生长素及其运输蛋白对植物铝胁迫的响应_吴道铭
植物生理学报 Plant Physiology Journal 2014, 50 (8): 1135~1143 doi: 10.13592/https://www.360docs.net/doc/047381026.html,ki.ppj.2014.01681135
收稿 2014-04-18 修定 2014-06-18
资助 国家自然科学基金项目(30471040、31172026和31372125)
和国际科学基金(C/3042-1、C/3042-2和C/3042-3)。
* 通讯作者(E-mail: hshen@https://www.360docs.net/doc/047381026.html,; Tel: 020-********)。
生长素及其运输蛋白对植物铝胁迫的响应
吴道铭, 曹华苹, 沈宏*
华南农业大学资源环境学院, 广州510642摘要: 铝对植物的毒害作用主要表现为抑制根尖生长, 而根尖生长与生长素及其运输密切相关, 铝可能影响了生长素及其代谢过程, 但目前尚不清楚生长素及其运输蛋白如何参与植物应对铝胁迫响应。本文通过分析、总结前人研究, 并结合自己的前期研究结果, 初步阐述生长素或其运输蛋白对植物铝胁迫的响应, 即铝影响生长素代谢的相关基因, 干扰根尖生长素运输蛋白在细胞内分布及其囊泡运输, 调控生长素的极性运输, 进而抑制根尖生长。另一方面, 生长素或其运输蛋白又参与了植物应对铝胁迫过程, 这主要体现在参与了植物铝毒信号传递、根系铝内置化过程和减缓铝诱导的氧化胁迫。最后, 本文提出了生长素及其运输蛋白对植物铝胁迫响应的可能模型。关键词: 铝胁迫; 生长素; PINs 蛋白; 信号传递; 内吞作用
Response of Auxin and Its Transporter to Aluminum Stress in Plants
WU Dao-Ming, CAO Hua-Ping, SHEN Hong *
College of Resources and Environment, South China Agricultural University, Guangzhou 510642, China
Abstract: The main symptom of aluminum (Al) toxicity is a rapid inhibition of root tip growth. The growth of root tip is associated with auxin and its transportation. It is hypothesized that Al might in ? uence auxin and its metabolic processes. In this review, we tried to elucidate the response of auxin to Al stress by summarizing pre-viously published studies and our preliminary results. It is suggested that Al affects gene expression related to auxin metabolism and its cellular distribution, thus inhibits root growth. On the other hand, auxin and its trans-port protein are involved in the response to Al toxicity such as signal transmitting, Al internalizing, and reactive oxygen species regulating. Finally, a model is put forward to explain the response of auxin and its transporation to Al stress.
