查询字段 检索词
  华南农业大学学报  2019, Vol. 40 Issue (5): 175-185  DOI: 10.7671/j.issn.1001-411X.201905068

引用本文  

田江, 梁翠月, 陆星, 等. 根系分泌物调控植物适应低磷胁迫的机制[J]. 华南农业大学学报, 2019, 40(5): 175-185.
TIAN Jiang, LIANG Cuiyue, LU Xing, et al. Mechanism of root exudates regulating plant responses to phosphorus deficiency[J]. Journal of South China Agricultural University, 2019, 40(5): 175-185.

基金项目

广东省杰出青年基金(2015A030306034);广东省特支计划(2015TQ01N078,2015TX01N042)

作者简介

田 江(1976—),男,研究员,博士,E-mail: jtian@scau.edu.cn

文章历史

收稿日期:2019-05-21
网络首发时间:2019-07-22 14:58:36
根系分泌物调控植物适应低磷胁迫的机制
田江 , 梁翠月 , 陆星 , 陈倩倩     
华南农业大学 资源环境学院/根系生物学研究中心,广东 广州 510642
摘要:磷是植物生长发育的必需营养元素,土壤中有效磷含量低是限制作物高产的主要因素。由于长期不当施肥,土壤中累积大量磷素,其中大部分磷是植物难以直接吸收的难溶性无机磷和有机磷。植物在长期进化过程中形成了一系列适应低磷胁迫的机制,其中根系分泌物参与土壤磷活化利用的机制一直是研究的热点问题。本文总结了近十年来关于低磷胁迫调控根系分泌物(有机酸和紫色酸性磷酸酶)合成和分泌的研究进展,对根系分泌物在根际微生态中的重要作用提出了展望,旨在阐明通过控制作物根系分泌物来提高作物磷效率的途径,为培育磷高效作物品种和优化磷肥的田间管理提供思路和奠定理论基础。
关键词低磷    根系分泌物    紫色酸性磷酸酶    有机酸    
Mechanism of root exudates regulating plant responses to phosphorus deficiency
TIAN Jiang , LIANG Cuiyue , LU Xing , CHEN Qianqian     
Root Biology Center/College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
Abstract: Phosphorus (P) is an essential nutrient for plant growth and development. Low phosphate (Pi) availability in soil largely limits crop yield. Due to long-term improper P fertilizer application, a lot of P accumulates to form a huge P pool in soil. However, most P are insoluble inorganic P and organic P, and are difficult to be directly absorbed by plants. Plants have evolved a set of adaptive strategies to low P stress. Among them, the mechanism of root exudates participating in P acquisition and utilization has always been a hot issue. In this review, advances in low P stress regulating synthesis and exudation of root exudates (organic acid and purple acid phosphatases) were summarized. Furthermore, the vital functions of root exudates in rhizosphere ecological system are discussed to elucidate mechanism of P efficiency enhancement in crops through root exudate regulation, which would provide some clues and theoretical bases for development of high P efficiency cultivar and optimization of Pi fertilizer management in fields.
Key words: low phosphorus    root exudate    purple acid phosphatase    organic acid    

磷是植物生长发育的必需营养元素之一,不仅是生物大分子如核酸,蛋白质和脂质等的重要组成成分,而且参与多种代谢过程,例如核苷酸合成、光合作用、能量传递和信号转导等[1-4]。在土壤中,全磷质量分数一般在0.2~1.1 g·kg−1之间,其形态主要分为无机态磷和有机态磷[5]。其中,能直接被植物直接吸收利用的是无机磷酸根离子( ${{\rm{H}}_2}{\rm{PO}}_4^{ - 1}$ ${\rm{HPO}}_4^{ - 2}$ ),其含量一般占土壤全磷的0.1%左右,难以满足作物生长的需求[6-8]。当培养介质中有效磷浓度较低时,作物体内各种代谢活动受到显著的影响,从而表现出生长迟缓、植株瘦弱等缺磷症状,最终导致作物减产[9]。据统计,在全世界范围内低磷胁迫导致农作物产量减少30%~40%[7]。在我国的农业生产中,主要通过施用磷肥来缓解土壤中磷有效性低的问题。但是,由于作物对磷肥的当季利用率不到25%和磷肥的过量施用,我国土壤磷素不断累积,土壤有效磷质量浓度从20世纪90年代的17.1 mg·L−1增加到2012年的33.3 mg·L−1,全国平均磷(P2O5)盈余可达59.2 kg·hm−2[10-11]。过量施用磷肥也带来了水体富营养化等一系列环境问题,并加速了自然界磷矿资源的枯竭[12]。因此,优化磷肥资源的田间管理和培育磷肥利用率高的作物品种,并对二者进行有机结合,是提高磷肥利用效率的必由之路,也是农业可持续发展的必然要求[7, 13-14]

在长期进化过程中,植物形成了一系列适应低磷胁迫的机制,包括重建根系的形态构型、促进根系分泌物(如有机酸和酸性磷酸酶)的分泌、形成植物–微生物共生体系等[1-4, 15]。阐明植物适应低磷胁迫的分子和遗传机制,不仅可以解析作物磷高效的机理,而且为培育磷高效的作物品种奠定了理论基础。本文总结了近十年来关于低磷胁迫调控根系分泌物合成和分泌的研究进展,旨在阐明通过控制作物根系分泌物来提高作物磷效率的途径,为培育磷高效作物品种和优化磷肥的田间管理提供思路。

1 低磷胁迫下植物根系分泌物的功能

根系分泌物是植物在生长过程中,根系以主动或被动方式向培养介质分泌的所有物质的总称,包括有机/无机离子、植物激素、根细胞脱落物及其分解产物等[16-17]。根系分泌物的合成和分泌过程是实现植物与根际环境互作的重要途径,不仅可以改善根际土壤性质,调控根际微生物的群落组成,而且植物可以通过感受根系分泌物及其根际微生态的变化,反馈调节植物的生长[17]。以往的研究表明,低磷胁迫可以调控植物根系紫色酸性磷酸酶(Purple acid phosphatase, PAP)活性以及有机酸的合成和分泌,从而分别影响植物对根际有机磷和难溶性无机磷活化利用[17-19]

2 根系分泌紫色酸性磷酸酶的功能及其调控机制

酸性磷酸酶(Acid phosphatase, APase; E.C. 3.1.3.2)是一类能催化水解磷酸单酯或酸酐,释放无机磷酸根离子(Pi)的水解酶类,其酶活性的最适pH一般低于7.0[20]。在植物中,具有酸性磷酸酶酶学性质的蛋白种类比较多,其中一类是紫色酸性磷酸酶。紫色酸性磷酸酶除了具备以上酸性磷酸酶的特性外,还具有其他明显的生物化学特征,即蛋白存在双金属离子的催化中心、在水溶液中呈紫色或粉红色以及L−酒石酸对其活性无明显抑制作用等[19, 21-22]

