Historical Differentiation and Recent Hybridization in Natural Populations of the Nematode-Trapping Fungus Arthrobotrys oligospora in China
Abstract
:1. Introduction
2. Materials and Methods
2.1. Strains
2.2. Identification of Tandem Repeat Loci and Development of Amplification Primers
2.3. DNA Extraction, PCR Amplification and Sequencing
2.4. Data Analysis
2.5. Intraspecific Phenotypic Variation
2.5.1. Comparison of Mycelial Growth and Conidial Shape
2.5.2. Trap Formation and Bioassay
2.5.3. Nematicidal Activity of Fermentation Broth
2.5.4. Statistical Analysis
3. Results
3.1. Genetic Diversity of the Chinese Samples of A. oligospora Detected by STRs and MLST
3.2. Genetic Differentiation and Population Structure
3.3. Phylogenetic Divergence
3.4. Clonality and Recombination
3.5. Phenotypical Characterization
3.5.1. Conidial Morphology
3.5.2. Mycelial Growth
3.5.3. Conidial Yield, Trap Formation and Nematode-Trapping Bioassay
4. Discussion
4.1. Development of Novel STRs for NTF
4.2. Historical Population Differentiation
4.3. Recent Hybridization and Recombination
4.4. Intraspecies Diversification
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Population | No. Isolates | No. Alleles in Each Locus (No. Private Alleles) | ||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
A3 | A5 | A17 | A25 | A51 | A74 | A80 | A83 | A87 | A101 | A103 | A126 | A149 | A154 | A156 | A160 | A177 | A187 | A191 | A192 | Total | ||
Hubei (HuB) | 17 | 1 | 1 | 3 | 2 | 1 | 2 | 1 | 2 | 1 | 2 | 2 | 2 | 2 (1) | 2 | 2 | 3 (1) | 3 | 2 | 3 | 1 | 38 (2) |
Henan (HeN) | 8 | 2 | 1 | 2 (1) | 1 | 1 | 3 | 2 | 2 | 2 | 3 | 3 | 2 | 2 | 2 | 3 | 2 | 2 | 3 | 5 | 2 | 45 (1) |
Zhejiang (ZheJ) | 5 | 1 | 2 | 3 | 1 | 2 (1) | 3 | 2 | 2 | 1 | 4 | 2 | 2 | 1 | 1 | 3 | 1 | 4 | 2 | 3 | 2 | 42 (1) |
Nei Mongol (NeiM) | 7 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 2 | 1 | 1 | 2 | 1 | 1 | 23 |
Shaanxi (ShanX) | 17 | 2 | 1 | 3 | 2 | 2 | 4 | 2 | 4 | 2 | 5 | 5 | 4 (1) | 2 | 3 | 3 | 3 | 3 | 3 | 4 | 2 | 59 (1) |
Jilin (JiL) | 14 | 1 | 1 | 2 | 1 | 1 | 3 | 1 | 2 | 1 | 3 | 2 | 2 | 1 | 3 (1) | 2 | 1 | 1 | 2 | 3 (1) | 1 | 34 (2) |
Qinghai (QingH) | 10 | 2 | 2 | 3 | 3 | 2 | 4 | 3 | 2 | 2 | 5 | 5 | 3 | 2 | 3 | 3 | 3 | 5 | 3 | 5 | 3 | 63 |
Kanas lake, Xinjiang (XinJ1) | 10 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 21 |
Urumqi Botanical Garden, Xinjiang (XinJ2) | 13 | 1 | 1 | 2 | 2 | 2 | 1 | 2 | 2 | 1 | 2 | 2 | 2 | 1 | 2 (1) | 2 | 2 | 1 | 2 | 1 | 1 | 32 (1) |
