Phylogenetic Analysis of Trichoderma Species Associated with Green Mold Disease on Mushrooms and Two New Pathogens on Ganoderma sichuanense
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Isolation
2.2. Growth Characterization
2.3. Morphological Study
2.4. DNA Extraction, PCR, and Sequencing
2.5. Phylogenetic Analyses
3. Results
3.1. Molecular Phylogeny
3.2. Taxonomy
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
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Species | Strains | GenBank Accession Number | References | |
---|---|---|---|---|
TEF1 | RPB2 | |||
T. afarasin | GJS 99-227 | AF348093 | — | [45] |
T. afroharzianum | LESF229 | KT279013 | KT278945 | [46] |
T. afroharzianum | GJS04-186 (T) | FJ463301 | FJ442691 | In GenBank |
T. aggregatum | HMAS248864 | KY688063 | KY688002 | [47] |
T. aggressivum | CBS100525 | AF534614 | AF545541 | [48] |
T. aggressivum | DAOM222156 | AF348098 | FJ442752 | [45] |
T. alni | CPK2494 | EU498313 | EU498350 | [49] |
T. alni | CBS120633 = CPK1982 (T) | EU498312 | EU498349 | [49] |
T. alpinum | HMAS248870 | KY688017 | KY687963 | [47] |
T. alpinum | HMAS248821 (T) | KY688012 | KY687958 | [47] |
T. amazonicum | IB95 | HM142377 | HM142368 | [50] |
T. asperellum | CBS433.97 = TR3 (T) | AF456907 | EU248617 | [51] |
T. atrobrunneum | S3 | KJ665376 | KJ665241 | [20] |
T. atrobrunneum | GJS92-110 (T) | AF443942 | — | [16] |
T. atrogelatinosum | CBS237.63 (T) | — | KJ842201 | In GenBank |
T. azevedoi | CEN1403 | MK696638 | MK696800 | [52] |
T. azevedoi | CEN1422 | MK696660 | MK696821 | [52] |
T. bannaense | HMAS248865 | KY688038 | KY688003 | [47] |
T. bannaense | HMAS248840 (T) | KY688037 | KY687979 | [47] |
T. breve | HMAS248845 | KY688046 | KY687984 | [47] |
T. breve | HMAS248844 (T) | KY688045 | KY687983 | [47] |
T. brunneoviride | CBS121130 = CPK2014 | EU498316 | EU498357 | [49] |
T. camerunense | GJS99-231 | AF348108 | — | [45] |
T. camerunense | GJS99-230 (T) | AF348107 | — | [45] |
T. catoptron | GJS02-76 = CBS114232 (T) | AY391963 | AY391900 | [53] |
T. christiani | CBS132572 = S442 (T) | KJ665439 | KJ665244 | [20] |
T. cinnamomeum | GJS97-237 (T) | AY391979 | AY391920 | [53] |
T. compactum | CBS121218 | KF134798 | KF134789 | [54] |
T. concentricum | HMAS248858 | KY688028 | KY687997 | [47] |
T. concentricum | HMAS248833 (T) | KY688027 | KY687971 | [47] |
T. endophyticum | DIS220J | FJ463330 | FJ442690 | [55] |
T. endophyticum | DIS221E | FJ463316 | FJ442775 | In GenBank |
T. epimyces | CPK1980 | EU498319 | EU498359 | [49] |
T. epimyces | CBS120534 = CPK1981 (T) | EU498320 | EU498360 | [49] |
T. ganodermatigerum | CCMJ5245 (T) | ON567195 | ON567189 | This study |
T. ganodermatigerum | CCMJ5246 | ON567196 | ON567190 | This study |
T. ganodermatigerum | CCMJ5247 | ON567197 | ON567191 | This study |
T. ganodermatigerum | CCMJ5248 | ON567198 | ON567192 | This study |
T. ganodermatigerum | CCMJ5249 | ON567199 | ON567193 | This study |
