摘要
目的
明确不同根腐病发病率青稞农田根际土壤真菌多样性特征及差异,为其精准、高效防控提供理论依据。
方法
采集青稞农田内健康及根腐病发病率为5%、10%、15%、20%的根际土壤样品,对真菌18S rRNA基因进行扩增,采用Illumina-MiSeq平台进行高通量测序。数据经质控、分类及注释后,从不同角度及分类水平对物种多样性进行分析。
结果
健康与发病率为5%的样本真菌多样性最为丰富,发病率为10%的样本最低。共现网络分析发现,健康与发病率为5%的样本内物种间相互作用更为复杂。发病率越高,子囊菌门(Ascomycota)相对丰度越低,而担子菌门(Basidiomycota)、球囊菌门(Glomeromycota)相对丰度越高。优势真菌集中于伞菌纲(Agaricomycetes)、壶菌纲(Chytridiomycetes)、粪壳菌纲(Sordariomycetes)等。在各样本中,平均相对丰度较高的菌群分布差异更为显著。健康样本中散囊菌目(Eurotiales)相对丰度最高,球囊霉目(Glomerales)相对丰度最低;发病样本中则相反。裸囊菌科(Arthrodermataceae)显著富集于健康样本,粪壳菌科(Sordariaceae)、粘毛菌科(Myxotrichaceae)、油壶菌科(Olpidiaceae)分别显著富集于发病率为10%、15%、20%的样本。在属、种水平上,健康与发病率为5%的样本优势真菌群落构成相近,发病率为10%、15%、20%的样本更为相近。FUNGuild功能预测分析发现,发病率越高,植物病原菌相对丰度越低,而土壤腐生菌相对丰度越高。
结论
青稞根腐病的发生蔓延与根际土壤真菌群落结构失衡密切相关,青稞根腐病的精准防控应考虑调控并维持根际优势真菌类群的丰度平衡。
根际土壤微生物是植物根际土壤生态中最为活跃的组分,也是“植物-土壤-微生物”互作过程中物质运输、能量流动及信息交换的关键枢纽,其多样性及群落结构变化与植物和土壤健康动态密切相
青稞是禾本科大麦属一年生粮饲兼用型作物,具有营养价值丰富、耐寒、耐旱、应用范围广等优良特性,是我国青藏高原地区的主要优势作物之一,被誉为“高原之宝
因此,本研究以甘南藏族自治州临潭县健康及根腐病发病率为5%、10%、15%、20%的成株期青稞根际土壤为研究对象,通过高通量测序技术对真菌18S rRNA基因进行扩增和测序,分析并明确不同根腐病发病率青稞农田根际土壤真菌多样性特征及差异,探讨其根际土壤中不同功能类群真菌的分布特点,发掘其中潜在的病原菌和有益真菌,阐明不同发病率农田内根际土壤真菌群落的构建机制,以及根腐病发生和蔓延的微生态机制,以期为青稞根腐病的精准、高效防控奠定基础。
1 材料与方法
1.1 研究区概况
研究区位于甘肃省甘南藏族自治州临潭县,地处青藏高原东北边缘,103°10′E-103°52′E,34°30′N-35°05′N,平均海拔约2 767 m,年均气温4.6 ℃,降水量约580 mm,无霜期约119 d。区域内青稞种植面积在农作物种植总面积中排名第二,前期调查发现区域内青稞成株期根腐病发病率为0-20
1.2 土壤样品采集与预处理
采用五点取样
发病率=(根腐病发病面积/地块总面积)×100%
(1)
1.3 土壤DNA提取与PCR扩增、测序
采用试剂盒(Omega公司),并按照其说明书步骤提取土壤样品总DNA。采用1%琼脂糖凝胶电泳检测所提取DNA的浓度和纯度,检测合格后委托上海欧易生物医学科技有限公司采用引物817F (5′-TTAGCATGGAATAATRRAATAG GA-3′)和1196R (5′-TCTGGACCTGGTGAAGTT TCC-3′),对所提取DNA的18S rRNA基因进行PCR扩增,共进行2轮,第1轮扩增产物电泳检测合格后使用磁珠纯化,作为第2轮扩增模板,再次检测、纯化后利用Qubit荧光仪(ThermoFisher公司)进行Qubit定量。最后通过Illumina-MiSeq平台进行高通量测序,并将测序结果上传至NCBI的SRA数据库(https://www.ncbi.nlm.nih.gov/sra),获得BioProject登录号为PRJNA1224487。
1.4 测序数据质控
将测序原始图像数据经碱基识别后转化为原始双端序列(raw data),采用Trimmomatic v0.35软件,滑动窗口切除扫描质量低于20的滑窗及长度小于50 bp的序
1.5 物种信息分类与注释
使用Vsearch v2.4.2软件,将所得优质序列以97%相似度为最低阈值划分为不同的可操作分类单元(operational taxonomic units, OTUs
1.6 根际土壤真菌多样性
根据不同样品中OTUs丰度信息,采用R v4.3.2的UpSetR v1.4、VennDiagram v1.7.3包绘制Upset-Venn图。去掉不同样品中OTUs平均相对丰度低于0.01%、显示频次少于总样本量20%的OTUs,使用WGCNA v1.73包计算各样本中真菌共现网络指标,将所得结果导入Gephi v0.10绘制共现网络图,并根据各样本中真菌共现网络平均度信息采用ggplot2 v1.0.1包绘制柱状图。采用MicrobiotaProcess v1.14、ggplot2 v1.0.1、phyloseq v3.19包等计算α多样性并绘制箱线图。根据不同分类层级上各样本真菌群落注释信息及其相对丰度,通过GenesCloud平台(https://www.genescloud.cn)绘制交互彩带柱状图、Excel 2021绘制柱状图对门水平优势菌群进行可视化分析。纲、目水平上优势菌群多样性分布特点及差异通过fmsb、ggradar包和Excel 2021进行可视化分析。科水平上,通过ggplot2 v1.0.1、ComplexHeatmap v2.22包绘制环形热图,采用类平均法(average)进行层次聚类,并通过Excel 2021绘制柱状图比较各样本间主要优势菌科的分布特点及差异。属、种水平上均通过ggplot2 v1.0.1、ComplexHeatmap v2.22包绘制热图并进行聚类分析。通过OmicStudio tools (https://www.omicstudio.cn/tool)设置显著性水平过滤阈值为0.05、线性判别分析值(linear discriminant analysis score, LDA score)过滤阈值为3,进行线性判别分析效应大小(linear discriminant analysis effect size, LEfSe)分析,并绘制LDA值分布柱状图对各样本内显著富集生物标记物进行可视化。采用FUNGuild预测各样本内真菌功
2 结果与分析
2.1 不同根腐病发病率青稞根际土壤真菌OTU多样性及差异
OTU是扩增子测序结果中评估真菌种类数的重要指标,如

