Gerdemann & Trappe (1974)根据 AM 真菌孢子形成于产孢细胞末端这一特性，建立了巨孢囊霉属Gigaspora (内囊霉科Endogonaceae；接合菌门Zygomycota)，包括5个种，极大巨孢囊霉Gigaspora gigantea为模式种，到1985年，该属共有18个物种(Becker & Hall 1976；Bhattacharjee & Mukerji 1980；Koske & Walker 1984, 1985)。Walker & Sanders (1986)根据孢子壁或发芽盾特征，建立了一个新属——盾巨孢囊霉属Scutellospora，含原巨孢囊霉属中的17个物种，美丽盾巨孢囊霉Scutellospora calospora为模式种。Morton & Benny (1990)再次根据孢子壁结构和发芽盾特征，建立了巨孢囊霉科Gigasporineae (球囊霉目Glomerales)，含巨孢囊霉属和盾巨孢囊霉属。Schüßler & Walker (2004)利用核糖体小亚基(SSU)序列确立了多样孢囊霉目Diversisporales，并将巨孢囊霉科归入其中。目前，巨孢囊霉科包含8个属：裂盾囊霉属Racocetra、盾孢囊霉属Cetraspora、齿盾囊霉属Dentiscutata、巨孢囊霉属Gigaspora、盾巨孢囊霉属Scutellospora、内饰孢囊霉属Intraornatospora、类齿盾霉属Paradentiscutata和葱状囊霉属Bulbospora (王幼珊和刘润进 2017)。
Oehl et al. (2008)根据具孢子壁层结构、发芽盾特征、SSU和LSU序列分析，将盾巨孢囊霉属中的5个种分离出来建立了新属——盾孢囊霉属Cetraspora，吉尔莫盾孢囊霉C. gilmorei为模式种。目前该属包括杏黄盾孢囊霉C. armeniaca (Błaszkowski 1992)、吉尔莫盾孢囊霉C. gilmorei (Gerdemann & Trappe 1974)、透明盾孢囊霉C. pellucida (Nicolson & Schenck 1979)、条纹盾孢囊霉C. Striata (Cuenca & Herrera-Peraza 2008)、结节盾孢囊霉C. nodosa (Błaszkowski 1991)、瑞士盾孢囊霉C. helvetica (Oehl et al. 2010)和金黑盾孢囊霉C. auronigra (Lima et al. 2014)共7个物种(
本研究从贵州大学校内金佛山方竹根际土壤中分离到AM真菌的一个物种，经研究属于盾孢囊霉属中未被描述物种，对其进行了形态学描述和分子系统发育分析。
1 材料与方法
1.1 样品采集和AM真菌孢子分离
1.2 AM真菌单物种培养和离体培养
1.3 菌根结构染色
将单物种培养和离体培养所获得的根剪成0.5-1.0 cm，利用醋酸-墨水改良染色法(Vierheilig et al. 1998)进行染色。软化：将根样装入试管中，加入10%氢氧化钾溶液没过根样，90 ℃水浴10-15 min，至根样软化褪色，自来水缓慢冲洗，完全去除根样中的氢氧化钾。漂白：上述根样中加入20%的H2O2溶液，室温下静置30 min，自来水漂洗后，放置于新试管中。酸化：加入5%乙酸溶液酸化5 min，倒掉乙酸溶液。染色：加入含有5%醋酸-墨水染液(95 mL的5%醋酸+ 5 mL的Sheaffer Skrip蓝墨水)，66 ℃水浴20- 30 min。脱色：倒掉染液，蒸馏水冲洗，根样浸泡在清水中进行褪色处理12 h，制片观察。
1.4 形态学分析
将湿筛法分离到的孢子去除表面杂质后，放置于载玻片上，以水或PVLG为载浮剂，在复合显微镜(Olympus BX53)和摄像系统(Olympus DP70)下观察、测量孢子颜色、大小、形状、孢子壁表面纹饰、层数、厚度、发芽壁结构，以及在Melzer’s试剂中的反应等特征，并进行拍照。参照国际丛枝菌根真菌保藏中心(INVAM,
1.5 DNA提取、PCR扩增及测序
表1 SSUmAf-LSUmAr与SSUmCf-LSUmBr引物信息
Table 1
| Nested-PCR | 引物 Primers | 序列 Sequence (5ʹ→3ʹ) | PCR产物长度 Length of PCR product (bp) |
|---|---|---|---|