T. ganodermatigerum | CCMJ5250 | ON567200 | ON567194 | This study |
T. guizhouense | S278 | KF134799 | KF134791 | [54] |
T. guizhouense | S628 | KJ665511 | KJ665273 | [20] |
T. harzianum | GJS05-107 | FJ463329 | FJ442708 | In GenBank |
T. harzianum | GJS04-71 | FJ463396 | FJ442779 | In GenBank |
T. harzianum | Thaum12 | MT081433 | MT118248 | In GenBank |
T. harzianum | CBS226.95 (T) | AF534621 | AF545549 | [48] |
T. hausknechtii | Hypo649 = CBS133493 (T) | KJ665515 | KJ665276 | [20] |
T. helicolixii | S640 = CBS133499 (T) | KJ665517 | KJ665278 | [20] |
T. hengshanicum | HMAS248853 | KY688055 | KY687992 | [47] |
T. hengshanicum | HMAS248852 (T) | KY688054 | KY687991 | [47] |
T. hirsutum | HMAS248859 | KY688030 | KY687998 | [47] |
T. hirsutum | HMAS248834 (T) | KY688029 | KY687972 | [47] |
T. ingratum | HMAS248824 | KY688019 | KY687964 | [47] |
T. ingratum | HMAS248873 | KY688022 | KY688010 | [47] |
T. ingratum | HMAS248822 (T) | KY688018 | KY687973 | [47] |
T. inhamatum | CBS273.78 (T) | AF348099 | FJ442725 | [45] |
T. italicum | S131 = CBS132567 (T) | KJ665525 | KJ665282 | [20] |
T. lentiforme | DIS167C | FJ463309 | FJ442689 | In GenBank |
T. lentiforme | GJS98-6 (T) | AF469195 | — | [16] |
T. liberatum | HMAS248832 | KY688026 | KY687970 | [47] |
T. liberatum | HMAS248831 (T) | KY688025 | KY687969 | [47] |
T. linzhiense | HMAS248874 | KY688048 | KY688011 | [47] |
T. linzhiense | HMAS248846 (T) | KY688047 | KY687985 | [47] |
T. lixii | CBS110080 = GJS97-96 | FJ716622 | KJ665290 | [20] |
T. neocrassum | DAOM164916 = CBS336.93 (T) | AF534615 | AF545542 | [48] |
T. neotropicale | LA11 | HQ022771 | — | [56] |
T. peberdyi | CEN1387 | MK696619 | MK696781 | [52] |
T. peberdyi | CEN1388 | MK696620 | MK696782 | [52] |
T. pleuroticola | T1295 | EU279973 | — | [57] |
T. pleuroticola | CBS124383 (T) | HM142381 | HM142371 | [50] |
T. pleuroti | CBS124387 (T) | HM142382 | HM142372 | [50] |
T. polypori | HMAS248855 | KY688058 | KY687994 | [47] |
T. polypori | HMAS248861 | KY688059 | KY688000 | [47] |
T. priscilae | S129 | KJ665689 | KJ665332 | [20] |
T. pseudodensum | HMAS248829 | KY688024 | KY687968 | [47] |
T. pseudodensum | HMAS248828 (T) | KY688023 | KY687967 | [47] |
T. pseudogelatinosum | TUFC60186 (T) | JQ797397 | JQ797405 | [58] |
T. pyramidale | S573 | KJ665698 | — | [20] |
T. pyramidale | S73 = CBS135574 (T) | KJ665699 | KJ665334 | [20] |
T. rifaii | DIS337F | FJ463321 | FJ442720 | In GenBank |
T. rifaii | DIS355B (T) | FJ463324 | — | In GenBank |
T. simmonsii | GJS90-22 | AY391984 | AY391925 | [53] |
T. simmonsii | GJS92-100 | AF443937 | FJ442710 | [16] |
T. simmonsii | GJS91-138 | AF443935 | FJ442757 | [16] |
T. simplex | HMAS248860 | KY688042 | KY687999 | [47] |
T. simplex | HMAS248842 (T) | KY688041 | KY687981 | [47] |
T. solum | HMAS248848 | KY688050 | KY687987 | [47] |
T. solum | HMAS248847 (T) | KY688049 | KY687986 | [47] |
T. spirale | DAOM183974 | EU280049 | — | [57] |
T. spirale | LESF107 | KT279022 | KT278956 | [46] |
