Reasearch Advancements on Strigolactones and its Regulatory effect on Root Growth and Development in Plants

Jiu Songtao^*　Xu Yan^*　Zhang Caixi　Wang Lei　Ma Chao　Xu Wenping　Wang Shiping^**

School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240

* The authors contributed equally to this work

** Corresponding authors, fruit@sjtu.edu.cn

Abstract　Plants can regulate the root growth and development through endogenous hormones or environmental cues, further affecting their root morphological characteristics. Strigolactones (SLs) and their derivatives are a novel kind of phytohormones, which play an important role in promoting the branching of arbuscular mycorrhizal fungi and nutrient absorption, stimulating the seed germination of parasitic plants, mediating plant resistance to pathogen and nutrient deficiency stress, and regulating the shoot-branching of plants. In addition, some studies have shown that SLs also participate in the regulation of growth of axial roots, formation of lateral root, formation and elongation of adventitious roots and root hairs in plants. This review concludes the structures and biological functions, biosynthesis and signal transduction pathways of strigolactones, as well as the research progress in regulating the root growth and development in plants. The research direction and application prospects about strigolactones were also discussed. This paper will provide reference for further in-depth study of strigolactones.

Keywords　Strigolactones, Biosynthesis, Signal transduction, Root, Growth and development

根系作为植物重要的营养器官，其不仅能固定植株，还负责从土壤中吸收水和养分，并合成氨基酸、内源激素等物质(Kohlen et al., 2011)。根系的生长发育状况在很大程度上决定了植物对水和养分的吸收效率。植物根系的生长发育受植物激素、外界环境信号、遗传物质等多重因素的调控，是一个十分复杂的生物学问题(Potocka and Szymanowska-Pulka, 2018)。其中，植物激素在众多调控信号中处于核心地位，显著影响着植物根系的生长发育过程。正如前人所述，常见的五大类植物激素是生长素(auxins)、赤霉素(gibberellins, GAs)、细胞分裂素(cytokinins, CKs)、脱落酸(abscisic acid, ABA)和乙烯(ethylene, ETH)。伴随植物生理学和生物化学的不断发展，除上述五大类植物激素外，又有许多植物生长调节物质被定义为新型植物激素。2008年，科研人员将独脚金内酯(strigolactones, SLs)定义为一类新型的植物激素(Gomez-Roldan et al., 2008; Umehara et al., 2008)。

1966年，科学家首次棉花根系分泌物中分离到一种称为独脚金醇的物质，当时发现其在促进恶性寄生杂草——独脚金(Striga spp.)种子萌发上功效显著(Cook et al., 1966)。科学家将天然的独脚金醇类化合物和人工合成类似物统称为独脚金内酯。目前，已有36种天然SLs被分离，其主要在根中合成，由于SLs可通过木质部向上运输到地上部器官，因此在叶和茎等器官中也有少量SLs存在(Kohlen et al., 2011; Delaux et al., 2012)。研究表明，SLs是以类胡萝卜素为前体物质，通过类胡萝卜素(carotenoid)生物合成途径中一系列酶促反应合成的(Alder et al., 2012)。近年来，国内外大量研究集中在SLs的分离、生物学功能、生物合成和信号转导途径以及调控植物分枝的分子机制解析等方面，对SLs调控根系生长发育的研究相对较少(陈虞超等, 2015; 李叶, 2018)。为进一步提升人们对独脚金内酯调控根系发育的认识，本文首先对SLs的结构和生物学功能以及生物合成和信号转导途径进行介绍，重点对SLs调控植物根系生长发育的研究概况进行综述，展望SLs的应用前景和研究方向，旨在为SLs调控植物根系发育的深入研究提供参考。