2.1 紫色酸性磷酸酶的蛋白结构和酶学特性

随着不同物种基因组测序完成,紫色酸性磷酸酶家族成员的组成、表达模式及其功能在不同植物中都有报道,如拟南芥Arabidopsis thaliana、水稻Oryza sativa、大豆Glycine max和菜豆Phaseolus vulgaris[19, 23-26]。虽然,不同物种之间紫色酸性磷酸酶的同源性较低,但是其结构上具有高度的保守性,例如催化位点均含有β-α-β-α-β折叠[19, 27-28]。同时,紫色酸性磷酸酶的氨基酸序列均包含5个保守的结构域,即 DXG/G DXX Y/G NH(D/E)/VXX H/G HX H(下划线表示7个保守的氨基酸),其中保守结构域中包含的7个保守氨基酸可以结合Fe3+-X2+(X2+表示Fe2+,Mn2+或Zn2+)等金属离子,形成紫色酸性磷酸酶的催化中心[28-31]。以往的研究表明,其催化中心的三价金属离子具有高度保守性,主要是Fe3+。但是,二价离子的种类会存在差异,例如大豆和菜豆的紫色酸性磷酸酶包含Zn2+、在黄花羽扇豆Lupinus luteus中包含Mn2+、在甘薯Ipomoea batatas中包含Zn2+或Mn2+,表明紫色酸性磷酸酶在酶催化中心结构上的多样性[32-35]

根据植物紫色酸性磷酸酶单亚基的大小,其成员可分为大分子量和小分子量的紫色酸性磷酸酶[19, 28]。其中,小分子量紫色酸性磷酸酶的相对分子质量约为35 000,常以单体的形式存在于植物体中,如拟南芥的AtPAP17和菜豆的PvPAP3等[25, 36]。大分子量紫色酸性磷酸酶的亚基相对分子质量在45 000~75 000之间[19, 28]。在植物体中,大分子量紫色酸性磷酸酶的亚基通常会通过二硫键或非共价结合的方式形成同质二聚体或异质二聚体,如菜豆的KbPAP和黄羽扇豆的LlPPD1[28, 35, 37]

一般而言,紫色酸性磷酸酶对含有磷酸单脂键的底物都具有水解活性,尤其是对三磷酸腺苷(ATP)、焦磷酸(PPi)、磷酸化糖类、磷酸化氨基酸或植酸等的水解活性较高。但是,同源性相差较远的紫色酸性磷酸酶的最适底物具有显著的差别。例如,在植物紫色酸性磷酸酶的进化树中(图1),属于Ia亚家族成员的大部分紫色酸性磷酸酶对ATP和磷酸烯醇丙酮酸盐(PEP)具有较高的水解酶活性,包括拟南芥的AtPAP10、AtPAP12、AtPAP25和AtPAP26,大豆的GmSAP,菜豆的KeACP (PvPAP1)和KbPAP (PvPAP2),甘薯的IbPAP1,轮花大戟Euphorbia characias的ELPAP,洋葱Allium cepa的AcPEPP和烟草Nicotiana tabacum的NtPAP12等[38-46]。而且,NtPAP12和AtPAP25还兼有蛋白磷酸酶的酶学性质,分别参与了细胞壁中的α−木糖苷酶和β−葡糖苷酶脱磷酸化过程[43, 46]。与其他紫色酸性磷酸酶不同,Ib-1亚家族的紫色酸性磷酸酶大部分对植酸具有较高的水解活性,包括拟南芥的AtPAP15和AtPAP23、水稻的OsPHY1、烟草的NtPAP、大豆的GmPhy和GmPAP14、玉米Zea mays的ZmPAPhy_b、大麦Hordeum vulgare的HvPAPhy_a和HvPAPhy_b2、小麦Triticum aestivum的TaPAPhy_a1和TaPAPhy_b1、枸橘Poncirus trifoliate的PtPAP3等[47-55]。在IIb亚家族中,部分紫色酸性磷酸酶成员具有核苷酸水解酶的活性。根据金属离子是否激活其活性,将其分为依赖金属离子的双磷酸核苷磷酸酶/磷酸二酯酶和不依赖金属离子的核苷酸焦磷酸酶/磷酸二酯酶[56-58]。其中,黄羽扇豆的LlPPD1是最早发现的依赖金属离子的双磷酸核苷磷酸酶/磷酸二酯酶[35]。紫云英Astragalus sinicus的AsPPD1具有水解磷酸二酯酶活性,也是依赖金属离子的双磷酸核苷磷酸酶/磷酸二酯酶[59]。但是,不依赖金属离子的核苷酸焦磷酸酶/磷酸二酯酶主要催化核苷酸或核苷酸糖类的焦磷酸键/磷酸二酯键的水解[56-57]。例如,在水稻中对UDP−葡萄糖和淀粉合成前体ADP−葡萄糖具有水解活性的OsNPP1和OsNPP6,以及对UDP和ADP具有水解活性的OsNPP2[60]。第III亚家族紫色酸性磷酸酶中,只有拟南芥的AtPAP17 (AtACP5)和菜豆的PvPAP3具有相关的报道[25, 36]。其中,菜豆的PvPAP3对ATP具有较高的水解活性,暗示了PvPAP3参与ATP代谢的生物学功能[25]。虽然,紫色酸性磷酸酶最适底物的研究结果为阐明其生物学功能奠定了基础,但是,由于体外试验难以准确模拟植物细胞内复杂的催化条件,而且植物细胞内存在多种含磷酸单酯键的代谢物,难以逐一进行测试。所以,只有结合生物化学、遗传学和分子生物学等研究手段才能明确紫色酸性磷酸酶的生物学功能。

图 1 植物紫色酸性磷酸酶进化树分析 Fig. 1 Phylogenetic tree analysis of plant purple acid phosphatase Ac: 洋葱Allium cepa; As: 紫云英Astragalus sinicus; At: 拟南芥Arabidopsis thaliana; Ec: 轮花大戟Euphorbia characias; Gm: 大豆Glycine max; Hv: 大麦Hordeum vulgare; Ib: 甘薯Ipomoea batatas; La: 白花羽扇豆Lupinus albus; Ll: 黄花羽扇豆Lupinus luteus; Mt: 截形苜蓿Medicago truncatula; Nt: 烟草Nicotiana tabacum; Os: 水稻Oryza sativa; Pt: 枳Poncirus trifoliate; Pv: 菜豆Phaseolus vulgaris; St: 马铃薯Solanum tuberosum; Ta: 小麦Triticum aestivum; Zm: 玉米Zea mays
2.2 磷有效性对植物紫色酸性磷酸酶表达的调控

低磷胁迫在转录、翻译和蛋白修饰等水平调控紫色酸性磷酸酶的活性,从而促进了植物体内或分泌的酸性磷酸酶的活性[19]。例如:对不同植物紫色酸性磷酸酶家族成员表达模式进行分析,发现低磷胁迫显著提高了拟南芥中29个成员中的9个、大豆中35个成员中的23个、水稻26个成员中的10个、玉米33个成员中的11个紫色酸性磷酸酶基因的表达[19, 61]。同时,也有报道,低磷胁迫增强紫色酸性磷酸酶蛋白积累,比如番茄Lycopersicon esculentum的LeSAP1和LeSAP2、拟南芥的AtPAP10、AtPAP12和AtPAP26,菜豆的PvPAP3,白花羽扇豆Lupinus albus的LaSAP2和大豆GmPAP1-like等[21, 25, 36, 45-46, 62-64]。而且,最近的研究结果表明,在植物的磷信号网络中存在调控紫色磷酸酶表达的重要调控因子。例如:在水稻中,OsPAP10a的表达受转录因子OsMYB2P-1OsPHR2以及OsSPX-MSF1的正调控,但受到生长素响应因子OsARF12OsSPX1OsSPX3OsSPX5的负调控[13, 65];在拟南芥中,AtPAP10的表达受转录因子AtPHR1AtPHL2的正调控,但受到AtTHO1AtTHO3的负调控[66-67];同时,有研究结果显示在拟南芥中乙烯信号途径参与调控了AtPAP10的表达[24]。这些结果说明,低磷胁迫参与调控紫色酸性磷酸酶的表达。但是,由于其组成的复杂性决定了低磷胁迫对其表达调控的途径具有多样性。

