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罗振鹏, 谢芳
硝酸盐调控豆科植物与根瘤菌共生固氮的机制研究
生物技术通报, 2019, 35(10): 34-39

LUO Zhen-peng, XIE Fang
Mechanism of Nitrate Regulating Symbiotic Nitrogen Fixation Between Legumes and Rhizobium
Biotechnology Bulletin, 2019, 35(10): 34-39

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收稿日期:2019-08-27

硝酸盐调控豆科植物与根瘤菌共生固氮的机制研究
罗振鹏1,2, 谢芳1     
1. 中国科学院分子植物科学卓越创新中心 植物生理生态研究所 植物分子遗传国家重点实验室,上海 200032;
2. 中国科学院大学,北京 100049
摘要:氮是植物生长发育所需的大量营养元素之一。硝态氮不仅可以被植物直接吸收利用,还可以作为重要的信号分子调控植物对氮素的响应、吸收、代谢相关基因的表达,从而影响植物的生长和发育。豆科植物可以通过与根瘤菌共生互作来获得生长所需的氮,但共生固氮是一个耗费植物能量的过程。当土壤中存在高浓度的氮素时,氮作为信号分子会影响共生固氮基因的功能从而抑制共生固氮过程。目前的研究表明,硝酸盐通过局部和系统的调控方式抑制共生固氮过程;结瘤自主调控(Autoregulation of nodulation,AON)和NLPs(NIN-like proteins)转录因子在硝酸盐抑制豆科植物根瘤形成中有着重要的作用。本文结合最近的研究进展,重点讨论NLPs转录因子和AON途径在硝酸盐抑制共生固氮过程的作用。
关键词硝酸盐    共生固氮    NLPs转录因子    AON途径    CEP短肽    
Mechanism of Nitrate Regulating Symbiotic Nitrogen Fixation Between Legumes and Rhizobium
LUO Zhen-peng1,2, XIE Fang1     
1. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032;
2. University of the Chinese Academy of Sciences, Beijing 100049
Abstract: Nitrogen is one of major macronutrients to support plants growth and development. Nitrate-nitrogen not only can be directly absorbed and utilized by plants, also affects the development and growth of plants via acting as a molecular signal to regulate the expressions of genes related to nitrogen-responding, absorbing and metabolizing. Legumes plants can obtain the demanded nitrogen for plant growth by establishing a symbiotic interaction with rhizobia; however, nodule formation and nitrogen fixation are energy-consuming processes for plants. When there is high concentration of nitrogen in soil, nitrogen as a signal molecule will affect the function of symbiotic nitrogen fixation gene and thus inhibit the process of symbiotic nitrogen fixation. Current researches reveal that nitrate inhibits symbiotic nitrogen fixation through a local and systemic regulation pathway. Autoregulation of nodulation (AON) and NIN-like proteins (NLPs) play a critical role in symbiotic nitrogen fixation. Combined with the latest researches, this review focuses on discussing the roles of NLPs transcription factors and AON pathways in symbiotic nitrogen fixation.
Key words: nitrate    symbiotic nitrogen fixation    NLPs transcription factor    AON pathway    CEP short peptide    

氮是生命活动的必须元素,也是植物生长发育所需的大量营养元素。氮在自然界中主要以氮气的形式存在,氮气含量丰富却不能被植物直接吸收利用,而是需要被固定还原为氨,才能进一步为生物所利用。生物固氮,特别是豆科植物与根瘤菌之间的共生固氮,是自然界中固氮效率最高、也最具开发利用价值的体系。

豆科植物与根瘤菌之间的共生固氮是一个非常复杂且精细调控的过程,需要共生双方的“分子对话”和信号交流[1-2]。豆科植物通过与根瘤菌间的共生固氮作用获取生长发育所需的氮素,在缺乏氮素的条件下生长。但共生固氮过程也是一个非常耗能的过程,需要消耗植物大量的生物能。为了平衡生长和固氮,豆科植物演化出一套有效的机制来形成“合适”的根瘤数目。目前的研究表明,豆科植物可以通过结瘤自主调控(Autoregulation of nodulation,AON)途径抑制根瘤共生[3-4]。此外,当土壤中存在充足的氮素,豆科植物会选择直接吸收外界环境中的氮而抑制共生固氮[5]。当土壤中存在高浓度的硝酸盐时,共生过程会被抑制,表现为侵染线、根瘤数目显著减少,根瘤形成小且没有固氮能力的白色根瘤[6-8]。通过遗传、嫁接及分根等实验表明硝酸盐抑制结瘤涉及局部和系统性信号[9-10]。NLPs(NIN-like proteins)转录因子在根部发挥功能,通过调控下游靶标基因的方式参与硝酸盐抑制共生固氮过程[11],而AON途径被硝酸盐信号激活后通过系统性调控的方式抑制根瘤的形成[8, 12]。而本文将结合最近在模式植物百脉根(Lotus japonicus)和蒺藜苜蓿(Medicago truncatula)中的一些研究结果,讨论NLPs转录因子、AON途径如何协调参与硝酸盐抑制豆科植物与根瘤菌之间的共生固氮过程。