1独脚金内酯的结构和生物学功能

SLs属于类胡萝卜素衍生物，是一类倍萜烯类小分子化合物。SLs是由α, β-不饱和呋喃环(D环)和三环内酯(ABC三环)通过烯醇醚键(Enol ether bridge)耦合形成稳定的四环结构，构成SLs的碳骨架。目前，根据其立体结构可将SLs分为两类，一类SLs的BC环与(+)-独脚金醇的立体结构相同，这一类被称作独脚金醇家族；另一类是SLs的BC环则与(-)-列当醇的类似，被称为列当醇家族(图1)。独脚金醇家族的C环构型为β构象，称为构型Ⅰ；列当醇家族的C环位置是构型Ⅰ的对映异构体(enantionmer of structure-Ⅰ, ent-Ⅰ)，称为构型Ⅱ；而构型ⅡⅠ是构型Ⅱ的差向异构体(epimer of structure Ⅱ, epi-Ⅱ)；由于每种构型的A、B环都可以通过羟基化、环氧化、甲基化等进行修饰。因此，独脚金内酯的种类多样。目前，人工合成的独脚金内酯类似物主要有GR3、GR7和GR24等，其中以GR24活性最高，应用最广(Bergmann et al., 1993)。目前，关于SLs结构与其功能的相关性一直是研究的热点，就诱导寄生杂草种子萌发而言，不同结构的SLs对诱导寄生杂草种子萌发的效率也存在差异(Nomura et al., 2013)。

图1 两个独脚金内酯家族(Zwanenburg and Blanco-Ania 2017) Figure 1 Two families of SLs (Zwanenburg and Blanco-Ania 2017)

SLs的生物学功能主要体现在以下几个方面：刺激寄生植物种子萌发、促进丛枝菌根真菌菌丝分枝和养分吸收、介导植物对营养匮乏及病原菌等逆境胁迫的抗性反应、调控植物生长发育。早在1966年，Cook等(1966)研究发现，SLs能刺激列当(Orobanche spp.)和独脚金(Striga spp.)等根寄生杂草种子萌发。随后，Akiyama等从百脉根中分离出一种SLs类似物5-脱氧独脚金醇(5-deoxy-strigol)，并证实其在促进从枝菌根真菌菌丝分枝上具有重要作用(Akiyama et al., 2005)。在缺氮、缺磷等营养胁迫下，SLs在植物体内的合成上调，被运输到作用部位，或促进植物根毛发生和伸长以增加营养吸收，或抑制植物分枝以减少养分消耗，从而在整体上调控植物株型以适应逆境胁迫(Waters et al., 2017)。SLs有助于促进植物对细菌病原菌(如丁香假单胞菌)和真菌病原菌(如核盘菌)的抗性。此外，研究还表明，外源施加SLs还可抑制灰霉菌等真菌病原菌的生长(Waters et al., 2017)。另外，SLs也参与植物许多的生长发育过程，如调节植物的分枝结构，抑制不定根的发生和伸长(Rasmussen et al., 2012)、影响根毛的发生和伸长(Kapulnik et al., 2011a)，抑制植物侧根的形成(Kapulnik et al., 2011b)，促进节间伸长(De et al., 2013)，抑制腋芽生长，增加茎的细胞壁厚度，加速叶片衰老(Al-Babili et al., 2015) (图2)。Ferrero等(2018)研究表明，外源独脚金内酯与脱落酸协同可调控葡萄果实花青苷的积累。

图2 独脚金内酯在植物生长发育中的作用(Al-Babili et al., 2015) Figure 2 Roles of strigolactone (SLs) in plant development (Al-Babili et al., 2015)

2独脚金内酯的生物合成和信号转导途径

目前，普遍认为SLs来源于类胡萝卜素生物合成途径。Matusova等(2005)利用类异戊二烯途径抑制剂和玉米(Zea mays)类胡萝卜素(carotenoid)缺失突变体，表明SLs是以类胡萝卜素为前体，经过许多酶促反应生成独脚金醇，然后再进一步转化为具备生物活性的SLs。目前，已明确的SLs合成过程如下：all-trans-β-类胡萝卜素在类胡萝卜素异构酶D27催化作用下生成9-cis-β-类胡萝卜素，随后催化产物在类胡萝卜素裂解双加氧酶CCD7裂解作用下生成9-cis-β-apo-10’-胡萝卜醛，此裂解产物又在CCD8的作用下经过分子重新排列后，生成己内酯(carlactone, CL)，己内酯在己内酯氧化酶作用下生成5-脱氧独脚金醇，再经过列当醇氧化酶，最终生成列当醇；也可在P450等酶的作用下形成己内酯酸(Carlactonoic acid, CLA)，在一些未知酶的作用下生成甲基己内酯酸(MeCLA)，进而转变为独脚金内酯(Zhang et al., 2018) (图3A)。