2.3 根分泌的紫色酸性磷酸酶活化利用有机磷的机制

根据紫色酸性磷酸酶的酶学特性和低磷促进其酶活性增加的特性,一般认为紫色酸性磷酸酶参与了植物体内和根际有机磷的活化利用[19, 28]。据报道,根系分泌或根系细胞壁定位的紫色酸性磷酸酶能水解根际或质外体空间的有机磷化合物,释放出无机磷酸根离子,从而参与植物对有机磷的活化利用。在菜豆中,Liang等[25]通过分子筛和亲和层析等蛋白纯化的方法,从菜豆根系纯化获得了一个受低磷上调表达的紫色酸性磷酸同工酶PvPAP3,结合其最适底物的酶学性质和超量表达该基因的表型,揭示了PvPAP3参与菜豆根系对外源ATP活化利用的功能。随后,在拟南芥和水稻中也报道了根系分泌紫色酸性磷酸酶具有类似的功能[13, 45, 63, 65]。除了对外源ATP有活化功能外,在大豆、菜豆、柱花草Stylosanthes guianensis和拟南芥中发现根系分泌的紫色酸性磷酸酶具有活化外源dNTP、DNA、ADP和6−磷酸果糖等有机磷的功能,暗示了植物根系分泌的紫色酸性磷酸酶功能的多样性[13, 45, 61, 63-65, 68]

除了核酸磷、磷酸化糖类和磷酸化氨基酸等有机磷外,土壤还存在着大量的植酸磷。早期通过转基因技术,在植物中超量表达分泌型紫色酸性磷酸酶能显著提高转基因植物根际植酸酶活性,从而增强其对外源植酸磷的活化利用能力。例如,在大豆中超量表达含分泌信号肽的AtPAP15,能显著促进转基因大豆对植酸磷活化利用的能力[69]。此外,在白三叶Trifolium repens中超量表达来源于蒺藜苜蓿Medicago sativaMtPHY1,在烟草中超量表达来源于水稻OsPHY1或来源于白花羽扇豆的LaSAP3,也发现类似的结果[26, 70-71]。最近,在柱花草根系中克隆了低磷加强表达的紫色酸性磷酸酶SgPAP23基因,其编码的蛋白对植酸磷具有较高的酶活性,而且超量表达该基因显著提高了转基因菜豆毛根和拟南芥根系分泌植酸酶的活性,从而提高对外源植酸磷的活化利用能力,进一步揭示了根系分泌植酸酶活化利用根际植酸磷的机制[54]

3 根系有机酸的分泌及其活化利用磷的功能

植物在生长的过程中会通过主动或被动的方式向根际分泌多种有机酸[72-73]。低磷条件下,大多数植物根系有机酸的组成和分泌量均明显改变,这对于促进土壤难溶性无机磷的活化利用,改善植物的根际磷营养具有十分重要的作用[17-18]

3.1 有机酸对土壤难溶性无机磷的活化作用

土壤中难溶性无机磷只有在水解后产生磷酸根离子,才能被植物直接吸收利用。在难溶性无机磷的水解过程中,根系分泌的有机酸具有重要的作用[2, 17]。在早期的研究中发现,在土壤中添加有机酸能够降低土壤对磷酸根离子的吸持作用,而且三元羧酸对土壤磷酸根离子的解吸附作用最强,二元羧酸次之,一元羧酸最弱[74]。在比较草酸对FePO4、CaHPO4、AlPO4和磷矿粉等难溶性无机磷活化利用的研究中发现,草酸对AlPO4的活化效果较显著[75]。现在,一般认为有机酸参与活化土壤难溶性无机磷的主要机制包括:1)与土壤中的铁、铝和钙等金属离子进行络合反应,提高这些含磷化合物的溶解性;2)有机酸阴离子与磷酸根离子之间竞争土壤颗粒的结合位点,降低土壤对磷酸根的吸附;3)通过络合反应,改变土壤中的铁铝氧化物等吸附剂表面的电荷,从而降低其对磷酸根的吸附固定;4)降低根际pH,促进难溶性无机磷的溶解等[17, 76]

3.2 低磷对植物根系有机酸合成和分泌的影响

有机酸是植物碳代谢过程中重要的中间产物。低磷胁迫下,植物细胞内与有机酸合成相关的途径会发生改变。同时,有机酸可以通过细胞质膜上的特定转运蛋白或通道分泌到根际。在油菜Brassica napus的研究中发现,低磷条件下其叶片中的磷酸烯醇式丙酮酸羧化酶的活性和柠檬酸含量均显著增加。而且14CO2标记结果显示,叶片合成的柠檬酸大部分转运至根系及根系分泌物中[77]。随后,在番茄、豌豆Pisum sativum和菜豆等植物中也发现低磷胁迫促进了磷酸烯醇式丙酮酸羧化酶的活性,从而增强了根系对有机酸的分泌[78-80]。另外,在白花羽扇豆的研究中发现,低磷胁迫除了加强磷酸烯醇式丙酮酸羧化酶的活性,还增加了柠檬酸合成酶和苹果酸脱氢酶等与有机酸代谢相关酶的活性,从而促进白花羽扇豆排根中有机酸的分泌[81-83]。这些结果说明了植物可以协同调控有机酸的合成和分泌来适应低磷胁迫。

虽然,促进根系有机酸的分泌是植物适应低磷胁迫的普遍机制,但不同植物种类,甚至是同种植物内不同基因型间,其分泌的有机酸种类和数量都存在显著的差异。据报道,低磷胁迫显著促进了玉米、水稻、柱花草和洋白菜Brassica oleraceae等植物根系柠檬酸的分泌[84-87]。在白花羽扇豆和大豆中,低磷胁迫同时促进了柠檬酸和苹果酸的分泌,尤其是白花羽扇豆柠檬酸的分泌量增加了13倍左右[81, 88-89];除了苹果酸和柠檬酸以外,低磷胁迫下植物根系也会分泌其他类型的有机酸包括番石榴酸、草酸、酒石酸和丁二酸等。例如,在低磷条件下木豆Cajanus cajan根系可以分泌大量的番石榴酸[90]。而且在大麦中,对难溶性无机磷活化能力强的基因型分泌的柠檬酸较多,表明了柠檬酸的分泌是影响大麦活化利用难溶性无机磷的重要机制。

