Advances in epigenetic regulation of plant male germline cell development
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摘要:
植物雄性生殖系细胞在发育过程中需经历染色质重塑、组蛋白修饰、DNA甲基化以及小RNA等途径所介导的表观遗传重编程。现已发现诸多基因参与塑造雄性生殖系细胞的表观遗传状态，并调控植物雄性育性。此外，随着各类组学技术的不断进步，一系列关于雄性生殖系细胞在不同发育阶段的特定表观遗传信息被揭示。本文简要梳理了近年来植物雄性生殖系细胞发育过程中表观遗传动态及其所涉及的分子机理的研究进展，并对表观遗传调控植物雄性生殖系细胞发育的后续研究进行了展望。
Abstract:Male germline cells in plants undergo epigenetic reprogramming mediated by chromatin remodeling, histone modification, DNA methylation, and small RNA during development. Many genes are involved in shaping the epigenetic state of male germline cells and regulating plant male fertility. Recent advances in multi-omics techniques have helped elucidate specific epigenetic profiles of male germline cells at different stages of development. In this review, we summarize recent advances in epigenetic dynamics and molecular mechanisms involved in the development of male germline cells in plants and discuss prospects for future studies on the epigenetic regulation of this developmental process.
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花色苷（Anthocyanin），又称花色素苷，是普遍存在于自然界中的一类天然水溶性色素，广泛分布于高等植物各种组织和器官中，如种子、叶、花和果实等，赋予其丰富的色彩。花色苷在结构上由花色素（Anthocyanidin）通过糖苷键与同一个或多个糖基团（阿拉伯糖、葡萄糖、鼠李糖、半乳糖、木糖等）结合形成。在自然环境下，游离状态的花色素极不稳定，糖基化后可转化为稳定的花色苷存在于植物体内[1]。目前自然界中已知的花色素约20余种，以矢车菊花色素、矮牵牛花色素、芍药花色素、飞燕草花色素、锦葵花色素和天竺葵花色素最为常见，其中，矢车菊花色素（花青素）与葡萄糖形成的矢车菊花色素3’-O-葡萄糖苷（即花青苷）为植物界分布最广泛的花色苷[2]。
花色苷作为植物体内重要的次生代谢产物，在植物繁衍、响应生物和非生物逆境中具有重要的生物学功能[3]，如防御病菌感染、抵御低温和干旱等外界环境胁迫[4]。在人体健康方面，具有改善血糖平衡、降低血脂和预防心血管疾病等功能[5]，近年来已经开展了许多花色苷的人类营养学和生物活性研究[6]。研究发现，花色苷可与MAPK和Akt信号传导相互作用，防止细胞凋亡[7]；抑制皮肤表皮中环氧合酶2的表达，降低促炎细胞因子的产生[8]；有效预防紫外辐射在哺乳动物皮肤中引发的炎症和癌变[9]。在健康饮食的大背景下，花色苷以其安全性高、天然、几乎无毒副作用、具有潜在医疗价值和营养价值的特点，成为果品健康品质的重要标志之一。因此，研究花色苷积累机制对于改善果实外观品质、提高营养保健价值具有重要意义。
