Research progress on the genetic regulatory mechanism of flowering in Chrysanthemum
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摘要:
开花是植物发育过程中一个关键的质变过程,是植物从营养生长向生殖生长阶段的转变。对于观赏植物来说,开花的早晚决定了其市场应用和经济价值。植物开花受到内外信号的复杂调控,基于模式植物拟南芥(Arabidopsis thaliana (L.) Heynh)的研究,目前已经阐明了6条主要的开花调控途径,这些途径彼此独立又互相交叉,形成复杂的遗传调控网络。菊花(Chrysanthemum × morifolium Ramat)作为起源于中国的世界名花,是世界花卉市场的重要一员,但因其是典型的短日照植物,不仅增加了生产中开花期调控成本,也限制了菊花的应用范围。本文以高等植物开花遗传调控网络为基础,综述了菊花开花遗传调控机制的研究进展,以期为菊花开花时间改良育种工作提供理论指导,同时也为解析高等植物开花机制提供新见解。
Abstract:Flowering represents a critical transition in plant development, shifting from the vegetative to reproductive growth stages. In ornamental plants, the timing of flowering significantly impacts marketability and economic value. Plant flowering is regulated by complex internal and external signals. Studies on the model plant Arabidopsis thaliana have identified six primary pathways related to flowering regulation. These independent but intersecting pathways form a complex genetic regulatory network. Chrysanthemum × morifolium, a famous flower originating from China, holds a considerable share of the world flower market. However, its typical short-day flowering requirements not only increase production costs but also limit its application scope. Based on the flowering regulatory networks of higher plants, this review discusses current research progress on the genetic regulatory mechanisms underlying chrysanthemum flowering, thus providing theoretical guidance for the breeding and improvement of flowering time, as well as new insights into the flowering mechanisms of higher plants.
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Keywords:
- Chrysanthemum × morifolium /
- Flowering /
- Environmental factors /