Key words: aluminum stress; auxin; PINs protein; signal transmitting; endocytosis 生长素(auxin)广泛存在各种植物中, 参与了植物许多生长发育过程, 如顶端优势、根系发育和向性生长等(Benjamins 和Scheres 2008; Vanneste 和Friml 2009)。目前发现的生长素运输载体主要有五种, 分别是负责向细胞内运输生长素的载体AUX1 (AUXIN-RESISTANT1)/LAXs (AUX1-LIKEs)蛋白家族、向细胞外运输生长素的载体P I N s (P I N -F O R M E D s )蛋白家族和A B C B (ATP-binding-cassette B)/PGP (P-glycoprotein)蛋白家族(Grunewald 和Friml 2010)、介导细胞内生长素运输的PILS (PIN-LIKES)蛋白家族(Barbez 等2012)以及定位于液泡膜介导由细胞质与液泡间生长素运输的WAT1 (WALLS ARE THIN1)蛋白(Ranocha 等2013)。据报道, 在模式植物拟南芥中, AUX1家族有AUX1、LAX1、LAX2和LAX3共4个成员; PINs 蛋白家族有8个成员, 分别命名为PIN1~PIN8 (Petrá?ek 等2006); ABCB 蛋白家族有21
位成员, 但目前发现只有ABCB1、ABCB4、ABCB19和ABCB21共4个成员参与生长素运输(Geisler 等2005; Kube?等2012; Yang 等2013); PILS 蛋白家族有7个成员, 分别是PILS1~PILS7 (Barbez 等2012); WAT1是否有其他同源蛋白尚未清楚(Ranocha 等2013)。依赖于这些蛋白作用, 生长素在细胞间运输, 实现在植物组织或器官中建立不对称分布, 进而发挥对植物生长发育的调控作用。铝的毒害作用被认为是酸性土壤中植物生长最主要的限制因素之一(Kochian 等2004)。铝对植物的最主要毒害作用是抑制根尖的生长, 并且这种抑制作用最早可以表现在铝处理的15 min 内(Krtková等2012)。另一方面, 植物根尖生长又主要
植物生理学报
1136受生长素调控, 那么, 铝是否影响生长素及其代谢, 生长素及其转运蛋白又如何响应植物铝胁迫？1 铝影响根尖生长素极性运输
植物体内生长素主要形成于幼嫩的叶片, 然后通过极性运输(polar transport)输送到植物根尖(Zhao 2010)。根尖生长素在PIN 蛋白家族参与作用下, 通过向顶运输(acropetal transport)和向基运输(basipetal transport)的“伞形”运输, 建立起根尖各部分生长素不对称分布, 进而影响植物根尖生长(图1) (Petrá?ek 等2006; Wi ?niewska 等2006)。如果根尖生长素的向顶运输受影响, 即由基部向根尖运输的生长素受阻, 易造成根尖生长素不足, 进而影响根尖分生区细胞分裂和根系生长; 而当根尖生长素向基运输, 即由根尖分生区向伸长区的生长素运输受抑制, 将导致根尖分生区和过渡区生长素过多累积而伸长区生长素不足, 进而造成根尖膨胀和根系伸长受抑制(Friml 2003)。Kollmeier 等(2000)发现, 与生长素运输抑制剂N PA (1-N-naph-thylphalamic acid)和TIBA (2,3,5-triiodo-benzoic acid)一样, 铝也能抑制玉米根尖生长素的向基运输, 导致大部分生长素累积在分生区和过
渡区, 进而干扰细胞分裂和抑制根系生长(Donche-va 等2005); 而在伸长区外加适量生长素, 铝对根系生长的抑制作用会得到一定缓解。Shen 等(2008)在拟南芥上的研究也表明, 铝主要抑制根尖过渡区生长素运输, 这种抑制率高达66%。
铝是如何影响生长素运输的？生长素主要通过囊泡途径的实现胞内运输。这种囊泡主要借助细胞骨架肌动蛋白微丝(actin filaments)的延伸或挪动实现运输(Geldner 等2003; Blilou 等2005; Maisch 和Nick 2007), 肌动蛋白微丝被固定(stabi-lized)、捆绑(bundled)或破坏(impaired)都会影响生长素的运输(Dhonukshe 等2008; Nick 等2009)。Siv-aguru 等(1999)借助酶联免疫法, 观察到短时间的铝处理会导致玉米根尖过渡区细胞的肌动蛋白微丝发生明显变化。Ahad 和Nick (2007)则注意到, 受铝处理影响, 这些肌动蛋白微丝捆成束状, 并以细胞核为中心向周围扩散。Shen 等(2008)借助拟南芥肌动蛋白微丝GFP 标记材料, 通过激光共聚焦技
术观察到2 h 的100 μmol ?L -1 Al 3+
