2024, Vol. 40
表1(Table 1)
BTB蛋白泛素化介导植物发育和逆境应答的研究进展
http://dx.doi.org/10.13345/j.cjb.230213
中国科学院微生物研究所、中国微生物学会主办
中国科学院微生物研究所、中国微生物学会主办
文章信息
- 吕彤彤, 颜文慧, 梁艳, 丁寅, 颜庆霞, 李金华
- LÜ Tongtong, YAN Wenhui, LIANG Yan, DING Yin, YAN Qingxia, LI Jinhua
- BTB蛋白泛素化介导植物发育和逆境应答的研究进展
- Advances on BTB protein ubiquitination mediated plant development and stress response
- 生物工程学报, 2024, 40(1): 63-80
- Chinese Journal of Biotechnology, 2024, 40(1): 63-80
- 10.13345/j.cjb.230213
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文章历史
- Received: March 22, 2023
- Accepted: May 15, 2023
- Published: May 17, 2023
引用本文
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吕彤彤, 颜文慧, 梁艳, 丁寅, 颜庆霞, 李金华. BTB蛋白泛素化介导植物发育和逆境应答的研究进展[J]. 生物工程学报, 2024, 40(1): 63-80.
LÜ Tongtong, YAN Wenhui, LIANG Yan, DING Yin, YAN Qingxia, LI Jinhua. Advances on BTB protein ubiquitination mediated plant development and stress response[J]. Chinese Journal of Biotechnology, 2024, 40(1): 63-80.
BTB蛋白泛素化介导植物发育和逆境应答的研究进展
1. 西南大学创新创业学院 含弘学院, 重庆 400715;
2. 西南大学园艺园林学院 长江上游农业生物安全与绿色生产教育部重点实验室, 重庆 400715
2. 西南大学园艺园林学院 长江上游农业生物安全与绿色生产教育部重点实验室, 重庆 400715
摘要：BTB (broad-complex, tramtrack, and bric-à-brac)结构域是在真核生物中发现的高度保守的蛋白质相互作用基序。含有BTB结构域的一类蛋白统称为BTB蛋白，它们广泛参与转录调控、蛋白质降解等过程。越来越多的研究表明，该基因在植物生长发育、生物与非生物胁迫等生理过程中具有重要的作用。本文以蛋白结构域为基础，系统总结了该基因家族蛋白在泛素化介导植物发育和逆境应答等过程中的研究进展，为植物中该类基因的研究提供了参考。
关键词：BTB结构域蛋白 蛋白泛素化 植物发育 逆境应答
Advances on BTB protein ubiquitination mediated plant development and stress response
1. Hanhong College, Institute of Innovation & Entrepreneurship, Southwest University, Chongqing 400715, China;
2. Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400715, China
2. Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400715, China
Abstract: The BTB (broad-complex, tramtrack, and bric-à-brac) domain is a highly conserved protein interaction motif in eukaryotes. They are widely involved in transcriptional regulation, protein degradation and other processes. Recently, an increasing number of studies have shown that these genes play important roles in plant growth and development, biotic and abiotic stress processes. Here, we summarize the advances of these proteins ubiquitination-mediated development and abiotic stress responses in plants based on the protein structure, which may facilitate the study of this type of gene in plants.
Keywords:
BTB domain protein protein ubiquitination plant development abiotic stress responses