- Genetic regulation
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在被子植物雄配子体发育过程中,源自体细胞的孢原细胞分化形成小孢子母细胞,其经历减数分裂形成由胼胝质壁包裹的四分体结构。随后在绒毡层细胞分泌的酶的作用下,胼胝质壁被降解,单核小孢子从四分体中游离至花药室内。游离小孢子的细胞核逐渐移至边缘紧贴细胞壁从而转变为极性小孢子。极性小孢子经过不均等的花粉第一次有丝分裂形成两个形态结构、生理功能高度分化的细胞:一个较大的营养细胞和一个较小的生殖细胞,二者具有截然不同的细胞命运。在随后的发育过程中,营养细胞不再进行细胞分裂,而生殖细胞则经历花粉第二次有丝分裂形成两个精细胞,生殖细胞与精细胞被统称为雄性生殖系细胞。因而,成熟的雄配子体为具有两种细胞系类型的三细胞结构[1, 2]。研究发现,细胞系特异性的表观遗传动态变化对于植物雄性生殖系细胞的发育以及雄性育性至关重要[3-7],包括编码各类甲基化酶/去甲基化酶在内的多种基因家族参与植物雄性生殖系细胞发育过程中的表观重编程[8-11]。近年来关于表观遗传调控植物雄性生殖系细胞发育的分子机理研究取得了诸多进展(表1),本文拟从染色质重塑、组蛋白翻译后修饰、DNA甲基化以及小RNA途径等4个方面对已取得的成果进行综述,并讨论如何进一步揭示与完善植物雄性生殖系细胞发育的表观遗传调控网络。
表 1 拟南芥精细胞与营养细胞的表观遗传修饰总结Table 1. Epigenetic modifications in sperm and vegetative cells of Arabidopsis thaliana类别
Category组蛋白变体
Histone variant类别
Category组蛋白修饰
Histone modification类别
CategoryDNA甲基化
DNA methylation营养细胞
VC精细胞
SC营养细胞
VC精细胞
SC营养细胞
VC精细胞
SCH1.1 – * H3K4me3 + + + + CG + + + + + H1.2 – * H3K9me2 – + + + CHG + + + + H2B.8 – * H3K27me3 + + + – CHH + + + + H3.3 * * H3K9ac + + + + H3.10 – * H3.14 * – cenH3 – * 注:VC,营养细胞;SC,精细胞;*,表示存在;–,表示不存在; + 、 + + 、 + + + ,分别表示营养细胞与精细胞之间的相对丰富度。组蛋白变体结果主要参考融合蛋白材料和免疫荧光实验数据;组蛋白修饰结果主要参考免疫荧光实验数据;DNA甲基化结果主要参考组学数据。 Notes: VC, vegetative cell; SC, sperm cell; *, indicates presence; –, indicates absence; + , + + , + + + , indicate relative abundance between vegetative and sperm cells. Histone variant results mainly refer to fusion protein plants and immunofluorescence assay data. Histone modification results mainly refer to immunofluorescence assay data. DNA methylation results mainly refer to -omics data. 1. 染色质重塑调控雄性生殖系细胞发育