处理, 会导致根尖过渡区细胞肌动蛋白微丝排列发生无序化。Amenós 等(2009)在玉米根尖过渡区细胞也观察到类似结果。在运输载体方面, Shen 等(2008)发现铝会增强PIN2基因的转录表达, 并诱导PIN2蛋白大量累积于细胞膜。Sun 等(2010)也发现铝对AUX1和PIN2基因表达均有影响, 这种影响与乙烯有关, 铝诱导根尖大量乙烯产生, 乙烯则会作为信号分子进一步影响AUX1和PIN2基因表达, 并干扰这两者介导的生长素极性运输。根据上述结果, 我们初步猜测铝在分子水平上会影响运输载体相关基因AUX1和PIN2的转录表达, 在细胞水平上破坏肌动蛋白微丝, 阻碍运输载体囊泡蛋白向胞内运输, 进而干扰生长素运输。
2 生长素及其运输载体对植物铝耐性影响
铝抑制植物根尖生长的机制是极其复杂的。目前认为影响根尖细胞生长和细胞分裂是铝抑制根尖生长的主要原因(Poschenrieder 等2009)。铝会改变细胞壁成分, 如果胶、纤维素和半纤维素等含量和性质; 铝诱发活性氧产生和累积; 铝改变质
膜两侧H +、K +和Ca 2+
平衡; 这些影响导致细胞壁变脆, 质膜去极化和过氧化, 进而抑制根尖细胞生长
(Horst 等2010)。铝影响根尖细胞分裂方面, 主要表
图1 PIN 蛋白在根尖的定位及生长素运输Fig.1 Localization of PIN proteins and auxin flux
参考Blilou 等(2005)、Petrá?ek 等(2006)、Wi ?niewska 等(2006)、Kleine-Vehn 和Friml (2008)
文献修改。
吴道铭等: 生长素及其运输蛋白对植物铝胁迫的响应1137
现为铝抑制S期DNA复制(Doncheva等2005)。为减缓铝毒害作用, 植物自身也进化出复杂的耐铝机制。植物启动耐铝机制, 主要分以下几步: (1)通过一些信号物质感受铝毒信号, 并将铝毒信号传递回细胞核(Kochian等2004); (2)细胞核获知铝毒信号后, 激活定位于细胞核的上游转录调控因子的基因表达, 如拟南芥中的STOP1 (Iuchi等2007), 在水稻中发现的ART1 (Yamaji等2009); (3)这些上游基因则会进一步调控参与解铝毒基因表达, 启动外部和内部耐铝机制, 如调节有机酸分泌(Shen等2005), 将铝固定于细胞壁或分室于液泡, 通过主动运输将Al3+排出胞外等(Delhaize等2012); (4)启动细胞自我修复, 如启动抗氧化系统清除活性氧, 启动程序化死亡(Zhan等2013)。相关研究表明, 生长素或其运输载体直接或间接参与了这些解铝毒过程。
2.1生长素可能是解铝毒过程中重要信号物质
根尖过渡区(root transition zone)是植物最先感受铝毒信号的区域, 而铝抑制根系伸长主要表现为抑制根尖伸长区(elongation zone)的细胞伸长(Sivaguru和Horst 1998; Rangel等2007)。Kollmeier 等(2000)发现, 仅仅在伸长区进行铝处理是不会抑制根系伸长的, 而在过渡区的铝处理会明显抑制根系伸长。因而他们推测在过渡区和伸长区之间应该存在某些信号途径, 负责将过渡区感受到的铝信号转导到伸长区。基于铝会影响从分生区到伸长区的生长素流, 一定程度上将流向伸长区的生长素截留在过渡区的结果, 他们推测这种铝信号转导可能是生长素介导的。生长素是一种重要的信号分子, 通过信号途径对植物生长发育发挥调控作用(Friml和Wisniewska 2005)。生长素信号途径主要由受体识别生长素信号、信号转导及下游基因响应等三部分构成。目前发现, 生长素受体主要有生长素结合蛋白1 (auxin binding protein 1, ABP1)和运输抑制剂响应蛋白1 (transport inhibi-tor resisrant 1, TIR1), 在信号转导过程中的关键蛋白有Aux/IAA蛋白、生长素响应因子(auxin re-sponse factors, ARFs)和SCF复合体(Mockaitis和Es-telle 2008; Santner和Estelle 2009)。生长素信号途径大概过程表现为: (1)在低浓度生长素的情况下, ABP1识别生长素信号, Aux/IAA与其他转录抑制子共同抑制ARF的转录激活功能, 并进一步阻止下游响应基因转录; (2)生长素浓度升高时, 生长素起分子胶作用, 将Aux/IAA蛋白与ARFs和SCF复合体SCF TIR1结合, 形成SCF TIR1-生长素-Aux/IAA复合体, 之后Aux/IAA被26S蛋白酶体途径降解, Aux/IAA 对ARF的抑制被解除, ARF转录激活下游响应基因转录。
