Diversity and Evolution of Entomocorticium (Russulales, Peniophoraceae), a Genus of Bark Beetle Mutualists Derived from Free-Living, Wood Rotting Peniophora
Abstract
:1. Introduction
2. Material and Methods
2.1. Fungus Isolation
2.2. Morphological Observations
2.3. Taxa Sampling and Sources
2.4. DNA Extraction, PCR Amplification, and Sequencing
2.5. Phylogenetic Analyses
2.6. Ancestral Character State Reconstruction
2.7. Post-Analyses Graphical Display
3. Results
Taxonomy
4. Discussion
4.1. How Did Such Relationships Arise?
4.2. Distinct Associations across Bark Beetles and Entomocorticium
4.3. Distinct Functional Traits in Basidiomycota and Ascomycota Associated with Bark Beetles
4.4. Domestication of Entomocorticium by Beetles Facilitated the Loss of Morphological Traits
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Species | Voucher (Extype) | Beetle Vector | Tree Host | Isolate Origin | Material Source | Reference |
---|---|---|---|---|---|---|
Entomocorticium belizense | 18050 (CBS 148421) | Dendroctonus frontalis | Pinus caribaea | Belize | Mycangium | This study |
18051 | Dendroctonus frontalis | Pinus caribaea | Belize | Mycangium | This study | |
Entomocorticium cobbii | B720 | Dendroctonus frontalis | Pinus taeda | Rapides Parish, LO, USA | Mycangium | Harrington et al. (2021) |
Entomocorticium dendroctoni | DAVFP 23165 | Dendroctonus ponderosae | Pinus ponderosa | British Columbia, Canada | Pupal Chamber | Whitney et al. (1987) |
Entomocorticium fibulatum | 17762 (CBS 148418) | Pityoborus comatus | Pinus elliotii | Miami-Dade, FL, USA | Mycangium | This study |
Entomocorticium perryae | UT16 (CBS 148419) | Dendroctonus brevicomis | Pinus ponderosa | Tropic, UT, USA | Mycangium | This study |
Entomocorticium kirisitsii | B1065 | Dendroctonus ponderosae | Pinus ponderosa | Estes Park, CO, USA | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium macrovesiculatum | PL6 | Dendroctonus brevicomis | Pinus ponderosa | Placerville, CA, USA | Mycangium | This study |
LF21 | Dendroctonus brevicomis | Pinus ponderosa | Greenough, MT, USA | Mycangium | This study, Bracewell and Six (2014) | |
CQ11 | Dendroctonus brevicomis | Pinus ponderosa | Chiloquim, OR, USA | Mycangium | This study, Bracewell and Six (2014) | |
MI17 | Dendroctonus brevicomis | Pinus ponderosa | Missoula, MT, USA | Mycangium | This study, Bracewell and Six (2014) | |
Ro10 | Dendroctonus brevicomis | Pinus ponderosa | Ruisoso, NM, USA | Mycangium | This study, Bracewell and Six (2014) | |
SB13 | Dendroctonus brevicomis | Pinus ponderosa | San Bernardino Mtns, CA, USA | Mycangium | This study, Bracewell and Six (2014) | |
MC16 (CBS 148421) | Dendroctonus brevicomis | Pinus ponderosa | McCloud, CA, USA | Mycangium | This study, Bracewell and Six (2014) | |
Entomocorticium oberwinkleri | B1053 | Dendroctonus ponderosae | Pinus contorta | Pilot Springs, CA, USA | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium parmeteri | B1503 | Dendroctonus brevicomis | Pinus ponderosa | Tuolumme County, CA, USA | Gallery | Harrington et al. (2021) |