目前，研究人员已在许多植物中克隆到一些SLs生物合成密切相关的基因。Lin等(2009)在水稻(Oryza sativa)中分离得到了OsD27基因，其负责编码类胡萝卜素异构酶，在维管细胞中的表达量最高。Zou等(2006)、Booker等(2004)、Morris等(2001)、Vogel等(2009)、Drummond等(2009)分别从水稻、拟南芥(Arabidopsis thaliana)、豌豆(Pisum sativum)、番茄(Solanum lycopersicum)和矮牵牛(Petunia hybrida Vilm.)中克隆到编码CCD7的同源基因AtMAX3、PsRMS5、SlCCD7和PeDAD3。Arite等(2007)、Sorefan等(2003)、Proust等(2011)、Snowden等(2005)分别在拟南芥、矮牵牛、豌豆、水稻和小立碗藓 (Physcomitrella patens)等四个物种中分离到编码CCD8的同源基因AtMAX4、PeDAD1、PsRMS1、OsD10和PpCCD8。Stirnberg等(2002)在拟南芥中克隆出编码P450蛋白的基因AtMAX1，证实其参与拟南芥腋芽的生长发育。Booker等(2005)也在拟南芥编码P450的基因AtMAX1，证实其位于AtMAX3和AtMAX4基因的下游，参与类胡萝卜素衍生物类激素的合成。Drummond等(2012)矮牵牛中克隆出编码P450蛋白的PhMAX1基因，过表达该基因可以恢复拟南芥max1突变体的突变表型。

关于独脚金内酯信号转导途径的研究目前还不够深入。根据先前的研究结果，可初步判断SLs在植物体内是通过受体蛋白介导的信号转导发挥作用。目前，普遍认为参与SLs信号转导途径主要有以下三种。第一种是D14蛋白，属于α/β折叠水解酶家族，其在植物激素信号转导或代谢途径中扮演重要作用。Arite等(2009)、Liu等(2009)、Gao等(2009)分别在水稻基因组中分离出编码D14蛋白的三个等位基因OsD14、OsHTD2和OsD88。Hamiaux等(2012)在矮牵牛中克隆得到了一个α/β折叠水解酶D14的同源编码基因PhDAD2，同时对其蛋白的晶体结构进行了分析，结果表明该蛋白结构中包含一个可以容纳SLs的空腔。第二种是F-box蛋白，也是激素信号传导过程中的一类常见结构特征蛋白。研究人员先后从水稻、拟南芥和豌豆中克隆得到了编码F-box蛋白的同源基因OsD3、AtMAX2和PsRMS4 (Stirnberg et al., 2002; Ishikawa et al., 2005; Johnson et al., 2006)。此外，在拟南芥中，SLs被认为以依赖MAX2的方式诱导蛋白酶体介导的D14降解(Chevalier et al., 2014)，这表明SLs及其自身信号通路存在负调控回路。第三种是D53蛋白，它是SLs信号路径的一个关键抑制因子，负责连接SLs信号的接收和应答。Jiang等(2013)和Zhou等(2013)的研究发现，水稻D53基因位于D14/DAD2和D3/MAX2基因的下游。随后D53在拟南芥中的直系同源蛋白SMXL6/7/8也得到了鉴定(Soundappan et al., 2015)。近年来，在拟南芥上的研究表明，SLs信号转导通路中，D14基因编码α/β水解酶，D14的结构类似一个打开的口袋，当SLs存在时，D14会水解SLs，得到一个D环衍生的共价连接中间分子(CLIM)，CLIM是SLs的活化形式，CLIM与D14的催化口袋相结合，使得D14蛋白的构象发生改变，与下游D3/MAX2等F-box蛋白结合形成复合体，这种复合体又反过来使D14蛋白口袋闭合，激发SLs信号转导，SLs的信号转导通路如图3B所示(Ferrero et al., 2018)。

