• Scopus收录期刊
  • CSCD(核心库)来源期刊
  • 中文核心期刊
  • 中国科技核心期刊
  • F5000顶尖学术来源期刊
  • RCCSE中国核心学术期刊
高级检索

丛枝菌根真菌对银中杨叶片物质代谢及化学防御的影响

武帅, 姜礅, 马庆辉, 谭明涛, 赵佳齐, 刘晓霞, 孟昭军, 严善春

武帅, 姜礅, 马庆辉, 谭明涛, 赵佳齐, 刘晓霞, 孟昭军, 严善春. 丛枝菌根真菌对银中杨叶片物质代谢及化学防御的影响[J]. 北京林业大学学报, 2021, 43(5): 86-92. DOI: 10.12171/j.1000-1522.20200172
引用本文: 武帅, 姜礅, 马庆辉, 谭明涛, 赵佳齐, 刘晓霞, 孟昭军, 严善春. 丛枝菌根真菌对银中杨叶片物质代谢及化学防御的影响[J]. 北京林业大学学报, 2021, 43(5): 86-92. DOI: 10.12171/j.1000-1522.20200172
Wu Shuai, Jiang Dun, Ma Qinghui, Tan Mingtao, Zhao Jiaqi, Liu Xiaoxia, Meng Zhaojun, Yan Shanchun. Effects of arbuscular mycorrhizal fungi on metabolism and chemical defense of Populus alba × P. berolinensis leaves[J]. Journal of Beijing Forestry University, 2021, 43(5): 86-92. DOI: 10.12171/j.1000-1522.20200172
Citation: Wu Shuai, Jiang Dun, Ma Qinghui, Tan Mingtao, Zhao Jiaqi, Liu Xiaoxia, Meng Zhaojun, Yan Shanchun. Effects of arbuscular mycorrhizal fungi on metabolism and chemical defense of Populus alba × P. berolinensis leaves[J]. Journal of Beijing Forestry University, 2021, 43(5): 86-92. DOI: 10.12171/j.1000-1522.20200172

丛枝菌根真菌对银中杨叶片物质代谢及化学防御的影响

基金项目: 国家重点研发计划项目(2018YFC1200400)
详细信息
    作者简介:

    武帅。主要研究方向:昆虫化学生态。Email:1072443533@qq.com 地址:150040 黑龙江省哈尔滨市香坊区和兴路26号东北林业大学林学院

    责任作者:

    严善春,教授,博士生导师。主要研究方向:昆虫化学生态。Email:yanshanchun@126.com 地址:同上

  • 中图分类号: S718.43;S792.119

Effects of arbuscular mycorrhizal fungi on metabolism and chemical defense of Populus alba × P. berolinensis leaves