Entomocorticium cf. perryae | 17783 (CBS 148417) | Dendroctonus frontalis | Pinus taeda | Gainesville, FL, USA | Mycangium | This study |
Entomocorticium portiae | B1039 | Dendroctonus ponderosae | Pinus lambertiana | Blodgett Res. Forest, CA, USA | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium portiae | B1060 | Dendroctonus ponderosae | Pinus contorta | San Bernardino Mts., CA, USA | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium sp. | MMF-4485 | Pitioborus comatus | Pinus ponderosa | Florida | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium sp. | 9470 | Pityoborus comatus | unknown | Gainesville, FL, USA | Mycangium | This study |
Entomocorticium sp. | 9576 | Pityoborus comatus | Pinus taeda | Gainesville, FL, USA | Mycangium | This study |
Entomocorticium sullivanii | B1252 | Ips avulsus | Pinus taeda | Athens, GA, USA | Pupal Chamber | Harrington et al. (2021) |
Entomocorticium whitneyi | B1069 | Dendroctonus ponderosae | Pinus ponderosa | Estes Park, CO, USA | Pupal Chamber | Harrington et al. (2021) |
Species | Host | Voucher | SSU | ITS | LSU | TEF | Citation |
---|---|---|---|---|---|---|---|
Entomocorticium belizense | Pinus caribaea | 18050 | – | MZ098132 | MZ098117 | – | This study |
18051 | – | MZ098133 | MZ098116 | – | This study | ||
Entomocorticium cobbii | Pinus taeda | B720 | – | MT741707 | MT741692 | – | Harrington et al. (2021) |
Entomocorticium fibulatum | Pinus elliottii | 17762 | MZ098147 | MZ098135 | MZ098120 | – | This study |
Entomocorticium perryae | Pinus ponderosa | UT16 | MZ098145 | MZ098123 | MZ098118 | MZ144591 | This study, Bracewell and Six (2014) |
Entomocorticium kirisitsii | Pinus ponderosa | B1065 | – | MT741714 | MT741699 | – | Harrington et al. (2021) |
Entomocorticium macrovesiculatum | Pinus ponderosa | MI17 | MZ098143 | MZ098129 | – | MZ144589 | This study, Bracewell and Six (2014) |
RO10 | MZ098149 | MZ098130 | MZ098108 | MZ144590 | This study, Bracewell and Six (2014) | ||
SB13 | MZ098141 | MZ098125 | MZ098110 | MZ144586 | This study, Bracewell and Six (2014) | ||
B1037 | MZ098138 | MZ098124 | MZ098109 | MZ144585 | This study, Bracewell and Six (2014) | ||
LF21 | MZ098139 | – | MZ098113 | MZ144587 | This study, Bracewell and Six (2014) | ||
PL6 | MZ098140 | MZ098126 | MZ098114 | MZ144588 | This study | ||
MC16 | MZ098144 | MZ098128 | MZ098112 | – | This study, Bracewell and Six (2014) | ||
CQ11 | MZ098142 | MZ098127 | MZ098111 | – | This study, Bracewell and Six (2014) | ||
Entomocorticium oberwinkleri | Pinus contorta | B1053 | – | MT741712 | MT741697 | – | Harrington et al. (2021) |
Entomocorticium parmeteri | Pinus ponderosa | B1503 | – | MT741709 | MT741694 | – | Harrington et al. (2021) |
Entomocorticium cf. perryae | Pinus taeda | 17783 | MZ098146 | MZ098131 | MZ098115 | MZ144592 | This study |