1 结瘤自主调控(AON)参与硝酸盐抑制结瘤

豆科植物通过与根瘤菌共生互作的方式获得了生长发育所需的氮素,但共生固氮也会消耗植物大量的碳源。为了平衡生长和固氮,豆科植物演化出一套系统性调控根瘤数目的负反馈调节信号途径,称为结瘤自主调控[3, 13-14]。AON途径相关的基因发生突变,植物根瘤数目会失去了控制,就会表现出超结瘤(Hypernodulation)的表型,导致过度固氮并消耗植物大量的光合产物,植物表现出生长矮小等表型[5, 15-17]。AON途径涉及植物地下和地上的长距离信号传导。在百脉根的研究中发现,结瘤因子信号激活NIN(Nodule Inception)的表达,NIN作为转录因子激活CLE-RS1(CLE-Root Signal 1)和CLE-RS2的表达[18]。CLE-RS1/2短肽被剪切及加工后通过木质部从根部转运至地上部,被地上部的类受体激酶(Leucine-rich repeat(LRR)-type receptor-like kinase)HAR1(Hypernodulation Aberrant Root 1)所识别[5, 19],随后激活SDI(Shoot-Derived Inhibitor)信号从地上部转移至根部抑制根瘤的形成[20]。Kelch-repeat的F-box蛋白TML(Too Much Love)位于HAR1的下游,在根部负调控根瘤的数目[20]

AON途径在豆科植物中十分保守,在蒺藜苜蓿、豌豆(Pisum sativum)、大豆(Glycine max)和菜豆(Phaseolus vulgaris)中均发现了HAR1的同源基因,包括MtSUNN(Super numeric nodules)、PsSYM29GmNARK(Nodule autoregulation receptor kinase)和PvNARK[21-24],这些基因突变后都表现出相似的超结瘤表型,以及受根瘤菌诱导的CLE短肽:MtCLE12、MtCLE13和GmRIC1(Rhizobia induced CLE 1)、GmRIC2、PvRIC1和PvRIC2等[24-27]。最近的研究表明,根瘤菌诱导豆科植物地上部miR2111的表达,随后miR2111通过韧皮部从地上运输到根部,与TML结合从而调控根瘤的形成[28]

有意思的是,AON途径中的突变体在根瘤数目上也表现出一定的硝酸盐耐受性(Nitrate tolerance)[4]。通过在高硝酸盐条件下筛选大豆突变体,得到了一批硝酸盐不敏感的突变体nts(Nitrate tolerant symbiosis)。这些突变体在高硝酸盐条件下依然具有超结瘤的表型[29]。通过对这些突变体的基因克隆发现,它们都是由类受体激酶GmNARK基因突变导致[23]。随后在其它豆科植物中也发现了与AON途径相关的突变体对硝酸盐不敏感,在高硝酸盐条件下依然表现出超结瘤表型。例如,百脉根中的har1klv(klavier)、plenty,蒺藜苜蓿中的sunnlss(like sunn supernodulator)、rdn1,豌豆中的sym29[5, 15, 17, 21, 30-32]。除此之外,一些CLE短肽也受硝酸盐诱导表达,如百脉根中的CLE-RS2CLE-RS3[33]。遗传和嫁接实验表明,CLE-RS2过表达引起根瘤数目降低,且依赖于植物地上部受体HAR1[33]。而大豆中的NIC1(Nitrate induced CLE 1)同样受硝酸盐诱导,但NIC1在根部发挥功能,且依赖于植物地下部的受体NARK[25]。以上结果都表明AON途径在硝酸盐抑制结瘤中起着重要的作用。

高浓度的硝酸盐除了抑制根瘤的形成,也会抑制根瘤发育以及固氮酶活性[8]。Cabeza等[34]发现蒺藜苜蓿的根瘤在处理硝酸盐后,编码豆血红蛋白(Leghemoglobins)的相关基因显著下调,固氮酶需要在低氧的环境才能维持活性,而豆血红蛋白可以与氧气结合,为固氮酶提供低氧的环境。这暗示着硝酸盐抑制固氮酶活性可能是通过影响豆血红蛋白的表达,导致根瘤内氧气浓度过高,引起固氮酶的活性下降。除此之外,高浓度的硝酸盐还会抑制侵染线的形成,影响侵染效率[6]。而AON途径中的sunnrdn1har1等突变体虽然在高硝酸盐条件下依然能形成过量的根瘤,但根瘤发育受到限制,只能形成大量小且没有固氮能力的白色根瘤。这说明除了AON途径外,还存在着其它途径参与硝酸盐抑制豆科植物与根瘤菌之间的共生固氮过程。

