叢枝菌根真菌參與下植物-土壤系統(tǒng)的養(yǎng)分交流及調(diào)控

韋莉莉, 盧昌熠, 丁　晶, 俞　慎

1 中國科學(xué)院城市環(huán)境研究所，廈門　361021　　2 中國科學(xué)院大學(xué)，北京　100049

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叢枝菌根真菌參與下植物-土壤系統(tǒng)的養(yǎng)分交流及調(diào)控

韋莉莉1,*, 盧昌熠1,2, 丁晶1,2, 俞慎1

1 中國科學(xué)院城市環(huán)境研究所，廈門3610212 中國科學(xué)院大學(xué)，北京100049

近幾年隨著有機(jī)農(nóng)業(yè)的發(fā)展，叢枝菌根的作用受到特別關(guān)注。叢枝菌根是由植物根系與叢枝菌根真菌(AMF)形成的一種共生體。在植物-AMF-土壤系統(tǒng)中，AMF為植物提供N、P等營養(yǎng)的同時(shí)從根系得到所需的C。概述了植物-AMF-土壤系統(tǒng)中C、N、P等營養(yǎng)物質(zhì)的交流以及AMF與土壤微生物的互作關(guān)系。叢枝菌根的形成可顯著提高植物對P的吸收，且在高P條件下多余的P可儲(chǔ)存于AMF中。AMF對土壤N循環(huán)的影響相當(dāng)復(fù)雜，可能參與調(diào)控N循環(huán)的多個(gè)過程，如硝化作用、反硝化作用和氨氧化作用等。在有機(jī)質(zhì)豐富的土壤中AMF菌絲可快速擴(kuò)增并吸收其中的N，主要供菌絲自身所需，只有一小部分傳遞給植物。AMF對土壤C庫的影響尚存爭議，可能存在時(shí)間尺度的差異。短期內(nèi)可活化土壤C，而在長期尺度上可能有利于土壤C的儲(chǔ)存。AMF能夠通過改變土壤微生物群落結(jié)構(gòu)而影響植物-土壤體系的物質(zhì)交流。AMF與解磷菌、根瘤菌和放線菌的協(xié)同增效作用可促進(jìn)土壤有機(jī)質(zhì)的降解或增強(qiáng)其固氮能力；AMF對氨氧化菌的抑制作用可降低氨的氧化減少N2O的釋放。AMF與外生共生真菌EMF共存時(shí)，表現(xiàn)出協(xié)同增效作用，但EMF的優(yōu)先定殖會(huì)限制AMF的侵染。AMF不同類群之間則主要表現(xiàn)為競爭和拮抗關(guān)系。AMF與土壤微生物之間的互作關(guān)系受土壤無機(jī)環(huán)境的影響，在養(yǎng)分虧缺條件下微生物之間往往表現(xiàn)為競爭關(guān)系。因植物、AMF與土壤微生物之間存在復(fù)雜的互作關(guān)系，為此AMF并不總是表現(xiàn)出其對植物營養(yǎng)的促進(jìn)作用。目前關(guān)于AMF的作用機(jī)理仍以假說為主，需要進(jìn)一步的實(shí)驗(yàn)驗(yàn)證。在植物-AMF-土壤系統(tǒng)中N與C的交流和P與C的交流并未表現(xiàn)出一致性，對N、P循環(huán)相互關(guān)系的進(jìn)一步探討有助于深入理解植物-土壤體系中的養(yǎng)分循環(huán)。植物、AMF和土壤微生物的養(yǎng)分來源及其對養(yǎng)分的相對需求強(qiáng)度和吸收效率尚未可知，因此無法深入理解AMF在植物-土壤體系中養(yǎng)分交流和轉(zhuǎn)化的作用。在方法上，傳統(tǒng)的土壤學(xué)方法在養(yǎng)分動(dòng)態(tài)研究中存在局限性，現(xiàn)代分子生物學(xué)手段和化學(xué)計(jì)量學(xué)的結(jié)合值得嘗試。

叢枝菌根；根際；土壤微生物；養(yǎng)分循環(huán)；植物-AMF-土壤系統(tǒng)

菌根是植物根系與菌根真菌形成的共生體，廣泛存在于自然界中，約80%的陸地植物能夠形成菌根[1]。其中，叢枝菌根(Arbuscularmycorrhiza)是最古老且分布最為廣泛的一類菌根[2]，是由叢枝菌根真菌(Arbuscularmycorrhizalfungi，AMFs)在植物根細(xì)胞內(nèi)形成的一種分枝共生結(jié)構(gòu)。叢枝菌根真菌不僅存在于自然生態(tài)系統(tǒng)中，還可與大部分農(nóng)作物的根系形成菌根[1]。AMF為宿主植物提供N、P等無機(jī)養(yǎng)分，同時(shí)從宿主植物獲得C源。植物固定的含碳化合物近20%為AMF所利用[3-4]。AMF作為養(yǎng)分交換的通道，能夠促進(jìn)生態(tài)系統(tǒng)地上和地下部分進(jìn)行養(yǎng)分交流，因而在生態(tài)系統(tǒng)養(yǎng)分循環(huán)中起重要的調(diào)節(jié)作用[5-7]。但過去關(guān)注的焦點(diǎn)在于AMF對植物營養(yǎng)方面的貢獻(xiàn)，很少從植物-AMF-土壤系統(tǒng)，整體考察物質(zhì)循環(huán)及其之間的平衡關(guān)系。本文重點(diǎn)闡述植物-AMF-土壤體系的碳氮磷物質(zhì)流及AMF與土壤微生物的互作關(guān)系，旨在為今后開展植物養(yǎng)分利用率的協(xié)同調(diào)控研究和生產(chǎn)實(shí)踐提供參考。