  • 摘要:
      目的   探究两种丛枝菌根真菌摩西球囊霉(GM)和根内球囊霉(GI)对银中杨物质代谢及化学防御的影响。
      方法   本研究采用孢子含量均为15 个/g的GM、GI基质,分别称取20 g孢子基质与1.3 kg灭菌土混合均匀制成混合基质,将银中杨扦插苗移栽至混合基质中。在丛枝菌根真菌侵染率达到最高时(第90天),分析银中杨叶片内N、P元素、营养物质和次生代谢产物含量,以及防御蛋白活性。
      结果   GM和GI处理组银中杨,叶片内N和P、可溶性蛋白质含量均显著高于对照组(P < 0.05),可溶性糖含量显著低于对照组(P < 0.05),淀粉含量与对照组差异不显著(P > 0.05)。次生代谢产物木质素、黄酮、总酚和单宁含量均显著高于对照组(P < 0.05)。防御蛋白苯丙氨酸解氨酶(PAL)、多酚氧化酶(PPO)、胰蛋白酶抑制剂(TI)和胰凝乳蛋白酶抑制剂(CI)活性均显著高于对照组(P < 0.05)。
      结论   GM和GI能促进银中杨物质代谢,叶片内营养元素N、P和可溶性蛋白含量升高,可溶性糖含量降低,改变叶片品质,改善其耐受性;增强叶部化学防御能力,次生代谢产物含量和防御蛋白活性增加,改变银中杨对叶部害虫的抗性。因此,丛枝菌根真菌最终能否增强银中杨的抗虫性还有待进一步生物测定试验继续研究。
    Abstract:
      Objective   This study aims to investigate the effects of two arbuscular mycorrhizal fungi, Glomus mosseae (GM) and Glomus intraradices (GI) on the metabolism and chemical defense of Populus alba × P. berolinensis leaves.
      Method   In this study, each poplar seedling cut was planted into a pot filled with 1.3 kg sterilized soil mixed with 20 g fungal substrate containing 15 spore/g of either GM or GI. The contents of N, P elements, nutrients and secondary metabolites, as well as the activity of defense proteins in leaves of the poplar seedlings were analyzed on the 90th day after the planting when the fungal infection rate reached the peak.
      Result   The contents of N, P elements and soluble proteins in the poplar leaves from the GM or GI treatment group were significantly higher than those from the control group (P < 0.05), whereas the soluble sugar content was significantly lower (P < 0.05). There were no significant differences in starch contents between the GM or GI treatment group and the control group (P > 0.05). The contents of secondary metabolites, lignin, flavonoids, total phenols and tannins were significantly higher in the GM or GI treatment group than those in the control group (P < 0.05). The activities of defense proteins, phenylalanine ammonia-lyase (PAL), polyphenol oxidase (PPO), trypsin inhibitor (TI) and chymotrypsin inhibitor (CI) were all significantly higher in the treatment groups than those in the control group (P < 0.05).
      Conclusion   The above results indicate that GM and GI might promote the metabolism of Populus alba × P. berolinensis leaves, including increase in the contents of N, P elements and soluble proteins and decrease in the content of soluble sugars, resulting in potential changes in leaf quality, and improvement of leaf tolerance. GM or GI infestation seems to increase the chemical defense ability of the poplar leaves, such as the increase of secondary metabolite contents and activity of defense proteins, thus might affect the resistance of Populus alba × P. berolinensis leaves to pests. However, further research is surely needed to determine whether these two arbuscular mycorrhizal fungi can significantly enhance the resistance of Populus alba × P. berolinensis to pest insects.
  • 丛枝菌根真菌(arbuscular mycorrhiza fungi,AMF),作为一种与植物关系最为密切的微生物,广泛分布于地球,能与陆地上大约90%的植物产生共生关系[1]。AMF能够为植物提供一个良好的根际环境,并通过增进营养吸收、提高光合效率等多种途径,改善植物的生长发育,促进植物与生态系统的C、N、P循环,提高植物生长量。Wu等[2]研究表明,AMF定殖欧美杨107(Populus × euramericana ‘Neva’)可以显著提高其氮素吸收及光合作用。

    植物可通过提高次生代谢产物含量、防御蛋白活性或者改变体内营养成分含量等一系列生理生化反应提高其化学防御能力,抵御植食性昆虫的危害[3]。植物次生代谢产物是非营养物质,能够增加昆虫的代谢负担、降低昆虫对食物的利用效率,进而影响其正常生长发育[4-5]。防御蛋白包括防御酶和蛋白酶抑制剂。防御酶是植物由初生代谢转为次生代谢途径中的关键酶,对降低植物的营养价值和毒害植食昆虫方面具有重要意义[6],主要包括苯丙氨酸解氨酶(PAL)和多酚氧化酶(PPO);蛋白酶抑制剂能削弱昆虫肠道内蛋白酶活性或阻断消化酶对食物中蛋白质的消化利用,还能诱导昆虫消化酶的过度分泌,造成昆虫营养不良,进而影响昆虫的生长[7]。尽管,植物体内营养物质的含量是衡量植物抗虫性的另一种生理指标[8],但是,营养物质与次生代谢产物和防御蛋白对抗虫性的调控机制并不一致,因为营养物质含量与抗虫性并不一定呈线性相关,主要取决于含碳、氮营养物质的比例[9-10]。大量研究表明,AMF作为一种生物制剂在与植物形成共生体后,会与植物进行复杂的信号分子交换并产生诱导因子,诱导激发植物的化学防御[11],在一定程度上诱导激发植物的抗病性、抗虫性或抗应激能力,间接提高植物对不利环境条件的适应性[12]。例如:异形根孢囊霉(Rhizophagus irregularis)定殖车前草(Plantago lanceolata)后,能显著提高其叶片中次生代谢产物梓醇的含量,使甜菜夜蛾(Spodoptera exigua)的死亡率显著升高[13]。Nishida等[14]研究显示,将日本百脉根(Lotus japonicus)分别接种根内球囊霉(Glomus intraradices,GI)、幼套近明球囊霉(Glomus etunicatum,GE)、聚丛球囊霉(Glomus aggregatum,GA)、稍长无梗囊霉(Acaulospora longula)、球状巨孢囊霉(Gigaspora margarita)或玫瑰红巨孢囊霉(Gigaspora rosea)6种AMF可以显著提高其叶片内酚类的含量,使二斑叶螨(Tetranychus urticae)的取食和产卵受到显著抑制。GI能通过茉莉酸途径诱导黄瓜(Cucumis sativus)产生防御性物质葫芦素C,使甜菜夜蛾的取食量显著低于对照[15]