被子植物雄配子体中,精细胞与营养细胞具有截然不同的染色质状态,前者染色质高度凝缩,而后者染色质则高度松散。然而,研究表明精细胞并非处于基因沉默的状态,包括精细胞特异基因在内的一系列基因仍进行着活跃的表达,从而形成精细胞所特有的转录组[9, 12, 13]。这暗示着雄配子体发育过程中,伴随着细胞命运决定,两个细胞系的染色质状态会发生相应的特异性变化,从而介导细胞系所需基因的表达。在真核生物中,DNA被组蛋白八聚体包裹,形成染色质的基本结构单位—核小体。组蛋白类型包括核心组蛋白H2A、H2B、H3、H4和连接组蛋白H1[14]。H1、H2A、H2B和H3这4类组蛋白包含大量修饰基因组特定区域的组蛋白变体,它们对维持染色质结构的多样性,实现有效的表观遗传调控至关重要[15]。植物雄配子体发育过程中,不同类型的组蛋白变体在雄性生殖系细胞和营养细胞间差异表达从而重编程两个细胞系的染色质状态与活力[16]。
拟南芥(Arabidopsis thaliana (L.) Heynh.)中存在3种H1蛋白,其中H1.1和H1.2在雄配子体发育过程中表达[17]。二者起初存在于早期小孢子中,但在后期小孢子中消失。在随后的营养细胞和雄性生殖系细胞发生过程中,H1.1和H1.2在雄性生殖系细胞中重新特异性地表达与维持,而在营养细胞中则不再表达[6, 17]。研究发现,营养细胞内的H1清除有助于DNA去甲基化酶DEMETER(DME)介导的DNA去甲基化过程,以及异染色质的解凝缩及其相关转座子的激活。若在营养细胞中异位表达H1.1,将减弱DNA的去甲基化和营养细胞特异转座子的激活,并最终导致花粉败育[17]。此外,百合( Lilium brownii var. viridulum Baker)营养细胞内的H1含量在雄配子体发育过程中也会逐渐减少,直至在成熟花粉时期近乎缺失,这表明营养细胞中H1的清除在不同的植物类群中可能是一个保守的发育事件,对营养细胞的发育及其功能至关重要[18]。
H2B.8在雄配子体内特异性地定位于精细胞核中,其缺失将导致精细胞染色质无法正常凝缩进而形成膨大的精细胞核,并影响花粉育性。此外,在体细胞中异位表达H2B.8可以促进体细胞核的凝缩[8]。这些结果说明H2B.8是精细胞染色质凝缩的关键因子,对于精细胞的功能行使至关重要。随后进一步的研究显示,有别于其他H2B变体的是,H2B.8在其氨基酸末端具有一个可以介导相分离的内在无序区(Intrinsically disordered region,IDR)[8, 19-22]。此外,H2B.8通常位于富含AT序列且转录不活跃的染色质区域。因此,H2B.8可以通过聚拢精细胞内不表达的染色质区域从而促进染色质的凝缩,同时却又不影响精细胞发育所需基因的表达。进化分析结果显示,H2B.8在开花植物中具有一定的保守性,因此H2B.8在不影响精细胞所需基因转录的同时介导精细胞染色质凝缩可能是开花植物中一个普适的机制[8]。
拟南芥小孢子染色质中的H3主要包括H3.1和H3.3两种变体。H3.1表现为DNA复制依赖性表达,主要在细胞周期S期形成;而H3.3则沉积在不依赖DNA复制的转录活性位点上[23-25]。在成熟花粉内,营养细胞染色质中的H3为H3.3和H3.14这两种类型的组蛋白变体,而H3.1完全消失[26]。与此同时,精细胞染色质中的H3则为H3.3和H3.10两种类型的组蛋白变体,H3.1也完全消失,这表明在雄性生殖系细胞发育过程中,小孢子分裂产生的子细胞内经历了一个特异性的染色质重塑过程,即H3.1在不同细胞系内被不同的H3变体所替换[27]。拟南芥通过富集雄性生殖系细胞特异性的组蛋白变体H3.10以实现精细胞染色质的重塑[23]。编码H3.10的基因HISTONE THREE RELATED 10(HTR10)受到雄性生殖系细胞特异性转录因子DUO POLLEN 1(DUO1)的直接调控。DUO1可与HTR10启动子区域的MYB binding sites(MBSs)结合,进而激活HTR10的表达[13]。同时,DUO1可直接激活转录因子DUO1-ACTIVATED ZINC FINGER PROTEIN 1(DAZ1)和DAZ2表达,而DAZ1可能与TOPLESS(TPL)相互作用从而形成一个针对DUO1的负调控通路[28]。因此,在雄性生殖系细胞发育过程中,DUO1-DAZ1/2调控网络是控制HTR10表达与H3.10积累的关键。