1　叢枝菌根促進(jìn)植物-土壤系統(tǒng)的物質(zhì)交流

1.1對植物-土壤系統(tǒng)磷的調(diào)控

磷素極易被固定于土壤中而使其有效性降低[8]，尤其在C∶P 比值較高(>300)的土壤中。因此土壤中有效P的水平通常很低，一般只占總P的2%—3%。加之植物對P的吸收往往使根際處于低P狀態(tài)，根細(xì)胞中的P含量遠(yuǎn)高于根際土壤，使植物對P的進(jìn)一步吸收更加困難，因此P的吸收過程需要高親和轉(zhuǎn)運(yùn)蛋白(PiTs)的協(xié)助，同時(shí)消耗代謝釋放的能量[9]。植物在長期進(jìn)化過程中形成了特定的適應(yīng)機(jī)制協(xié)助植物從土壤中攝取P。其中，菌根的形成可有效地促進(jìn)植物對土壤P的吸收。在形成叢枝菌根的植物體中，AMF可為植物提供高達(dá)100%的P[10]。

AMF菌絲可直接從土壤中吸收無機(jī)P，大大擴(kuò)展了植物吸收P的范圍。AMF菌絲的長度遠(yuǎn)超過植物的根長，在熱帶森林中，菌絲長度可達(dá)根長的13倍[11]，覆蓋范圍可超過根系的700倍。同時(shí)，AMF的侵染可引起一系列土壤理化性質(zhì)的改變，這些變化有可能促進(jìn)有機(jī)P的礦化和難溶態(tài)P的解離。比如，植物對P的吸收與菌絲分泌的磷酸酶含量呈正相關(guān)，接種AMF后的土壤根際磷酸酶活性增加[12]。但根系和菌絲體的分泌物存在一定差異，致使根際和菌絲圈的理化性質(zhì)也有所區(qū)別，如根際的水解酶活性較高，而菌絲圈的磷酸酶活性較高[13]。另外，AMF分泌的有機(jī)酸可降低土壤pH值，也可能活化土壤P[14]。

根系和AMF兩種吸收途徑對植物P的相對貢獻(xiàn)隨P含量的變化而不同。在低P條件下，植物主要依賴于菌絲對P的吸收[10]。通常菌絲吸收的P遠(yuǎn)超過根系直接吸收的量。模型模擬的結(jié)果顯示，菌絲吸收P的速率比根的吸收速率高一個(gè)數(shù)量級(jí)[14]，根對P的吸收甚至可能因接種AMF而完全被抑制[15]。研究表明，雖然接種和未接種作物P的吸收總量沒有顯著差異，但接種作物吸收的P大部分來自菌絲[10]。AMF對根系吸收的限制可能由兩者的競爭所致，也可能由于轉(zhuǎn)運(yùn)蛋白的減少[16]。因根的吸收過程需要消耗能量，因此推測AMF對根吸收的抑制作用可能在一定程度上能夠減少能量的消耗。

在高P條件下，AMF的生物量顯著減少[17]。Balzergue 等觀察到在P含量高達(dá)750 mM條件下，豌豆(Pisumsativum)根系與AMF的物質(zhì)交流幾乎完全停止[17]。最新的研究表明，在高P條件下AMF限制P向地上部傳遞。隨P施入量的增加，未接種的豆科植物地上部的P含量增加了143%，而接種植物地上部分的P含量僅增加了53%，地下部分P的增加幅度沒有顯著差異[18]?？梢姡诟逷條件下多余的P可能儲(chǔ)存在菌絲里。AMF在植物P吸收方面的研究相對較多，但仍然未能解答土壤高P對AMF抑制作用的機(jī)理。雖然有學(xué)者認(rèn)為獨(dú)腳金內(nèi)酯可能參與了調(diào)節(jié)過程，但在高P條件下植物產(chǎn)生的獨(dú)腳金內(nèi)酯也隨之減少，因而很可能存在其他信號(hào)物質(zhì)參與調(diào)節(jié)AMF的定殖[18]。

1.2對植物-土壤系統(tǒng)氮循環(huán)的調(diào)節(jié)

