沙冬青及其伴生植物深色有隔内生真菌物种多样性
孙茜, 薛子可, 解琳琳, 贺学礼*, 赵丽莉
河北大学生命科学学院, 河北保定 071002

* 通信作者Author for correspondence (E-mail:xuelh1256@aliyun.com)

摘要

2013年7月从内蒙古磴口, 宁夏银川、沙坡头和甘肃民勤采集沙蒿( Artemisia desertorum)、红花锦鸡儿( Caragana rosea)、白刺( Nitraria tangutorum)、柠条锦鸡儿( Caragana korshinskii)等4种沙冬青( Ammopiptanthus mongolicus)伴生植物的根系样品, 采用形态特征结合rDNA ITS序列分析进行真菌分类鉴定, 研究了深色有隔内生真菌(DSE)群落组成和物种多样性。从4种伴生植物根样中共分离鉴定7类DSE(即 Alternaria Curvularia Embellisia Phialocephala Phoma Podospora和Pleosporales), 其中 Alternaria Embellisia Curvularia Podospora为荒漠生态系统首次报道的DSE。同一样地伴生植物与沙冬青DSE群落组成差异明显, 不同样地沙冬青与伴生植物DSE物种多样性指数差异显著。结果表明, 自然条件下沙冬青DSE定殖率和物种数量, 特别是产孢种类和数量多于其伴生植物, 暗示DSE能够与沙冬青根系形成更好的共生关系, 增强沙冬青对极端荒漠环境的生态适应性。

关键词: 深色有隔内生真菌; 群落组成; 物种多样性; 沙冬青; 伴生植物
doi: 10.17521/cjpe.2016.0270
Diversity of dark septate endophyte in the roots of Ammopiptanthus mongolicus and its companion plants
SUN Qian, XUE Zi-Ke, XIE Lin-Lin, HE Xue-Li*, ZHAO Li-Li
College of Life Sciences, Hebei University, Baoding, Hebei 071002, China
Abstract

Aims Dark septate endophytes (DSE) extensively colonize in plant root tissues in different ecosystems. However, our understanding of the ecological significance of DSE in semiarid and arid lands is limited. The main objective of this study was to compare the community composition and species diversity of DSE in Ammopiptanthus mongolicusand its companion plants in desert habitats. Methods Healthy root samples of Ammopiptanthus mongolicus’s companion plants, Artemisia desertorum, Caragana rosea, Nitraria tangutorumand Caragana korshinskii,were collected separately from four main locations of Ammopiptanthus mongolicus plantation in Dengkou of Nei Mongol, Minqin of Gansu, Yinchuan and Shapotou of Ningxia in July 2013. Important findings A total of 103 strains belonging to seven species (i.e Alternaria, Curvularia, Embellisia, Phialocephala, Phoma, Podosporaand Pleosporales) of DSE were isolated from the four types of companion plants by means of morphological identification and molecular identification. Among the seven genera, Alternaria, Embellisia, Curvularia and Podospora are found for the first time in desert ecosystems. Ammopiptanthus mongolicusand its companion plants at the same site had significantly different community composition of DSE. Ammopiptanthus mongolicus and its companion plants at different sites had significantly different DSE diversity index. The colonization and species richness of DSE, especially the species and the quantity of spores were higher in roots of Ammopiptanthus mongolicusthan in its companion plants. This study supports the results that DSE can form a better symbiotic relationship with the roots of Ammopiptanthus mongolicusthan with its companion plants, and can enhance the ecological adaptability of Ammopiptanthus mongolicus to the extreme desert environment.

Key words: dark septate endophyte; community composition; species diversity; Ammopiptanthus mongolicus; companion plants

深色有隔内生真菌(DSE)泛指一群定居在植物根组织细胞内或细胞间隙的子囊菌和无性繁殖真菌, 其典型特征是细胞壁有黑色素沉淀, 能够形成深色有隔菌丝(Jumpponen, 2001; Grü nig et al., 2008)。已有研究表明, DSE具有广泛的宿主和生态分布特性, 广泛存在于沙漠(姜桥等, 2014)、干旱草原(闫姣等, 2014)和亚北极高山地区(Kauppinen et al., 2014)等不同生态环境中, 并在重金属矿区(Ban et al., 2012; Zhan et al., 2015)、盐胁迫地区(邓勋等, 2015)发挥着重要的生态修复作用。与丛枝菌根(AM)真菌仅能侵染宿主植物根皮层组织不同, DSE既可侵染宿主植物根皮层, 又能以薄壁菌丝侵染根维管组织(Muthukumar et al., 2006)。Scervino等(2009)的研究表明, DSE能够改变植物菌根状况, 调节根际不同共生关系, 并在一定程度上补偿自然条件下AM真菌定殖率低或共生前期对宿主植物营养物质消耗的问题(Mandyam & Jumpponen, 2008)。因此, 研究荒漠环境中DSE多样性和生态分布规律, 有助于充分理解土壤真菌共生体在荒漠生态系统中的功能和意义(Rudgers & Clay, 2007)。

