矿质养分和激素对根毛生长发育的影响及作用机制

2016-08-30 02:51张德健夏仁学
植物营养与肥料学报 2016年3期
关键词:根毛毛细胞生长素

张德健, 夏仁学, 曹 秀

(华中农业大学教育部园艺植物生物学重点实验室, 湖北武汉 430070)



矿质养分和激素对根毛生长发育的影响及作用机制

张德健, 夏仁学*, 曹 秀

(华中农业大学教育部园艺植物生物学重点实验室, 湖北武汉 430070)

【目的】植物矿质养分和水分的吸收利用赖于根系,根系中根毛的生长发育不仅扩大了根系吸收表面积,促进了矿质养分和水分的吸收还有助于植物根的固定以及与土壤微生物的互作。本文从矿质养分角度(氮、 磷、 钾、 钙、 铁)和激素角度(生长素、 乙烯、 茉莉酸、 独脚金内酯、 油菜素内酯)探讨影响根毛生长发育的因子及作用机理。【主要进展】氮对根毛生长发育的影响与茉莉酸和乙烯有关, 磷与生长素、 乙烯、 独脚金内酯互作调控根毛生长发育;生长素和乙烯以交互作用调控根毛生长发育,茉莉酸、 独角金内酯和油菜素甾醇对根毛生长发育的作用是部分依赖生长素或乙烯途径;植物体内生长素和乙烯等激素的平衡对根毛的生长发育起着重要作用。【建议和展望】基于以上分析,从蛋白激酶及其相关调控基因及转录因子等方面可深入探析矿质养分、 植物激素等对根毛和丛枝菌根生长发育的影响。

根毛; 发育; 氮; 磷; 生长素; 乙烯; 丛枝菌根

根毛是植物根表皮细胞特化而形成向外凸起且顶端封闭的管状器官,是根的一种特殊结构[1]。根毛扩大了根系吸收矿质养分和水分的表面积,有利于提高根系吸收土壤中矿质养分和水分的效率,尤其是对土壤中短距离运输的磷、 钾等矿质养分的吸收特别重要[2-7]。根毛生长发育过程大致可分为4个阶段: 根毛细胞命运决定、 根毛起始、 根毛顶端生长、 根毛成熟[8]。矿质养分和激素影响着根毛生长发育各个阶段,尤其对根毛顶端生长影响很大,相关转录因子及特异基因参与矿质养分和激素对其生长发育的调控[5, 9-12]。本文拟从氮、 磷、 钾、 钙、 铁等矿质养分和生长素、 乙烯等激素对根毛生长发育的影响及其作用机制进行综述,为深入研究植物根毛的生长发育和提高植物对矿质养分及水分的吸收利用提供参考。

1 矿质养分对根毛生长发育的影响

1.1氮

1.2磷

磷(P)是植物生长发育所必需的元素之一,然而土壤中可直接被吸收利用的有效磷浓度较低,这迫使植物进化出一套应对磷缺乏响应机制,其中较典型的是促进根毛生长发育[21]。

磷对根毛生长发育的影响已在拟南芥(Arabidopsisthaliana)、 番茄、 蓟草(Cirsiumjaponicum)、 油菜(Brassicacampestris)、 甜菜(Betavulgaris)、 大麦(Hordeumvulgare)、 菜豆(Phaseolusvulgaris)、 枳(Poncirustrifoliate)等植物中有较深入研究。缺磷能够使枳主根根毛密度从150条/mm2提升到250条/mm2, 长度从45 μm增加到60 μm[5, 9]。缺磷条件下的拟南芥根毛密度和长度是不缺磷时的35倍,且生长速度也提高了1倍,使根的表面积从0.21 mm2/mm提升到1.44 mm2/mm[22-24]。磷胁迫能引起拟南芥根毛密度增加主要是由于促进生毛细胞最终凸起成为根毛的比例, 促进非生毛细胞凸起成为异位根毛, 降低生毛细胞直径以提高单位面积生毛细胞数量[22, 25-26]。

不同磷效率植物根毛对磷胁迫的响应不一样,如菜豆磷吸收低效品种在低磷条件下有大量根毛形成,而磷吸收高效品种却没有[27]。磷对根毛的影响在不同基因型植株中也有区别,如拟南芥根毛缺失突变体,缺磷促进了其根毛长度的增加,却对根毛密度没有显著影响[28]。