BTB (broad-complex, tramtrack, and bric-à-brac)结构域(也称为POZ结构域)最初被认为是存在于果蝇中保守的蛋白相互作用基序[1-2]。Laski等[1, 3]发现果蝇转录因子bric-a-brac、tramtrack和broad complex在其编码蛋白N端有1个序列保守的区域，将其命名为BTB结构域。同时，Bardwell和Treisman发现一些痘病毒蛋白与锌指蛋白ZID、GAGA和ZF5的一部分相似，他们将这一区域命名为痘病毒和锌指(pox virus and zinc finger, POZ)结构域[2]。POZ基序与BTB结构域相同，于是统称为BTB/POZ结构域，通常简称为“BTB结构域”。
BTB/POZ家族蛋白存在DNA结合结构域，众多研究证明其可能参与调节基因表达。一方面，有些蛋白质只由BTB组成，比如Skp1和ElonginC，Skp1参与蛋白质降解，ElonginC控制转录延伸[4]；另一方面，BTB结构域也与其他结构域结合，从而扩大了BTB蛋白家族的功能范围[5]。根据这些结构域，BTB蛋白基因家族可以分为许多亚家族，包括BTB-Only蛋白、BTB-锌指(BTB zinc-finger, BTB-ZF)蛋白、BTB-Kelch蛋白、BTB-BACK蛋白、BTB-Back-Kelch蛋白、Math-BTB蛋白、BTB-ANK蛋白、BTB-Back、BTB-PHR蛋白和Rho-BTB蛋白[6-7]。这表明BTB蛋白还包括其他多种不同的结构域，在植物中可能有多种功能。
关于BTB蛋白在植物的发育与非生物胁迫中的重要作用的研究已有一定的进展，但仍存在待解决的问题。本文以蛋白结构为基础，就目前在植物中发现的BTB基因家族成员泛素化介导植物发育和逆境应答等过程进行总结和深入解析，为后续研究提供参考。
1 BTB蛋白在植物应激反应和信号传导中的作用植物在应激反应中，泛素蛋白酶系统(ubiquitin protease system, UPS)结构性或条件性地降解激活物或者抑制物。在泛素化途径中，泛素连接酶(也称为E3酶或E3S)参与抑制或激活应激反应关键步骤，它促进泛素化的氨基酸转移到底物蛋白上，然后通过26S蛋白酶体进行降解[8-9]。CRL (cullin-ring)连接酶是最常见的一类泛素连接酶多聚体[8-9]，它包含1个特定的CUL (cullin)蛋白作为分子支架，将由环指结构域蛋白[如RBX (ring box protein 1)]和泛素结合酶(也称为E2)组成的催化聚合体连接到特定的底物识别结构域，同时该聚合体与靶蛋白相互结合。在CRL多聚体中，比较常见的是SCF [Skp1/CUL1/F-box protein (FBP)]复合体[10-11]。真核生物中，除了CUL1，还有一些其他的CUL (CUL2、CUL3、CUL4、CUL5和CUL7)[12-13]，这些CUL蛋白同样是具有E3活性的蛋白复合体组成部分，通过不同的识别结构域来使各种蛋白底物泛素化。
最近的研究表明CUL3是控制不同发育和应激反应以及人类病理的一大类CRL的分子支架，它存在于所有真核生物的基因组中，在蛋白水平上CUL3与BTB蛋白相互作用，作为底物特异性识别器[14-15]。同时BTB结构域另一端通过蛋白相互作用结构域(protein-protein interaction domain, PID)特异地结合底物。与CUL1需要通过SCF复合体与底物结合不同的是，CUL3可以直接与BTB结构域相结合[14-15]，这说明了BTB结构域在蛋白质泛素化过程中的重要作用。
下文将分别阐述BTB蛋白各个亚家族通过介导蛋白泛素化在植物发育和逆境应答中的作用。
1.1 BTB-MATHMATH是肿瘤坏死因子受体相关因子(tumor necrosis factor receptor-associated factor, TRAF)类结构域的1个亚型，TRAF蛋白有分子衔接剂或E3泛素连接酶的功能，有助于将细胞表面受体的上游信号传导到下游效应物[16]。含有MATH和BTB/POZ结构域的蛋白称作BPM (BTB/POZ and MATH protein)蛋白，其中MATH结构域作为底物受体，BTB/POZ结构域结合CUL3[17]，CUL3和BPM蛋白结合形成CUL3BPM复合体。
拟南芥(Arabidopsis thaliana)核心分支BPM基因家族已经得到了广泛的研究。拟南芥基因组只编码6个BPM基因，对应AtBPM1–6[18]。BPM蛋白作为基于CUL3的E3连接酶的底物特异性结合蛋白，与不同的转录因子家族成员相互结合，因此被认为是各种发育过程和胁迫反应的重要调节因子。过表达BPM3或BPM5会增强植物脱落酸(abscisic acid, ABA)的敏感性，抑制种子萌发、幼苗形态建成和根生长[19]。同时，过表达BPM3或BPM5的植物失水减少，气孔关闭增加，抗旱性提高[19]。
BPM通过和CUL3的结合形成CULBPM，其通过介导ABA反应的负调节转录因子AtHB6 (homeobox 6)和PP2C (protein phosphatases type 2C)的降解来调节ABA信号传导[19-20]。此外，BPM蛋白也与乙烯反应有关。例如，BPM蛋白负调控乙烯反应转录因子WRI1 (wrinkled1)，从而影响拟南芥的脂肪酸代谢和种子发育[21]。BPM蛋白还可以促进耐旱和耐热胁迫的脱水响应性元件结合蛋白2A蛋白(dehydration-responsive element binding protein2A, DREB2A)的降解，负向调节拟南芥的热应激反应[22]，防止过量的DREB2A的积累。由此可见，BPM可能介导相关转录因子的降解来调节植物的发育和逆境应答。
