, 汤青林1,2 1. 西南大学 园艺园林学院 南方山地园艺学教育部重点实验室，重庆 400715;
2. 重庆市蔬菜学重点实验室，重庆 400715
收稿日期：2020-03-12；接收日期：2020-05-11；网络出版时间：2020-05-27
基金项目：重庆市自然科学基金(Nos. cstc2019jcyj-msxmX0335, cstc2019jcyj-zdxmX0022)资助
摘要：表皮毛是植物地上部分表皮细胞向外突出延伸的特化毛状结构，不仅可以保护植物免受病虫的危害，还具有一定的经济和药用价值，对其调控的分子机制的阐明有利于植物的分子设计育种和遗传改良。近年来，模式植物拟南芥表皮毛形成的调控模式基本被阐明，其他植物表皮毛的调控机制也取得很大进展。鉴于此，文中综述了拟南芥和棉花(单细胞表皮毛)及番茄和青蒿(多细胞表皮毛)在基因和激素水平上对表皮毛的发育调控，同时简要介绍了其他典型单、双子叶植物表皮毛相关的研究进展，最后，展望了植物表皮毛的研究方向和应用前景。
关键词：表皮毛转录因子单细胞多细胞调控模型
Research progress in regulation model in different types of plant trichome
Xiao Ma1,2, Kui Li1,2, Zhimin Wang1,2, Dayong Wei1,2
, Qinglin Tang1,2 1. Key Laboratory of Horticulture Science for Southern Mountainous Regions Ministry of Education, College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400715, China;
2. Chongqing Key Laboratory of Olericulture, Chongqing 400715, China
Received: March 12, 2020; Accepted: May 11, 2020; Published: May 27, 2020
Supported by: Natural Science Foundation of Chongqing, China (Nos. cstc2019jcyj-msxmX0335, cstc2019jcyj-zdxmX0022)
Corresponding author: Dayong Wei. Tel: +86-23-68251274; E-mail: swuwdy@swu.edu.cn;
Qinglin Tang. Tel: +86-23-68251274; Email: swutql@163.com.
Abstract: Plant trichomes are special structures that originate from epidermal outgrowths. Trichomes play an important role in plant defense against pests and diseases, and possess economic and medicinal values. Study on molecular mechanism of plant trichomes will contribute to the molecular design breeding and genetic improvement of crops. In recent years, the regulation mechanism of trichome development has been basically clarified in the model plant Arabidopsis thaliana, while great progresses are also found in other plant species. In