随着花色苷在果实品质和营养保健中的重要性逐渐被认可，有关果实花色苷合成、转运积累及其调控方面的研究受到了广泛关注。目前，植物花色苷生物合成途径已十分清晰，且在不同物种中高度保守。花色苷是类黄酮途径的终产物，由位于内质网膜上的一系列酶催化合成，主要包括查尔酮合成酶（Chalcone synthase，CHS）、查尔酮异构酶（Chalcone isomerase，CHI）、黄烷酮3-羟化酶（Flavanone 3-hydroxylase，F3H）、类黄酮3’-羟化酶（Flavonoid 3’-hydroxylase，F3’H）、类黄酮3’5’-羟化酶（Flavonoid 3’, 5’-hydroxylase，F3’5’H）、二氢黄酮醇4-还原酶（Dihydroflavonol 4-reductase，DFR）、花色素合成酶（Anthocyanidin synthase，ANS）和UDP葡萄糖-类黄酮3-O-葡糖基转移酶（UDP-glucose: flavonoid 3-O-glucosyltransferase，UFGT）[2,10]。花色苷合成相关的结构基因受转录水平上的调控。MYB转录因子是最先被证实参与花色苷合成调控的关键基因，它与bHLH和WD40转录因子形成MBW复合体，协同调控结构基因的转录[11-13]。
1. 花色苷转运模型
花色苷在细胞内质网膜上合成后稳定地储存于液泡中，这一过程依赖于植物体内高效的转运机制[14]。花色苷转运至液泡中储存对植物自身而言有着重要的生物学意义[15]，低pH值的液泡条件是花色苷呈现鲜艳色彩的必要先决条件，此外，花色苷作为活性代谢物，液泡隔离可有效减少细胞损伤。花色苷转运过程极大程度地影响其积累，然而其胞内运输机制仍不清晰。目前，关于花色苷转运有3类主要模型，分别为谷胱甘肽S-转移酶（Glutathione S-transferases，GST）、膜转运蛋白（Membrane transporters）以及囊泡运输（Vesicle trafficking）介导的转运（图1）[16-18]。
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花色苷主要通过GST、膜转运蛋白（ABC、MATE、BTL-homologue等）以及自噬作用、内质网和高尔基体的囊泡运输系统转运至液泡。ABC：ATP-结合框；BTL-homologue：胆红素易位酶同族体；GST：谷胱甘肽S-转移酶；MATE：多药和毒性化合物外排。Anthocyanins are primarily transported to the vacuole by GST, membrane transporters (e.g., ABC, MATE, BTL-homologue), and vesicle transport system of autophagy, endoplasmic reticulum, and Golgi apparatus. ABC: ATP-binding cassette; BTL-homologue: Bilitranslocase-homologue; GST: Glutathione S-transferase; MATE: Multidrug and toxic compound extrusion.1.1 GST介导的花色苷转运机制
谷胱甘肽S-转移酶，即谷胱甘肽转移酶，是一类广泛存在于生物体中的酶类，可催化还原型谷胱甘肽与代谢产物上电子亲和度较高的官能团发生结合反应，形成较为稳定的结构，从而起到解毒和代谢作用[19]。GST对于维持细胞内外环境平衡、促进化学物质代谢和区域性隔离具有重要的生理意义。此外，GST也可作为非酶配体蛋白发挥其功能。在高等植物中，GST为一类具有多成员的超家族，包括Phi、TAU、THETA、ZETA、LAMBDA、DHAR和TCHQD等7个亚家族。由于各亚家族成员在底物特异性和转运靶向上存在差异，使其在植物体内具有丰富的功能，如参与类黄酮代谢及生物和非生物胁迫响应等[20-22]。