最近的研究表明，CULBPM影响茉莉酸(jasmonic acid, JA)信号传导。JA是一种含氧的脂肪衍生物，是植物必需的激素。骨髓细胞组织增生蛋白(myelocytomatosis protein, MYC)是JA诱导的信号通路的关键分子之一，在番茄(Solanum lycopersicum)中的研究表明其在应激代谢中具有双重作用[23]。CULBPM被证实可以促进MYC2/3/4的降解，并调控信号传导阻止茉莉酸介导的生物有害进程[24]。此外，JA通过稳定转录因子AP2 (APETALA2)/ERF (ethylene response factor)中的成员氧化还原响应转录因子(redox-responsive transcription factors 1, RRTF1)来促进植物分泌抗性物质p-香豆酰胍基丁胺(p-coumaroylagmatine, CouAgm)，而CULBPM通过介导RRTF1降解负调控JA信号[25]。但是JA还可以促进BPM3蛋白的稳定，表明还存在负反馈调节机制来控制MYC活性，避免有害的应激反应[24]。
BPM蛋白不仅影响植物体内激素信号的传导，还被证明与植物开花有关。在拟南芥中，bpm突变体表现为晚花[26]，而AtBPM1的超表达植株表现为早花[27]，因此预测BPM正向调控植物的开花时间。此外，转录因子AtMYB56和AtMYB106与营养到生殖转换的关键调节因子AtFT (flowering locus T)的启动子结合，从而抑制其转录，而CULBPM介导转录因子AtMYB56和AtMYB106的泛素化降解，从而使AtFT转录增加并促进开花[26, 28]。因此，BPM蛋白在植物开花中起重要作用。
综上所述，这些发现证明BPM参与了激素介导的应激反应和开花调控，是植物生理应答的蛋白质翻译后调节因子。值得注意的是，虽然6个拟南芥BPM蛋白都被证明与AtHB6、WRI1、MYB56和DREB2A等蛋白质相互作用[20-22, 29]，但只有特定的成员被证明与PP2C相互作用[19]，并且不同的BPM在结合3种MYC蛋白方面存在相似的功能[24]。此外，只有BPM1、BPM2和BPM4与MYB106相互作用[28]，只有BPM1和BPM3与RRTF1相互作用[25](图 1A)。这意味着在这个高度保守的蛋白质家族中既存在功能冗余又存在个别不同的功能，其中一些可能在特定的环境条件下才表现出来。
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| 图 1 BTB-MATH (A)和BTB-TPR (B)在植物中的作用模式图 Fig. 1 Modes of action of BTB-MATH (A) and BTB-TPR (B) in plants. |
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BTB-TPR蛋白的特征是存在1个N-末端的BTB结构域和6个TPR基序，以及在C末端的1个卷曲基序，该类型蛋白是植物中所特有的[30]。拟南芥中有3个BTB-TPR蛋白：ETO1 (ethylene overproducer1)、EOL1 (ETO1-like1)和EOL2 (ETO1-like2)，它们一起通过介导乙烯合成关键酶1-氨基环丙烷-1-羧酸合酶(1-aminocyclopropane-1- carboxylic acid synthase, ACS)的降解来负调控乙烯的合成[31]，并且这个过程是受到环境影响的。光会通过降低ETO1/EOLs复合体的稳定性促进乙烯的合成[32]，在各种生物和非生物胁迫中EOL2表达量会增高[31]，同时干旱胁迫和水淹胁迫会影响EOL1的表达模式。研究表明，在生殖阶段，水稻(Oryza sativa) OsETOL1的转录水平受到干旱和脱落酸的强烈诱导，使水稻成熟延迟；而水淹条件下，OsETOL转录本在5 d后被抑制，可能促使上部叶片生长到水面以上[33]。其中ETO1以2种截然不同的方式作用于ACS5：一方面，它通过直接结合酶来抑制ACS5的活性；另一方面，它通过与CUL3的相互作用促进ACS5的降解[34]。此外，在cul3a/b基因敲除突变体中，ACS5蛋白和乙烯含量的提高证实了CUL3ETO1对乙烯生物合成的调控[35]。这些说明BTB-TPR蛋白亚基在植物的泛素化介导的乙烯调控途径中具有重要的作用(图 1B)。
1.3 BTB-ANK (ankyrin-repeat)病程相关的非表达因子(nonexpressor of pathogenesis related, NPR)蛋白包含1个N-末端的BTB结构域、1个中央ANK结构域和1个C-末端的反式激活结构域[36-37]。拟南芥中NPR1是水杨酸(salicylic acid, SA)诱导的病程相关基因(pathogenesis-related gene, PR)表达和对病原菌抗性所必需的[38-39]。NPR3和NPR4是NPR1的2个直系同源基因，其编码的蛋白结构与NPR1具有很高的相似性。研究表明NPR1、NPR3和NPR4与植物免疫反应中的SA介导的转录调控有关。SA是植物的防御激素，对植物免疫反应至关重要，拟南芥的NPR1、NPR3和NPR4蛋白被认为是SA的受体[40]。SA结合NPR1并调控其转录激活活性，同时抑制NPR3/NPR4的转录活性，并通过招募防御相关基因的转录抑制物TGAs (TGACG-binding factors)诱导防御相关基因的表达[41](图 2)。