this review, we focus on the developmental regulation of trichome formation from gene and phytohormones levels in Arabidopsis and cotton (with unicellular trichomes), as well as in tomato and Artemisia annua (with multicellular trichomes). The research progress associated with trichomes is also introduced in other typical monocotyledons and dicotyledons. Finally, the research and application of plant trichomes are prospected.
Keywords: trichometranscription factorunicellularmultilcellularregulation model
表皮毛(Trichome)由植物地上部分表皮细胞发育而来，是一种特化的毛状结构，不仅可以保护植物抵抗生物和非生物胁迫，还具有很高的经济和药用价值[1]。
表皮毛根据其是否具有分泌能力分为非腺毛和腺毛两种[2]。非腺毛存在于大多数的被子植物以及部分裸子植物和苔藓植物中，不具备合成和储存次级代谢产物的能力，部分可以抵御食草动物和昆虫的侵害，例如棉花表皮毛(棉纤维)在抵抗棉铃象鼻虫等害虫时起重要作用[3]。腺毛可以合成、分泌或储存多种次生代谢产物[4]，具有很高的经济和药用价值，例如青蒿素是治疗疟疾的主要成分，在青蒿的腺毛中合成，迷迭香腺毛可以产生治疗神经性疾病的酚类化合物，薄荷腺毛中合成的薄荷醇是一种重要的香料[5]。
表皮毛按形态学分为单细胞表皮毛和多细胞表皮毛两类。单细胞表皮毛结构简单，大多没有腺体，通常不具备分泌次生代谢物的能力，如拟南芥、棉花和十字花科蔬菜等植物的表皮毛。多细胞表皮毛结构复杂，有的具有分泌能力，如番茄Ⅰ、Ⅳ、Ⅵ、Ⅶ型表皮毛和青蒿表皮毛[6]，有的不具有分泌能力，如番茄Ⅱ、Ⅲ、Ⅴ和Ⅷ表皮毛。模式植物拟南芥表皮毛发育的调控机制已基本清楚，近几年，其他植物表皮毛发育的分子调控取得很大进展，本文将从基因和植物激素调控两方面，对单细胞植物(拟南芥和棉花)和多细胞植物(番茄和青蒿)表皮毛(图 1)的研究进展作详细阐述，并简要介绍其他单、双子叶植物表皮毛的研究进展。
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| 图 1 拟南芥、番茄、青蒿、棉花表皮毛形态[7-10] Fig. 1 Trichome morphology of Arabidopsis, tomato, sweet wormwood and cotton. (A) Trichome of Arabidopsis thaliana. Bar=100 μm[7]. (B) Glandular trichomes of tomato (Solanum lycopersicum), Ⅳ: type Ⅳ glandular trichome. Bar=50 μm[8]. (C) Glandular trichomes of sweet wormwood (Artemisia annua). Bar=15 μm[9]. (D) Trichomes of cotton (Gossypium hirsutum) Bar=50 μm[10]. |
