Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae

Abstract Background Achlorophyllous orchids are mycoheterotrophic plants, which lack photosynthetic ability and associate with fungi to acquire carbon from different environmental sources. In tropical latitudes, achlorophyllous forest orchids show a preference to establish mycorrhizal relationships...

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Main Authors: Lorenzo Pecoraro, Xiao Wang, Giuseppe Venturella, Wenyuan Gao, Tingchi Wen, Yusufjon Gafforov, Vijai Kumar Gupta
Format: Article
Language:English
Published: BMC 2020-08-01
Series:BMC Microbiology
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Online Access:http://link.springer.com/article/10.1186/s12866-020-01906-4
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author Lorenzo Pecoraro
Xiao Wang
Giuseppe Venturella
Wenyuan Gao
Tingchi Wen
Yusufjon Gafforov
Vijai Kumar Gupta
author_facet Lorenzo Pecoraro
Xiao Wang
Giuseppe Venturella
Wenyuan Gao
Tingchi Wen
Yusufjon Gafforov
Vijai Kumar Gupta
author_sort Lorenzo Pecoraro
collection DOAJ
description Abstract Background Achlorophyllous orchids are mycoheterotrophic plants, which lack photosynthetic ability and associate with fungi to acquire carbon from different environmental sources. In tropical latitudes, achlorophyllous forest orchids show a preference to establish mycorrhizal relationships with saprotrophic fungi. However, a few of them have been recently found to associate with ectomycorrhizal fungi and there is still much to be learned about the identity of fungi associated with tropical orchids. The present study focused on mycorrhizal diversity in the achlorophyllous orchid C. inverta, an endangered species, which is endemic to southern China. The aim of this work was to identify the main mycorrhizal partners of C. inverta in different plant life stages, by means of morphological and molecular methods. Results Microscopy showed that the roots of analysed C. inverta samples were extensively colonized by fungal hyphae forming pelotons in root cortical cells. Fungal ITS regions were amplified by polymerase chain reaction, from DNA extracted from fungal mycelia isolated from orchid root samples, as well as from total root DNA. Molecular sequencing and phylogenetic analyses showed that the investigated orchid primarily associated with ectomycorrhizal fungi belonging to a narrow clade within the family Ceratobasidiaceae, which was previously detected in a few fully mycoheterotrophic orchids and was also found to show ectomycorrhizal capability on trees and shrubs. Russulaceae fungal symbionts, showing high similarity with members of the ectomycorrhizal genus Russula, were also identified from the roots of C. inverta, at young seedling stage. Ascomycetous fungi including Chaetomium, Diaporthe, Leptodontidium, and Phomopsis genera, and zygomycetes in the genus Mortierella were obtained from orchid root isolated strains with unclear functional role. Conclusions This study represents the first assessment of root fungal diversity in the rare, cryptic and narrowly distributed Chinese orchid C. inverta. Our results provide new insights on the spectrum of orchid-fungus symbiosis suggesting an unprecedented mixed association between the studied achlorophyllous forest orchid and ectomycorrhizal fungi belonging to Ceratobasidiaceae and Russulaceae. Ceratobasidioid fungi as dominant associates in the roots of C. inverta represent a new record of the rare association between the identified fungal group and fully mycoheterotrophic orchids in nature.