荒漠生态系统中植物和微生物的生长和分布及其相互作用是荒漠生物学过程的重要部分, 揭示植物、微生物与环境之间的相互作用, 有助于我们深刻理解荒漠生态系统过程和植被演变规律; 而DSE作为荒漠化过程中非常重要的一类内生真菌, 能够连接地上生态系统和地下生态系统物质传输, 调节植物群落结构、植物多样性以及植物生态系统的生产力(Jumpponen, 2001; Porras-Alfaro et al., 2008; Li et al., 2015; 张娟等, 2015)。沙冬青(Ammopiptanthus mongolicus)是第三纪残遗种, 也是我国干旱荒漠区惟一超旱生常绿阔叶豆科灌木, 具有很强的抗逆性(杨期和等, 2004)。张淑容等(2013)和姜桥等(2014)研究发现, 荒漠植物根组织有较高的DSE定殖率。Li等(2015)研究了内蒙古地区沙冬青DSE和土壤因子的相关性, 并分离鉴定了Exophiala sp.、Phialophora sp.和Phialocephala sp. 3个DSE菌株; 陈严严等(2014)研究了甘肃和宁夏3个样地沙冬青DSE共生及分离培养特征, 共分离鉴定了10种DSE。在西北荒漠带, 同沙冬青相伴生长着一些生长年限较短的灌木和半灌木, 这些伴生植物与沙冬青既存在竞争抑制, 又协同进化, 与沙冬青共同发挥防风固沙的作用(孙茜等, 2015)。

本研究在前期对沙冬青及其伴生植物DSE定殖规律分析(孙茜等, 2015)的基础上, 分离培养定殖于根组织的DSE, 比较分析沙冬青及其伴生植物DSE群落结构和物种多样性的差异性, 为阐明沙冬青适应极端荒漠环境的机理提供依据。

1 材料和方法
1.1 样品采集

2013年7月于内蒙古磴口、甘肃民勤、宁夏银川和沙坡头, 选取以沙冬青为建群种的样地, 每个样地随机选取长势相似的沙冬青和一种伴生植物各4株, 其中磴口样地伴生植物为沙蒿(Artemisia desertorum), 银川样地为白刺(Nitraria tangutorum), 沙坡头样地为柠条锦鸡儿(Caragana korshinskii), 民勤样地为红花锦鸡儿(Caragana rosea), 每株植物间距大于100 m。除去土壤表层枯枝落叶层, 在距植株主干0-30 cm范围内挖土壤剖面, 采集0-50 cm土层土样和根系样品, 将样品编号装入塑料袋密封带回实验室。自然风干后, 过筛分离根样用于DSE分离培养。沙冬青伴生植物采样地及其生境情况见表1

表1 沙冬青伴生植物采样地及其生境 Table 1 Sampling site characteristics of companion plants of Ammopiptanthus mongolicus
1.2 深色有隔内生真菌菌株的分离培养及纯化

将根样用自来水清洗干净, 再用无菌水冲洗2次后用75%乙醇表面消毒5 min, 用无菌水漂洗2次, 再用10%次氯酸钠消毒2 min, 用无菌水漂洗3次后将根样切成1-2 cm的根段, 分散置于加有抗生素(陈严严等, 2014)(含50 mg· L-1氨苄青霉素和50 mg· L-1硫酸链霉素)的PDA培养基中, 每皿5-8个根段, 于27 ℃恒温培养箱中倒置培养。利用漂洗液检验法和组织印迹法检验表面消毒是否彻底。待菌丝长出后, 立即挑取形态不同的菌落尖端菌丝于新的加有抗生素(含50 mg· L-1氨苄青霉素和50 mg· L-1硫酸链霉素)的PDA平板上进行培养。

挑取少许初步分离得到的DSE菌落于装有玻璃珠的三角瓶内(内含40 mL无菌水), 并于150 r· min-1振荡培养12 h后, 取100 µ L于PDA培养基上, 用涂布棒均匀涂布, 置于27 ℃培养箱中黑暗培养, 每天观察并及时挑取纯菌落进一步培养。