圖1　叢枝菌根參與調(diào)控的土壤氮循環(huán)過程示意圖Fig.1　Nitrogen processes regulated by AMF

最新的研究結(jié)果預(yù)示，AMF可能在溫室氣體控制方面具有重要的調(diào)控作用。Storer[27]通過一系列實(shí)驗(yàn)證明，接種AMF能夠降低土壤N2O的釋放。AMF對N2O的調(diào)控主要是通過抑制硝化菌來完成的。因?yàn)榻臃N叢枝菌根的植物對N的吸收量增加，因而減少了硝化作用的底物，這可能也是N2O排放量減少的原因之一。另外，N2O也可能被反硝化細(xì)菌所消耗，該過程發(fā)生在反硝化作用的最后階段，并在氧化亞氮還原酶的參與下完成[28]。因水分條件直接影響氮循環(huán)過程，因此推測叢枝菌根對N2O 的調(diào)控可能還與叢枝菌根對植物水分狀態(tài)的調(diào)節(jié)有關(guān)[29]。

近年來的研究發(fā)現(xiàn)，叢枝菌根可直接吸收有機(jī)質(zhì)中的N[19-23]。同位素示蹤實(shí)驗(yàn)顯示，在有機(jī)質(zhì)斑塊中AMF菌絲迅速擴(kuò)增[19-23]，菌絲中高達(dá)31%的15N來自有機(jī)質(zhì)斑塊，并將一小部分吸收的15N傳遞給宿主植物，但菌絲中的13C并未顯著增加[19]。可見，菌絲吸收的N來自有機(jī)質(zhì)降解后的無機(jī)含氮化合物。不過目前的研究只觀察到Glomeraceae類AMF具有吸收有機(jī)質(zhì)N源的特性，而接種Gigasporaceae的菌根對植物N吸收的貢獻(xiàn)較小[24-25]。AMF菌絲并不具有降解有機(jī)質(zhì)的功能[26]，可能通過菌絲分泌物刺激特定微生物群落的生長，加速對有機(jī)質(zhì)的降解，間接影響菌絲對N的吸收[19-25]。而且，AMF從有機(jī)質(zhì)中吸收的N主要用于菌絲自身的生長[19]。雖然磷脂脂肪酸圖譜分析的結(jié)果顯示，微生物群落結(jié)構(gòu)并未因菌絲的存在而發(fā)生改變，但13C磷脂脂肪酸和DNA的分析結(jié)果表明，AMF菌絲的介入改變了土壤微生物的組成[28-30]。Toljander 等驗(yàn)證了菌絲分泌物對土壤微生物組成的改變，并鑒定出菌絲分泌物包含如蔗糖和有機(jī)酸等小分子化合物，以及一些尚未鑒別的大分子聚合物[30]。但上述實(shí)驗(yàn)并未探明菌絲分泌物是否促進(jìn)特定微生物群落，如具有降解有機(jī)質(zhì)功能的微生物群落的生長。

1.3影響土壤碳庫

雖然已有研究觀察到叢枝菌根的形成能夠加速有機(jī)質(zhì)的降解，但其生態(tài)意義并未得到關(guān)注。2012年Cheng等在Science上發(fā)文指出，由于菌根促進(jìn)表層土新鮮凋落物和土壤有機(jī)質(zhì)的降解，可能影響到土壤碳庫的儲(chǔ)量[11]。該文引發(fā)了激烈的討論。Kowalchuk[31]在同期Science上以“Bad news for carbon sequestration?”為題，強(qiáng)調(diào)了這一研究結(jié)果的生態(tài)意義，即叢枝菌根通過促進(jìn)有機(jī)質(zhì)的降解可能使土壤CO2排放量增加，同時(shí)減少土壤C庫的存量。2013年，德國和澳大利亞學(xué)者聯(lián)合發(fā)表了一篇論述，分析了由叢枝菌根引起的表層有機(jī)質(zhì)降解對生態(tài)系統(tǒng)土壤C庫的短期和長期效應(yīng)，指出短期內(nèi)叢枝菌根的存在會(huì)引起土壤C庫的暫時(shí)性減少，但從長期來看，多種因素的綜合作用反而可能增加土壤C的儲(chǔ)存[32]。比如，有機(jī)質(zhì)降解后產(chǎn)生的難降解物質(zhì)的輸入、菌絲的輸入、菌絲對土壤團(tuán)聚體的穩(wěn)定作用(保護(hù)有機(jī)質(zhì)不被降解)、以及植物凋落物輸入的增加等，都可能引起土壤有機(jī)碳的增加(圖2)[33-36]。

