植物与线虫互作的信号传导及调控机制研究进展

叶德友，漆永红，李敏权

(1.甘肃省农业科学院蔬菜研究所，甘肃 兰州 730070；2.甘肃省农业科学院植物保护研究所，甘肃 兰州 730070；3.甘肃省农业科学院，甘肃 兰州 730070)



植物与线虫互作的信号传导及调控机制研究进展

叶德友1*，漆永红2，李敏权3

(1.甘肃省农业科学院蔬菜研究所，甘肃 兰州 730070；2.甘肃省农业科学院植物保护研究所，甘肃 兰州 730070；3.甘肃省农业科学院，甘肃 兰州 730070)

植物寄生线虫严重危害农业生产，对全球作物产量造成重大经济损失。植物对线虫的抗病和感病性作为作物生产中的关键性影响因子，一直是作物遗传育种学家研究的重要课题之一，探明植物对线虫抗病和感病性的内在机理对于指导作物抗线虫育种具有重要的理论意义和实践价值。本文综述了影响植物对线虫抗病和感病性的内在因素，包括植物抗性基因或蛋白、激素合成与信号传导以及线虫胁迫过程中产生的活性氧等信号传导。国内外近年来的研究认为，植物对线虫的抗病或感病性取决于多种信号通路间的协调互作，各种与线虫抗性相关的信号通路间的交互对话构成了复杂的信号传导网络，多种转录因子与小RNAs通过转录、转录后以及翻译参与了信号传导网络的精细调控，这一高效控制的信号传导网络决定了寄主植物对线虫的抗病或感病性。这些研究成果将为深入阐明植物与线虫互作的信号传导和调控机制奠定基础，从而为植物线虫防控新策略的制定提供理论依据。

线虫；抗性基因；激素；活性氧；小RNA

植物在生长环境中往往会受到真菌、细菌、病毒和线虫等病原微生物的胁迫，这些病原微生物分泌效应分子进入植物细胞引起植物发病。植物能够识别病原相关的分子模式(pathogen-associated molecular patterns, PAMPs)，病原利用该模式识别植物受体(pattern recognition receptors, PRRs)，从而引起模式触发免疫(pattern-triggered immunity, PTI)。植物为应对病原微生物进化出了一些特异的抗性(resistance, R)蛋白，R蛋白能够识别病原效应子引起效应子触发的免疫反应(effector-triggered immunity, ETI)[1]。R蛋白通常含有核苷酸结合位点(nucleotide-binding site, NBS)与胞外富亮氨酸重复结构域(leucine-rich repeat, LRR)，NBS具有NTP酶活性，LRR与植物受体和病原效应子的互作有关，当与病原效应子接触时，NBS作为分子调节器激活下游信号传导，R蛋白能够直接识别病原效应子，也可以通过其他辅助因子识别病原[2]。PTI或ETI反应的激活增强了植物对病害的抗性，抑制了病原菌的生长，抗病性与感病性植物的主要区别就在于抗病性植物能够适时地识别入侵微生物，并能够快速有效地启动防卫反应[3]。

植物线虫是农业生产中的一类重要病原微生物，危害农作物生产的植物线虫主要包括根结线虫(Meloidogynespp., root-knot nematodes, RKN)和孢囊线虫(Globodera和Heteroderaspp., cyst nematodes, CN)。这些线虫与寄主作物进化出了复杂的互作关系，在植物体内形成了高度特化的线虫取食位点(nematode feeding site, NFS)。NFS是线虫侵染植物后在根系中形成的细胞核分裂而细胞质未经分裂的多核细胞，是线虫赖以生存的营养来源，如RKN在根系中形成的巨型细胞(giant cells)[4]，而CN将初始取食细胞与相邻细胞间的细胞壁打破融合形成合胞体(syncytia)[5]。线虫通过口针从NFS中摄取养分，口针分泌的效应物对于NFS的形成与维持至关重要，这些效应蛋白作为PAMPs或致病效应子促使线虫寄生，或调节植物的防卫反应，或改变植物的生理[6]。线虫分泌的效应蛋白既可以进入细胞质，与细胞周期、细胞骨架和细胞代谢组分发生互作，也可以在胞外积累，降解植物细胞壁，改变细胞壁结构[7]。

