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作者简介:

张艺灿(1992-),女,河北石家庄人,研究实习员,硕士,从事葡萄微生物菌肥研究。E-mail:zhangyic1992@163.com。

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目录contents

    摘要

    溶磷微生物是广泛存在于植株根际土壤中的一类重要功能微生物,它们可以溶解难溶性磷酸盐以释放出可溶性磷供植株吸收利用。溶磷微生物在促进植株生长方面发挥着重要作用,本文从矿质元素、激素、根系构型、 光合作用、土壤肥力等方面综述了溶磷微生物对植株生长的促生机制,并提出了今后研究的发展方向。

    Abstract

    Phosphate-solubilizing microbes(PSM)represent a large group of rhizosphere microbes which can dissolve insoluble phosphate to release dissolved phosphate.PSM play a vital role in promoting plant growth.In this work,we reviewed the plant-growth-promoting mechanisms of PSM involving in mineral elements,hormone,root system architecture, photosynthesis,and soil fertility,and proposed the emphasis of further research,expecting to provide theoretical information for further research.

  • 磷是植株所必需的大量元素之一,参与植株光合作用、能量转移、信号转导、大分子生物合成以及呼吸作用等过程[1-2]。然而,土壤中可供植株吸收的磷却十分有限。这主要与磷元素在土壤中易被固定且吸收运输困难有关。土壤中有机磷含量约占总磷含量的20%~ 80%,主要为植素类、核酸类、 磷酯类以及其他有机磷化合物。但是,这些有机磷需转化为无机磷后才能被植株吸收利用[3]。而土壤中约70%~ 90%无机磷会在吸附、沉淀、淋湿等过程中被土壤固定[4]。例如,在碱性土壤中大部分无机磷会与钙镁结合,形成不溶物,在酸性土壤中则会与铁铝结合,从而被固定在土壤中,难以移动, 不能被植株吸收[5]。因此,解决植株缺磷问题的关键是减少土壤中固定磷元素的量,提高可溶性磷含量。

  • 植株根际土壤中存在着大量微生物,它们与植株的生长代谢密切相关。其中一类微生物可将土壤中不溶性磷转化为可溶性磷并释放到土壤中供给植株,即解磷微生物[6]。早在1903 年,Stalstrom[7] 即发现有些细菌可以溶解难溶性磷酸盐以及磷矿石释放出可溶性磷, 这一发现在1948 年被进一步证实[8],随后受到了研究者们的广泛关注。目前已报道的解磷微生物主要包括细菌、真菌、放线菌。其中细菌包括假单胞菌属(Pseudomonas Migula 1894,237.Nom.Cons.Opon.5,Jud.Comm.1952,121)、 肠杆菌属(Enterobacter Hormaeche and Edwards 1960,72)、芽孢杆菌属(Bacillus Cohn 1872,174;nom.-gen.cons.Nomencl.Comm.Intern.Soc.Microbiol.1937,28;Opin.A.Jud.Comm.1955,39)、欧文氏菌属(Erwinia Winslow, Broadhurst,Buchanan,Krumwiede,Rogers and Smith 1920,209)、固氮菌属(Azotobacter Beijerinck 1901,567)、根瘤菌属(Rhizobium Frank 1889,338.Nom.gen.cons.Opin 34,Jud.Comm.1970,11)、 生根瘤菌属(Mesorhizobium)、 不动杆菌属(Acinetobacter Brisou and Prévot 1954, 727)、黄杆菌属(Flavobacterium Bergey et al.,1923, 97)、克雷伯氏菌属(Klebsiella Trevisan,1885, 105)、 微球菌属(Micrococcus Cohn 1872,151)、 气单胞菌属(Aeromonas Kluyver and van Niel 1936, 398)、普罗威登斯菌属(Providencia Ewing)、土壤杆菌属(Agrobacterium Conn 1942,359.Nom.gen.cons.Opin.33,Jud.Comm.1970,10)、埃希氏菌属(Escherichia Castellani and Chaumers 1919)、沙门氏菌属(Salmonella Ligniéres 1990,389)、伯克霍尔德氏菌属(Burkholderia Yabunchi et al)、无色杆菌属(Achromobacter)、 色杆菌属(Chromobacterium Bergonzini 1881,153.Nom.gen.cons.Opin 16,Jud.Comm.,1958,152)、 沙雷氏菌属(Serratia Bizio 1823,288)、固氮螺菌属(Azospirillum)、产碱菌属(Alcaligenes Castellani and Chalmers 1919,936)、 嗜麦芽寡养单胞菌(Stenotrophomonas maltophilia)、 贪铜菌属(Cupriavidusp)、葡萄球菌属(Staphylo-coccus Rosenbach 1884,18 nom.cons.Opin 17 Jud.Comm.1958,153)、 黄色单胞菌属(Flavimonas Holmes et al 1987)、纤维单胞菌属[Cellulomonas(Bergey et al,1923).Claek 1952]等30 多个属[9-14]; 溶磷真菌包括曲霉菌(Aspergillus)、粉状毕赤酵母(Picha farinose)、 克鲁斯假丝酵母(Candida krissii)、分枝毛霉(Mucor Ramosissimus)、小菌核菌(Sclerotinia ninor)、镰刀菌(Fusarium)、扩展青霉(Penicillum expansum)、 根霉属(Rhizopus)、 青霉属(Penicillium)、蓝状菌属(Talaromyces)等[15-18]; 溶磷放线菌则主要为链霉菌属(Streptomyces Waksman and Henrici 1943,339)[19]