Entomocorticium portiae | Pinus lambertiana | B1039 | – | MT741710 | MT741695 | – | Harrington et al. (2021) |
Pinus contorta | B1045 | – | MT741711 | MT741696 | – | Harrington et al. (2021) | |
Entomocorticium sp. | Pinus taeda | 9576 | MZ098148 | MZ098134 | – | MZ144593 | This study |
Entomocorticium sp. | Pinus ponderosa | TSpCB896 | – | AF119510 | – | – | Harrington et al. (2021) |
Entomocorticium sullivanii | Pinus taeda | CBS 146270 | – | MT741715 | MT741700 | – | Harrington et al. (2021) |
Entomocorticum dendroctoni | Pinus contorta | DAVFP 23165 | – | AF119506 | – | – | Hsiau & Harrington (2003) |
Entomocorticum whitneyi | Pinus ponderosa | B1069 | – | MT741713 | MT741698 | – | Harrington et al. (2021) |
Peniophora albobadia | Angiosperms | CBS 329.66 | – | MH858809 | MH870448 | – | Andreasen & Hellenberg (2009) |
Peniophora aurantiaca | Alnus (Betulaceae) | – | – | Boidin (1994) | |||
Peniophora bicornis | Pentaclethra (Fabaceae), Musanga (Urticaceae), Anthocleista (Gentianaceae), Casuarina (Casuarinaceae), Acacia (Fabaceae), Acanthophoenyx (Areceae) | He4767 | – | MK588764 | MK588804 | – | Boidin et al. (1991) |
He3609 | – | MK588763 | MK588803 | – | Boidin et al. (1991) | ||
Peniophora borbonica | Hypericum (Hypericaceae), Acacia (Fabaceae), Fuchsia (Onagraceae) | He4597 | – | MK588766 | MK588806 | – | Boidin et al. (1991) |
He4606 | – | MK588765 | MK588805 | – | Boidin et al. (1991) | ||
Peniophora cinerea | “Angiosperms and Gymnosperms” | B1020 | – | MN475151 | MN475818 | – | Andreasen & Hellenberg (2009) |
Peniophora crassitunicata | Morinda (Rubiaceae), Schinus (Anacardiaceae), Casuarina (Casuarinaceae), Lantana (Verbenaceae), Tylophora (Apocynaceae), Acanthophoenyx (Arecaceae), Scaevola (Goodeniaceae) | CBS 663.91 | – | MH862292 | MH873972 | – | Boidin et al. (1991) |
Peniophora duplex | Gymnosperm “similar to P. pini/pseudo-pini” | CBS 286.58 | – | MH857787 | MH869321 | – | Andreasen & Hellenberg (2009) |
B1022 | – | MN475153 | MN475820 | – | Andreasen & Hellenberg (2009) | ||
Peniophora eriksonii | Alnus glutinosa (Betulaceae) | CBS 287.58 | – | MH857788 | MH869322 | – | Boidin (1994) |
Cui11871 | – | MK588771 | MK588811 | – | Boidin (1994) | ||
Peniophora exima | Abies (Pinaceae) | B1012 | – | MN475159 | MN475826 | – | Boidin (1994) |
B1011 | – | MN475155 | MN475821 | – | Boidin (1994) | ||
T523 | – | MK588772 | MK588812 | – | Boidin (1994) | ||
Peniophora fasticata | Angiosperms | CBS 942.96 | – | MH862624 | – | – | Andreasen & Hellenberg (2009) |
Peniophora fissilis | Cryptomeria (Cupressaceae), Lantana (Verbenaceae) | CBS 681.91 | MZ233430 | MH862298 | MH873975 | – | Boidin et al. (1991) |
CBS 684.91 | MZ233431 | MH862299 | MH873976 | – | Boidin et al. (1991) | ||
Peniophora gabonensis | Pandanus (Pandanaceae) | CBS 673.91 | – | MH862293 | – | – | Andreasen & Hellenberg (2009) |
Peniophora gilbertsonii | Prosopis juriflora (Fabaceae), Baccharis (Asteraceae), Cercidium (Fabaceae), Condalia (Rhamnaceae), Fouquieria (Fouquieraceae) | CBS 357.95 | – | MH862528 | MH874164 | – | Boidin et al. (1991) |