3.3 低磷对有机酸合成和分泌的分子调控机制 3.3.1 有机酸合成的分子调控机制

有机酸是植物碳代谢过程中重要的中间产物,所以,碳代谢过程相关酶的活性及其编码基因的表达量会影响有机酸的合成。目前,低磷胁迫调控有机酸合成相关的酶及其基因主要是苹果酸脱氢酶(Malate dehydrogenase, MDH)和柠檬酸合成酶(Citrate synthase, CS)。对多种植物的研究发现,低磷胁迫明显提高了植物MDH基因的表达水平,暗示了其表达量与苹果酸合成和分泌具有较高的相关性[91-94]。随后,在棉花Gossypium hirsutum的研究中发现,超量表达GhmMDH1基因后,其根系苹果酸浓度和分泌量显著增加。而且,在供给Al-P、Fe-P和Ca-P等难溶性无机磷时,超量表达GhmMDH1的转基因株系具有较高的生物量,且磷含量高,进一步说明了GhmMDH1基因可以通过调控苹果酸合成和分泌,影响棉花对难溶性无机磷的活化利用的生物学功能[95]。与该结果相似,在苜蓿中超量表达neMDH基因和在烟草中异源表达菌根真菌的MDH基因也显著提高了苹果酸浓度和分泌量,进一步说明了MDH参与调控苹果酸合成和分泌的功能[96-97]。与MDH基因相似,CS基因的表达水平也影响了植物柠檬酸的合成和分泌,从而参与调控植物活化利用难溶性无机磷的能力。在烟草中超量表达CS基因导致柠檬酸合成酶的活性提高约2倍,柠檬酸的分泌量提高2~4倍[98]。而且,与野生型相比,转基因株系对难溶性无机磷的活化利用能力明显增强[98]。在油菜和拟南芥的研究中也获得了类似的结果,即超量表达CS基因,显著提高了转基因材料内源柠檬酸含量与根系柠檬酸的分泌量,从而分别促进了油菜对Fe-P和拟南芥对Al-P的活化利用能力[99-101]。这些研究结果表明,植物MDH 和CS 可以分别调控植物苹果酸和柠檬酸的合成,从而控制有机酸的分泌和植物对难溶性无机磷活化利用的能力。

3.3.2 低磷调控有机酸转运的分子机制

根系苹果酸的分泌主要通过铝激活型苹果酸转运蛋白(Aluminum-activated malate transporter, ALMT)所介导[102]。植物苹果酸转运子的蛋白结构比较保守,在其N端通常含有5~7个跨膜结构域。但是,其C端的保守性较低,部分成员含有一段较长的跨膜结构域,部分成员则为亲水氨基酸序列[103-106]。虽然,关于ALMT控制植物根系分泌苹果酸的研究较多,但主要是关于苹果酸分泌与植物耐铝毒害的研究。其中,小麦TaALMT1是第1个在植物中克隆到的、编码苹果酸转运蛋白的基因[107]。超量表达该基因显著增加了小麦、大麦和烟草悬浮细胞苹果酸分泌及其耐铝毒害的能力[107-108]。随后,在拟南芥、油菜、苜蓿和大豆等植物研究中,也发现其同源基因具有类似的功能,说明了ALMT参与调控植物根系分泌苹果酸的功能[109-114]。最近,对大麦、橙Citrus sinensis和大豆等植物的研究也表明,苹果酸转运子参与调控了植物对低磷胁迫的响应[92, 115-116]。例如,在大麦中,Delhaize等[115]通过超量表达TaALMT1基因提高酸性土壤中转基因大麦的生物量及磷含量,说明TaALMT1通过调控苹果酸的分泌,促进大麦根系的生长和磷吸收。在大豆根系的研究中发现,34个GmALMT家族成员中仅有4个成员的表达量显著受低磷胁迫加强[116]。而且,超量表达GmALMT5不仅提高了转基因材料根系苹果酸的分泌量,而且促进了转基因拟南芥对难溶性Ca-P的活化和利用,说明ALMT介导的根系苹果酸分泌是植物适应低磷胁迫的重要机制。

与苹果酸的分泌不同,植物根系柠檬酸的分泌主要是由Multidrug and toxic compound extrusion (MATE)家族成员所控制[117]。虽然,在多种植物中已克隆了MATE的同源基因,但目前的研究主要集中在植物MATE调控植物适应缺铁胁迫或铝毒害方面[117],而MATE参与植物适应低磷胁迫的机制鲜有报道。最近Valentinuzzi等[118]在草莓Fragaria×ananassa中发现,2个MATE基因的表达水平受低磷上调,暗示MATE可能介导低磷调控根系柠檬酸分泌的机制。

4 展望

根系分泌物是根际微生态环境的重要组成部分,也是植物根系–土壤–根际微生物产生互作的主要桥梁。以往的研究表明,低磷胁迫下有机酸和紫色酸性磷酸酶的分泌显著影响了根际磷营养的状况,充分说明了根系分泌物调控植物适应低磷胁迫的机制。而且,随着对根际微生物的深入研究,发现植物根系分泌物显著调控了根际微生物群落的组成和活性[119-120]。因此,低磷胁迫下根际微生物群落组成和活性是否发生改变?这些变化是否与根系分泌物(有机酸和酸性磷酸酶)的组成和含量有关?这些科学问题的解答,将有助于全面解析根系分泌物对植物适应低磷胁迫的生物学意义。