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1 单细胞植物表皮毛调控机制1.1 拟南芥表皮毛1.1.1 基因对拟南芥表皮毛形成的调控拟南芥Arabidopsis thaliana表皮毛分布于茎、叶和萼片表面，多数为3个分支，属于典型的单细胞非腺毛，主要受R2R3-MYB、WD40 (WD40-repeat)、bHLH (Basic helix-loop-helix)和C2H2 (C2H2 zinc finger protein)等正调控因子和R3-MYB类负调控因子的调控。R2R3-MYB转录因子GL1/MYB23、WD40类蛋白TTG1和bHLH类转录因子GL3/EGL3共同形成一个三聚体复合激活因子MBW，直接作用于下游GL2/TTG2，调控表皮毛的发育[11]。
正调节因子GL1、MYB23和MYB82属于R2R3-MYB基因家族。其中，GL1最早被克隆[12]，gl1突变体表现为叶片无毛，超表达GL1叶片表皮毛密度降低[13]。GL1同源基因MYB23的突变体表皮毛分支减少，超表达则会导致下胚轴产生异位表皮毛[14]。GL1的另一个同源基因MYB82，可以部分恢复由gl1突变引起的表皮毛缺失的表型[15]。正调节因子TTG1，编码一种具有4–5个WD-40重复基序的蛋白，可在幼嫩组织间自由移动，ttg1的突变体表现出无表皮毛表型[16]。正调节因子GL3、EGL3、TT8和MYC1编码bHLH型转录因子。其中，GL3和EGL3功能冗余，二者在幼叶中表达量较高，gl3和egl3单突变体导致表皮毛数量和分支减少，双突变则表现为完全无毛[17]。超表达TT8可促进表皮毛形成，tt8突变体叶缘无表皮毛[18]。超表达MYC1表皮毛数量增长1倍，突变体表皮毛减少[19]。C2H2锌指蛋白家族的GIS、GIS2、GIS3、ZFP5、ZFP6和ZFP8也参与表皮毛的发育[20]。其中，GIS和GIS2分别在茎和花序表皮毛形成中起作用[21]，GIS3可通过直接激活GIS和GIS2的表达来调控表皮毛的形成[22]。ZFP5激活GIS、GIS2和ZFP8的表达，促进表皮毛发生[23]。ZFP6位于ZFP5上游，直接调控ZFP5的表达[24]。Kim等[25]发现一个新的转录因子TRP，可以与ZFP5相互作用，阻止ZFP5结合到ZFP8启动子上，抑制表皮毛的发生。
R3-MYB家族的TRY、CPC、ETC1、ETC2、ETC3、TCL1和TCL2是拟南芥表皮发育的负调控因子，超表达其中任意一个基因，都会形成无表皮毛的表型[26]。它们可以通过与R2R3-MYB蛋白(GL1/MYB23)竞争，与bHLH蛋白(GL3/EGL3)结合，阻止MBW复合体的形成，从而抑制表皮毛的发育[27]。其中，TRY和CPC是主要的负调控因子，try突变体表皮毛成簇生长且分支增加，cpc突变体表皮毛密度增大[28]，TCL1和TCL2主要在茎表皮毛中起负调控作用[29]。研究发现，SPL9和NTL8都可以直接调控TRY和TCL1的表达[30-31]。Vadde等[32]发现TCP4与TCL1和TCL2的启动子结合，直接调控其转录。Kirik等[33]发现etc1突变体表皮毛无明显变化，etc2和etc3突变体表皮毛增多。
除上述调节因子外，最新研究发现，泛素蛋白酶体相关调节因子GCN5通过调控GL1、GL2、GL3和CPC的表达来调控表皮毛的形成[34]。E3泛素蛋白连接酶UPL3通过降解GL3/EGL3抑制表皮毛的形成[35]。在m6A结合蛋白ECT2的突变体中，TTG1、ITB1和DIS2的mRNA稳定性降低，最后导致表皮毛分支增多[36]。RAV (RELATED TO ABI3 AND VP1)家族的TEM1和TEM2通过调节叶肉细胞中赤霉素(Gibberellin，GA)的合成和转运抑制表皮毛的形成。另外，TEM2还可以通过直接结合GL1、GL2、GIS2和ZFP8的启动子，抑制表皮毛的形成[37]。