很多研究认为磷对根毛生长发育的调控伴随着内源激素信号途径,且主要有以下3种状况:

1) 磷与生长素互作于根毛生长发育拟南芥生长素信号传导突变体axr1、axr2、aux1因缺乏生长素信号致使根毛生长发育受阻,而缺磷能回复根毛正常生长[23]。生长素运输抑制剂2-(对-氯苯氧基)-2-甲基丙酸(CMPA)会显著抑制低磷对根毛生长发育的促进作用[25]。

2) 磷与乙烯互作于根毛生长发育乙烯信号突变体ein2因缺乏乙烯信号导致根毛生长发育受阻,而缺磷能诱导其根毛正常生长[23, 29]。深入研究发现缺磷诱导根产生乙烯的量是不缺磷的2倍左右,因此认为缺磷刺激乙烯信号突变体ein2产生乙烯,进而促进根毛正常生长[23, 29]。采用乙烯生物合成抑制剂AVG处理发现其能够抑制低磷对根毛生长的促进效应[30]。

3) 磷与独脚金内酯互作于根毛生长发育磷胁迫对根毛生长促进效应在拟南芥独脚金内酯突变体max2和max4中被降低,该突变体也降低了磷胁迫响应基因PSI的表达量,而外源施加独脚金内酯(GR24)能够提高PSI的表达量,并促进根毛生长[31]。

1.3钾

近些年的研究发现钾(K)能影响根毛的生长发育[32]。如低钾(0.05 mmol/L)条件下,烟草的根毛密度、 长度显著大于正常供钾(5 mmol/L)的根毛密度和长度[33]。低钾对根毛生长作用机理可能是低钾能激活植物高亲和性钾离子转运蛋白和打开钾离子通道[34]。钾离子转运蛋白突变体akt1和钾离子生化阻断剂能够证明钾离子通道对根毛顶端生长十分重要[35-36]。在拟南芥trh1突变体中,发现生长素输出载体PIN1异位表达,从而影响生长素体内运输和分布,最终阻碍根毛生长,其中TRH1是编码钾离子运输载体,由此可推测钾通过生长素正调控根毛生长发育[36-37]。然而在枳的研究中发现缺钾处理时,主根和侧根的根毛密度、 长度及直径均显著低于正常供钾处理[3-5]。由此可见钾对不同植物种类根毛生长发育的影响及作用机理或许存在差异。

1.4钙

钙(Ca)作为细胞信号传导的第二信使,已被证实在植物生长、 发育以及抗逆性等方面具有重要作用。研究发现钙也参与根毛的生长发育,外界钙离子浓度对根毛发育具有显著影响。如当外加钙离子浓度为0.33 mmol/L时,拟南芥根毛长度达到最大值[38]。钙离子螯合剂乙二醇-双-(2-氨基乙基醚)四乙酸(EGTA) 和钙调素拮抗剂三氟拉嗪(TFP)及氯丙嗪 (CPZ)均可显著抑制根毛发生和生长,外源施加钙调素可减弱此抑制作用[32, 39]。由此表明钙离子在根毛形成和生长过程中具有十分重要的作用。

利用激光共聚焦技术发现钙离子在根毛顶端生长过程中浓度梯度的变化。根毛进入顶端生长阶段,其顶端形成一个钙离子浓度梯度,当根毛进入成熟阶段或因外界环境干扰使其停止生长时,钙离子浓度梯度将消失[40]。人为让钙离子浓度梯度消失,根毛顶端生长直接被终止[41]。外源处理使顶端一侧的钙离子浓度升高时,根毛生长方向被改变[42]。这种钙离子浓度梯度可能通过影响根毛中细胞骨架的形成以及肌动蛋白、 囊泡的移动、 微管排列等来影响其顶端生长,质膜上PCaP2作为钙离子结合蛋白以信号传导模式参与此过程[43]。最近的研究发现钙离子相关蛋白CAP1通过维持细胞质中钙离子浓度梯度调控根毛顶端生长[20]。根毛顶端生长与其顶端钙离子浓度梯度密切相关。

