植物学报 ›› 2021, Vol. 56 ›› Issue (6): 651-663.DOI: 10.11983/CBB21103
张长生, 魏滔, 周玉萍, 范甜, 吕天晓, 田长恩(
)
首页收稿日期:2021-06-29
接受日期:2021-09-10
出版日期:2021-11-01
发布日期:2021-11-12
通讯作者:
田长恩
作者简介:* E-mail: changentian@aliyun.com基金资助:
Changsheng Zhang, Tao Wei, Yuping Zhou, Tian Fan, Tianxiao Lü, Chang'en Tian()
Received:2021-06-29
Accepted:2021-09-10
Online:2021-11-01
Published:2021-11-12
Contact:
Chang'en Tian
摘要：
FLC是植物成花关键抑制因子, 主要通过结合到其下游2个关键的成花促进基因(FT和SOC1)启动子上而抑制二者的表达。此外, 还可以与其它调控因子结合调控开花。然而, 关于FLC在成花调控中的具体分子机制仍需深入研究。该文主要结合8条成花调控遗传途径, 梳理近年来与FLC相关的新进展, 并展望了未来的研究方向。
张长生, 魏滔, 周玉萍, 范甜, 吕天晓, 田长恩. FLC调控植物成花的分子机制研究新进展. 植物学报, 2021, 56(6): 651-663.
Changsheng Zhang, Tao Wei, Yuping Zhou, Tian Fan, Tianxiao Lü, Chang'en Tian. Progress in Flowering Regulation Mechanisms of FLC. Chinese Bulletin of Botany, 2021, 56(6): 651-663.
| 调控类型 | 调控因子 | 分子机制 | 参考文献 |
|---|---|---|---|
| 染色质重塑 | EFS | 一个组蛋白甲基转移酶, 通过下调FLC染色质H3Lys 4三甲基化水平, 抑制FLC表达; 同时也能与FRI形成复合物, 通过甲基化修饰促进FLC表达 | Kim et al., |
| LHP1 | 通过介导PRC2向染色质招募组蛋白甲基转移酶促进FLC染色质的H3K27me3积累, 进而维持FLC沉默 | Zhou et al., | |
| ICU11 | 一个2-氧戊二酸依赖的双加氧酶, 与非特异性组蛋白去甲基化有关, 其功能缺失后破坏低温诱导的PRC2复合物介导的FLC沉默, 从而导致晚花 | Bloomer et al., | |
| VRN1与VRN2 | 分别通过提高FLC启动子和第1个内含子区域内H3K9me2和H3K27 me2的水平, 抑制FLC表达 | Sung and Amasino, | |
| SWP与CZS | 二者形成复合体, 通过调控FLC染色质的H3K9和H3K27甲基化和H4去乙酰化, 抑制FLC表达 | Jiang et al., | |
| REF6 | 一个H3K27去甲基化转移酶, 使FLC去甲基化而抑制FLC表达 | Lu et al., | |
| PRMT5 | 通过调控FLC染色质H4R3对称性双甲基化, 下调FLC表达 | 牛丽芳, | |
| JMJ18 | 一个组蛋白H3K4去甲基化酶, 通过与FLC结合, 降低H3K4甲基化水平, 抑制FLC表达 | Yang et al., | |
| JMJ27 | 通过调控FLC染色质上的H3K9me2促进FLC表达 | Dutta et al., | |
| JMJ30与JMJ32 | JMJ30与JMJ32能够在高温下调节FLC位点的H3K27me3水平, 延缓H3K27me3介导的FLC抑制 | Bastow et al., | |
| PAF1复合物 | 具有RNA聚合酶II活性, 通过招募组蛋白甲基转移酶提高FLC染色质上H3K4和H3K36的甲基化水平, 从而促进FLC表达 | He et al., | |
| FRI | 通过上调FLC染色质H3K4三甲基化水平, 促进FLC表达 | He and Amasino, | |
| VIN3 | 通过参与FLC启动子区域组蛋白H3K9和H3K14的去乙酰化下调FLC表达 | Sung and Amasino, | |
| VIL1与VIL3 | 通过形成二聚体参与FLC的去乙酰化和甲基化, 进而抑制其表达 | Sung et al., | |
| FLD | 一个组蛋白乙酰化酶复合体, 对FLC组蛋白去乙酰化, 抑制FLC表达 | He et al., | |
| FVE | 对FLC染色质去乙酰化修饰, 抑制FLC表达 | Baek et al., | |
| HDA6 | 分别与FLD和HDA5互作, 形成复合物, 行使去乙酰化酶功能 | Cheng et al., | |