1.4叢枝菌根調(diào)節(jié)下植物-土壤系統(tǒng)中C、N、P的交互作用

AMF與宿主植物之間的物質(zhì)交流處于動(dòng)態(tài)平衡中，隨植物-AMF-土壤系統(tǒng)中能量和養(yǎng)分狀態(tài)而進(jìn)行調(diào)整。AMF與根系的相互識(shí)別和物質(zhì)交流依賴于信號(hào)物質(zhì)的調(diào)控。根系分泌的獨(dú)腳金內(nèi)酯能夠促進(jìn)AMF的代謝和分枝，AMF則分泌信號(hào)物質(zhì)刺激根系做出響應(yīng)[3]。在缺P條件下，根系選擇性地為傳遞較多養(yǎng)分的菌絲提供較多的C。比如，向貧瘠土壤中添加少量或適量的P，菌根根際的水溶性C含量增加[16]；但當(dāng)植物體內(nèi)P含量較高時(shí)，根向AMF提供的C則減少[18]。根系提供的C是AMF的唯一碳源，因此植物的生長狀況直接影響AMF可獲得的碳量。遮陰處理后植物供給AMF的C減少，但在根際添加蔗糖后，根系和AMF吸收利用的C量均隨之增加[19]。Konvalinková等[37]觀察到，即使是短期的遮蔭處理對AMF的功能也會(huì)產(chǎn)生較大的影響，AMF傳遞給植物的P顯著減少，雖然定殖率和菌絲的生長未出現(xiàn)顯著變化。離體實(shí)驗(yàn)的結(jié)果顯示，當(dāng)外源C的供給減半，AMF(Glomusintraradices)的孢子和菌絲里能累積高達(dá)7倍的P，占真菌干重的4%[38]。在低C條件下，菌絲未減弱自身的生長但限制了養(yǎng)分向植物的傳遞。儲(chǔ)存在AMF里的P主要以復(fù)合磷酸鹽的形式存在，植物在缺P條件下，復(fù)合磷酸鹽能夠被堿性磷酸酶解聚成為植物可利用的形式。因而，植物中的C、P含量跟AMF中的C、P含量處于動(dòng)態(tài)平衡中(圖3)。

圖2　土壤有機(jī)質(zhì)的長期和短期動(dòng)態(tài)概念圖Fig.2　Conceptual short-term vs long-term dynamics of organic matter 根據(jù)Verbruggen[32-36]修正

圖3　植物-AMF-土壤系統(tǒng)中C-N-P的動(dòng)態(tài)平衡示意圖Fig.3　Trade-offs between C-N-P in the Plant-AMF-soil system灰色的箭頭粗細(xì)代表元素流的量

過去曾推測AMF與植物進(jìn)行著類似的C-N交換，即AMF為能夠供給較多C的根系傳遞較多的N。但最近的研究表明，AMF菌絲對N的吸收和向植物的傳遞不受植物供給C量的影響[19]。菌絲的定殖和擴(kuò)增受土壤有機(jī)質(zhì)C∶N比的調(diào)控。AMF菌絲往往定殖于C∶N比較低的有機(jī)質(zhì)土壤中，隨著C∶N比的增加，N礦化速率和N2O通量隨之降低(圖3)[39]。AMF的定殖還與土壤中有機(jī)氮和無機(jī)氮的比例有關(guān)。叢枝菌根常形成于有機(jī)氮含量較低(有機(jī)氮∶無機(jī)氮比較低)的土壤中(圖3)，但AMF菌絲在富含有機(jī)氮的土壤中可快速擴(kuò)增[19,23]。可見，AMF對土壤N和P的吸收以及向植物的傳遞及其與植物C源的交流并未表現(xiàn)出一致性。

2　叢枝菌根與土壤微生物的相互作用

對AMF與土壤中特定微生物之間相互作用的認(rèn)識(shí)，有助于我們對土壤養(yǎng)分循環(huán)的深入理解，同時(shí)也為土壤溫室氣體排放的調(diào)控提供理論支持[40]。目前對AMF與其他土壤微生物的相互作用還知之甚少。土壤是非常復(fù)雜的系統(tǒng)，且處于極端動(dòng)態(tài)的過程中，要對土壤進(jìn)行微觀尺度的觀察和研究具有一定的難度[41]。近年來，以DNA為基礎(chǔ)的分析技術(shù)和方法得以快速發(fā)展。DNA量化分析的結(jié)果表明，AMF與土壤微生物具有很強(qiáng)的相互作用[42-45]。

Marschner等[46]證明了菌根植物和非菌根植物根際具有不同的細(xì)菌群落。Miransari M等證明，AMF的侵染可直接或間接地影響根際微生物群落的數(shù)量和結(jié)構(gòu)，使其發(fā)生變化并達(dá)到新的平衡[45]。在大多數(shù)陸生植物中，菌根真菌與土壤微生物存在著互惠互利的關(guān)系[46]。AMF接種后，菌絲分泌的磷酸酶能夠提高土壤可利用P含量，球囊霉素可改變土壤結(jié)構(gòu)、抑制病原菌、促進(jìn)有益微生物的生長等。土壤微生物可能通過產(chǎn)生植物激素、改善土壤養(yǎng)分狀況和土壤結(jié)構(gòu)、控制病原菌和影響植物生長等途徑，促進(jìn)AMF的生長。但土壤微生物也可能因競爭養(yǎng)分資源對AMF產(chǎn)生抑制作用[47]。