1.5铁

铁(Fe)广泛参与植物一系列重要的生理生化代谢,如光合作用、 叶绿素的合成、 植株体内氧化还原反应和电子传递等。当土壤中可直接被吸收利用的有效铁较少时,植物将做出一系列反应以应对铁胁迫,其中典型的是促进根毛生长发育,如铁胁迫可促进枳和拟南芥根毛的生长发育,增加其根吸收表面积,进而提高了铁元素的吸收[3-5, 26]。铁胁迫可能通过铁氧化还原蛋白PFLP (plant ferredoxin-like protein)在NADPH氧化酶(NOX)作用下影响体内ROS含量[44-47]。ROS能够激活ACC合成酶(ACO)促进乙烯合成,进而促进根毛生长发育[48]。因此铁可能通过乙烯信号影响根毛生长发育。然而缺铁和低铁对拟南芥根毛作用机理有所区别, 缺铁是通过促进根毛分叉以增加根毛数量,而低铁促进根毛生长发育主要是通过诱发更多的表皮细胞凸起成为根毛并促进凸起后的顶端生长[26]。

2 激素对根毛生长发育的调控

2.1生长素

生长素(auxin)作为调控植物生长发育的主要激素,影响着植物根毛凸起和伸长生长。拟南芥生长素响应突变体axr1的根毛长度显著低于野生型,证明生长素对根毛顶端生长很重要,但其表皮细胞发育成为根毛的比例与野生型无显著差异[49],这与先前生长素对生毛细胞比例的作用无显著影响的结论相似[50]。然而后期研究结果表明生长素也参与调控根毛起始。外源生长素类似物萘乙酸(NAA)提高了拟南芥根毛数量和长度,外源施加的生长素运输抑制剂1-萘氧乙酸(1-NOA)和1-萘氨甲酰苯甲酸(NPA)则阻碍了根毛凸起和伸长生长[51]。这些不同的结果可能与其施用外源生长素的浓度等有关,而生长素在根毛细胞中的浓度对根毛的凸起和顶端生长十分重要[52-53]。根毛细胞中的生长素浓度与生长素运输相关,然而生长素不是从根尖直接运输到生毛细胞,而是以非生毛细胞作为中转站进行极性运输,从而影响生毛细胞中生长素的浓度进而影响根毛生长发育[54]。外源施加NAA可导致生长素响应报告基因DR5:GUS在非生毛细胞中大量表达,非生毛细胞积累生长素,然后运输到生毛细胞促其发育成为根毛[55]。生长素在根中的极性运输是需要载体的,拟南芥生长素流入载体基因PIN2突变后,将抑制生长素从根尖向根毛区运输,同时抑制生长素从非生毛细胞运输到生毛细胞,生毛细胞缺乏生长素信号,将阻碍根毛的凸起和顶端生长[56]。PIN7、PGP4和PDR8作为生长素流出载体基因,其表达量下降能降低拟南芥生毛细胞中的生长素流出速度,因而生毛细胞积累较多的生长素,在一定的浓度范围内促进根毛生长发育[52, 55, 57-58]。生长素作为信号物质影响根毛发育,合适浓度的生长素对根毛生长发育有利。如NAA施加过量将使拟南芥根毛的长度显著下降[59-60],1 μmol/L的吲哚丁酸(IBA)促进枳根毛生长效果最佳[9-10]。

2.2乙烯

乙烯(ethylene)以双重作用影响根毛发育,即提高凸起率和促进顶端生长。拟南芥乙烯不敏感突变体etr1的根毛数量和长度显著低于野生型,而乙烯过量突变体eto1由于产生了大量乙烯,提高了根毛的数量和长度[61]。经乙烯合成前体1-氨基环丙烷-1-羧酸(ACC)诱导的野生型拟南芥,它们根毛长度和密度均得到了提高,通过切片等试验证明其密度的增加是由于提高了生毛细胞最终凸起成为根毛的比例和更多异位根毛的产生[62]。乙烯生物合成抑制剂氨基乙氧基乙烯甘氨酸(AVG)则能阻碍生毛细胞凸起以及凸起后的顶端生长[50]。在生毛细胞凸起启动之后,采用乙烯生物合成抑制剂1-甲基环丙烯(1-MCP)处理,发现根毛的密度无显著变化,但顶端生长受抑制[63]。这说明乙烯作为信号物质在根毛凸起之前调控表皮细胞凸起发育成根毛,在根毛凸起之后调控其顶端生长。

