Award Abstract # 1456958
Collaborative Research: Functional and evolutionary bases of substrate-specificity in wood-decaying basidiomycetes

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: REGENTS OF THE UNIVERSITY OF CALIFORNIA, THE
Initial Amendment Date: March 18, 2015
Latest Amendment Date: March 18, 2015
Award Number: 1456958
Award Instrument: Standard Grant
Program Manager: Irwin Forseth
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: April 1, 2015
End Date: March 31, 2020 (Estimated)
Total Intended Award Amount: $221,870.00
Total Awarded Amount to Date: $221,870.00
Funds Obligated to Date: FY 2015 = $221,870.00
History of Investigator:
  • Igor Grigoriev (Principal Investigator)
    ivgrigoriev@lbl.gov
Recipient Sponsored Research Office: University of California-Berkeley
1608 4TH ST STE 201
BERKELEY
CA  US  94710-1749
(510)643-3891
Sponsor Congressional District: 12
Primary Place of Performance: JOINT GENOME INSTITUTE
2800 Mitchell Drive
Walnut Creek
CA  US  94598-1698
Primary Place of Performance
Congressional District:
10
Unique Entity Identifier (UEI): GS3YEVSS12N6
Parent UEI:
NSF Program(s): Integrtv Ecological Physiology
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 9178, 9179
Program Element Code(s): 765700
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Wood (lignocellulose) is one of the most abundant carbon pools in terrestrial ecosystems. Fungal decomposition of wood is a critical component of the carbon cycle, impacts soil productivity, and has the potential to be exploited in the production of biofuels and other 'green' technologies. The major wood-decaying fungi are mushroom-forming (Agaricomycetes). The physical characteristics and chemical composition of wood vary among plant species, and most wood-decaying Agaricomycetes have characteristic wood substrate ranges. However, it is not understood why individual species of wood decaying fungi tend to occur on specific plant hosts. This project will investigate the mechanisms of substrate specificity and substrate switching in wood-decaying Agaricomycetes using a combination of analyses of genes expressed during decay, and physical and chemical characterization of the decay process. Fungal enzymes that are involved in wood decay or degradation have potential applications in emerging bioprocesses, such as energy-related bioconversions, including biofuel production, and bioremediation. Enhanced understanding of the mechanisms that allow different species of fungi to exploit particular wood substrates could help guide development of genetic resources that could be used for such applied purposes. This project will support one Postdoctoral Fellow and two graduate students, and will provide training to undergraduates at three collaborating academic institutions in the US. To bring information about fungi and wood decomposition to a wide audience, this project will create interactive exhibits and develop accompanying public programs at the Worcester EcoTarium (http://www.ecotarium.org/), a science and nature museum which serves over 140,000 visitors annually including large numbers of students from regional public schools. Exhibits will illustrate fungal diversity, the decay process, and the role of fungi in the carbon cycle.

The proposed research will focus on four species of Agaricomycetes (with distinct substrate preferences) with available genome sequences. The fungi will be cultured on solid wafers of four different tree species (two conifers and two hardwoods). Transcriptome profiling will be performed with the Illumina HiSeq 2000 platform, focusing on genes encoding enzymes known or suspected to be involved in wood decay, as well as co-expressed genes of unknown function. Phylogenomic analyses will make use of all available genomes of wood-decaying Agaricomycetes, focusing on gene families that are likely to play a role in decay, as informed by expression profiles. Physical and chemical characteristics of decay will be addressed using microscopy, mass spectrometry, and chemical analyses of colonized substrates. The proposed research is a collaboration between researchers with expertise in fungal systematics and molecular evolution, wood decay and forest products pathology, fungal genomics, and genetics and biochemistry of decay systems. This project will capitalize on recent advances in genomics of wood-decaying basidiomycetes. It will provide insight into the functioning and evolution of fungi in forest ecosystems, and create a framework for future studies aimed at understanding the specific plant-derived compounds that affect expression of particular fungal genes.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Balasundaram SV, Hess J, Durling MB, Moody SC, Thorbek L, Progida C, LaButti K, Aerts A, Barry K, Grigoriev IV, Boddy L, Högberg N, Kauserud H, Eastwood DC, Skrede I. "The fungus that came in from the cold: dry rot's pre-adapted ability to invade buildings." ISME J. , v.12 , 2018 , p.791 10.1038/s41396-017-0006-8
Castanera R, Pérez G, López-Varas L, Amselem J, LaButti K, Singan V, Lipzen A, Haridas S, Barry K, Grigoriev IV, Pisabarro AG, Ramírez L. "Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales." BMC Genomics , v.18 , 2017 , p.883 10.1186/s12864-017-4243-z
Gaskell J, Kersten P, Larrondo LF, Canessa P, Martinez D, Hibbett D, Schmoll M, Kubicek CP, Martinez AT, Yadav J, Master E, Magnuson JK, Yaver D, Berka R, Lail K, Chen C, LaButti K, Nolan M, Lipzen A, Aerts A, Riley R, Barry K, Henrissat B, Blanchette R, "Draft genome sequence of a monokaryotic model brown-rot fungus Postia (Rhodonia) placenta SB12." Genom Data , v.14 , 2017 , p.21 10.1016/j.gdata.2017.08.003
Nagy LG, Riley R, Tritt A, Adam C, Daum C, Floudas D, Sun H, Yadav JS, Pangilinan J, Larsson KH, Matsuura K, Barry K, Labutti K, Kuo R, Ohm RA, Bhattacharya SS, Shirouzu T, Yoshinaga Y, Martin FM, Grigoriev IV, Hibbett DS. "Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities." Molecular Biology and Evolution. , v.33 , 2016 , p.959 10.1093/molbev/msv337
Nagy L, Riley R, Bergmann PJ, Krizsán K, Martin FM, Grigoriev IV, Cullen D and Hibbett DS "Genetic Bases of Fungal White Rot Wood Decay Predicted by Phylogenomic Analysis of Correlated Gene-Phenotype Evolution." Molecular Biology and Evolution. , v.34 , 2017 , p.35 10.1093/molbev/msw238
Wu, Baojun, Jill Gaskell, Benjamin Held, Cristina Toapanta, Thu Vuong, Steven Ahrendt, Anna Lipzen, Jiwei Zhang, Jonathan Schilling, Emma Master, Igor Grigoriev, Robert Blanchette, Daniel Cullen, and David Hibbett "Substrate-Specific Differential Gene Expression and RNA editing in the Brown Rot Fungus Fomitopsis pinicola." Applied and Environmental Microbiology. , v.84 , 2018 , p.e00991 10.1128/AEM.00991-18
Wu, Baojun, Jill Gaskell, Jiwei Zhang, Cristina Toapanta, Steven Ahrendt, Igor V. Grigoriev, Robert Blanchette, Jonathan Schilling, Emma Master, Daniel Cullen, and David Hibbett "Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi." ISME Journal , v.13 , 2019 , p.1391 10.1128/AEM.00991-18