图1 不同根腐病发病率青稞农田土壤真菌OTU数量组成及差异
Figure 1 Composition and variation of fungal community OTU numbers in rhizosphere soil of naked barley with different root rot incidences. NCH: Healthy sample; NCD1: Sample with root rot incidence of 5%; NCD2: Sample with root rot incidence of 10%; NCD3: Sample with root rot incidence of 15%; NCD1: Sample with root rot incidence of 20%. The same as below.
不同根腐病发病率青稞农田土壤真菌OTUs结构特征及多样性各有差异(

图2 不同根腐病发病率青稞农田土壤真菌OTU结构特征及多样性
Figure 2 Structural characteristics and diversity of fungal community OTU in rhizosphere soil of naked barley with different root rot incidences. * in G represents significant differences at the P<0.05 level. A, B, C, D and E representatively performed the co-occurrence network of the OTUs in NCH, NCD1, NCD2, NCD3 and NCD4. D represents the degree in the co-occurrence network of different samples. E represents different α-diversity indexes of the OTUs in the samples.
2.2 不同分类水平下真菌多样性分布特点及差异
2.2.1 门水平
由各样本内不同真菌门相对丰度分布特点(

图3 门水平上不同根腐病发病率青稞农田土壤真菌多样性分布特点及差异
Figure 3 Characteristics and differences of fungal community diversity in rhizosphere soil of naked barley with different root rot incidences at the phylum level. Different lowercases above the bars represent significant differences at the P<0.05 level.
2.2.2 纲、目水平
在各样本中,除未培养(uncultured)及相对丰度较低的其他(others)纲真菌外,检测到伞菌纲、壶菌纲、地位未定纲(Incertae Sedis)、粪壳菌纲下真菌目分布最为丰富,数量分别为9、8、7、11个(

图4 纲水平及不同纲下真菌目的多样性分布特点及差异
Figure 4 Characteristics and differences of fungal community diversity at class level and within different orders.