    目前,关于AMF的研究,多以豆科植物或农业经济型植物的抗逆性为主,其对林木抗虫性影响的研究较少。本研究以银中杨(Populus alba × P. berolinensis)为对象,对其接种摩西球囊霉(Glomus mosseae,GM)或GI,在侵染率达到最高时,测定银中杨叶片N和P元素、营养物质、次生代谢产物含量和防御蛋白活性,分析AMF对银中杨物质代谢及化学防御的影响,为利用AMF诱导增强林木化学防御及提高林木抗虫性提供理论依据。

    供试植物:1年生银中杨扦插苗。扦插前一周对插穗进行沙埋,并定期浇水。将插穗取出后,用500 mg/L生根粉溶液浸泡12 h后扦插。

    供试菌剂:摩西球囊霉(GM)和根内球囊霉(GI)由甘肃农科院提供,通过宿主玉米和三叶草扩繁完成,菌剂中包含孢子、菌丝、根段和沙子,其中孢子含量15 个/g。

    土壤:草炭土∶蛭石∶沙子 = 3∶1∶1,混合后在121 ℃下高压灭菌2 h。

    试验前,将高11.5 cm的32孔塑料穴盘和容量为1 L的花盆用0.3%KMnO4溶液浸泡2 h进行消毒处理。在穴盘内装入灭菌后的土壤。将浸泡后的插穗扦插于穴盘,每穴1株,定期浇水,一个月后移栽至花盆。将花盆分为3组,在AMF处理组的每个花盆中,分别装入1.3 kg灭菌土壤与20 g GM或GI的均匀混合物,对照组只装入1.3 kg灭菌土壤,不加菌剂。每盆移栽1株扦插苗,每组150株,3组共450株。移栽后,在东北林业大学林木遗传育种苗圃温室进行培养,并进行定期浇水除草。

    根据Phillips等[16]方法修改。在移植后30、60、90和100 d,从每组随机各选取5株样树,检测AMF侵染率。将样树根部须根剪下,洗净,剪成1 ~ 2 cm长的小段,先加入10%KOH,放入90 ℃水浴锅加热30 min使根透明(溶液变黄要及时更换,直至溶液不再变黄)。根透明后用蒸馏水清洗3 ~ 5次,再加入20%过氧化氢使根软化,静置10 ~ 15 min,取出根用蒸馏水洗净;然后加入2%稀盐酸酸化5 min,用蒸馏水洗净,接着加入曲利苯蓝溶液(乳酸(mL)∶甘油(mL)∶曲利苯蓝(g) = 100∶100∶0.2)进行染色30 min。染色完成后用蒸馏水清洗两次,最后放入乳酸−甘油(1∶1)中脱色12 h,取出后置于乳酸甘油溶液(乳酸∶甘油∶水 = 1∶1∶1)中,4 ℃保存,蒸馏水清洗后取样镜检。通过网格线相交法[17]计算AMF侵染率,以根段上出现孢子或丛枝为标准。在每次取样时,每个样树至少观察50小段根样,每个处理共观察250小段根样。在侵染率达到最高时,取样测定叶片内营养元素、营养物质和次生代谢产物含量,以及防御蛋白活性。

    每个处理组随机选取9株样树,每3株一个重复,测3个重复。每株选取第3、第4片子叶进行测定,下同。N元素采用奈氏比色法,测定P元素采用钼锑抗比色法[18]

    可溶性蛋白质含量采用考马斯亮蓝法[19]测定,可溶性糖和淀粉含量采用蒽酮比色法[20]测定。

    PAL采用苯丙氨酸比色法[20],PPO采用邻苯二酚比色法[21]。TI和CI依据孟昭军[20]和段文昌等[22]方法测定。总酚采用福林酚比色法[23]测定,单宁依据范旭东[24]的方法测定,黄酮含量依据Jia等[25]的方法测定,木质素含量依据任琴等[26]的方法测定。

    使用Excel2010统计数据的平均值和标准误差。使用SPSS22.0 one-way ANOVA进行差异显著性方差分析,多重比较采用LSD法在0.05水平下检验各组之间的差异显著性。

    在处理30、60、90、100 d后GM和GI侵染率随时间变化如图1所示。随着处理时间的延长,侵染率呈显著升高,且GM和GI处理组之间差异显著(P < 0.05)。在30 d时,GM侵染率为10.8%,GI为15.6%;60 d时,GM为20.1%,GI为30.5%;在90 d时侵染率达到最大值,GM为45.6%,GI为61.7%;在100 d时侵染率降低,GM为43.7%,GI为60.8%。CK组没有检测到侵染。