通常，叢枝菌根的形成可顯著增加根表面細(xì)菌、放線菌和固氮菌的數(shù)量，而對真菌的影響很小。但亦有少數(shù)實(shí)驗(yàn)并未觀察到菌根對根際微生物產(chǎn)生促進(jìn)作用。不同類群的微生物對AMF的響應(yīng)不同，比如何氏球囊霉(Glomushoi)表現(xiàn)為正響應(yīng)效應(yīng)，而放線菌和叢毛單胞菌則顯示負(fù)響應(yīng)效應(yīng)。AMF還可能通過影響微生物酶活性而改變微生物群落結(jié)構(gòu)。其他土壤微生物對AMF的影響表現(xiàn)為多元化，既可能促進(jìn)，也可能不產(chǎn)生任何影響，甚至可能抑制AMF的生長。

2.1AMF與非共生土壤微生物

2.1.1AMF與非共生細(xì)菌

AMF與土壤細(xì)菌可協(xié)同促進(jìn)植物對P的吸收。Zhang等[48]利用尼龍網(wǎng)隔實(shí)驗(yàn)證明了AMF (Rhizophagusirregularis)和解磷菌(Pseudomonasalcaligenes)具有協(xié)同增效作用。單獨(dú)接種AMF或解磷菌均能刺激土壤中酸性磷酸酶的活性。相對而言，單獨(dú)接種AMF的土壤中酸性磷酸酶活性較高，而同時(shí)接種AMF和解磷菌土壤中酸性磷酸酶活性更高。但如果土壤P很低，AMF與土壤微生物可能因競爭有限的養(yǎng)分而發(fā)生相互抑制作用[13,39]。

2.1.2AMF與非共生真菌

關(guān)于AMF與非共生真菌相互作用的研究相對較少。AMF可能會(huì)抑制其他真菌或者與特定真菌表現(xiàn)為協(xié)同效應(yīng)。例如，油松幼苗的叢枝菌根抑制了根際土壤中一部分真菌的生長，使油松幼苗根際土壤中真菌的數(shù)量和種類減少[53]；AMF(Glomusmosseae)與黃海葵附生真菌(Penicilliunmthomii)能夠協(xié)同促進(jìn)英國薄荷(Menthapiperita)的生長，提高植株的營養(yǎng)水平[54]。AMF的侵染可顯著改變腐生真菌的群落結(jié)構(gòu)，尤其是降低對葡萄糖敏感的菌群生物量[55]。

2.2AMF與其他共生菌

2.2.1AMF與根瘤菌

AMF和根瘤菌往往同時(shí)存在于豆科植物的根系。AMF定殖于根的皮質(zhì)，固氮菌則一般定殖于根瘤。但在胞外菌絲上也可能著生固氮菌[56]。最近的實(shí)驗(yàn)還觀察到AMF直接定殖于根瘤上[16,57]。叢枝菌根能夠促使根瘤菌的形成并增強(qiáng)固氮作用[58]，但根瘤菌在根部的侵染抑制了AMF的定殖。叢枝菌根可能為根瘤提供P和其他營養(yǎng)元素如銅和鋅，從而增強(qiáng)根瘤的固氮作用[59-60]。而Larimer等和Kaschuk等對大量實(shí)驗(yàn)結(jié)果的Meta分析表明，雖然單獨(dú)接種AMF和根瘤菌對植物N營養(yǎng)都有促進(jìn)作用，但同時(shí)接種兩種菌類并未起到協(xié)同增效作用[61-62]。

低P是根瘤形成的主要限制因子，AMF與根瘤菌的相互作用取決于土壤P含量[63]。AMF為固氮菌提供其所需要的P，加強(qiáng)其固氮能力，進(jìn)而為植物提供更多的N[64-65]。此外，接種AMF促進(jìn)宿主植物的生長發(fā)育，為根瘤菌提供充足的能量，最終將促進(jìn)植物固N(yùn)。在豆科植物中，AMF與根瘤菌在根中的定殖過程享有一條共同的信號(hào)傳導(dǎo)途徑，這對AMF與根瘤菌的相互作用非常重要。土壤N的水平也影響AMF與根瘤菌的相互作用。施N可降低根瘤的形成，但叢枝菌根的形成能夠在一定程度上抵消因N增加對根瘤產(chǎn)生的抑制作用[58]。在只有根瘤菌存在的根系中，如果不施肥則會(huì)形成較多的根瘤，但如果同時(shí)接種AMF，則施肥對根瘤不產(chǎn)生顯著影響。