图5 不同根腐病发病率青稞根际土壤中主要优势真菌目的差异性分布特点
Figure 5 Differential distribution characteristics of prominent fungal orders in rhizosphere soil of naked barley with different root rot incidences. Different lowercases below the bars represent significant differences at the P<0.05 level.
2.2.3 科水平
从各样本中共检测到135个真菌科,根据各科在不同样本内的相对丰度平均值,定义相对丰度排名前30的科为主要优势菌科,其平均相对丰度为0.06%-47.26%。聚类分析发现,自聚类树根结点处可划分为2个支(

图6 不同根腐病发病率青稞根际土壤中主要真菌科的差异性分布特点
Figure 6 Differential distribution characteristics of prominent fungal families in rhizosphere soil of naked barley with different root rot incidences. A represents the relative abundance of prominent fungal families in different samples and the clustering results among different fungal families. B, C, D, E, and F represent the relative abundance of Sordariaceae, Olpidiaceae, Myxotrichaceae, Arthrodermataceae, and Cystofilobasidiaceae in different samples, respectively. Different lowercases above the bars represent significant differences at the P<0.05 level.
在各样本中,粪壳菌科相对丰度为33.25%-58.53% (
2.2.4 属水平
从各样本中共检测到133个真菌属,根据各属在5个样本内的相对丰度平均值,定义相对丰度排名前16的属为青稞根际土壤中的主要优势菌属,其相对丰度平均值为0.20%-47.26% (

图7 不同根腐病发病率青稞根际土壤中主要优势真菌属的差异性分布特点
Figure 7 Differential distribution characteristics of prominent fungal genus in rhizosphere soil of naked barley with different root rot incidences.
2.2.5 种水平
从各样本中共检测到108个真菌种,除未分类种(unclassified)、未培养种(uncultured)外,根据各种在5个样本内的相对丰度平均值,将排名前10的种定义为青稞根际土壤的主要优势种,其相对丰度平均值为0.20%-47.26% (

图8 不同根腐病发病率青稞根际土壤中主要优势真菌种的差异性分布特点
Figure 8 Differential distribution characteristics of prominent fungal species in rhizosphere soil of naked barley with different root rot incidences.
2.3 不同根腐病发病率青稞根际土壤真菌主要差异物种分析
LEfSe分析发现,各样本中显著富集的真菌各有不同(

图9 不同根腐病发病率青稞根际土壤真菌群落内显著富集生物标记物
Figure 9 Significant enrichment biomarkers in fungal communities in rhizosphere soil of naked barley with different root rot incidences.
2.4 不同根腐病发病率青稞根际土壤真菌功能预测
各样本内真菌FUNGuild功能预测分析发现(

图10 不同根腐病发病率青稞根际土壤真菌FUNGuild功能预测
Figure 10 Functional prediction of fungi in rhizosphere soil of naked barley with different root rot incidences by FUNGuild. Different lowercases around the bubbles represent significant differences at the P<0.05 level.
3 讨论
根际是植物与微生物互作的核心区域,根际土壤真菌多样性是寄主植物根部健康状态的直接指示因子之
现有报道表明,青稞根腐病病原真菌均属于子囊菌门或担子菌
本研究通过LEfSe分析发现,不同根腐病发病率青稞根际土壤中显著富集的菌群均为各分类水平上的主要优势菌群,且不同发病率根际土壤中显著富集的真菌类群各有差异,表明青稞根际土壤中主要优势菌群是调控其根际土壤生态、影响其根腐病发生蔓延进程的关键核心因子。根腐病的发生蔓延伴随着这些关键核心因子的剧烈波动。然而,由于目前部分真菌类群的分类地位尚不明确、培养难度大、受环境影响复
4 结论
青稞根腐病的发生是其根际土壤生态更利于病原真菌生存繁殖的必然结果。在发病初期,青稞根际虽能招募并富集大量内生真菌、丛枝菌根菌等有益微生物类群以抵御病情恶化,但有益真菌与病原真菌的相互作用过程中也会刺激更多病原群体占据生态位。病原真菌以“量变”策略抗击有益真菌,占据优势地位,从而引发根际土壤生态的“质变”,伴随大量有益真菌及病原真菌的消亡,最终改变土壤生态的演化方向。不同根腐病发病率青稞农田根际土壤中主要优势真菌类群是调控土壤生态、影响根腐病发生蔓延的关键核心因子。积极关注并有效调理此类核心因子,避免其丰度剧烈波动,或可快速、有效地遏制青稞根腐病的发生蔓延进程。
作者贡献声明
许世洋:数据处理、论文撰写;李雪萍:实验设计、DNA提取、论文润色;漆永红:样品采集、保障实验条件;李建军:数据核查。
利益冲突
作者声明不存在任何可能会影响本文所报告工作的已知经济利益或个人关系。
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