microRNAs (miRNAs)在生长素信号转导的调控中扮演重要角色(J o n e s-R h o a d e s等2006; Sanan-Mishra等2013)。目前, 发现与生长素信号转导有关的miRNAs主要有6个, 分别是miR160、miR167、miR164、miR390、miR393以及豆科特有的miR1514。miR160的靶基因是ARF10、ARF16和ARF17 (Rhoades等2002); miR167可以负调控ARF2、ARF6和ARF8 (Williams等2005); miR164和miR1514主要对下游响应基因NAC家族起作用(Guo等2005; Song等2011); miR390直接靶基因是ARF2、ARF3和ARF4 (Marin等2010); miR393的靶基因则与生长素受体有关, 如TIR1、AFB1、AFB2和AFB3 (Gray等2001)。这些miRNAs 的表达会不同程度受铝处理影响(表1), 而这些miRNAs的表达变化又进一步作用于下游与生长素信号有关的靶基因, 如AFRs基因。这表明, miR-NAs介导的生长素信号转导可能在植物耐铝机制中扮演重要角色(Mendoza-Soto等2012; Gupta等2014; He等2014)。
生长素作为信号物质参与植物解铝毒过程, 可能与一氧化氮存在协同作用。一氧化氮是生长素的下游信号物质, 它们通过相互调控对方在植株内水平, 来调控各种生理活动(Fernández-Marcos
表1 参与生长素信号应答并受铝处理影响的miRNAs
Table 1 List of miRNAs target auxin signal transduction
under Al stress
miRNAs 物种对铝响应作用靶基因文献
miR390 苜蓿下调ARFs Chen等2012大豆上调ARFs Zeng等2012 miR393 苜蓿上调TIR1/AFBs Zhou等2008大豆上调TIR1 Zeng等2012
水稻下调TIR1 Lima等2011 miR160 水稻上调ARF16 Lima等2011大豆下调ARFs Zeng等2012
苜蓿下调ARF10和ARF16 Chen等2012 miR167 烟草上调ARF6和ARF8 Burklew等2012 miR164 大豆下调NAC1 Zeng等2012 miR1514 大豆上调NACs Zeng等 2012
植物生理学报1138
等2011; Terrile等2012)。一氧化氮对植物耐铝性具有重要影响(Tian等2007; Wang等2010; He等2012a)。He等(2012b)认为一氧化氮提高植物耐铝性可能与植物激素有关, 一氧化氮通过调控植物体内各种植物激素的平衡, 如ABA/GA、IAA/GA、ABA/(IAA +GA+ ZR)和IAA/ZR的平衡, 建立复杂的信号网络, 进而调控植物的各种耐铝机制。
2.2生长素及其运输载体影响铝内置化
将铝内置无毒化是植物重要的耐铝机制。其主要表现为, 植物将吸收的铝以无毒或毒性较小的化合物储存起来或将毒性较大的铝离子储存在细胞内非敏感部位, 如内源有机酸、蛋白质或其它有机化合物与铝离子发生螯合作用, 变成毒性较小的化合物, 将铝储存在液泡、表皮等中(Ma等1997, 2014; Ma和Furukawa 2003; Kochian等2004; Klug和Horst 2010)。而在这个机制中, 铝进入细胞是关键。目前的研究表明, 铝可能通过两种途径进入细胞内。这两种途径分别是通过转运蛋白(Larsen等2005, 2007; Huang等2009, 2012; Xia等2010, 2013)和借助内吞途径(Vázquez 2002; Illé?等2006; Shen等2008; Krtková等2012)。在这两种途径中, 生长素或其运输载体可能扮演着某些角色。
通过突变体筛选, Larsen等(2005, 2007)推测拟南芥类ABC转运蛋白ALS3和half-size ABC转运蛋白ALS1可能参与细胞铝内置化。ALS3主要定位于质膜, 其可能负责根尖细胞铝的再次分布(Larsen等2005)。而ALS1主要定位于液泡膜, 可能负责铝向液泡中运输, 进而将铝隔离在液泡中(Larsen等2007)。Zhu等(2013)通过morin染色标记细胞内铝分布发现, 外源加入人工合成生长素NAA处理会促进铝内置化。结合NAA处理也会影响ALS1表达, 他们猜测生长素可能通过调控ALS1表达来参与细胞铝内置化。由于ALS1基因的启动子区没有生长素响应元件TGTCTC, 因此排除NAA直接调控ALS1表达的可能性。在这个过程中, 生长素NAA扮演的具体角色, 目前尚未清楚。