    图  1  GM、GI处理组侵染率随时间变化的趋势
    CK.对照;GM.摩西球囊霉;GI.根内球囊霉。数据均为平均值 ± 标准差(n = 3);不同小写字母表示处理组与对照组之间差异显著(P < 0.05)。下同。CK, control; GM, Glomus mosseae; GI, Glomus intraradices. The data annotation in the picture is average value ± SD (n = 3); different lowercase letters mean significant differences between treatment group and control group (P < 0.05). The same below.
    Figure  1.  Trend of infection rate of GM and GI with time

    银中杨接种GM、GI 90 d后叶片内N、P及营养物质含量如图2所示。GM和GI处理组叶片N、P元素含量显著高于CK组(P < 0.05)。P元素含量,GI组显著高于GM组(P < 0.05);N元素含量,GM与GI组差异不显著(如图2A)。可溶性蛋白质含量,GM和GI处理组显著高于CK组(P < 0.05),GM和GI组间差异不显著;可溶性糖含量,GM和GI处理组显著低于CK组(P < 0.05),GM与GI处理组差异不显著;淀粉含量3组间差异均不显著(如图2B)。

    图  2  GM、GI处理组叶片中营养元素(N、P)和营养物质的含量
    Figure  2.  Contents of nutrient elements (N, P) and nutrients in leaves with GM or GI treatment

    接种GM、GI 90 d后,银中杨叶片内次生代谢产物含量如图3所示。总酚、黄酮、木质素和单宁含量,GM和GI处理组均显著高于CK组(P < 0.05)。在2个处理组间,木质素和单宁差异显著(P < 0.05),总酚和黄酮差异不显著(P > 0.05)。

    图  3  GM和GI处理组叶片中总酚、黄酮、木质素和单宁的含量
    Figure  3.  Contents of total phenols, flavonoids, lignin and tannins in leaves of GM or GI treatments

    接种GM、GI 90 d后,银中杨叶片内防御蛋白苯丙氨酸解氨酶(PAL)、多酚氧化酶(PPO)、胰凝乳蛋白酶抑制剂(CI)和胰蛋白酶抑制剂(TI)的活性均显著大于对照(见图4)。在2个处理组间,PAL活性差异显著(见图4A),PPO、CI和TI活性差异不显著(见图4BCD)。

    图  4  GM和GI处理组叶片中PAL、PPO、CI和TI的活性
    Figure  4.  Activities of PAL, PPO, CI and TI in leaves of GM or GI treatments

    本研究表明,外源接种AMF(GM或GI)可以显著提高银中杨的物质代谢和化学防御,具体表现为叶片内N、P、可溶性蛋白质含量增加,可溶性糖含量减少,次生代谢产物含量增加,防御蛋白活性增强。

    研究报道,GI可以改善欧美杨107对N、P的吸收和利用,其中N吸收与蛋白质的含量变化有关[2]。Tao等[27]研究显示,用不同浓度的GM、GI和GE混合菌种处理马利筋属(Asclepias)6种植株,能显著提高其根系和叶片内的N、P含量;随着P浓度的增加,马利筋生长速率显著加快,因而对黑脉金斑蝶(Danaus plexippus)危害的耐受性显著提高;同时N含量的增加使马利筋叶片的乳胶(主要防御物质)渗出量显著提高。用GM、GI和地表球囊霉(Glomus versiforme,GV)等3种AMF分别处理黄瓜,均可以在不同程度上显著提高其对土壤基质中N、P元素的吸收能力[28]。本研究结果进一步证实了这一点。N、P在植物生长过程中起到重要的生理作用,不仅可以提高植物叶片的营养水平,而且参与氮代谢和磷代谢等生理进程,进而提高植物的耐受性[29]。本试验显示,AMF处理组可溶性糖含量显著低于对照,淀粉含量差异不显著,其原因可能是植物碳素营养物质与AMF消耗植物糖类的水平有关[30]。Bonfante和Genre研究报道,在植物生长早期AMF会起到抑制作用,可能是由于真菌的生长需要寄主植物提供糖类[31]。相关研究[32]表明,接种GE和GM促进了柑橘幼苗叶片可溶性蛋白等的积累,提高了防御蛋白的活性,进而增强植物对干旱的适应能力。在我们的研究中,可溶性糖含量降低即碳素含量降低,氮素含量升高,碳氮比降低。据报道,植物体内的碳氮比是研究抗虫性的重要指标,碳氮比的高低对不同植物的抗虫性影响不同[33-34]。Gherlenda等[35]研究发现,高浓度的CO2条件下,细叶桉(Eucalyptus tereticornis)的C/N升高,对桉树龟金花虫(Paropsis atomaria)幼虫体重显著降低,血淋巴蛋白含量显著降低。马艳等[36]研究表明,在棉铃虫(Helicoverpa armigera)幼虫取食C/N低的棉花(Gossypium spp.)后,成虫产卵量增加,雄性成虫寿命显著增加。因此,本研究中银中杨碳氮比与抗虫性的关系有待我们进一步生物测定。