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| 图 2 NPR在植物中的作用途径 Fig. 2 Modes of action of NPR in plants. |
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NPR参与的SA信号传导作用过程如下：SA浓度增加时，位于核外的NPR1稳定性发生变化，一部分进入细胞核形成三元复合体促进致病相关基因PRs的表达。在细胞核内会形成HAC-NPR1-TGAs复合体和NPR1-CDK8-TGAs复合体，SA结合的两者都会被招募到致病相关基因PRs启动子上，随后前者被组蛋白乙酰化的染色质重编程来转录激活[42]，后者中的CDK8s及其结合的其他因子还会将RNA聚合酶Ⅱ (RNA polymerase Ⅱ, Pol Ⅱ)招募到PR1基因的启动子和编码区，以促进PR1基因的表达，从而激活植物病程防御[43]。细胞核内还会形成NPR1-CDK8-WRKYs三元复合体正调控NPR1的合成。WRKYs作用于W-Box序列上的NPR1启动子，CDK8s及其结合的其他因子将RNA聚合酶Ⅱ招募到NPR1基因上，促进NPR1基因的转录，合成更多的NPR1[43](图 2)。
然而NPR1虽然有BTB结构域，但不与CUL3直接相互作用，而是由NPR3和NPR4将其招募至CUL3进行泛素化降解[44]。同时SA也增强了NPR3/NPR4与茉莉酸之间的相互作用，促进茉莉酸在植物效应免疫(effector-triggered- immunity, ETI)过程中触发免疫因子，从而促进中早期的有害蛋白的降解。NPR3/NPR4也可以促进植物免疫调节的核心蛋白之一——疾病易感性增强1 (enhanced disease susceptibility 1, EDS1)的降解[45]，而NPR1在其中起到与之相同的作用，其也可以促进EDS1及其在EIT期间诱导细胞凋亡的正调节因子WRKY54/70的降解，从而促进植物细胞的存活[46] (图 2)。
BTB参与的泛素化过程还在其他发育过程中发挥作用。BOP1 (blade-on-petiole 1)和BOP2也属于BTB-ankyrin家族，是基于CUL3的E3连接酶的底物适配子，与其他BTB结构域家族不同，此蛋白亚家族有多种蛋白组合形式。研究发现BOP1/2与转录因子LFY (LEAFY)一起促进花分生组织的形成[47]。矛盾的是，BOP1/2在体外促进LFY的泛素化并调节LFY的活性，但在体内却是LFY稳定所必需的，这2个E3连接酶如何调节LFY功能尚不清楚。
1.4 BTB-TAZ拟南芥BTB-TAZ (BT)结构域蛋白含有1个位于N-端的BTB结构域、1个位于中心的TAZ锌指蛋白结构域和1个位于C-末端的钙调蛋白结合域[48-49]。BT蛋白是陆地植物所特有的[48]，根据编码蛋白的氨基酸序列同源性，拟南芥BT家族的5个成员可以划分出2组：第1组由BT1和BT2组成，第2组由BT3、BT4和BT5组成。BT成员之间存在相当大的功能冗余，BT在雄配子体和雌配子体发育的早期阶段都是至关重要的[48]。在这一过程中，BT2基因是主导基因，在BT2功能缺失突变体中，BT2基因在功能上被BT3取代，在BT2功能缺失突变体中也被BT1部分取代，通过转录相互调节[48]。这种表达补偿是BTs基因功能冗余的重要机制。
前期研究预测BT2是逆境互联信号网络中心的关键蛋白，其响应多种逆境[50]。在苹果(Malus pumila)中，MdBT2可以与多种底物蛋白相互作用，参与不同的信号传导途径，如MdBT2与MdbHLH104 (basic helix-loop-helix)、MdbHLH93和MdMYB23相互作用，负向调节铁的动态平衡、叶片衰老和冷胁迫[51-53]。
此外，在拟南芥中的研究表明，BT2是植物氮利用效率(nitrogen use efficiency, NUE)网络的保守的负调控因子，也是NUE网络中最核心和联系最紧密的基因[54]。MdBT2受到硝酸盐的诱导表达[55-58]，推测其通过介导植物对硝酸盐的响应来调控苹果植物生长发育及抗旱性。MdBT2通过直接与DELLA蛋白MdRGL3a相互作用，发挥调节植物生长的作用[59]，从而促进其泛素化和响应硝酸盐的降解。
NAC (NAM, ATAF1/2, CUC)转录因子被证明通过增强ABA信号传导而提高植物的耐旱性[60]。对BT基因介导的干旱响应的研究中，苹果中的MdBT2通过与转录因子MdNAC143相互作用负调控干旱胁迫响应[61]。干旱水平下MdBT2在蛋白质水平受到抑制，但MdNAC143不再受抑制，其激活与耐旱性相关的下游基因的表达，从而降低了活性氧(reactive oxygen species, ROS)积累和水分流失率[61]，提高植物的抗旱性。除此之外，MdBT2可能通过介导MdNAC1的蛋白稳定性负调控铁离子的吸收利用[62]，改善植物的缺铁逆境，这说明NAC基因在植物体内存在更多未知的靶基因，从而扩展了BT2基因的功能。