参考文献
[1]
CHIOU T J, LIN S I. Signaling network in sensing phosphate availability in plants[J]. Annu Rev Plant Biol, 2011, 62: 185-206. DOI:10.1146/annurev-arplant-042110-103849 (0)
[2]
LIANG C, WANG J, ZHAO J, et al. Control of phosphate homeostasis through gene regulation in crops[J]. Curr Opin Plant Biol, 2014, 21(14): 59-66. (0)
[3]
GUTIÉRREZ-ALANÍS D, OJEDA-RIVERA J O, YONG-VILLALOBOS L, et al. Adaptation to phosphate scarcity: Tips from Arabidopsis roots[J]. Trends Plant Sci, 2018, 23(8): 721-730. DOI:10.1016/j.tplants.2018.04.006 (0)
[4]
HAM B K, CHEN J, YAN Y, et al. Insights into plant phosphate sensing and signaling[J]. Curr Opin Biotechnol, 2018, 49: 1-9. DOI:10.1016/j.copbio.2017.07.005 (0)
[5]
HESTERBERG D. Macroscale chemical properties and X-ray absorption spectroscopy of soil phosphorus[J]. Develop Soil Sci, 2010, 34: 313-356. DOI:10.1016/S0166-2481(10)34011-6 (0)
[6]
KOCHIAN L V, HOEKENGA O A, PIÑEROS M A. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency[J]. Annu Rev Plant Biol, 2004, 55: 459-493. DOI:10.1146/annurev.arplant.55.031903.141655 (0)
[7]
VANCE C P, UHDE-STONE C, ALLAN D L. Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource[J]. New Phytol, 2003, 157(3): 423-447. DOI:10.1046/j.1469-8137.2003.00695.x (0)
[8]
RICHARDSON A E, HOCKING P J, SIMPSON R J, et al. Plant mechanisms to optimise access to soil phosphorus[J]. Crop Pasture Sci, 2009, 60(2): 124-143. DOI:10.1071/CP07125 (0)
[9]
RAGHOTHAMA K G. Phosphate acquisition[J]. Ann Rev Plant Physiol Mol Bio, 1999, 50(1): 665-693. DOI:10.1146/annurev.arplant.50.1.665 (0)
[10]
MA J C, HE P, XU X P, et al. Temporal and spatial changes in soil available phosphorus in China (1990—2012)[J]. Field Crop Res, 2016, 192: 13-20. DOI:10.1016/j.fcr.2016.04.006 (0)
[11]
夏文建, 冀建华, 刘佳, 等. 长期不同施肥红壤磷素特征和流失风险研究[J]. 中国生态农业学报, 2018, 26(12): 1876-1886. (0)
[12]
VENEKLAAS E J, LAMBERS H, BRAGG J, et al. Opportunities for improving phosphorus-use efficiency in crop plants[J]. New Phytol, 2012, 195(2): 306-320. DOI:10.1111/j.1469-8137.2012.04190.x (0)
[13]
TIAN J, WANG C, ZHANG Q, et al. Overexpression of OsPAP10a, a root-associated acid phosphatase, increased extracellular organic phosphorus utilization in rice[J]. J Integr Plant Biol, 2012, 54(9): 631-639. DOI:10.1111/j.1744-7909.2012.01143.x (0)
[14]
LÓPEZ-ARREDONDO D L, LEYVA-GONZÁLEZ M A, GONZÁLEZ-MORALES S I, et al. Phosphate nutrition: Improving low-phosphate tolerance in crops[J]. Annu Rev Plant Biol, 2014, 65: 95-123. DOI:10.1146/annurev-arplant-050213-035949 (0)
[15]
SHAHZAD Z, AMTMANN A. Food for thought: How nutrients regulate root system architecture[J]. Curr Opin Plant Biol, 2017, 39: 80-87. DOI:10.1016/j.pbi.2017.06.008 (0)
[16]
严小龙.根系生物学原理与应用[M]. 北京: 科学出版社, 2007. (0)
[17]
CANARINI A, KAISER C, MERCHANT A, et al. Root exudation of primary metabolites: Mechanisms and their roles in plant responses to environmental stimuli[J]. Front Plant Sci, 2019, 10: 157. DOI:10.3389/fpls.2019.00157 (0)
[18]
CHEN Z C, LIAO H. Organic acid anions: an effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils[J]. J Genet Genom, 2016, 43(11): 631-638. DOI:10.1016/j.jgg.2016.11.003 (0)
[19]
TIAN J, LIAO H. The role of intracellular and secreted purple acid phosphatases in plant phosphorus scavenging and recycling[M]//PLAXTON W C, LAMBERS H. Annual plant reviews: Phosphorus metabolism in plants: Volume 48. Oxford, UK: Wiley-Blackwell, 2015: 265-287. (0)
[20]
DUFF S M, SARATH G, PLAXTON W C. The role of acid phosphatases in plant phosphorus metabolism[J]. Physiol Plant, 1994, 90(4): 791-800. DOI:10.1111/ppl.1994.90.issue-4 (0)
[21]
BOZZO G G, RAGHOTHAMA K G, PLAXTON W C. Structural and kinetic properties of a novel purple acid phosphatase from phosphate-starved tomato (Lycopersicon esculentum) cell cultures [J]. Biochem J, 2004, 377(2): 419-428. DOI:10.1042/bj20030947 (0)
[22]
MATANGE N, PODOBNIK M, VISWESWARIAH S S. Metallophosphoesterases: Structural fidelity with functional promiscuity[J]. Biochem J, 2015, 467(2): 201-216. DOI:10.1042/BJ20150028 (0)
[23]
LI D P, ZHU H F, LIU K F, et al. Purple acid phosphatases of Arabidopsis thaliana: Comparative analysis and differential regulation by phosphate deprivation [J]. J Biol Chem, 2002, 277(31): 27772-27781. DOI:10.1074/jbc.M204183200 (0)
[24]
ZHANG Y, WANG X, LU S, et al. A major root-associated acid phosphatase in Arabidopsis, AtPAP10, is regulated by both local and systemic signals under phosphate starvation [J]. J Exp Bot, 2014, 65(22): 6577-6588. DOI:10.1093/jxb/eru377 (0)
[25]
LIANG C, TIAN J, LAM H, et al. Biochemical and molecular characterization of PvPAP3: A novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization[J]. Plant Physiol, 2010, 152(2): 854-865. DOI:10.1104/pp.109.147918 (0)
[26]
LI R, LU W, GUO C, et al. Molecular characterization and functional analysis of OsPHY1, a purple acid phosphatase (PAP) - type phytase gene in rice (Oryza sativa L.) [J]. J Integr Agr, 2012, 11(8): 1217-1226. DOI:10.1016/S2095-3119(12)60118-X (0)
[27]
OLCZAK M, MORAWIECKA B, WATOREK W. Plant purple acid phosphatases: Genes, structures and biological function[J]. Acta Biochim Pol, 2003, 50(4): 1245-1256. (0)
[28]
TRAN H T, HURLEY B A, PLAXTON W C. Feeding hungry plants: The role of purple acid phosphatases in phosphate nutrition[J]. Plant Sci, 2010, 179(1/2): 14-27. (0)
[29]
BECK J L, DE JERSEY J, ZERNER B, et al. Properties of the Fe(II)-Fe(III) derivative of red kidney bean purple phosphatase: Evidence for a binuclear zinc-iron center in the native enzyme[J]. J Am Chem Soc, 1988, 110(10): 3317-3318. DOI:10.1021/ja00218a061 (0)
[30]
STRÄTER N, KLABUNDE T, TUCKER P, et al. Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II) active site[J]. Science, 1995, 268(5216): 1489-1492. DOI:10.1126/science.7770774 (0)
[31]
SCHENK G, GE Y, CARRINGTON L E, et al. Binuclear metal centers in plant purple acid phosphatases: Fe-Mn in sweet potato and Fe-Zn in soybean[J]. Arch Biochem Biophys, 1999, 370(2): 183-189. DOI:10.1006/abbi.1999.1407 (0)
[32]
DURMUS A, EICKEN C, SIFT B H, et al. The active site of purple acid phosphatase from sweet potatoes (Ipomoea batatas): Metal content and spectroscopic characterization [J]. Eur J Biochem Banner, 1999, 260(3): 709-716. DOI:10.1046/j.1432-1327.1999.00230.x (0)