CBS 360.95 | – | MH862530 | MH874165 | – | Boidin et al. (1991) | ||
Peniophora guadelupensis | Leguminosae | CBS 715.91 | – | MH862304 | MH873977 | – | Andreasen & Hellenberg (2009) |
Peniophora halimi | Atriplex (Amaranthaceae) | CBS 862.84 | – | MH861843 | MH873531 | – | Andreasen & Hellenberg (2009) |
CBS 860.84 | – | MH861842 | MH873530 | – | Andreasen & Hellenberg (2009) | ||
Peniophora incarnata | On angiosperms, rarely on Gymnosperms | B1016 | – | MN475156 | MN475822 | – | Andreasen & Hellenberg (2009) |
CBS 430.72 | – | MH860518 | MH872230 | – | Andreasen & Hellenberg (2009) | ||
AF506425 | – | AF506425 | – | – | Andreasen & Hellenberg (2009) | ||
NH10271 | – | AF506425 | – | – | Andreasen & Hellenberg (2009) | ||
Peniophora junipericola | Juniperus | He2462 | – | MK588773 | MK588813 | – | Boidin (1994) |
Peniophora laeta | Carpinus (Betulaceae), Ostrya (Betulaceae) | CBS 256.56 | – | MH857617 | MH869165 | – | Andreasen & Hellenberg (2009) |
CBS 255.56 | – | MH857616 | MH869164 | – | Andreasen & Hellenberg (2009) | ||
Peniophora laurentii | Populus (Salicaceae), Betula (Betulaceae), Salix (Salicaceae) | CBS 325.73 | – | – | MH872397 | – | Boidin (1994) |
Peniophora laxitexta | Angiosperms | BAFC 3309 | – | FJ882040 | – | – | Andreasen & Hellenberg (2009) |
LGMF1159 | – | JX559580 | – | – | Andreasen & Hellenberg (2009) | ||
BAFC 4687 | – | MN518328 | – | – | Andreasen & Hellenberg (2009) | ||
Peniophora lilacea | Celtis (Cannabaceae), Staphylea (Staphyleaceae), Alnus (Betulaceae), Gleditsia (Fabaceae), Fraxinus (Olaceae) | CBS 337.66 | – | MH858813 | MH870452 | – | Boidin (1994) |
CBS 337.66 | – | MH858813 | MH870452 | – | Boidin (1994) | ||
Peniophora limitata | Fraximus, Syringa, Ligustrum, Phillyrea | CLZhao 5716 | – | MK269148 | – | – | Boidin (1994) |
Peniophora lycii | Unkonwn | CBS 264.56 | – | MH857624 | MH869169 | – | Andreasen & Hellenberg (2009) |
CBS 261.56 | – | MH857621 | MH869167 | – | Andreasen & Hellenberg (2009) | ||
CBS 352.54 | – | MH857357 | MH868899 | – | Andreasen & Hellenberg (2009) | ||
Peniophora malaiensis | Calophyllum (Calophyllaceae) | CBS 679.91 | – | MH862297 | MH873974 | – | Andreasen & Hellenberg (2009) |
He4870 | – | MK588775 | MK588815 | – | Andreasen & Hellenberg (2009) | ||
Peniophora manshurica | Quercus (Fagaceae) | He2956 | – | MK588776 | MK588816 | – | Andreasen and Hellenberg (2009) |
He3729 | – | MK588777 | MK588817 | – | |||
Peniophora meridionalis | Quercus, Cistus (Cistaceae), Lentiscus, Eucalyptus (Myrtaceae), Erica (Ericaceae) | CBS 289.58 | – | MH857789 | MH869323 | – | Boidin et al. (1991) |
Peniophora molesta | Unknown | CBS 678.91 | – | MH862296 | – | – | Andreasen & Hellenberg (2009) |
CBS 677.91 | – | MH862295 | – | – | Andreasen & Hellenberg (2009) | ||
CBS 676.91 | – | MH862294 | MH873973 | – | Andreasen & Hellenberg (2009) | ||
