舒 波， 李偉才， 劉麗琴， 魏永贊， 石勝友

(中國(guó)熱帶農(nóng)業(yè)科學(xué)院南亞熱帶作物研究所， 農(nóng)業(yè)部熱帶果樹(shù)生物學(xué)重點(diǎn)實(shí)驗(yàn)室， 廣東湛江 524091)

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叢枝菌根(AM)真菌與共生植物物質(zhì)交換研究進(jìn)展

舒 波， 李偉才， 劉麗琴， 魏永贊， 石勝友*

(中國(guó)熱帶農(nóng)業(yè)科學(xué)院南亞熱帶作物研究所， 農(nóng)業(yè)部熱帶果樹(shù)生物學(xué)重點(diǎn)實(shí)驗(yàn)室， 廣東湛江 524091)

叢枝菌根(Arbuscular Mycorrhizal，AM)真菌能與約 80% 的陸生植物形成共生關(guān)系，植、 菌間礦質(zhì)養(yǎng)分、 碳水化合物的物質(zhì)交換是自然界物質(zhì)循環(huán)的重要內(nèi)容。目前，AM 真菌促進(jìn)共生植物礦質(zhì)養(yǎng)分吸收的研究相對(duì)較多。研究表明, AM 真菌可通過(guò)根外菌絲更小的吸收直徑，加強(qiáng)礦質(zhì)養(yǎng)分的空間有效性； 通過(guò)釋放有機(jī)酸、 土壤酶，活化土壤中被固定的礦質(zhì)養(yǎng)分； 通過(guò)根外菌絲上較低Km值的礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白，保證養(yǎng)分從土壤至根外菌絲的轉(zhuǎn)運(yùn)效率； 通過(guò)礦質(zhì)養(yǎng)分在菌絲內(nèi)運(yùn)輸形式的改變，增強(qiáng)養(yǎng)分的運(yùn)輸速率； 通過(guò)誘導(dǎo)共生植物礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白表達(dá)，提高植、 菌間養(yǎng)分的轉(zhuǎn)運(yùn)效率。相較于 AM 真菌促進(jìn)共生植物養(yǎng)分吸收，植物反饋真菌碳水化合物的研究相對(duì)較少。鑒于 AM 真菌與植物共生關(guān)系在生態(tài)系統(tǒng)中的重要作用，明晰植、 菌間礦質(zhì)養(yǎng)分和碳水化合物交換的具體場(chǎng)所(叢枝、 根內(nèi)菌絲、 根外菌絲)、 具體形式(離子、 聚合物、 氨基酸、 蔗糖、 單糖)、 具體過(guò)程(主動(dòng)運(yùn)輸)具有重要科學(xué)意義。本文對(duì) AM 真菌與共生植物物質(zhì)交換的叢枝、 菌絲雙膜結(jié)構(gòu)，氮(N)、 磷(P)、 糖等物質(zhì)交換的具體形式以及跨雙膜、 耗能量、 互耦連的物質(zhì)交換過(guò)程進(jìn)行綜述，并從物質(zhì)交換的場(chǎng)所、 形式、 過(guò)程三個(gè)方面提出了植、 菌物質(zhì)交換的研究方向。