[33]
DURMUS A, EICKEN C, SPENER F, et al. Cloning and comparative protein modeling of two purple acid phosphatase isozymes from sweet potatoes (Ipomoea batatas) [J]. Biochim Biophys Acta, 1999, 1434(1): 202-209. DOI:10.1016/S0167-4838(99)00176-4 (0)
[34]
MITIC N, SMITH S J, NEVES A, et al. The catalytic mechanisms of binuclear metallohydrolases[J]. Chem Rev, 2006, 106(8): 3338-3363. DOI:10.1021/cr050318f (0)
[35]
ANTONYUK S V, OLCZAK M, OLCZAK T, et al. The structure of a purple acid phosphatase involved in plant growth and pathogen defence exhibits a novel immunoglobulin-like fold[J]. IUCr J, 2014, 1(2): 101-109. DOI:10.1107/S205225251400400X (0)
[36]
DEL POZO J C, ALLONA I, RUBIO V, et al. A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions [J]. Plant J, 1999, 19: 579-589. DOI:10.1046/j.1365-313X.1999.00562.x (0)
[37]
SCHENK G, MITIC N, HANSON G R, et al. Purple acid phosphatase: A journey into the function and mechanism of a colorful enzyme[J]. Coord Chem Rev, 2013, 257(2): 473-482. DOI:10.1016/j.ccr.2012.03.020 (0)
[38]
LEBANSKY B R, MCKNIGHT T D, GRIFFING L R. Purification and characterization of a secreted purple phosphatase from soybean suspension cultures[J]. Plant Physiol, 1992, 99(2): 391-395. DOI:10.1104/pp.99.2.391 (0)
[39]
CASHIKAR A G, KUMARESAN R, RAO N M. Biochemical characterization and subcellular localization of the red kidney bean purple acid phosphatase[J]. Plant Physiol, 1997, 114(3): 907-915. DOI:10.1104/pp.114.3.907 (0)
[40]
SHINANO T, YONETANI R, USHIHARA N, et al. Characteristics of phosphoenolpyruvate phosphatase purified from Allium cepa [J]. Plant Sci, 2001, 161(5): 861-869. DOI:10.1016/S0168-9452(01)00480-0 (0)
[41]
YONEYAMA T, SHIOZAWA M, NAKAMURA M, et al. Characterization of a novel acid phosphatase from embryonic axes of kidney bean exhibiting vanadate: Dependent chloroperoxidase activity[J]. J Biol Chem, 2004, 279(36): 37477-37484. DOI:10.1074/jbc.M405305200 (0)
[42]
VELJANOVSKI V, VANDERBELD B, KNOWLES V L, et al. Biochemical and molecular characterization of AtPAP26: A vacuolar purple acid phosphatase up-regulated in phosphate-deprived Arabidopsis suspension cells and seedlings [J]. Plant Physiol, 2006, 142(3): 1282-1293. DOI:10.1104/pp.106.087171 (0)
[43]
KAIDA R, SERADA S, NORIOKA N, et al. Potential role for purple acid phosphatase in the dephosphorylation of wall proteins in tobacco cells[J]. Plant Physiol, 2010, 153(2): 603-610. DOI:10.1104/pp.110.154138 (0)
[44]
PINTUS F, SPANO D, CORONGIU S, et al. Purification, primary structure, and properties of Euphorbia characias latex purple acid phosphatase [J]. Biochem (Moscow), 2011, 76(6): 694-701. DOI:10.1134/S0006297911060101 (0)
[45]
WANG L, LI Z, QIAN W, et al. The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation[J]. Plant Physiol, 2011, 157(3): 1283-1299. DOI:10.1104/pp.111.183723 (0)
[46]
DEL VECCHIO H A, YING S, PARK J, et al. The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation [J]. Plant J, 2014, 80(4): 569-581. DOI:10.1111/tpj.12663 (0)
[47]
HEGEMAN C E, GRABAU E A. A novel phytase with sequence similarity to purple acid phosphatases is expressed in cotyledons of germinating soybean seedlings[J]. Plant Physiol, 2001, 126(4): 1598-1608. DOI:10.1104/pp.126.4.1598 (0)
[48]
ZHU H F, QIAN W Q, LU X Z, et al. Expression patterns of purple acid phosphatase genes in Arabidopsis organs and functional analysis of AtPAP23 predominantly transcribed in flower [J]. Plant Mol Biol, 2005, 59(4): 581-594. DOI:10.1007/s11103-005-0183-0 (0)
[49]
LUNG S, LEUNG A, KUANG R, et al. Phytase activity in tobacco (Nicotiana tabacum) root exudates is exhibited by a purple acid phosphatase [J]. Phytochemistry, 2008, 69(2): 365-373. DOI:10.1016/j.phytochem.2007.06.036 (0)
[50]
ZHANG W, GRUSZEWSKI H A, CHEVONE B I, et al. An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate[J]. Plant Physiol, 2008, 146(2): 431-440. DOI:10.1104/pp.107.109934 (0)
[51]
KUANG R, CHAN K, YEUNG E, et al. Molecular and biochemical characterization of AtPAP15, a purple acid phosphatase with phytase activity in Arabidopsis [J]. Plant Physiol, 2009, 151(1): 199-209. DOI:10.1104/pp.109.143180 (0)
[52]
DIONISIO G, MADSEN C K, HOLM P B, et al. Cloning and characterization of purple acid phosphatase phytases from wheat, barley, maize, and rice[J]. Plant Physiol, 2011, 156(3): 1087-1100. DOI:10.1104/pp.110.164756 (0)
[53]
SHU B, WANG P, XIA R. Characterisation of the phytase gene in trifoliate orange (Poncirus trifoliata (L.) Raf.) seedlings [J]. Sci Hortic-Amsterdam, 2015, 194: 222-229. DOI:10.1016/j.scienta.2015.08.028 (0)
[54]
LIU P, CAI Z, CHEN Z, et al. A root-associated purple acid phosphatase, SgPAP23, mediates extracellular phytate-P utilization in Stylosanthes guianensis [J]. Plant Cell Environ, 2018, 41(12): 2821-2834. DOI:10.1111/pce.v41.12 (0)
[55]
KONG Y, LI X, WANG B, et al. The soybean purple acid phosphatase GmPAP14 predominantly enhances external phytate utilization in plants[J]. Front Plant Sci, 2018, 9: 292. DOI:10.3389/fpls.2018.00292 (0)
[56]
KANEKO K, OKA H, IKARASHI N, et al. Characterization of a plastidial N-glycosylated nucleotide pyrophosphatase/phospliodiesterase in rice[J]. Plant Cell Physiol, 2006, 47: 89. (0)
[57]
NANJO Y, OKA H, IKARASHI N, et al. Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway[J]. Plant Cell, 2006, 18(10): 2582-2592. DOI:10.1105/tpc.105.039891 (0)
[58]
OLCZAK M, CIURASZKIEWICZ J, WOJTOWICZ H, et al. Diphosphonucleotide phosphatase/phosphodiesterase (PPD1) from yellow lupin (Lupinus luteus L.) contains an iron-manganese center [J]. FEBS Lett, 2009, 583(19): 3280-3284. DOI:10.1016/j.febslet.2009.09.024 (0)
[59]
WANG J, SI Z, LI F, et al. A purple acid phosphatase plays a role in nodule formation and nitrogen fixation in Astragalus Sinicus [J]. Plant Mol Biol, 2015, 88(6): 515-529. DOI:10.1007/s11103-015-0323-0 (0)
[60]
KANEKO K, INOMATA T, MASUI T, et al. Nucleotide pyrophosphatase/phosphodiesterase 1 exerts a negative effect on starch accumulation and growth in rice seedlings under high temperature and CO2 concentration conditions [J]. Plant Cell Physiol, 2014, 55(2): 320-332. DOI:10.1093/pcp/pct139 (0)
