F-box蛋白家族在植物抗逆响应中的作用机制*

贾 琪, 孙 松, 孙天昊, 林文雄



F-box蛋白家族在植物抗逆响应中的作用机制*

贾 琪, 孙 松, 孙天昊, 林文雄**

(福建农林大学作物科学学院/作物遗传育种与综合利用教育部重点实验室/作物生态与分子生理学福建省高校重点实验室 福州 350002)

SCF复合体泛素连接酶E3介导的泛素化蛋白降解是翻译后水平上对生命进程进行调控的一个重要方式。它的关键组分F-box蛋白负责识别被降解的靶底物蛋白。植物F-box基因家族成员众多, 极具多样性。F-box蛋白N端常含F-box基序, C端常为蛋白互作保守结构域, 该结构具多样性, 可识别不同底物, 是F-box蛋白分类的依据。研究表明, F-box蛋白参与调控植物的许多生命进程, 包括抗逆反应。本文就近年来F-box蛋白在植物抗逆反应中的作用机制进行总结。F-box蛋白大多以SCF复合体泛素连接酶E3介导的泛素化蛋白降解目标蛋白的方式调控抗逆反应, 也有不依赖形成SCF复合体的方式行使功能, 不少F-box蛋白参与了植物激素信号传导, 通过调控转录因子活性而改变下游基因的表达, 由此影响了植物的抗逆反应。基因表达谱的生物信息学预测表明, 大多数F-box基因参与了植物抗逆反应, 目前只有其中一小部分已报道了其抗逆调节功能。在此综述了这些F-box蛋白在植物抗逆胁迫中的研究进展。在干旱和盐碱胁迫反应中, F-box基因常通过影响植物激素脱落酸、乙烯等植物激素信号传导而调控抗逆。由于干旱和盐碱胁迫具协同性, 不少F-box基因同时参与抗旱和抗盐碱胁迫, 但调节方式有所不同, 一些F-box基因对抗干旱和盐碱的反应具协同性, 从总体上调控植物的渗透胁迫和离子毒害反应; 而另一些F-box基因对干旱和盐胁迫反应的调节作用相反, 它们可能在植物抗逆的精细调节中起作用。在低温胁迫反应中, F-box蛋白可调节植物抗低温的CBF信号途径。在生物胁迫反应中, F-box基因常通过影响植物激素茉莉酸和水杨酸途径来调控抗病, 病原菌也以攻击植物SCF复合体使植物致病。此外, 植物激素信号途径之间相互作用, 共同影响抗逆反应。

F-box蛋白家族; SCF复合体; 植物; 环境胁迫; 抗逆反应

环境胁迫对植物生长发育影响很大, 是危害作物产量的重要因素。环境胁迫主要包括水胁迫、盐碱胁迫、温度胁迫和重金属毒害胁迫等的非生物胁迫和病虫害侵染等生物胁迫。在长期进化过程中, 植物已进化出多种调节机制来响应环境胁迫, 其中, 泛素介导的蛋白质降解系统(ubiquitin proteasome system, UPS)就是一个重要的生物调节体系。UPS通过调节功能蛋白或调节因子的丰度, 从而调控生物体的生命进程, 包括生长发育及对逆境胁迫的响应[1–3]。UPS的调节方式属于翻译后调控, 泛素共价修饰标记目标蛋白, 再通过26S蛋白酶体催化降解。UPS主要包括3种酶: 泛素活化酶E1(ubiquitin activating enzyme)、泛素结合酶E2(ubiquitin conjugating enzyme)和泛素连接酶E3(ubiquitin ligase)。泛素连接酶E3负责识别底物特异性, 是UPS中种类最多的一类酶, 目前发现的有7种类型, 包括2类单亚基亚类及5类多亚基亚类[4]。单亚基亚类根据其所含结构域的不同分为HECT (homology to E6-AP C-terminus)、RING(really interesting new gene)/U-box两类, 而多亚基CRLs亚类分为SCF (SKP1-Cullin1-F-box)、VHL-ELONGIN-CUL2/5、BTB- CUL3 (Bric a brac, Tramtrack and broad complex/Pox virus-Cullin3)、DDB-CUL4(UV-damaged DNA-binding protein1-Cullin4)和APC(anaphase promoting complex)5类。SCF复合体是E3连接酶中最大的一类, 结构如图1所示, 由SKP1(S phase kinase-associated protein 1)/ASK1 (Arabidopsis SKP1 like 1, 拟南芥SKP1同源物)、CUL1 (Cullin1)、F-box蛋白(FBX)和RBX1(Ring- box 1)组成, 其中RBX1、CUL1和SKP1组成复合物骨架, RBX1结合泛素结合酶E2, SKP1结合F-box蛋白。泛素结合酶E2负责提供修饰底物的泛素。F-box蛋白负责底物结合特异性, SCF复合体通过替换不同的F-box蛋白来决定UPS降解的目标底物[5]。

