Research and progress on the biological function of plant aquaporin Nodulin 26-like Intrinsic Proteins
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摘要:
水通道蛋白(AQPs)是植物体内水分跨膜运输的主要通道，有关AQPs维持水稳态的研究近年来已被广泛报道。在AQPs的7个亚家族中，类NOD26膜内在蛋白 (Nodulin 26-like Intrinsic Proteins, NIPs) 是植物所特有的一个亚族，它在植物中转运水的能力相对较弱，但在类金属的运输上发挥了重要功能。NIPs蛋白结构高度保守，具有2个结构域：NPA基序和ar/R选择性过滤器，它们对底物选择性至关重要。NIPs作为典型的类金属跨膜通道蛋白，根据ar/R区的氨基酸组成可分为3个亚类，包括NIP I、NIP II和NIP III，不同亚类在底物运输上存在着特异性和冗余性。NIP I介导砷和锑的转运，NIP II参与硼、砷和锗的运输，NIP III运输硅、硒、硼、砷、锑和锗。NIPs在植物体内对必需和有益类金属(硼、硅和硒)的调节，增强了植物抵御逆境胁迫的能力；对有害类金属(砷和锑)的调节，一方面通过减少其向种子的分配进而保障食品安全和人体健康，另一方面通过在植物体内超富集以达到环境修复的目的。此外，NIPs作为一种多功能通道蛋白，还能够运输过氧化氢、甘油、乳酸、尿素和氨气等，在植物信号转导和多种生理代谢活动中起作用。随着全球变暖，极端天气频发，植物在生长发育过程中将面临更大的挑战。因此，基于NIPs对多种底物的选择性和功能多样性，可考虑将其作为培育高抗逆性作物的靶基因。NIPs在植物中的表达具有器官、组织和细胞特异性，其表达丰度及蛋白活性在转录水平和蛋白水平上被严格调控。明确NIPs的调控机制对于进一步解析其在植物中的生物学功能是非常必要的。综上，本文在介绍NIPs结构和分类基础上，重点阐述了NIPs底物运输及其相关的生物学功能和调控机制，以期为通过基因工程技术来增强作物抗逆性并提高作物产量和品质提供关键候选基因。
Abstract:Aquaporins (AQPs) are the main channel for water transport across membranes in plants, and studies on maintaining water homeostasis by AQPs have been widely reported in recent years. Among the seven subfamilies of AQPs, Nodulin 26-like intrinsic proteins (NIPs), a plant-specific subfamily, have relatively weak roles in water transport in plants, but play an important function in metalloid transport. The protein structure of NIPs is highly conserved with two structural domains: the NPA motif and the ar/R selectivity filter, which are critical for substrate selectivity. NIPs, as typical metalloid transmembrane channel proteins, can be classified into three subclasses based on the amino acid composition of the ar/R region, including NIP I, NIP II, and NIP III, and the different subclasses have specificity and redundancy in substrate transport. The NIP I subfamily mediates the transport of arsenic and antimony, the NIP II subfamily is involved in the transport of boron, arsenic and germanium, and the NIP III subfamily transports silicon, selenium, boron, arsenic, antimony and germanium. NIPs enhance plant resistance to adversity stress by regulating essential and beneficial metals (boron, silicon and selenium). NIPs regulate harmful metalloids (arsenic and antimony) to ensure food safety and human health by reducing their distribution to seeds on the one hand, and to achieve environmental remediation by hyper-enrichment in plants on the other hand. In addition, as a multifunctional channel protein, NIPs can transport hydrogen peroxide, glycerol, lactate, urea, and ammonia, which play a role in plant signal transduction and various physiological and metabolic activities. With global warming and frequent occurrence of extreme weather, plants will face greater challenges during growth and development. Therefore, NIPs can be considered as target genes for breeding highly resistant crops based on their multiple substrate selectivity and functional diversity. The expression of NIPs in plants is organ-, tissue- and cell-specific, and the abundance of their expression and protein activity are tightly regulated at the transcriptional and protein levels. To further understand the biological functions of NIPs in plants, it is necessary to clarify their regulatory mechanisms. In summary, based on the introduction of the structure and classification of NIPs, this paper focuses on their substrate transport and related biological functions and regulatory mechanisms. It aims to provide key candidate genes for enhancing crop resistance and improving crop yield and quality through genetic engineering techniques.