Peniophora monticola | Hypericum (Hypericaceae), Dombeya (Malvaceae) | CBS 649.91 | – | MH862289 | MH873970 | – | Boidin et al. (1991) |
Peniophora nuda | Angiosperms, rarely Gymnosperms | AFTOL_ID_660 | – | DQ411533 | DQ435788 | – | Andreasen & Hellenberg (2009) |
Peniophora ovalispora | Acacia (Acaciae), Cryptomeria (Cupressaceae), Fuchsia (Onagraceae), Solanum (Solanaceae), Cyathea (Fern) | CBS 653.91 | – | MH862290 | MH873971 | – | Boidin et al. (1991) |
Peniophora parvocystidiata | Pinus (Pinaceae) | CBS 716.91 | – | MH862305 | MH873978 | – | Andreasen & Hellenberg (2009) |
CBS 717.91 | – | MH862306 | MH873979 | – | Andreasen & Hellenberg (2009) | ||
Peniophora piceae | Abies, Pseudotsuga (Pinaceae) | B1010 | – | MN475158 | MN475825 | – | Boidin (1994) |
B1009 | – | MN475157 | MN475824 | – | Boidin (1994) | ||
Peniophora pilatiana | Quercus, Cistus, Nerium, Vitis, Prunus, Pistacia, Olea, Rhammus, Salix, Eucalyptus, Ilex | CBS 269.56 | – | MH857627 | MH869172 | – | Boidin (1994) |
CBS 265.56 | – | MH857625 | MH869170 | – | Boidin (1994) | ||
CBS 266.56 | – | MH857626 | MH869171 | – | Boidin (1994) | ||
Peniophora pini | Pinus sylvestris (Pinaceae) | CBS 272.56 | – | CBS 272.56 | MH869175 | – | Gibson (1960) |
CBS 273.56 | – | MH857631 | MH869176 | – | Gibson (1960) | ||
CBS 270.56 | – | MH857628 | MH869173 | – | Gibson (1960) | ||
CBS 274.56 | – | MH857632 | MH869177 | – | Gibson (1960) | ||
CBS 414.34 | – | MH855589 | MH867099 | – | Gibson (1960) | ||
Peniophora pithya | On Gymnosperms (Pinaceae), rarely on Salix | CBS 276.56 | MZ233428 | MH857634 | MH869179 | – | Boidin et al. (1991) |
B1013 | – | MN475160 | MN475827 | – | |||
CBS 275.56 | MZ233427 | MH857633 | MH869178 | – | |||
Peniophora polygonia | Populus (Salicaceae) | He3668 | – | MH669233 | MH669237 | – | Boidin (1994) |
CBS 404.50 | – | MH856684 | MH868201 | – | Boidin (1994) | ||
Peniophora proxima | Buxus (Buxaceae) | CBS 406.50 | – | MH856686 | MH868203 | – | Boidin (1994) |
CBS 405.50 | – | MH856685 | MH868202 | – | |||
Peniophora pseudo-pini | Pinus, Abies, Pseudotsuga | B1025 | – | MN475164 | MN475830 | – | Gibson (1960) |
DAOM-30124 | – | MK588784 | MK588824 | – | Gibson (1960) | ||
B1024 | – | MN475163 | MN475829 | – | Gibson (1960) | ||
B1007 | – | MN475162 | MN475828 | – | Gibson (1960) | ||
Peniophora pseudonuda | Quercus, Fagus (Fagaceae) | FCUG 2384 | – | GU322866 | – | – | Boidin (1994) |
FCUG 2390 | – | GU322865 | – | – | Boidin (1994) | ||
FCUG 86 | – | GU322867 | – | – | Boidin (1994) | ||
Peniophora pseudoversicolor | Quercus (Fagaceae) | CBS 125881 | – | MH864303 | MH875753 | – | Boidin (1994) |
CBS 338.66 | – | MH858814 | MH870453 | – | Boidin (1994) | ||
Peniophora quercina | Betula, Castanea, Fagus, Salix | CBS 409.50 | – | MH856689 | MH868206 | – | Boidin (1994) |
CBS 408.50 | – | MH856688 | MH868205 | – | Boidin (1994) | ||
CBS 407.50 | – | MH856687 | MH868204 | – | Boidin (1994) | ||