SCF复合体由SKP1、CUL1、RBX1和F-box蛋白组成, 介导了靶蛋白的泛素化降解。泛素活化酶E1在ATP供能时, 活化泛素, 转移泛素到泛素结合酶E2上, SCF复合体利用泛素结合酶E2上的泛素，对底物蛋白进行泛素化标记, 泛素化的蛋白底物被26S蛋白酶体识别并降解。

F-box蛋白家族成员众多, 生物功能极具多样性。到目前为止, 已有诸多报道表明不少F-box蛋白在调节植物生命进程中起了关键作用, 包括植物生长发育与植物生理的诸多方面, 如激素信号转导、光信号传导、生物钟调节、侧根形成、分枝、衰老、花发育、自交不亲和等生长发育过程及植物对外界生物和非生物胁迫的应答过程[6–10]。虽然生物信息学预测了不少F-box基因参与植物抗逆反应, 但对其进行深入功能研究的并不多。本文对近年来关于F-box蛋白参与逆境胁迫的研究进展加以综述, 探讨其蛋白结构及作用机理, 为今后深入探究植物F-box蛋白调控抗逆反应提供参考。

图1 SCF复合体介导的蛋白泛素化降解

1 植物F-box蛋白的进化与结构

F-box蛋白(FBX)由在细胞周期蛋白Cyclin F中发现的一个新的蛋白结构域而得名[11], 它广泛存在于真核生物中, 不同物种中的F-box基因(FBX)数量差距很大[12], 出芽酵母中含有14个F-box基因, 人有38个F-box基因, 果蝇有24个F-box基因, 线虫有337个F-box基因。在大多数的植物中, F-box基因家族成员众多且变异度很大[13]。从全基因组水平系统研究F-box基因的报告表明, 在拟南芥()、水稻()、玉米()、大豆()、鹰嘴豆()、苜蓿()、苹果()和梨(spp.)中, 分别含有694、687、359、509、285、972、517和226个F-box基因[14-21]。有研究表明一年生草本植物的F-box基因家族数目扩增度比多年生木本植物大[22], 而随后的一项研究更大范围分析了18种植物的F-box基因家族, 认为植物F-box基因家族数目扩增度与植物种类、进化度、基因组大小及复杂度等都没有统一的相关性[13]。目前普遍认为造成植物F-box基因数目众多的主要因素为基因重复事件。在长期进化过程中, 植物为适应环境, 重复基因会产生变异, 也有可能消失。这可能使在亲缘关系相近的植物之间, F-box基因数目存在差异。植物F-box基因的染色体分布及基因重复情况分析表明, F-box基因通常分布于每一条染色体的两臂中, 但其分布并不均一, C末端含同一保守区的亚家族基因常在基因组中聚集分布, 可能起源于始祖基因的串联复制重复(tandem duplications)或片段复制(segmental duplications)。F-box基因重复的情况在各植物中的偏好度并不一致[22-23], 例如拟南芥、水稻、蒺藜苜蓿()中主要为串联复制重复为主, 大豆中主要以片段复制为主。同源性高的F-box基因极有可能来源于共同祖先基因的重复, 他们常聚集存在于基因组中, 他们可能会识别同一种类型的底物, 存在功能冗余, 或一起协同调控某一生命进程。