  • 目前,研究人员已从多种生态环境中分离培养出多种溶磷微生物,并验证了其对植株生长具有明显地促进效应(表1)。但,有关溶磷菌的促生机制研究仍不成体系,本文就近年来对溶磷菌的研究进行了总结探讨。

  • 表1 部分溶磷菌促生效应研究

  • 1 溶磷菌可提高根际矿质元素浓度,促进植株生长

  • 矿质元素在植株的生长过程中具有十分重要的作用,缺素会抑制植株的生长甚至导致死亡。而溶磷微生物可在一定程度上提高根际矿质元素含量从而促进植株生长(图1)。Ogut等[27]在小麦上的研究发现,接种溶磷菌芽孢杆菌Bacillus sp.后根际土壤及植株磷含量均显著增加,且其他元素如钾、 镁、锌、锰等含量也显著增加。在玉米根际接种溶磷菌L.fusiformis 31MZR,与对照相比,接菌显著增加了土壤中氮及磷的含量[42]。从大豆根际中分离出溶磷菌并接种到百脉根植株上,植株中全氮、全磷含量均显著增加[43]。表明,溶磷菌接种可显著改善植株营养状况,而矿质元素含量的增加或与菌株的解磷能力相关。

  • 根际酸化为溶磷菌的解磷机制之一。Halde等[44] 在溶磷菌根瘤菌Rhizobium培养基中添加NaOH,发现菌种的解磷能力消失,说明解磷能力或是由低pH值引起。后续的很多研究均表明,土壤(培养液)pH值与溶磷量呈显著负相关[45-46]。 解磷微生物可以分泌大量的有机酸,如柠檬酸、草酸、酒石酸、苹果酸、乳酸等,以降低土壤pH值[47-49]。Huang等[50]利用测序技术测定了溶磷菌B.megaterium strain JX285 的全基因组序列,发现了与有机酸合成相关基因,如柠檬酸合成酶。李小冬等[51]利用转录组测序技术测定了不同磷源条件下阴沟肠杆菌(E.cloacae)的差异表达基因,发现, 多条与有机酸相关的代谢通路被上调表达,且在不同磷浓度下受诱导表达的有机酸种类不同。唐超西等[52]从黑曲霉的cDNA文库中克隆得到了溶磷基因psg A,并将其转移至E.coil HST08 中发现,大肠杆菌可分泌更多种类的有机酸并溶解磷酸三钙。 江红梅[53]通过SMART技术,成功构建了溶磷真菌草酸青霉的cDNA文库,并获得了4 条具有稳定溶磷功能的新基因片段,试验证明,4 个克隆子可通过分泌有机酸来溶解难溶性磷。此外,有学者提出,葡萄糖酸的产生是溶磷菌溶磷的重要机制[54]。 葡萄糖在葡萄糖脱氢酶(GDH)及其协同因子吡咯喹啉奎宁(PQQ)的作用下可转化为葡萄糖酸以溶解难溶性磷酸盐[55]。Goldstein等[56]从溶磷菌E.herbicola中克隆出了pqqE基因,并在大肠杆菌中表达,发现其可促进无机磷的溶解。Ludueña等[57] 发现在缺失PQQ的突变体菌种中,葡萄糖酸产量降低了78%且溶磷能力减少了80%。不同溶磷菌株溶解磷酸的有机酸种类不同,或溶磷菌产生的有机酸的种类及数量不同,是其溶磷能力不同的主要原因[58]