了解植物-线虫互作中的信号传导与调控机制对于确定控制植物与线虫互作关系的生物进程至关重要。本文对国内外近年来在影响植物对线虫的抗病性(R)和感病性(susceptibility, S)因素等方面取得的研究进展进行了综述，包括参与植物防卫反应的信号分子及其传导途径，不同R基因介导的线虫抗性及其信号传导，植物应答线虫胁迫中的植物激素合成、信号传导以及活性氧(reactive oxygen species, ROS)的产生及其信号传导，小RNAs在植物-线虫互作中的调控作用等，旨在为全面解析植物与线虫互作的信号传导和调控机制奠定基础。

1　植物-线虫互作中的R蛋白及信号传导

植物中蕴藏着大量的抗线虫资源，现已在植物基因组中定位了许多抗线虫基因[8]。Cai等[9]首次从甜菜(Betavulgaris)中克隆出抗线虫基因Hs1pro-1，此后其他一些抗线虫基因如Mi-1[10]、Gpa2[11]、HeroA[12]、Gro1-4[13]和Ma[14]陆续获得克隆，这些基因均编码胞内NBS-LRR类R蛋白。前人将NBS-LRR类蛋白分为TIR-NBS-LRR和CC-NBS-LRR两种类型[8,15]，研究发现蛋白质白介素受体(toll-interleukin receptor, TIR)与卷环结构(coiled-coil, CC)在免疫反应的信号传导中发挥关键性作用[2]。NBS-LRR蛋白作为病原受体，通过检测病原效应子引发以过敏反应(hypersensitive response, HR)为主要特征的ETI类抗性反应。目前已从HR中鉴定到了一些与植物NBS-LRR蛋白互作的线虫效应子，如PCN效应蛋白RBP-1，含SPRY结构域，与Gpa2蛋白互作[16]，MAP-1、Cg-1基因编码的RKN效应蛋白，可能与番茄Mi-1蛋白互作[17-18]。植物NBS-LRR基因介导的线虫抗性往往伴随着HR类细胞坏死[16,19]，可能还存在其他一些未知的与植物R蛋白互作的线虫效应子。因此，深入研究不同结构域如何感知病原进行信号传导将有助于解析R基因介导的线虫抗性中的信号传导通路。

番茄(Solanumlycopersicom)Mi-1是目前研究得较为透彻的抗线虫基因，其编码的R蛋白参与了RKN抗性。Mi-1介导的RKN抗性依赖于病原识别和Mi-1蛋白中LRR结构域介导的抗性信号传导[20]以及与NBS结构域相关的ATP酶活性介导的抗性信号传导[21]。现已证实，Mi-1蛋白N端在激活Mi-1蛋白时既有正调控作用也有负调控作用[22]，番茄RKN抗性需要Mi-1上游Rme1基因的参与[23]。通过病毒诱导的基因沉默(virus-induced gene silencing, VIGS)证实，番茄Mi-1介导的RKN抗性需要HSP90-1和SGT1的参与[24]。依据R蛋白介导的信号传导模型[2]，Mi-1编码的NBS-LRR蛋白与HSP90-1和SGT1蛋白结合构成R蛋白信号复合物，通过检测线虫效应子诱导的Rme1编码蛋白的构象变化激活下游信号传导通路，而Rme1可能是Mi-1蛋白的互作因子和线虫效应子的直接靶标[24]。Gpa2介导的马铃薯(Solanumtuberosum)孢囊线虫(potato cyst nematodes, PCN)抗性需要RNA-GTP的参与，RNA-GTP可激活Gpa2辅因子蛋白质2的活性[16]。