    次生代谢产物含量和防御蛋白活性是衡量植物抗虫性的生理指标。分月扇舟蛾(Clostera anastomosis)危害69杨(P. deltoides)和895杨(P. delotides × P.euramericana cv.‘Nanlin895’)后,诱导杨树叶片内单宁、黄酮和总酚含量显著升高,延长分月扇舟蛾的幼虫期和蛹期,显著降低其化蛹率、蛹重、羽化率和产卵量 [37]。Jiang等[38]在研究茉莉酸诱导下长白落叶松(Larix olgensis)的抗虫机制时发现,针叶内防御蛋白酶和蛋白酶抑制剂活性的增加是抑制舞毒蛾(Lymantria dispar)生长发育的主要原因之一。本研究中,在接种AMF的银中杨叶片内,次生代谢产物总酚、黄酮、木质素和单宁的含量及防御蛋白PAL、PPO、CI和TI活性均显著高于对照,进一步说明AMF诱导可以提高银中杨的化学防御。相似的研究发现,接种GI的黑吉豆(Vigna mungo)叶片中积累大量的防御代谢产物,如酚类,木质素以及防御蛋白,大大降低了斜纹夜蛾(Spodoptera litura)的取食率[39]。接种不同浓度的GM、GI和GE混合菌种能够显著提高马利筋叶片内的次生代谢产物卡烯内酯含量,使黑脉金斑蝶的生长发育和繁殖(体重、取食量和产卵量)受到抑制[27]。本试验中AMF诱导银中杨化学防御的改变是否会增强银中杨的抗虫性,有待进一步生物测定来验证。

    不同AMF对寄主植物的适应性不同[40],即不同的AMF和植物共生对植食昆虫的抗性有不同的影响。在本研究中,GI对银中杨的侵染率显著高于GM,说明GI对银中杨的适应性更强。接种GI的银中杨生长发育显著高于接种GM(另文发表),GI组P含量显著高于GM组,但GM组木质素、单宁含量和PAL活性显著高于GI组。因此,在实践中,可根据生产目的选取AMF菌种。

    本试验结果说明AMF能够促进银中杨的物质代谢,增强树势,改善其耐受性;提高银中杨的化学防御,改变其抗虫性。但对抗虫性是否具有积极地意义,有待我们进一步的生物测定结果来验证,从而为之后关于AMF的研究奠定理论基础。

  • 图  1   GM、GI处理组侵染率随时间变化的趋势

    CK.对照;GM.摩西球囊霉;GI.根内球囊霉。数据均为平均值 ± 标准差(n = 3);不同小写字母表示处理组与对照组之间差异显著(P < 0.05)。下同。CK, control; GM, Glomus mosseae; GI, Glomus intraradices. The data annotation in the picture is average value ± SD (n = 3); different lowercase letters mean significant differences between treatment group and control group (P < 0.05). The same below.

    Figure  1.   Trend of infection rate of GM and GI with time

    图  2   GM、GI处理组叶片中营养元素(N、P)和营养物质的含量

    Figure  2.   Contents of nutrient elements (N, P) and nutrients in leaves with GM or GI treatment

    图  3   GM和GI处理组叶片中总酚、黄酮、木质素和单宁的含量

    Figure  3.   Contents of total phenols, flavonoids, lignin and tannins in leaves of GM or GI treatments

    图  4   GM和GI处理组叶片中PAL、PPO、CI和TI的活性

    Figure  4.   Activities of PAL, PPO, CI and TI in leaves of GM or GI treatments

  • [1]

    Rosendahl S. Communities, populations and individuals of arbuscular mycorrhizal fungi[J]. New Phytologist, 2008, 178(2): 253−266.