T. stramineum | GJS02-84 = CBS114248 (T) | AY391999 | AY391945 | [53] |
T. tawa | GJS97-174 = CBS114233 (T) | AY392004 | AY391956 | [53] |
T. tomentosum | S33 | KF134801 | KF134793 | [54] |
T. tomentosum | DAOM178713A (T) | AF534630 | AF545557 | [48] |
T. velutinum | DAOM230013 = CPK298 | AY937415 | KF134794 | [59] |
T. virens | DIS162 | FJ463367 | FJ442696 | In GenBank |
T. zayuense | HMAS248836 | KY688032 | KY687975 | [47] |
T. zayuense | HMAS248835 (T) | KY688031 | KY687974 | [47] |
Species | Host Range | Isolates | GenBank Accession Number | References | |
---|---|---|---|---|---|
TEF1 | RPB2 | ||||
T. aggressivum | Agaricus bisporus | CBS100525 | AF534614 | AF545541 | [48] |
T. aggressivum f. aggressivum | Agaricus bisporus | GJS99-30 | AF348109 | — | [60] |
DAOM222156 | AF348098 | FJ442752 | [45] | ||
T. aggressivum f. europaeum | Agaricus bisporus | CBS100526 (T) | KP008993 | KP009166 | [45] |
— | TRS27 | KP008994 | KP009163 | In GenBank | |
— | CBS435.95 | KP008998 | KP009169 | In GenBank | |
T. alni | Macrotyphula cf. contorta | CBS120633 | EU498312 | EU498349 | [49] |
CPK2494 | EU498313 | EU498350 | |||
T. asperellum | Pleurotus ostreatus | T11 (ACCC32725) | MF049065 | — | [61] |
Pleurotus eryngii | — | — | — | [62] | |
— | CGMCC6422 | KF425756 | KF425755 | [63] | |
— | CBS433.97 = TR3 (T) | AF456907 | EU248617 | In GenBank | |
T. atrobrunneum | Ganoderma sichuanense | CGMCC3.19070 | MH464779 | — | [64] |
— | T17-27 | MW232537 | MW232508 | [65] | |
T. atroviride | Pleurotus ostreatus | CPK3277 | EU918154 | — | [66] |
Ganoderma sichuanense | 2015005 | — | — | [10] | |
Agaricus bisporus | T33 | — | — | [67] | |
Lentinula edodes | T25 | — | — | [68] | |
Pleurotus eryngii | — | — | — | [69] | |
— | PARC1011 | MT454114 | MT454130 | [70] | |
— | PARC1018 | MT454121 | MT454137 | ||
— | DAOM222144 | AF456889 | FJ442754 | [71] | |
— | Th002 | AB558906 | AB558915 | [72] | |
T. aureoviride | Pleurotus ostreatus | HMAS266607 | KF923280 | KF923306 | [73] |
T. austriacum | Peziza sp. | CBS122494 (T) | FJ860619 | FJ860525 | [19] |
T. capillare | Agaricus bisporus | CPK2883 | JN182283 | JN182312 | [74] |
GJS99-3 | JN175584 | JN175529 | |||
T. catoptron | Aphyllophorales s. l. | GJS02-76 (T) | AY391963 | AY391900 | [53] |
T. cerinum | Lentinula edodes | S357 | KF134797 | KF134788 | [75] |
T. chromospermum | black mycelium and black pyrenomycete | GJS95-196 | AY391975 | AY391914 | [53] |
GJS98-73 | AY391976 | AY391915 | |||
GJS94-68 = CBS114577 | — | AY391913 | |||
— | HMAS252537 | KF729986 | KF730004 | [25] | |
— | HMAS252539 | KF923287 | KF923314 | ||
— | HMAS252535 | KF923292 | KF923315 | ||
T. citrinoviride | Lentinula edodes | TAMA0154 | AB807641 | AB807653 | [76] |
Pleurotus ostreatus | GJS92-8 | JN175595 | JN175544 | [77] | |
Pleurotus eryngii | GJS01-364 | AY225860 | AF545565 | [69] | |
Polypore mushroom | TAMA0188 | AB807644 | AB807656 | [76] | |