| HAM | 通过FLC及MAF3/MAF4染色质H4K5的乙酰化修饰抑制FLC表达 | Xiao et al., | |
| COOLAIR | 通过反义剪切调控FLC染色质上甲基化水平, 抑制FLC表达 | Csorba et al., | |
| 调控类型 | 调控因子 | 分子机制 | 参考文献 |
| 启动子结合 | SUF4 | 与FRI形成复合物后结合到FLC启动子, 抑制其表达 | Choi et al., |
| FLX与FLX4 | 与FRI形成复合物后结合到FLC启动子, 促进其表达 | Ding et al., | |
| PRC2复合物 | 通过其特异组分PHD抑制FLC转录起始蛋白与FLC启动子的结合, 引起FLC沉默 | Turck et al., | |
| TAF15b | 与FLC和COOLAIR的转录起始位点结合, 抑制FLC表达 | Eom et al., | |
| ABI4 | 与FLC的启动子CCAC基序结合, 促进FLC表达 | Shu et al., | |
| ABI5 | 与FLC启动子的ABRE/G-box (CACGTG)结合, 促进FLC的表达 | Xiong et al., | |
| 内含子及其它区域结合 | BIM | 结合到FLC的第1个内含子中的BR反应元件, 并招募去甲基化酶抑制H3K27三甲基化, 从而拮抗PRC2介导的FLC沉默 | Li et al., |
| BZR1 | 结合到FLC第1个内含子中的BR反应元件, 并招募去甲基化酶, 促进FLC表达 | Li et al., | |
| ASL | 其转录本结合到FLC的第1个内含子中, 影响其中关键位点的H3K27 me3水平 | Shin and Chekanova, | |
| JMJ28 | 靶向FLC的内含子区域和3′区域, 与FLC结合, 其是否通过调控FLC参与成花尚不确定 | Hung et al., | |
| mRNA结合 | FCA | 通过调控非编码RNA对邻近多聚腺苷化位点的选择, 从而在表观遗传学水平上调控FLC的表达 | Liu et al., |
| FY | 3′末端加工因子, 与FCA互作, 共同抑制FLC表达 | Simpson et al., | |
| GRP7与GRP8 | 富含甘氨酸的RNA结合蛋白, 二者都抑制FLC的表达, 具体分子机制有待阐明 | Wu et al., | |
| FPA | 具有RNA识别基序的RNA结合域, 参与FCA对RAN的修饰加工, 通过控制IncRNA的选择性聚腺苷化和FLC的3′端形成抑制FLC表达 | Cheng et al., | |
| 蛋白质稳定 | SIZ1 | 一个E3泛素连接酶, 能稳定FLC不被降解 | Son et al., |
表1 FLC基因表达的调控机制
Table1 Regulatory mechanism of FLC expression
| 调控类型 | 调控因子 | 分子机制 | 参考文献 |
|---|---|---|---|
| 染色质重塑 | EFS | 一个组蛋白甲基转移酶, 通过下调FLC染色质H3Lys 4三甲基化水平, 抑制FLC表达; 同时也能与FRI形成复合物, 通过甲基化修饰促进FLC表达 | Kim et al., |
| LHP1 | 通过介导PRC2向染色质招募组蛋白甲基转移酶促进FLC染色质的H3K27me3积累, 进而维持FLC沉默 | Zhou et al., | |
| ICU11 | 一个2-氧戊二酸依赖的双加氧酶, 与非特异性组蛋白去甲基化有关, 其功能缺失后破坏低温诱导的PRC2复合物介导的FLC沉默, 从而导致晚花 | Bloomer et al., | |
| VRN1与VRN2 | 分别通过提高FLC启动子和第1个内含子区域内H3K9me2和H3K27 me2的水平, 抑制FLC表达 | Sung and Amasino, | |
| SWP与CZS | 二者形成复合体, 通过调控FLC染色质的H3K9和H3K27甲基化和H4去乙酰化, 抑制FLC表达 | Jiang et al., | |
| REF6 | 一个H3K27去甲基化转移酶, 使FLC去甲基化而抑制FLC表达 | Lu et al., | |
| PRMT5 | 通过调控FLC染色质H4R3对称性双甲基化, 下调FLC表达 | 牛丽芳, | |
| JMJ18 | 一个组蛋白H3K4去甲基化酶, 通过与FLC结合, 降低H3K4甲基化水平, 抑制FLC表达 | Yang et al., | |
| JMJ27 | 通过调控FLC染色质上的H3K9me2促进FLC表达 | Dutta et al., | |
| JMJ30与JMJ32 | JMJ30与JMJ32能够在高温下调节FLC位点的H3K27me3水平, 延缓H3K27me3介导的FLC抑制 | Bastow et al., | |
