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism.Plant Cell 20, 2117-2129.
doi: 10.1105/tpc.108.058941
[2] Agarwal M, Hao YJ, Kapoor A, Dong CH, Fujii H, Zheng XW, Zhu JK (2006). A R2R3 type MYB transcription factor is involved in the cold regulation ofCBF genes and in acquired freezing tolerance. J Biol Chem 281, 37636-37645.
[3] Baker SS, Wilhelm KS, Thomashow MF (1994). The 5'- region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24, 701-713.
[4] Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA (2008). Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome.Plant Physiol 147, 263-279.
doi: 10.1104/pp.108.118059 pmid: 18375597
[5] Blázquez MA, Ahn JH, Weigel D (2003). A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33, 168-171.
[6] Canella D, Gilmour SJ, Kuhn LA, Thomashow MF (2010). DNA binding by the Arabidopsis CBF1 transcription factor requires the PKKP/RAGRxKFxETRHP signature sequen- ce.Biochim Biophys Acta 1799, 454-462.
doi: 10.1016/j.bbagrm.2009.11.017 pmid: 19948259
[7] Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, Agarwal M, Zhu JK (2003). ICE1: a regulator of cold- induced transcriptome and freezing tolerance in Arabidopsis.Genes Dev 17, 1043-1054.
doi: 10.1101/gad.1077503 pmid: 12672693
[8] Deng CY, Ye HY, Fan M, Pu TL, Yan JB (2017). The rice transcription factors OsICE confer enhanced cold tolerance in transgenic Arabidopsis.Plant Signal Behav 12, e1316442.
doi: 10.1080/15592324.2017.1316442 pmid: 28414264
[9] Ding YL, Li H, Zhang XY, Xie Q, Gong ZZ, Yang SH (2015). OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis.Dev Cell 32, 278-289.
doi: 10.1016/j.devcel.2014.12.023 pmid: 25669882
[10] Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009). Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance.Plant Cell 21, 972-984.
doi: 10.1105/tpc.108.063958
[11] Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006). The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1.Proc Natl Acad Sci USA 103, 8281-8286.
doi: 10.1073/pnas.0602874103
[12] Dong MA, Farré EM, Thomashow MF (2011). Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis.Proc Natl Acad Sci USA 108, 7241-7246.
doi: 10.1073/pnas.1103741108 pmid: 21471455
[13] Eremina M, Unterholzner SJ, Rathnayake AI, Castellanos M, Khan M, Kugler KG, May ST, Mayer KFX, Rozhon W, Poppenberger B (2016). Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants.Proc Natl Acad Sci USA 113, E5982-E5991.
doi: 10.1073/pnas.1611477113 pmid: 27655893
[14] Espinoza C, Bieniawska Z, Hincha DK, Hannah MA (2008). Interactions between the circadian clock and cold- response in Arabidopsis.Plant Signal Behav 3, 593-594.
doi: 10.4161/psb.3.8.6340 pmid: 2634507
[15] Franklin KA, Whitelam GC (2007). Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39, 1410-1413.
[16] Fursova OV, Pogorelko GV, Tarasov VA (2009). Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Ge- ne 429, 98-103.
[17] Gilmour SJ, Fowler SG, Thomashow MF (2004). Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities.Plant Mol Biol 54, 767-781.
doi: 10.1023/B:PLAN.0000040902.06881.d4
[18] Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998). Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR ge- ne expression. Plant J 16, 433-442.