礦質(zhì)養(yǎng)分； 碳水化合物； 膜結(jié)構(gòu)； 轉(zhuǎn)運(yùn)蛋白

AM 真菌侵染植物后，植物礦質(zhì)養(yǎng)分的吸收轉(zhuǎn)變?yōu)閮煞N方式，一種依賴(lài)于植物根毛吸收養(yǎng)分—根系直接吸收方式； 另一種則依賴(lài)根外菌絲吸收養(yǎng)分—菌根吸收方式。相較于根系直接吸收方式，菌根吸收方式存在諸多優(yōu)勢(shì)。AM 真菌通過(guò)根外菌絲更小的吸收直徑，增加養(yǎng)分吸收面積，加強(qiáng)礦質(zhì)養(yǎng)分的空間有效性[7]； 通過(guò)自身或誘導(dǎo)共生植物釋放有機(jī)酸、 土壤酶等物質(zhì)，活化土壤中被固定的礦質(zhì)養(yǎng)分，提高礦質(zhì)養(yǎng)分有效濃度[8-9]； 通過(guò)根外菌絲上較低Km值和較高 Vmax 值的礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白，保證養(yǎng)分從土壤轉(zhuǎn)運(yùn)至根外菌絲的效率[10-11]； 通過(guò)礦質(zhì)養(yǎng)分在 AM 真菌菌絲內(nèi)運(yùn)輸形式的改變，加快養(yǎng)分的運(yùn)輸速度[12-13]； 通過(guò)誘導(dǎo)定位于叢枝前體質(zhì)膜(peri-arbuscular membrane)上共生植物礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白表達(dá)，提高植、 菌間養(yǎng)分的轉(zhuǎn)運(yùn)效率[14]。以此為交換，共生植物反饋 AM 真菌碳水化合物，以幫助此類(lèi)嚴(yán)格活體營(yíng)養(yǎng)型真菌完成其生活史[5]。具體地，共生植物光合作用產(chǎn)生的碳水化合物運(yùn)抵根系叢枝細(xì)胞后，在叢枝前體質(zhì)膜與叢枝膜(arbuscular membrane)上相關(guān)轉(zhuǎn)運(yùn)蛋白作用下穿過(guò)雙膜結(jié)構(gòu)，完成植物碳水化合物向 AM 真菌的轉(zhuǎn)運(yùn)[15-16]。

AM 真菌與共生植物間的物質(zhì)交換相互促進(jìn)、 互相關(guān)聯(lián)。目前，關(guān)于 AM 真菌利用自身優(yōu)勢(shì)促進(jìn)共生植物礦質(zhì)養(yǎng)分吸收的研究已較為廣泛，但涉及植、 菌間碳水化合物與礦質(zhì)養(yǎng)分的交換過(guò)程卻少有歸納。鑒于植、 菌共生關(guān)系在自然與農(nóng)業(yè)生態(tài)系統(tǒng)中的重要作用，明確兩者物質(zhì)交換的過(guò)程有重要科學(xué)意義。本文對(duì) AM 真菌與共生植物間礦質(zhì)養(yǎng)分和碳水化合物物質(zhì)交換場(chǎng)所、 物質(zhì)交換形式、 物質(zhì)交換過(guò)程進(jìn)行梳理，以探討植、 菌物質(zhì)交換的研究方向。

1　AM 真菌與共生植物物質(zhì)交換的場(chǎng)所

1.1AM 真菌與共生植物物質(zhì)交換的雙膜結(jié)構(gòu)

AM 真菌與共生植物間絕大部分的物質(zhì)交換發(fā)生于叢枝細(xì)胞內(nèi)[17]。叢枝雙膜結(jié)構(gòu)的形成，標(biāo)志真菌與植物互利共生關(guān)系的真正建立。叢枝是根內(nèi)菌絲在特定細(xì)胞內(nèi)的密集分支，其本質(zhì)是 AM 真菌與共生植物于根系細(xì)胞內(nèi)形成的雙膜結(jié)構(gòu)。叢枝內(nèi)部為真菌膜(叢枝膜)，外部則由植物膜包被(叢枝前體質(zhì)膜)，雙膜之間為儲(chǔ)存交換物質(zhì)的間隙[18]。形式上，雙膜結(jié)構(gòu)將植、 菌雙方間隔開(kāi)來(lái)，叢枝膜一側(cè)為 AM 真菌，叢枝前體質(zhì)膜一側(cè)為共生植物； 功能上，雙膜結(jié)構(gòu)又將植、 菌雙方緊密聯(lián)系起來(lái)，雙膜結(jié)構(gòu)上附著的大量轉(zhuǎn)運(yùn)蛋白與離子通道是植、 菌雙方物質(zhì)交換的載體[15-18]。雖然菌絲也可作為植、 菌間礦質(zhì)養(yǎng)分與單糖物質(zhì)交換的場(chǎng)所，但普遍認(rèn)為其作用甚微[15]。