2 NIN-like proteins(NLPs)转录因子介导硝酸盐抑制结瘤

NIN是第一个被分离鉴定到的豆科植物基因,协同调控根瘤菌侵染和根瘤器官发育[35]。近些年在拟南芥及其它植物中的研究发现,NIN-like protein(NLPs)在硝酸盐信号途径中具有重要作用[36]。NLPs与NIN一样C端都具RWP-RK和PB1结构域[37]。拟南芥基因组中存在9个NLP基因[37]。NLP7感受到硝酸盐后,NLP7蛋白从细胞质中穿梭到细胞核,从而调控硝酸盐信号相关基因的表达[38]。NLP7作为响应硝酸盐信号的核心转录因子可以结合包括硝酸盐吸收、代谢、信号转导相关基因的启动子上,激活这些基因的表达,从而向下传递硝酸盐信号[38-39]。NLP8在感受硝酸盐信号后,能够直接激活ABA水解酶CYP707A2(cytochrome P450,family 707,subfamily A,polypeptide 2)的表达,从而降低ABA含量,打破种子休眠,该研究表明NLP8参与硝酸盐调控种子萌发的过程。与NLP7不同的是,NLP8定位于细胞核,其定位不受硝酸盐影响[40]

最近,在蒺藜苜蓿和百脉根中分别发现NLPs转录因子在调控硝酸盐抑制根瘤共生的过程中发挥着重要作用。Lin等[11]研究发现,蒺藜苜蓿中存在5个NLP基因,5个NLP均可以与NIN蛋白相互作用。他们对这5个NLP基因进行RNA干扰发现,除了NLP2外,其它4个NLP基因的下调,在结瘤上均表现出一定的硝酸盐耐受性。随后获得的两个NLP1 Tnt1插入突变体在氮素缺乏的条件下,形成与野生型一致的根瘤数目和可以正常固氮的根瘤。但在高浓度硝酸盐存在的条件下,nlp1在根瘤数目、侵染线的形成以及固氮酶活性和野生型相比都有显著的提高,说明NLP1在硝酸盐抑制共生固氮的过程中发挥着重要的作用。进一步的研究发现,与拟南芥中的NLP7一样,NLP1能够响应硝酸盐信号从细胞质进入到细胞核中。NLP1通过C端的PB1结构域与NIN互作,并能抑制NIN对下游靶标基因CRE1NF-YA1的激活。该研究表明NLP1感受硝酸盐信号之后,通过干扰NIN的功能从而抑制共生过程。然而,NLP结合的NRE(Nitrate response element)元件与NIN结合元件NBS序列较为相似,体外EMSA实验表明NIN也可以直接结合到NRE上[41]。过表达NIN会抑制响应硝酸盐信号基因的表达[42],说明NIN和NLPs存在着相互竞争靶标基因的可能性。因此,NLP1抑制NIN对下游靶标基因的激活,是因为蛋白复合体的形成减弱了NIN对下游靶标基因的激活能力,还是二者竞争结合到NIN的靶标基因的启动子区并减弱了NIN对靶标基因的激活能力,还有待于进一步研究。

此外,Nishida等[12]在百脉根中也发现了NRSYM1(LjNLP4)参与硝酸盐抑制共生固氮过程。与蒺藜苜蓿nlp1突变体表型一样,nrsym1nitrate unresponsive symbiosis 1)突变体在根瘤数目,侵染线的形成以及固氮酶活性表现出很强的硝酸盐耐受性。NRSYM1同样能响应硝酸盐入核,随后结合在靶标基因启动子区域的NRE元件上激活包括硝酸盐信号NIA(Nitrate reductase)、NIR1(Nitrite reductase 1)以及与AON途径相关的CLE-RS2基因的表达,然后通过HAR1介导的AON途径系统性抑制根瘤形成。虽然Nishida等通过遗传、生化和嫁接实验证明了硝酸盐能够诱导NRSYM1入核,激活CLE-RS2的表达,随后通过AON途径抑制根瘤数目。但AON途径只参与硝酸盐抑制根瘤数目,不参与抑制其它共生过程[8, 12]。而NRSYM1除了调控根瘤数目以外,还参与了硝酸盐抑制结瘤的其它共生过程,包括侵染线的形成、根瘤发育及固氮酶活性。这说明除了AON途径以外,NRSYM1还能通过其它途径激活不同下游的靶标基因介导硝酸盐抑制共生固氮过程。