F-box蛋白结构包含N端与SKP1结合的F-box基序和C端与目标底物结合的蛋白结合序列(图1)。F-box蛋白通常只含有一个F-box基序(PF00646, http://pfam.xfam.org/), 一般由40~60个氨基酸组成。FBX基序在不同物种中结构相对保守, 而F-box蛋白C端的底物结合域的变异度很大, 通常是F-box蛋白亚家族分类的依据[24-25]。植物F-box蛋白C端保守区有目前已知的典型蛋白之间互作结构域, 也有未知结构域。出现频率比较高的已知结构域有LRR(富含亮氨酸重复序列域)、Kelch、FBA、FBD、WD40等[22,26-27]。在不少植物中, 超过半数的F-box蛋白C末端为未知结构域, 而这些未知结构域有可能在该物种甚至在植物中都保守。例如, 对大豆含未知结构域的F-box蛋白序列进行比对分析, 发现了39个保守区, 它们有些是豆科植物所专有, 有些是在植物中普遍存在, 说明这些未知保守结构域可能在调节生物体某一生命进程中起作用, 其功能及作用机制尚待进一步探究[14]。有意思的是, F-box蛋白N端的F-box基序和C端的蛋白互作结合域可能存在同步进化的现象[14,21,24]。以大豆F-box蛋白为例, 单以F-box结构域序列比对, 建立系统进化树, 含相同C端保守结构域的F-box蛋白常会聚集在一个分支, 且同一进化枝的基因也常具有类似的结构, 含有相同数目的内含子, 说明同一进化枝的基因很可能起源于同一祖先, F-box蛋白N端的F-box基序和C端的蛋白互作结合域可能存在同步进化的现象[14]。

2 植物F-box蛋白参与抗逆的作用机理

2.1 F-box蛋白的作用机制概况

目前为止, 已报道的大部分F-box蛋白主要是通过形成SCF复合体参与泛素介导蛋白降解途径行使生物功能, 如图1所示, 8.5 kD的小分子多肽泛素广泛存在于生物体中, 在ATP供能时, 泛素活化酶E1与泛素结合, 形成复合物, 并将泛素活化和转移到泛素结合酶E2上, 再经SCF型的泛素连接酶E3作用, 将多个泛素逐步转移到目标底物上, 使目标底物被26S蛋白酶体识别, 最终被降解成多肽和单体泛素。而少数FBX蛋白亦可通过非SCF复合体形式行使功能[28-30], 它们可能仍依赖F-box基序与SKP1蛋白结合形成复合体, 但不形成SCF复合体行使功能, 或是不依赖F-box基序与SKP1蛋白结合而独自行使功能, 这种作用模式在酵母、果蝇、老鼠和人等中均有发现, 植物中鲜见此类报道。例如, 拟南芥F-box蛋白AFBA1经酵母双杂筛选得其互作蛋白MYB44, 虽MYB44受蛋白水解酶水解调控, 但在过表达AFBA1的原生质体中, MYB44的降解是受抑制的, 说明AFBA1其互作蛋白MYB44的结合并不介导MYB44泛素化降解, 反而促进了MYB44的稳定, 但其具体作用机制仍然未知。

2.2 F-box蛋白参与抗逆反应的作用机制

F-box蛋白常通过形成SCF复合体介导泛素化降解逆境相关蛋白的机制调控植物逆境反应, 这些抗逆相关蛋白可能为正调节蛋白或负调节蛋白。在正常条件下, F-box蛋白识别并泛素化抗逆反应正调节蛋白, 使正调节蛋白降解, 而负调节蛋白处于活性状态, 抗逆反应关闭。而在逆境条件下, 诱导降解抗逆反应负调节蛋白的F-box蛋白表达, 解除抗逆反应的抑制, 启动抗逆反应; 或降解抗逆反应中正调节蛋白的F-box蛋白不再表达, 正调节蛋白不被降解, 从而激发抗逆反应。植物受到环境胁迫后, 会诱导参与抗逆反应的功能基因高表达, 产生大量抗逆功能蛋白, 在胁迫解除后, 通过F-box蛋白识别并介导它们泛素化降解, 使抗逆的功能蛋白恢复到正常状态。F-box蛋白自身的表达与活性也受到调控, 有些受到泛素化降解调控, 有些可以通过miRNA降解其靶基因的mRNA来抑制活性, 从而影响植物抗逆反应[31-33]。miR394a/b是保守的小RNA, 它们可抑制F-box蛋白LCR(leaf curing responsiveness)的表达, 通过影响ABA途径, 调控植物抗旱、抗盐性。参与植物抗逆反应的调节蛋白包括调控基因表达的转录因子、参与信号传导途径中的成员等。转录因子通常可以调控一系列相关基因表达, 对转录因子稳定性的调控, 可间接调控参与抗逆反应的一系列基因的表达, 从而调控抗逆反应。植物激素是植物内源的信号小分子, 主要包括生长素(auxin)、茉莉酸(jasmonate, JA)、水杨酸(salicylic acid, SA)、赤霉素(gibberellin, GA)、细胞分裂素(cytokinins, CK)、乙烯(ethylene, ET)、脱落酸(abscisic acid, ABA)、芸苔素(brassinosteroids, BR)和独角金内酯(strigolactone, SL), 激素信号传导不但对植物生长发育作用重要, 也常常参与植物的抗逆反应[34]。各激素信号通路往往参与了多种抗逆反应, 如ABA信号传导途径常参与植物对非生物环境胁迫的应答, 如干旱、盐、温度胁迫和损伤等, 而各激素信号通路之间也常有交叉作用, 相互影响, 共同作用于某一逆境反应, 如SA、JA、ET信号传导途径常参与植物抗生物胁迫应答[35], 生长素不但调控植物生长, 在植物抗病及抗非生物胁迫中也起作用[36-37]。这些主要的植物激素途径中, 都发现有F-box蛋白直接参与或间接影响了其信号传导[29,38]。在激素信号传导途径起关键作用的F-box蛋白信息总结在表1, 其中不少激素的受体蛋白都是F-box蛋白, 他们受激素的调节, 进一步通过降解目标底物去调控生物进程[6]。生长素受体TIR1和AFB1-5都是F-box蛋白, 他们识别生长素形成SCFTIR1/AFB1-5复合物, 介导负调控蛋白AUX/IAA的泛素化降解, 使生长素特异的转录因子ARFs解除阻遏, 从而诱导生长素传导途径基因表达[39-41]。与此类似的还有茉莉酸受体COI1、与赤霉素受体GID1结合的SLY1/SNE、与独角金内酯的受体D14结合的MAX2/DWARF3都是F-box蛋白, 它们如同一个分子连接胶, 胶合了传导信号的激素小分子(或其与蛋白的复合物)与传导途径的调节蛋白, 通过泛素化降解调节蛋白调控信号传导途径。