Guangdong (GuangD) | 5 | 1 | 1 | 4 | 1 | 2 | 2 | 2 | 2 | 2 | 5 | 2 | 3 | 2 | 1 | 3 (1) | 2 | 2 | 2 | 4 | 2 | 45 (1) |
Guangxi (GuangX) | 19 | 1 | 1 | 1 | 1 | 2 | 3 | 1 | 3 | 2 (1) | 5 (2) | 3 | 2 | 2 | 2 | 2 | 2 (1) | 3 | 2 | 4 (1) | 2 (1) | 44 (6) |
Hainan (HaiN) | 22 | 1 | 3 | 4 | 5 | 3 | 3 | 3 | 5 | 4 | 4 | 4 | 4 (1) | 6 (2) | 2 | 3 | 2 | 4 | 3 | 5 (2) | 3 | 71 (5) |
Dianchi lake, Yunnan (Dianchi_YunN) | 13 | 3 | 3 | 2 | 4 | 2 | 3 | 4 | 4 (2) | 4 (1) | 4 | 5 | 6 | 4 | 2 | 3 | 3 | 4 | 3 | 4 (1) | 4 | 71 (4) |
Gejiu, Yunnan (GeJ_YunN) | 15 | 3 | 2 | 3 | 3 | 4 | 3 | 3 | 3 | 3 | 5 | 5 (1) | 2 | 3 | 3 | 4 (1) | 3 (1) | 4 | 3 (1) | 5 | 3 (1) | 67 (5) |
Yimen, Yunnan (YiM_YunN) | 24 | 3 | 2 | 4 | 3 | 3 | 4 | 6 (2) | 5 (1) | 3 | 5 (1) | 3 | 4 | 4 | 3 | 4 | 4 (2) | 6 (2) | 3 | 7 (1) | 3 | 79 (9) |
Heijing, Yunnan (HeiJ_YunN) | 15 | 2 | 5 | 2 | 3 | 3 | 5 | 3 | 5 | 4 | 8 (1) | 4 | 5 | 2 | 4 (1) | 4 | 5 | 5 | 6 | 8 (1) | 5 | 88 (3) |
Guizhou (GuiZ) | 9 | 2 | 2 | 3 | 1 | 3 (1) | 2 | 2 | 3 | 2 | 3 (1) | 3 | 3 | 2 | 2 | 3 | 2 | 2 | 3 | 2 | 2 | 47 (2) |
Sichuan (SiC) | 13 | 1 | 2 | 2 | 2 | 2 | 3 | 2 | 3 | 2 | 3 | 3 (1) | 2 | 3 | 1 | 2 | 2 | 3 | 2 | 2 | 2 | 44 (1) |
Tibet | 3 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 2 | 3 (1) | 1 | 2 | 2 | 2 (1) | 2 | 2 | 3 | 1 | 3 (2) | 1 | 2 | 41 (4) |
Total | 239 | 3 | 5 | 7 | 5 | 9 | 10 | 7 | 10 | 8 | 16 | 13 | 10 | 11 | 6 | 8 | 11 | 12 | 9 | 21 | 7 | 188 (48) |
Locus | Forward Primer Sequence | Reverse Primer Sequence | Repeat Unit | PIC | Allele Frequency | Availability | Gene Diversity |
---|---|---|---|---|---|---|---|
A3 | FAM-GGAGTGGAAGTTAGATTGGAG | GGGGAACTAATTTACTTGCAT | GTG | 0.244 | 0.849 | 0.941 | 0.265 |
A5 | HEX-CGATGAAGACGTGAGTTAGTT | TGTCTGTCACCACCTTTAATC | GATG | 0.333 | 0.795 | 0.958 | 0.353 |
A17 | TET-CTCTGCTGAGACGTTAATGAT | GTAAATCGTACCCAAGAGGTT | TGG | 0.534 | 0.563 | 0.967 | 0.593 |
A25 | FAM-GGGCATACCTCTCTTCTCTTA | GGATTGCTAGGTATGGTCTTT | AGT | 0.347 | 0.785 | 0.954 | 0.367 |
A51 | HEX-ATTAACAATGGTCCGAAACTT | GACAAGGAGAAAGCCATTAGT | AAGC | 0.465 | 0.702 | 0.941 | 0.486 |
A74 | TET-GATCGATTCTCGCTTAAAGAC | TCCTGCTCCACTATACTCTCA | TGC | 0.790 | 0.286 | 0.979 | 0.814 |
A80 | FAM-GGGACATCGACAATATGTAAG | GAGCTCTGCTTTGAGACATAA | CTG | 0.552 | 0.603 | 0.937 | 0.588 |
A83 | HEX-GAATCTTTCGGTTTAATGGTT | GGGAATGGTGGTATCATAGTA | CTTT | 0.644 | 0.532 | 0.975 | 0.671 |
A87 | TET-GGAGAAACATCAATCAATCAA | CTGAGAGGAACCAAGATGTC | AGCA | 0.508 | 0.651 | 0.958 | 0.540 |