另一方面,在水稻(Oryza sativa L.)中,HTR10的同源基因HTR709可能通过编码H3的变体H3.709以实现雄性生殖系细胞染色质的重塑[29, 30]。H3变体cenH3对减数分裂和有丝分裂过程中着丝粒的组装至关重要[31, 32]。在雄配子体中,cenH3特异性地存在于精细胞中,其缺失虽然不影响精细胞的受精功能,却会导致父本基因组在随后的胚胎发育过程中丢失,从而诱导单倍体的产生[33, 34]。因此,研究H3变体对于雄性生殖系细胞发育的作用,对于揭示单倍体诱导机理以及作物育种具有重要意义。
2. 组蛋白翻译后修饰调控雄性生殖系细胞发育
组蛋白翻译后修饰是指核心组蛋白氨基末端的翻译后共价修饰,其作为组蛋白密码构成了一种重要的表观遗传机制。组蛋白修饰主要包括甲基化、乙酰化、泛素化、苏素化和磷酸化等,其中甲基化不仅发生在不同位点的不同残基(赖氨酸K和精氨酸R)上,且添加的甲基基团数量也不同[35]。组蛋白甲基化的动态调控是通过组蛋白甲基化酶和组蛋白去甲基化酶介导的酶促反应实现的[14, 35]。植物组蛋白赖氨酸甲基化主要发生在H3的4、9、27和36位点上,其在基因转录的激活和抑制方面发挥着重要作用,是组蛋白修饰的重点研究方向。目前通常认为,H3K9和H3K27的甲基化抑制基因表达,反之,H3K4和H3K36的甲基化则激活基因表达[14]。此外,组蛋白乙酰化参与转录激活,在植物发育过程中同样发挥着重要作用[14, 36]。
基于百合、大麦(Hordeum vulgare L.)和黑麦(Secale cereale L.)雄配子体的研究显示,雄性生殖系细胞内的H3K4me2水平均高于营养细胞;百合和黑麦雄性生殖系细胞内的H3K9me2水平高于营养细胞,而大麦中这种差异并不显著;H3K27me3特异性地存在于百合和大麦的营养细胞中,然而在黑麦中表现为营养细胞中的优势累积[3, 5, 26, 37, 38]。这些结果表明,雄配子体内两个细胞系之间存在着差异的组蛋白甲基化修饰状态,并且这种差异状态在不同植物之间具有一定的保守性。随后,基于拟南芥雄配子体的研究进一步揭示,两个细胞系之间差异的组蛋白甲基化修饰对于营养细胞和精细胞的发生与命运决定具有重要作用。
拟南芥雄配子体发育过程中,小孢子分裂产生的子细胞经历了特定的组蛋白修饰重编程,致使最终营养细胞与精细胞具有截然不同的组蛋白甲基化状态。H3K9me2和H3K27me3分别特异性地存在于精细胞和营养细胞中,与此同时,H3K4me3在两个细胞系中均存在,但优势累积于精细胞中[9, 26, 39, 40]。拟南芥SET DOMAIN GROUP 2(SDG2)编码一种含有SET结构域的组蛋白甲基转移酶,其可催化H3K4的甲基化。在sdg2突变体花粉中,H3K4me3的水平显著降低,同时H3K9me2异位地出现在营养细胞中。这种异常的组蛋白甲基化状态导致营养细胞的染色质凝缩,且部分生殖细胞无法进行第二次花粉有丝分裂以形成两个精细胞。这些结果表明H3K4甲基化能够促进拟南芥雄配子体由二细胞阶段向三细胞阶段转变,因而对雄性生殖系细胞的发育至关重要[41]。然而值得注意的是,SDG2缺失导致的H3K4me3和H3K9me2异常状态影响花粉内营养细胞和雄性生殖系细胞的发育,但并不改变二者的细胞命运[41]。植物生殖系细胞源自花器官内的体细胞,在雄配子发生过程中,雄性生殖系细胞内体细胞的H3K27me3修饰位点经历了广泛的重编程[27, 42]。在精细胞形成过程中H3.10置换了原先的H3.1,该H3变体的K27周围特定的氨基酸残基可以阻止由PRC2(Polycomb group repressor complex 2)复合体所催化的H3K27me3的形成,从而导致精细胞染色质中H3K27me3逐步减少以实现父本染色质的重编程[23, 27, 43]。与此同时,营养细胞则保留了小孢子原有的H3K27me3状态[9, 27]。在营养细胞中异位表达H3K27去甲基化酶RELATIVE OF ELF 6(REF6)可有效地清除营养细胞内的H3K27me3。缺失H3K27me3的营养细胞由于无法萌发花粉管从而导致其传递精细胞的功能丧失,同时,其细胞核中可以异位地观察到HTR10-RFP、DUO1-RFP和H3K9me2等雄性生殖系细胞特异的分子标记。借由多组学分析以及超微结构分析,进一步揭示了H3K27me3擦除导致营养细胞的命运向精细胞命运发生了转变。因此,这些工作以多维度详实的实验手段证明了组蛋白修饰参与调控雄性生殖系的细胞命运决定,H3K27me3有助于维持营养细胞命运,而其擦除则激活雄性生殖系细胞命运[9]。