    [2]

    Wu F, Zhang H, Fang F, et al. Arbuscular mycorrhizal fungi alter nitrogen allocation in the leaves of Populus × canadensis ‘Neva’[J]. Plant and Soil, 2017, 421: 477−491. doi: 10.1007/s11104-017-3461-0

    [3]

    Hoffman M J, Stafford G I, Makunga N P. The role of alkaloids in chemical defence in chemical defence in Clivia miniata (Amaryllidaceae) against herbivory by Brithys crini[J]. South African Journal of Botany, 2018, 115: 319−320.

    [4]

    Dučaiová Z, Sajko M, Mihaličová S, et al. Dynamics of accumulation of coumarin-related compounds in leaves of Matricaria chamomilla after methyl jasmonate elicitation[J]. Plant Growth Regulation, 2015, 79(1): 81−94.

    [5]

    Shahabinejad M, Shojaaddini M, Maserti B, et al. Exogenous application of methyl jasmonate and salicylic acid increases antioxidant activity in the leaves of pistachio (Pistacia vera L. cv. Fandoughi) trees and reduces the performance of the phloem-feeding psyllid Agonoscena pistaciae[J]. Arthropod-Plant Interactions, 2014, 8(6): 525−530.

    [6]

    Heredia J B, Cisneros-Zevallos L. The effect of exogenous ethylene and methyl jasmonate on pal activity, phenolic profiles and antioxidant capacity of carrots (Daucus carota) under different wounding intensities[J]. Postharvest Biology & Technology, 2009, 51(2): 242−249.

    [7]

    Medel V, Palma R, Mercado D, et al. The effect of protease inhibitors on digestive proteolytic activity in the raspberry weevil, Aegorhinus superciliosus (Guérin) (Coleoptera: Curculionidae)[J]. Neotropical Entomology, 2015, 44(1): 77−83. doi: 10.1007/s13744-014-0250-9

    [8] 姜礅. 重金属胁迫下银中杨抗虫性及食叶害虫舞毒蛾解毒机制研究[D]. 哈尔滨: 东北林业大学, 2019.

    Jiang D. Study on the insect resistance of Populus alba × P. berolinensis and the detoxification mechanism of defoliator, Lymantria dispar under heavy metal stress[D]. Harbin: Northeast Forestry University, 2019.

    [9]

    Mehrkhou F, Mahmoodi L, Mouavi M. Nutritional indices parameters of large white butterfly Pieris brassicae (Lepidoptera: Pieridae) on different cabbage crops[J]. Archives of Phytopathology and Plant Protection, 2013, 8(25): 3294−3298.

    [10] 王小菲, 高文强, 刘建锋, 等. 植物防御策略及其环境驱动机制[J]. 生态学杂志, 2015, 34(12):3542−3552.

    Wang X F, Gao W Q, Liu J F, et al. Plant defense strategy and its environmental driving mechanism[J]. Journal of Ecology, 2015, 34(12): 3542−3552.

    [11]

    Oliveira J S F D, Xavier L P, Lins A, et al. Effects of inoculation by arbuscular mycorrhizal fungi on the composition of the essential oil, plant growth, and lipoxygenase activity of Piper aduncum L[J/OL]. AMB Express, 2019, 9(1): 29 [2020−02−11]. https://link.springer.com/article/10.1186/s13568-019-0756-y.

    [12]

    Hill E M, Robinson L A, Abdul-Sada A, et al. Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes[J]. Journal of Chemical Ecology, 2018, 44(2): 198−208. doi: 10.1007/s10886-017-0921-1

    [13]

    Wang M G, Bezemer T M, Putten W H, et al. Effects of the timing of herbivory on plant defense induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status[J]. Journal of Chemical Ecology, 2015, 41(11): 1006−1017. doi: 10.1007/s10886-015-0644-0

    [14]

    Nishida T, Katayama N, Izumi N, et al. Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite[J]. Population Ecology, 2010, 52(4): 507−515. doi: 10.1007/s10144-010-0208-7

    [15]

    Barber N A. Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus[J]. Journal of Plant Ecology, 2013, 6(2): 171−176. doi: 10.1093/jpe/rts026

    [16]

    Phillips J M, Hayman D S. Improved procedures for clearing roots and staining parasitic and vesicular arbuscular fungi for rapid assessment of infection[J]. Transactions of the British Mycological Society, 1970, 55: 158−161. doi: 10.1016/S0007-1536(70)80110-3

    [17]

    Mcgonigle T P, Miller M H, Evans D G, et al. A new method which gives an objective measure of colonization of roots by vesicular: arbuscular mycorrhizal fungi[J]. New Phytologist, 1990, 115(3): 495−501.

    [18] 赵静. 土壤酸化对土壤有效养分、酶活性及黄金梨品质的影响[D]. 泰安: 山东农业大学, 2011.