内吞作用(endocytosis)是植物根系细胞通过质膜变形运动将细胞外物质转入细胞内的重要手段(Irani和Russinova 2009)。Vázquez (2002)通过透射电镜观察发现, 20 μmol?L-1 Al3+处理96 h后, 玉米根尖过渡区(2 mm)细胞的细胞壁与细胞膜间、内质体和液泡内均出现一定量具有多层结构的髓磷脂象(myelin figures), 并且在这些髓磷脂象中均观察到铝结合物(Al-phytin), 由此他推测这些髓磷脂象可能参与铝的内置化。这些髓磷脂象, 也就是Balu?ka等(2005)发现的多层膜内吞体(multilamel-lar endosomes), 它们主要由高尔基体产生, 在细胞壁果胶和木葡聚糖的内吞过程中扮演重要角色。越来越多的研究, 根尖细胞壁是铝累积的主要部位, 而果胶和木葡聚糖则是细胞壁中结合铝的主要组份(Horst等1999; Schmohl和Horst 2000; Yang 等2011a; Zhu等2012)。由此推测, 铝处理过程中, 铝伴随果胶和木葡聚糖的内吞至胞内可能是铝进入细胞的一种途径。Illé?等(2006)借助FM4-64标记内吞体或质膜, morin标记铝, 经50 μmol?L-1 Al3+处理30 min, 在拟南芥根尖分生区和远端过渡区细胞内观察到FM4-64和morin互相重合干涉的有趣现象, 进一步验证了铝可能通过内吞途径进入细胞。有意思的是, 受铝处理影响, 这些区域也观测到NO的累积。鉴于这些区域也是生长素活跃区、生长素易受NO影响以及生长素的极性运输和胞间转运也依赖于内吞途径等这三种因素, 他们推测这些区域的铝内置化与生长素运输存在一定联系。
生长素运输载体PINs蛋白通过囊泡运输来完成在质膜与细胞内部之间循环(Geldner等2003; Kleine-Vehn等2008, 2011)。其主要过程如下: PINs 蛋白通过网格蛋白介导的内吞作用(clathrin medi-ated endocytic, CME)从质膜进入早期内吞小泡(early endosomes, EE), 之后有两条途径, 一条是进入后期内吞小泡(late endosomes)或液泡前体区室(prevacuolar compartment, PVC), 并最终到达液泡降解; 另一条是借助循环小泡(recycling endosomes, RE)再回到质膜上, 从而完成极性循环(polarrecy-cling) (Lam等2007; Robinson等2008)。在拟南芥中, PIN2蛋白是唯一一个特异性定位于根尖分生区到伸长区的表皮和皮层表达, 并负责生长素在皮层的向基运输和在表皮的向顶运输(图1) (Blilou 等2005; Paponov等2005; Men等2008; Kleine-Vehn 和Friml 2008)。生长素运输蛋白PIN2主要在表层细胞, 位于根系表层, 与其他PINs蛋白(如PIN1、PIN3、PIN4、PIN7等)相比, PIN2蛋白更容易、更
吴道铭等: 生长素及其运输蛋白对植物铝胁迫的响应1139
早感受到铝的毒害作用(Shen 等2008; Sun 等
2010)。Shen 等(2008)在拟南芥上研究发现, 铝增强PIN2基因表达, 并且对PIN2蛋白的囊泡运输产生了影响。进一步的实验发现, 与伸长区细胞相比, 拟南芥根尖过渡区PIN2蛋白的囊泡运输频率很高并且铝吸收量多。借助PIN2的GFP 标记拟南芥材料, 我们发现正常生长时, PIN2蛋白在细胞水平方向分布较为均匀(图2-A 和B); 而铝胁迫处理时, PIN2蛋白在根尖细胞水平方向分布发生变化, 表现为细胞膜上的PIN2蛋白呈簇状集中, 并向胞内运动(图2-C 和D)。可见, 铝处理条件下, 细胞膜上的PIN2蛋白分布和囊泡运输发生了变化。高频率的囊泡内吞循环是否直接与较多的铝运输相关？更多的直接证据需要更为深入的研究。