2.2.2AMF與放線菌

AMF與放線菌的相互作用能夠有效的提高宿主植物的固N(yùn)能力，改善植物的營養(yǎng)狀況從而促進(jìn)宿主植物的生長發(fā)育。弗蘭克氏放線菌(Frankia)與非豆科植物共生形成根瘤[66]。放線根瘤與叢枝菌根同時(shí)接種于黑榿木(Alnusglutinosa)幼苗6個(gè)月后，表現(xiàn)出顯著地協(xié)同增效作用，接種放線菌還促進(jìn)了AMF菌絲的伸長生長[67]。AMF對放線菌也有促進(jìn)作用，如辣椒根系中的放線菌數(shù)量因接種AMF而增加。同時(shí)接種AMF和放線菌，對植物的生長具有更明顯的促進(jìn)作用，植物吸收更多的養(yǎng)分元素，形成的根瘤數(shù)量更多、更大；但相對而言，單獨(dú)接種AMF對植物生長的促進(jìn)作用更加顯著[66-68]。放線菌的侵染可促進(jìn)AMF的定殖和植物養(yǎng)分的吸收。混合接種AMF和弗蘭克放線菌的西藏沙棘，植株的固N(yùn)水平和生物量明顯高于單獨(dú)接種AMF或單獨(dú)接種弗蘭克放線菌的植株[69]。但AMF與放線菌并非始終保持協(xié)同增效作用。在一定條件下，AMF與根際放線菌之間會(huì)產(chǎn)生拮抗作用，并對宿主植物的生長有抑制作用[70]。

2.2.3AMF與EMF

有些植物如木麻黃屬植物能夠同時(shí)與AMF和外生菌根真菌(EMF)形成共生體[1]。雙重接種AMF和EMF能促進(jìn)植物的生長和植物對P的吸收，同時(shí)也能促進(jìn)N向其他植物的傳遞[71-73]。自然條件下AMF比EMF先定殖，AMF的定殖對EMF沒有影響。但如果EMF先定殖，可通過形成包膜隔絕AMF在根表面定殖。有實(shí)驗(yàn)觀察到AMF與EMF發(fā)生拮抗，表現(xiàn)為EMF具有較高的定殖率，而AMF定殖率降低[74]。

2.3AMF的種間競爭

長期以來，關(guān)于AMF與植物相互關(guān)系的研究通常在土壤滅菌條件下進(jìn)行，忽略了AMF之間相互作用的影響。然而最新的研究表明，AMF存在種間競爭[75-76]。Janou?ková等[75]觀察到，增加AMF侵染密度并未促進(jìn)植物的生長，甚至因AMF的種間競爭而抑制植物的生長。相對于根際，AMF之間的競爭在根內(nèi)表現(xiàn)更加劇烈[76]。AMF之間的競爭強(qiáng)度還與宿主提供的C量有關(guān)[77]。蔭蔽處理(向AMF傳輸?shù)腃減少)的菌根共生體中，競爭力相對較弱的真菌(如Rhizophagusirregularis)其生長將被完全抑制[78]。Werner和Kiers發(fā)現(xiàn)[79]，AMF之間的相互作用還與定殖順序有關(guān)。先定殖的AMF對后定殖的AMF產(chǎn)生抑制作用，且隨定殖時(shí)間間隔的延長，抑制作用加強(qiáng)，但后定殖的AMF并未對先定殖的AMF產(chǎn)生顯著影響。土壤養(yǎng)分含量可在一定程度上調(diào)控AMF的種間相關(guān)性。施肥可改變AMF的群落結(jié)構(gòu)，施入少量的P肥使Glomus spp.類AMF成為優(yōu)勢種，且有新的AMF定殖。當(dāng)施入大量P肥，只觀察到其中的兩種AMF存在于土壤中[57]。

3　問題與展望

叢枝菌根在改善土壤結(jié)構(gòu)、增加土壤養(yǎng)分、促進(jìn)植物對養(yǎng)分的吸收以及減少溫室氣體排放等方面的作用，對整個(gè)生態(tài)系統(tǒng)的養(yǎng)分循環(huán)和養(yǎng)分平衡的維持具有重要意義。更好地理解AMF與其他土壤微生物的互作關(guān)系對于可持續(xù)農(nóng)業(yè)管理也是必要的。

相對P而言，叢枝菌根對植物-土壤系統(tǒng)N循環(huán)的研究起步較晚，存在疑問較多。與P不同的是，AMF對N的吸收與植物提供的C似乎無關(guān)，而與有機(jī)質(zhì)含量密切相關(guān)。AMF可在有機(jī)質(zhì)斑塊中快速擴(kuò)增，使有機(jī)質(zhì)降解加快，吸收其中的N供自身生長所需，并傳遞其中的一小部分N給植物，同時(shí)將來自有機(jī)質(zhì)的C傳遞給其他土壤微生物[7]。有大量實(shí)驗(yàn)結(jié)果顯示，接種AMF的植物其N含量并沒有顯著增加[4,25,80]。因此，叢枝菌根在N循環(huán)和植物N營養(yǎng)方面的生態(tài)意義尚存在較大爭議。Reynolds等[24]提出，只有在缺N條件下菌根對植物N的吸收才有意義。Hodge和Fitter[19]以及Veresoglou[25]則認(rèn)為即使在高N水平下，AMF仍然對植物的N營養(yǎng)發(fā)揮作用，并認(rèn)為其意義可能與減少代謝消耗有關(guān)。因?yàn)橄鄬τ诟刀?，菌絲的生長需要消耗的能量較少[81]。