表1 参与植物激素信号传导的F-box蛋白

“?”表示酵母双杂交找到的互作底物蛋白, 未有介导26S蛋白水解酶降解的证据。“?”: the substrates had been identified by yeast two hybrid, but no evidence supported that they would be degraded by 26S proteasome.

3 F-box蛋白与非生物胁迫

在水稻、玉米、苜蓿、大豆和苹果等植物中, 在全基因组水平上研究F-box蛋白基因家族的报道表明, F-box蛋白基因家族成员广泛参与到植物非生物胁迫的抗逆性反应中[14,16,19,21,23,80]。不少已克隆的植物F-box基因功能研究表明它们也参与了抗逆反应。目前关于F-box蛋白参与植物抗逆的报道大多都集中在抗干旱和盐碱胁迫方面, 也有一些关于抗温度胁迫方面, 参与其他非生物胁迫反应的证据较少, 如重金属胁迫等, 这些研究主要来自对基因文库或基因表达转录组的分析研究, 其具体的作用机制尚不明确[8], 在此不再深入讨论。

3.1 F-box蛋白与干旱、盐碱胁迫

干旱和盐碱胁迫是全球影响农业生产的重要环境胁迫因子。干旱导致植物缺水, 影响植物一系列生理进程, 细胞膜结构破坏, 光合作用减弱, 正常代谢受阻, 最终影响植物的生长和发育。在干旱、半干旱及沿海地区又常见土壤盐碱化现象, 盐碱化对植物有渗透胁迫和离子毒害, 早期渗透胁迫使植物水分外渗, 造成生理干旱, 影响植物新芽发育, 而晚期离子进入植物体内, 造成离子毒害, 使细胞内离子失衡, 造成质膜伤害和代谢混乱, 加速植物老叶及整体死亡[81]。