相较于组蛋白甲基化而言,关于被子植物中组蛋白乙酰化调控雄性生殖系细胞发育的研究较少。研究表明,H3K9ac在开花植物的雄性生殖系细胞和营养细胞中均存在,但不同植物之间存在一定的差异。在拟南芥和黑麦的雄配子体中,H3K9ac在雄性生殖系细胞中的水平明显高于营养细胞;而大麦和百合的雄性生殖系细胞与营养细胞中的H3K9ac水平则相差无几[3, 5, 40]。在拟南芥雄配子体发育过程中, ARID1(AT-Rich interacting domain-containing protein 1)可以与雄性生殖系细胞特异性基因DUO1的启动子结合,促进DUO1的表达。当arid1突变时,伴随着DUO1位点的H3K9ac水平的明显降低,花粉内DUO1的表达量减少,这暗示ARID1在雄性生殖系发育过程中可能通过介导组蛋白乙酰化调控雄性生殖系细胞发育[44]。此外,关于组蛋白乙酰化对雄性生殖系细胞发育的研究在苔藓植物中也有所报道。染色质重塑复合体(Chromatin-remodeling complexes,CRCs)是转录调控通路的关键枢纽,可以参与基因的激活或抑制[45, 46]。SWI3A/B是SWITCH/SUCROSE NONFERMENTING (SWI/SNF) CRC的重要组成部分,研究发现SWI3A/B参与调控小立碗藓(Physcomitrium patens (Hedw.) Mitt.)的精细胞成熟,其功能丧失会导致雄性不育[45, 47]。在分子水平上,SWI/SNF复合物可调节H3K27乙酰化,其与PRC2的功能相拮抗,从而抑制H3K27me3的产生从而促进相关基因的表达[48-50]。因此,组蛋白乙酰化对于种子植物与非种子植物的雄性生殖系细胞发育均具有广泛而重要的作用。
3. DNA甲基化调控雄性生殖系细胞发育
DNA甲基化通常是指在胞嘧啶的5号碳位共价键结合一个甲基基团,从而形成5-甲基胞嘧啶(5-mC),其为一种普遍的DNA修饰,在真核生物基因组中起着重要的调控作用[51-53]。哺乳动物中DNA甲基化主要发生在CG二核苷酸序列,而植物中DNA甲基化可发生在CG、CHG和CHH(H代表A,T或C)3种序列中[54]。特定位点的DNA甲基化状态是在多种DNA甲基化酶/去甲基化酶的参与下所进行的DNA甲基化建立、维持以及擦除等过程动态调控的结果。拟南芥DNA甲基化酶DOMAINS REARRANGED METHYLTRANSFERASE1(DRM1)和DRM2通过small RNA-directed DNA methylation pathway(RdDM)在3种序列中从头合成DNA甲基化[54]。RdDM由形成small interfering RNAs(siRNAs)的RNA聚合酶Ⅳ(RNA Pol Ⅳ)通路和负责DNA甲基化的RNA 聚合酶Ⅴ(RNA Pol Ⅴ)通路构成。在Pol Ⅳ通路中,由RNA Pol Ⅳ产生转录本通过RNA-dependent RNA polymerase 2(RDR2)转化为双链,随后被Dicer-like 3(DCL3)切割成24 nt siRNAs[55, 56]。在Pol Ⅴ通路中,siRNAs被装载至含有ARGONAUTE(AGO)的复合物中,该复合物与RNA Pol Ⅴ产生的转录本结合,并招募DRMs[56]。DNA甲基转移酶MET1通过在DNA复制过程中甲基化半甲基化状态的CG位点从而维持CG甲基化,而非CG位点的甲基化则可以通过DRM1和DRM2来维持[54]。