[61]
LIU P D, XUE Y B, CHEN Z J, et al. Characterization of purple acid phosphatases involved in extracellular dNTP utilization in Stylosanthes[J]. J Exp Bot, 2016, 67(14): 4141-4154. DOI:10.1093/jxb/erw190 (0)
[62]
MILLER S S, LIU J, ALLAN D L, et al. Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin[J]. Plant Physiol, 2001, 127(2): 594-606. DOI:10.1104/pp.010097 (0)
[63]
ROBINSON W D, PARK J, TRAN H T, et al. The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana [J]. J Exp Bot, 2012b, 63(18): 6531-6542. DOI:10.1093/jxb/ers309 (0)
[64]
WU W, LIN Y, LIU P, et al. Association of extracellular dNTP utilization with a GmPAP1-like protein identified in cell wall proteomic analysis of soybean roots[J]. J Exp Bot, 2018, 69(3): 603-617. DOI:10.1093/jxb/erx441 (0)
[65]
LU L, QIU W, GAO W, et al. OsPAP10c, a novel secreted acid phosphatase in rice, plays an important role in the utilization of external organic phosphorus[J]. Plant Cell Environ, 2016, 39(10): 2247-2259. DOI:10.1111/pce.v39.10 (0)
[66]
SUN L, SONG L, ZHANG Y, et al. Arabidopsis PHL2 and PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate starvation[J]. Plant Physiol, 2016, 170(1): 499-514. DOI:10.1104/pp.15.01336 (0)
[67]
TAO S, ZHANG Y, WANG X, et al. The THO/TREX complex active in miRNA biogenesis negatively regulates root-associated acid phosphatase activity induced by phosphate starvation[J]. Plant Physiol, 2016, 171(4): 2841-2853. (0)
[68]
LIANG C, SUN L, YAO Z, et al. Comparative analysis of PvPAP gene family and their functions in response to phosphorus deficiency in common bean [J]. PLoS One, 2012, 7(5): e38106. DOI:10.1371/journal.pone.0038106 (0)
[69]
WANG X, WANG Y, TIAN J, et al. Overexpressing AtPAP15 enhances phosphorus efficiency in soybean[J]. Plant Physiol, 2009, 151(1): 233-240. DOI:10.1104/pp.109.138891 (0)
[70]
MA X, WRIGHT E, GE Y, et al. Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant: Derived phytase and acid phosphatase genes [J]. Plant Sci, 2009, 176(4): 479-488. DOI:10.1016/j.plantsci.2009.01.001 (0)
[71]
MARUYAMA H, YAMAMURA T, KANEKO Y, et al. Effect of exogenous phosphatase and phytase activities on organic phosphate mobilization in soils with different phosphate adsorption capacities[J]. Soil Sci Plant Nutr, 2012, 58(1): 41-51. DOI:10.1080/00380768.2012.656298 (0)
[72]
RYAN P, DELHAIZE E, JONES D. Function and mechanism of organic anion exudation from plant roots[J]. Annu Rev Plant Physiol and Plant Mol Biol, 2001, 52: 527-560. DOI:10.1146/annurev.arplant.52.1.527 (0)
[73]
HAICHAR F E Z, SANTAELLA C, HEULIN T, et al. Root exudates mediated interactions below ground[J]. Soil Biol Biochem, 2014, 77: 69-80. DOI:10.1016/j.soilbio.2014.06.017 (0)
[74]
STRÖM L, OWEN A G, GODBOLD D L, et al. Organic acid behaviour in a calcareous soil implications for rhizosphere nutrient cycling[J]. Soil Biol Biochem, 2005, 37(11): 2046-2054. DOI:10.1016/j.soilbio.2005.03.009 (0)
[75]
徐锐, 彭新湘. 草酸在提高大豆磷吸收利用及抗铝性中的作用[J]. 西北植物学报, 2002, 22(2): 291-295. DOI:10.3321/j.issn:1000-4025.2002.02.012 (0)
[76]
ADELEKE R, NWANGBURUKA C, OBOIRIEN B. Origins, roles and fate of organic acids in soils: A review[J]. South Afr J Bot, 2017, 108: 393-406. DOI:10.1016/j.sajb.2016.09.002 (0)
[77]
HOFFLAND E, BOOGAARD R V D, NELEMANS J, et al. Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants[J]. New Phytol, 1992, 122: 675-680. (0)
[78]
PILBEAM D J, CAKMAK I, MARSCHNER H, et al. Effect of withdrawal of phosphorus on nitrate assimilation and PEP carboxylase activity in tomato[J]. Plant Soil, 1993, 154(1): 111-117. DOI:10.1007/BF00011079 (0)
[79]
RIVERE-ROLLAND H, CONTARD P.BETSCHE T. Adaptation of pea to elevated atmospheric CO2: Rubiso, phosphoenlopyruvate carboxylase and chloroplast phosphate translocator at different levels of nitrogen and phosphorus nutrition [J]. Plant Cell Environ, 1996, 19(1): 109-117. DOI:10.1111/pce.1996.19.issue-1 (0)
[80]
KONDRACKA A, RYCHTER A M. The role of Pi recycling processes during photo synthesis in phosphate deficient bean plants[J]. J Exp Bot, 1997, 48(7): 1461-1468. DOI:10.1093/jxb/48.7.1461 (0)
[81]
NEUMANN G, MASSONNEAU A, LANGLADE N, et al. Physiological aspects of cluster root function and development in phosphorus: Deficient white lupin (Lupinus albus L.) [J]. Ann Bot, 2000, 85(6): 909-919. DOI:10.1006/anbo.2000.1135 (0)
[82]
UHDE-STONE C, GILBERT G, JOHNSON M F, et al. Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism[J]. Plant Soil, 2003, 248: 99-116. DOI:10.1023/A:1022335519879 (0)
[83]
PEÑALOZA E, MUÑOZ G, SALVO-GARRIDO H, et al. Phosphate deficiency regulates phosphoenolpyruvate carboxylase expression in proteoid root clusters of white lupin[J]. J Exp Bot, 2005, 56(409): 145-153. (0)
[84]
DECHASSA N, SCHENK M K. Root exudation of organic anions by cabbage, carrot and potato plants as affected by P supply[M]// HORST W J, SCHENK M K, BÜRKERT A, et al. Plant nutrition: Developments in plant and soil sciences: Volume 92. [S.L]: Springer, Dordrecht, 2001: 544-545. (0)
[85]
GAUME A, MÄCHLER F, DE LEÓN C, et al. Low-P tolerance by maize (Zea mays L.) genotypes: Significance of root growth, and organic acids and acid phosphatase root exudation [J]. Plant Soil, 2001, 228(2): 253-264. DOI:10.1023/A:1004824019289 (0)
[86]
LI X F, ZUO F H, LING G Z, et al. Secretion of citrate from roots in response to aluminum and low phosphorus stresses in stylosanthes[J]. Plant Soil, 2009, 325(1/2): 219-229. (0)
[87]
YOKOSHO K, YAMAJI N, MA J F. An Al-inducible MATE gene is involved in external detoxification of Al in rice[J]. Plant J, 2011, 68(6): 1061-1069. DOI:10.1111/tpj.2011.68.issue-6 (0)
[88]
JOHNSON J F, ALLAN D L, VANCE C P, et al. Root carbon dioxide fixation by phosphorus-deficient Lupinus albus: Contribution to organic-acid exudation by proteid roots [J]. Plant Physiol, 1996, 112: 19-30. DOI:10.1104/pp.112.1.19 (0)
[89]
LIAO H, WAN H, SHAFF J, et al. Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance: Exudation of specific organic acids from different regions of the intact root system[J]. Plant Physiol, 2006, 141(2): 674-684. DOI:10.1104/pp.105.076497 (0)
[90]
AE N, ARIHARA J, OKADA K., et al. Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent[J]. Science, 1990, 284: 477-480. (0)