Peniophora reidii | Quercus (Fagaceae), Laurus, Betula, Salix, Fagus, Eucalyptus | CBS 397.83 | – | MH861616 | MH873334 | – | Boidin (1994) |
Peniophora rufa | Populus tremuloides (Salicaceae) | CBS 351.59 | – | MH857891 | MH869432 | – | Chamuris & Falk (198) |
B1014 | – | MN475165 | MN475831 | – | Chamuris & Falk (198) | ||
Peniophora rufomarginata | Quercus, Populus, Tilia and Arbutrus (Ericaceae) | CBS 282.56 | – | MH857640 | MH869184 | – | Andreasen & Hellenberg (2009) |
CBS 281.56 | – | MH857639 | MH869183 | – | Andreasen & Hellenberg (2009) | ||
Peniophora septentrionalis | Picea, Abies (Pinaceae) | CBS 294.58 | MZ233429 | MH857791 | MH869325 | – | Andreasen & Hellenberg (2009) |
Peniophora simulans | Fagus | CBS 875.84 | – | MH861850 | MH873538 | – | Reid (1969) |
CBS 874.84 | – | MH861849 | MH873537 | – | Reid (1969) | ||
Peniophora subsalmonea | Mimosaceae | CBS 697.91 | – | MH862303 | – | – | Andreasen & Hellenberg (2009) |
CBS 696.91 | – | MH862302 | – | – | Andreasen & Hellenberg (2009) | ||
Peniophora taiwanensis | Angisosperms | Wu 9206 28 | – | MK588793 | MK588833 | – | Andreasen & Hellenberg (2009) |
Wu 9209 14 | – | MK588794 | MK588834 | – | Andreasen & Hellenberg (2009) | ||
Peniophora tamaricicola | Tamarix (Tamaricaceae) | CBS 439.62 | – | MH858204 | MH869803 | – | Gilbertson (1975) |
CBS 441.62 | – | MH858205 | MH869804 | – | Gilbertson (1975) | ||
CBS 438.62 | – | MH858203 | MH869802 | – | Gilbertson (1975) | ||
Peniophora versicolor | Salix (Salicaceae), Acer (Sapindaceae), Ostrya (Betulaceae), Celtis (Cannabaceae), Robinia (Fabaceae) and Ceratonia (Fabaceae) | CBS 358.61 | – | MH858082 | MH869651 | – | Boidin (1994) |
Peniophora violaceolivida | Salicaceae, rarely on “Gymnosperms” | CBS 348.52 | – | MH857077 | MH868613 | – | Andreasen & Hellenberg (2009) |
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Araújo, J.P.M.; Li, Y.; Six, D.; Rajchenberg, M.; Smith, M.E.; Johnson, A.J.; Klepzig, K.D.; Crous, P.W.; Leal-Dutra, C.A.; Skelton, J.; et al. Diversity and Evolution of Entomocorticium (Russulales, Peniophoraceae), a Genus of Bark Beetle Mutualists Derived from Free-Living, Wood Rotting Peniophora. J. Fungi 2021, 7, 1043. https://doi.org/10.3390/jof7121043
Araújo JPM, Li Y, Six D, Rajchenberg M, Smith ME, Johnson AJ, Klepzig KD, Crous PW, Leal-Dutra CA, Skelton J, et al. Diversity and Evolution of Entomocorticium (Russulales, Peniophoraceae), a Genus of Bark Beetle Mutualists Derived from Free-Living, Wood Rotting Peniophora. Journal of Fungi. 2021; 7(12):1043. https://doi.org/10.3390/jof7121043
Chicago/Turabian StyleAraújo, João P. M., You Li, Diana Six, Mario Rajchenberg, Matthew E. Smith, Andrew J. Johnson, Kier D. Klepzig, Pedro W. Crous, Caio A. Leal-Dutra, James Skelton, and et al. 2021. "Diversity and Evolution of Entomocorticium (Russulales, Peniophoraceae), a Genus of Bark Beetle Mutualists Derived from Free-Living, Wood Rotting Peniophora" Journal of Fungi 7, no. 12: 1043. https://doi.org/10.3390/jof7121043