    Zhao J. Effects of soil acidification on available soil nutrients, soil enzyme activities and characters of Whangkeumbae in pear orchards[D]. Taian: Shandong Agricultural University, 2011.

    [19]

    Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding[J]. Analytical Biochemistry, 1976, 72(1−2): 248−254. doi: 10.1016/0003-2697(76)90527-3

    [20] 孟昭军. 外源茉莉酸类化合物对两种落叶松的诱导抗虫性研究[D]. 哈尔滨: 东北林业大学, 2008.

    Meng Z J. Study on the induced resistance of two larch species treated with exogenous jasmonates to insects[D]. Harbin: Northeast Forestry University, 2008.

    [21] 王燕芳. 茉莉酸甲酯和水杨酸诱导棉花抗虫性的初步研究[D]. 阿拉尔: 塔里木大学, 2015.

    Wang Y F. A preliminary study on induced resistance against cotton insect by methyl jasmonate and salicylate[D]. Alaer: Tarim University, 2015.

    [22] 段文昌, 段立清, 李海平, 等. 外源茉莉酸及枸杞瘿螨危害诱导的枸杞防御反应[J]. 昆虫学报, 2012, 55(7):804−809.

    Duan W C, Duan L Q, Li H P, et al. Defense responses in wolfberry (Lycium barbarum) induced by exogenous jasmonic acid and gall mite Aceria pallida (Acari: Eriophyidae)[J]. Acta Entomologica Sinica, 2012, 55(7): 804−809.

    [23] 黄文烨. 山竹壳中果胶和酚类物质的提取纯化及理化性质研究[D]. 广州: 暨南大学, 2016.

    Huang W Y. Extraction and characterization of pectin and phenolics from Mangosteen rind[D]. Guangzhou: Jinan University, 2016.

    [24] 范旭东. 浙江千岛湖地区苦槠叶片昆虫取食状类型和取食强度研究[D]. 上海: 华东师范大学, 2008.

    Fan X D. Intensity and patterns of Castanopsis sclerophylla leaf eaten by insects at Qiandao Lake, Zhejiang[D]. Shanghai: East China Normal University, 2008.

    [25]

    Jia Z S, Tang M C, Wu J M. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals[J]. Food Chemistry, 1999, 64(4): 555−559. doi: 10.1016/S0308-8146(98)00102-2

    [26] 任琴, 胡永建, 李镇宇, 等. 受害马尾松木质素含量及其过氧化物酶活性[J]. 生态学报, 2007, 26(11):4895−4899. doi: 10.3321/j.issn:1000-0933.2007.11.060

    Ren Q, Hu Y J, Li Z Y, et al. Content variation of lignin and peroxidase activities from damaged Pinus massioniana[J]. Journal of Ecology, 2007, 26(11): 4895−4899. doi: 10.3321/j.issn:1000-0933.2007.11.060

    [27]

    Tao L, Ahmad A, de Roode J C, et al. Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms[J]. Journal of Ecology, 2016, 104(2): 561−571. doi: 10.1111/1365-2745.12535

    [28] 王倡宪, 秦岭, 冯固, 等. 三种丛枝菌根真菌对黄瓜幼苗生长的影响[J]. 农业环境科学学报, 2003, 22(3):301−303. doi: 10.3321/j.issn:1672-2043.2003.03.012

    Wang C X, Qin L, Feng G, et al. Effects of three arbuscular mycorrhizal fungi on growth of cucumber seedlings[J]. Journal of Agricultural Environmental Science, 2003, 22(3): 301−303. doi: 10.3321/j.issn:1672-2043.2003.03.012

    [29]

    Wang L, Pokharel S S, Chen F J. Arbuscular mycorrhizal fungi alter the food utilization, growth, development and reproduction of armyworm (Mythimna separata) fed on Bacillus thuringiensis maize[J/OL]. PeerJ, 2019: 7 [2020−01−23]. https://doi.org/10.7287/peerj.preprints.27643v1.

    [30] 邹碧莹, 张云翼. 丛枝菌根(AM)真菌对植物营养代谢的影响研究进展[J]. 现代农业科技, 2008(15):10−13. doi: 10.3969/j.issn.1007-5739.2008.15.003

    Zou B Y, Zhang Y Y. Research progress on the effect of arbuscular mycorrhizal (AM) fungi on plant nutrient metabolism[J]. Modern Agricultural Science and Technology, 2008(15): 10−13. doi: 10.3969/j.issn.1007-5739.2008.15.003

    [31]

    Bonfante P, Gnre A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis[J]. Nat Commun, 2010, 1: 1−11.