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Keywords:
- aquaporins /
- NIPs gene /
- substrate /
- metalloid /
- biological function /
- regulatory mechanism
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植物生长发育离不开水分。水通道蛋白(Aquaporins, AQPs)作为主要内在蛋白(Major intrinsic proteins, MIPs)超家族成员，在植物体内的水分跨细胞途径运输中发挥着重要功能[1]。1988年，首个水通道蛋白CHIP28 (AQP1)在人体血红细胞膜上被分离纯化[2]，Preston等[3]通过卵母细胞异源表达系统证实CHIP28具有水转运活性。定位在拟南芥液泡膜上的 γ-TIP是植物中第一个报道的具有水渗透性的通道蛋白[4]。随着基因组测序技术的发展，AQPs已经在多种植物中被鉴定。根据氨基酸序列的同源性，AQPs可被分成7个亚家族：质膜内在蛋白(Plasma membrane intrinsic proteins, PIPs)、液泡膜内在蛋白(Tonoplast intrinsic proteins, TIPs)、类NOD26膜内在蛋白(Nodulin 26-like intrinsic proteins, NIPs)、小分子碱性膜内在蛋白(Small basic intrinsic proteins, SIPs)、类GlpF膜内在蛋白(GlpF-like intrinsic proteins, GIPs)、杂合内在蛋白(Hybrid intrinsic proteins, HIPs)和X类内在蛋白(X intrinsic proteins, XIPs)。在植物的不断进化过程中，PIPs、TIPs、NIPs和SIPs广泛分布在各种陆生植物中，但单子叶植物缺失了XIPs，GIPs和HIPs被发现仅存在于苔藓类植物中，并在高等植物中发生了丢失事件[5]。AQPs作为一种多功能跨膜通道蛋白，不仅可以转运水，还可以转运甘油、尿素、类金属、NH3和CO2等，在调节植物生长发育及抵御逆境胁迫等方面发挥重要作用[6]。类NOD26膜内在蛋白(NIPs)是植物所特有的一个亚家族，因其与大豆NOD26序列相似性高而得此名[7]。细菌AqpN是NIPs进化的起源，陆生植物对营养的需求迫使NIPs进行功能分化[8]。与具有高效水转运活性的PIPs和TIPs不同，NIPs运水能力相对较低。NIPs在植物中定位于质膜或内质网上[9−10]，大量研究表明其最主要特征是转运类金属。本文主要综述植物水通道蛋白NIPs的结构、分类、底物运输、生物学功能和调控机制，为深入研究NIPs功能提供参考。
1. 植物NIPs结构和分类
水通道蛋白结构高度保守，在生物膜上通常以四聚体形式存在，每个单体都可以作为功能通道起作用[11]。如图1所示，单体蛋白是由5个环(loop A-loop E)连接6个α-螺旋(TM1-TM6)组成的“沙漏”型跨膜结构。其中，loop B和loop D以及氨基末端(-NH2)和羧基末端(-COOH)位于细胞内，loop A、loop C和loop E则位于细胞外；B环和E环形成两个短的α-螺旋结构(HB和HE)，并有部分嵌入膜中，其顶端处各含有一个高度保守的NPA基序，由天门冬酰胺(Asn)、脯氨酸(Pro)和丙氨酸(Ala)组成，两个NPA基序构成NPA区，参与孔通道的形成[12]。在NPA区上方0.8 nm处是芳香族/精氨酸区(ar/R)，ar/R是通道最窄的部分，由位于螺旋TM2 (H2)、TM5 (H5)和环loopE (LE1和LE2)上4个分散的氨基酸残基组成，可以作为底物过滤器起作用[13]。NPA和ar/R结构对NIPs的底物选择性具有重要意义。NIPs家族基因根据ar/R区的差异可分成三个亚族：NIP I (W、V/I、A、R)、NIP II (A、I/V、A/G、R)和NIP III (G、S、G和R)[7, 14]。
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图 1 NIPs单体蛋白结构示意图注：A和B分别代表AtNIP3;1 (At1g31885) 蛋白的二级结构和三级结构。蛋白的三级结构由Phyre2 (http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=idex) 网站预测，并通过PyMOL 3.0软件进行美化。Figure 1. Schematic diagram of structure of NIPs monomer proteinNote: A and B represent the secondary and tertiary structures of the AtNIP3;1 (At1g31885) protein, respectively. The tertiary structure of the protein is predicted by the Phyre2 website (http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=index) and beautified by PyMOL 3.0 software.2. 植物NIPs的运输底物与功能
2.1 水