| PAF1复合物 | 具有RNA聚合酶II活性, 通过招募组蛋白甲基转移酶提高FLC染色质上H3K4和H3K36的甲基化水平, 从而促进FLC表达 | He et al., | |
| FRI | 通过上调FLC染色质H3K4三甲基化水平, 促进FLC表达 | He and Amasino, | |
| VIN3 | 通过参与FLC启动子区域组蛋白H3K9和H3K14的去乙酰化下调FLC表达 | Sung and Amasino, | |
| VIL1与VIL3 | 通过形成二聚体参与FLC的去乙酰化和甲基化, 进而抑制其表达 | Sung et al., | |
| FLD | 一个组蛋白乙酰化酶复合体, 对FLC组蛋白去乙酰化, 抑制FLC表达 | He et al., | |
| FVE | 对FLC染色质去乙酰化修饰, 抑制FLC表达 | Baek et al., | |
| HDA6 | 分别与FLD和HDA5互作, 形成复合物, 行使去乙酰化酶功能 | Cheng et al., | |
| HAM | 通过FLC及MAF3/MAF4染色质H4K5的乙酰化修饰抑制FLC表达 | Xiao et al., | |
| COOLAIR | 通过反义剪切调控FLC染色质上甲基化水平, 抑制FLC表达 | Csorba et al., | |
| 调控类型 | 调控因子 | 分子机制 | 参考文献 |
| 启动子结合 | SUF4 | 与FRI形成复合物后结合到FLC启动子, 抑制其表达 | Choi et al., |
| FLX与FLX4 | 与FRI形成复合物后结合到FLC启动子, 促进其表达 | Ding et al., | |
| PRC2复合物 | 通过其特异组分PHD抑制FLC转录起始蛋白与FLC启动子的结合, 引起FLC沉默 | Turck et al., | |
| TAF15b | 与FLC和COOLAIR的转录起始位点结合, 抑制FLC表达 | Eom et al., | |
| ABI4 | 与FLC的启动子CCAC基序结合, 促进FLC表达 | Shu et al., | |
| ABI5 | 与FLC启动子的ABRE/G-box (CACGTG)结合, 促进FLC的表达 | Xiong et al., | |
| 内含子及其它区域结合 | BIM | 结合到FLC的第1个内含子中的BR反应元件, 并招募去甲基化酶抑制H3K27三甲基化, 从而拮抗PRC2介导的FLC沉默 | Li et al., |
| BZR1 | 结合到FLC第1个内含子中的BR反应元件, 并招募去甲基化酶, 促进FLC表达 | Li et al., | |
| ASL | 其转录本结合到FLC的第1个内含子中, 影响其中关键位点的H3K27 me3水平 | Shin and Chekanova, | |
| JMJ28 | 靶向FLC的内含子区域和3′区域, 与FLC结合, 其是否通过调控FLC参与成花尚不确定 | Hung et al., | |
| mRNA结合 | FCA | 通过调控非编码RNA对邻近多聚腺苷化位点的选择, 从而在表观遗传学水平上调控FLC的表达 | Liu et al., |
| FY | 3′末端加工因子, 与FCA互作, 共同抑制FLC表达 | Simpson et al., | |
| GRP7与GRP8 | 富含甘氨酸的RNA结合蛋白, 二者都抑制FLC的表达, 具体分子机制有待阐明 | Wu et al., | |
| FPA | 具有RNA识别基序的RNA结合域, 参与FCA对RAN的修饰加工, 通过控制IncRNA的选择性聚腺苷化和FLC的3′端形成抑制FLC表达 | Cheng et al., | |
| 蛋白质稳定 | SIZ1 | 一个E3泛素连接酶, 能稳定FLC不被降解 | Son et al., |
图1 FLC与成花调控网络 图中箭头表示促进, 钝线表示抑制。蓝色虚线表示有待研究。由于目前油菜素甾醇(BR)途径和脱落酸(ABA)途径证据较少, 故用虚线箭头表示。(1) 自主途径中, FVE、PDP和MSI5共同调控PRC2复合物, 抑制FLC表达; COOLAIR受FCA、FY和FPA影响, 同时, CstF64、CstF77和PRP8反义剪切产生的ASL维持FLC的甲基化修饰; FY与FCA互作, 在染色质水平上抑制FLC表达; FPA与FCA互作, 控制IncRNA的选择性聚腺苷化和FLC的3′端形成; FLD编码组蛋白乙酰化酶复合体, 抑制FLC表达; FVE下调FLC表达; FVE与FLD互作, 两者均参与组蛋白去乙酰化复合物, 但其机制尚不清楚; 组蛋白去乙酰化酶HDA5与HDA6互作, 两者均显示去乙酰化酶活性; HDA6与FLD互作, 这4种蛋白(FVE、FLD、HDA5和HDA6)可能形成蛋白复合物, 并通过组蛋白修饰相互作用, 抑制FLC表达; SWP1和CZS能形成SWP1/CZS复合体, 通过甲基化和去乙酰化调控FLC; REF6调控FLC的H3K27去甲基化; HAM参与FLC及MAF3/MAF4染色质H4K5的乙酰化修饰; HAC可能通过翻译后修饰FPA蛋白间接影响FLC表达; PRMT5介导FLC染色质H4R3对称性双甲基化,下调FLC表达; DA促进FLD、REF6和FVE的转录, 抑制FLC表达; GRP7的突变体中FLC表达上调并表现延迟开花, GRP8还能进一步晚花, 二者都能抑制FLC表达。