Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia

Rafflesia, known for producing the world’s largest flowers, is a holoparasite found only in Southeast Asia's rapidly diminishing tropical forests. Completely dependent on its Tetrastigma host plants, Rafflesia grows covertly within its host until flowering, but the ecological factors driving ho...

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Main Authors: Jeanmaire Molina, Roche C. de Guzman, Rinat Abzalimov, Wenkai Huang, Anusha Guruprasad, Ronniel Pedales, Adhityo Wicaksono, Destiny Davis, John Rey Callado, Hans Bänziger, Piyakaset Suksathan, William Eaton, Pride Yin, Marco Bürger, Mick Erickson, Stephen Jones, James Adams, Susan Pell
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Current Plant Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2214662825000246
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author Jeanmaire Molina
Roche C. de Guzman
Rinat Abzalimov
Wenkai Huang
Anusha Guruprasad
Ronniel Pedales
Adhityo Wicaksono
Destiny Davis
John Rey Callado
Hans Bänziger
Piyakaset Suksathan
William Eaton
Pride Yin
Marco Bürger
Mick Erickson
Stephen Jones
James Adams
Susan Pell
author_facet Jeanmaire Molina
Roche C. de Guzman
Rinat Abzalimov
Wenkai Huang
Anusha Guruprasad
Ronniel Pedales
Adhityo Wicaksono
Destiny Davis
John Rey Callado
Hans Bänziger
Piyakaset Suksathan
William Eaton
Pride Yin
Marco Bürger
Mick Erickson
Stephen Jones
James Adams
Susan Pell
author_sort Jeanmaire Molina
collection DOAJ
description Rafflesia, known for producing the world’s largest flowers, is a holoparasite found only in Southeast Asia's rapidly diminishing tropical forests. Completely dependent on its Tetrastigma host plants, Rafflesia grows covertly within its host until flowering, but the ecological factors driving host susceptibility are unknown. With most Rafflesia species on the brink of extinction due to habitat loss, understanding the complex ecological interactions between Rafflesia and its host is crucial for conservation. In this study, we integrated metagenomic data with metabolomic profiles to identify potential functional relationships between microbial communities and specific metabolites, shedding light on their ecological roles in Rafflesia's life cycle. Key findings reveal that microbial taxa such as Microbacteriaceae and Nocardioidaceae correlate with elevated levels of polyphenols, particularly gallic acid derivatives, which may shape the chemical environment conducive to Rafflesia development. Complex-carbon-degrading bacteria thrive in the chemically distinct environment of Rafflesia buds, while an unknown group of Saccharimonadales was enriched in Tetrastigma host species. Docosenamide production in Rafflesia buds and their hosts may facilitate parasitic infection, while coumarin compounds in non-host Tetrastigma species may exert allelopathic effects. The enrichment of gallic acid derivatives, the phytohormone adenine, and gall-associated bacteria suggests that Rafflesia buds may function similarly to plant galls, manipulating host tissues to support their reproductive development. This study highlights the dynamic microbial shifts during Rafflesia’s development, emphasizing its symbiotic relationship with microbial communities and hosts. In identifying essential microbial and chemical conditions that could improve propagation techniques, this research has practical applications in ex situ conservation efforts, aiding in the rescue of the world’s largest flowers from the brink of extinction.