    [32] 张妮娜. 接种丛枝菌根真菌(AMF)对盆栽柑橘幼苗抗旱性的影响[D]. 重庆: 西南大学, 2018.

    Zhang N N. Influences of arbuscular mycorrhizal fungi(AMF)inoculation on drought resistance mechanism of the potted citrus plantlets[D]. Chongqing: Southwest University, 2018.

    [33]

    Moeser J, Vidal S. Response of larvae of invasive maize pest Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to carbon/nitrogen ratio and phytosterol content of European maize varieties[J]. Journal of Economic Entomology, 2004, 4: 1335.

    [34]

    Zhang X, Lu C H, Chen Y, et al. Relationship between leaf C/N ratio and insecticidal protein expression in Bt cotton as affected by high temperature and N rate[J]. Journal of Integrative Agriculture, 2014, 13(1): 82−88. doi: 10.1016/S2095-3119(13)60348-2

    [35]

    Gherlenda A N, Haigh A M, Moore B D, et al. Climate change, nutrition and immunity: effects of elevated CO2 and temperature on the immune function of an insect herbivore[J]. Journal of Insect Physiology, 2016, 85: 57−64.

    [36] 马艳, 夏敬源. 取食不同施氮量棉花对棉铃虫发育与繁殖的影响[J]. 中国棉花, 1997(1):14−15.

    Ma Y, Xia J Y. Effects of feeding on Gossypium spp. with different nitrogen application rates on the development and reproduction of Helicoverpa armigera[J]. Chinese Cotton, 1997(1): 14−15.

    [37] 钱为. 分月扇舟蛾诱导杨树防御反应的研究[D]. 南京: 南京林业大学, 2010.

    Qian W. Defense responses of poplar induced by Clostera anastomosis [D]. Nanjing: Nanjing Forestry University, 2010.

    [38]

    Jiang D, Yan S C. MeJA is more effective than JA in inducing defense responses in Larix olgensis[J]. Arthropod Plant Interactions, 2018, 12(1): 49−56. doi: 10.1007/s11829-017-9551-3

    [39]

    Selvaraj A, Thangavel K, Uthandi S, et al. Arbuscular mycorrhizal fungi (Glomus intraradices) and diazotrophic bacterium (Rhizobium BMBS) primed defense in blackgram against herbivorous insect (Spodoptera litura) infestation[J]. Microbiological Research, 2020, 231: 126355. doi: 10.1016/j.micres.2019.126355

    [40] 周志强, 胡燕妮, 彭英丽, 等. 3种丛枝菌根真菌对不同种源黄檗幼苗的影响[J]. 植物研究, 2015, 35(1):92−100. doi: 10.7525/j.issn.1673-5102.2015.01.015

    Zhou Z Q, Hu Y N, Peng Y L, et al. Effects of three arbuscular mycorrhizas on different provenances of amur cork seedlings[J]. Bulletin of Botanical Research, 2015, 35(1): 92−100. doi: 10.7525/j.issn.1673-5102.2015.01.015

  • 期刊类型引用(5)

    1. 李娜娜,张冬冬,李鑫,刘小东,李海江,李宜璇. 放牧强度对草地丛枝菌根真菌多样性的影响. 现代畜牧科技. 2025(02): 85-89 . 百度学术
    2. 王琪,马宇佳,赵佳齐,严善春. 从枝菌根真菌对青山杨生长及其物质代谢的影响. 林业科技. 2024(05): 36-42 . 百度学术
    3. 邓薪岐,王谢,严晓军,柯佳君,杨叶,李艳,徐丹萍,卓志航,严贤春. 转录组和代谢组在林木真菌病害防御反应中的应用研究进展. 世界林业研究. 2022(04): 27-32 . 百度学术
    4. 方静,武帅,姜礅,谭明涛,赵佳齐,孟昭军,严善春. 丛枝菌根真菌定殖银中杨对舞毒蛾幼虫食物利用及适应性的影响. 菌物学报. 2022(12): 2016-2024 . 百度学术
    5. 张守攻. 林木重要性状形成的分子基础研究进展. 中国农业科技导报. 2022(12): 48-58 . 百度学术

    其他类型引用(8)

图(4)
计量
  • 文章访问数:  1217
  • HTML全文浏览量:  400
  • PDF下载量:  62
  • 被引次数: 13
出版历程
  • 收稿日期:  2020-06-04
  • 修回日期:  2020-09-21
  • 网络出版日期:  2021-04-20
  • 发布日期:  2021-05-26

目录

/

返回文章
返回