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

OVERVIEW
Wood, the tough, durable material that is used to make everything from houses to chopsticks, is a major reservoir of carbon in the global ecosystem. The task of recycling this carbon falls largely to fungi, especially Agaricomycetes, which includes polypores, gilled mushrooms, puffballs, and coral fungi. Wood decaying Agaricomycetes tend to occur on specific tree species and to specialize on different classes of wood (e.g., live vs. dead trees, massive logs vs. twigs, aerial limbs vs. roots and stumps, and so on). In recent years, through advances in genomics and biochemistry, we have learned a great deal about how Agaricomycetes decay wood. We have cataloged diverse enzymes that break down the components of wood, and identified their genes. However, we still know very little about why wood decaying Agaricomycetes occur on specific substrates. This project leveraged recent advances in fungal genomics and evolutionary biology to address the causes of substrate-specificity in wood decaying Agaricomycetes.
INTELLECTUAL MERIT
We grew selected species of Agaricomycetes on different types of wood, and studied gene expression. Our main goal was to determine if wood decaying Agaricomycetes can adjust the suite of enzymes that they produce in response to different substrates. We also used mass spectrometry to study changes in wood chemistry during decay, and we studied the evolution of wood decay and other nutritional modes in Agaricomycetes. This was a collaborative project involving four laboratories at Clark University, the University of Toronto, University of Minnesota, and the University of California Berkeley. We also collaborated with colleagues at the USDA Forest Products laboratory in Madison, Wisconsin.
So far, we have published nine articles reporting the results of this project (as of this writing, three more are in review). We conducted two major studies, one in the "red belt polypore" Fomitopis pinicola, and another that compared five different species. In both, we found that wood-decaying Agaricomycetes are able to modify gene expression according to substrate type. We also performed several evolutionary analyses that provided a broad view of the origins of decay mechanisms, and how those mechanisms have changed over geologic time. 
BROADER IMPACTS
This project served to develop and strengthen professional networks involving four universities (three public, one private) and a federal research laboratory, in two countries. Trainees who were supported included postdoctoral fellows, graduate students, and undergraduates.
The major outreach component of this project involved creation of exhibits on fungal biology (emphasizing decay) and evolution at the EcoTarium in Worcester, Massachusetts opened to the public in September, 2018, and remain on display (see https://hibbettlablog.wordpress.com/2018/09/18/fungi-at-the-ecotarium/). In addition, we participated in outreach activities including mushroom forays for the public, and presentations to amateur mycology clubs.
Wood decay has profound impacts not only on the functioning of natural ecosystems, but also on human affairs. Decay of wood in service (e.g., in buildings) is costly and damaging. At the same time, the enzymes produced by wood decay fungi have potential applications in industrial bioconversions, including biofuel production and bioremediation. While this project was not directly motivated by applied goals, the basic research that we performed provides resources for scientists who seek to harness the enzymatic machinery of wood decay fungi for the benefit of humanity.


Last Modified: 06/18/2020
Modified by: Igor Grigoriev

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