1.3 深色有隔内生真菌菌株形态观察与分子鉴定

用直径6 mm的打孔器挑取纯化菌株接种到直径9 cm的PDA平板上27 ℃倒置培养, 每2-3天观察并记录菌落表面形态、大小、颜色、质地、生长速率等形态特征。一段时间后, 在菌落边缘将盖玻片1/3以45° 插入培养基内继续培养, 在BS53显微镜(Olympus, Tokyo, Japan)下观察菌丝体、产孢结构、孢子形态与颜色等特征, 进行分类鉴定。

选用核糖体内转录间隔区(ITS)基因序列对不产孢菌株进行分子鉴定(Yadav et al., 2016)。每个菌种选择2-5株菌株, 在PDA平板上27 ℃培养14天后, 刮取新鲜菌丝10 mg, 置于Eppendorf管中, 杵棒研磨充分后, 采用真菌基因组DNA提取试剂盒(北京索莱宝科技有限公司提供)提取菌丝DNA, 将所得PCR原液进行测序。将本研究所测序列和参考序列用DNASTAR软件包的Megign程序进行排序, 用 Mega 4软件构建NJ树。结合菌株形态特征确定菌株分类地位(Yu et al., 2013)。

1.4 深色有隔内生真菌多样性测度

定殖率(%) = (定殖根段数/被镜检根段总数) × 100%

分离率(IR%) = (分离DSE菌株数/分离总根段数) × 100%

分离频率(IF%)或相对频率(RF%) = (某种真菌菌株数/分离所得总菌株数) × 100%

Shannon-Wiener多样性指数: $H=-\sum\limits_{i=1}^{s}{{{P}_{i}}}\ {{P}_{i}}$

Pielou均匀度指数: J = H/lnS, S是样地物种数目

Simpson优势度: $D = 1-\sum\limits_{i=1}^{s}{P_{i}^{2}}$。式中Pi = Ni/N即第i种真菌菌株数占样地分离所得总菌株数N的比例。

1.5 数据处理

采用SPSS 19.0统计软件对试验数据进行方差分析。

2 结果和分析
2.1 伴生植物深色有隔内生真菌分离数量

在磴口、民勤、银川和沙坡头4个样地, 沙冬青伴生植物DSE平均总定殖率分别为42.35%、31.28%、43.15%和29.39%。共分离DSE 103株, 其中, 磴口49株, 银川26株, 民勤11株, 沙坡头17株。各样地DSE菌株分离率各不相同(表2), 其中, 磴口样地最高, 为12.37%, 民勤样地最低, 为3.83%, 样地间DSE分离率表现为磴口> 银川> 沙坡头> 民勤。磴口样地优势菌种为DK-0-10, 共23株, 相对频率22.33%; 民勤只有MQ-1和MQ-4, 分别为6株和5株; 银川样地优势菌种为YC-2-1, 共15株, 相对频率为14.56%。

表2 伴生植物深色有隔内生真菌分离率 Table 2 Isolation rate of dark septate endophyte in the companion plants of Ammopiptanthus mongolicus
2.2 伴生植物深色有隔内生真菌群落组成

本研究分离的DSE纯培养菌落颜色以灰色、褐色、黑色为主, 形状呈圆形或近圆形, 表面平整或隆起, 常被覆绒毛或絮状绒毛, 菌丝有隔, 颜色从浅灰、褐色到深褐色不等, 部分DSE菌株产孢, 孢子多为短柱、棒状或球形, 颜色从灰色到灰黑色或褐色。将不产孢菌株置于10 ℃低温培养箱内诱导产孢, 仅两类型菌株产孢(图1, 图2)。

图1 产孢深色有隔内生真菌形态特征。A, E, DK-1. B, F, MQ-4. C, G, YC-2-1. D, H, SPT-1。Fig. 1 The morphological characteristics of sporulating dark septate endophyte. A, E, DK-1. B, F, MQ-4. C, G, YC-2-1. D, H, SPT-1.

图2 不产孢深色有隔内生真菌形态特征。A, F, DK-0-10. B, G, DK-4. C, H, MQ-1. D, I, YC-2-1. E, J, YC-2-3。Fig. 2 The morphological characteristics of sterile dark septate endophyte. A, F, DK-0-10. B, G, DK-4. C, H, MQ-1. D, I, YC-2-1. E, J, YC-2-3.