| 第一轮扩增 First amplification | SSUmAf1 | TGGGTAATCTTTTGAAACTTYA | 1 800 |
| SSUmAf2 | TGGGTAATCTTRTGAAACTTCA | ||
| LSUmAr1 | GCTCACACTCAAATCTATCAAA | ||
| LSUmAr2 | GCTCTAACTCAATTCTATCGAT | ||
| LSUmAr3 | TGCTCTTACTCAAATCTATCAAA | ||
| LSUmAr4 | GCTCTTACTCAAACCTATCGA | ||
| 第二轮扩增 | SSUmCf1 | TCGCTCTTCAACGAGGAATC | 1 500 |
| Second amplification | SSUmCf2 | TATTGTTCTTCAACGAGGAATC | |
| SSUmCf3 | TATTGCTCTTNAACGAGGAATC | ||
| LSUmBr1 | DAACACTCGCATATATGTTAGA | ||
| LSUmBr2 | AACACTCGCACACATGTTAGA | ||
| LSUmBr3 | AACACTCGCATACATGTTAGA | ||
| LSUmBr4 | AAACACTCGCACATATGTTAGA | ||
| LSUmBr5 | AACACTCGCATATATGCTAGA |
1.6 序列比对和系统发育分析
将获得的正、反向序列利用SeqMan v. 7.0 (DNASTAR, Madison)进行校对和拼接，并将拼接序列提交到GenBank数据库中获得登录号。经BLAST比对后，下载盾孢囊霉属中具有SSU-ITS-LSU序列的全部物种及巨孢囊霉科其他属的物种共32个近缘种。以闪亮和平囊霉Pacispora scintillans (FM876831)为外群，进行最大似然法(ML)和贝叶斯法(BI)分析构建系统发
育树。需要说明的是目前盾孢囊霉属的7个物种中C. helvetica、C. Striata和C. auronigra无SSU-ITS-LSU序列。多基因片段数据矩阵通过MEGA 11软件中的MUSCLE功能进行校准。最大似然法(ML)分析是在CIPRES科学门户上使用RAxML-HPC2进行计算，选择GTRGAMMA模型，运行1 000次(Eduardo et al. 2020)。利用PhyloSuite v1.2.2软件中的ModeFinder选择最佳模型后(Zhang et al. 2020)，使用Mrbayes 3.2进行贝叶斯系统发育分析。系统发育树在TreeGraph 2中进行查看与调整。
2 结果与分析
2.1 系统发育分析
将测序所得的3条序列提交至NCBI GenBank数据库，获得登录号为OP004057、OP004058和OP004059，基于SSU-ITS-LSU序列，采用最大似然法(ML)和贝叶斯法(BI)，以闪亮和平囊霉Pacispora scintillans (FM876831)为外群，构建系统发育树(图1)。结果显示：本研究物种属于盾孢囊霉属，3条序列以较高的支持率聚在一起形成独立分支，并与吉尔莫盾孢囊霉形成姊妹分支。
图1
图1
基于SSU-ITS-LSU序列的贝叶斯系统发育树 ML树的拓扑结构与贝叶斯分析结果相似，本图以贝叶斯拓扑结构展示；该系统发育树以闪亮和平囊霉Pacispora scintillans为外群；贝叶斯后验概率≥0.6及ML自举值≥50% (BYPP/MLBP)标注在节点位置；加粗标注为本研究分离的菌株；核苷酸替代率0.02
Fig. 1
Phylogenetic tree generated from Bayesian analysis based on SSU-ITS-LSU sequence, including Pacispora scintillans as outgroup. The tree topology of the maximum likelihood was similar to that of Bayesian analyses. Bayesian posterior probabilities ≥0.6 and ML bootstrap values ≥50% (BYPP/MLBP) are given above the nodes. The strains isolated in this study in bold; Scale in 0.02 substitution per site.