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spelling doaj.art-b9f292f0093f474992c968ff0e82f20f2022-12-22T03:01:57ZengBMCBMC Microbiology1471-21802020-08-0120111310.1186/s12866-020-01906-4Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and RussulaceaeLorenzo Pecoraro0Xiao Wang1Giuseppe Venturella2Wenyuan Gao3Tingchi Wen4Yusufjon Gafforov5Vijai Kumar Gupta6School of Pharmaceutical Science and Technology, Health Sciences Platform, Tianjin UniversitySchool of Pharmaceutical Science and Technology, Health Sciences Platform, Tianjin UniversityDepartment of Agricultural, Food and Forest Sciences, University of PalermoSchool of Pharmaceutical Science and Technology, Health Sciences Platform, Tianjin UniversityThe Engineering Research Center of Southwest Bio-Pharmaceutical Resources, Ministry of Education, Guizhou UniversityLaboratory of Mycology, Institute of Botany, Academy of Sciences of UzbekistanAgroBioSciences and Chemical & Biochemical Sciences Department, University Mohammed VI PolytechnicAbstract Background Achlorophyllous orchids are mycoheterotrophic plants, which lack photosynthetic ability and associate with fungi to acquire carbon from different environmental sources. In tropical latitudes, achlorophyllous forest orchids show a preference to establish mycorrhizal relationships with saprotrophic fungi. However, a few of them have been recently found to associate with ectomycorrhizal fungi and there is still much to be learned about the identity of fungi associated with tropical orchids. The present study focused on mycorrhizal diversity in the achlorophyllous orchid C. inverta, an endangered species, which is endemic to southern China. The aim of this work was to identify the main mycorrhizal partners of C. inverta in different plant life stages, by means of morphological and molecular methods. Results Microscopy showed that the roots of analysed C. inverta samples were extensively colonized by fungal hyphae forming pelotons in root cortical cells. Fungal ITS regions were amplified by polymerase chain reaction, from DNA extracted from fungal mycelia isolated from orchid root samples, as well as from total root DNA. Molecular sequencing and phylogenetic analyses showed that the investigated orchid primarily associated with ectomycorrhizal fungi belonging to a narrow clade within the family Ceratobasidiaceae, which was previously detected in a few fully mycoheterotrophic orchids and was also found to show ectomycorrhizal capability on trees and shrubs. Russulaceae fungal symbionts, showing high similarity with members of the ectomycorrhizal genus Russula, were also identified from the roots of C. inverta, at young seedling stage. Ascomycetous fungi including Chaetomium, Diaporthe, Leptodontidium, and Phomopsis genera, and zygomycetes in the genus Mortierella were obtained from orchid root isolated strains with unclear functional role. Conclusions This study represents the first assessment of root fungal diversity in the rare, cryptic and narrowly distributed Chinese orchid C. inverta. Our results provide new insights on the spectrum of orchid-fungus symbiosis suggesting an unprecedented mixed association between the studied achlorophyllous forest orchid and ectomycorrhizal fungi belonging to Ceratobasidiaceae and Russulaceae. Ceratobasidioid fungi as dominant associates in the roots of C. inverta represent a new record of the rare association between the identified fungal group and fully mycoheterotrophic orchids in nature.http://link.springer.com/article/10.1186/s12866-020-01906-4Achlorophyllous orchidsCeratobasidiaceaeEctomycorrhizal fungiEndangered speciesOrchid mycorrhizaPlant-fungus interactions
spellingShingle Lorenzo Pecoraro
Xiao Wang
Giuseppe Venturella
Wenyuan Gao
Tingchi Wen
Yusufjon Gafforov
Vijai Kumar Gupta
Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
BMC Microbiology
Achlorophyllous orchids
Ceratobasidiaceae
Ectomycorrhizal fungi
Endangered species
Orchid mycorrhiza
Plant-fungus interactions
title Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
title_full Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
title_fullStr Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
title_full_unstemmed Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
title_short Molecular evidence supports simultaneous association of the achlorophyllous orchid Chamaegastrodia inverta with ectomycorrhizal Ceratobasidiaceae and Russulaceae
title_sort molecular evidence supports simultaneous association of the achlorophyllous orchid chamaegastrodia inverta with ectomycorrhizal ceratobasidiaceae and russulaceae
topic Achlorophyllous orchids
Ceratobasidiaceae
Ectomycorrhizal fungi
Endangered species
Orchid mycorrhiza
Plant-fungus interactions
url http://link.springer.com/article/10.1186/s12866-020-01906-4
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