MdBT2还是苹果中不定根(adventitious root, AR)形成的负调节剂，主要通过直接作用和间接作用2种方式。一方面，MdBT2通过直接与MdARF8 (auxin response factor 8)和MdIAA3 (indole-3-aceticacid inducible 3)相互作用来抑制AR的形成。另一方面，MdARF通过诱导MdGH3s (gretchen hagen)的转录来调节AR的形成，而MdBT2通过26S蛋白酶体途径促进MdARF8的泛素化和降解，并负调控MdGH3.1和MdGH3.6的表达。同时，MdIAA3通过与MdARFs形成异二聚体来抑制AR的形成，MdBT2促进了MdIAA3的稳定性并略微促进了其与MdARF8的相互作用，稳定了异二聚体结构，间接抑制了AR的形成[63](图 3)。
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| 图 3 MdBT2在多种合成途径中的作用 Fig. 3 Modes of MdBT2 in multiple pathways. |
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研究表明，苹果MdBT2在不同激素和环境信号诱导的花青素生物合成中起负调控作用，表明MdBT2整合了胁迫信号和花青素的生物合成；研究发现，苹果中的MdBT2通过泛素化途径加速花青素生物合成的正调控蛋白MdMYB1的降解，从而负面调节氮缺乏情况下的花青素的生物合成[64]。有研究提出了“BT2-靶蛋白- MdMYB1”的机制，即在尚无非生物逆境胁迫的情况下，MdBT2与靶蛋白相互作用，对其进行泛素化降解，从而负调控靶蛋白促进的花青素的生物合成；在非生物逆境胁迫条件下，MdBT2的表达受到抑制，从而抑制了靶蛋白的降解，从而促进了胁迫诱导的花青素的生物合成。目前发现的靶蛋白有MdBZIP44、MdWRKY40、MdERF38和MdTCP46，在ABA诱导、创伤、干旱和高光强的情况下，MdBT2的表达受到抑制，以上靶蛋白的表达量就会增高并与MdMYB1相结合，促进花青素的生物合成[65-68]。
MdBBX22直接与光形态建成和花青素合成的正调节因子下胚轴5 (hypocotyl 5, MdHY5)相互作用[69]，增强MdHY5与其靶基因的结合活性，然而MdBBX22通过泛素-蛋白酶体途径被MdBT2介导降解[70]。氮素充足的条件下，MdBT2促进了构成型光形态1 (constitutively photomorphogenic 1, MdCOP1)介导的泛素化和MdMYB2蛋白的降解[64, 71]，抑制了花青素合成基因的表达和花青素的积累；氮素缺乏条件下，14-3-3蛋白家族成员生长调节因素11 (growth- regulating factors 11, MdGRF11)促进了MdBT2的降解，从而增加了MdMYB1蛋白的丰度进而诱导花青素积累以响应氮素的缺乏[72]。14-3-3蛋白是一个高度保守的磷酸肽结合蛋白家族，通过磷酸化介导蛋白质间的相互作用。该蛋白家族参与了广泛的细胞功能，包括调节激素对胁迫刺激的诱导[73]。这些结果表明，MdBT2是一种整合多种胁迫信号的多功能蛋白，也是调节花青素生物合成的关键蛋白(图 3)。
那么BT2如何影响多条信号通路呢？前期有研究预测其可能与其他BTB家族成员或溴域蛋白相互作用。有研究表明，CULBT2泛素连接酶通过与GTE9和GTE11相互作用来调节拟南芥中35S增强子的活性[74-75]，因此BT2还是维持多聚化的35S增强子转录活性所必需的，缺乏BT2会导致35S增强子的高度甲基化[74]。除此之外，拟南芥AtBET10 (bromodomain and extra-terminal domain)也是一种含有溴结构域的蛋白，是糖和ABA信号的负调节因子，并在花粉萌发和花粉管伸长过程中起作用[49]。研究发现玉米(Zea mays)中ZmBT4、ZmBT2b蛋白的BTB结构域ZmBT4-BTB、ZmBT2b-BTB均能与ZmBET10互作[76]，表明BTB结构域在BTB-TAZ蛋白与转录因子ZmBET10互作过程中具有重要作用，同时在水杨酸、茉莉酸、乙烯处理后玉米植株体内的ZmBT2表达水平发生明显的变化[77]，该研究结果进一步证明了BTB-TAZ蛋白在玉米抗病中的功能与调控机制。因此，对相关溴域蛋白的研究有助于探究BT2同时影响多条信号通路的分子机制，进而促进对植物抗生物和非生物胁迫的研究。
1.5 BTB-NPH3在拟南芥中，有21个BTB-NPH3 (nonphototropic hypocotyl 3)蛋白，它们是植物特有的蛋白[7]。BTB-NPH3含有1个N-末端的BTB结构域和1个C末端NPH3结构域，一些成员还含有1个额外的C末端卷曲结构域。随后的研究者将拟南芥中的33个以NPH3结构域为中心结构域的蛋白鉴定为NRL (NPH3/RPT2-like)蛋白家族，其中只有2个无BTB结构域，该家族的生物功能还有待详细研究[78]。其中，NPH3蛋白和根向光性2 (root phototropism 2, RPT2)蛋白是主要成员。其中NPH3有助于建立这种差异生长反应所需的横向生长素梯度分布[79]。RPT2通过改变NPH3的定位和磷酸化状态来调节光响应[80]。