— | HZA9 | MK850831 | MK962804 | [78] | |
T. epimyces | Polyporus umbellatus | CPK1980 | EU498319 | EU498359 | [49] |
CBS120534 (T) | EU498320 | EU498360 | |||
T. erinaceum | — | DIS7 | DQ109547 | EU248604 | [79] |
T. fasciculatum | Hypocrea ascospores | CBS118.72 | — | — | [80] |
— | DAOM172827 | AF534628 | AF545555 | [48] | |
T. fomiticola | Fomes fomentarius | CBS121136 | FJ860639 | FJ860538 | [18] |
CPK3137 | FJ860640 | FJ860539 | |||
T. ghanense | Agaricus bisporus | NBRC30902 | AB807638 | AB807650 | [76] |
T. ganodermatis | Ganoderma sichuanense | HMAS248856 | KY688060 | KY687995 | [47] |
HMAS248869 | KY688061 | KY688007 | [47] | ||
T. ganodermatigerum | Ganoderma sichuanense | CCMJ5245(T) | ON567195 | ON567189 | This study |
CCMJ5246 | ON567196 | ON567190 | |||
CCMJ5247 | ON567197 | ON567191 | |||
CCMJ5248 | ON567198 | ON567192 | |||
CCMJ5249 | ON567199 | ON567193 | |||
CCMJ5250 | ON567200 | ON567194 | |||
T. ghanense | Agaricus bisporus | NBRC30902 | AB807638 | — | [76] |
T. hamatum | Agaricus bisporus | Tham20-3 | — | — | [81] |
Lentinula edodes | — | — | — | [82] | |
— | DAOM167057 (T) | EU279965 | AF545548 | [57] | |
— | Hypo647 = WU31629 | KJ665513 | KJ665274 | [20] | |
— | Hypo648 = CBS132565 | KJ665514 | KJ665275 | [20] | |
T. harzianum | Pleurotus ostreatus | KACC40558 | — | — | [66] |
Cyclocybe aegerita | JB1 | — | — | [73] | |
Lentinula edodes | T50 | — | — | [83] | |
Pleurotus eryngii | KACC40784 | — | — | [69] | |
Pleurotus ostreatus | |||||
Agaricus bisporus | — | — | — | [45] | |
Pleurotus ostreatus | — | — | — | [84] | |
Polypores/Corticiaceous | — | — | — | [18] | |
Pleurotus tuoliensis | — | — | — | [85] | |
Tremella fuciformis | |||||
Flammulina filiformis | |||||
— | CBS226.95 | AF348101 | AF545549 | [48] | |
— | Thaum12 | MT081433 | MT118248 | [86] | |
— | CBS227.95 | AF348100 | — | [45] | |
— | GJS05-107 | FJ463329 | FJ442708 | In GenBank | |
— | GJS04-71 | FJ463396 | FJ442779 | In GenBank | |
T. hengshanicum | Ganoderma sichuanense | 1009 | — | — | [87] |
— | HMAS248852 (T) | KY688054 | KY687991 | [47] | |
— | HMAS248853 | KY688055 | KY687992 | ||
T. inhamatum | Agaricus bisporus | CBS273.78 (T) | AF348099 | FJ442725 | [81] |
Pleurotus tuoliensis | — | — | — | [85] | |
T. koningii | Pleurotus eryngii | — | — | — | [69] |
Agaricus bisporus | — | — | — | [88] | |
Lentinula edodes | — | — | — | [85] | |
Pleurotus ostreatus | |||||
Pleurotus tuoliensis | |||||
Flammulina filiformis | |||||
Volvariella volvacea | |||||
Hypsizygus marmoreus | |||||
Ganoderma sichuanense | TFl040917 | — | — | [75] | |
Tremella fuciformis | TGy040604 | — | — | ||
— | 7723 | KJ634753 | KJ634720 | [89] | |
— | GJS90-18 | DQ289007 | EU248600 | [23] | |
— | CBS979.70 | AY665703 | EU248601 | In GenBank | |
— | S22 | KC285595 | KC285749 | [90] | |
T. koningiopsis | Phaiius rubrovolvata | CXYL | MN135988 | MT038997 | [91] |
Ganoderma sichuanense | CCMJ5253 | ON567187 | ON567201 | This study | |