Rhg1和Rhg4是与大豆(Glycinemax)孢囊线虫(soybean cyst nematodes, SCN)的R/S有关的2个数量性状位点(quantitative trait loci, QTL)，不同于上述抗线虫R基因，QTL编码区的胞外LRR激酶类R蛋白可能调控SCN抗性[25]。现已证实，Rhg1介导的SCN抗性由3个基因决定，即编码氨基酸转运蛋白、α-SNAP蛋白和损伤诱导的结构蛋白基因，SCN抗性可能与包含这3个基因31 kb重复序列的拷贝数有关，多拷贝产生抗性，而单拷贝则对SCN表现感病。此外，Rhg1内存在的差异甲基化区域与SCN抗性有关，预测一些表观遗传因素可能在Rhg1介导的SCN抗性中发挥重要作用[26-27]。Rhg4介导的SCN抗性与编码丝氨酸羟甲基转移酶(serine hydroxymethyltransferase, SHMT)基因中的2个单核苷酸多态性有关[28]，SHMT可能通过调控叶酸碳代谢影响植物对线虫的R/S反应，这是由于叶酸缺失导致线虫诱导的合胞体细胞发生降解，线虫因饥饿而死，Suzuki等[25]研究认为Rhg4位点邻近的LRR基因调控SCN抗性。迄今，国内外尚未从Rhg1与Rhg4位点分离获得与R蛋白类似的基因产物，今后仍需开展相关研究进一步解析Rhg1与Rhg4在SCN抗性中的确切作用。

2　植物-线虫互作中的激素信号传导

线虫侵染植物后，多种植物激素参与激活PTI和ETI的下游反应，从而诱导或抑制对线虫的防卫反应。水杨酸(salicylic acid, SA)、茉莉酸(jasmonic acid, JA)、乙烯(ethylene, ET)等信号分子在植物应答线虫胁迫中发挥重要作用，一些激素还参与了受线虫侵染的植物生长发育的调控，如生长素(auxin, AX)等。胁迫类激素SA、JA和ET主要通过PR基因以及其他抗性因子调控植物对线虫的R/S，生长类激素AX则通过调控NFS的起始与发育影响线虫的寄生。植物应答线虫胁迫中每一种激素的作用较为复杂，这不仅与植物和线虫的物种特异性有关，还取决于线虫侵染时间的差异。此外，不同的激素信号通路之间存在着错综复杂的互作关系。

2.1水杨酸

SA信号参与了R基因介导的线虫防卫反应，SA信号在R基因HeroA[29]、Mi-1[30]与QTL基因Rhg1[31]介导的线虫抗性中表达增强，携带R基因Mi-1和HeroA的番茄中过表达NahG(编码SA羟化酶)，转基因植株降低了对RKN和CN的抗性[29,32]。SA同源物苯并噻二唑(benzothiadiazole, BTH)能够恢复转NahG番茄(含Mi-1)的RKN抗性，而缺失Mi-1的感病植株则未能获得RKN抗性[32]。拟南芥(Arabidopsisthaliana)R基因介导的抗性和基础防卫需要SA信号下游组分AtWRKY70的参与[33]。外源施用SA后发现，含Mi-1的番茄中WRKY70表达增强，沉默WRKY70则使Mi-1介导的RKN抗性降低[34]。WRKY转录因子参与了PTI与ETI中防卫反应的表达调控[33]，甜菜孢囊线虫(beet cyst nematode, BCN,Heteroderaschachtii)侵染拟南芥后，其根系中WRKY6、WRKY11、WRKY17、WRKY33均下调表达，促进了线虫及其NFS的发育[35]。

除了R基因介导的抗性之外，参与SA生物合成、信号传导以及SA响应的相关基因促进了植物对线虫的基础抗性。拟南芥异分支酸合成酶基因(iso-chorismate synthase,ICS)突变体和NahG转基因品系增强了拟南芥对SCN的敏感性[36]，说明SCN抗性需要内源SA的积累。ICS是SA合成中的关键酶，大豆中过表达SA甲基转移酶(SA methyltransferase, SAMT)基因，其根系中ICS表达增强，大豆对SCN表现出抗性[37]。SAMT通过将SA转换为甲基水杨酸(methyl salicylic acid, MeSA)调控SA水平[38]，MeSA作为移动性信号分子参与了植物系统获得性抗性(systemic acquired resistance, SAR)[39]。PAD4位于SA信号通路上游，通过与病原敏感性增强子(enhanced disease susceptibility 1, EDS1)互作对病原胁迫作出应答[38]。Atpad4突变增加了拟南芥对SCN的敏感性，过表达Atpad4的野生型大豆对RKN的抗性增强[40]。在大豆与SCN亲和与非亲和互作中，根系中EDS1转录水平增加[41]，表明SA信号通路上游组分参与了线虫抗性。SA信号通路下游主要受制于SA受体病程相关非表达子基因(non-expressor of pathogensis related 1,NPR1)的调控[42]，拟南芥NPR1缺失突变体增强了对SCN的感病性，而npr1-1诱导型抑制子(suppressor ofnpr1-1 inducible,SNI1)缺失突变体则增强了SCN抗性[36]，通过转基因在烟草(Nicotianatabacum)和大豆中表达AtNPR1分别获得了RKN和SCN抗性[43-44]，大豆中过表达AtTGA2使得SCN在根系中的寄生受到抑制[45]。