非光致性下胚轴1 (nonphototropic hypocotyl 1, NPH1)编码大小为120 kDa、依赖蓝光进行蛋白磷酸化的蛋白[81-82]。作为一种新的光受体蛋白，研究者又将NPH1命名为PHOT1 (phototropin1)[83]。同时研究表明NPH3和PHOT1在酵母中是相互作用的[84]。低强度蓝光下，CRL3NPH3介导Phot1的单、多泛素化，从而调节蓝光诱导的生长素转运蛋白的重新定位[85-86]。高强度蓝光下，CRL3NPH3介导的Phot1的多聚泛素化以及其后的降解可能使受体失去特异性[85]。蓝光刺激的NPH3去磷酸化和从质膜释放后，Phot1-NPH3的相互作用被破坏[79]，导致受体信号传导停止(图 4)。因此在连续高光强下，要重建和维持光致信号，Phot1-NPH3复合体必须重建，RPT2的存在对促进这一过程是必需的[79]。基于这些发现，RPT2被认为有助于光感官适应，并在较亮的光条件下促进高效的向光性。
拟南芥的大多数NRL蛋白包含1个BTB结构域，它可以作为底物适配器来招募特定的蛋白质进行泛素化和降解[80]。阐明NRL蛋白如何在生化水平上发挥作用，以及它们的定位和磷酸化状态的变化如何影响它们的活性，这对于理解生长素梯度如何促进向光性、叶片定位和叶片展开等反应是至关重要的。
1.6 BTB-Kelch研究证明拟南芥中一对光响应BTB蛋白——光响应BTB1 (light-response BTB1, LRB1)和LRB2 (light-response BTB2)与植物光反应有关。这2个蛋白均含有BTB结构域，同时通过比对和同源性搜索发现，在BTB结构域下游有1个Kelch结构域，并且在所有多肽的N端附近都有1个可能的核定位序列[87]。过量光胁迫触发的局部和系统气孔关闭反应以及ROS反应，都依赖于光敏色素B (phytochrome B, phyB)的功能[88]，与LRB1/2组装的泛素连接酶作为光形态发生的负调控因子。LRB1和LRB2似乎并不直接促进phyA的积累，而是通过抑制phyB的过程来依赖性地间接促进phyA的积累，从而抑制phyA转录[88]，LRB1/2更可能通过直接地控制phyB/D水平或者作用于phyB/D而间接地发挥作用[87]，但LRB1/2是否直接参与光敏色素的转换仍有待确定。
CUL3LRB介导光敏色素相互作用因子3 (phytochrome interacting factor 3, PIF3)和phyB的降解。光激活的phyB通过直接相互作用诱导PIF3的磷酸化，这种磷酸化增强了PIF3与LRB的亲和力，导致PIF3和phyB的降解[89]。同时PIF3的降解改变了下游靶基因的转录，而PhyB的降解作为反馈调节，使细胞对红光不敏感[89]。研究发现BOPs (上文提到的BTB-ANK蛋白)在体外促进光敏色素相互作用因子PIF4的泛素化以促进光形态发生和调节热形态发生[90]，与PIF3和CUL3LRBs结合不同，BOP2与PIF4结合可能不需要PIF4的磷酸化(图 5)。
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| 图 5 BTB-Kelch在植物中的作用途径 Fig. 5 Modes of action of BTB-Kelch in plants. |
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CRL3也参与植物对春化的反应。FRI (frigida)作为抑花因子开花位点C (flowering locus C, FLC)的激活剂，增加FLC表达并延迟开花[91]。冷胁迫后，LRB1和LRB2与CUL3a和FRI结合，促进FRI降解。此外，冷诱导的WRKY34转录因子促进CUL3a的积累，从而促进FRI蛋白降解[92]。
1.7 BTB-onlySkp1和ElonginC是BTB-only蛋白，只含有BTB结构域[7]。作为CUL1 SCF复合物的一个关键组成部分，Skp1形成了CUL2和底物识别蛋白之间的结构连接，它作为接头的同时结合CUL的N端和泛素降解过程中的F-box蛋白和F-box基序。在本实验室早期的一份研究中，番茄SlBTB14、SlBTB15和SlBTB16含Skp1结构[93]，因此可能在泛素化中发挥作用。拟南芥AtSIBP1是盐胁迫的正调节因子，属于Skp或ElonginC家族，正向调控拟南芥中的盐信号[94]，可能与CUL1参与的蛋白质泛素化过程有关，其酶作用底物还有待探究。
2 展望在动物中，BTB蛋白结构域还有一个重要的功能就是参与转录调控。在转录因子中经常观察到二聚化，可以提高DNA的亲和力和特异性，并提供一种简单的机制使因子在一定浓度的阈值下失活[95]。BTB在转录因子中的功能是提供二聚化界面和招募转录辅助因子。如在动物中PLZF是致癌的BRB-ZF转录因子，其中的BTB结构域驱动视黄酸受体a (retinic acid receptor A, RARa)的同源二聚化[96]，招募转录辅助抑制因子SMRT从而抑制RARa的靶基因并阻断骨髓祖细胞的分化[97]。
然而在植物中，BTB结构域蛋白更多以参与泛素连接酶E3的组成来介导应激反应和信号传导，本文对其进行了总结(表 1)。但是仍有许多关于这些连接酶的问题需要深入研究，包括泛素连接酶E3的未知功能、其组分的进化历史和活性的精确调控。同时已有BTB蛋白结构域介导二聚体化的研究[63]，它在植物中是否具有进一步参与转录调控的功能还有待研究。
表 1 不同含BTB结构域的蛋白在植物不同泛素化过程中的作用
Table 1 Functions of various proteins containing the BTB domain in different ubiquitination processes in plants
| Adaptor name | Protein subfamily | Substrate | CRL3 E3 function | Physiological function | References |