将不同菌株PCR产物测序与GenBank数据库中真菌序列进行比对分析, 其序列相似性为97%-100%。结合形态学特征, 确定伴生植物DSE群落包括Alternaria alternata (DK-0-10)、Alternariasp. (DK-4)、Alternaria japonica (YC-1)、Curvularia eragrostidis (MQ-4)、Embellisiasp. (YC-2-1)、Phialocephala fluminis (YC-3)、Phoma medicaginis (SPT-1)、Podospora anserina (DK-1)和Pleosporales sp. (MQ-1)等9种(表3; 图3)。

表3 序列对比结果 Table 3 The results of sequence Blast

图3 基于伴生植物深色有隔内生真菌ITS1-5.8S-ITS2序列构建的NJ树。DK-1、DK-0-10、DK-4是磴口样地伴生植物3种深色有隔内生真菌ITS1-5.8S-ITS2序列编号; MQ-1、MQ-4是民勤样地伴生植物两种深色有隔内生真菌ITS1-5.8S-ITS2序列编号; YC-1、YC-2-1、YC-3是银川样地伴生植物3种深色有隔内生真菌ITS1-5.8S-ITS2序列编号; SPT-1是沙坡头样地伴生植物深色有隔内生真菌ITS1-5.8S-ITS2序列编号。图中其他编号均为伴生植物深色有隔内生真菌在GenBank中Blast比对得到的ITS1-5.8S-ITS2序列的同源序列号。Fig. 3 Neighbor-Joining tree of dark septate endophyte in the roots of the companion plants of Ammopiptanthus mongolicus. DK-1, DK-0-10, DK-4 represent the sequence numbers of ITS1-5.8S-ITS2 form three kinds of dark septate endophyte in the roots of the companion plants of Ammopiptanthus mongolicus in Dengkou; MQ-1, MQ-4, represent the sequence numbers of ITS1-5.8S-ITS2 form two kinds of dark septate endophyte in the roots of the companion plants of Ammopiptanthus mongolicus in Minqin; YC-1, YC- 2-1, YC-3, represent the sequence numbers of ITS1-5.8S-ITS2 form three kinds of dark septate endophyte in the roots of the companion plants of Yinchuan; SPT-1 represents the sequence numbers of ITS1-5.8S-ITS2 form dark septate endophyte in the roots of the companion plants of Ammopiptanthus mongolicus in Shapotou. Other accession numbers in the figure are homologous sequence of dark septate endophyte in the roots of the companion plants of Ammopiptanthus mongolicus.obtained by Blast.

2.3 沙冬青与伴生植物深色有隔内生真菌多样性分析

2.3.1 深色有隔内生真菌分离频率

表4可知, 在各样地伴生植物中, 磴口样地沙蒿的优势种为Alternaria alternata, 民勤样地红花锦鸡儿仅有Curvularia eragrostidis和Pleosporales sp., 银川样地白刺优势种为Embellisia属菌株, 沙坡头柠条锦鸡儿仅有Phoma medicaginis。不同样地DSE分离频率差异显著, 其中磴口最高为17.19%; 民勤最低为3.86%, 样地间表现为: 磴口> 银川> 沙坡头> 民勤。各样地伴生植物均无共有种。

表4 沙冬青及其伴生植物深色有隔内生真菌分离频率 Table 4 Isolation frequency of dark septate endophyte in Ammopiptanthus mongolicusand its companion plants

在各样地沙冬青中, 磴口样地仅有Cladosporium属菌株, 民勤样地优势种为Paraphoma chrysanthemicola, 银川样地有Exophiala canceraePhoma sp., 沙坡头样地优势种为Exophiala属菌株。不同样地DSE分离频率差异显著, 其中民勤最高为28.42%; 磴口最低为5.61%, 样地间表现为: 民勤> 沙坡头> 银川> 磴口。仅Pleosporales目是沙冬青与其伴生植物在民勤样地共有菌株。

2.3.2 深色有隔内生真菌属水平多样性测度

表5可知, 样地间, 沙冬青及其伴生植物DSE种类组成存在差异, 从属水平看, 民勤的沙冬青DSE种类最多, 沙坡头次之, 而银川伴生植物白刺DSE种类比沙坡头柠条锦鸡儿多, Alternariasp.、Embellisiasp.、Phialocephalasp.、Podospora sp.、Curvulariasp.仅存在于伴生种中, 而Paraphoma sp.、Exophialasp.、Cladosporiumsp.、Phialophorasp. 仅存在于沙冬青中, Pleosporales sp.和Phomasp.在沙冬青和伴生植物中均有分布。

表5 不同样地沙冬青及其伴生植物深色有隔内生真菌类群比较 Table 5 The comparison between dark septate endophyte in roots of Ammopiptanthus mongolicusand that in A. mongolicus’ s companion plants from different sampling sites