PR是研究较为透彻的防卫基因，PR的诱导表达可作为SA介导的抗性反应激活的重要标志[38]。将SCN效应子10A06转入拟南芥抑制PR-1、PR-2和PR-5的表达，转基因植株增强了对SCN的敏感性[46]。SA防卫反应的信号中断影响SCN的寄生，抑制PR-1和PR-5的表达发现SCN在大豆根系中建立了NFS，而过表达AtPR-5检测到大豆根系中SCN的寄生受到抑制，表明SA响应的防卫基因参与了线虫抗性[45,47-48]。对RKN敏感的玉米(Zeamays)lox3突变体中PR-1强烈诱导表达[49]，LOX3编码9-脂氧合酶，9-脂氧合酶将脂肪酸氧化成脂氧合酶和JA[50]，lox3突变体增加了JA与ET响应及其生物合成基因的表达水平[49]。与施用茉莉酸甲酯(methyl jasmonic acid, MeJA)相比，外源喷施SA同源物BTH仅能轻微增强水稻(Oryzasativa)RKN抗性[51]。因此，尽管SA在植物对线虫的R/S中发挥关键性作用，其他一些激素及其参与的信号通路在植物应答线虫胁迫中的作用也不容忽视。

2.2茉莉酸

与SA合成和信号传导不同，JA信号与植物对线虫的敏感性有关。通过COI受体中断JA信号，发现携带Mi-1的抗性番茄对RKN的抗性减弱[52-53]。Mi-1介导的RKN抗性中JA与SA信号相互拮抗，外源MeJA处理后SA诱导的WRKY70的表达受到抑制[54]。现已证实JA受体coi-1突变体显著降低了感病番茄根系中RKN的卵块数目，对线虫敏感的番茄中JA生物合成增加[49,52,55]。拟南芥lox4突变体中参与JA生物合成的基因诱导表达使植物对RKN更敏感，暗示JA积累与线虫敏感性有关[55]，对RKN敏感的玉米lox3突变体中JA合成基因同样诱导表达[49]，RKN侵染后LOX4与ZmLOX3表达增强。因此，JA生物合成可能正调控植物对线虫的敏感性[49,55]。

蛋白酶抑制剂(protease inhibitors, PI)可能是JA诱导线虫抗性的下游调控子，番茄根系中高量表达多半胱氨酸蛋白酶抑制子(multicystatin)类基因与PI基因时发现RKN的侵染受到抑制[56]。Mj-FAR-1是对RKN特异的脂肪酸和视黄醇(retinol)结合家族蛋白成员，番茄中超量表达Mj-FAR-1发现JA响应的蛋白酶抑制子(Pin2)和γ-硫堇(thionin)编码基因的表达受到抑制[57]，表明Mj-FAR-1可能负调控RKN抗性。JA和ET在水稻RKN抗性中的作用强于SA，外源MeJA和ET处理均可增强RKN抗性，这与抗性相关基因的高量表达有关，叶面喷施JA或ET生物合成抑制剂增加了水稻RKN敏感性[51]，RKN侵染后水稻根系和茎中参与JA、ET生物合成与信号传导的基因表达受到抑制[58]。此外，JA是水稻RKN抗性中必不可少的信号分子，而ET介导的RKN抗性依赖于JA的生物合成。JA合成受阻的水稻突变体叶面喷施ET不影响RKN的侵染，但ET信号传导受阻后JA诱导的防卫反应仍然发挥作用[51]。