(2) 年龄途径中, JMJ18直接抑制FLC的表达; SPL15作为FLC下游的靶标, FLC直接结合SPL15的启动子下调其表达。(3) 春化途径FRI复合物中的SUF4通过转录抑制FLC的表达, EFS能激活转录因子FLX和FLX4, 促进FLC的表达。(4) 光周期途径JMJ28和FBH共同调控CO, 促进FT表达, JMJ28与FLC结合, 但是否调控FLC表达还有待研究; JMJ27在光周期途径中通过抑制CO表达和促进FLC表达来参与成花调控。(5) 温度途径中, JMJ30/JMJ32在温暖条件下能够抑制FLC表达, 进而解除FLC对FT的抑制。(6) 赤霉素(GA)途径中, DEELA蛋白与FLC之间存在互作, DEELA蛋白中的RGA能直接促进FLC对SOC1的抑制; 同时SVP-FLC复合物也能抑制SOC1的表达。(7) BR通路中, BZR1能够与FLC内含子中的BR元件结合, 调控FLC表达, 同时BZR1和相互作用的MYC-like蛋白(BIM)与FLC第1个内含子中的BR反应元件结合, 对PRC2介导的FLC染色质沉默起拮抗作用。(8) ABA通路中, ABI4和ABI5既能通过启动子结合促进FLC表达, 也能共同作用促进FLC表达。
Figure 1 Schematic diagram of the FLC in flowering time regulation Arrows represent gene activation and blunted lines represent gene repression. The blue dotted line indicates the pathways that are not identified. The brassinosteroids (BR) pathway and abscisic acid (ABA) pathway are represented by dotted lines because there is less evidence. (1) Regulation of the PRC2 complex by FVE, PDP, and MSI5 in the autonomous pathway in repressing FLC; COOLAIR was affected by FCA, FY, FPA, while ASL generated by antisense splicing at Cstf64, Cstf77, and PRP8 maintained the methylation modification of FLC; FY interacts with FCA to repress FLC expression at the chromatin level; FPA interacts with FCA to control selective polyadenylation of IncRNA and 3′ end formation of FLC; FLD encodes a histone acetylase complex that represses FLC expression; FVE downregulates FLC expression; FVE interacts with FLD, both of which participate in the histone deacetylation complexes, which mechanism is currently unknown; the histone deacetylase HDA5 interacts with HDA6 and both display deacetylase activity; HDA6 interacts with FLD, and these 4 proteins (FVE, FLD, HDA5 and HDA6) may exist in protein complexes and repress FLC expression through histone modification interactions; SWP1 and CZS form the complex to regulate FLC through methylation and deacetylation; REF6 regulates H3K27 demethylation