值得注意的是生长素和乙烯可能以交互作用调控根毛生长发育[64]。拟南芥生长素响应突变体axr1和乙烯响应突变体etr1的根毛生长受到阻碍,外源施加乙烯前体ACC均能回复其根毛正常生长,甚至其长度和密度超过野生型植株,切片分析其密度的提高是由于产生了异位根毛[49]。拟南芥乙烯信号传导突变体ein2-1的根毛顶端生长受到显著抑制,外源施加NAA能够使其回复至野生型水平[65]。研究认为表皮细胞中生长素水平对根毛的凸起和顶端生长至关重要,乙烯突变体根毛生长回复到正常水平需要NAA的量是生长素突变体的1倍[65]。通过转录组数据发现生长素和乙烯均能够使90%与根毛发育相关的基因上调表达,这充分证明生长素和乙烯部分通过共同的路径参与调控根毛的发育[66]。然而它们在调控根毛发育过程中的作用和关联有两种相反看法。

1)生长素在乙烯上游调控根毛发育。生长素能够促进乙烯的生物合成,因此生长素促进根毛的生长被认为可能是通过内源乙烯途径[49-50]。外源生长素能够回复拟南芥短根毛突变体rhd6的根毛长度至野生型水平,而乙烯生物合成抑制剂1-MCP能够阻碍该效应[63]。拟南芥生长素信号缺失突变体arf7和arf9的根毛凸起和顶端生长受阻,外源ACC处理能够回复根毛的正常生长[67]。据报道,根毛的顶端生长需要生长素诱导的微管不规则分布,而乙烯能够启动微管不规则分布[68]。由此认为生长素位于乙烯的上游调控根毛生长发育。

2)生长素在乙烯下游调控根毛发育。乙烯能够刺激生长素的生物合成和信号传导,并能促进生长素运输到根伸长区的表皮细胞[69-70]。外源生长素能够回复拟南芥乙烯不敏感突变体ein2-1短根毛表型[65]。拟南芥乙烯超量突变体eto1根毛较长,生长素突变体aux1的根毛发育受阻,而其双突变体eto1aux1的根毛凸起和伸长生长受阻[71]。所以认为生长素在乙烯下游调控根毛生长发育。

但也有研究认为生长素提高根毛密度的机理可能独立于乙烯。乙烯主要是通过异位根毛影响根毛密度,外源施加IAA和生长素类似物2, 4-二氯苯氧乙酸(2, 4-D)不能诱导拟南芥产生异位根毛。生长素增加根毛数量的机理是:增加皮层细胞数量、 减小表皮细胞的长度,从而增加生毛细胞的数量;促进更多的生毛细胞凸起成为根毛[11, 50-51, 62]。

2.3茉莉酸和茉莉酸甲酯

除了生长素和乙烯对根毛生长发育有着显著促进作用外,茉莉酸(jasmonic acid, JAs)和茉莉酸甲酯(methyl jasmonate, MeJAs)也具有类似作用。适宜浓度的茉莉酸和茉莉酸甲酯能够提高拟南芥根毛长度和密度,其密度的提高部分是由于产生了分叉根毛[72]。茉莉酸可通过上调生长素合成基因YUCCA8 和YUCCA9 的表达,促进拟南芥内源生长素的合成[73]。拟南芥生长素信号传导突变体axr1的主根生长受抑制,外源施加茉莉酸能够回复主根正常生长,推测茉莉酸可能通过生长素路径调控根系及根毛生长发育[74]。另有研究表明茉莉酸和茉莉酸甲酯促进拟南芥根毛生长发育的效应可被乙烯效应抑制剂银离子(Ag+)和乙烯合成抑制剂AVG消除,茉莉酸合成抑制剂布洛芬和水杨羟肟酸能够抑制ACC促进根毛生长,它们也能够减少拟南芥乙烯过量突变体eto2根毛的数量和长度[16, 72],由此说明茉莉酸和茉莉酸甲酯对根毛生长发育的作用是部分依赖根中生长素或乙烯途径。