CCMJ5254 | ON567188 | ON567202 | |||
T. kunigamense | Lentinula edodes | TAMA193 | AB807645 | AB807657 | [76] |
T. leguminosarum | dark corticiaceous fungus | S391 | KJ665548 | KJ665287 | [20] |
CBS130014 | KJ665551 | KJ665288 | |||
S503 | KJ665552 | KJ665289 | |||
T. lieckfeldtiae | Moniliophthora roreri | GJS00-14 = CBS123049 (T) | EU856326 | EU883562 | [92] |
T. longibrachiatum | Pleurotus ostreatus | TUFC61535 = CBS816.68(T) | EU401591 | DQ087242 | [40] |
Agrocybe aegerita | JB4 | — | — | [73] | |
Lentinula edodes | T57 | — | — | [83] | |
Ganoderma sichuanense | TFl040921 | — | — | [75] | |
Pleurotus eryngii | — | — | — | [93] | |
Agaricus bisporus | — | — | — | [81] | |
Pleurotus tuoliensis | — | — | — | [85] | |
Hypsizygus marmoreus | |||||
Volvariella volvacea | |||||
T. mienum | Lentinula edodes | TUFC61517 | JQ621975 | JQ621965 | [94] |
T. orientale | Ganoderma applanatum | LESF516 | KT279041 | KT278976 | [46] |
Ganoderma applanatum | LESF540 | KT279042 | KT278977 | ||
Ganoderma applanatum | LESF544 | KT279043 | KT278978 | ||
Ganoderma applanatum | TRS707 | KP008888 | KP009202 | ||
T. oblongisporum | Lentinula edodes | T37 | — | — | [83] |
— | DAOM167085 | AF534623 | AF545551 | [48] | |
T. parareesei | Pleurotus eryngii | TAMA0153 | AB807640 | AB807652 | [76] |
T. parestonica | Hymenochaete tabacina | CBS120636 (T) | FJ860667 | FJ860565 | [18] |
T. pleuroticola | Pleurotus ostreatus | CBS124383 (T) | HM142381 | HM142371 | [66] |
CPK2885 | EU918161 | EU918141 | |||
Pleurotus eryngii | CAF-TP3 | — | — | [69] | |
Lentinula edodes | T22 | — | — | [83] | |
Cyclocybe aegerita | JB7 | — | — | [73] | |
— | T1295 | EU279973 | — | [57] | |
T. pleuroti | Pleurotus ostreatus | KACC44537 | — | — | [69] |
Pleurotus eryngii var. ferulae | — | — | — | [95] | |
— | CBS124387 (T) | HM142382 | HM142372 | [50] | |
T. polypori | Lentinula edodes | HMAS248861 | KY688059 | KY688000 | [47] |
Polyporus sp. | HMAS248855 (T) | KY688058 | KY687994 | ||
T. polysporum | Lentinula edodes | — | — | — | [96] |
— | 8232 | KJ634779 | KJ634746 | [89] | |
— | 8147 | KJ634771 | KJ634738 | ||
T. priscilae | Crepidotus sp. | S168 = CBS131487 (T) | KJ665691 | KJ665333 | [20] |
Stereum sp. | S129 | KJ665689 | KJ665332 | ||
— | HMAS245002 | KT343760 | KT343764 | In GenBank | |
T. protopulvinatum | Fomitopsis pinicola | CPK2434 | FJ860677 | FJ860574 | [18] |
T. pulvinatum | Fomitopsis pinicola | CBS121279 | FJ860683 | FJ860577 | [18] |
T. pseudokoningii | Lentinula edodes | DUCC4021 | KX431217 | — | [77] |
Cyclocybe aegerita | TGc050619 | — | — | [75] | |
Ganoderma sichuanense | TFl040926 | — | — | ||
Pleurotus eryngii | — | — | — | [97] | |
Flammulina filiformis | — | — | — | [98] | |
Pleurotus tuoliensis | — | — | — | [85] | |
Volvariella volvacea | |||||
Hypsizygus marmoreus | |||||
— | DAOM167678 | AY865641 | KJ842214 | [99] | |
— | GJS99-149 | JN175589 | JN175536 | [17] | |
— | GJSNS19 | JN175588 | JN175535 | ||