水是植物生命活动的重要因子，对于植物生长发育至关重要。水分(H2O)被植物根系吸收后，在植物体内存在以下3种运输途径：质外体途径、共质体途径和跨细胞途径[1]。水通道蛋白以跨膜运水的能力而闻名，在跨细胞途径中负责水分的运输。果实的生长发育及成熟过程与水分密切相关，并受水通道蛋白基因表达的严格调控。CmNIP2;2和CmNIP5;1是两个水高效运输基因，在有裂纹的甜瓜中被诱导表达，参与甜瓜体内水分运输[15]。FaNIP1;1在草莓果实中特异性表达，受缺水胁迫显著上调表达，在维持果实膨胀中起作用[16]。CsNIP5;1具有水转运活性，超表达CsNIP5;1降低了柑橘愈伤组织透水性，增加了果实抵御水分流失的能力[17]。水稻OsNIP1;1、OsNIP2;1和OsNIP3;3[17]，大麦HvNIP1s和HvNIP2s[18]，拟南芥AtNIP4;1、AtNIP4;2[19]和AtNIP5;1[10]在异源表达系统中对水也具有渗透性，但是缺少植物中相关功能研究，参与何种生理过程仍不是很清楚。
2.2 类金属
类金属(metalliods)又叫做准金属或半金属，在元素周期表中位于金属和非金属的过渡区域。准金属包括硼(B)、硅(Si)、锗(Ge)、砷(As)、锑(Sb)、蹄(Te)和钋(Po)，有时砹(At)、硒(Se)和铝(Al)也被认为是准金属。在常见的准金属中，B是植物必需的微量营养元素，Si和Se是植物有益元素，在植物的生长发育及抵御生物和非生物胁迫等方面发挥功能；As、Sb、Ge、Al等对植物有毒，易于被作物吸收，并通过食物链进入人体危害健康。为调节类金属在植物中的吸收、转运、分布及外排，植物进化出了高效的膜转运系统。在各类转运蛋白中，水通道蛋白NIPs亚家族在类金属运输中起主要作用。
硼的主要生物学功能是可以与细胞壁果胶中两个鼠李糖半乳糖醛酸II(RG-II)进行交联，形成一种稳定且更具有延伸性的二聚化复合物，对维持细胞壁结构和功能具有重要作用[20]。硼在土壤中主要以硼酸分子(H3BO3)形态存在，这也是植物根系吸收硼的形式。BORs和NIPs是调控植物硼稳态的两类重要转运蛋白，其中BORs为外向型硼转运蛋白，而NIPs是内向型硼转运蛋白[21]。AtNIP5;1是Takano等人[10]在拟南芥中鉴定到的首个植物硼酸通道蛋白，主要在根的分生区和伸长区表达，极性定位在侧根冠细胞和表皮细胞靠近土壤一侧的质膜上，介导根从土壤中吸收硼[22]。AtNIP6;1在地上部的节点处表达，参与木质部和韧皮部间硼的转运，在维持地上部生长中起作用[23]。甘蓝型油菜是我国油菜的主要栽培品种，对低硼胁迫极其敏感且需硼较多。BnaA03.NIP5;1是利用图位克隆获得的甘蓝型油菜硼高效基因，它极性定位在根尖分生区侧根冠细胞靠土壤侧的质膜上，负责根尖硼的吸收以维持根系生长发育[24, 25, 26]。BnaA02.NIP5;1是BnaA03.NIP5;1的同源基因，在根分生区和伸长区的外皮层细胞中表达，参与从土壤中吸收硼并将硼向地上部运输[27]。OsNIP3;1是水稻质膜定位的硼酸通道蛋白，缺硼时负责优先将硼分配到发育中的组织[28]。HvNIP2;1是大麦高浓度硼适应性的重要因子，在高硼土壤中，HvNIP2;1通过降低表达量以减少根系对硼的吸收[29]。植物生殖生长对硼的需求远高于营养生长，在花器官中高度表达的基因对于花发育及植株育性具有决定性作用。AtNIP7;1在花药绒毡层表达，充当门控硼酸通道，参与花粉发育过程[30]。AtNIP4;1和AtNIP4;2是花粉特异性水通道蛋白，在缺硼时，其双敲低株系的花粉萌发率和花粉管长度显著低于野生型[19]。ZmNIP3;1 在玉米穗丝中表达量最高，促进硼向地上部顶端运输，介导花序发育过程[31]。BnaA02.NIP6;1a参与硼向地上部转运，可以恢复拟南芥nip6;1苗期缺硼敏感表型，同时还参与调节油菜花器官的发育[32]。
硅是植物生长发育的有益元素，主要以硅酸的形式(H4SiO4)被植物根系吸收，具有提高植物逆境胁迫适应性的作用[33]。水稻是典型的硅积累植物，是目前硅转运系统研究最清楚的。Ma等[34]在水稻中首次鉴定到硅内流转运基因OsNIP2;1 (Lsi1)，参与根从外部吸收硅，其突变体硅含量显著降低，使植株易于发生虫害，最终导致严重减产。OsNIP2;2 (Lsi6)是OsNIP2;1同源基因，负责从木质部卸载硅[35]，并参与维管束间硅的转运[36]。Yamaji等[37]通过构建硅分布的数学模型，发现OsNIP2;2及硅外排转运基因OsLsi2和OsLsi3位于水稻节点处表达，共同调节硅向发育组织优先分配，这种机制使得籽粒中硅含量增加，进而减少有毒有害物质积累。随后，硅转运基因在玉米(ZmNIP2;1和ZmNIP2;2)[38]、大麦(HvNIP2;1和HvNIP2;2)[39−40]和小麦(TaNIP2;1)[41]等单子叶植物中被相继报道。不同植物种类硅含量存在极显著差异，相较于单子叶植物而言，双子叶植物体内积累更少的硅。研究发现，在水稻硅吸收缺陷突变体lsi1中异源表达黄瓜水通道基因CsNIP2;1，以及在黄瓜中超表达CsNIP2;1，均显著增加了植株体内硅浓度，这说明CsNIP2;1参与黄瓜根部硅吸收[42]。番茄硅转运蛋白SlNIP2;1参与硅的吸收，但是番茄并非喜硅植物，Sun等[43]猜测番茄低硅积累特征与硅外排转运基因SlLsi2活性丧失有关。马铃薯StNIP2;1几乎不转运硅，但是施加硅肥后增加了根和叶片中StNIP2;1表达水平，这表明StNIP2;1可能在应对非生物胁迫中发挥功能[44]。拟南芥中不存在Lsi1同源基因，Montpetit[41]等首次在拟南芥中组成型表达小麦TaNIP2;1和水稻OsNIP2;1，显著增加了拟南芥中硅积累，但过多的硅对植物产生了毒害。然而，在拟南芥中采用AtNIP5;1根特异性启动子驱动TaNIP2;1表达后，植株硅含量增加，且长势正常[41]。这些研究表明硅转运蛋白基因在根中高表达时，增强了低硅积累植物根部的硅吸收能力，使植株积累更多的硅，进而提高植株抵御外界各种胁迫的能力。
硒是人类和动物必需微量营养元素之一，具有增强免疫力并降低癌症风险的功能[45]。硒在植物生长中表现出双重作用，低浓度硒可以作为植物的有益元素起作用，但硒浓度过高则对植株有毒[46]。硒酸盐和亚硒酸盐是植物吸收硒的主要形式，硒酸盐通过硫酸盐转运蛋白运输，而亚硒酸盐通过磷酸盐转运蛋白或水通道蛋白运输[45]。Zhao等[47]研究发现OsNIP2;1对亚硒酸具有渗透性，其突变体根中亚硒酸盐浓度显著降低，说明OsNIP2;1参与亚硒酸吸收。茶树具有较强的富硒能力，Ren等[48]通过转录组和蛋白组分析发现，在亚硒酸盐处理下CsNIP2;1上调表达，表明茶树CsNIP2;1基因在亚硒酸吸收方面具有潜在功能。