3.1.1 F-box蛋白参与干旱、盐碱胁迫的机制

研究表明植物激素ABA、ET等广泛参与了植物抗逆反应, 不少参与植物抗旱或抗盐碱反应的F-box基因也通过直接或间接影响植物激素信号传导途径而影响植物的抗旱及抗盐碱性, 尤其是ABA信号途径。参与ABA信号途径的F-box蛋白AFBA1正调控植物抗旱反应, 在缺失突变体中, 气孔闭合受阻, 水分损失率提高, 对干旱敏感, 而在过表达突变体AFBA1-OX中, 受ABA信号影响气孔更快关闭, 抗旱能力增强[74]。F-box蛋白DOR可能参与ABA生物合成, 影响气孔开闭, 进而负调控植物的抗旱性[70]。F-box蛋白RIFP1降解ABA受体RCAR3, 负向调控ABA信号传导, 在缺失突变体中, ABA通路的效应基因、、和的表达都有所提高, 且抗旱性增强[66]。F-box蛋白EBF1/2介导降解乙烯途径正调节蛋白EIN3/EIL1。高盐胁迫会诱导EBF1/2降解, 造成EIN3/EIL1积累, 促进乙烯途径, 此过程并不依赖EIN2调控[80]。进一步研究发现, 虽然EIN2和EIN3并不调控参与抗盐SOS途径基因、、的表达, 但SOS2可以激活EIN3的一个作用靶基因表达[81]。而外源预处理乙烯则提高植物抗盐性, 这都说明乙烯途径也调节了植物抗盐反应[82-83]。此外, 关于参与独角金内酯途径的MAX2、茉莉酸途径的苹果MdJAZ22及生长素途径的mTIR1的研究报道都表明这些激素途径可能也直接或间接影响了抗旱或抗盐碱反应[33,84-85]。MAX2是个多功能蛋白, 它参与光形态建成和逆境胁迫的反应, 其缺失突变体对干旱和盐胁迫都敏感[84,86]。在干旱胁迫后, 采用qRT-PCR分析野生型和突变体的抗性相关基因及参与ABA途径基因表达变化, 发现突变体的抗性相关基因、、、和表达受损, 参与ABA途径基因如、等的表达也受损, 暗示的突变可能是因为影响了植物ABA途径, 而导致植物抗旱性下降。通过对突变体与对ABA非敏感的突变体和分别杂交后遗传分析, 发现突变体不能回复和的表型, 可能在这些基因的上游起作用[86]。是独角金内酯信号途径的重要基因, 在独角金内酯合成后的下游途径起作用。这项研究也同时检测了参与独角金内酯合成的和对干旱胁迫反应的影响认为对抗旱的调节机制与和关系不大。而同期的另一项研究则发现突变体和对干旱和盐胁迫也敏感, 在补充外源独角金内酯后, 则抗性有所恢复, 而在补充外源独角金内酯后的抗性变化不大, 认为独角金内酯途径影响了植物抗旱性和抗盐性[84]。但如何调控植物干旱胁迫及盐胁迫反应的分子机制却并不明晰。酵母双杂试验表明MdJAZ22是JA受体F-box蛋白MdCOI1的一个互作蛋白, 过表达的转基因拟南芥植株对盐处理和PEG处理更耐受, 预示JA途径与植物干旱和盐胁迫反应相关[85]。植物miR393能使编码生长素受体的F-box基因、和沉默, 不被miR393沉默的TIR1异构体记作mTIR1(miR393-resistant TIR1), 过表达的转基因拟南芥抗盐性提高, 植株的渗透调节能力和钠离子外排能力提高, 这可能与高度激活的生长素信号传导相关[33]。

3.1.2 同时参与抗干旱和盐碱胁迫的F-box蛋白

由于盐碱胁迫在早期也造成了植物的生理干旱胁迫, 干旱地区也常相伴土壤盐碱化, 不少基因同时正调节了植物对干旱和盐碱胁迫的抗逆反应, 也有一些基因对干旱和盐胁迫反应的调节作用相反, 这些基因可能在抗逆的精细调节中起作用。上述的拟南芥缺失突变体对干旱和盐胁迫都敏感[84,86], 过表达苹果同源基因的转基因拟南芥或苹果愈伤组织的抗旱和抗盐能力均有所提高[87]。小麦()F-box基因在烟草()中过表达, 也同时提高了植物的抗旱性和抗盐性[88-91], 过表达的烟草植株受到干旱或盐胁迫后, 其活性氧物质ROS(reactive oxygen species)的积累、MDA含量和膜损伤程度等都较野生型低, 而光合作用速率、抗氧化酶的活性则比野生型高, 在盐胁迫下, 钠钾比率较野生型低。郑成超教授组克隆的F-box基因在植物抗旱和抗盐反应中却作用相反[67,69]。通过F-box基因上游的启动子元件是否含有干旱反应相关的DRE(drought responsive element)元件的生物信息学分析和基因表达的检测, 筛选出一个受干旱诱导显著表达的F-box基因, 在拟南芥中过表达该基因却显著增强了植株对干旱的敏感性, 通过酵母双杂筛选得到其互作底物蛋白AtLEA14, 它属于与植物抗干旱胁迫相关的LEA蛋白家族成员, AtPP2-B11可介导AtLEA14降解, 同时也在转录水平抑制基因表达, 说明AtPP2-B11是抗干旱胁迫的负调控蛋白[69]。的表达亦受到盐胁迫诱导, 超表达拟南芥抗盐性提高, 而反义RNA干扰表达的转基因拟南芥植株则对盐胁迫更加敏感, 过表达抑制了盐胁迫下植物体内ROS积累, 降低了体内钠离子积累, 从而提高了抗盐性, 是植物抗盐的正调控蛋白[67]。最近的一篇报道表明AtPP2-B11介导ABA信号转导途径中的重要调节蛋白SnRK2.3激酶降解, 从而负调控ABA信号转导和抗逆应答反应[68]。