1.2雙膜結(jié)構(gòu)上的轉(zhuǎn)運(yùn)蛋白

叢枝雙膜上附著的水分、 離子通道、 礦質(zhì)養(yǎng)分以及單糖轉(zhuǎn)運(yùn)蛋白是植、 菌間物質(zhì)交換的基礎(chǔ)。真菌源離子通道、 轉(zhuǎn)運(yùn)蛋白定位于叢枝膜，植物源離子通道、 轉(zhuǎn)運(yùn)蛋白則定位于叢枝前體質(zhì)膜，且 AM 真菌的侵染能特異誘導(dǎo)定位于叢枝前體質(zhì)膜上的植物源礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白表達(dá)，以轉(zhuǎn)運(yùn)根外菌絲吸收的礦質(zhì)養(yǎng)分[19-20]。

2　AM 真菌與共生植物物質(zhì)交換的形式

2.1礦質(zhì)養(yǎng)分的交換形式

2.2碳水化合物的交換形式

作為共生植物附加的一個(gè) “庫(kù)”，AM 真菌碳水化合物需求促使蔗糖從共生植物流向 AM 真菌[44]。蔗糖在運(yùn)抵叢枝細(xì)胞后于叢枝前體質(zhì)膜上蔗糖轉(zhuǎn)運(yùn)蛋白的作用下轉(zhuǎn)運(yùn)至雙膜間隙。而后在植物蔗糖裂解酶、 蔗糖轉(zhuǎn)移酶催化下，裂解為葡萄糖和果糖[45-46]。再經(jīng)叢枝膜上 AM 真菌單糖轉(zhuǎn)運(yùn)蛋白交換至根內(nèi)菌絲，最后葡萄糖和果糖在菌絲內(nèi)轉(zhuǎn)化為海藻糖與糖原，為 AM 真菌所用[45]。但新近研究表明，葡萄糖并非 AM 真菌碳源利用的唯一形式， 叢枝亦不是 AM 真菌獲取碳源的唯一場(chǎng)所，即便是根外菌絲也能吸收諸如木糖，甘露糖等單糖[15]。因此，關(guān)于 AM 真菌碳源的獲取還需要廣泛深入的探索。

3　AM真菌與共生植物物質(zhì)交換過(guò)程

3.1轉(zhuǎn)運(yùn)蛋白的結(jié)構(gòu)

AM 真菌與共生植物間礦質(zhì)養(yǎng)分、 碳水化合物的交換由跨膜轉(zhuǎn)運(yùn)蛋白實(shí)現(xiàn)。真菌源、 植物源礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白共同負(fù)責(zé)礦質(zhì)養(yǎng)分跨過(guò)真菌膜與叢枝前體質(zhì)膜由 AM 真菌向共生植物運(yùn)輸，而植物源、 真菌源蔗糖、 單糖轉(zhuǎn)運(yùn)蛋白則擔(dān)負(fù)碳水化合物跨過(guò)叢枝前體質(zhì)膜與真菌膜由共生植物向 AM 真菌轉(zhuǎn)運(yùn)[47-48]。真菌源與植物源磷轉(zhuǎn)運(yùn)蛋白具有一致的框架結(jié)構(gòu)，總共都包括十二個(gè)跨膜域，N 端、 C 端各六個(gè)。十二個(gè)跨膜域在中間圍成一個(gè)親水環(huán)，具有“6-環(huán)-6”的二級(jí)結(jié)構(gòu)[49]。細(xì)節(jié)上，不同親和力磷轉(zhuǎn)運(yùn)蛋白在跨膜結(jié)構(gòu)上存在差異。一般而言，高親和力磷轉(zhuǎn)運(yùn)蛋白的親水環(huán)在第六和第七個(gè)跨膜域之間，低親和力磷轉(zhuǎn)運(yùn)蛋白的親水環(huán)則在第八和第九個(gè)跨膜域之間[50-51]，高親和力磷轉(zhuǎn)運(yùn)蛋白氨基酸序列的 N 端和 C 端均朝向細(xì)胞膜內(nèi)，低親和力磷轉(zhuǎn)運(yùn)蛋白則相反。