砷是一种具有毒性和致癌性的类金属元素，可以被植物吸收的砷包括砷酸盐(As (V))、亚砷酸盐(As (III))和甲基化砷(MMA和DMA)3种形式[49]。研究发现，磷酸盐转运蛋白(PHT)介导植物吸收As (V)，水通道蛋白参与亚砷酸(H3AsO3)和甲基化砷的吸收和转运[50]。拟南芥9个NIPs成员中有6个被证明能转运亚砷酸。AtNIP3;1[51]及硼通道蛋白AtNIP5;1、AtNIP6;1和AtNIP7;1在酵母中[52−53]可以双向运输亚砷酸，AtNIP1;1和AtNIP1;2在爪蟾卵母系统中[53]具有亚砷酸转运活性。Kamiya等[54]研究表明，AtNIP1;1参与根部亚砷酸吸收，nip1;1突变体在亚砷酸盐处理下具有强耐受性，其根长是野生型的3倍以上。Xu等[51]研究发现，在亚砷酸盐胁迫下，nip3;1突变体地上部长势显著优于其野生型。nip1;1nip3;1双突变体与其相对应的单突和野生型相比，极大提高了植株对亚砷酸盐抵抗能力，表现出更长的根系和长势更好的地上部[51]。AtNIP7;1是亚砷酸盐中等耐受基因，参与拟南芥根部亚砷酸吸收[53]。As和Si结构相似，因此硅酸转运蛋白亦可运输亚砷酸。小麦TaNIP2;1在拟南芥中异源表达后增加了植株对亚砷酸盐敏感性[55]。水稻根系通过OsNIP2;1吸收硅的同时也会导致亚砷酸流入根细胞，从而使籽粒砷污染水平增加[56]。同时，OsNIP2;1也介导亚砷酸的外排，但是仅占总砷外排的20%左右[57]。土壤中存在少量甲基化砷，OsNIP2;1对于未解离的甲基化砷也有吸收功能[58]。水稻其它NIPs成员，OsNIP1;1、OsNIP2;2、OsNIP3;1、OsNIP3;2和OsNIP3;3同样具有亚砷酸转运活性[56, 59−60]。敲除硼酸通道OsNIP3;1不影响硼的累积及产量形成，但能减少地上部砷含量[61]，这说明OsNIP3;1是适合作物品种改良并实现食品安全的潜在靶基因。
锑过量对植物有毒害作用，并对人体具有慢性毒性和致癌性[62]。锑(Sb)在土壤中有Sb(III)和Sb(V)两种无机形式，在中性条件下，Sb(III)主要以H3SbO3分子形式存在，其结构和化学性质类似于H3AsO3[63]。因此，锑可以通过亚砷酸转运蛋白进入植物体内。Kamiya等[64]发现As转运基因AtNIP1;1能运输锑，但AtNIP1;2和AtNIP5;1不转运锑，说明NIPs基因在底物选择性上存在差异。Huang等[65]研究表明OsNIP2;1具有锑转运活性，参与根部锑吸收，但是由于水稻体内缺少锑酸盐外排转运蛋白，因此进入植物体内的Sb大部分被积累在根部外皮层细胞中，向地上部转运过程被限制。
锗在自然界中是一种稀散的元素，难以形成单独矿床，通常需要依附在其它矿物中[66]。Ge作为Si的类似物，可用于鉴定硅吸收缺陷突变体[67]，锗的同位素(68Ge)和氧化锗(GeO2)也可以用做硅的示踪剂[68]。据报道，硅转运蛋白OsNIP2;1和HvNIP2;1及亚砷酸转运蛋白OsNIP3;3在异源表达系统中可以介导锗的运输[29, 60]。锗在植物中的研究多数集中在生理生化层面，而关于锗在植物中运输的分子机制尚不明确，仍需深入研究。
铝在酸性(pH＜5.5)土壤上以有毒的Al3+ 形式存在，是作物生长的主要限制因子。铝毒使植物根系严重受损，进而抑制水分和营养物质运输，为应对铝胁迫，植物进化出了铝外排和内部铝耐受两种解毒机制[69]。水通道蛋白可以运输不带电的小分子物质，而金属离子被螯合后也能被水通道蛋白家族基因转运。AtNIP1;2是定位在质膜上的铝双向通道蛋白，特异性运输苹果酸-铝(Al-Mal)，介导根部Al-Mal吸收和木质部Al-Mal装载，在拟南芥内部解铝毒机制中发挥功能[70]。Wang等[71]研究发现， AtALMT1在遗传途径上位于AtNIP1;2的上游，在铝胁迫条件下，由AtALMT1介导的铝外排机制优先被激活，随后由AtNIP1;2介导的内部铝耐受机制启动，两种机制的协同作用极大地提高了植物铝毒抗性。最新研究表明，AtNIP1;1也可以运输Al-Mal，AtNIP1;1和AtNIP1;2在铝毒条件下介导苹果酸的再利用，从而节省植物体内碳源[72]。OsNIP1;2编码的蛋白运输半胱氨酸-铝(Al-Cys)，是实现水稻内部铝毒抗性的关键基因，其突变体根细胞壁积累大量铝，铝向地上部的运输被阻断，降低了水稻对铝耐受性[73]。Wang等[73]认为，OsNIP1;2是AtNIP1;2的同源基因，二者含有相同的ar/R保守序列(WVAR)，但是NPA区存在差异(NPA/NPA; NPA/NPG)，这可能是两个基因在底物选择上存在偏好性的原因之一。
2.3 其他底物
水通道蛋白是一个具有底物多样性的转运蛋白，除了上述提到的水和类金属外，还可以运输过氧化氢、有机小分子化合物(尿素、甲酰胺、甘油和乳酸)及气体(NH3)等，在植物的信号转导、营养物质吸收和生理代谢中发挥功能。
植物在遭受逆境胁迫时会产生过氧化氢(H2O2)等活性氧(ROS)，对植物生长具有正负两种效应，在低浓度时可以作为信号分子起作用，但随着浓度的增高会对细胞造成损伤甚至死亡[74]。Sadhukhan等[75]以相对根长为指标进行拟南芥全基因组关联分析(GWAS)，鉴定到一个H2O2敏感基因AtNIP1;1，其突变体对H2O2具有耐受性。草莓FaNIP1;1蛋白能够运输H2O2，在草莓成熟过程中参与果实的氧化应激[16]。研究报道，AtNIP4;1、AtNIP4;2、OsNIP3;2和OsNIP3;3在酵母中均能转运H2O2，它们可能在应对植物氧化胁迫方面起作用[18−19]。