植物與叢枝菌根真菌之間的物質(zhì)交流是有選擇的維持著動(dòng)態(tài)平衡。土壤C、N、P之間存在復(fù)雜的聯(lián)系。對這些錯(cuò)綜復(fù)雜關(guān)系的深入理解將有利于有效利用叢枝菌根調(diào)控土壤養(yǎng)分循環(huán)。在植物-AMF-土壤系統(tǒng)中，AMF的作用是從土壤中吸收N和P，在滿足自身需求的前提下將養(yǎng)分輸送給植物和土壤微生物，同時(shí)將來自植物和有機(jī)質(zhì)中的C傳輸給土壤微生物。那么，在植物-AMF-土壤系統(tǒng)中C、N、P究竟如何分配，C、N、P循環(huán)存在怎樣的耦合關(guān)系目前尚不清楚。最新研究表明，在劇烈氣候變化條件下，由于控制這些元素生物地球化學(xué)過程的不同步，C、N、P循環(huán)的平衡關(guān)系可能被打破[82]。據(jù)此推測，人為干擾下造成的AMF多樣性的改變將引起生態(tài)系統(tǒng)中C、N、P循環(huán)的解耦合。因此，變化環(huán)境條件下AMF與C、N、P循環(huán)的關(guān)系值得特別關(guān)注。

AMF增效作用的發(fā)揮受多種環(huán)境因素的調(diào)控。一方面受土壤環(huán)境中無機(jī)養(yǎng)分含量的影響，另一方面受植物生長和土壤微生物群落結(jié)構(gòu)的調(diào)控。雖然目前尚未開展相關(guān)的研究，但依據(jù)生態(tài)學(xué)種間關(guān)系的原理，AMF、植物和土壤微生物的C、N和P來源及三者對養(yǎng)分的相對需求強(qiáng)度在植物-AMF-土壤微生物的相互關(guān)系中起決定性作用。隨著土壤可供養(yǎng)分的增加，三者之間的關(guān)系可由競爭轉(zhuǎn)為互利。已有實(shí)驗(yàn)表明，在養(yǎng)分虧缺條件下，AMF向植物和土壤微生物傳輸?shù)腘、P顯著減少， AMF與植物和土壤微生物表現(xiàn)為競爭關(guān)系。隨著養(yǎng)分的增加，AMF與土壤微生物對植物養(yǎng)分的吸收表現(xiàn)為協(xié)同增效作用。因此，進(jìn)一步探討其相互關(guān)系的前提首先是確定AMF、植物和土壤微生物的養(yǎng)分來源。AMF的C源來自植物，土壤微生物的C則一方面來自植物，另一方面來自土壤有機(jī)質(zhì)。有趣的是雖然來自植物的C是AMF的唯一碳源，但對熱帶森林菌根的研究發(fā)現(xiàn)，無論在根際還是AMF的菌絲圈植物分泌的C都優(yōu)先供給土壤微生物[13]。那么這一現(xiàn)象是否普遍存在于菌根土壤中值得進(jìn)一步探討。AMF、植物和土壤微生物的N和P均來自土壤，那么由菌絲吸收的養(yǎng)分優(yōu)先供給自身所用還是優(yōu)先供給土壤微生物或宿主植物尚不可知。雖然，目前已知菌絲從有機(jī)質(zhì)中吸收的N可能首先用于自身的擴(kuò)增，但其在菌絲體N營養(yǎng)所占比例如何也還不清楚。

目前的研究集中于根際范圍，而AMF菌絲遠(yuǎn)遠(yuǎn)超越了根系分布的范圍，菌絲圈(即圍繞菌絲的區(qū)域)也是土壤微生物活躍的區(qū)域[23,69]，需要尋找有效的方法開展菌絲圈的研究。另外，將叢枝菌根真菌與傳統(tǒng)的有機(jī)肥和化學(xué)肥料相結(jié)合，大規(guī)模的推廣運(yùn)用到現(xiàn)實(shí)農(nóng)業(yè)中，對農(nóng)業(yè)生產(chǎn)和生態(tài)環(huán)境都具有重要意義。如何將叢枝菌根真菌運(yùn)用到現(xiàn)實(shí)農(nóng)業(yè)生產(chǎn)中應(yīng)成為今后研究的重點(diǎn)。

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Functional relationships between arbuscular mycorrhizal symbionts and nutrient dynamics in plant-soil-microbe system

WEI Lili1,*, LU Changyi1,2, DING Jing1,2, YU Shen1

1InstituteofUrbanEnvironment,ChineseAcademyofScience,Xiamen361021,China2UniversityofChineseAcademyofSciences,Beijing100049,China