| BPMs | BTB-MATH | AtHB6 | CUL3BPM targets AtHB6 for ubiquitylation and protein degradation | Negatively regulates ABA signaling | [19] |
| BTB-MATH | PP2Cs | CUL3BPM3/5 targets PP2Cs for degradation in the nucleus | Positively regulates ABA signaling | [20] | |
| BTB-MATH | WR1 | CUL3BPM targets ethylene reaction transcription factorsWR1 for degradation | Affects Arabidopsis fatty acid metabolism and seed development | [21] | |
| BTB-MATH | DREB2A | CUL3BPM2/4 negatively regulates heat stress by promoting the degradation of DREB2A |
Negatively regulates heat stress response and prevents accumulation of excess DREB2A | [22] | |
| BTB-MATH | MYC2/MYC3/MYC4 | CUL3BPM can promote degradation of MYC2, MYC3, and MYC4, which are regulators fine-tune jasmonate defense and plant growth |
Reset the signal and prevent the harmful JA reaction from getting out of hand | [24] | |
| BTB-MATH | RRTF1 | CUL3BPM promotes RRTF1 degradation | Affects JA signaling and promotes the secretion of CouAgm | [25] | |
| BTB-MATH | MYB56 MYB106 | CUL3BPM targets MYB56 and MYB106 for degradation | Promotes flowering | [26, 28] | |
| ETO1/EOL1/EOL2 | BTB-TPR | ACSs | ETO1 inhibits the activity of ACS5 by directly binding the enzyme, it promotes the degradation of ACS5 by interacting with CUL3 as well EOL1 and EOL2 also contribute to ACS degeneration | Negatively regulates ethylene production | [31-35] |
| NPR3/NPR4 | BTB-ankyrin | EDS1 | NPR3/NPR4 recruit NPR1 to CUL3 for degradation. NPR3/NPR4 can also promote the degradation of EDS1 | Negatively regulate plant immunity | [45] |
| NPR1 | BTB-ankyrin | EDS1 WRKY54/70 | NPR1 can promote the degradation of EDS1 and WRKY54/70 | Promote cell survival during EIT | [46] |
| BOP1/2 | BTB-ANK | LFY | BOP1/2 promotes ubiquitylation of LFY in vitro and also regulates LFY activity, and contributes to the stability of LFY in vivo | Promotes flower development | [47] |
| BTB-ANK | PIF4 | BOPs promote ubiquitylation of PIF4 in vitro | Promotes photomorphogenesis and modulates thermomorphogenesis | [90] | |
| MdBT2 | BTB-TAZ | MdbHLH104/MdbHLH93/MdMYB23 | MdBT2 can interact with a variety of substrate proteins |
Negatively regulates iron homeostasis, leaf senescence and cold stress | [51-53] |
| BTB-TAZ | MdRGL3a | MdBT2 directly interacting with MdRGL3a | Promotes MdRGL3a ubiquitination and degradation in response to nitrate | [59] | |