2.2 物种描述
花溪盾孢囊霉 新种 图2
Cetraspora huaxica D.Y. Chen, R.J. He & L. Jiang, sp. nov. Fig. 2
图2
图2
花溪盾孢囊霉形态特征 A-C：完整的孢子. D：PVLG中的破碎的孢子. 显示孢子壁层(OW和GW)，发芽盾(gs)，产孢细胞(Sc)，萌发管(gt). E，F：Melzer’s试剂中孢子壁层结构(OW+MW+IW). IWL3与Melzer’s试剂反应呈深粉色至亮红棕色. G：产孢细胞壁层结构(ScWL1-2)及“菌丝钉”结构(peg). H-J：发芽盾上具有一个中央胚芽孔(gp)，通常被大的折叠(f)隔开形成几个裂片，每个裂片上出现一个胚芽管起始点(gti). I，J：在PVLG溶液中用解剖针将发芽盾从孢子上剖离，且发芽盾壁(gsWL1-2)与Melzer’s试剂不发生反应. K，L：离体培养中的辅助细胞
Fig. 2
Microscopic morphological characteristics Cetraspora huaxica. A-C: Intact spores. D: Crushed spore on PVLG showing spore wall layers (OW and GW), germination shield (gs), a sporogenous cell (Sc), germinal tube (gt). E, F: In Melzer’s reagent, the spore wall layers (OW+MW+IW). IWL3 shows deep pink to bright red-brown reaction in Melzer’s reagent. G: Sporogenous cell wall layers (ScWL1-2) and ‘hyphal pegs’ structure. H-J: Germination shields (gs) with a initial central germ pore (gp), and several lobes that are generally separated by large folds (f); The lobes may regularly bear one germ tube initiation (gti). I, J: Independent germinated shields were completely separated from spores by tearing with a dissecting needle in PVLG liquid, and these shield wall layers (gsWL1-2) did not react in Melzer’s reagent. K, L: Auxiliary cells (aux) in root organ culture.
Fungal Name FN571069
Etymology: Huaxica (Latin), referring to Huaxi District, Guizhou Province, China, where this fungus was originally found.
Holotype: China. Guizhou Province: Huaxi District of Guiyang City (106°39ʹ31ʺE, 26°27ʹ13ʺN; 1 100-1 140 m above sea level), January 2022 and March 2022, D.Y. Chen, C.L. Long. Holotype, Fungarium of Insititute of Microbiology, CAS, voucher HMAS 286821. Isotypes were deposited at the Plant Physiology Laboratory of the University of Guizhou (GZ-HX-G01 to G07).
Description: Sporocarps unknown. Spores borne singly in soil, globose to subglobose, hyaline/white, 187-361×210-378 µm (wide× long), formed terminally on bulbous sporogenous cell (Figs. 2A-2C). The spore contents are hyaline and oil droplet shaped, and these oil droplets appear milky white near the germination shield as the spore maturates (Fig. 2B).
Subcellular structure of spores consists of an outer, middle and inner wall (Fig. 2D). Outer wall is composed of three layers. Outermost wall layer (OWL1) is hyaline, permanent, about 0.5-1.2 µm thick. OWL2 laminate and extremely rigid, hyaline, 3.80-8.76 µm thick, staining deep pink to bright red-brown in Melzer’s reagent (Figs. 2E, 2F). OWL3 tightly adherent to OWL2, 0.6-1.0 µm thick, difficult to observe in crushed spores.