Arbuscular mycorrhizal symbioses (AM symbioses), formed between Arbuscular mycorrhizal fungi (AMFs) and the majority (ca. 80%) of terrestrial plants, play an important part in the regulation of nutrient cycling in plant-soil systems. Owing to their potentially promising role in sustainable agriculture, AM symbioses have attracted increasing interest in the last decade. This review emphasized the functional interrelations among AM symbioses, soil free-living microbes, and the dynamics of carbon (C), nitrogen (N), and phosphorus (P) in plant-soil systems. The contribution of AM symbioses to plant P has become central to our understanding of AM symbiotic function over the past few decades. There is accumulating evidence that plant P uptake is bidirectionally regulated by AM symbioses. More specifically, plant P uptake is enhanced by AMF infection when the soil is P deficient, but when there is excessive soil P, its transfer to the plant is restricted and excessive P accumulates in hyphae, spores, or vessels. The ability of plants to take in P has been correlated with the volume of soil that their roots can explore. However, in the presence of AMF, mycorrhizal P uptake becomes the dominant pathway, even though plant growth or total P uptake may not be enhanced by the interaction. A benefit of AMF infection to plant P uptake is associated with carboxylate exudation produced by hyphae, which promote the mineralization and disaggregation of organic matter through enhancing the activities of phosphate-solubilizing bacteria. Comparatively, the effects of AMFs on N cycling are particularly complex since fungi are likely involved in all N processes. Arbuscular mycorrhizal fungi can take up both inorganic N and low-molecular-weight organic N from soil organic matter, which is primarily used by the fungus, with only a small amount being transferred to the roots. Arbuscular mycorrhizal fungi can also reduce N loss by regulating the trade-off between nitrification and denitrification, through reducing the concentrations of soil mineral N due to AMF uptake, improving rhizosphere aggregate stability, and decreasing the pH of soil subjected to AMF inoculation. Nitrogen loss as N2O is reduced as well from the soil inoculation with exogenous AMF. The reduction of N2O emissions is related to the shift of microbial community composition with the decrease of the microbial community responsible for N2O production and the increase of those microbial groups responsible for N2O consumption. Other soil microorganisms, including ammonia-oxidizing bacteria, can be suppressed by AMF infection, which also contributes to reduced N2O production. Arbuscular mycorrhizal fungi can also be associated with other root symbionts such as root nodules. While the exact mechanisms remain unclear, it is generally believed that AMFs deliver nutrients (such as P) for N fixation in nodules or by enhancing the activity of rhizobia. Because of increasing concerns regarding global climate change, AMF contribution to soil C storage has attracted considerable attention in recent years. Whether AMFs facilitate soil C sequestration or induce soil C loss remains under debate. One proposed explanation is that if AMFs promote soil C storage, then this becomes a short-term liability through the stimulation of organic matter decomposition and acceleration of litter degradation, while the long-term benefits include the incorporation of organic matter into soil aggregates and increased litter production due to enhanced plant growth. The flux of nutrient elements in plant-AMF-soil systems are associated with the interactions between AMF and pertinent soil microbes. Arbuscular mycorrhizal fungi generally facilitate the growth of phosphate-solubilizing bacteria, rhizobia, actinomycetes, and ectomycorrhizal fungi (EMF), and the inoculation of actinomycetes also promotes the growth of AMF. However, rhizobia and EMF appear to suppress the colonization and growth of AMF when they arrive before AMF. The interactions between AMF and soil microbes can also be regulated by soil nutrient level, such as the case of low soil nutrient conditions, in which AMFs compete for soil nutrients with free-living soil microbes. Competition can also occur among different AMF taxa. Indeed, the biogeochemical cycles of C, N, and P are interlinked in plant-soil systems, where there is an interaction between free-living soil microorganisms and AMFs, but it is unknown to date how the interactions among soil organisms regulate biogeochemical cycles of soil macro elements. A combined technique that uses both microbiological and stoichiometry methods may be needed to explore this “mystical territory”.

arbuscular mycorrhiza symbosis; rhizosphere; soil microorganism; nutrient dynamic; plant-soil system

中國科學(xué)院戰(zhàn)略性先導(dǎo)科技專項(xiàng)(B類)“土壤-生物系統(tǒng)功能及其調(diào)控”(XDB15030301)；國家自然科學(xué)基金項(xiàng)目(31070463)

2014-12-04; 網(wǎng)絡(luò)出版日期:2015-11-02

Corresponding author.E-mail: llwei@iue.ac.cn

10.5846/stxb201412042407

韋莉莉, 盧昌熠, 丁晶, 俞慎.叢枝菌根真菌參與下植物-土壤系統(tǒng)的養(yǎng)分交流及調(diào)控.生態(tài)學(xué)報(bào),2016,36(14):4233-4243.

Wei L L, Lu C Y, Ding J, Yu S.Functional relationships between arbuscular mycorrhizal symbionts and nutrient dynamics in plant-soil-microbe system.Acta Ecologica Sinica,2016,36(14):4233-4243.