  • 除有机酸外, 一些无机酸, 如H2S、HCl、 H2CO3 等的产生也可以溶解磷矿物以增加磷含量[59]。然而,Altomare等[60]在利用真菌溶解磷矿物时发现,此过程中并没有检测出有机酸,并且溶液pH值一直高于5,故降低根际环境pH值并不是溶磷菌溶磷的唯一途径。Asea等[61]分别在添加与不添加NH4 + 的条件下,检测P.fuscumde的溶磷能力,结果发现当不添加NH4 + 时,菌种未表现出溶磷性。在呼吸作用或NH4 + 同化过程中产生的H+ 或为某些菌种溶磷的唯一机制[62]。Reyes等[63]研究了不同碳源、磷源对青霉菌及其突变体的溶磷效应,结果发现青霉菌的溶磷机制包括产生葡萄糖酸、柠檬酸或者H+ 泵,且这些机制的转化受到氮、 磷及碳源的影响。

  • 除根际酸化外,溶磷微生物还可以通过螯合作用增加土壤中磷含量[964]。溶磷菌分泌的有机酸除直接酸解磷酸盐外,还可利用自身的羟基和羧基螯合土壤中的金属阳离子,如Ca2+、Fe3+、Al3+

  • 图1 溶磷微生物溶磷机理图

  • 等,以释放出更多的磷酸根离子供植株吸收[65]。 Kucey[66]通过在培养基中添加0.05 mol/L的阳离子螯合剂二乙胺四乙酸(EDTA),发现其表现出与接种溶磷微生物P.bilaji相同的溶磷效果,表明螯合作用也是解磷微生物解磷的重要机制之一。与有机酸的螯合作用相似,溶磷菌分泌的胞外多糖可与Al3+、Cu2+、Zn2+、Fe3+、Mg2+ 及K+ 等阳离子形成复合物以增加磷酸根离子的释放[67]。Yi等[68]的研究表明,在有机酸存在的情况下,胞外多糖的分泌可进一步增加培养基中可溶性磷含量,且两者之间的协同作用效果取决于胞外多糖的种类和浓度。故胞外多糖的存在或可进一步促进磷的溶解。除有机酸与胞外多糖外,溶磷菌还可分泌另一种效率极高的螯合剂,即铁载体。铁载体是一类低分子量物质,与Fe3+ 具有极高的亲和性[69]。许多细胞膜受体都可以固定铁/铁载体复合物,从而增加铁元素在植株内的吸收效率以促进植株生长[70]。Ghavami等[71]研究发现,铁载体除促进铁元素吸收外,也可促进植株对锌及磷元素的吸收。

  • 解磷微生物可以分泌磷酸酶、磷酸水解酶、肌醇六磷酸酶等,这些酶可以催化有机磷的矿化[72]。 将解磷微生物接种到鹰嘴豆上,发现土壤中酸性磷酸酶活性升高。且在低磷条件下,磷浓度与酸性磷酸酶活性呈显著正相关[33]。刘春艳等[73]在枳(Poncirus trifoliata)上的研究发现,接种有益微生物丛枝菌根真菌(AM真菌)Funneliformis mosseae可显著增加根系酸性磷酸酶的分泌并增强磷转运蛋白(PtaPT3,PtaPT5 和PtaPT6)的表达以改善枳的磷素营养。Sajidan等[74]已从Klebsiella sp.菌株中分离并克隆出了肌醇六磷酸酶基因(phy),且含有phy的菌株可显著增强对肌醇六磷酸盐的分解利用[75]。此外,溶磷微生物作为一个小型的磷库, 在细胞死亡时释放出的磷素营养可供给植株吸收利用[76]。但一些研究也表明,接种溶磷菌后增加了植株生物量及产量却并未增加植株内磷元素的含量。推测溶磷菌释放出的磷可能被土壤中的其他微生物固定,或者受到了土壤理化性质的影响,使得磷的移动、吸收、吸附等过程中受阻[77]。溶磷菌的促生机制除增加矿质元素吸收外,还存在其他机制且有待进一步研究。