at FLC; HAM is involved in acetylation of H4K5 on chromatin at FLC and MAF3/MAF4; HAC may affect FLC expression indirectly through posttranslational modification of FPA proteins; PRMT5 mediates FLC chromatin H4R3 symmetric dimethylation, downregulating FLC expression; DA promoted the transcription of FLD, REF6 and FVE and inhibited FLC expression; in the mutants of GRP7, the expression of FLC was up-regulated and delayed flowering, and GRP8 could further late flowering, both of which could inhibit the expression of FLC. (2) The expression of FLC is directly inhibited by JMJ18 in the age pathway; SPL15 is a downstream target of FLC, FLC directly bind to the promoter of SPL15 to downregulate its expression. (3) SUF4 in the FRI complex of the vernalization pathway transcriptionally represses FLC expression, while EFS can activate the transcription factors FLX and FLX4 to promote FLC expression. (4) In the photoperiod pathway, JMJ28 and FBH jointly regulate CO, promote FT expression, and bind JMJ28 to FLC, but whether it regulates the expression of FLC remains to be investigated; JMJ27 functions in the photoperiod pathway to participate in the flowering regulation by repressing CO expression and promoting FLC expression. (5) JMJ30/JMJ32 in the temperature pathway is able to repress FLC expression under warm conditions and release the expression of FT. (6) An interaction between DEELA proteins and FLC was found in the gibberellins (GA) pathway, and RGA in DEELA proteins can directly promote the inhibition of SOC1 by FLC; at the same time, the SVP-FLC complex can also inhibit the expression of SOC1. (7) BZR1 in the BR pathway is able to bind BR elements in the FLC intron and regulate FLC expression. Meanwhile, BZR1 interacts with MYC-like protein (BIM) and binds to BR responsive elements in the first intron of FLC, which plays an antagonistic role in the PRC2-mediated silencing of FLC. (8) In the ABA pathway, ABI4 and ABI5 can not only promote the expression of FLC through promoter binding, but also promote the expression of FLC together.
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