图3 水稻和拟南芥中独脚金内酯的生物合成和信号转导通路(Ferrero et al., 2018) Figure 3 Strigolactone biosynthesis and signal transduction pathways in rice (Oryza sativa) and Arabidopsis thaliana (Ferrero et al., 2018)

3独脚金内酯对植物根系生长发育的调控

SLs在植物根系生长发育过程中发挥着重要作用(Ruyter-Spira et al., 2011)。Ruyter-Spira等(2011)研究发现，与拟南芥野生型植株相比，SLs不敏感型突变体和SLs缺陷型突变体植株的主根变短，突变体植物中的分生组织细胞数量较野生型减少。也有研究表明，外源施加SLs类似物GR24可使SLs缺陷型突变体的表型得以恢复，但是SLs不敏感型突变体无法通过添加GR24恢复其正常表型。Kapulnik等(2011a; 2011b)通过对拟南芥突变体max3-11、max4-1的研究发现，SLs可促进根毛的伸长和抑制侧根的形成。Koltai等(2011; 2013)对番茄和拟南芥的研究表明，与野生型相比，SLs合成和信号转导突变体的侧根密度显著增加，外源施加GR24后番茄和拟南芥的侧根密度降低，表明SLs能抑制番茄和拟南芥侧根的形成。Koltai等(2011)的研究结果显示，高浓度27 μM GR24处理能够显著抑制番茄根毛的发生和伸长。Kapulnik等(2011a; 2011b)的研究结果显示，低浓度3 μM GR24却对拟南芥根毛的发生有显著促进作用。这表明独脚金内酯对植物根系生长发育的调控作用与外源施加的浓度密切相关。Rasmussen等(2012)对豌豆和拟南芥的研究结果显示，SLs可抑制不定根的形成。Mayzlish-Gati等(2012)研究发现，在低磷胁迫下，SLs参与诱导拟南芥的根毛发育过程。Arite等(2012)的研究发现，水稻SLs合成突变体(d10)和信号转导突变体(d3)的不定根伸长受到显著影响，但侧根数量与野生型相比差异并不显著。Soto等(2010)和Foo等(2011)的研究表明，外源GR24处理可显著诱导紫花苜蓿(Medicago sativa)和豌豆根瘤的发生。

SLs和其它植物激素在调控根系生长发育过程中存在着密切的关系。Koltai等(2011)的研究发现，外源施加GR24会导致番茄主根弯曲。研究人员认为这种现象可能是由于GR24影响到生长素外流蛋白进而影响Auxins在根细胞的流动，主要由于Auxins的极性运输和根细胞的不均衡生长有着密切的关系。已有研究报道，拟南芥突变体植株主根根尖的Auxins含量显著高于野生型植株，外源GR24处理可以恢复max1和max4两种突变体的表型(Ruyter-Spira et al., 2011)。Stepanova和Alonso (2009)研究发现，SLs突变体可以响应乙烯前体，这表明SLs信号并不直接参与根毛响应乙烯的过程。然而，在乙烯突变体ein和etr中，对SLs响应显著减小，通过乙烯合成抑制剂2-(AVG) 抑制乙烯生物合成会导致SLs促进根毛伸长的效应消失，而用GR24处理会提高AtACS2基因的转录水平(Kapulnik et al., 2011a; 2011b)，其中AtACS2是一种乙烯合成的关键速率决定酶。这些研究结果推测，SLs诱导乙烯(ETH)生物合成，ETH可能在SLs调控根毛生长发育途径起着上位效应。在ABA突变体植株的根中SLs的含量减少，这表明ABA可能参与调控SLs的生物合成。也有研究发现，SLs、Auxins和ETH共同形成激素网络调节根毛发育(Kapulnik et al., 2011a)。那么关于调节根毛生长的过程中SLs、ABA、Auxins和ETH间的上下游关系，还需进一步的研究。