花色苷被认为是GST关键内源底物之一[23]。大量GST突变体，如玉米（Zea mays L.）bz2（Bronze 2）[24]、矮牵牛（Petunia hybrida (Hook.) E. Vilm.）an9（Anthocyanin 9）[25, 26]、康乃馨（Dianthus caryophyllus L.）fl3（Flavonoids 3）[27]和拟南芥（Arabidopsis thaliana (L.) Heynh.）tt19（Transparent testa 19）[28]等，均呈现出花色苷含量显著降低的表型，说明GST在花色苷积累中有着至关重要的作用。参与花色苷转运的GSTs主要来源于Phi亚家族，已在紫苏（Perilla frutescens (L.) Britt.）[29]、仙客来（Cyclamen persicum Mill.）[30]、茶（Camellia sinensis (L.) Kuntze）[31]和菊花（Chrysanthemum morifolium Ramat.）[32]等多种植物中相继被分离与鉴定。曾有人提出GST通过其酶活性介导花色苷转运过程的假说[33]，但目前仍未发现关于GST催化亲核性的谷胱甘肽与花色苷发生反应的直接证据。近年来的研究表明，GST在花色苷转运过程中可能仅扮演着运输媒介，通过直接与花色苷物理结合形成谷胱甘肽交联复合物，促进它们从细胞质向液泡传递[26, 34]。
果树中参与花色苷转运的GST基因及其相应的转录调控机制逐渐被揭示。LcGST4参与了荔枝（Litchi chinensis Sonn.）的花色苷积累，并响应外界光照和ABA的调控[35]。苹果（Malus × domestica Borkh.）果实发育过程中MdGSTF6的表达水平与花色苷含量呈显著正相关[36]。类似的研究在中华猕猴桃（Actinidia chinensis Planch.）、梨（Pyrus pyrifolia (Burm. f.) Nakai）和杨梅（Morella rubra Lour.）中也有报道[37-39]。除果实着色外，GST也参与了其他器官中花色苷的积累。草莓（Fragaria × ananassa Duch.）RAP编码的谷胱甘肽转移酶蛋白，在叶片和茎段着色中起关键作用[40, 41]。PpGST1先后被发现与桃（Prunus persica (L.) Batsch）花色形成和果实着色密切相关，参与花色苷从内质网膜上转出的过程[42, 43]。GST在不同物种中存在功能分化，一些GST具有较强的底物特异性，只特定参与花色苷积累，而有些GST除了介导花色苷转运外，还参与其他次生代谢物的转运[44]。例如，葡萄（Vitis vinifera L.）中VviGST3特异性介导原花青素的积累，而VviGST4同时参与花色苷和原花青素的转运[45]。在多种植物中均发现，花色苷生物合成过程中关键MYB转录因子可通过调控GST的表达水平参与花色苷转运，从而影响其花色苷的积累[46, 47]。上述研究为GST介导花色苷的积累提供了重要生物学证据，但关于其作为配体蛋白参与花色苷转运的作用机制，以及花色苷与GST结合后如何跨膜运输转至液泡内的分子机制尚不清晰。此外，除已报道的参与花色苷转运的主要GST成员，是否存在其他功能冗余的GST成员？参与花色苷转运的GST基因是否具备转运其他类黄酮物质的功能？GST对不同花色苷单体是否表现出底物特异性和转运活性差异？这些问题仍有待解决。相关研究的深入开展将有助于更加全面地了解GST在植物花色苷转运中的作用。
1.2 膜转运蛋白介导的花色苷转运机制
越来越多的遗传、生物化学和分子生物学证据表明，ATP-结合框（ATP-binding cassette，ABC）及多药和毒性化合物外排（Multidrug and toxic compound extrusion，MATE）两类膜转运蛋白参与花色苷的跨膜转运过程[48]。