[19] Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.Science 290, 2110-2113.
doi: 10.1126/science.290.5499.2110 pmid: 11118138
[20] He JX, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang ZY (2005). BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses.Science 307, 1634-1638.
doi: 10.1126/science.1107580 pmid: 2925132
[21] Hong JH, Savina M, Du J, Devendran A, Ramakanth KK, Tian X, Sim WS, Mironova VV, Xu J (2017). A sacrifice-for-survival mechanism protects root stem cell niche from chilling stress.Cell 170, 102-113.
doi: 10.1016/j.cell.2017.06.002 pmid: 28648662
[22] Hu Y, Jiang LQ, Wang F, Yu DQ (2013). Jasmonate regulates the INDUCER OF CBF EXPRESSION-C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 cascade and freezing tolerance in Arabidopsis.Plant Cell 25, 2907-2924.
doi: 10.1105/tpc.113.112631 pmid: 23933884
[23] Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001). Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127, 910-917.
[24] Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tole- rance. Science 280, 104-106.
doi: 10.1126/science.280.5360.104 pmid: 9525853
[25] Jia YX, Ding YL, Shi YT, Zhang XY, Gong ZZ, Yang SH (2016). The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol 212, 345-353.
doi: 10.1111/nph.14088 pmid: 27353960
[26] Jiang BC, Shi YT, Zhang XY, Xin XY, Qi LJ, Guo HW, Li JG, Yang SH (2017). PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc Natl Acad Sci USA 114, E6695-E6702.
doi: 10.1073/pnas.1706226114 pmid: 28739888
[27] Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao MJ, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Sch?fer E, Jaeger KE, Wigge PA (2016). Phytochromes function as thermosensors in Arabidopsis.Science 354, 886-889.
doi: 10.1126/science.aaf6005 pmid: 27789797
[28] Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999). Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.Nat Biotechnol 17, 287-291.
doi: 10.1038/7036 pmid: 10096298
[29] Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004). A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45, 346-350.
[30] 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.Plant Cell 29, 760-774.
doi: 10.1105/tpc.16.00669 pmid: 28351986
[31] Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim JY, Chung WS (2017). Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis.Nucleic Acids Res 45, 6613-6627.
doi: 10.1093/nar/gkx417 pmid: 28510716
[32] Kim Y, Park S, Gilmour SJ, Thomashow MF (2013). Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis.Plant J 75, 364-376.
doi: 10.1111/tpj.12205 pmid: 23581962
[33] Lee BH, Henderson DA, Zhu JK (2005). The Arabidopsis cold-responsive transcriptome and its regulation by ICE1.Plant Cell 17, 3155-3175.
doi: 10.1105/tpc.105.035568 pmid: 16214899
[34] Lee CM, Thomashow MF (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance inArabidopsis thaliana. Proc Natl Acad Sci USA 109, 15054-15059.
doi: 10.1073/pnas.1211295109 pmid: 22927419
[35] Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hiltbrunner A, Wigge PA, Sch?fer E, Vierstra RD, Casal JJ (2016). Phytochrome B integrates light and temperature signals in Arabidopsis.Science 354, 897-900.
doi: 10.1126/science.aaf5656 pmid: 27789798
[36] Leivar P, Monte E (2014). PIFs: systems integrators in plant development.Plant Cell 26, 56-78.
doi: 10.1105/tpc.113.120857
[37] Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, Huq E, Quail PH (2008). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness.Curr Biol 18, 1815-1823.
doi: 10.1016/j.cub.2008.10.058 pmid: 19062289
[38] Li H, Ding YL, Shi YT, Zhang XY, Zhang SQ, Gong ZZ, Yang SH (2017a). MPK3- and MPK6-mediated ICE1 pho- sphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis.Dev Cell. doi:10.1016/ j.devcel.2017.09.025.
[39] Li H, Ye KY, Shi YT, Cheng JK, Zhang XY, Yang SH (2017b). BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabi- dopsis.Mol Plant 10, 545-559.
doi: 10.1016/j.molp.2017.01.004 pmid: 28089951
[40] Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (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 ge- ne expression, respectively, in Arabidopsis.Plant Cell 10, 1391-1406.
doi: 10.1105/tpc.10.8.1391 pmid: 9707537
[41] Liu ZY, Jia YX, Ding YL, Shi YT, Li Z, Guo Y, Gong ZZ, Yang SH (2017). Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response.Mol Cell 66, 117-128.
doi: 10.1016/j.molcel.2017.02.016 pmid: 28344081
[42] Lu X, Yang L, Yu MY, Lai JB, Wang C, McNeil D, Zhou MX, Yang CW (2017). A novel Zea mays ssp. mexicana L. MYC-type ICE-like transcription factor gene ZmmICE1, en- hances freezing tolerance in transgenic Arabidopsis tha- liana. Plant Physiol Biochem 113, 78-88.
