Research Publications

(Selected publications)

2024

Tapia AC, Jaromczyk JW, Moore N, Schardl CL (2024) RNA-clique: A method for computing pairwise genetic distances from RNA-seq data. BMC Bioinformatics 25: 205. doi 10.1186/s12859-024-05811-9

2023

Schardl CL, Afkhami ME, Gundel PE, Iannone LJ, Young CA, Creamer R, Cook DD, Berry D (2023) Diversity of seed endophytes: causes and implications. In B Scott, C Mesarich, eds, The Mycota V Plant Relationships-Fungal-Plant Interactions, Ed 3 Vol V (462 pp.). Springer Nature, Berlin, pp 83-132

2022

Chakrabarti M, Nagabhyru P, Schardl CL, Dinkins RD (2022) Differential gene expression in tall fescue tissues in response to water deficit. Plant Genome 2022: e20199. doi 10.1002/tpg2.20199

Berry D, Lee K, Winter D, Mace W, Becker Y, Nagabhyru P, Treindl AD, Bogantes EV, Young CA, Leuchtmann A, Johnson LJ, Johnson RD, Cox MP, Schardl CL, Scott B (2022) Cross-species transcriptomics identifies core regulatory changes differentiating the asymptomatic asexual and virulent sexual life cycles of grass-symbiotic Epichloë fungi. G3 Genes|Genomes|Genetics 12: jkac043. doi 10.1093/g3journal/jkac043

Leuchtmann A, Schardl CL (2022) Genetic diversity of Epichloë endophytes associated with Brachypodium and Calamagrostis host grass genera including two new species. Journal of Fungi (Basel) 8: 1086. doi 10.3390/jof8101086

Nagabhyru P, Dinkins RD, Schardl CL (2022) Transcriptome analysis of Epichloë strains in tall fescue in response to drought stress. Mycologia 114: 697-712. doi 10.1080/00275514.2022.2060008

2021

Florea S, Jaromczyk J, Schardl CL (2021) Non-transgenic CRISPR-mediated knockout of entire ergot alkaloid gene clusters in slow-growing asexual polyploid fungi. Toxins (Basel) 13: 153. doi 10.3390/toxins13020153

2020

Kang Q, Schardl CL, Moore N, Yoshida R (2020) CURatio: Genome-wide phylogenomic analysis method using ratios of total branch lengths. IEEE/ACM Transactions on Computational Biology and Bioinformatics. doi 10.1109/TCBB.2018.2878564

2019

Berry D, Mace W, Grage K, Wesche F, Gore S, Schardl CL, Young CA, Dijkwel PP, Leuchtmann A, Bode HB, Scott B (2019) Efficient nonenzymatic cyclization and domain shuffling drive pyrrolopyrazine diversity from truncated variants of a fungal NRPS. Proceedings of the National Academy of Sciences USA 116: 25614–25623. doi 10.1073/pnas.1913080116

Dinkins RD, Nagabhyru P, Young CA, West CP, Schardl CL (2019) Transcriptome analysis and differential expression in tall fescue harboring different endophyte strains in response to water deficit. Plant Genome 12: 2-180071. doi 10.3835/plantgenome2018.09.0071

Nagabhyru P, Dinkins RD, Schardl CL (2019) Transcriptomics of Epichloë-grass symbioses in host vegetative and reproductive stages. Molecular Plant-Microbe Interactions32: 194-207. doi 10.1094/MPMI-10-17-0251-R

2018

Pan J, Bhardwaj M, Zhang B, Chang W-c, Schardl CL, Krebs C, Grossman RB, Bollinger JM, Jr. (2018) Installation of the ether bridge of lolines by the iron- and 2-oxoglutarate-dependent oxygenase, LolO: regio- and stereochemistry of sequential hydroxylation and oxacyclization reactions. Biochemistry 57: 2074-2083. doi 10.1021/acs.biochem.8b00157

Shi C, An S, Yao Z, Young CA, Panaccione DG, Lee ST, Schardl CL, Li C (2018) Epichloë bromicola strains symbiotic with the forage grass, Elymus dahuricus, in China. Mycologia 110: (in press). doi 10.1080/00275514.2018.1426941

Winter DJ, Ganley ARD, Young CA, Liachko I, Schardl CL, Dupont PY, Berry D, Ram A, Scott B, Cox MP (2018) Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae. PLoS Genetics 14: e1007467. doi 10.1371/journal.pgen.1007467

2017

Cook D, Donzelli BGG, Creamer R, Baucom DL, Gardner DR, Pan J, Moore N, Krasnoff SB, Jaromczyk JW, Schardl CL (2017) Swainsonine biosynthesis genes in diverse symbiotic and pathogenic fungi. G3: Genes - Genomes - Genetics 7: 1791-1797. doi 10.1534/g3.117.041384