Middle wall (MWL1-2) is 1.1-2.4 µm thick in total and two hyaline layers: a flexible outer layer MWL1 and a semi-flexible layer MWL2. MWL1 is 0.3-0.8 µm thick and generally does not separate from underlying MWL2 but often shows several folds in crushed spores. MWL2 is 0.8-1.6 µm thick, and generally more rigid than MWL1. None of the layers reacts to Melzer’s (Fig. 2E).
Inner wall (IW) is triple-layered (Fig. 2E). The outer IW layer (IWL1) is hyaline, semi-flexible and 0.5-1.4 μm thick. The second layer (IWL2) is semi-flexible, and is 0.6-1.2 µm thick. The innermost layer (IWL3) is rigid, mostly tightly adherent to IWL2. IWL3 stains deep pink to bright red-brown when exposed to Melzer’s reagent.
Germination shield forms on the outer IW surface, pale yellow to pale yellow brown, ellipsoid to cardioid, 88.6-126.1×113.3-147.9 µm wide × long, partitioning 4-8 lobes with nicked margins formed by shallow incisions. Generally, each lobe had a circular germ tube origin (gti; 4.2-10.3 µm in diam.) (Figs. 2H-2J).
Sporogenous cell (Sc) is globose to elongate, 32-49 µm wide and generally pale yellow to pale yellow brown. Two wall layers are visible on the young sporogenous cell, which are continuous with OWL1 and with laminated OWL2. Layer 1 is hyaline, 0.4-0.9 µm thick. Layer 2 is pale yellow to pale yellow brown, 1.2-2.6 µm thick at the sporebase, thinning distally to about 1 µm. One to two (rarely) ‘hyphal pegs’ are often formed on the sporogenous cells (Figs. 2C, 2G).
Auxiliary cells (aux) are formed in small aggregates (2-8 cells) on coiled hyaline hyphae 3.5-5.5 μm in diameter. Each cell (14.80-28.35× 21.20-30.65 μm, wide × long) in aggregates is subglobose, pale-yellow, cells almost smooth or ornamented with tuberculate surface, with swellings 1-6 μm high and 3-8 μm wide (Figs. 2K, 2L).
Mycorrhizal associations. By dual culture and in single-species cultures with Trifolium repens L. as host plant, C. huaxica formed mycorrhiza with vesicles, intra- and extra-radical hyphae (Fig. 3).
Distribution and habitat: Spores of C. huaxica were isolated from rhizosphere soil of Chimonobambusa utilis in Huaxi District, Guizhou Province, China where had typical subtropical humid mild climate, with no severe cold in winter and no heat in summer. It has a long frost-free period (The average frost-free period is 246 d) and abundant rainfall (the annual rainfall is 1 178.3 mm) and high humidity (the mean annual temperature was about 14.9 ℃). Soils are yellowish soil, with 2.7% of organic matter and a pH ranging from 4.5-5.5. At the same time, this site is the only place where this fungus has been found so far.