植物转座子中的CHH和CHG位点也可以被两种植物所特有的DNA甲基转移酶CHROMOMETHYLASE2(CMT2)(CHH)和CMT3(CHG)所甲基化[57-59]。CMTs优先结合异染色质上由组蛋白甲基转移酶SU(var)3-9 homologue 4/5/6(SUVH4/5/6)所形成的H3K9me2,以催化该位置的非CG甲基化;同时,甲基化后的DNA序列可反向促进SUVH4/5/6介导的H3K9me2形成,进而产生一个自我强化的反馈环[60-66]。另一方面,DNA甲基化的清除可以通过两种方式实现,即DNA复制过程中的维持失败,以及DNA糖基化酶REPRESSOR OF SILENCING 1(ROS1)、DME、DEMETER-LIKE PROTEIN 2 (DML2)和DML3所介导的主动DNA去甲基化[67-72]。
DNA甲基化模式在体细胞分裂过程中被准确地复制,然而在生殖系细胞形成过程中则会经历必要的重编程过程[7, 52, 73-75]。哺乳动物生殖系细胞在胚胎中形成之后会发生一个全基因组范围的DNA去甲基化和重建甲基化的过程,从而重置表观遗传信息[74, 76]。与动物在胚胎发生中形成生殖系不同,植物的生殖系分化自体细胞,其并不经历胚胎发育过程中的全基因组范围内的DNA甲基化擦除与重建,取而代之的是在生殖系分化时的动态DNA甲基化过程[77, 78]。
雄性生殖系细胞的CG甲基化程度高于体细胞和营养细胞,目前尚不清楚雄性生殖系细胞内CG甲基化呈现此种状态的具体机制。花粉相较于体细胞而言,在具有较低的H1表达水平的同时却具有较高的CG甲基化水平,因此,H1的缺乏可能有助于CG甲基化的增强[6]。进一步而言,花粉中MET1可能在雄性生殖系细胞DNA复制过程中维持其CG甲基化[6, 7]。然而,营养细胞虽然不具备精细胞所具有的H1.1和H1.2,但其CG甲基化程度却低于精细胞,这可能是由于营养细胞中CG甲基化位点的DNA去甲基化更为活跃所造成的[6, 79]。针对营养细胞内221个低甲基化CG位点的研究表明,这些位点大多是DNA去甲基化酶的结合位点;而雄配子体中ROS1、DME、DML2、DML3等均仅在营养细胞中表达,因此营养细胞内CG甲基化的缺失可能是由于DNA去甲基化酶的作用所导致,这也为精细胞可以维持比营养细胞更高水平的CG甲基化提供了一个可能的解释[4]。
CHG甲基化水平在小孢子、雄性生殖系细胞与营养细胞之间具有相类似的程度[6, 7]。而在小孢子发生过程中,CHH甲基化程度由小孢子母细胞至小孢子呈现渐增的趋势。随着营养细胞和精细胞的产生,CHH甲基化在精细胞中基本维持了小孢子的水平,反之,在营养细胞中则持续增强[7]。CHH甲基化可通过DRM2或者CMT2维持[59, 80]。RdDM在小孢子母细胞、小孢子、营养细胞和精细胞中可以促进一类称为MetGenes的特异性位点的CHH甲基化[7, 81]。在drm1 drm2和rdr2等突变体的小孢子母细胞中MetGenes的CHH基本无法甲基化,这表明RdDM在雄配子体发育过程中对于CHH甲基化的持续增强至关重要[7]。另一方面,CMT2的缺失会导致CHH甲基化程度降低[6]。因此,小孢子不对称分裂后,雄配子体内雄性生殖系细胞的CHH甲基化程度低于营养细胞的情况可能是由于前者相较于后者而言具有较低的CMT2活性[7, 81]。
4. 小RNA途径调控雄性生殖系细胞发育
植物基因组中存在大量非编码RNA,其中在表观遗传调控方面发挥重要作用的小RNA(small RNA)根据生物发生和作用方式可分为两类,即microRNAs(miRNAs)和siRNAs[82, 83]。现已知包括RDR、DCL和AGO等在内的基因家族在小RNA途径中发挥关键作用[12, 84-86]。在拟南芥中,miRNA基因由RNA Pol Ⅱ转录为初始miRNAs,其经DCL1切割形成成熟miRNAs后与AGO1结合以介导mRNA的切割或者翻译抑制[87]。而siRNAs则是以DNA重复序列和TEs(Transposable elements)为模板,主要通过RdDM途径形成,从而用于DNA甲基化的维持[88]。动植物均趋同地产生护卫细胞以滋养发育中的生殖系细胞[89]。在被子植物中,绒毡层细胞可以滋养小孢子母细胞,而营养细胞可以滋养生殖细胞与精细胞,这些护卫细胞对于雄性生殖系细胞的发育至关重要[1, 89, 90]。例如,雄性生殖系细胞所需的siRNAs并非完全通过自身的RdDM途径产生,护卫细胞来源的siRNAs同样参与调控雄性生殖系细胞发育[10, 91]。