A101 | FAM-ACAACATCAACTACCATCCAC | GGCTATTGGAAGAAGGATAAG | CTC | 0.811 | 0.330 | 0.925 | 0.828 |
A103 | HEX-TCACTGCACTATCTCCAATCT | ACACGACATCGAAACATACTT | TGTA | 0.734 | 0.329 | 0.979 | 0.765 |
A126 | TET-GCCAGGTGGTTAGGAGTATAA | TATTTGAACCACCATAACGTC | AAAG | 0.697 | 0.420 | 0.967 | 0.733 |
A149 | FAM-AAAGAATGTGTGTCATCGAAT | TTCATCCTAGTTCCGTCAGTA | CA | 0.458 | 0.714 | 0.908 | 0.474 |
A154 | HEX-TAATCTGAATGGTTGGTTGTT | CATGAAGGACTGTCAACTAGC | GCTA | 0.475 | 0.640 | 0.954 | 0.528 |
A156 | TET-ATGTTTAATTTCCCTCCAAAC | TTCTCTCAACTCGCAATTCT | TGA | 0.682 | 0.475 | 0.933 | 0.712 |
A160 | FAM-GAACATGCACGTGTGAGATA | GACTCCATACGAGACCATACA | AGTC | 0.430 | 0.726 | 0.933 | 0.452 |
A177 | HEX-GTTCGAGGGATAGTAGTGGTT | CCAACGCATATCTTTTACCTA | AG | 0.712 | 0.358 | 0.912 | 0.747 |
A187 | TET-GTCCAAGTTTGTCCAGTACAC | ATCGTGGAGAATATACCGAAT | CCT | 0.628 | 0.491 | 0.937 | 0.672 |
A191 | FAM-AACACATCTCATTCATCCATC | ACCTGACATTTGACAGTTGAC | CAC | 0.858 | 0.225 | 0.950 | 0.870 |
A192 | HEX-CCTAATACCCAACCGAATAAC | AAACAGGTGTAACTGGGTTCT | CTC | 0.541 | 0.610 | 0.933 | 0.579 |
Population | No. of Isolates | MLST Genotype (No. of Isolates in Each Genotype) | Private MLST Genotype | Genotypic Diversity |
---|---|---|---|---|
HuB | 17 | 1 (3); 2 (1); 4 (1); 21 (1); 23 (4); 28 (1); 29 (1); 30 (3); 36 (2) | 4; 21; 28; 29; 30 | 0.904 |
HeN | 8 | 1 (1); 23 (4); 24 (1); 25 (1); 50 (1) | 25; 50 | 0.786 |
ZheJ | 5 | 1 (1); 7 (1); 16 (1); 23 (2) | 0.900 | |
NeiM | 7 | 5 (1); 6 (2); 7 (4) | 5; 6 | 0.667 |
ShanX | 17 | 1 (1); 2 (1); 19 (1); 20 (1); 23 (10); 24 (2); 57 (1) | 19; 20; 57 | 0.662 |
JiL | 14 | 7 (14) | 0 | |
QingH | 10 | 1 (1); 2 (1); 7 (2); 23 (2); 31 (1); 47 (1); 51 (1); 52 (1) | 31; 47; 51; 52 | 0.956 |
XinJ1 | 10 | 23 (10) | 0 | |
XinJ2 | 13 | 23 (13) | 0 | |
GuangD | 5 | 3 (1); 7 (1); 23 (3) | 3 | 0.700 |
GuangX | 19 | 1 (7); 2 (1); 22 (1); 23 (4); 24 (6) | 0.754 | |
HaiN | 22 | 9 (1); 10 (1); 11 (10); 12 (1); 13 (1); 22 (1); 23 (2); 26 (1); 41 (4) | 9; 10; 11; 12; 13; 26; 41 | 0.775 |
Dianchi_YunN | 13 | 23 (8); 45 (1); 48 (1); 49 (2); 53 (1) | 48; 49 | 0.628 |
GeJ_YunN | 15 | 1 (3); 23 (6); 53 (2); 58 (4) | 0.286 | |
YiM_YunN | 24 | 8 (1); 33 (1); 34 (4); 35 (1); 37 (1); 38 (1); 39 (1); 53 (1); 54 (1); 55 (1); 56 (1); 58 (9); 59 (1) | 8; 33; 35; 37; 38; 39; 54; 55; 56; 59 | 0.848 |
HeiJ_YunN | 15 | 14 (1); 16 (1); 18 (1); 24 (1); 32 (1); 34 (1); 36 (2); 40 (1); 42 (1); 44 (1); 45 (1); 46 (1); 53 (2) | 14; 18; 32; 40; 42; 44; 46 | 0.981 |