[43] Ma Y, Dai XY, Xu YY, Luo W, Zheng XM, Zeng DL, Pan YJ, Lin XL, Liu HH, Zhang DJ, Xiao J, Guo XY, Xu SJ, Niu YD, Jin JB, Zhang H, Xu X, Li LG, Wang W, Qian Q, Ge S, Chong K (2015). COLD1 confers chilling tolerance in rice. Cell 160, 1209-1221.
[44] Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999). The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins who- se expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119, 463-470.
doi: 10.1104/pp.119.2.463 pmid: 9952441
[45] Medina J, Catalá R, Salinas J (2011). The CBFs: three Arabidopsis transcription factors to cold acclimate.Plant Sci 180, 3-11.
doi: 10.1016/j.plantsci.2010.06.019 pmid: 21421341
[46] Meshi T, Iwabuchi M (1995). Plant transcription factors.Plant Cell Physiol 36, 1405-1420.
[47] Mikkelsen MD, Thomashow MF (2009). A role for circadian evening elements in cold-regulated gene expression in Arabidopsis.Plant J 60, 328-339.
doi: 10.1111/j.1365-313X.2009.03957.x pmid: 19566593
[48] Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ash- worth EN, Bressan RA, Yun DJ, Hasegawa PM (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/DRE- B1A expression and freezing tolerance in Arabidopsis. Plant Cell 19, 1403-1414.
doi: 10.1105/tpc.106.048397 pmid: 17416732
[49] Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T (2012). Trans- criptional repressor PRR5 directly regulates clock-output pathways.Proc Natl Acad Sci USA 109, 17123-17128.
doi: 10.1073/pnas.1205156109
[50] Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009). Transcript profiling of an Arabidopsis PSEUDO RESP- ONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50, 447-462.
doi: 10.1093/pcp/pcp004 pmid: 19131357
[51] Ni M, Tepperman JM, Quail PH (1998). PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein.Cell 95, 657-667.
doi: 10.1016/S0092-8674(00)81636-0 pmid: 9845368
[52] Ni WM, Xu SL, González-Grandío E, Chalkley RJ, Huhmer AFR, Burlingame AL, Wang ZY, Quail PH (2017). PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3.Nat Commun 8, 15236.
doi: 10.1038/ncomms15236 pmid: 28492231
[53] Ni WM, Xu SL, Tepperman JM, Stanley DJ, Maltby DA, Gross JD, Burlingame AL, Wang ZY, Quail PH (2014). A mutually assured destruction mechanism attenuates light signaling in Arabidopsis.Science 344, 1160-1164.
doi: 10.1126/science.1250778 pmid: 24904166
[54] Nosenko T, B?ndel KB, Kumpfmüller G, Stephan W (2016). Adaptation to low temperatures in the wild tomato speciesSolanum chilense. Mol Ecol 25, 2853-2869.