[91]
LIGABA A, SHEN H, SHIBATA K, et al. The role of phosphorus in aluminium-induced citrate and malate exudation from rape (Brassica napus) [J]. Physiol Plant, 2004, 120: 575-584. DOI:10.1111/ppl.2004.120.issue-4 (0)
[92]
YANG L T, JIANG H X, QI Y P, et al. Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in citrus roots[J]. Mol Biol Rep, 2012, 39: 6353-6366. DOI:10.1007/s11033-012-1457-7 (0)
[93]
CHEN Z, CUI Q, LIANG C, et al. Identification of differentially expressed proteins in soybean nodules under phosphorus deficiency through proteomic analysis[J]. Proteomics, 2011, 11(24): 4648-4659. DOI:10.1002/pmic.v11.24 (0)
[94]
WANG Z, STRAUB D, YANG H, et al. The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing [J]. Physiol Plant, 2014, 151: 323-338. DOI:10.1111/ppl.12187 (0)
[95]
WANG Z A, LI Q, GE X Y, et al. The mitochondrial malate dehydrogenase1 gene GhmMDH1 is involved in plant and root growth under phosphorus deficiency conditions in cotton [J]. Sci Rep-UK, 2015, 5: 10343. DOI:10.1038/srep10343 (0)
[96]
TESFAYE M, TEMPLE S J, ALLAN D L, et al. Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum[J]. Plant Physiol, 2001, 127(4): 1836-1844. DOI:10.1104/pp.010376 (0)
[97]
LÜ J, GAO X, DONG Z, et al. Improved phosphorus acquisition by tobacco through transgenic expression of mitochondrial malate dehydrogenase from Penicillium oxalicum [J]. Plant Cell Rep, 2012, 31(1): 49-56. DOI:10.1007/s00299-011-1138-3 (0)
[98]
LÓPEZ-BUCIO J, DE LA VEGA O M, GUEVARA-GARCÍA A, et al. Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate[J]. Nat Biotechnol, 2000, 18(4): 450-453. DOI:10.1038/74531 (0)
[99]
KOYAMA H, TAKITA E, KAWAMURA A, et al. Overexpression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium[J]. Plant Cell Physiol, 1999, 40: 482-488. DOI:10.1093/oxfordjournals.pcp.a029568 (0)
[100]
KOYAMA H, KAWAMURA A, KIHARA T, et al. Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphoruslimited soil [J]. Plant Cell Physiol, 2000, 41: 1030-1037. DOI:10.1093/pcp/pcd029 (0)
[101]
WANG Y, XU H, KOU J J, et al. Dual effects of transgenic Brassica napus overexpressing CS gene on tolerances to aluminum toxicity and phosphorus deficiency [J]. Plant Soil, 2013, 362(1/2): 231-246. DOI:10.1007/s11104-012-1289-1 (0)
[102]
MEYER S, DE ANGELI A, FERNIE A R, et al. Intra - and extracellular excretion of carboxylates[J]. Trends Plant Sci, 2010, 15: 40-47. (0)
[103]
DELHAIZE E, GRUBER B D, RYAN P R. The roles of organic anion permeases in aluminium resistance and mineral nutrition[J]. FEBS Lett, 2007, 581: 2255-2262. DOI:10.1016/j.febslet.2007.03.057 (0)
[104]
MOTODA H, SASAKI T, KANO Y, et al. The membrane topology of ALMT1: An aluminum-activated malate transport protein in wheat (Triticum aestivum) [J]. Plant Signal Behav, 2007, 2(6): 467-472. DOI:10.4161/psb.2.6.4801 (0)
[105]
FURUICHI T, SASAKI T, TSUCHIYA Y, et al. An extracellular hydrophilic carboxy terminal domain regulates the activity of TaALMT1: The aluminum-activated malate transport protein of wheat[J]. Plant J, 2010, 64: 47-55. (0)
[106]
LIGABA A, DREYER I, MARGARYAN A, et al. Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter, TaALMT1[J]. Plant J, 2013, 76: 766-780. DOI:10.1111/tpj.12332 (0)
[107]
SASAKI T, YAMAMOTO Y, EZAKI B, et al. A wheat gene encoding an aluminum-activated malate transporter[J]. Plant J, 2004, 37: 645-653. DOI:10.1111/tpj.2004.37.issue-5 (0)
[108]
PEREIRA J F, ZHOU G F, DELHAIZE E, et al. Engineering greater aluminium resistance in wheat by over-expressing TaALMT1 [J]. Ann Bot, 2010, 106(1): 205-214. DOI:10.1093/aob/mcq058 (0)
[109]
HOEKENGA O A, MARON L G, PIÑEROS M A, et al. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminium tolerance in Arabidopsis [J]. Proc Natl Acad Sci USA, 2006, 103(25): 9738-9743. DOI:10.1073/pnas.0602868103 (0)
[110]
LIGABA A, KATSUHARA M, RYAN P R, et al. The BnALMT1 and BnALMT2 genes from rape encode aluminium-activated malate transporters that enhance the aluminium resistance of plant cells [J]. Plant Physiol, 2006, 142: 1294-1303. DOI:10.1104/pp.106.085233 (0)
[111]
LIGABA A, MARON L G, SHAFF J, et al. Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux[J]. Plant Cell Environ, 2012, 35(7): 1185-1200. DOI:10.1111/pce.2012.35.issue-7 (0)
[112]
CHEN Q, WU K H, WANG P, et al. Overexpression of MsALMT1, from the aluminum-sensitive Medicago sativa, enhances malate exudation and aluminum resistance in tobacco [J]. Plant Mol Biol Rep, 2013, 31(3): 769-774. DOI:10.1007/s11105-012-0543-2 (0)
[113]
CHEN Z C, YOKOSHO K, KASHINO M, et al. Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus [J]. Plant J, 2013, 176: 10-23. (0)
[114]
LIANG C, PIÑEROS M A, TIAN J, et al. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils [J]. Plant Physiol, 2013, 161(3): 1347-1361. DOI:10.1104/pp.112.208934 (0)
[115]
DELHAIZE E, TAYLOR P, HOCKING P J, et al. Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminum resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil [J]. Plant Biotechnol J, 2009, 7(5): 391-400. DOI:10.1111/pbi.2009.7.issue-5 (0)
[116]
PENG W, WU W, PENG J, et al. Characterization of the soybean GmALMT family genes and the function of GmALMT5 in response to phosphate starvation[J]. J Integr Plant Biol, 2018, 60(3): 216-231. DOI:10.1111/jipb.v60.3 (0)
[117]
UPADHYAY N, KAR D, DEEPAK MAHAJAN B, et al. The multitasking abilities of MATE transporters in plants[J/OL]. J Exp Bot, 2019, [2019-05-20]. https://academic.oup.com/jxb/advance-article/doi/10.1093/jxb/erz246/5491795. doi: 10.1093/jxb/erz246. (0)
[118]
VALENTINUZZI F, PII Y, VIGANI G, LEHMANN M, et al. Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria×ananassa [J]. J Exp Bot, 2015, 66(20): 6483-6495. DOI:10.1093/jxb/erv364 (0)
[119]
HUANG A C, JIANG T, LIU Y X, et al. A specialized metabolic network selectively modulates Arabidopsis root microbiota [J]. Science, 2019, 364(6440): 546-554. (0)
[120]
ZHANG S, ZHOU J, WANG G, et al. The role of mycorrhizal symbiosis in aluminum and phosphorus interactions in relation to aluminum tolerance in soybean[J]. Appl Microbiol Biot, 2015, 99(23): 10225-10235. DOI:10.1007/s00253-015-6913-6 (0)