2.3乙烯

ET及其信号传导能够影响RKN和CN的基础抗性。外源ET处理大豆根系使大豆对SCN更敏感，而ET抑制剂1-甲基环丙烯(1-methycyclopropene, MCP)和2,5-降冰片二烯(2,5-norbornadiene, NBD)减少了大豆根系中SCN的侵染，表明ET负调控线虫抗性[59]。拟南芥ET突变体eto1、eto2和eto3对CN表现高感[60]，但对RKN的抗性增强[61]，说明ET突变体在CN和RKN抗性中的作用相反。拟南芥ET受体突变体etr1和ET信号突变体ein2、ein3对CN的敏感性减弱[60]，编码UDP-葡萄糖异构酶的基因受ET信号基因EIN2和EIN3的负调控，而UDP-葡萄糖异构酶能够促进CN抗性[62]。ET非敏感突变体etr1、ers2、ein4和番茄Nr正向调控ET信号基因ein2、ein3、ein5和ein7，导致RKN侵染数量增加，而负调控ET信号突变体ctr1使RKN的侵染数目减少。因此，ET生物合成及其信号传导负调控CN抗性而正调控RKN抗性，但其具体的作用机理尚不明晰。

ET响应的转录因子EREBPs在大豆与SCN的非亲和性互作中诱导表达，而在亲和性互作中其表达受到抑制[63]，大豆和拟南芥中过表达大豆GmEREBP1，根系中PR类基因诱导表达，但转基因植株并未增强拟南芥对SCN的抗性[64]。在过表达GmEREBP1的转基因植株中，除了ET诱导的GmPR2、GmPR3和AtPDF1.2基因表达增强之外，SA响应的AtPR1、GmPR1和AtPR2基因以及JA响应的GmPR3和AtPDF1.2同样诱导表达[64]。这些研究表明，ET生物合成及其信号传导在对不同的线虫R/S中发挥不同的作用，因此，ET在植物线虫抗性中可能具有多效性。一是由于ET合成和信号基因突变体对CN和RKN的反应不同，不同的线虫种类与其寄主之间可能存在独特的作用机制；另外，GmEREBP1转基因植株中不同种类的PR蛋白得以诱导表达，说明线虫侵染植物过程中，ET、SA和JA信号通路之间发生了复杂的交互对话。目前还很难确定ET在线虫侵染过程中的确切作用，但可以肯定，ET在一些线虫的致病性中发挥重要作用，可能间接影响线虫抗性。

2.4生长素

线虫侵染过程中AX的极性运输影响其在取食细胞中的分布。在CN侵染的初始阶段，LAX3/AUX1增加AX输入而PIN1减少AX输出，使AX在侵染部位积累，而当合胞体细胞扩张时，PIN3和PIN4通过横向运输将AX输送至初始合胞体周围细胞[65-66]。LAX3是线虫分泌蛋白Hs19C07的直接靶标，Hs19C07与LAX3结合激活了LAX3，促进了合胞体的发育[66]。AX非敏感突变体对CN抗性强于其野生型，CN建立的NFS及其相邻细胞中的AX水平瞬间增加[67-68]。在顺式作用元件NtCel7中发现了AX响应元件，NtCel7编码烟草β-1,4-内葡聚糖酶降解植物细胞壁，在RKN与CN取食细胞中强烈诱导表达[69]。上述研究表明，线虫侵染后取食细胞中AX的局部与瞬时积累促进了线虫NFS的建立与线虫寄生。

AX对线虫R/S的影响通过AX响应因子ARFs来实现，ARFs能够激活或抑制AX响应基因的表达[70]。BCN侵染拟南芥后ARFs基因家族表现出明显的差异表达，AX积累和ARFs表达在NFS起始与早期发育中瞬间增加[68]，成熟合胞体和AX诱导的成熟根结中ARFs持续高量表达[71]，说明AX和ARFs在成熟NFS中发挥重要作用[72]。ARFs下游的AX响应基因LBD16受RKN侵染后激活，暗示其在根结和侧根中诱导表达，从而建立了根结形成与侧根发育间的分子联系[72]。ARFs是一些小RNAs和干扰RNAs的直接调控靶标，ARFs对于NFS的生长发育具有明显的促进作用。NFS的启动与形态建成依赖于AX，BCN侵染后ARFs下游的AtWRKY23在早期的合胞体发育中诱导表达，但与AX无关[73]，表明其他一些信号分子参与调控植物对线虫早期侵染的应答。AX通常与ET协同互作，但ET介导的线虫敏感性与AX无关[61-62]，这种侵染和非侵染植株信号通路中AX依赖性的不一致，说明线虫分泌的效应子可能通过植物AX信号调控植物响应[66]，线虫分泌物中AX类物质也可能在植物对线虫的R/S中发挥调控作用[6-7]。