2.4独角金内酯

新型激素独角金内酯(strigolactone, SL)也能促进根毛的生长发育,并且与乙烯、 生长素在调控根毛发育过程中具有协同效应[67, 75]。虽有研究认为独脚金内酯可通过乙烯途径调控根毛生长发育,然而其更有可能是依托生长素来调控根毛生长发育,因为独角金内酯能够调控PINs和TIR1的表达,以此影响生长素的运输和信号传导[76-77]。拟南芥生长素运输突变体arf7、arf9添加外源独角金内酯,突变体根毛恢复正常生长[75],这说明独角金内酯可能独立或位于生长素下游调控根毛生长。然而,外源生长素也可恢复独角金内酯信号传导突变体max2、max4根毛至野生型水平[77],说明独角金内酯也可能位于生长素的上游调控根毛发育。

2.5油菜素甾醇

油菜素甾醇(brassinosteroids, BR)是近几十年来确认的新型植物激素,被称为继生长素、 细胞分裂素、 赤霉素、 脱落酸、 乙烯之后的第六大激素。虽然它在植物茎、 叶、 根的生长以及维管组织的分化、 育性、 种子萌发、 顶端优势的维持、 植物光形态建成等方面与生长素具有协同作用,然而在根毛生长发育方面却与生长素差异较大,即对根毛生长发育既有促进又有抑制作用。在双子叶模式植物拟南芥中的研究表明油菜素甾醇抑制根毛凸起和顶端伸长生长,而在单子叶模式植物水稻(Oryzasativa)中,油菜素甾醇对根毛的发育存在剂量效应,在一定范围内促进根毛发育[78-80]。对拟南芥的研究还发现,油菜素甾醇促进AXR3/IAA17(生长素信号抑制基因)上调表达[78],因此可推测油菜素甾醇有可能通过AXR3/IAA17抑制生长素信号传输,从而抑制根毛生长。

3 结语

在植物根系中,矿质养分胁迫通过诱导根系细胞内源激素信号变化以调控根毛发育,从而增加植物对有限养分的吸收能力以适应胁迫环境。如磷、 铁、 钾等胁迫能够增加根系内源生长素和乙烯含量,促进根毛生长发育[29-30]。APSR1是磷胁迫响应因子,其突变后,能使PIN7(生长素流出载体基因)表达下调,促进根毛生长发育[58, 81]。乙烯生物合成抑制剂AVG处理能够抑制低磷对根毛生长的促进效应[30]。乙烯过量突变体eto3的根毛密度和长度得到显著提高,然而缺铁能促进其密度和长度进一步增加[23]。钾胁迫能够促进烟草根毛发育,推测生长素输出载体PIN1可能参与钾对根毛发育的影响[33, 37, 82]。然而本课题组研究发现钾胁迫能够降低枳根毛密度和长度[3-5],这或许与钾胁迫程度或不同植物应对钾胁迫机制不同有关。总之,矿质养分对植物根毛生长发育的影响不仅与激素信号相关,而且与根毛发育的遗传相关,相关基因的表达等影响着根毛的发生和生长。

已有研究表明缺磷不仅能够促进根毛发育,也能促进丛枝菌根发育,且根毛和丛枝菌根不仅能够提高植物对磷的吸收,也能增强植物抗旱能力[3, 9, 83-84]。可见根毛和菌根都是植物适应环境胁迫的一种途径,然而它们抵抗胁迫环境的能力差别较大。大麦根毛相对于丛枝菌根在磷胁迫环境条件下更具优势,而丛枝菌根相对于根毛能够更有效的帮助植物适应干旱环境[85-86]。近年来的研究从转录组数据中得到缺磷条件下有3000个差异表达基因,通过全基因组共表达分析可知缺磷主要是通过蛋白激酶(protein kinases)促进根毛发育[87]。同时,蛋白激酶对菌根的形成也是不可或缺的[88]。从蛋白激酶及其相关调控基因或转录因子等方面进行研究,或许可深入探析矿质养分(如磷、 铁等)对根毛和丛枝菌根的影响及其相互关系,进一步挖掘植物对胁迫环境的适应机制。