雄配子体发育过程中,MetGenes的重新甲基化可以调控小孢子母细胞中的基因表达,这些基因中就包括促进减数分裂的关键基因MULTIPOLAR SPINDLE 1(MPS1),其可以确保减数分裂的顺利完成,从而保障雄性生殖系细胞的形成[7]。同一时期,小孢子母细胞中siRNAs的形成可能会导致RNA Pol Ⅳ通路被抑制,使得TE有被重激活的风险,而生命周期较短的绒毡层细胞就成为了形成siRNAs的良好选择[81]。首先,RdDM途径具有自我强化性质,然而小孢子母细胞内却不具备与MetGenes完美匹配的24 nt siRNAs,这表明siRNAs的生物发生并非在小孢子母细胞中进行。其次,小孢子母细胞被绒毡层细胞所包围,二者在减数分裂早期阶段通过胞间连丝相连通。研究发现,绒毡层细胞具有与小孢子母细胞相类似的siRNA谱,提示调控小孢子母细胞发育所需的24 nt siRNAs可能源自绒毡层[10, 92, 93]。rdr2突变体中,小孢子母细胞和精细胞中MetGenes的甲基化缺失。将绒毡层特异性启动子pA9驱动RDR2(pA9::RDR2载体)转入rdr2突变体后可以恢复MetGenes的正常甲基化水平,这表明来源于绒毡层的siRNAs不仅可以介导小孢子母细胞的DNA甲基化,还可以介导雄性生殖系细胞的DNA甲基化[10]。值得注意的是,花粉壁会阻碍siRNAs在花粉和绒毡层之间的直接转运,因此绒毡层产生的siRNAs最有可能通过小孢子母细胞转移至雄性生殖系细胞并影响其发育[79, 90, 91]。CLASSY(CLSY)1-4在不同细胞中具有不同的表达模式,CLSY1和CLSY2主要在体细胞中表达,CLSY3特异在雄性和雌性生殖器官中表达,CLSY4则主要在小孢子母细胞中表达。这些CLSYs通过募集RNA Pol Ⅳ促使在不同基因组位点上产生siRNAs[10, 94-96]。具体而言,CLSY3特异性地存在于花药的绒毡层中,其负责与小孢子母细胞中MetGenes甲基化相关的siRNAs的形成,它的缺失会消除小孢子母细胞以及随后产生的精细胞中的MetGene甲基化,这进一步表明小孢子母细胞中绝大多数的24 nt siRNAs来源于绒毡层[10]。
与拟南芥在减数分裂前期的绒毡层中积累24 nt siRNAs相类似,单子叶植物积累24 nt phased siRNAs(phasiRNAs)并可能借此调控雄性生殖系细胞的DNA甲基化重编程[97-101]。虽然玉米(Zea mays L.)和水稻等单子叶植物的phasiRNAs形成过程与拟南芥中siRNAs的合成过程并不相同,即phasiRNAs是由RNA Pol Ⅱ转录,DCL5加工所形成[101-104];然而,现有研究表明二者之间存在相似之处。通常认为phasiRNAs也是在绒毡层中形成后转运至小孢子母细胞中发挥作用[100, 105-107]。
在拟南芥营养细胞异染色质的程序性去凝缩过程中,数百个TEs(主要为逆转录转座子)被重激活并由RNA Pol Ⅱ转录[91, 108, 109]。首先,这是由于雄配子体内营养细胞特异表达的DNA去甲基化酶DME可以通过TEs的DNA去甲基化将其激活[4, 110]。然而,小孢子在花粉第一次有丝分裂前特异性地清除H1则可能有助于营养细胞中TEs,尤其是异染色质TEs的DNA去甲基化[17]。TEs在营养细胞中转录后,其mRNAs将被AGO1切割,随后RDR6以断裂产物为模板合成双链RNAs(dsRNAs),并最终通过DCL4加工形成21-22 nt easiRNAs(表观遗传激活的siRNAs)。