Dinkins RD, Nagabhyru P, Graham MA, Boykin D, Schardl CL (2017) Transcriptome response of Lolium arundinaceum to its fungal endophyte Epichloë coenophiala. New Phytologist 213: 324-337. doi 10.1111/nph.14103

Florea S, Panaccione DG, Schardl CL (2017) Ergot alkaloids of the family Clavicipitaceae. Phytopathology 107: 504-518. doi 10.1094/phyto-12-16-0435-rvw

Liu J, Nagabhyru P, Schardl CL (2017) Epichloë festucae endophytic growth in florets, seeds, and seedlings of perennial ryegrass (Lolium perenne). Mycologia 109: 691-700. doi 10.1080/00275514.2017.1400305

Shi C, An S, Yao Z, Young CA, Panaccione DG, Lee ST, Schardl CL, Li C (2017) Toxin-producing Epichloë bromicola strains symbiotic with the forage grass, Elymus dahuricus, in China. Mycologia 109: 847-859. doi 10.1080/00275514.2018.1426941

2016

Florea S, Phillips TD, Panaccione DG, Farman ML, Schardl CL (2016) Chromosome-end knockoff strategy to reshape alkaloid profiles of a fungal endophyte. G3: Genes - Genomes - Genetics 6: 2601-2610. doi 10.1534/g3.116.029686

2015

Florea S, Schardl CL, Hollin W (2015) Detection and isolation of Epichloë species, fungal endophytes of grasses. Current Protocols in Microbiology 38: 19A.11.11-19A.11.24. doi 10.1002/9780471729259.mc19a01s38

Young CA, Schardl CL, Panaccione DG, Florea S, Takach JE, Charlton ND, Moore N, Webb JS, Jaromczyk J (2015) Genetics, genomics and evolution of ergot alkaloid diversity. Toxins (Basel) 7: 1273-1302. doi 10.3390/toxins7041273

Chen L, Li XZ, Li CJ, Swoboda GA, Young CA, Sugawara K, Leuchtmann A, Schardl CL (2015) Two distinct Epichloë species symbiotic with Achnatherum inebrians, drunken horse grass. Mycologia (in press). doi 10.3852/15-019

Berry D, Takach JE, Schardl CL, Charlton ND, Scott B, Young CA (2015) Disparate independent genetic events disrupt the secondary metabolism gene perA in certain symbiotic Epichloëspecies. Applied and Environmental Microbiology 81: 2797-2807. doi 10.1128/AEM.03721-14

2014

Pan J, Bhardwaj M, Nagabhyru P, Grossman RB, Schardl CL (2014) Enzymes from fungal and plant origin required for chemical diversification of insecticidal loline alkaloids in grass-Epichloë symbiota. PLoS ONE 9: e115590. doi 10.1371/journal.pone.0115590

Schardl CL, Chen L, Young CA (2014) Fungal endophytes of grasses and morning glories, and their bioprotective alkaloids. In A Osbourn, RJ Goss, GT Carter, eds, Natural products: discourse, diversity, and design, Ed First. John Wiley & Sons, Inc., Hoboken, New Jersey, pp 125-145

Schardl CL, Young CA, Moore N, Krom N, Dupont P-Y, Pan J, Florea S, Webb JS, Jaromczyk J, Jaromczyk JW, Cox MP, Farman ML (2014) Genomes of plant-associated Clavicipitaceae.Advances in Botanical Research 70: 291-327. doi http://dx.doi.org/10.1016/B978-0-12-397940-7.00010-0

Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 106: 202-215. doi 10.3852/106.2.202

Mc Cargo PD, Iannone LJ, Vignale MV, Schardl CL, Rossi MS (2014) Species diversity of Epichloë symbiotic with two grasses from southern Argentinean Patagonia. Mycologia 106: 339-352. doi 10.3852/106.2.339

Pan J, Bhardwaj M, Faulkner JR, Nagabhyru P, Charlton ND, Higashi RM, Miller A-F, Young CA, Grossman RB, Schardl CL (2014) Ether bridge formation in loline alkaloid biosynthesis.Phytochemistry 98: 60-68. doi 10.1016/j.phytochem.2013.11.015

Weyenberg G, Huggins PM, Schardl CL, Howe DK, Yoshida R (2014) kdetrees: Nonparametric estimation of phylogenetic tree distributions. Bioinformatics. doi 10.1093/bioinformatics/btu258

2013

Bec S, Liu J, Schardl C (2013) Molecular and genetic basis guiding the establishment of a mutualistic relationship between Epichloë festucae and perennial ryegrass. Phytopathology 103: 13-13. 