4独脚金内酯的应用前景

目前对SLs的作用机制及其代谢途径等诸多方面还有待深入研究，但能够确信独脚金内酯存在着广阔的应用前景。利用SLs促进寄生植物种子萌发和抑制真菌病原菌的特性，可将其应用于新型除草剂和杀菌剂的研发，具有广阔的前景。在亚洲和非洲的很多国家，玉米、高粱、等农作物，时常受独脚金或列当等寄生植物的危害，导致农作物大幅减产，每年损失约10亿美元(Parker, 2009; Westwood et al., 2010)。在作物种植前，可将SLs施用于农田中，促使根寄生杂草种子出现“自身性萌发”，通过这种方式可消除寄生杂草种子对作物生长的影响(Abebe et al., 2005)。天然的SLs在土壤中的稳定性较差，而独家金内酯人工合成类似物虽能有效促使寄生杂草种子萌发，减小其危害，但现阶段生产成本较高，在取得官方许可和田间推广应用上仍面临较大挑战。许多重要作物根部存在共生的丛枝真菌，丛枝真菌可改善其营养状况、促进生长、提高其抗逆性(王曙光等, 2001)。因此，SLs还可作为激素应用在农业生产上，增加产量，实现丰产丰收。SLs参与调控植物根系的生长发育，通过施用独脚金内酯类似物或其抑制剂来调控作物的根系构型，促使根系更加粗壮、形成更多的毛细根以提高水和养分的吸收效率。SLs还可与Auxins、ETH等激素相互协同调控植物分枝及株型(Hayward et al., 2009; Dun et al., 2012; 周晓燕, 2016)。在水稻、小麦等粮食作物方面，通过外源喷施SLs类似物抑制无效分枝(分蘖)，塑造高产优质的理想株型，提高产量。在苹果、樱桃、柑橘等果树作物方面，可通过施用SLs抑制剂促进分枝，对于细长纺锤形(主干形)树型的构建意义重大，可避免刻芽等劳力投入，助力果树产业提质增效。在矮牵牛等观赏植物方面，通过控制SLs的合成，促使矮牵牛等观赏植物分枝数量增加，以实现最佳的观赏效果。目前，SLs人工合成的生产成本较高，但伴随相关研究的进一步深入以及生产工艺的不断成熟，SLs的应用前景将更加广阔。

5 总结与展望

SLs参与调控植物根系的生长发育，通过外源施用独脚金内酯来调控作物根部构型和营养吸收状况，提高作物对水和养分的吸收效率，对作物产量提升意义重大。近年来研究发现，SLs、ETH和Auxin等多种激素之间可能通过相互协同调控根系生长发育过程，对此进行深入解析有望成为未来科学研究的一个重要方向。其次，对于SLs的生物合成和信号转导途径还需深入解析。虽然已经确定CCD7/8、D14、D53等几个关键的蛋白参与SLs生物合成和信号转导途径，但从类胡萝卜素作为前体物质，到与激素受体结合，再进行信号传递，这是一个极其复杂的生物学过程，其中必定涉及很多的反应过程，完整的SLs合成、运输以及信号传递过程还需要深入探索，为未来SLs在实际生产中广泛应用提供科学依据。最后，SLs是由植物根系分泌到土壤中的，其在土壤中的活性变化和作用机制还不清晰。总之，SLs的发现为植物科学研究开拓了一个全新的领域，其中存在的众多科学问题亟待科学家去探索解答。

作者贡献

纠松涛和徐岩负责资料的收集和论文的写作；张才喜、王磊、马超和许文平参与资料的收集和整理；王世平是项目的构思者及负责人，指导论文写作与修改。全体作者都阅读并同意最终的文本。

致谢

本研究由国家重点研发计划项目(2018YFD0201300)、国家博士后创新人才支持计划项目(BX20180199)和中国博士后科学基金面上项目(2018M642028)共同资助。

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