3 CEP短肽在硝酸盐抑制结瘤中的作用

除了AON途径系统性负调控根瘤数目以外,近年来还在蒺藜苜蓿中发现CRA2(Compact Root Architecture 2)介导的正向调控结瘤途径,CRA2也编码一个富含亮氨酸重复的类受体激酶[43]cra2突变体侧根数量显著增加,但根瘤数目显著减少[43]。嫁接实验发现地上部CRA2控制结瘤,而地下部CRA2控制侧根的形成[43]。Mu等[36]发现在蒺藜苜蓿中,CRA2与SUNN介导的AON途径在调控根瘤数目方面相互独立;cra2突变体在根瘤数目上表现出对硝酸盐敏感,但cra2 sunn双突变体在根瘤数目上表现出硝酸盐耐受性。CRA2是拟南芥中CEP(C-terminally Encoded Peptide)受体CEPR1(CEP Receptor 1)和CEPR2在蒺藜苜蓿中的同源基因[44]CEP被低氮诱导表达,随后被剪切加工为成熟的短肽后,从根部转运到地上部被受体CEPR1和CEPR2识别,激活地上部信号CEPD(Downstream of CEP)基因的表达,CEPD短肽通过韧皮部转运至地下正向调控NRT2.1基因的表达,从而促进植物对硝酸盐的吸收[44-45]。与拟南芥中一样,蒺藜苜蓿中的CEP基因在低氮条件下被诱导表达。过表达CEP1基因或体外添加CEP1短肽都能增加根瘤数目及抑制侧根的形成[46],而在cra2突变体中则不能,说明CRA2极有可能是CEP的受体[46-47]。此外,过表达CEP1基因或体外添加CEP1短肽均能提高根瘤对硝酸盐的耐受性,根瘤数目与对照相比有显著的提高[46],而且CEP1短肽提高蒺藜苜蓿根瘤对硝酸盐的耐受性依赖于地上部的CRA2的存在(本实验室未发表数据)。施加浓度梯度硝酸盐实验表明,cra2突变体对硝酸盐更加敏感,在低浓度硝酸盐处理下,根瘤数目显著降低(本实验室未发表数据)。这些研究结果表明CRA2所介导的正向调控结瘤途径和CEP1都参与了硝酸盐抑制结瘤的过程。

4 总结及展望

高浓度的氮抑制根瘤的形成和固氮酶活性,这被称为“氮阻遏”现象。尽管这一现象很早就被观察到,但其中的分子机制还不十分清楚。硝酸盐信号组分NLPs广泛参与了硝酸盐抑制共生固氮过程,包括侵染线的形成、根瘤发育、根瘤数目及固氮酶活性。目前的研究结果表明,NLPs通过AON途径系统性抑制根瘤数目,但NLPs是否与另一系统性途径CRA2途径存在着cross-talk目前还不清楚。嫁接结果表明NLPs在根部发挥作用,暗示着NLPs可能介导局部信号参与硝酸盐抑制共生过程。NLPs虽然在硝酸盐抑制根瘤共生中发挥重要作用,但其它硝酸盐信号组分是否参与硝酸盐抑制结瘤还需要进一步的探究。此外,植物激素乙烯也参与硝酸盐抑制共生固氮的过程。乙烯负向调控共生过程,外部施加乙烯会抑制根瘤菌的侵染和结瘤[48]。乙烯信号途径组分EIN2(Ethylene INsensitive 2)突变体Mtsickle具有超侵染和超结瘤的表型[49]。从紫花苜蓿(M. sativa)中的研究发现,硝酸盐处理会增加植物根部乙烯的含量,而乙烯合成抑制剂AVG处理可以提高结瘤的硝酸盐耐受性[50]。这些结果都说明乙烯在硝酸盐抑制结瘤的过程中发挥作用。然而乙烯如何参与硝酸盐抑制结瘤,以及与其它途径是否存在着联系还需要进一步的研究。

豆科作物可以通过共生固氮来满足植物对氮的需求,因此在农业生产中可以减少对豆科作物氮肥的施用量。但由于片面追求作物产量而过度施加氮肥导致大量的氮素残留在土壤中,抑制了豆科植物与根瘤菌间的共生固氮作用。了解硝酸盐抑制豆科植物与根瘤菌共生固氮的机制可以避免施用过多的氮肥,同时也可以通过分子育种和基因工程手段提高豆科作物共生固氮的硝酸盐耐受性,提高共生固氮效率以减少无机氮肥的使用,从而改善土壤环境。

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