μmol ?L -1 Al 3+和50 μmol ?L -1 IAA 协同处理可以诱导小麦根尖分泌更多的苹果酸。Wang 等(2013)也观察到类似的现象, 并且注意到外加IAA 会显著减少根尖铝累积, 他们推测可能是IAA 促进分泌更多的苹果酸将根际铝离子络合, 进而减少小麦对铝的吸收。铝胁迫促使活性氧累积, 进而加剧对植物毒害作用, 清除活性氧也是植物减缓铝毒害的一种机制(Yamamoto 等2002; Kochian 等2004; Navas-cués 等2012)。Krishnamurthy 和Rathinasabapathi (2013)发现, 生长素及其运输蛋白AUX1可以通过调控ROS 信号来提高植物耐受砷诱导的活性氧毒害能力。我们的结果则发现, 与野生型相比, 拟南芥PIN2缺失突变体根系生长对铝更为敏感, 并且根尖会累积更多的过氧化氢(图3)。据此推测, 生长素及其运输载体可能在减缓铝诱导的活性氧毒
图2 铝处理对拟南芥根尖细胞PIN2蛋白的影响
Fig.2 Effect of Al on the distribution of PIN2 proteins in the
root apex of transgenic Arabidopsis
本实验室未发表数据, 其中A 和B: 正常生长条件下, 拟南芥根尖细胞PIN2蛋白的分布; C 和D: 铝处理条件下, 拟南芥根尖细胞PIN2蛋白的分布; B 和D 分别是A 和C
的局部放大图。
2.3 生长素及其运输载体在其他解铝毒机制中的作用
铝诱导根系有机酸分泌也是植物的一种重要解铝毒机制(Kochian 等2004; Shen 等2005)。根际分泌的有机酸可以有效络合根际溶液中的活性铝, 形成对植物没有毒害的铝螯合物, 降低了铝对质膜的渗透和其对共质体的毒害(Ma 2000)。Yang 等(2011b)发现, 与50 μmol ?L -1 Al 3+处理相比, 50
图3 铝对拟南芥PIN2缺失突变体和野生型根长及根尖过
氧化氢的累积的影响
Fig.3 Effect of Al on root growth and hydrogen peroxide
accumulation in Arabidopsis PIN2 mutant
and wild-type seedlings
本实验室未发表数据, 其中A 和B: 20 μmol ?L -1 Al 3+处理对拟南芥PIN2缺失突变体(A)和野生型(B)根系生长的影响; C: 根尖DAB
染色。
植物生理学报
1140害中也扮演积极角色。然而, 其作用机理需要后续的的研究。3 结语
铝抑制根尖生长与铝干扰根尖生长素极性运输有关, 其可能机制是铝直接或间接会影响生长素运输蛋白相关基因的转录表达, 并改变甚至破坏肌动蛋白微丝, 阻碍生长素运输蛋白囊泡运输, 进而影响生长素运输。生长素及其运输蛋白在植物耐铝机制又扮演着一定角色, 生长素可能是植物解铝毒的信号物质, 负责感受和传递铝毒信号; 或者启动甚至直接参与下游的耐铝机制, 如参与介导铝内置化、调节有机酸分泌和启动抗氧化系统等(图4)。然而, 生长素及其运输蛋白对植物解
铝毒的作用, 大部分来源于间接证据, 更多的直接证据需要更为深入的研究。如果生长素信号参与植物解铝毒作用, 那信号通路是如何构建的, 在这条通路中生长素信号是主控信号还是辅助信号？如果生长素或其运输蛋白介入铝内置化, 这存在三种可能: (1)生长素作为信号物质调控铝运输载体; (2)生长素运输蛋白直接结合铝, 借助生长素向胞内运输途径将铝转运至胞内; (3)生长素运输蛋白没有结合铝, 而是相关的运输囊泡结合了铝, 这样原本结合在细胞壁或细胞膜上的铝借助囊泡的运输, 通过“搭便车”的方式内吞进入胞内(图4)。具体铝是如何在生长素或其运输载体介导下进入细胞的, 有待不断深入的研究。
图4 生长素及其运输蛋白对植物铝胁迫响应的可能模式图
Fig.4 A possible model of auxin and its transporters responding aluminum stress in plants
生长素可能通过以下途径参与植物铝胁迫响应: ①作为信号分子, 参与位于质膜的铝受体和位于细胞核的转录调控因子(如ART1)间的铝信号传递; ②间接调控铝转运蛋白(如Nrat1和ALS1); ③间接调控有机酸转运蛋白(如ALMT1和OsFRDL4); ④参与细胞内ROS 的解除。生长素运输蛋白可能通过以下途径参与植物铝胁迫响应: (1)直接结合铝, 借助生长素向胞内运输途径将铝转运至胞内; (2)生长素运输相关囊泡结合铝, 通过“搭便车”将结合在细胞壁或细胞膜上的铝内吞进入胞内; 而这部分的铝可能有两种去处, 即由于生长素运输囊泡的降解而滞留在细胞质或液泡中(A), 或者跟随生长素运输囊泡从细胞一端转运到另一端, 实现细胞与细胞间的转运(B)。参考Ma 等(2014)
文献修改。
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