1.2.1 MRP型ABC转运蛋白
ABC是一类广泛存在于真核生物和原核生物中的转运蛋白，可通过ATP水解产生的能量来驱动底物跨膜运输，是目前已知数量和功能最丰富的一类家族。ABC蛋白通过转运不同底物而参与植物体的一系列生理过程，如次生代谢产物与激素转运、脂质代谢、重金属解毒和器官形成与发育等。
植物体内ABC转运蛋白包含8大亚家族（ABCA-ABCG和ABCI），其中ABCC亚家族即多药耐药相关蛋白（Multidrug resistance-associated protein，MRP）被证实在花色苷跨膜转运中发挥重要作用，相关工作在拟南芥、水稻（Oryza sativa L.）、玉米、葡萄及桃中均已有报道。拟南芥AtMRP1和AtMRP2与有毒异源和内源性物质（如除草剂和花色苷）的含量密切相关[49, 50]。玉米ZmMRP3定位于液泡膜，其表达水平与花色苷合成基因具有一定的相关性，敲除ZmMRP3后的突变体与bz2有着相似的表型，呈现花色苷转运至液泡过程受阻而保留在细胞质中的现象，但该突变体糊粉层组织表型未受到影响。ZmMrp3同源基因ZmMrp4可能在糊粉层花色苷的积累中起到了关键作用[51]。在不同品种桃果实中，PpABCC1的转录水平与花色苷含量显著正相关，过表达PpABCC1可促进果肉和果皮着色[52]。ABCC以花色苷单体为特异转运底物仅在葡萄和拟南芥中有直接的证据：体外转运实验表明，VvABCC1靶向转运葡萄中锦葵色素3’-O-葡萄糖苷，且这一过程依赖谷胱甘肽[53]；拟南芥中AtABCC2特异参与矢车菊花色素3’-O-葡萄糖苷的积累[54]。
1.2.2 MATE转运蛋白
MATE是广泛存在于各种生物体中的一种跨膜转运蛋白，其作用机制是以膜两侧质子浓度梯度作为驱动力介导底物的跨膜转运[55]。MATE转运蛋白通过识别并结合不同大小、结构和化学性质的底物，选择性地对其进行跨膜运输。MATE蛋白在植物中执行着相对保守、基础的转运功能，在拟南芥和葡萄中已有报道其介导花色苷的积累。TT12（TRANSPARENT TESTA 12）编码的MATE转运蛋白定位于液泡膜上，作为质子逆向转运蛋白，调节拟南芥种皮中原花青素和花色苷向液泡内的跨膜转运过程。tt12突变体中积累的花色苷含量显著低于野生型，且种皮呈浅棕色或透明色[56, 57]。FFT编码的MATE转运蛋白参与拟南芥未成熟种子中的花色苷积累[58]。葡萄中AM1和AM3特异性介导酰基花色苷的跨膜转运[59]。多个MATE转运蛋白对酰基花色苷表现出特异的偏好性或较高的转运活性，但有关花色苷修饰（如酰基化和糖基化）对MATE蛋白转运活性的影响机制还需要进一步探究。研究表明，除在花色苷转运中起重要作用，MATE还参与其他类黄酮物质的积累过程。在蒺藜苜蓿（Medicago truncatula Gaertn.）中，表儿茶素3’-O-葡萄糖苷和酰化黄酮醇分别为MtMATE1和MtMATE2的靶向转运底物[60, 61]；VvMATE1和VvMATE2参与葡萄果实发育过程中原花青素的积累[62]。草莓中TT12的同源基因FaTT12-1不参与花色苷的转运，仅特异在原花青素的跨膜转运过程发挥重要作用，并能响应外界红光的调控[63]。
膜转运蛋白在花色苷跨膜转运过程中发挥着关键作用，但相关的机制研究仍较为缺乏，关于其底物识别与结合机制、跨膜方式、水解机制等转运机理知之甚少。有研究推测，膜转运蛋白与GST协同参与花色苷跨膜运输至液泡的过程，GST可能作为载体蛋白与花色苷共价结合，形成谷胱甘肽交联复合物以标记花色苷，并将其传递至液泡膜上，使其被液泡膜上的膜转运蛋白识别，进而实现花色苷的跨膜转运[55]。目前已经初步鉴别了多种在植物中参与花色苷转运的膜转运蛋白。除上述ABC和MATE两类蛋白外，康乃馨和葡萄中还发现了与花色苷积累水平显著相关的胆红素易位酶同族体BTL-homologue（Bilitranslocase-homologue）[17, 23]，但目前仍缺乏其介导花色苷跨膜转运的直接生物学证据。不同类型膜转运蛋白在介导花色苷转运过程中的相互关系，如是否存在底物竞争关系、协作和整合效应等，尚需深入探讨。