尿素(CH4N2O)是广泛使用的酰胺态氮肥，也是植物的氮代谢产物。土壤中的尿素分子可以直接被植物根系吸收，也可以水解为铵或进一步硝化为硝酸盐后进入植物体内[76]。尿素的主动运输由高亲和尿素转运蛋白DUR3介导，而AQPs参与尿素被动运输过程[76]。有研究表明，尿素与硼酸分子大小相近[77]，因而很可能通过硼酸通道转运尿素。AtNIP5;1、AtNIP6;1和AtNIP7;1在卵母细胞中已被证明具有尿素转运活性[78, 79, 80]。甲酰胺(CH3NO)和尿素结构相似，AtNIP6;1在卵母中也可以渗透甲酰胺[79]。AtNIP5;1是缺硼条件下植物的主要尿素通道，参与根部吸收尿素[78]。然而，AtNIP6;1基因在尿素处理的幼苗转录组中显著下调表达，这说明AtNIP6;1可能在植物中对尿素的转运和分配贡献低[78]。黄瓜CsNIP2;1促进尿素吸收，在根中受尿素诱导上调表达[81]。ZmNIP2;1和ZmNIP2;4在酵母中运输尿素，但其在玉米根部的表达量不受氮缺乏影响[82]。此外，AtNIP4;1和OsNIP2;1和在酵母中也具有尿素运输能力，AtNIP4;1还可以运输NH3，表明可能在植物氮运输和代谢方面起作用[19, 14]。
甘油(C3H8O3)具有渗透调节功能，也可以作为植物的碳源起作用[83−84]。AtNIP6;1、AtNIP7;1、AtNIP4;1和AtNIP4;2分别在卵母[79]、脂质体[30]和酵母中[19]被证明转运甘油。Zou等[85]研究发现光叶百脉根(Lotus japonicus)与丛枝菌根真菌(AMF)相互作用后，共生根中LjNIP1;5被显著上调表达，推测LjNIP1;5可能通过运输甘油为真菌提供碳源来促进丛枝菌根的生长，同时真菌给寄主植物提供水分和养分，增加植物抵抗逆境胁迫的能力。
随着洪涝灾害频繁发生，淹水胁迫成为制约植物生长和存活的重要环境因素，其实质是水分过多导致氧气减少，使植物细胞的有氧呼吸被抑制，无氧呼吸加强，进而产生乙醇、乙醛、乳酸等物质[86]。研究发现，AtNIP2;1可以运输不带电的质子化形式乳酸(C3H6O3)，在转录水平上受涝水或缺氧胁迫显著诱导[87]。随后，Beamer等人[88]证实，AtNIP2;1是一个乳酸外排通道蛋白，在厌氧胁迫下，通过将细胞质中的乳酸转运到质外体，最终排出到根际，以使植物免受乳酸毒害，增强了植物在逆境下的存活率。
综上所述，NIPs作为植物水通道蛋白家族成员，并非狭义上仅能运输水的一类蛋白，其底物运输广泛，还可以转运类金属、过氧化氢、甘油、乳酸等物质，在调节植物生长发育及抵御逆境胁迫等方面发挥重要功能(表1)。
表 1 植物NIPs家族蛋白的运输底物和功能Table 1. Substrate transport and function of NIPs family genes in plantsNIP亚族
NIP subfamily蛋白名称
Protein name底物
Substrate功能
Function参考文献
ReferenceI AtNIP1;1 H3AsO3; H3SbO3;
H2O2; Al-Mal吸收；响应氧化应激
Uptake; Response to oxidative stress[54, 64, 72, 75] I AtNIP1;2 Al-Mal; H3AsO3 提高铝毒耐受性
Improve aluminum toxicity tolerance[54, 70] I AtNIP2;1 C3H6O3 介导乳酸外排
Mediate lactic acid efflux[87−88] I AtNIP3;1 H3AsO3 参与砷吸收和向地上部转运
Involve in arsenite uptake and transport to shoot[51] I AtNIP4;1 H2O; H2O2; H3BO3 ;
CH4N2O; C3H8O3; NH3参与花粉发育和授粉过程
Involve in pollen development and pollination[19] I AtNIP4;2 H2O; H2O2; C3H8O3 参与花粉管生长过程
Involve in pollen tube growth[19] I OsNIP1;1 H3AsO3; H2O 抑制木质部装载砷
Inhibit xylem loading of arsenite[18, 60] I OsNIP1;2 Al-Cys 介导内部解铝毒
Mediate internal detoxification of aluminum[73] I FaNIP1;1 H2O; H2O2; H3BO3 维持果实膨胀；响应氧化应激
Maintain fruit expansion; Response to oxidative stress[16] I LjNIP1;5 C3H8O3 响应干旱胁迫 Response to drought stress [85] I CsNIP5;1 H2O 调节柑橘水分平衡
Regulate the water balance of citrus[17] II AtNIP5;1 H3BO3; H3AsO3; H2O; CH4N2O 缺硼条件下参与硼和尿素吸收
Participate in boron and urea absorption under
boron deficiency conditions[10, 52, 78] II AtNIP6;1 H3BO3; H3AsO3 ; CH4N2O;
C3H8O3; CH3NO负责地上部硼转运和分配
Responsible for shoot boron transport and distribute[23, 52, 79] II AtNIP7;1 H3BO3; H3AsO3 ;
CH4N2O; C3H8O3参与花粉外壁发育
Involve in pollen outer wall development[30, 53, 80] II OsNIP3;1 H3BO3; H3AsO3 转运和分配 Transport and distribute [28, 61] II OsNIP3;2 H3AsO3; H2O2 参与侧根吸收砷
Participate in the absorption of a