1.1.2 激素对拟南芥表皮毛的调控表皮毛的发育受多种植物激素的严格调控，激素信号通过介导下游基因的表达，参与调节表皮毛的形成。其中，GA、茉莉酸(Jasmonic acid，JA)和细胞分裂素(Cytokinin，CK)对表皮毛发育有促进作用，水杨酸(Salicylic acid，SA)对表皮毛生长具有抑制作用[38]。外施GA可以促进表皮毛发生，Jacobsen等[39]发现SPY是GA信号通路的负调控因子，其突变体的表皮毛数量增多。拟南芥DELLA蛋白编码的5个基因GAI、RGA、RGL1、RGL2和RGL3对GA信号通路具有抑制作用，其中，RGA和GAI起关键作用[40]。Kim等[25]发现外源GA处理TRP超表达系，可以促进表皮毛的形成。GA和CK信号会被ZFP6整合，调控表皮毛的形成[24]。JA通过抑制JAZ蛋白的合成，可以消除JAZ蛋白与bHLH转录因子和MYB转录因子的相互作用，从而促进表皮毛的形成[41]。Peng等[42]克隆得到一个细胞周期调控因子CPR5，cpr5突变体的表皮毛长度和分支均减小，测定发现其含有较高的SA含量，推测CPR5可能参与SA的合成。
1.1.3 拟南芥表皮毛发育调控模型已有报道发现，基因对拟南芥表皮毛的调控主要是通过激活-抑制模式和激活(底物)-消耗模型[43-44]。Balkunde等[45]证实了上述2个模型，认为在表皮毛发育过程中确实存在一个MBW复合体(GL1-GL3-TTG1)，启动表皮毛的发育，而且该复合体可以调控TRY等负调控因子向邻近的非表皮毛细胞移动，进而阻止MBW复合体的形成，抑制表皮毛的启动。植物表皮毛调控是个复杂的过程，随着研究成果的不断涌现，张继伟等[46]拓宽了上述模型，增加了植物激素对表皮毛的调控，认为在表皮毛细胞中，GA和JA调控MBW复合体，GA和CK作用于GIS2，然后，MBW复合体和GIS2进一步作用于下游的GL2，调控表皮毛的启动。TRY等负调控因子向邻近非表皮毛细胞移动，与GL1竞争性结合在GL3上，形成TRY-GL3- TTG1复合体，阻碍GL2的表达，从而抑制表皮毛的形成。综合以上理论模式和近期的研究成果，我们进一步拓展了该模型，使其更加系统完善，在表皮毛细胞中，GA的合成受SPY的调控，GA通过DELLA和C2H2锌指蛋白调控MBW复合体，JAZ通过JAZ、SA通过CPR5也调控该复合体，CK通过ZFP6作用于C2H2锌指蛋白，进而激活下游GL2的表达，同时MBW复合体和GL2还受GCN5和TEM2的调控，最后指导表皮毛的形成(图 2)。
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| 图 2 拟南芥表皮毛调控模型[17] Fig. 2 Regulation model of trichome in Arabidopsis[17]. |
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1.2 棉花纤维1.2.1 基因对棉纤维形成的调控棉花Gossypium hirsutum是我国重要的经济作物。棉纤维是由棉花种子表皮细胞发育而来的毛状体，属于单细胞表皮毛。棉纤维发育分为起始期、伸长期、次生壁增厚期和成熟期4个阶段[47]。其发育过程主要受MYB、MADS和HD-Zip等转录因子的调控。
在起始期和伸长期，有多个MYB转录因子参与棉纤维的发育。其中，GhMYB109起正调控作用，它影响下游基因GhACO1、GhACO2、GhTUB1和GhACT1的表达[48]。GhMYB25和GhMYB25-like也起正调控作用，二者氨基酸序列相似度为69%，Walford等[49]发现GhMYB25-like在GhMYB25和GhMYB109的上游发挥作用。Sun等[50]发现GhMYB212直接调控蔗糖转运蛋白基因GhSWEET12的表达，进而调控棉纤维的伸长。GhMYB2受miR828和miR858的调控，促进棉纤维发育[51]。Wan等[52]和Wu等[53]发现2个MML (MYB-MIXTA-LIKE)转录因子GhMML3_A12和GhMML4_D12分别与短绒毛和长绒毛的形成有关。MADS转录因子家族成员GhMADS11在棉纤维中积累，促进细胞伸长[54]。Zhou等[55]发现异源超表达GhMAD14可降低GA含量，并缩短拟南芥下胚轴长度。HD-Zip蛋白GhHD1通过调节乙烯和活性氧(Reactive oxygen species，ROS)的积累，正向调控棉纤维的形成[56]。