3　植物-线虫互作中的ROS及信号传导

植物在光合作用与呼吸作用中通常会产生ROS，ROS是含氧的化学分子，包括单线态氧(singlet oxygen, 1O2)、超氧化物(superoxide, O2-)、过氧化氢(hydrogen peroxide, H2O2)和羟基自由基(hydroxyl radical, ·OH)。ROS的产生与清除机制竞争性协调使体内ROS水平保持相对稳定，ROS的过量积累通常会导致脂类、蛋白质和DNA等的氧化，进而引起细胞坏死；植物遭受病原物侵染后，体内ROS含量迅速增加引起氧化迸发，导致局部细胞坏死[74]。病原侵染后局部迸发的ROS能够通过细胞间的传输系统传递，也可以和其他信号传导通路结合产生SAR反应。ROS的产生通常与植物防卫反应有关，质外体中ROS的快速积累往往会导致HR类细胞坏死，从而限制了病斑的进一步蔓延，引起抗病反应[75]。

RKN能够侵入抗、感番茄的根系中，但在侵染后48 h，携带Mi-1的抗线虫番茄根系中的RKN侵入数目显著少于感病番茄[76]。线虫侵染后12 h，在亲和与非亲和互作的根系侵染部位均检测到了氧化迸发，但是在非亲和反应(携带Mi-1的抗线虫番茄)中，氧化迸发持续延长至侵染后48 h，同时出现明显的细胞坏死[76]。NADPH氧化酶是植物与病原非亲和反应中ROS产生的主要来源，通过亚细胞定位在非亲和反应的HR中检测到了H2O2[76]。RKN侵染后ROS迅速积累，可作为监控细胞代谢变化最灵敏的信号之一，ROS积累的时空差异对于确定RKN促使寄主植物的发病进程至关重要。质外体中ROS的快速积累与植物抗病性有关[74-75]，编码ROS清除酶(如过氧化物酶B)的RKN基因在线虫寄生阶段大量转录，保护RKN免受寄主植物氧化损伤，将这些RKN基因敲除导致RKN寄生数目减少[77]。最新研究表明，ROS负调控细胞坏死与拟南芥BCN抗性，RbohD和RbohF是ROS产生中必需的编码NADPH氧化酶的2个基因，RbohD和RbohF缺失突变体在BCN侵染24 h后BCN寄生数目减少，合胞体体积减小，细胞坏死增多[78]。此外，RbohD和RbohF缺失突变体中细胞坏死的抑制与SA的积累无关，RbohD/RbohF双突变体中SA响应基因诱导表达，而过表达RbohD的转基因植株中SA响应基因的表达受到抑制，表明SA与ROS相互拮抗[78]。新发现的ROS能够抑制细胞死亡和促进BCN寄生，表明HR类细胞坏死的激活可能存在其他未知的信号传导机理[79]，这进一步说明ROS在植物对线虫的R/S中具有不同的作用。

4　sRNAs在植物-线虫互作中发挥调控作用

sRNAs(20-24nt)是在表观遗传、转录、转录后以及翻译水平对植物防卫反应具有重要调控作用的小分子物质，植物sRNAs主要包括小RNAs(miRNAs)和短干扰RNAs(siRNAs)[80]。miRNAs和siRNAs源于通过DICER类蛋白对双链RNA前体的加工，产生的miRNAs和siRNAs装入AGO蛋白形成RNA诱导沉默复合体，该复合体可与靶RNAs和DNAs结合[81]。植物miRNAs和siRNAs在生物胁迫中发挥重要作用，miRNAs和siRNAs调控参与重要生物过程的基因表达，如ROS的产生及其信号传导[82]、激素信号传导[83]以及PTI和ETI[80]等。