rsenite by lateral roots[18, 59] II OsNIP3;3 H3AsO3; H2GeO3; H2O ; H2O2 抑制木质部装载砷
Inhibit xylem loading of arsenite[18, 60] II ZmNIP3;1 H3BO3 调节花序发育
Regulate inflorescence development[31] II BnaA3.NIP5;1 H3BO3 负责根尖硼吸收以促进根系伸长
Responsible for root tip uptake boron
to promote root elongation[26−27] II BnaA2.NIP5;1 H3BO3 参与硼吸收和向地上部转运
Involve in boron uptake and transport to the shoot[27] II BnaA2.NIP6;1a H3BO3 调节花器官发育
Regulate the development of flower organs[32] II CmNIP5;1 H2O 参与甜瓜开裂过程的水分运输
Involve in water transport during the
cracking process of Cucumis melo[15] III OsNIP2;1 H4SiO4; H2SeO3; H3AsO3; H3SbO3;
H2GeO3; H2O; CH4N2O; MMA; DMA吸收和外排 Uptake and efflux [14, 18, 29, 34, 47,
56, 57, 58, 65]III OsNIP2;2 H4SiO4; H3AsO3 转运和分配 Transport and distribute [35, 37, 56] III ZmNIP2;1 H4SiO4; CH4N2O 吸收和转运 Uptake and transport [38, 82] III ZmNIP2;2 H4SiO4 木质部卸载硅
Unloading silicon from the xylem[38] III ZmNIP2;4 CH4N2O 吸收和转运 Uptake and transport [82] III HvNIP2;1 H4SiO4; H3BO3; H3AsO3;
H2GeO3; H2O增强硼毒适应性；介导硅吸收
Enhance boron toxicity adaptability;
Mediate silicon uptake[18, 29, 39] III HvNIP2;2 H4SiO4; H2O 参与硅吸收和转运
Involve in silicon uptake and transport[18, 40] III TaNIP2;1 H4SiO4; H3AsO3 吸收和转运 Uptake and transport [41, 55] III CsNIP2;1 H4SiO4; CH4N2O 吸收 Uptake [42, 81] III SlNIP2;1 H4SiO4 介导硅吸收 Mediate silicon absorption [43] III StNIP2;1 H4SiO4 响应非生物胁迫信号
Response to abiotic stress signals[44] III CmNIP2;2 H2O 参与甜瓜开裂过程的水分运输
Involve in water transport during the
cracking process of Cucumis melo[15] III CsNIP2;1 H2SeO3 介导茶树吸收硒
Mediate the uptake of selenium in Camellia sinensis[48] 注：At—拟南芥；Os—水稻；Zm—玉米；Hv—大麦；Ta—小麦；Bna—甘蓝型油菜；Fa—草莓；Cm—甜瓜；Cs—柑橘、黄瓜、茶树；Sl—番茄；St—马铃薯；Lj—光叶百脉根。
Note: At— Arabidopsis thaliana; Zm—Zea mays; Hv—Hordeum vulgare; Ta—Triticum aestivum; Bna—Brassica napus; Fa—Fragaria ananassa; Cm—Cucumis melo; Cs—Citrus、Cucumis sativus、Camellia sinensis; Sl—Solanum lycopersicum; St—Solanum tuberosum; Lj—Lotus japonicus.3. 植物NIPs调控机制
NIPs蛋白在植物中丰度和活性受多种机制严格调节，主要包括转录调控、翻译后修饰、蛋白质寡聚化和门控机制等。明确NIPs调控机制，对于理解NIPs基因在植物中特异性表达及发挥的功能具有重要意义。
3.1 转录调控
转录调控是基因表达的关键步骤，但调节速度相对缓慢。NIPs基因在转录水平上的调控与逆境胁迫、植物器官和发育阶段紧密相关，已被大量文献报道。转录因子作为一种重要的调控因子，可以与NIPs启动子区结合以激活或抑制基因表达。在缺硼条件下，NGAL1转录因子正向调控硼运输基因AtNIP5;1、AtNIP6;1、AtNIP7;1和AtBOR1表达上调，而在高硼条件下AtBOR4被诱导表达，这表明NGAL1在调节植物体内硼稳态方面发挥作用[89]。BnaA9.WRKY47转录因子可以与BnaA03.NIP5;1的启动子直接结合并激活其表达，正向调控甘蓝型油菜对低硼胁迫的适应性[90]。CsWRKY4激活CsNIP5;1表达，CsWRKY28则抑制CsNIP5;1表达，可能在柑橘采后贮藏期间的水分平衡和衰老过程起作用[91]。OsARM1是R2R3型MYB转录因子，通过负调控As转运基因OsNIP2;1、OsNIP2;2和OsLsi2表达来调节水稻As的吸收和转运[92]。DNA甲基化属于表观遗传学调控机制，通常会抑制基因的转录[93]。AtVIM1作为DNA甲基化调节因子，通过增强AtNIP3;1启动子中CpG位点的甲基化水平来降低其表达量，以减少根部亚砷酸吸收和向地上部的转运，提高植株对亚砷酸抗性[94]。