Shan等[57]发现GhHOX3可以结合到棉花细胞壁松弛蛋白基因GhRDL1和GhEXPA1的启动子上，激活其表达，促进棉纤维伸长。Liu等[58]发现GhCPC与GhTTG1和GhMYC1间存在相互作用，GhMYC1可进一步与GhHOX1的启动子结合，调控下游GhHOX1的表达。在次生壁增厚期，GhFSN1通过调控下游基因GhIRX12、GhMYB1、GhGUT1和GhDUF231L1的表达，来正调控棉纤维细胞次生壁形成[59]。此外，转录抑制因子GhKNL1可以被GhHUB2通过泛素-26S蛋白酶体途径降解，消除GhKNL1对棉纤维次生壁积累的抑制作用[60]。Huang等[61]通过对棉花基因组的分析，确定MYB46_D9和MYB46_D13在棉纤维次生壁积累中起作用。
1.2.2 激素对棉纤维的调控激素水平与棉纤维的生长发育密切相关，其中乙烯(Ethylene，ETH)、GA、生长素(Auxin，AUX)、油菜素内酯(Brassinosteroid，BR)和JA促进棉纤维的发育，CK对棉纤维的调控根据时期不同作用也不同，即开花前促进棉纤维发育，开花后抑制棉纤维发育[62]。1-氨基环丙烷-1-羧酸氧化酶(1-aminocyclopropane-1-1carboxylic acid oxidase，ACO)是ETH合成的最后一种限速酶，编码ACO限速酶的3个基因在棉纤维伸长期正向表达。Deng等[63]发现抑制GbPDF1的表达会积累大量H2O2，延缓棉纤维的发育。当GA浓度升高时，GhSLR1迅速降解，释放GhHOX3形成转录复合体，并激活下游GhRDL1和GhEXPA1等基因的表达，促进棉纤维增长[57]。通过用特异性启动子FBP7驱动IAA合成基因iaaM的表达，显著增加了IAA含量，促进棉纤维的形成[64]。Wang等[65]研究发现，GhTCP14和生长素途径中的关键基因AUX1和IAA3与PIN2的启动子结合，调控棉纤维的发育，GhTCP14还能促进GA的合成[66]。Luo等[67]克隆到一个编码BR合成限速酶5α-还原酶的基因GhDET2，在棉纤维的密度和长度方面均有促进作用。Sun等[68]发现编码BR应答激酶BRI1的基因GhBRI1，促进棉纤维中纤维素的积累，影响棉纤维的成熟。GhPAG1与拟南芥CPY734A1同源抑制棉纤维发生，pag1突变体表现出缺乏BR的典型表型，推测其通过参与BR途径调节棉纤维[69]。Gh14-3-3是一种酸性调控蛋白，它可以和GhBZR1相互作用调节BR信号，促进棉纤维的伸长[70]。棉花中JA调控表皮毛的途径与拟南芥相似，JA可通过抑制负调控因子GhJAZ2的表达，促进棉纤维形成。GhJAZ2可与GhMYB25-like和GhGL1相互作用，抑制GhMYB25-like和GhGL1功能[71]。GhCKX是CK合成途径中的关键负调控因子，超表达GhCKX可使CK含量降低，棉纤维数量减少[72]。
1.2.3 棉纤维调控模型棉纤维与拟南芥一样，都属于单细胞非分泌型，但棉纤维长而不分支，拟南芥表皮毛短且分支，形态差异表明二者调控机理有所不同。Wang等[73]通过比较棉花和拟南芥表皮毛的调控机制，从激素和基因水平对棉纤维的调控模型进行了总结：在棉纤维起始期，JA通过JAZ2，调控下游基因MYB25-like，同时CPC阻止TTG1/MYC1的表达，促进HOX1的表达，启动棉纤维的形成。在伸长期，MYB212促进SWEET12的表达，PDF促进ROS的积累，最后调控棉纤维的伸长。在起始期向伸长期过渡间，ETH和ROS相互介导调控棉纤维的起始和伸长。在棉纤维次生壁增厚期，MYB46_D9/D13和FSN1促进SCW相关基因的表达，同时KNL1抑制Rev-08和XTH1的表达，促进棉纤维次生壁增厚，整个过程参与的激素有JA、乙烯和生长素，参与的基因主要是MYB、bHLH和HD-bZIP转录因子。随着棉花参考基因组的公布，结合近两年棉纤维的研究成果，我们拓宽了上述模型，增加了GA、CK和BR对棉纤维的调控。GA途径介导棉纤维的起始和伸长，GA的合成受MADS14和TCP14的调控，调控下游基因的表达和ETH含量。CK促进棉纤维的伸长，其合成受CKX的抑制。BR通过促进Gh14-3-3和BZR1互作促进棉纤维起始和伸长，BR还通过BRI1促进棉纤维次生壁增厚(图 3)。