植物源蔗糖、 單糖轉(zhuǎn)運(yùn)蛋白和真菌源單糖轉(zhuǎn)運(yùn)蛋白都屬于 MFS 家族(major facilitator superfamily)，兩者均為高疏水性蛋白，序列高度保守。MFS 成員二級(jí)結(jié)構(gòu)一致，含有十二個(gè)跨膜結(jié)構(gòu)域。中間面向細(xì)胞質(zhì)的部分由一個(gè)大的胞質(zhì)環(huán)，將蛋白分為各含六個(gè)跨膜結(jié)構(gòu)域的兩個(gè)半?yún)^(qū)。雖然跨膜域具有很高的一致性，但在一些重要結(jié)構(gòu)域內(nèi)，部分保守氨基酸存在差異，且這幾個(gè)氨基酸的差異與底物特異性相關(guān)[52]。植物源單糖轉(zhuǎn)運(yùn)蛋白的數(shù)量隨物種的不同呈現(xiàn)差異。迄今，擬南芥有至少五十三個(gè)單糖轉(zhuǎn)運(yùn)蛋白被鑒定分離，蓖麻與灰綠藜中各發(fā)現(xiàn)八個(gè)與七個(gè)單糖轉(zhuǎn)運(yùn)蛋白[53-54]。AM 真菌Glomussp(DAOM 19789)基因組預(yù)測(cè)其不具備編碼蔗糖裂解酶的能力，但其至少編碼三個(gè)單糖轉(zhuǎn)運(yùn)蛋白[15]。真菌源單糖轉(zhuǎn)運(yùn)蛋白的數(shù)量是否因種的不同而變化？另外，蔗糖轉(zhuǎn)運(yùn)蛋白擔(dān)負(fù)碳水化合物轉(zhuǎn)運(yùn)過(guò)叢枝前體質(zhì)膜的任務(wù)，但植物細(xì)胞內(nèi)的單糖是否作為蔗糖的補(bǔ)充形式導(dǎo)入雙膜間隙，進(jìn)而進(jìn)入 AM 真菌也有待進(jìn)一步研究。

3.2物質(zhì)交換的過(guò)程

AM 真菌與共生植物間礦質(zhì)養(yǎng)分和碳水化合物的交換同時(shí)進(jìn)行，兩者相互耦連，互相促進(jìn)。如圖1所示，諸如氮、 磷等礦質(zhì)養(yǎng)分，從真菌一側(cè)經(jīng)叢枝膜上的真菌源轉(zhuǎn)運(yùn)蛋白[圖1中(a)、 (d)，多數(shù)為未知蛋白]導(dǎo)入?yún)仓η绑w質(zhì)膜與真菌膜之間的間隙，再由定位于叢枝前體質(zhì)膜上的植物源礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白[圖1中(c)、 (e)，多數(shù)為已知蛋白]轉(zhuǎn)運(yùn)至共生植物[18, 54]。與礦質(zhì)養(yǎng)分相對(duì)應(yīng)，蔗糖經(jīng)定位于叢枝前體質(zhì)膜上的蔗糖轉(zhuǎn)運(yùn)蛋白轉(zhuǎn)運(yùn)至雙膜間隙[圖1中(g)]，而后于雙膜間隙內(nèi)酶解為單糖，再由叢枝膜上的真菌源單糖轉(zhuǎn)運(yùn)蛋白導(dǎo)入胞內(nèi)菌絲。無(wú)論礦質(zhì)養(yǎng)分由雙膜間隙導(dǎo)入共生植物還是單糖由雙膜間隙導(dǎo)入 AM 真菌，都包括與 H+的同向共轉(zhuǎn)運(yùn)。而 H+離子濃度梯度的驅(qū)動(dòng)則由 H+-ATPase[圖1中(b)]所供給，即 AM 真菌與共生植物間礦質(zhì)養(yǎng)分和碳水化合物的交換為涉及能量的主動(dòng)運(yùn)輸過(guò)程[22]。礦質(zhì)養(yǎng)分、 碳水化合物轉(zhuǎn)運(yùn)蛋白與 H+-ATPases 共表達(dá)，H+-ATPases 活性被抑制后新的叢枝雙膜結(jié)構(gòu)無(wú)法形成，即便是已經(jīng)發(fā)育完好的叢枝也會(huì)慢慢消解[55]。叢枝結(jié)構(gòu)內(nèi)，質(zhì)膜 H+-ATPase 產(chǎn)生 H+梯度，驅(qū)動(dòng) H+與 Pi，H+與單糖同向轉(zhuǎn)運(yùn)的結(jié)論已在多種植、 菌共生體上得以證實(shí)[56-57]。因 H+的同向運(yùn)輸，礦質(zhì)養(yǎng)分與碳水化合物的轉(zhuǎn)運(yùn)相互關(guān)聯(lián)。高土壤磷條件下，真菌單糖轉(zhuǎn)運(yùn)蛋白基因MST2 與蒺藜苜蓿PT4 (AM 真菌侵染特異誘導(dǎo)的磷轉(zhuǎn)運(yùn)蛋白)同時(shí)下調(diào)，且 RNAi 抑制MST2 表達(dá)時(shí)，菌根結(jié)構(gòu)(尤其是叢枝)發(fā)育緩慢，PT4 表達(dá)水平下降[15]。與此相印證，高土壤磷條件下，根系中持續(xù)表達(dá)SUT1 糖轉(zhuǎn)運(yùn)蛋白基因的土豆株系擁有較高的菌根侵染率[58]。上述事實(shí)證明植物碳水化合物與真菌氮、 磷等礦質(zhì)養(yǎng)分的交換相耦連，AM 真菌吸收的礦質(zhì)養(yǎng)分與共生植物供給的碳水化合物實(shí)行“等價(jià)交換”，四個(gè)跨膜運(yùn)輸過(guò)程缺一則難以為繼[59-61]。