sRNAs在病程发生的调控网络体系中处于核心地位。RKN侵染番茄与水稻根系后，与miRNAs、siRNAs合成和生物功能相关蛋白的编码基因，包括DCLs、AGOs和RDRs，编码DNA甲基化酶的基因以及组蛋白甲基化和脱乙酰的相关基因表现差异表达[48,84]，DNA、组蛋白甲基化和乙酰化是介导植物表观遗传基因表达的重要调控机制[85]，说明miRNAs和siRNAs的生物合成及其功能在植物应答线虫胁迫中发挥重要作用。利用拟南芥单、双和三突变体检测到了SCN反应，检测到的基因包括DCLs、RDRs以及参与合成miRNAs和siRNAs的多种异构体，产生sRNAs的基因突变与野生型相比均降低了SCN敏感性[86]。差异表达miRNAs和siRNAs的预测靶标表明sRNAs在植物线虫病害发生中具有特定作用。R蛋白、ARFs、热激蛋白(heat shock proteins, HSP)和Cu/Zn超氧化物歧化酶的编码基因，以及各类转录因子均可作为一个或多个差异表达miRNAs和siRNAs的调控靶标。拟南芥miR396在SCN侵染4 d后下调表达而7 d后上调表达，miR396靶标生长调控因子(growth regulating factors, GRF)的表达则在SCN侵染后表现出与miR396相反的变化趋势[86]。拟南芥GRF缺失突变体和过表达miR396的转基因植株均降低了SCN感病性，过表达miR396的拟南芥根系中合胞体与SCN的侵染数目均减少，miR396结合位点缺失突变体中同样检测到了类似的特征[87]。GRF基因家族在细胞增殖与细胞体积变化中发挥正调控作用，miR396及其靶标基因GRF对于SCN侵染的合胞体的发育至关重要。此外，合胞体中差异表达的近半数基因与拟南芥GRF缺失和miR396抗性突变体中差异表达的基因相同，表明在SCN诱导的合胞体中，miR396/GRF是基因表达重编程必不可少的调控体系[87]。棉花(Gossypiumhirsutum)受肾形线虫(Rotylenchulusreniformis, reniform nematodes, RN)侵染后sRNAs的表达发生改变，一些miRNAs和siRNAs，如miR396和miR482在对RN存在抗、感差异的不同棉花基因型中表现出不同的表达模式。sRNAs的靶标基因源于差异表达的sRNAs，包括植物免疫、激素信号、ROS的产生及信号传导、sRNAs生物合成及其功能以及表观遗传调控基因，这进一步说明sRNAs对上述信号通路具有调控作用。

一些NBS-LRR基因能够从其mRNA转录本中逐级产生成簇的次生siRNAs，次生siRNAs的产生必需miRNA靶标[88-90]。此外，一些次生siRNAs能够将其他一些防卫基因作为靶标[89]，其余的siRNAs则参与了根系发育的AX信号调控[91-92]。NBS-LRR类蛋白与AX信号在植物对线虫的R/S中具有明显作用，推测miRNA/siRNA信号可能在整合线虫信号系统中发挥重要作用。棉花sRNAs调控网络涉及RN信号传导，预测对RN响应的miR482家族靶向NBS-LRR蛋白的编码mRNA可以裂解为一族次生siRNAs，这些siRNAs同样会将一系列的转录因子以及其他蛋白作为靶标，其中许多靶标是参与信号传导的致病相关基因，从而为sRNA调控网络通过产生次生siRNAs、编码miRNAs和NBS-LRR蛋白的基因参与棉花和RN互作提供了初步证据，这在其他病原侵染的植物免疫反应中已有过详细的研究报道[88-89,93]。上述研究表明，miRNA通过形成次生siRNAs调控NBS-LRR的基因表达，从而在植物线虫病害发生中发挥重要作用，但有关这一调控网络的确切作用目前尚不明晰。寄主植物能够进行自主防卫，可能通过下调特定miRNAs的表达，进而引起参与线虫抗性R基因的表达发生改变。通过sRNA抑制NBS-LRR的基因表达可作为植物自身的保护机制，这是因为NBS-LRR转录及其蛋白水平的增加能够引发植物HR或细胞坏死[94]。线虫分泌的特异效应子也可能通过诱导sRNA调控网络，抑制了NBS-LRR的基因表达，促进了线虫的寄生，可能是由于植物与线虫间的sRNAs传递抑制了线虫致病性及其发育必需的基因表达[95-96]，线虫分泌的效应RNAs启动了植物sRNA调控网络。