1.3 囊泡运输介导的花色苷转运机制
囊泡运输是一种高效、稳定的胞内底物转运方式，主要包含形成、运输和融合3个步骤。囊泡运输是花色苷从细胞质转至液泡中的另一种转运模型，有关囊泡运输介导的花色苷转运少有报道，该模型的提出源于显微镜观察结果[64]。花色苷被报道可通过自噬作用（Autophagy）、内质网和高尔基体的囊泡运输系统转运至液泡（图1），这些囊泡运输网络之间相互独立[55]。花色苷合成后，在细胞质中聚集形成有膜包裹的花色苷泡状体（Anthocyanoplast），该泡状体逐渐融合，继而被前液泡组成体（Pre-vacuolar compartments）所包裹，并运输至中央大液泡，最终在液泡中形成不规则、动态的花色苷液泡内涵体（Anthocyanic vacuolar inclusions，AVIs）[65]。AVIs的形成不仅可使花瓣颜色加深及出现蓝移现象，而且能优先选择聚集酰基化花色苷[66-68]。对诱导大量产生花色苷的拟南芥表皮进行镜检观察，发现了花色苷泡状体和液泡内涵体，类似的结构在葡萄中也存在[69, 70]，这一现象为囊泡运输介导花色苷的积累提供了理论支撑。在拟南芥未成熟种子和葡萄毛状根中进一步观察到了包含花色苷和原花青素的囊泡从内质网向中央液泡动态移动的过程，证实了类黄酮物质也可通过囊泡运输从内质网转出至液泡[71, 72]。拟南芥囊泡运输因子GFS9（GREEN FLUORESCENTSEED9）被认为是液泡内类黄酮物质积累的关键因子[73]。尽管已经发现了多种囊泡运输方式，但有关囊泡参与花色苷积累过程的分子和生化证据仍十分缺乏。
2. 小结与展望
色泽是影响果实外观和营养品质性状的重要指标，花色苷作为果实核心色素组分，研究其积累机制对完善花色苷从合成到积累这一完整代谢通路的理论具有重要意义。当前人们对果实中花色苷含量、分布和组成、生物合成的了解日益清晰，在花色苷合成及转录调控分子机制等方面已取得一系列成果，并对后续的转运过程开展了研究。解析胞内花色苷实时传递和跨膜动态运输已成为花色苷研究的难点。花色苷属于类黄酮合成途径的分支产物之一，与原花青素和黄酮醇等物质在生物合成上密切关联。鉴于其他类黄酮物质与花色苷属于同一代谢途径的不同产物，且其分子结构具有相似性，它们是否共享相似的转运机制及载体蛋白也是值得深思的问题。虽然还缺乏对类黄酮物质转运机制的系统研究，但深入理解花色苷转运可为进一步解析类黄酮物质在果实中的积累机制奠定基础。
为适应复杂多变的外界环境，植物体内转运机制具有多样化、高效性和冗余性等特点，不同转运机制在底物特异性、定位及转运效率上各异[18]，而在果实上有关多种转运模型协调转运花色苷的研究较为缺乏。近年来，GST、膜转运蛋白以及囊泡运输介导的果实花色苷转运相关研究已取得了初步进展，但不同转运模型的分子生物学证据仍不充足。以下方面的研究亟待进一步深入开展，以全面明晰果实花色苷的转运机制：（1）不同转运蛋白的转运活性差异及其底物特异性，花色苷修饰差异是否会影响其跨膜转运效率；（2）转运蛋白响应内在激素和外界环境因子参与花色苷积累的分子机制，以及表观调控对花色苷转运的影响；（3）GST如何与花色苷结合并促发其转运，GST-花色苷复合物如何在膜转运蛋白的协助下实现跨膜运输；（4）GST与囊泡动态移动间的关系，GST-花色苷复合物是否参与花色苷装载至囊泡及囊泡裂变和动态融合的过程；（5）多种转运机制如何分工协同参与胞内花色苷的转运过程。
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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. 
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