4　植、 菌間碳水化合物與礦質(zhì)養(yǎng)分交換研究展望

圖1　真菌氮(N)、 磷(P)與共生植物碳水化合物在雙膜界面上的物質(zhì)交換示意圖Fig.1　The scheme illustrates N, P, and carbohydrate exchanges at the mycorrhizal interface(改編自 Adopted from Harrison[18], Casieri[22], Guether[60])

AM 真菌與共生植物間礦質(zhì)養(yǎng)分、 碳水化合物的物質(zhì)交換廣泛存在于自然界。研究植、 菌間物質(zhì)交換的過(guò)程，對(duì)了解菌根類(lèi)植物的養(yǎng)分吸收具有重要意義。交換場(chǎng)所方面，AM 真菌與植物共生關(guān)系形成后二者物質(zhì)交換的主要場(chǎng)所為根內(nèi)叢枝。然而根內(nèi)菌絲與叢枝具有一致的雙膜結(jié)構(gòu)，且真菌源的磷轉(zhuǎn)運(yùn)蛋白在根內(nèi)菌絲上亦有表達(dá)。筆者推測(cè)根內(nèi)菌絲亦為 AM 真菌與共生植物間物質(zhì)交換的場(chǎng)所之一，其物質(zhì)交換的作用可能主要表現(xiàn)于叢枝形成前的早期侵染階段。除根內(nèi)菌絲外，在 AM 真菌發(fā)育的多個(gè)時(shí)期，根外菌絲能夠吸收諸如木糖，甘露糖等單糖[15]。因此，根外菌絲能否吸收土壤中植物根系分泌的某些碳源(諸如脂肪酸類(lèi))作為 AM 真菌與共生植物間物質(zhì)交換的補(bǔ)充，有待進(jìn)一步研究。同時(shí)，栽培生產(chǎn)上是否能通過(guò)外源單糖，加強(qiáng) AM 真菌碳源強(qiáng)度以此促進(jìn)菌根效應(yīng)的提升，可作為 AM 真菌應(yīng)用研究的一個(gè)方向。交換形式方面，AM 真菌與共生植物間物質(zhì)雙向交換，真菌供給共生植物氮、 磷的交換形式較為明晰而其他諸如鉀(K)、 鋅(Zn)等元素的交換形式有待研究。進(jìn)一步，因部分礦質(zhì)養(yǎng)分轉(zhuǎn)運(yùn)蛋白的轉(zhuǎn)運(yùn)功能存在多樣性(磷轉(zhuǎn)運(yùn)蛋白只能轉(zhuǎn)運(yùn)磷酸根離子，氮、 硫轉(zhuǎn)運(yùn)蛋白能轉(zhuǎn)運(yùn)氨基酸)。AM 真菌與共生植物間物質(zhì)交換形式是否隨環(huán)境條件(如逆境脅迫)而變化仍需要進(jìn)一步研究(圖1)； 目前，共生植物反饋 AM 真菌碳水化合物的研究相對(duì)較少，葡萄糖是共生植物供給 AM 真菌的主要碳源。但菌根植物種類(lèi)繁多，其光合產(chǎn)物亦存在多樣性(蔗糖、 山梨醇、 甘露醇、 木糖醇)，當(dāng) AM 真菌與植物共生關(guān)系形成后以糖醇類(lèi)物質(zhì)作為光合產(chǎn)物的共生植物是否能將糖醇類(lèi)物質(zhì)直接供給 AM 真菌(圖1)？如若不能，此類(lèi)物質(zhì)在碳水化合物及礦質(zhì)養(yǎng)分交換過(guò)程中的代謝途徑有待進(jìn)一步明晰。交換過(guò)程方面，AM 真菌、 共生植物間礦質(zhì)養(yǎng)分、 碳水化合物的物質(zhì)交換過(guò)程相互耦連、 相互促進(jìn)。而涉及此過(guò)程的信號(hào)分子、 調(diào)控模式、 代謝通路猶未可知，明晰二者交換耦連的機(jī)理對(duì) AM 真菌與植物共生的研究同樣具有理論與應(yīng)用意義。