词源：huaxica (拉丁语)，指中国贵州省花溪区，该真菌最初被发现的地方。
主模式标本：贵州省贵阳市花溪区(东经106°39′31ʺ，北纬26°27′13ʺ，2022年1月、 2022年3月，陈德瑶，龙春丽。模式标本存于中国科学院微生物研究所菌物标本馆(主模标本：HMAS 286821；副模标本：HMAS 286822-23)。同型标本保存于贵州大学植物生理实验室(GZ-HX-G01-G07)。
中壁层由2层(MWL1-2)，透明，厚度约为1.1-2.4 µm，MWL1为柔性壁，厚约0.3-0.8 µm，通常不与底层的MWL2分开，仅在压碎后的孢子中出现几条褶皱；MWL2为半柔性壁层，厚约0.8-1.6 µm，通常比MWL1坚硬。MWL1-2在Melzer’s试剂中不发生反应(图2E)。
内壁层3层(IWL1-3)。IWL1透明，半柔性壁，厚0.5-1.4 μm；IWL2半柔性壁，厚0.6-1.2 µm；IWL3为刚性壁，与IWL2紧密贴合，在Melzer’s试剂中染色为深粉色至亮红棕色。
发芽盾(gs)位于内壁层表面，颜色呈浅黄色至淡黄棕色，椭圆形至心形，大小88.6-126.1× 113.3-147.9 µm，具有4-8个裂片，裂片边缘有刻痕。每个裂片通常有一个圆形胚芽管起始点(gti)，直径4.2-10.3 μm (图2H-2J)。
产孢细胞(Sc)近球形至棒状，宽约32-49 µm，通常为浅黄色至淡黄棕色。具有2层壁组成(ScWL1-2)，分别与外壁层OWL1和OWL2相连。ScWL1透明，厚0.4-0.9 µm；ScWL2为浅黄色至淡黄棕色，孢子基部厚1.2-2.6 µm，远端变薄至约1 µm。通常在产孢细胞上形成1-2个(偶见)菌丝钉(peg) (图2C，2G)。
辅助细胞(aux)通常2-8个聚集成簇，着生于直径为3.5-5.5 μm的卷曲透明的菌丝上，近球形，细胞大小14.80-28.35×21.20-30.65 μm，细胞壁淡黄色，通常表面光滑或有瘤状突起，突起高1-6 μm，宽3-8 μm (图2K，2L)。
菌根染色：通过单物种培养和离体培养得到的菌根，经染色后观察到泡囊、根内和根外菌丝结构(图3)。
图3
图3
花溪盾孢囊霉菌根结构 A：离体培养中的菌丝网络和辅助细胞. B，C：利用0.5%醋酸墨水染色后的三叶草菌根图(菌丝和泡囊结构)
Fig. 3
Mycorrhizal structures of Cetraspora huaxica. A: Hyphal network and auxiliary cells in dual culture. B, C: Mycorrhizal structures of C. huaxica in roots of Trifolium repens L. stained in 0.5% ink-vinegar (hyphae and vesicles).
分布与生境：该物种是从贵州省花溪地区金佛山方竹根际土壤中分离得到。该地区(东经106°39′31ʺ，北纬26°27′13ʺ；海拔1 100-1 140 m)为典型的亚热带湿润温和型气候，年平均气温约14.9 ℃，平均无霜期246 d，年降雨量1 178.3 mm。土壤类型为黄壤，有机质含量为2.7%，pH值在4.5-5.5。这是迄今为止该物种的唯一发现地。
2.3 盾孢囊霉属Cetraspora物种检索表
本检索表在Oehl et al. (2008)的基础上进行更新与修正，表中共8个种。
1 孢子壁表面无纹饰 2
1 孢子壁表面有纹饰 3
2 孢子透明至白色 4
2 孢子有颜色 5
3 孢子颜色较淡，且孢子直径大小约250 μm左右 6
3 孢子呈微带粉红的黄褐色，直径110-190 μm，孢子表面有指纹状突起 条纹盾孢囊霉C. striata
4 孢子明亮透明，白色至浅灰色，一般呈球形到近球形，直径(60)120-250(-420) μm；产孢细胞透明至半透明，发芽盾一般不可见 透明盾孢囊霉C. pellucid
4 孢子透明，产孢细胞和发芽盾易观察 7