T. pseudolacteum | Lentinula edodes | TUFC61496 | JX238494 | JX238479 | [100] |
TUFC61502 | JX238480 | JX238471 | |||
T. samuelsii | Hymenochaete sp. | S5 = CBS130537 | JN715651 | JN715599 | [101] |
S42 | JN715652 | JN715598 | |||
T. songyi | Tricholoma matsutake | TC556 | KX266244 | KX266250 | [102] |
TC480 | KX266243 | KX266249 | |||
T. stilbohypoxyli | Stilbohypoxylon moelleri | Hypo256 = CPK1977 | FJ860702 | FJ860592 | [23] |
T. stromaticum | Agaricus bisporus | GJS97-181 | AY937447 | HQ342227 | [59] |
— | GJS07-88 | HQ342195 | HQ342258 | [103] | |
— | GJS03-47 | HQ342201 | HQ342264 | ||
— | GJS00-107 | HQ342202 | HQ342265 | ||
T. sulphureum | Laetiporus sulphureus | CBS119929 | FJ860710 | FJ179620 | [18] |
CPK1593 | FJ860709 | FJ860599 | |||
Thelephora sp. | GJS95-135 = CBS114237 | AY392006 | AY391958 | [53] | |
T. tsugarense | Lentinula edodes | TAMA203 (T) | AB807647 | AB807659 | [76] |
T. viride | Lentinula edodes | T13 | — | — | [83] |
Pleurotus ostreatus | — | — | — | [82] | |
Tremella fuciformis | TGc040905 | — | — | [75] | |
Ganoderma sichuanense | TFl080706 | — | — | [75] | |
Flammulina filiformis | TFj10010 | — | — | [75] | |
Cyclocybe aegerita | TGc040905 | — | — | [75] | |
Phallus indusiatus | TFl080706 | — | — | [75] | |
Tremella fuciformis | TGc040905 | — | — | [75] | |
Agaricus bisporus | — | — | — | [88] | |
Pleurotus eryngii | — | — | [69] | ||
— | TRS575 | KP008931 | KP009081 | In GenBank | |
— | LESF115 | KT278989 | KT278921 | [46] | |
T. virens | Agaricus bisporus | — | — | — | [88] |
Pleurotus eryngii | — | — | — | ||
— | DIS162 | FJ463367 | FJ442696 | In GenBank | |
— | DIS328A | FJ463363 | FJ442738 | In GenBank | |
T. cf. virens | Pleurotus eryngii | KACC40783 | — | — | [69] |
Pleurotus ostreatus | TUCIM2558 | KX655776 | — | [104] | |
T. viridarium | Steccherinum ochraceum | GJS89-142 | AY376049 | EU241495 | [51] |
Nemania sp. | GJS98-182 | DQ307511 | EU252011 | [23] | |
Protocrea farinosa | — | CBS121551 | EU703889 | EU703935 | [105] |
Protocrea pallida | — | CBS121552 | EU703897 | EU703944 |
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An, X.-Y.; Cheng, G.-H.; Gao, H.-X.; Li, X.-F.; Yang, Y.; Li, D.; Li, Y. Phylogenetic Analysis of Trichoderma Species Associated with Green Mold Disease on Mushrooms and Two New Pathogens on Ganoderma sichuanense. J. Fungi 2022, 8, 704. https://doi.org/10.3390/jof8070704
An X-Y, Cheng G-H, Gao H-X, Li X-F, Yang Y, Li D, Li Y. Phylogenetic Analysis of Trichoderma Species Associated with Green Mold Disease on Mushrooms and Two New Pathogens on Ganoderma sichuanense. Journal of Fungi. 2022; 8(7):704. https://doi.org/10.3390/jof8070704
Chicago/Turabian StyleAn, Xiao-Ya, Guo-Hui Cheng, Han-Xing Gao, Xue-Fei Li, Yang Yang, Dan Li, and Yu Li. 2022. "Phylogenetic Analysis of Trichoderma Species Associated with Green Mold Disease on Mushrooms and Two New Pathogens on Ganoderma sichuanense" Journal of Fungi 8, no. 7: 704. https://doi.org/10.3390/jof8070704