| BTB-TAZ | MdNAC143 | MdBT2 interacts with the transcription factor MdNAC143 | Negative regulation of drought stress response | [61] | |
| BTB-TAZ | MdARF8/MdIAA3 | MdBT2 interacts directly with MdARF8 and MdIAA3 | Inhibits adventitious root formation | [63] | |
| Promote the degradation of MdARFs and slightly promote the stability of MdIAA3 | [63] | ||||
| BTB-TAZ | MdMYB1 | CUL3BT2 targets MdMYB1 for degradation | Negatively regulate the biosynthesis of anthocyanins under nitrogen deficiency conditions | [64] | |
| BTB-TAZ | MdBZIP44\MdWRKY40\MdERF38\MdTCP46 | CUL3BT2 targets them for degradation | Negatively regulate anthocyanin synthesis | [65-68] | |
| BTB-TAZ | MdBBX22 | CUL3BT2 targets MdBBX22 for degradation，inhibits the binding of MdBBX22 to MdHY5 | Negatively regulate anthocyanin synthesis | [70] | |
| BTB-TAZ | MdCOP1\MdMYB2 | Promotes MdCOP1-mediated ubiquitination and degradation of MdMYB2 protein | Negatively regulate anthocyanin synthesis | [64, 71] | |
| BTB-TAZ | GTE9/GTE 11 | CULBT2 ubiquitin ligase interacts with GTE9 and GTE11 | Regulation of 35S enhancer activity in Arabidopsis | [74-75] | |
| NPH3 | BTB-NPH3 | PHOT1 | CRL3NPH3 promotes the degradation of PHOT1 | Regulates the blue light response | [85-86] |
| LRB1/2 | BTB-Kelch | PIF3/PhyB | CUL3LRB mediates the degradation of both PIF3 and PhyB | Feedback regulation in response to red light | [89] |
| BTB-Kelch | FRI | LRB1/LRB2 promote FRI degradation | Promote flowering | [92] | |
| Skp1/Elongin C | BTB-only | Skp1 forms the structural link between CUL1 and substrate recognition proteins | Plays a role in ubiquitination and positive regulation of salt signaling | [94] |
前期研究大多证明BTB结构域蛋白在加强植物防御中起到很重要的作用，但也有研究者在烟草中鉴定出一种含BTB结构域的蛋白质，负调节效应蛋白的积累，预测该蛋白是植物基础防御和ETI中的负调节剂，但它是否作为参与E3泛素复合体的成员来影响植物ETI的过程还不清楚[98]。同时，仍有一些功能蛋白的生理靶标未被发现。在拟南芥中过表达小麦(Triticum aestivum)的BTB-MATH蛋白TaMAB (triticum aestivum)，出现了多种表型的生理缺陷[99]，其影响了细胞长度，且与泛素共定位，说明与CUL3 E3酶参与的泛素化过程有关，因此可能与细胞骨架或者其他调节网络的蛋白互作，但目前并未在拟南芥中发现特定的生理靶标[100]。TaMAB2在酵母异源系统中无法被识别，是因为在BTB蛋白的扩张过程中，TaMAB2可能发生了太大的变化，也可能是因为受到翻译后修饰的限制，这些修饰无法在酵母中发生或其互作蛋白无法进入酵母核。用于分析蛋白质相互作用的其他技术的进步也有助于分析可能的体外相互作用或体内相互作用。除此之外，CUL3的新作用正在被发现。最近的研究发现BPM1在RNA引导的DNA甲基化中的1种新的CUL3非依赖性作用，BPM1可能促进DNA甲基化的活性[101]。
综上所述，BTB蛋白家族在植物泛素化介导的植物发育和逆境应答等过程中发挥着重要的作用，但仍有一些问题有待探索，相信随着研究的深入，会发现BTB蛋白更多的功能以及更多的靶标，推动植物相关领域的研究进程。
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