3.2 翻译后修饰
蛋白质翻译后修饰包括磷酸化、甲基化、泛素化和糖基化等过程[95]。磷酸化是NIPs蛋白最常见的一种修饰，研究发现，在NIPs氨基末端或羧基末端上存在保守的磷酸化位点，可以被蛋白激酶磷酸化来调节其活性[12]。AtNIP7;1、AtNIP4;1和AtNIP4;2的C末端在体外分别被AtMPK4和AtCPK34磷酸化[12, 19]。Wang等[96]研究揭示AtNIP5;1在质膜上的极性定位依赖于N末端三个TPG (Thr-Pro-Gly)序列中Thr残基的磷酸化，并且这种极性定位的稳定性需要由网格蛋白所介导的内吞作用来维持。
3.3 蛋白质寡聚化
蛋白质很少单独起作用，通常与其它蛋白质相互结合形成多亚基复合物来行使生物学功能。据报道，水通道蛋白多以同源四聚体形式存在，有时也形成异源四聚体，与蛋白的亚细胞定位和底物运输活性相关。例如，水通道蛋白亚族PIP1s单独表达时无活性，与PIP2s相互作用可以使其亚细胞定位发生变化，以调控蛋白功能[97]。Zhang等[17]研究发现，CsNIP5;1与PIPs互作后使其从质膜定位改变为“甜甜圈”状结构，增强了柑橘抵御渗透压和抗水分流失的能力。此外，NIPs还可以与其它蛋白质进行物理相互作用。AtNIP1;1在酵母中定位在质膜和内质网上[72]。研究揭示，AtCPK31与AtNIP1;1在细胞质膜上互作，正向调节拟南芥根系亚砷酸吸收[98]。AtSYP51与定位在内质网上的AtNIP1;1相互作用，影响了植株体内亚砷酸积累[99]。
3.4 门控机制
门控机制受pH值、磷酸化、蛋白质间相互作用等因子调节，是一种快速调控方式，可以直接操控植物水通道蛋白孔道的开和关，调节底物跨膜运输过程。Li等研究发现[80]，AtNIP7;1的硼酸转运活性受H2上保守酪氨酸残基(Tyr81)调节，Tyr81与Arg220互作使孔道闭合，当用Cys取代Tyr81后，孔道则打开，在花粉发育过程中充当门控硼酸通道。
4. 总结与展望
自1993年发现第一个植物水通道蛋白以来，越来越多的水通道蛋白家族成员在不同植物物种中被挖掘和鉴定。NIPs作为水通道蛋白家族一类仅在植物中存在的亚族，具有广泛的底物选择性和功能多样性(图2)。AtNIP4;1、AtNIP4;2、AtNIP7;1、ZmNIP3;1和BnaA2.NIP6;1a是影响植株育性的关键基因；FaNIP1;1、CmNIP2;2、CmNIP5;1和CsNIP5;1是维持果实水分稳态的关键基因；单子叶植物NIP2;1和NIP2;2主要介导硅运输，是提高植株非生物胁迫适应性的重要基因；AtNIP2;1是缺氧时增加植物存活率的关键基因；LjNIP5;1在与微生物AMF建立共生关系中起作用；AtNIP6;1和OsNIP3;1，AtNIP5;1、BnaA2.NIP5;1和BnaA3.NIP5;1分别是低硼条件下维持地上部和根系正常生长的重要基因；AtNIP1;2和OsNIP1;2是内部解铝毒的关键基因；AtNIP1;1和OsNIP3;2是亚砷酸吸收的基因，AtNIP3;1、OsNIP1;1、OsNIP3;1和OsNIP3;3是亚砷酸转运的关键基因，在抑制亚砷酸向地上部运输并减少籽粒亚砷酸积累中发挥功能。总的来说，植物NIPs基因通过吸收、转运、分配和外排多种物质，以提高植株在复杂生长环境中的适应性。因此，可将NIPs作为培育高抗逆性作物的潜在功能基因，利用分子生物学技术对候选基因进行敲除或超表达，能够有效增加必需营养元素或有益元素的吸收，降低有毒元素在体内积累，进而保障食品安全和人体健康。关于NIPs底物运输方面，尽管已经在酵母和卵母异源表达体系中明确一个基因可以运输多个底物，但是所转运的这些底物在植物中是否都具有功能，参与何种生理过程仍有很多未知之处，未来需要继续研究并完善其在植物中的作用。此外，相较于其它水通道蛋白，NIPs在植物中的表达量较低，并且存在器官、组织和细胞特异性[12]，其表达调控机制复杂，受到转录水平、翻译后水平、蛋白质与蛋白质相互作用和门控等机制的严格调节。目前，与NIPs表达调控机制有关的研究偏少，且现有的研究更多集中在转录水平上，而在蛋白层面上的机制仍需深入挖掘。未来可利用多种组学联合生物信息学技术进一步探究NIPs调控网络，并通过结构生物学等技术深入解析NIPs蛋白结构和功能位点，这对于系统认识NIPs在植物整个生命周期中所发挥的功能具有重要意义，同时也为作物育种提供了理论参考和基因资源。
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图 2 植物中NIPs生物学功能的模式图Figure 2. Pattern diagram of biological functions of NIPs in plants -
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图 1 NIPs单体蛋白结构示意图
注：A和B分别代表AtNIP3;1 (At1g31885) 蛋白的二级结构和三级结构。蛋白的三级结构由Phyre2 (http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=idex) 网站预测，并通过PyMOL 3.0软件进行美化。
Figure 1. Schematic diagram of structure of NIPs monomer protein
Note: A and B represent the secondary and tertiary structures of the AtNIP3;1 (At1g31885) protein, respectively. The tertiary structure of the protein is predicted by the Phyre2 website (http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id=index) and beautified by PyMOL 3.0 software.