  • 2 溶磷菌可合成激素,促进植株生长

  • 植株生长促进细菌可合成植株生长调节剂,如赤霉素(gibberellin,GA)、细胞分裂素(cytokinin, CK)以及生长素(auxin,IAA),它们可以直接或间接地为植株的生长提供有利条件[78]。Bensidhoum等[79]的研究表明,溶磷菌P.fluorescens可合成IAA并促进大麦的生长。Oshnoei等[80]发现内生溶磷菌B.firmus Bf172 在代谢过程中可以产生较多的IAA, 且IAA含量与溶磷量、铁载体以及蛋白酶的产生呈显著正相关。Ludueña等[81]对溶磷菌Serratia sp.S119 进行测序,发现其基因序列中含有编码吲哚丙酮酸脱羧酶基因(indolepyruvate decarboxylase, ipdC)以及吲哚乙醛脱氢酶基因(indole-3-acetaldehyde dehydrogenase,dhaS),其在依赖色氨酸的IAA合成途径中发挥着重要作用。此外,溶磷菌接种也可以刺激植株产生更多的IAA。Kudoyarova等[82]在小麦上接种溶磷菌P.illinoisensis后,促进了植株体内IAA的合成,并进一步刺激根系生长使得植株捕获磷素的能力增强,从而显著增加了植株的生物量,这一过程与溶磷菌自身产生的IAA并不相关。溶磷菌刺激植株生长可能存在两种模式,即自身合成IAA与诱导植株合成IAA。

  • GA在种子萌发、开花、结实、休眠、衰老等过程中发挥着重要作用[83-84]。外源施用GA可增强植株的生长[85]。Joo等[86]发现溶磷菌Burkholderis sp.KCTC 11096BP可以产生多个种类的GA。Ku等[87]研究表明,溶磷菌B.cereus合成的GA可促进植株生长。此外,溶磷菌产生的GA会影响植株体内其它激素的含量,从而引起激素网络的变化以调控植株的生长[88]。Zhao等[89]发现溶磷菌T.asperellum Q1 可以合成植物激素IAA、GA及脱落酸(abscisic acid,ABA),并且可提高黄瓜内IAA、 GA及ABA含量,增强根系生长,提高根系活力。 将溶磷菌Promicromonospora sp.SE188 接种到番茄根际中,发现溶磷菌可以合成GA,并诱导植株内GA及水杨酸的合成,抑制ABA的合成,以促进植株生长,抵抗病虫危害[90]。另一方面,溶磷菌产生的激素可促进根系分泌物的产生,从而为根际微生物的生长提供更多的物质来源[91]

  • 3 溶磷菌可促进根系发育,改善根系构型

  • Hinsinger等[92]指出,土壤中磷素的缺乏并不是植株吸收磷的能力有限,而是磷在土壤中的移动受阻,所以植株会通过增大根系面积来增加吸收面积。一些研究表明,溶磷菌接种可改善植株的根系形态。在扁穗雀麦根际接种溶磷菌后发现植株根系表现为主根变短、根数变多[93]。王志刚等[94]在西瓜上接种溶磷菌P.ananatis后,发现接种处理显著增加了西瓜幼苗总根长、根表面积及根系体积。在花生根际接种溶磷菌促进了根系发育,根长、根尖数以及根体积显著增加[95]。溶磷菌合成及诱导植株产生IAA则为根系系统发育提供了有利条件[96]。 植株促生细菌P.brassicacearum可以显著促进野生拟南芥侧根的生长,但在生长素运输和响应突变体植株上并无此效应,说明IAA对于侧根的生长是必不可少的[97]。此外,蔡璐等[23]在白三叶草上发现,接种溶磷菌抑制了根系生长,这可能与溶磷菌和植株的作用模式相关,具体的机制需进一步探讨。

