Transcriptomics of epichloë-grass symbioses in host vegetative and reproductive stages

Padmaja Nagabhyru; Randy D. Dinkins; Christopher L. Schardl

doi:10.1094/MPMI-10-17-0251-R

Transcriptomics of epichloë-grass symbioses in host vegetative and reproductive stages

Padmaja Nagabhyru, Randy D. Dinkins, Christopher L. Schardl

Plant Pathology

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

Epichloë species are fungal symbionts (endophytes) of cool-season grasses that transmit vertically via inflorescence primordia (IP), ovaries (OV), and ultimately, embryos. Epichloë coenophiala, an endophyte of tall fescue (Schedonorus arundinaceus), provides multiple protective benefits to the grass. We conducted transcriptome analysis of the tall fescue–E. coenophiala symbiosis, comparing IP, OV, vegetative pseudostems (PS), and the lemma and palea (LP) (bracts) of the young floret. Transcriptomes of host OV and PS exhibited almost no significant differences attributable to endophyte presence or absence. Comparison of endophyte gene expression in different plant parts revealed numerous differentially expressed genes (DEGs). The 150 endophyte DEGs significantly higher in PS over OV included genes for alkaloid biosynthesis and sugar or amino acid transport. The 277 endophyte DEGs significantly higher in OV over PS included genes for protein chaperones (including most heat-shock proteins), trehalose synthesis complex, a bax inhibitor-1 protein homolog, the CLC chloride ion channel, catalase, and superoxide dismutase. Similar trends were apparent in the Brachypodium sylvaticum–Epichloë sylvatica symbiosis. Gene expression profiles in tall fescue IP and LP indicated that the endophyte transcriptome shift began early in host floral development. We discuss possible roles of the endophyte DEGs in colonization of reproductive grass tissues.

Original language	English
Pages (from-to)	194-207
Number of pages	14
Journal	Molecular Plant-Microbe Interactions
Volume	32
Issue number	2
DOIs	https://doi.org/10.1094/MPMI-10-17-0251-R
State	Published - Feb 2019

Bibliographical note

Funding Information:
This work is supported by the U.S. Department of Agriculture Special Cooperative Agreement grant 2016-020508441 and National Institute of Food and Agriculture Hatch project KY012044. The authors thank T. Boss and S. Holton for maintaining plants in the greenhouse and W. Hollin for technical support. The authors also thank J. Jaromczyk for help with the MiSeq data processing and assembly and N. Moore for genome sequence annotation and public release at the University of Kentucky Genome Projects database. The authors also acknowledge AGTC at the University of Kentucky and the Iowa DNA sequencing facility for providing sequencing services. This is publication number 18-12-047 of the Kentucky Agricultural Experiment Station, published with the approval of the director.

Funding Information:
Funding: This work is supported by the U.S. Department of Agriculture Special Cooperative Agreement grant 2016-020508441 and National Institute of Food and Agriculture Hatch project KY012044.

Publisher Copyright:
© 2019 American Phytopathological Society. All Rights Reserved.

ASJC Scopus subject areas

Physiology
Agronomy and Crop Science

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10.1094/MPMI-10-17-0251-R

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title = "Transcriptomics of epichlo{\"e}-grass symbioses in host vegetative and reproductive stages",

abstract = "Epichlo{\"e} species are fungal symbionts (endophytes) of cool-season grasses that transmit vertically via inflorescence primordia (IP), ovaries (OV), and ultimately, embryos. Epichlo{\"e} coenophiala, an endophyte of tall fescue (Schedonorus arundinaceus), provides multiple protective benefits to the grass. We conducted transcriptome analysis of the tall fescue–E. coenophiala symbiosis, comparing IP, OV, vegetative pseudostems (PS), and the lemma and palea (LP) (bracts) of the young floret. Transcriptomes of host OV and PS exhibited almost no significant differences attributable to endophyte presence or absence. Comparison of endophyte gene expression in different plant parts revealed numerous differentially expressed genes (DEGs). The 150 endophyte DEGs significantly higher in PS over OV included genes for alkaloid biosynthesis and sugar or amino acid transport. The 277 endophyte DEGs significantly higher in OV over PS included genes for protein chaperones (including most heat-shock proteins), trehalose synthesis complex, a bax inhibitor-1 protein homolog, the CLC chloride ion channel, catalase, and superoxide dismutase. Similar trends were apparent in the Brachypodium sylvaticum–Epichlo{\"e} sylvatica symbiosis. Gene expression profiles in tall fescue IP and LP indicated that the endophyte transcriptome shift began early in host floral development. We discuss possible roles of the endophyte DEGs in colonization of reproductive grass tissues.",

author = "Padmaja Nagabhyru and Dinkins, {Randy D.} and Schardl, {Christopher L.}",

note = "Funding Information: This work is supported by the U.S. Department of Agriculture Special Cooperative Agreement grant 2016-020508441 and National Institute of Food and Agriculture Hatch project KY012044. The authors thank T. Boss and S. Holton for maintaining plants in the greenhouse and W. Hollin for technical support. The authors also thank J. Jaromczyk for help with the MiSeq data processing and assembly and N. Moore for genome sequence annotation and public release at the University of Kentucky Genome Projects database. The authors also acknowledge AGTC at the University of Kentucky and the Iowa DNA sequencing facility for providing sequencing services. This is publication number 18-12-047 of the Kentucky Agricultural Experiment Station, published with the approval of the director. Funding Information: Funding: This work is supported by the U.S. Department of Agriculture Special Cooperative Agreement grant 2016-020508441 and National Institute of Food and Agriculture Hatch project KY012044. Publisher Copyright: {\textcopyright} 2019 American Phytopathological Society. All Rights Reserved.",

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N2 - Epichloë species are fungal symbionts (endophytes) of cool-season grasses that transmit vertically via inflorescence primordia (IP), ovaries (OV), and ultimately, embryos. Epichloë coenophiala, an endophyte of tall fescue (Schedonorus arundinaceus), provides multiple protective benefits to the grass. We conducted transcriptome analysis of the tall fescue–E. coenophiala symbiosis, comparing IP, OV, vegetative pseudostems (PS), and the lemma and palea (LP) (bracts) of the young floret. Transcriptomes of host OV and PS exhibited almost no significant differences attributable to endophyte presence or absence. Comparison of endophyte gene expression in different plant parts revealed numerous differentially expressed genes (DEGs). The 150 endophyte DEGs significantly higher in PS over OV included genes for alkaloid biosynthesis and sugar or amino acid transport. The 277 endophyte DEGs significantly higher in OV over PS included genes for protein chaperones (including most heat-shock proteins), trehalose synthesis complex, a bax inhibitor-1 protein homolog, the CLC chloride ion channel, catalase, and superoxide dismutase. Similar trends were apparent in the Brachypodium sylvaticum–Epichloë sylvatica symbiosis. Gene expression profiles in tall fescue IP and LP indicated that the endophyte transcriptome shift began early in host floral development. We discuss possible roles of the endophyte DEGs in colonization of reproductive grass tissues.

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Transcriptomics of epichloë-grass symbioses in host vegetative and reproductive stages

Abstract

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