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| 图 3 棉纤维调控模型[73] Fig. 3 Regulation model of trichome in cotton[73]. |
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与拟南芥表皮毛调控机制相比，GL1、GL3和TTG1复合体在拟南芥表皮毛形成中起核心作用，但在棉花中，该复合体的同源基因在棉纤维的起始和伸长阶段仅起部分作用。另外，研究还发现，脱落酸(Abscisic acid，ABA)和生长素对棉纤维的形成分别起负向和正向调控作用，但二者在拟南芥表皮毛研究中还未见报道。
2 多细胞植物表皮毛调控机制2.1 番茄表皮毛2.1.1 基因对番茄表皮毛形成的调控番茄Solanum lycopersicum表皮毛类型众多，功能各不相同，根据形态结构可分为Ⅰ–Ⅷ八种类型，其中，Ⅱ、Ⅲ、Ⅴ和Ⅷ类型为非腺毛，由颈部和基部组成，作为物理屏障，具有抗病虫的功能；Ⅰ、Ⅳ、Ⅵ和Ⅶ类型为腺毛，除了颈部和基部外，还有一个腺体顶端，可分泌储藏各种次级代谢物，抵御食草动物的侵害[74]。到目前，控制腺毛的基因几乎都影响非腺毛的发育，只有SlMYC1基因只调控腺毛的形成。番茄表皮毛主要受R2R3-MYB、HD-Zip第Ⅳ亚族、C2H2和bHLH等基因家族的转录因子调控[8]。SlMX1属于R2R3- MYB基因亚家族，过表达使非腺毛和腺毛的密度和数量增加，低表达则会降低腺毛密度[75]。SlCD2和SlWo属于HD-Zip家族第Ⅳ亚族，Nadakuduti等[76]研究表明SlCD2对腺毛起始发育起正调控作用，突变体腺毛数量减少。SlWo是番茄中最早发现的参与调控表皮毛发育的基因，超表达SlWo能够增加Ⅰ型腺毛的数量，SlWo突变体中Ⅲ型和Ⅴ型表皮毛密度增大，Ⅳ型腺毛密度降低[77]。另外，刘金秋等[78]发现SlHZ45与SlWo高度同源，能够促进Ⅰ型和Ⅳ型表皮毛的形成。C2H2锌指蛋白家族的SlH基因缺失会抑制Ⅰ型表皮毛的形成，且SlH是关键正调控因子。Chang等[79]发现SlH蛋白和SlWo蛋白可以直接互作，形成异源二聚体促进Ⅰ型腺毛的发生。Xu等[80]发现部分敲除bHLH家族的SlMYC1基因会降低番茄Ⅵ型腺毛的密度和长度，完全敲除SlMYC1导致Ⅵ型腺毛消失。除了上述因子外，细胞周期蛋白也具有重要作用，SlCycB2编码B型细胞周期蛋白，SlCycB2超表达则植株中所有的非腺毛和腺毛基本消失，而干扰SlCycB2则会抑制Ⅰ型表皮毛，促进Ⅲ型和Ⅴ型表皮毛的形成[81]。
2.1.2 激素对番茄表皮毛的调控番茄表皮毛主要受JA、AUX和GA等植物激素的调控，其中，JA诱导腺毛发生的作用明显，SlJAZ2是番茄JA信号通路的阻遏蛋白，是腺毛发生的负调控因子，在SlJAZ2超表达植株中，SlWo基因和SlCycB2基因的表达量受到抑制，表明SlJAZ2通过抑制SlWo和SlCycB2的表达来抑制腺毛的起始[82]。Thines等[83]通过酵母双杂交发现SlJAZ2与SlCOI1有相互作用，且SlCOI1本身也是腺毛发生的正调控因子。AUX在调控腺毛生长方面同样具有重要作用，当番茄生长素家族基因SlIAA15和生长素响应因子SlARF3表达下调时，番茄Ⅰ型、Ⅴ型和Ⅵ型表皮毛数量减少[84]。SlbHLH95是Chen等[85]发现的一个番茄表皮毛负调控因子，其超表达植株表皮毛密度降低，并且SlbHLH95可以直接与GA合成相关基因SlGA20ox2和SlKS5的启动子结合，调控其表达。