表2表6可知, 不同样地沙冬青与其伴生植物DSE多样性指数差异显著, 在一定程度上反映出群落DSE总数及分布数量的不同。其中, 多样性指数最大值出现在民勤沙冬青中, 为0.735 1, 最小值出现在红花锦鸡儿中, 为0.152 2; 均匀度指数、多样性指数和分离频率在样地间变化规律一致。而Simpson指数变化趋势与前三者相反, 以民勤沙冬青最高, 红花锦鸡儿最低。

表6 沙冬青及其伴生植物深色有隔内生真菌物种多样性 Table 6 Species diversity of dark septate endophyte in the roots of Ammopiptanthus mongolicusand its companion plants
3 讨论
3.1 DSE群落组成和物种多样性

DSE广泛分布于各类生境, 尤其是广泛分布于胁迫环境和受干扰严重地区(Knapp et al., 2012; Postma et al., 2007; Zhao et al., 2015)。目前, 全世界已发现110科600余种植物根组织有DSE定殖(Mandyam & Jumpponen, 2005), 虽然DSE能在体外纯培养, 但大多数纯培养条件下, 无法还原DSE在植物体内的真实生境而不产孢, 加之DSE本身涵盖众多科属, 其组成的复杂性和不明确性, 使得仅通过形态特征难以确定DSE的分类地位, 分子测序技术极大地推动了DSE的分类研究(Bonfimet al., 2016; Yadav et al., 2016)。按照Sieber和Grü nig (2013)对DSE的定义, 本研究分离的菌株均有DSE典型黑化结构, 不同样地的DSE菌株平均分离率为7.48%, 低于沙冬青DSE菌株10.0%的分离率(陈严严等, 2014)。

本研究每个样地都选取300条根段进行DSE分离培养, 能够反映该样地DSE群落组成情况(Bonfim et al., 2016), 在分离的DSE中, AlternariaEmbellisiaCurvulariaPodospora均为荒漠生态系统未见报道的DSE属, 其中PhialocephalaPhoma和Pleosporales 三类DSE在沙冬青根中也有分布(陈严严等, 2014; Li et al., 2015)。与沙冬青DSE多样性对比发现, 磴口样地沙冬青仅有Cladosporiumsp., 与伴生植物沙蒿没有共有属种; 民勤样地沙冬青与伴生植物红花锦鸡儿共有菌株为Pleosporales, 但沙冬青DSE优势种为Paraphoma chrysanthemicola, 银川与沙坡头样地沙冬青与其伴生植物没有共有属种。同时, 沙冬青DSE分离率和多样性指数为民勤> 沙坡头> 银川, 而伴生植物为银川> 沙坡头> 民勤。说明DSE群落组成和物种多样性具有空间异质性, 并与植物种类和生长特性密切相关(Mandyam et al., 2012; Lugo et al., 2015)。

3.2 DSE与植物生态适应性的关系

许多研究表明, DSE与植物互惠共生, 赋予植物优良生长性状, 促进植物营养吸收, 提高植物抗病性及胁迫环境中的抗逆性(Usuki & Narisawa, 2007; Likar & Regvar, 2013; Mahmoud & Narisawa, 2013; Zhao et al., 2015)。与陈严严(2014)等的研究结果对比可知, 在民勤、银川和沙坡头样地, 沙冬青DSE平均总定殖率及种类数量显著高于该样地伴生植物。同时发现, 甘肃、宁夏地区沙冬青可培养DSE共6属10种, 4种产孢, 1种10 ℃诱导后产孢, 其余不产孢, 而伴生植物仅6属6种, 2种产孢, 1种诱导后产孢, 其余不产孢; 磴口样地, 沙冬青仅分离1属1种产孢DSE, 而伴生植物有2属3种, 1种在诱导后产孢(Li et al., 2015)。Mandyam和Jumpponen (2015)研究发现, 与植物有良好共生关系的内生真菌可以促进植物对生存环境的适应能力, 宿主植物进化与DSE丰富度协同一致。伴生植物与第三纪孑遗植物沙冬青相伴相生, 在漫长的进化过程中与DSE协同发展, 与伴生植物相比, DSE可能与沙冬青根系能够形成更好的共生关系, 增强了沙冬青对极端荒漠环境的生态适应性(Mandyam & Jumpponen, 2005; Wu & Guo, 2008; Lugo et al., 2015)。

The authors have declared that no competing interests exist.

作者声明没有竞争性利益冲突.

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