3.2 F-box蛋白与温度胁迫

植物生长需要适宜的温度, 冷害、冻害和热害都会影响植物生理生化的多个方面, 危害植物生长, 或影响有植物经济利用价值物质的积累。近年来, 由于全球污染恶化, 极端温度频繁出现, 常对农业生产造成损失。研究表明F-box家族成员确有参加植物对温度胁迫的抗逆反应, 但目前的研究尚较有限。

F-box蛋白可通过调节植物抗低温的信号途径, 如依赖CBF(C-repeat binding factor)基因的抗冷途径等, 从而调控植物抗冷的生理反应。参与乙烯途径的F-box蛋白EBF1/2除了与EIN3/EIL1互作外, 也能直接与负调节抗冻害胁迫的PIF3(phytochrome- interacting factor 3)互作, 介导PIF3被26S蛋白水解酶水解, 促进植物抗冻。PIF3是一个转录因子, 能与抗冻密切相关的CBF基因启动子结合, 从而抑制一系列CBF基因的表达。相应地,缺失突变体对冷害更加敏感[92]。

基因表达研究表明一些F-box基因表达受温度胁迫改变。分析Affymetrix ATH1芯片数据库发现拟南芥(F-box stress induced 1)受低温和盐胁迫高度诱导, 缺失突变体冻害后的转录组分析表明, FBS1调控了与ABA和JA途径相关的几百个基因的表达, 可能由此影响植株的抗冻性[93]。拟南芥基因受低温或高温诱导, 其酵母同源物YLR097c与蛋白翻译延长因子eEF-2互作, 推测它可能影响温度胁迫后的蛋白合成过程[94]。全基因组分析苜蓿F-box基因, 并通过qRT-PCR证实, 发现一些F-box基因表达受到热胁迫诱导[21]。不少杂草稻品种比栽培水稻对低温更为耐受, 对它们进行冷胁迫处理, 并分析差异表达基因, 发现F-box基因表达受低温诱导[95]。柑橘()耐低温的变种枳()经低温处理后, 发现了8个基因受低温诱导, 其中1个为F-box蛋白基因[96]。辣椒()F-box基因也受冷胁迫诱导[97]。这些研究进展多集中在转录水平上, 而对这些温度胁迫相关的F-box基因的作用机理尚不明晰。

4 F-box蛋白与生物胁迫

生物胁迫是指植物受到病原菌及虫害的侵袭, 植物激素茉莉酸和水杨酸都在植物免疫反应中起重要的调节作用, 表1列出参与了茉莉酸和水杨酸传导途径的F-box蛋白, 它们也直接影响了植物的免疫反应。参与水杨酸途径的F-box蛋白CPR1/ CPR30(constitutive expresser of pathogenesis-related genes 1/constitutive expresser of pathogenesis-related genes 30)是植物抗细菌性病原菌的负调控因子[75-77], 它的底物是两个NB-LRR类的抗病R基因(suppressor of, constitutive 1)和(resistant to2), CPR1/CPR30介导底物泛素化, E4连接酶MUSE3(mutant-enhancing 3)与SCF E3连接酶互作, 协助底物SNC1和RPS2多聚泛素化后降解, 从而抑制了水杨酸的信号传导[98]。基因突变后, 将使植物的免疫反应自激活, 增强了植物抗病性。茉莉酸信号途径参与防御腐生菌及虫害反应, 茉莉酸受体COI1是一个F-box蛋白, 它的作用模式与前面提到的生长素受体TIR1很类似, 它识别茉莉酸的活性形式茉莉酸-异亮氨酸(JA-Ile), 介导茉莉酸途径一系列阻遏蛋白JAZ的降解, 从而激活茉莉酸防御机制, 提高植物对霉菌的抵抗力[44,99]。