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spelling doaj-art-4928224fa35f491385a61e51271450e82025-02-08T05:00:30ZengElsevierCurrent Plant Biology2214-66282025-06-0142100456Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, RafflesiaJeanmaire Molina0Roche C. de Guzman1Rinat Abzalimov2Wenkai Huang3Anusha Guruprasad4Ronniel Pedales5Adhityo Wicaksono6Destiny Davis7John Rey Callado8Hans Bänziger9Piyakaset Suksathan10William Eaton11Pride Yin12Marco Bürger13Mick Erickson14Stephen Jones15James Adams16Susan Pell17Biology Department, Pace University, New York, NY, USA; Corresponding author.Bioengineering Program, Department of Engineering, Hofstra University, Hempstead, NY, USABiomolecular Mass Spectrometry Facility, Advanced Science Research Center, City University of New York, New York, NY, USABiology Department, Pace University, New York, NY, USABiology Department, Pace University, New York, NY, USAInstitute of Biology, University of the Philippines, Diliman, Quezon 1101, PhilippinesGenomik Solidaritas Indonesia (GSI) Lab, Jl. Sultan Agung No.29, Setiabudi, Jakarta 12980, IndonesiaUS Botanic Garden, Washington, DC, USADepartment of Science and Technology-Forest Products Research and Development Institute, Laguna, PhilippinesDepartment of Entomology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, ThailandHerbarium (QBG), Queen Sirikit Botanic Garden, P.O. Box 7, Mae Rim, Chiang Mai 50180, ThailandBiology Department, Pace University, New York, NY, USABiology Department, Pace University, New York, NY, USAPlant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, CA, USA; Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, CA, USAUS Botanic Garden, Washington, DC, USAUS Botanic Garden, Washington, DC, USAUS Botanic Garden, Washington, DC, USAUS Botanic Garden, Washington, DC, USARafflesia, known for producing the world’s largest flowers, is a holoparasite found only in Southeast Asia's rapidly diminishing tropical forests. Completely dependent on its Tetrastigma host plants, Rafflesia grows covertly within its host until flowering, but the ecological factors driving host susceptibility are unknown. With most Rafflesia species on the brink of extinction due to habitat loss, understanding the complex ecological interactions between Rafflesia and its host is crucial for conservation. In this study, we integrated metagenomic data with metabolomic profiles to identify potential functional relationships between microbial communities and specific metabolites, shedding light on their ecological roles in Rafflesia's life cycle. Key findings reveal that microbial taxa such as Microbacteriaceae and Nocardioidaceae correlate with elevated levels of polyphenols, particularly gallic acid derivatives, which may shape the chemical environment conducive to Rafflesia development. Complex-carbon-degrading bacteria thrive in the chemically distinct environment of Rafflesia buds, while an unknown group of Saccharimonadales was enriched in Tetrastigma host species. Docosenamide production in Rafflesia buds and their hosts may facilitate parasitic infection, while coumarin compounds in non-host Tetrastigma species may exert allelopathic effects. The enrichment of gallic acid derivatives, the phytohormone adenine, and gall-associated bacteria suggests that Rafflesia buds may function similarly to plant galls, manipulating host tissues to support their reproductive development. This study highlights the dynamic microbial shifts during Rafflesia’s development, emphasizing its symbiotic relationship with microbial communities and hosts. In identifying essential microbial and chemical conditions that could improve propagation techniques, this research has practical applications in ex situ conservation efforts, aiding in the rescue of the world’s largest flowers from the brink of extinction.http://www.sciencedirect.com/science/article/pii/S2214662825000246SapriaEndophyteHoloparasiteMetagenomicsSymbiosis
spellingShingle Jeanmaire Molina
Roche C. de Guzman
Rinat Abzalimov
Wenkai Huang
Anusha Guruprasad
Ronniel Pedales
Adhityo Wicaksono
Destiny Davis
John Rey Callado
Hans Bänziger
Piyakaset Suksathan
William Eaton
Pride Yin
Marco Bürger
Mick Erickson
Stephen Jones
James Adams
Susan Pell
Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
Current Plant Biology
Sapria
Endophyte
Holoparasite
Metagenomics
Symbiosis
title Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
title_full Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
title_fullStr Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
title_full_unstemmed Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
title_short Microbes and metabolites of a plant-parasite interaction: Deciphering the ecology of Tetrastigma host choice in the world’s largest parasitic flower, Rafflesia
title_sort microbes and metabolites of a plant parasite interaction deciphering the ecology of tetrastigma host choice in the world s largest parasitic flower rafflesia
topic Sapria
Endophyte
Holoparasite
Metagenomics
Symbiosis
url http://www.sciencedirect.com/science/article/pii/S2214662825000246
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