5 孢子杏黄色到黄棕色，直径140-240 μm 杏黄盾孢囊霉C. armeniaca
5 孢子亮黄色至金黄色，孢子内壁层L2在Melzer’s试剂中反应变为深紫色至紫黑色 金黑盾孢囊霉C. auronigra
6 幼嫩孢子呈亮白色，在土壤中老化后变暗至乳白色，孢子外壁有凸疣，外壁层OWL2-3和内壁层IWL2在Melzer’s试剂中反应呈深紫色到黑紫色，直径210-270 µm 瑞士盾孢囊霉C. helvetica
6 孢子透明至淡黄色，在孢子外壁上有结节状突起；直径大小为160-270 μm 结节盾孢囊霉C. nodosa
7 孢子透明，在福尔马林中呈奶油色，产孢细胞为棕色；发芽盾易观察，球形至近球形，直径200-320 μm，孢子壁层为3层(外壁层：OWL1-2, 中壁层：MWL1-2，内壁层：IWL1-2) 吉尔莫盾孢囊霉C. gilmorei
7 孢子透明，产孢细胞呈淡黄褐色，发芽盾呈浅黄色到淡黄棕色易观察，孢子外壁层(OWL1-3)和内壁层(IWL1-3)都有3层，且OWL2和IWL3在Melzer’s试剂中呈深粉红色到亮红棕色。孢子大小为187-361×210-378 μm 花溪盾孢囊霉C. huaxica
3 讨论
盾孢囊霉属物种的形态特征：孢子具有3个孢子壁层、发芽盾多裂，具4-12个裂片，孢子透明至近透明(Oehl et al. 2008)，花溪盾孢囊霉与以上特征吻合，鉴定为盾孢囊霉属，其内壁层3层(IWL1-3)，IWL3在Melzer’s试剂中呈深粉红色到亮红棕色，易于与本属其他已描述的物种区分。
在形态学上，花溪盾孢囊霉与透明盾孢囊霉、吉尔莫盾孢囊霉的孢子关系密切，孢子均透明至近透明，孢子都较大，通常在200-280 μm，但孢子壁层和Melzer’s试剂中染色特征具有明显差异。透明盾孢囊霉与花溪盾孢囊霉孢子均为无色，内含物呈油滴状，但透明盾孢囊霉发芽盾不可见，孢子内壁层仅有2层，IWL2在Melzer’s试剂中呈现深紫色到紫黑色(Gerdemann & Trappe 1974；Nicolson & Schenck 1979；Oehl et al. 2008)；而花溪盾孢囊霉发芽盾呈淡黄棕色易观察，孢子内壁层为3层，IWL3在Melzer’s试剂中呈现出深粉色到亮红棕色(图2E)。自然条件下花溪盾孢囊霉与吉尔莫盾孢囊霉孢子形状、颜色相近，但孢子壁结构存在差异。吉尔莫盾孢囊霉孢子外壁(OW)和内壁(IW)均为2层，而花溪盾孢囊霉孢子外壁(OW)和内壁(IW)均有3层。在Melzer’s试剂中，吉尔莫盾孢囊霉OWL2和IWL2染色均为红棕色(Gerdemann & Trappe 1974；Oehl et al. 2008)；花溪盾孢囊霉OWL2染色为亮红棕色，IWL3染色为深粉色到亮红棕色，IWL2在Melzer’s试剂中不发生反应。
综上所述，结合形态学与系统发育分析我们得出结论，本研究描述的物种为AM真菌的一个新种，迄今为止仅在贵阳市花溪区的金佛山方竹的根际土壤中发现，但该物种是否在其他地区及生境分布，还需进一步实地研究。中国地域辽阔，植被复杂多样，拥有超过3万种植物，AM 真菌物种资源潜力巨大。目前在中国发现并报道了包括17个新种在内的AM真菌共有158种(王幼珊和刘润进 2017；姚莉梅等 2019, 2020；He et al. 2021；朱青青等 2021；Long et al. 2022；Yu et al. 2022)，不到全球已报道AM真菌种数的一半，显然，我国AM真菌物种数量(新种)被严重低估，更多的AM真菌物种正在等待被发现。
致谢
感谢王艳和龙青在物种收集和鉴定及试验中的帮助，同时感谢苟光前教授(贵州大学)对新物种拉丁名称方面的指导。
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Three new recorded species of AM fungi from Fanjing Mountain in China
中国新记录种:巴西无梗囊霉的形态与分子生物学鉴定