除了茉莉酸和水杨酸外, F-box蛋白基因也常通过影响其他一些植物激素如生长素、脱落酸等, 或利用其他作用机制, 调控植物免疫反应。菌鞭毛蛋白相关肽诱导了拟南芥miRNA393的表达, miRNA393降解3个生长素受体F-box基因、和的mRNA, 阻遏了生长素信号传导, 抑制了植物的抗病反应[42]。在大麦()及烟草中发现了与基因激发抗病相关蛋白SGT1, 它可直接结合并活化SCF复合体, 激活生长素和茉莉酸信号传导, 提高植物抗病性[100-102]。最近有报道表明MAX2蛋白也参与了植物细菌病免疫反应, 它可能调节了生长素信号传导, 使气孔闭合, 阻止病原菌入侵[103]。超表达水稻F-box基因的转基因烟草对番茄花叶病毒ToMV和假单胞菌()的抗性增强, 在水杨酸处理或ToMV侵染后,过表达能上调抗病基因表达, 并增强ABA的敏感性[104]。在烟草和番茄()中, F-box蛋白ACIF1 (Avr9/Cf-9-induced F-box 1)调节抗病基因介导的抗病反应, ACIF1能形成SCF复合体, 暗示它可能也是通过泛素化降解底物而调节免疫反应, 对它的拟南芥同源基因表达进行生物信息学预测, 结果表明它调节了茉莉酸和脱落酸途径[105]。拟南芥F-box基因(suppressor of)的缺失突变对霜霉菌()和假单胞菌的抗性增强,调控抗病的机制与水杨酸途径和系统获得性免疫无关[106]。OsDRF1、ACIF1和SON1的作用底物仍未知, 作用机理尚不明确。

在植物进化防御系统的同时, 病原菌也进化了其侵染系统, 比如通过攻击宿主的SCF复合体而使植物感病。甜菜坏死性黄脉病毒致病因子P25与1个含Kelch结构域的F-box蛋白FBK结合, 从而抑制抗病反应, 在烟草叶片瞬时表达这个FBK蛋白则可引起超敏反应, 说明P25通过影响这个FBK蛋白功能而抑制植物的抗病反应, 帮助病毒致病[107]。马铃薯卷叶病毒(palerovirus)和豌豆耳突花叶病毒(enamovirus)的P0蛋白是一个F-box蛋白, 与植物的SCF复合体成员结合, 介导降解AGO1 (ARGOMAUTE1)蛋白, 抑制了宿主的RNA沉默系统, 促进病菌侵染[108-110]。

5 展望

总之, 在大多植物中, F-box蛋白基因家族成员众多, 在不同物种中的数量和种类不尽相同, 可以作为SCF复合体成员识别并介导底物泛素化降解的形式, 或不以SCF复合体的形式, 在植物抗逆境胁迫中起重要作用。鉴于已报道的植物F-box蛋白主要是依赖形成SCF复合体识别并降解底物调控生命进程, 寻找F-box蛋白的互作底物是研究它作用机制的关键。以往研究除了常规基于表型的遗传分析外, 常更多依赖于研究蛋白之间互作的方法, 如酵母双杂、双分子荧光互补(BiFC)、免疫共沉淀、pull down技术等。最近, 谢道昕和闫建斌团队建立了一种利用ASK辅助层析技术, 联合使用镍柱亲和层析、阴离子交换层析和尺寸排阻色谱, 可以高效纯化得到有活性的F-box蛋白, 解决了F-box蛋白纯化的难题[111]。在植物全基因组水平上, 对植物逆境胁迫后的F-box基因表达谱数据分析结果表明不少F-box基因与植物抗逆相关, 但其具体功能与作用机制仍需进一步试验验证。到目前为止, 亦有一些关于参与抗逆反应的F-box基因被克隆及其功能的研究报道, 如生长素受体TIR1、茉莉酸受体COI1、参与独角金内酯途径的MAX2等[6], 它们只占庞大的F-box基因家族的一小部分, 且多集中于植物干旱胁迫、盐胁迫和生物胁迫的研究。植物中含有种类如此多的F-box基因在植物进化中有何意义, 它们通过泛素化介导蛋白降解的翻译后水平上又是如何协同调控植物各种抗逆反应, 一些参与抗逆反应的F-box基因的具体的作用机制也还并不明晰, 如参与抗病反应的OsDRF1、ACIF1和SON1的作用底物还未知[38]等, 这些问题都有待进一步的深入研究。对F-box基因参与植物抗逆的研究也可望向其他胁迫因子方向进一步深入。基于对基因文库和基因表达谱的研究, 发现F-box基因也参与了重金属胁迫, 如镉、铝和汞[8], 但对其机理的研究并不深入, 需要进一步拓展对植物抵抗这些胁迫的认知。当前高速发展了海量数据分析技术, 组学应运而生, 有机结合表型组学、蛋白组学、降解组学、基因组学等, 将有望发掘更多参与抗逆的F-box基因并探究其功能机理。而目前关于F-box蛋白的功能性研究又多集中于模式植物拟南芥、水稻等, F-box基因功能性研究在重要作物中的报道却很有限。鉴于F-box家族成员在拟南芥抵抗逆境胁迫中的重要作用, 预示它们可能在其他植物的抗逆反应中也起着重要的作用, 需要我们进一步探索, 这对筛选新的作物抗逆遗传标记、培育新的作物抗逆品种和提高农业生产都具有重要意义。