dcl1、ago1、rdr6、dcl4突变体中较少的easiRNAs含量进一步证实了DCL1–AGO1–RDR6–DCL4途径参与调控easiRNAs的形成[109]。值得注意的是,虽然TEs重激活发生在营养细胞中,但是精细胞内也可检测到easiRNAs的存在[91]。随后的工作显示,人为地在营养细胞中特异性地生成easiRNAs能够有效地抑制相应基因在精细胞中的表达,这进一步证实了在雄性生殖系细胞发育过程中easiRNAs可能会通过某种细胞间通讯方式从营养细胞转移至精细胞以增强精细胞中TE的甲基化,从而达到沉默精细胞中TE序列的目的[91, 111]。那么,easiRNAs的转移发生在雄配子体发育的哪一阶段呢?现有研究推测营养细胞可能在花粉第一次有丝分裂(PMI)后染色质快速去凝缩的同时迅速加工生成easiRNAs,而这些生成的easiRNAs可能在花粉第二次有丝分裂(PMⅡ)前转移至生殖细胞并被最终分配至两个精细胞[83]。因此,植物雄配子体可能通过牺牲营养细胞基因组的稳定性而使雄性生殖系细胞基因组的稳定性得到保障。
植物精细胞富集的miRNAs在雄性生殖系细胞发育中的具体调控作用仍有待探索,但miR159的出现为这一领域的研究提供了重要的切入点[112]。研究发现,miR159可能参与调控包括DUO1在内的多种MYB转录因子家族基因的转录本[113]。miR159的缺失并不会影响花粉发育以及受精,这表明在雄配子体中miR159所介导的基因表达的转录后调控并非雄性生殖系细胞发生所必需[114]。然而,进一步的研究表明精细胞所携带的父本来源的miR159在进入中央细胞后能够抑制其MYB33和MYB65的功能,从而启动初生胚乳核分裂。因此,雄性生殖系细胞传递的miRNA对于胚乳中母本来源的细胞分裂抑制因子的清除以及种子发育至关重要[11]。
5. 展望
近年来,受益于细胞分离技术的进步以及测序技术的不断突破,有关植物雄性生殖系细胞发育的表观遗传调控机理研究取得了长足进展。一系列工作揭示了组蛋白变体对于雄性生殖系细胞的染色质重塑至关重要;组蛋白甲基化修饰在雄配子体内细胞命运决定中的关键调控作用;雄配子体发育过程中DNA甲基化在包括雄性生殖系在内的不同细胞系中的动态变化过程;以及源自绒毡层细胞和营养细胞等护卫细胞的siRNAs对于雄性生殖系细胞发育的重要性等。然而,仍有许多重要的科学问题亟待解决。不同的组蛋白变体如何协同调控雄性生殖系细胞的染色质重塑?雄性生殖系细胞命运决定的完整表观遗传调控网络是什么?siRNA具体在哪一发育阶段、通过何种路径实现在护卫细胞与雄性生殖系细胞之间的有效通讯?这些核心问题的深入研究将助力我们描绘植物雄性生殖系细胞发育的表观遗传调控全景,为其将来在实际农业生产与分子育种中的可能应用夯实理论基础。
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图 1 拟南芥中以光周期途径为主的开花途径和菊花中响应光周期的同源基因
红线代表在菊花中涉及的研究(参考网站:https://www.wikipathways.org/index.php/Pathway:WP622)。
Figure 1. Flowering pathway dominated by photoperiodic pathway in Arabidopsis thaliana and photoperiod-responsive homologous genes in Chrysanthemum
Red line represents research involving Chrysanthemum (Photoperiodic pathway available online: https://www.wikipathways.org/index.php/Pathway: WP2312).
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