2.1.3 番茄表皮毛调控模型虽然多细胞腺毛调控机制的研究相比单细胞表皮毛起步较晚，但番茄表皮毛调控模型已初步成型。Chalvin等[8]从基因和激素途径对番茄表皮毛调控模型进行了总结：JA通过JAZ2调控下游CycB2和WOOLLY的表达，WOOLLY与CycB2相互作用调控表皮毛发生，同时CycB2表达还受MX1和WOLLY的调控。此外，WOOLLY也能与HAIR形成二聚体调控表皮毛的发育，CD2和MYC1也可以促进表皮毛的发生。随着研究的深入，越来越多参与番茄表皮毛调控的基因和途径被发现，因此我们结合了近年来的研究结果，拓展了上述模型，增加了GA调控途径以及AUX途径相关基因。bHLH95通过GA20ox2和KS5调控GA合成调控表皮毛的形成。AUX途径相关基因IAA15以及JA途径相关基因COI1均能促进表皮毛发生(图 4)。
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| 图 4 番茄表皮毛调控模型[8] Fig. 4 Regulation model of trichome in tomato[8]. |
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2.2 青蒿表皮毛2.2.1 基因对青蒿表皮毛形成的调控青蒿Artemisia annua L.是菊科蒿属一年生草本药用植物，可以从中提取倍半萜内酯类化合物青蒿素。青蒿具有两种腺毛，即非分泌型腺毛和分泌型腺毛，非分泌腺毛因其外形类似于字母“T”，所以又称T型腺毛。青蒿素的合成和储存均在青蒿分泌型腺毛当中进行，因此可以通过提高青蒿腺毛密度提高青蒿素产量[86]。青蒿中参与腺毛发育调控的转录因子与番茄一样，大多数属于R2R3-MYB和HD-Zip基因亚家族[8]。AaMYB1和AaMIXTA1属于R2R3-MYB转录因子，超表达AaMYB1可以增加青蒿腺毛的密度[87]。AaMIXTA1正向调控腺毛发育起始和叶片表面角质层的合成[88]。HD-Zip家族的AaHD1和AaHD8对腺毛的起始起正调控作用，超表达AaHD1或AaHD8均会增加青蒿腺毛的密度，抑制二者中任何一个的表达，腺毛密度减少，进一步研究发现AaHD8与AaMIXTA1构成的转录复合物可促进AaHD1的表达[89]。
2.2.2 激素对青蒿表皮毛的调控青蒿表皮毛的形成主要受JA调控，AaJAZ8是青蒿JA信号通路的阻遏蛋白，它能抑制正调控因子AaHD1的活性，降低青蒿腺毛密度[90]。Wang等[91]报道了一个应激相关蛋白AaSAP1，其超表达系表皮毛密度明显增多，激素处理后发现GA、JA和ABA均能够促进AaSAP1的表达。
2.2.3 青蒿表皮毛调控模型近年来，青蒿素因其抗疟效果受到世界广泛关注，而青蒿腺毛是青蒿素合成贮藏的唯一场所。虽然通过增加表皮毛数量提高青蒿素产量办法可行，但关于青蒿表皮毛调控机制的研究尚处于初步阶段。Chalvin等[8]总结了基因和激素途径，初步建立了青蒿表皮毛调控模型：JA通过JAZ8调控下游HD1的活性来调控表皮毛，同时HD1的表达受HD8和MIXTA1所组成的复合物的调控。此外，正调控转录因子MYB1可以促进表皮毛的发生。基于上述模型，我们根据最新的研究结果，扩展了调控模型，增加了应激相关蛋白SAP1的调控机制。SAP1能够促进表皮毛发生，其表达受JA、ABA、GA的调控(图 5)。
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| 图 5 青蒿表皮毛调控模型[8] Fig. 5 Regulation model of trichome in Artemisia annua[8]. |