5　小结

植物R蛋白识别线虫分泌的效应物引发了植物线虫抗性，植物激素不仅在R基因介导的线虫抗性中发挥重要作用，而且在植物基础防卫反应中具有促进作用，每一种激素在特定的植物-线虫互作中具有不同的作用，ROS在R基因介导的非亲和互作的线虫寄生中发挥关键性作用，ROS的局部迸发与R基因介导的线虫抗性中的HR间存在着必然联系。可见，各种不同的信号分子在调控网络体系中彼此间协同作用，并非独立发挥其功能。线虫效应子与植物因子间的互作影响信号网络的调控行为，在植物应答线虫胁迫中同样发挥重要作用。sRNAs是病原抗性的重要调控子，参与了植物防卫反应中关键节点基因的调控，sRNAs可能在植物对线虫R/S决定中处于核心地位，但仍需通过研究进一步揭示和证实sRNAs在不同植物-线虫互作中发挥的具体作用。高通量二代测序技术与网络分析策略的应用，不仅有助于发现植物对线虫R/S中的关键信号通路，而且对于揭示信号通路间的交互对话机制与信号通路整合也将发挥重要作用。

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Research progress on signal transduction and regulation mechanisms in plant-nematode interactions

YE De-You1*, QI Yong-Hong2, LI Min-Quan3

1.Institute of Vegetables, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China; 2.Institute of Plant Protection, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China; 3.Gansu Academy of Agricultural Sciences, Lanzhou 730070, China

Plant parasitic nematodes pose a serious threat to agricultural production and result in significant economic losses in crops worldwide. A key factor in crop production is plant resistance or susceptibility to nematodes; therefore, this has been an important subject for researchers in the areas of crop genetics and breeding. Understanding the mechanisms of plant resistance or susceptibility to nematodes is of great theoretical significance and practical value to guide the breeding of nematode-resistant crops. In this paper, the mechanisms underlying plant resistance or susceptibility to nematodes are reviewed, including specific plant resistance genes or proteins, plant hormone synthesis and signaling pathways, and reactive oxygen signals that are generated in response to nematode attack. In recent years, many researchers have suggested that plant resistance or susceptibility to invading nematodes and nematode-secreted effectors is mainly determined by the coordination of different signaling pathways. Many studies have shown that crosstalk among various nematode resistance-related elements represents an integrated signaling network regulated by transcription factors and small RNAs at the transcriptional, posttranscriptional, and translational levels. Ultimately, the outcome of this highly controlled signaling network determines the resistance or susceptibility of the host plant to nematodes. These above-mentioned results lay the foundation for further research on the signal transduction and regulation mechanisms involved in the plant-nematode interaction, and thus, provide a theoretical basis for the development of new strategies to prevent and control plant nematodes.

nematodes; resistance genes; hormones; reactive oxygen species; small-RNA

10.11686/cyxb2015574

2015-12-23；改回日期：2016-01-27

国家自然科学基金项目(31560506)，农业部西北地区蔬菜科学观测实验站项目(2015-A2621-620321-G1203-066)，国家公益性行业(农业)科研专项(201503112-4)和甘肃省设施园艺作物高效栽培创新团队项目(2014GAAS02)资助。

叶德友(1972-)，男，甘肃民勤人，副研究员，博士。E-mail：ydy287@163.com

Corresponding author. E-mail：ydy287@163.com

http://cyxb.lzu.edu.cn

叶德友, 漆永红, 李敏权. 植物与线虫互作的信号传导及调控机制研究进展. 草业学报, 2016, 25(10): 191-201.

YE De-You, QI Yong-Hong, LI Min-Quan. Research progress on signal transduction and regulation mechanisms in plant-nematode interactions. Acta Prataculturae Sinica, 2016, 25(10): 191-201.