[55] Novillo F, Alonso JM, Ecker JR, Salinas J (2004). CBF2/ DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101, 3985-3990.
doi: 10.1073/pnas.0303029101 pmid: 15004278
[56] 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.Proc Natl Acad Sci USA 104, 21002-21007.
doi: 10.1073/pnas.0705639105 pmid: 18093929
[57] Ohme-Takagi M, Shinshi H (1995). Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element.Plant Cell 7, 173-182.
doi: 10.2307/3869993 pmid: 7756828
[58] Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997). The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis.Proc Natl Acad Sci USA 94, 7076-7081.
doi: 10.1073/pnas.94.13.7076
[59] Park S, Lee CM, Doherty CJ, Gilmour SJ, Kim Y, Thom- ashow MF (2015). Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network.Plant J 82, 193-207.
doi: 10.1111/tpj.12796 pmid: 25736223
[60] Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004). Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45, 1042-1052.
doi: 10.1093/pcp/pch118 pmid: 15356330
[61] Riechmann JL, Meyerowitz EM (1998). The AP2/EREBP family of plant transcription factors.Biol Chem 379, 633-646.
doi: 10.1515/bchm.1998.379.6.633 pmid: 9687012
[62] Seo E, Lee H, Jeon J, Park H, Kim J, Noh YS, Lee I (2009). Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21, 3185-3197.
doi: 10.1105/tpc.108.063883 pmid: 19825833
[63] Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock re- gulation of temperature responses in Arabidopsis.Plant Cell 24, 2427-2442.
doi: 10.1105/tpc.112.098723
[64] Shi YT, Tian SW, Hou LY, Huang XZ, Zhang XY, Guo HW, Yang SH (2012). Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24, 2578-2595.
doi: 10.1105/tpc.112.098640 pmid: 22706288
[65] Shimura Y, Shiraiwa Y, Suzuki I (2012). Characterization of the subdomains in the N-terminal region of histidine kinase Hik33 in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 53, 1255-1266.
doi: 10.1093/pcp/pcs068 pmid: 22555814
[66] Stockinger EJ, Gilmour SJ, Thomashow MF (1997). Ara- bidopsis thaliana CBF1 encodes an AP2 domaincon- taining 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. Proc Natl Acad Sci USA 94, 1035-1040.
[67] Yin YH, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005). A new class of transcription factors mediates br- assinosteroid-regulated gene expression in Arabidopsis.Cell 120, 249-259.
doi: 10.1016/j.cell.2004.11.044 pmid: 15680330
[68] Zabulon G, Richaud C, Guidi-Rontani C, Thomas JC (2007). NblA gene expression in Synechocystis PCC 6803 strains lacking DspA (Hik33) and a NblR-like protein. Curr Microbiol 54, 36-41.
[69] Zhao CZ, Wang PC, Si T, Hsu CC, Wang L, Zayed O, Yu ZP, Zhu YF, Dong J, Tao WA, Zhu JK (2017). MAP kinase cascades regulate the cold response by modulating ICE1 protein stability.Dev Cell. doi: 10.1016/j.devcel. 2017.09.024
doi: 10.1016/j.devcel.2017.09.024 pmid: 29056551
[70] Zhao CZ, Zhang ZJ, Xie SJ, Si T, Li YY, Zhu JK (2016). Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis.Plant Phy- siol 171, 2744-2759.
doi: 10.1104/pp.16.00533 pmid: 27252305
[1] 王劲东,周豫,余佳雯,范晓磊,张昌泉,李钱峰,刘巧泉. miR172-AP2模块调控植物生长发育及逆境响应的研究进展[J]. 植物学报, 2020, 55(2): 205-215.
[2] 杨小青,黄晓琴,韩晓阳,刘腾飞,岳晓伟,伊冉. 外源物质对茶树耐寒及蔗糖代谢关键基因表达的影响[J]. 植物学报, 2020, 55(1): 21-30.
[3] 王梦龙,彭小群,陈竹锋,唐晓艳. 植物凝集素类受体蛋白激酶研究进展[J]. 植物学报, 2020, 55(1): 96-105.
[4] 郭倩倩, 周文彬. 植物响应联合胁迫机制的研究进展[J]. 植物学报, 2019, 54(5): 662-673.
[5] 杜康兮, 沈文辉, 董爱武. 表观遗传调控植物响应非生物胁迫的研究进展[J]. 植物学报, 2018, 53(5): 581-593.