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图 2 植物中NIPs生物学功能的模式图
Figure 2. Pattern diagram of biological functions of NIPs in plants
表 1 植物NIPs家族蛋白的运输底物和功能
Table 1 Substrate transport and function of NIPs family genes in plants
NIP亚族
NIP subfamily蛋白名称
Protein name底物
Substrate功能
Function参考文献
ReferenceI AtNIP1;1 H3AsO3; H3SbO3;
H2O2; Al-Mal吸收；响应氧化应激
Uptake; Response to oxidative stress[54, 64, 72, 75] I AtNIP1;2 Al-Mal; H3AsO3 提高铝毒耐受性
Improve aluminum toxicity tolerance[54, 70] I AtNIP2;1 C3H6O3 介导乳酸外排
Mediate lactic acid efflux[87−88] I AtNIP3;1 H3AsO3 参与砷吸收和向地上部转运
Involve in arsenite uptake and transport to shoot[51] I AtNIP4;1 H2O; H2O2; H3BO3 ;
CH4N2O; C3H8O3; NH3参与花粉发育和授粉过程
Involve in pollen development and pollination[19] I AtNIP4;2 H2O; H2O2; C3H8O3 参与花粉管生长过程
Involve in pollen tube growth[19] I OsNIP1;1 H3AsO3; H2O 抑制木质部装载砷
Inhibit xylem loading of arsenite[18, 60] I OsNIP1;2 Al-Cys 介导内部解铝毒
Mediate internal detoxification of aluminum[73] I FaNIP1;1 H2O; H2O2; H3BO3 维持果实膨胀；响应氧化应激
Maintain fruit expansion; Response to oxidative stress[16] I LjNIP1;5 C3H8O3 响应干旱胁迫 Response to drought stress [85] I CsNIP5;1 H2O 调节柑橘水分平衡
Regulate the water balance of citrus[17] II AtNIP5;1 H3BO3; H3AsO3; H2O; CH4N2O 缺硼条件下参与硼和尿素吸收
Participate in boron and urea absorption under
boron deficiency conditions[10, 52, 78] II AtNIP6;1 H3BO3; H3AsO3 ; CH4N2O;
C3H8O3; CH3NO负责地上部硼转运和分配
Responsible for shoot boron transport and distribute[23, 52, 79] II AtNIP7;1 H3BO3; H3AsO3 ;
CH4N2O; C3H8O3参与花粉外壁发育
Involve in pollen outer wall development[30, 53, 80] II OsNIP3;1 H3BO3; H3AsO3 转运和分配 Transport and distribute [28, 61] II OsNIP3;2 H3AsO3; H2O2 参与侧根吸收砷
Participate in the absorption of a
rsenite by lateral roots[18, 59] II OsNIP3;3 H3AsO3; H2GeO3; H2O ; H2O2 抑制木质部装载砷
Inhibit xylem loading of arsenite[18, 60] II ZmNIP3;1 H3BO3 调节花序发育
Regulate inflorescence development[31] II BnaA3.NIP5;1 H3BO3 负责根尖硼吸收以促进根系伸长
Responsible for root tip uptake boron
to promote root elongation[26−27] II BnaA2.NIP5;1 H3BO3 参与硼吸收和向地上部转运
Involve in boron uptake and transport to the shoot[27] II BnaA2.NIP6;1a H3BO3 调节花器官发育
Regulate the development of flower organs[32] II CmNIP5;1 H2O 参与甜瓜开裂过程的水分运输
Involve in water transport during the
cracking process of Cucumis melo[15] III OsNIP2;1 H4SiO4; H2SeO3; H3AsO3; H3SbO3;
H2GeO3; H2O; CH4N2O; MMA; DMA吸收和外排 Uptake and efflux [14, 18, 29, 34, 47,
56, 57, 58, 65]III OsNIP2;2 H4SiO4; H3AsO3 转运和分配 Transport and distribute [35, 37, 56] III ZmNIP2;1 H4SiO4; CH4N2O 吸收和转运 Uptake and transport [38, 82] III ZmNIP2;2 H4SiO4 木质部卸载硅
Unloading silicon from the xylem[38] III ZmNIP2;4 CH4N2O 吸收和转运 Uptake and transport [82] III HvNIP2;1 H4SiO4; H3BO3; H3AsO3;
H2GeO3; H2O增强硼毒适应性；介导硅吸收
Enhance boron toxicity adaptability;
Mediate silicon uptake[18, 29, 39] III HvNIP2;2 H4SiO4; H2O 参与硅吸收和转运
Involve in silicon uptake and transport[18, 40] III TaNIP2;1 H4SiO4; H3AsO3 吸收和转运 Uptake and transport [41, 55] III CsNIP2;1 H4SiO4; CH4N2O 吸收 Uptake [42, 81] III SlNIP2;1 H4SiO4 介导硅吸收 Mediate silicon absorption [43] III StNIP2;1 H4SiO4 响应非生物胁迫信号
Response to abiotic stress signals[44] III CmNIP2;2 H2O 参与甜瓜开裂过程的水分运输
Involve in water transport during the
cracking process of Cucumis melo[15] III CsNIP2;1 H2SeO3 介导茶树吸收硒
Mediate the uptake of selenium in Camellia sinensis[48] 注：At—拟南芥；Os—水稻；Zm—玉米；Hv—大麦；Ta—小麦；Bna—甘蓝型油菜；Fa—草莓；Cm—甜瓜；Cs—柑橘、黄瓜、茶树；Sl—番茄；St—马铃薯；Lj—光叶百脉根。
Note: At— Arabidopsis thaliana; Zm—Zea mays; Hv—Hordeum vulgare; Ta—Triticum aestivum; Bna—Brassica napus; Fa—Fragaria ananassa; Cm—Cucumis melo; Cs—Citrus、Cucumis sativus、Camellia sinensis; Sl—Solanum lycopersicum; St—Solanum tuberosum; Lj—Lotus japonicus.
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