GuiZ | 9 | 15 (1); 16 (5); 17 (1); 27 (1); 58 (1) | 15; 17; 27 | 0.722 |
SiC | 13 | 23 (3); 45 (10) | 0.385 | |
Tibet | 3 | 43 (1); 58 (2) | 43 | 0.667 |
Sample Groups | Sample Size | Phylogenetic Compatibility (p Value) | rBarD (p Value) | ||
---|---|---|---|---|---|
MLST | STR | MLST | STR | ||
Total | 239 | 0 (1) | 0.01 (<0.001) | 0.6398 (<0.001) | 0.355 (<0.001) |
Central | 25 | 0.8667 (0.447) | 0.7 (0.038) | 0.1077 (0.009) | 0.1331 (<0.001) |
East | 5 | 1 (1) | 0.9947 (0.096) | 0.6805 (0.001) | 0.3039 (<0.001) |
North | 24 | 0.9333 (1) | 0.8 (<0.001) | 0.2784 (<0.001) | 0.2772 (<0.001) |
Northeast | 14 | 1 (1) | 0.9211 (0.009) | -nan * (<0.001) | 0.115 (<0.001) |
Northwest | 33 | 0.8 (0.889) | 0.8632 (<0.001) | 0.576 (<0.001) | 0.3988 (<0.001) |
South | 46 | 0.4667 (<0.001) | 0.2526 (<0.001) | 0.6867 (<0.001) | 0.288 (<0.001) |
Southwest | 92 | 0.2667 (<0.001) | 0.0579 (<0.001) | 0.661 (<0.001) | 0.3874 (<0.001) |
Clade I | 151 | 0.1333 (<0.001) | 0.021 (<0.001) | 0.5042 (<0.001) | 0.2019 (<0.001) |
Clade II | 46 | 0.5333 (<0.001) | 0.3052 (<0.001) | 0.6379 (<0.001) | 0.4439 (<0.001) |
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Zhou, D.; Xu, J.; Dong, J.; Li, H.; Wang, D.; Gu, J.; Zhang, K.-Q.; Zhang, Y. Historical Differentiation and Recent Hybridization in Natural Populations of the Nematode-Trapping Fungus Arthrobotrys oligospora in China. Microorganisms 2021, 9, 1919. https://doi.org/10.3390/microorganisms9091919
Zhou D, Xu J, Dong J, Li H, Wang D, Gu J, Zhang K-Q, Zhang Y. Historical Differentiation and Recent Hybridization in Natural Populations of the Nematode-Trapping Fungus Arthrobotrys oligospora in China. Microorganisms. 2021; 9(9):1919. https://doi.org/10.3390/microorganisms9091919
Chicago/Turabian StyleZhou, Duanyong, Jianping Xu, Jianyong Dong, Haixia Li, Da Wang, Juan Gu, Ke-Qin Zhang, and Ying Zhang. 2021. "Historical Differentiation and Recent Hybridization in Natural Populations of the Nematode-Trapping Fungus Arthrobotrys oligospora in China" Microorganisms 9, no. 9: 1919. https://doi.org/10.3390/microorganisms9091919
APA StyleZhou, D., Xu, J., Dong, J., Li, H., Wang, D., Gu, J., Zhang, K.-Q., & Zhang, Y. (2021). Historical Differentiation and Recent Hybridization in Natural Populations of the Nematode-Trapping Fungus Arthrobotrys oligospora in China. Microorganisms, 9(9), 1919. https://doi.org/10.3390/microorganisms9091919