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Progress on material exchange between arbuscular mycorrhizal(AM) fungi and host plant: A review

SHU Bo, LI Wei-cai, LIU Li-qin, WEI Yong-zan, SHI Sheng-you*

(SouthSubtropicalCropsResearchInstitute,CATAS,Zhanjiang/KeyLaboratoryofTropicalFruitBiology,MinistryofAgriculture,Zhanjiang,Guangdong524091,China)

Arbuscular mycorrhizal (AM) fungi can form symbiosis with 80% of terrestrial plant species. The exchange between mineral nutrients of AM fungi and carbohydrate of host plant is important for material cycle in whole ecosystem. Nowadays, there are many studies on the AM fungi promoting host plant mineral nutrient absorption. The AM fungi can enhance availability of mineral nutrients by small diameter of extraradical hyphae, activate soil nutrients by releasing organic acids and soil enzymes, ensure the efficiency of soil nutrition transport into extraradical hyphae by the lower value ofKmnutrient transporter on extraradical hyphae, ensure the rate of nutrition transport in intraradical hyphae by converting nutrients ions to suitable forms, and promote the efficiency of the nutrition transport into host plant by inducing symbiotic plant nutrients transporters. However, the progress of plant feedback carbohydrate to fungi is few. As the important role of AM symbiosis in whole ecosystem, researches about the locations (arbuscule, intraradical hyphae and extraradical hyphae), the forms (ionic forms, polymer, amino acid, sucrose and monosaccharide) and the process (active transport) of the mineral nutrients and carbohydrate exchange are significant. This review summarizes the characteristics of membrane system of arbuscule and intraradical hyphae, the forms of nitrogen (N), phosphate (P) and carbohydrate within the exchange, and the process of exchange which relates to transmembrane, energy expenditure and N or P coupling with carbohydrate. Finally, the prospect of AM fungi and host plant materials exchanges is proposed.

mineral nutrients; carbohydrate; membrane system; transporter

2014-11-25接受日期: 2015-05-25網(wǎng)絡(luò)出版日期: 2015-07-17

國(guó)家自然科學(xué)基金(31401818)； 中央級(jí)公益性科研院所基本科研業(yè)務(wù)費(fèi)專(zhuān)項(xiàng)(1630062014006)資助。

舒波(1985—)， 男， 四川廣安人， 博士， 助理研究員， 主要從事果樹(shù)菌根方面的研究。E-mail: bshbest@163.com

E-mail: ssy7299@163.com

Q945.12； S154.34

A

1008-505X(2016)04-1111-07