[6] 魏华, 王岩, 刘宝辉, 王雷. 植物生物钟及其调控生长发育的研究进展[J]. 植物学报, 2018, 53(4): 456-467.
[7] 李雁群, 吴鸿. 药用植物生长发育与有效成分积累关系研究进展[J]. 植物学报, 2018, 53(3): 293-304.
[8] 韩丹璐, 赖建彬, 阳成伟. SUMO E3连接酶在植物生长发育中的功能研究进展[J]. 植物学报, 2018, 53(2): 175-184.
[9] 刘广超, 丁兆军. 生长素介导环境信号调控植物的生长发育[J]. 植物学报, 2018, 53(1): 17-26.
[10] 孙万梅, 王晓珠, 韩二琴, 韩丽, 孙丽萍, 彭再慧, 王邦俊. 亲免素在植物体内的功能研究进展[J]. 植物学报, 2017, 52(6): 808-819.
[11] 张玲玲, 吴丹, 赵子捷, 赵立群. 植物一氧化氮信号分子的研究进展[J]. 植物学报, 2017, 52(3): 337-345.
[12] 孙鲁龙, 耿庆伟, 邢浩, 杜远鹏, 翟衡. 低温处理葡萄根系对叶片PSII活性的影响[J]. 植物学报, 2017, 52(2): 159-166.
[13] 何明洁, 孙伊辰, 程晓园, 时冬雪, 李迪秦, 陈益银, 冯永坤, 刘璐, 范腾飞, 杨超, 曹凤秋, 刘来华. 植物谷氨酸受体的研究进展[J]. 植物学报, 2016, 51(6): 827-840.
[14] 李倩倩, 焦杨, 于静洋, 李秋莉. 转辽宁碱蓬SlNAC4拟南芥差异表达基因分析[J]. 植物学报, 2016, 51(6): 764-773.
[15] 缴莉, 付淑芳, 张雅丽, 卢江. U-box泛素连接酶调控植物抗逆和生长发育[J]. 植物学报, 2016, 51(5): 724-735.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] 刘剑秋 张清其 吴文珊. 金樱子花粉形态及营养成分研究[J]. 植物学报, 1994, 11(04): 43 -44 .
[2] 董杰;齐凤慧;詹亚光. 茶条槭悬浮培养体系的建立与没食子酸合成的优化条件[J]. 植物学报, 2008, 25(06): 734 -740 .
[3] 李国珍 秦明波 康宁玲 谢德玉 叶和春 李国凤. 新疆紫草的组织培养及其染色体分析[J]. 植物学报, 1992, 9(01): 37 -41 .
[4] 韩碧文. 根系的合成作用及其与地上部分的相关[J]. 植物学报, 1984, 2(23): 23 -25 .
[5] 王桂玲 秦智伟 周秀艳 赵咫云. 黄瓜果瘤的遗传及SSR 标记[J]. 植物学报, 2007, 24(02): 168 -172 .
[6] 杨晖 安黎哲 王治业 周剑平 王勋陵. UV-B 辐射对番茄花粉生活力的影响与内源激素和多胺的关系[J]. 植物学报, 2007, 24(02): 161 -167 .
[7] 郝照 赵雪晨 曾淑军 屈春英. 冬小麦麦苗不同叶龄的耐寒力[J]. 植物学报, 1985, 3(05): 38 -40 .
[8] 张惠珠 管中天 周林 徐国士. 中国两个苏铁植物群落的比较[J]. 植物学报, 1995, 12(专辑): 52 -58 .
[9] 曲良焕, 孙蒙祥. 位置信息与植物发育[J]. 植物学报, 2005, 22(03): 366 -374 .
[10] 任德勇, 何光华, 凌英华, 桑贤春, 杨正林, 赵芳明. 基于单片段代换系的水稻穗长QTL加性及其上位性效应[J]. 植物学报, 2010, 45(06): 662 -669 .