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3 其他植物表皮毛研究进展3.1 双子叶植物除模式植物表皮毛研究外，黄瓜、烟草、猕猴桃和大豆等双子叶植物中参与调控表皮毛发育的基因也均有研究。黄瓜中有5个与表皮毛相关的突变体，分别是csgl1、tbh、mict、csgl3、tril。其中，csgl1、tbh和mict突变体表皮着生极细小的表皮毛，而csgl3和tril突变体表皮则完全无毛[90]。在csgl1、tbh和mict突变体中，TRIL/CsGL3表达量升高。说明TRIL/GsGL3可能在TBH/MICT/CSGL1上游调控其表达[93]。之后，Yang等[94]研究发现CsTRY可以抑制表皮毛的形成，并受上游CsMYB6的直接调控。李创等[95]从猕猴桃基因组数据库中筛选出两个与表皮毛发育相关的基因Achn116791和Achn302211，二者参与调控猕猴桃叶片表皮毛的长度和密度。烟草中NbGIS和NbWo可以促进表皮毛形成，NbWo通过促进NbCycB2的表达促进表皮毛发育，而NbCycB2则通过抑制NbWo的活性抑制表皮毛的形成[96]。周云霄等[97]从大豆中分离出6个与拟南芥AtTCL1同源的基因GmTCL1–GmTCL6，均能抑制拟南芥表皮毛的形成。此外，Wu等[98]发现大豆光敏色素基因GmPHYB1会导致拟南芥表皮毛增多。
3.2 单子叶植物除双子叶植物外，单子叶植物水稻、玉米等的表皮毛基因均有报道。水稻OsTCL1是拟南芥AtTCL1的同源基因，OsTCL1转化至拟南芥中可以抑制拟南芥表皮毛的形成，但在水稻中超表达却不会影响表皮毛的发育[99]。Xie等[100]研究发现OsGL6只能促进表皮毛伸长，却不影响表皮毛起始，进一步研究发现OsGL6可以与OSK3和CSN5蛋白相互作用，OsGL6可能通过与OSK3和CSN5形成复合物调控表皮发生。Sun等[101]研究表明AP2/ERF转录因子OsHL6可以促进表皮毛起始和伸长，进一步研究发现OsHL6蛋白可以和水稻表皮毛起始关键调控因子OsWOX3B相互作用，增强OsHL6与下游生长素相关基因OsYUCCA5的结合能力。另外，Lan等[102]报道了一个水稻耐盐性相关基因OsSPL10，同时发现该基因还可促进表皮毛的形成。Sturaro等[103]从玉米当中克隆了GLOSSY1，发现该基因与玉米表皮毛和蜡质积累有关。此外，Vernoud等[104]发现玉米中OCL4基因能够抑制表皮毛的形成。在小麦当中，Wang等[105]经过对TaLTP1的启动子分析，发现TaLTP1启动子?303 bp处的CCAACAT顺式元件是指导TaLTP1启动子在表皮毛中特异表达的关键元件。
4 展望基因和激素对单细胞表皮毛(拟南芥和棉花)和多细胞表皮毛(番茄和青蒿)生长发育具有重要的调控作用，通过总结不同类型表皮毛的调控模型，发现单细胞植物拟南芥表皮毛调控机制已基本阐明，鉴定出了大量的正调节因子和调控途径，但负调控机制和负调节因子报道较少。随着CRISPR-Cas9等基因编辑技术的快速发展，负调节因子的研究将更有价值，通过基因编辑技术将植物表皮毛负调节因子敲除，会得到正向的表型，对植物表皮毛的分子设计育种具有重要的意义。本课题组对收集到的周身覆盖表皮毛的野生甘蓝进行了初步研究，通过遗传定位和表达分析，锁定控制表皮毛的候选基因为BolTRY-like，研究发现该表皮毛对菜青虫具有显著的抗性，通过CRISPR-Cas9技术在花椰菜(无表皮毛)敲除BolTRY-like基因，期望获得有毛花椰菜，这些研究将为以花球为食用器官的甘蓝类蔬菜品种改良提供了新思路。
多细胞植物表皮毛的分子机制研究刚刚起步，主要集中在番茄和青蒿。番茄SlMYC1是唯一的只调控分泌型表皮毛的基因[8]，其余已被鉴定的多细胞表皮毛基因同时影响单细胞表皮毛，所以是否还有更多的基因特异调控分泌型表皮毛值得进一步探索。多细胞表皮毛的深入研究，对农艺性状的遗传改良具有重要意义，比如，番茄的Ⅳ型表皮毛的增加可以分泌大量的萜类化合物，从而抵抗昆虫的取食。青蒿中，超量表达AaMIXTA1、AaHD1或AaHD8能显著增加表皮毛中青蒿素的产量，同时不影响其他的农艺性状[89]。通过对表皮毛调控机制的不断探索和逐渐完善，为利用新技术新方法对植物的遗传改良提供了新的育种策略，也将是未来分子设计育种的新方向。
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