影响植物根毛生长发育的激素较多,但其中起调控作用的主要为生长素和乙烯,茉莉酸、 独脚金内酯、 油菜素甾醇等激素对根毛生长发育的作用主要是通过影响生长素和乙烯而起作用。虽然有研究认为,生长素提高根毛密度的机理可能独立于乙烯,但多数研究认为二者相关联,即它们在调控根毛发育过程中的作用或是生长素在乙烯上游调控根毛生长,亦或是生长素在乙烯下游调控根毛发育[70-71]。不同植物根毛生长发育过程中生长素和乙烯的作用位置不同或许与试材不同等有关,因为不同植物根毛发育方式有差别,且调控根毛发育的基因及其表达亦有差异。

值得注意的是,在植物根毛发育研究中曾有人提出“乙烯中心”假说,即土壤环境、 生长调节剂、 矿质养分等能影响根系生毛细胞中乙烯的浓度,进而调控根毛的生长发育[89]。如生长素、 茉莉酸、 独脚金内酯以及磷胁迫等因子对根毛生长发育的影响是通过乙烯途径作用的,同时从细胞学角度证实了乙烯提高根毛密度的机理是提高生毛细胞最终凸起成根毛的比例和更多异位根毛的产生[29-30, 62, 72, 75-76]。这些相互矛盾的结果不仅说明乙烯和生长素等激素对植物根毛生长发育的调控较为复杂,而且还受其它因素的影响(图1)。当遇到逆境时(如磷胁迫、 干旱等),植物为了规避风险,通过改变生长素合成运输和乙烯合成来打破其体内生长素和乙烯的平衡,从而触发根作出反应以保证根生长的可塑性。笔者认为,生长素和乙烯在植物体内的平衡状态可能对其根毛的生长发育起着重要作用。此外,不同种类植物可能对不同激素种类反应不同,因而所得到的根毛生长发育结果不同。即使是同一种植物,应用同一种激素,不同浓度其结果也不相同,如1 μmol/L的IBA促进枳根毛生长发育效果最佳,较高或较低浓度的IBA的效果都不显著甚至相反[10]。这从一个侧面再次说明植物体内生长素和乙烯等激素的平衡对其根毛的生长发育起着重要作用。

图1 矿质养分和植物激素调控根毛生长发育模式图Fig.1 The model of mineral nutrients and phytohormones regulating root hairs development

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Effects and mechanism of mineral nutrient and phytohormone on root hair development

ZHANG De-jian, XIA Ren-xue*, CAO Xiu

(MinistryofEducationKeyLaboratoryofHorticulturalPlantBiology,HuazhongAgriculturalUniversity,Wuhan430070,China)

【Objectives】 Root hairs are tubular projections from root epidermal cells. Their formation make a significant increase in root surface area, which play important roles in nutrients and water uptake, anchorage, and interaction with soil microorganisms. In this review, we discussed the effects of mineral nutrients (nitrogen, phosphorus, potssium, clacium, iron) and phytohormones (auxin, ethylene, jasmonic acid, strigolactone, brassinosteroids) on root hairs development and their relevant mechanisms. 【Major advances】The effect of nitrogen on root hairs development is related to jasmonic acid and ethylene. Interaction existes between phosphorus and phytohormones (auxin, ethylene, strigolactone) on root hairs growth. The interaction between auxin and ethylene regulates root hairs development. The effects of jasmonic acid, strigolactone and brassinosteroids partly depend on the way of auxin and ethylene. The balance of auxin/ethylene maybe important on root hairs growth and development.【Suggestions and expectations】 On the basis of the above review, it is important to study the regulatory genes and transcription factors, which will be helpful to deeper understand the effects of mineral nutrient and phytohormone on arbuscular mycorrhizas and root hairs development.

root hairs; development; nitrogen; phosphorus; auxin; ethylene; arbuscular mycorrhiza

2014-09-29接受日期: 2015-04-08

华中农业大学自选项目(52207-05019)资助。

张德健(1988—), 男, 安徽芜湖人, 博士研究生, 主要从事根系栽培生理学研究。

Tel: 027-87284181, E-mail: zhangdejian0551@126.com。 *通信作者 Tel: 027-87286913, E-mail: renxuexia@mail.hzau.edu.cn

Q945.12

A

1008-505X(2016)03-0802-09

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