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Mechanism of F-box protein family in plant resistance response to environmental stress*

JIA Qi, SUN Song, SUN Tianhao, LIN Wenxiong**

(College of Crop Sciences, Fujian Agriculture and Forestry University / Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Crop Utilization / Key Laboratory of Crop Ecology and Molecular Physiology (Fujian Province University), Fuzhou 350002, China)

The UPS (ubiquitin proteasome system) mediated by SCF type E3 ubiquitin-ligase is an important mechanism to regulate biological progress at post-translation level. F-box protein, as a key component in SCF complex, could recognize its target protein for degradation. F-box gene family contains numerous members with vast diversity. In general, F-box protein contains F-box motif at N terminus and conserved domain of protein-protein interaction for recognizing target at C terminus. Due to vast diversity of conserved C terminus domains, F-box proteins could recognize wide varieties of targets. Also based on C terminal domains, F-box proteins could be divided into several subfamilies. It showed that plant F-box proteins were involved in many life processes, including response to environmental stress. Here, we reviewed current knowledge of plant F-box proteins in responding to stress. Most of the reported F-box proteins had been shown to function via SCF-dependent protein degradation, with few using SCF-independent mechanisms. Some well-understood F-box proteins were involved in phytohormone signaling pathways. Some reacted to stress through regulating the activity of transcription factors, which influenced expression of downstream genes responding to stress. Bioinformatics analyses of transcriptome showed that many predicted F-box genes were involved in stress-response reactions. Among these, only a few studies had dealt with the functions. The knowledge on the functions under environmental stress was summarized in this study. For drought, salinity and alkality stresses, F-box genes often regulated abscisic acid or ethylene signal pathways. Since drought and salt-alkaline stresses often occurred concomitantly, quite a few F-box genes had been identified to be involved in the response to both stresses in different ways. Some regulated the response to osmotic stress and ionic stress synergistically. However, some functioned inversely, suggesting that they played a role in fine regulations. For cold stress, F-box genes regulated CBF signal pathways. For biotic stress, F-box genes always regulated jasmonate and salicylic acid pathways. Meanwhile, pathogens attacked plant SCF complex for infection. Moreover, phytohormones had crosstalk to coordinate resistance in plants.

F-box protein; SCF complex; Plant; Environment stress; Response to stress

, E-mail: wenxiong181@163.com

Dec. 15, 2017;

Apr. 20, 2018

Q945; Q948.1; Q37

A

1671-3990(2018)08-1125-12

10.13930/j.cnki.cjea.171170

* 中国博士后科学基金(2014T70603)、教育部留学归国人员科研启动基金(教育司留[2013]1792)和国家自然科学基金青年科学基金项目(31501232)资助

林文雄, 研究方向为植物生理与分子生态学。E-mail: wenxiong181@163.com 贾琪, 研究方向为植物抗逆性与分子遗传学。E-mail: jiaqi@fafu.edu.cn

2017-12-15

2018-04-20

* This study was supported by the China Postdoctoral Science Foundation (2014T70603), the Scientific Research Starting Foundation for the Returned Overseas Chinese Scholars, Ministry of Education of China (Education Department Liu[2013]1792) and the National Natural Sciences Foundation of China (31501232).

贾琪, 孙松, 孙天昊, 林文雄. F-box蛋白家族在植物抗逆响应中的作用机制[J]. 中国生态农业学报, 2018, 26(8): 1125-1136

JIA Q, SUN S, SUN T H, LIN W X. Mechanism of F-box protein family in plant resistance response to environmental stress[J]. Chinese Journal of Eco-Agriculture, 2018, 26(8): 1125-1136