  • 4 溶磷菌可改善光合系统,提高光合效率

  • 溶磷菌接种可显著改善植株的光合作用。 Elkoca等[98]在鹰嘴豆上接种溶磷菌B.megaterium M-3,发现接菌后植株叶绿素含量显著增加,生长增强。在水稻上接种溶磷菌Bacillus sp.显著增加了植株的光合作用[99]。余旋等[100]在山核桃上分别接种溶磷菌绿针假单胞菌、荧光假单胞菌以及蜡样芽孢杆菌,发现接种处理均表现出较高的净光合速率。光合系统的改善与植株体内矿质元素尤其是铁的含量相关,Pinto等[101]表明矿质元素含量会影响叶绿素以及类胡萝卜素的含量。此外, Zhang等[102]表明根际促生菌可通过调节植株内源糖/ABA信号来提高拟南芥的光合效率。故,光合效率的提升或为植株营养的改善、内源激素含量变化共同作用的结果。此外,光合系统的改善会产生更多的光合产物并以根系分泌物形式释放到土壤中,从而吸引更多的根际微生物定殖以丰富根际的菌落组成[103]

  • 5 溶磷菌可改善根际微生物群落结构,提高土壤肥力

  • 溶磷菌在根际接种后会引起微生物群落结构变化。土壤中三大微生物比例是衡量土壤肥力的重要指标,细菌数量增加可显著提高土壤中氮和磷含量,放线菌可显著促进有机质的分解、促进植物激素的产生,而真菌数量与土壤肥力呈显著负相关[104-105]。余旋等[106]在山核桃上分别接种溶磷菌绿针假单胞菌、荧光假单胞菌以及蜡样芽孢杆菌后,发现根际细菌及放线菌数量增加,而真菌的数量减少,土壤肥力显著提高。张云霞等[107]研究发现,接种溶磷菌B.subtilis JT-1 可显著提高土壤微生物数量,丰富微生物种类,提高土壤活力。在大豆根际添加溶磷菌后,土壤中细菌、解磷菌以及氨化细菌的数量均显著增加[108]。在施用溶磷微生物菌肥后,改变了植株根际细菌群落组成,并增加了功能微生物的丰富度[109]。此外,溶磷菌接种还可促进土壤AM真菌对植物根系的侵染[110]。由此可知,溶磷菌接种到根际后,对根际微生物环境产生了重要影响。

  • 根际微生物菌落结构的变化可能与根际环境及植株营养状态有关。Estrada-Bonilla等[111]在堆肥研究中发现,pH值与微生物种群的变化密切相关, 推测,溶磷菌接种通过改变根际pH值从而影响根际微生物群落结构。变形菌门、酸杆菌门以及放线菌门是不同类型土壤的优势菌落,统计发现这些优势菌种在土壤中的丰度与土壤速效磷含量及土壤酶活变化有关[112]。溶磷菌接种后引起的速效磷含量增加以及土壤酶活的变化也可能诱导了微生物群落的改变。此外,溶磷菌接种可改善根系构型,从而为根际细菌的侵染定殖提供了更大的空间。

  • 6 展望

  • 溶磷微生物作为重要的生物资源,在减少磷肥施用,改善土壤,促进植株生长中发挥着重要作用。然而,目前有关溶磷微生物的促生机制研究仍停留在表观物质变化研究并在推广使用中存在较多问题。接下来可从以下3 方面进行深入研究:(1) 利用全基因组测序技术解析溶磷微生物的基因序列,寻找溶磷促生相关基因,并利用分子生物学手段鉴定基因功能,为溶磷微生物的快速筛选提供理论依据。(2)寻找更加有效的分离培养土壤微生物的方法以获得更加丰富的菌种资源。(3)运用分子生物学手段寻找溶磷微生物的“最佳伴侣”,以组合形式接入到根际土壤中,以提高溶磷微生物的定殖率。

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