Iannone LJ, Mc Cargo PD, Giussani LM, Schardl CL (2013) Geographic distribution patterns of vertically transmitted endophytes in two native grasses in Argentina. Symbiosis 59: 99-110. Doi 10.1007/s13199-012-0214-y

Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND, Nagabhyru P, Chen L, Shi C, Leuchtmann A (2013) Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins 5: 1064-1088. doi 10.3390/toxins5061064

Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach J, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z (2013) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 9: e1003323. doi. 10.1371/journal.pgen.1003323.

Schardl CL, Florea S, Pan J, Nagabhyru P, Bec S, Calie PJ (2013) The epichloae: alkaloid diversity and roles in symbiosis with grasses. Current Opinion in Plant Biology 16: 480-488. doi 10.1016/j.pbi.2013.06.012.

Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biology 13: 127. doi 10.1186/1471-2229-13-127.

2012

Florea S, Machado C, Andreeva K, Schardl CL (2012) The Cre/lox system: a practical tool to efficiently eliminate selectable markers in fungal endophytes. Methods in Molecular Biology 824: 371-379. doi 10.1007/978-1-61779-433-9_19.

2009

Zhang D-X, Nagabhyru P, Schardl CL (2009) Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiology 150: 1072-1082. doi 10.1104/pp.109.138222.

2008

Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R (2008) A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses.Systematic Biology 57: 483-498. doi 10.1080/10635150802172184.

2007

Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68: 980-996. doi 10.1016/j.phytochem.2007.01.010.

2006

Schardl CL, Panaccione DG, Tudzynski P (2006) Ergot alkaloids--biology and molecular biology.Alkaloids: Chemistry and Biology 63: 45-86. doi 10.1016/S1099-4831(06)63002-2.

Faulkner JR, Hussaini SR, Blankenship JD, Pal S, Brannan BM, Grossman RB, Schardl CL (2006) On the sequence of bond formation in loline alkaloid biosynthesis. Chembiochem 7: 1078-1088. (NSF Support)

Panaccione DG, Cipoletti JR, Sedlock AB, Blemings KP, Schardl CL, Machado C, Seidel GE (2006) Effects of ergot alkaloids on food preference and satiety in rabbits, as assessed with gene-knockout endophytes in perennial ryegrass (Lolium perenne). J Agric Food Chem: in press. (USDA Support)

Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB (2006) Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode,Pratylenchus scribneri, on perennial ryegrass. Nematology: in press. (USDA Support)

2005

Blankenship JD, Houseknecht JB, Pal S, Bush LP, Grossman RB, Schardl CL (2005) Biosynthetic precursors of fungal pyrrolizidines, the loline alkaloids. Chembiochem 6: 1016-1022. (NSF Support)

Du M., Schardl CL, Nuckles EM, Vaillancourt LJ (2005) Using mating-type gene sequences for improved phylogenetic resolution of Collectotrichum species complexes. Mycologia 97: 641-658.

Funnell DL, Lawrence CB, Pedersen JF, Schardl CL (2005) Expression of the tobacco b-1,3-glucanase gene PR-2d, following induction of SAR with Peronospora tabacina. Physiological and Molecular Plant Pathology: 65: 285-296.

Gentile A, Rossi MS, Cabral D, Craven KD, Schardl CL (2005) Origin, divergence, and phylogeny of epichloë endophytes of native Argentine grasses. Molecular Phylogenetics and Evolution 35:196-208. (NSF Support)

Haarmann T, Machado C, Lübbe Y, Correia T, Schardl CL, Panaccione DG, Tudzynski P (2005) The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66: 1312-1320. (USDA Support)

Damrongkool P, Sedlock AB, Young CA, Johnson RD, Goetz KE, Scott B, Schardl CL, Panaccione DG (2005). Structural analysis of a peptide synthetase gene required for ergopeptine production in the endophytic fungus Neotyphodium lolii. DNA Sequence 16: 379-385. (USDA Support)

Spiering MJ, Moon CD, Wilkinson HH, Schardl CL ( 2005 ) Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169: 1403-1414. (NSF Support) 

Zhuang J, Marchant MA, Schardl CL, Butler CM (2005) Economic analysis of replacing endophyte-infected with endophyte-free tall fescue pastures. Agronomy Journal 97: 711-716.

2004

Heist EP, Zaitlin D, Funnell DL, Nesmith WC, Schardl CL* (2004) Necrotic-lesion resistance induced by Peronospora tabacina on leaves of Nicotiana obtusifolia. Phytopathology 94: 1178-1188.

Moon CD,Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004). Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Molecular Ecology 13: 1455-1467. (NSF Support)

Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55: 315–340. (see abstract)

Wang J, Machado C, Panaccione DG, Tsai H-F, Schardl CL (2004) The determinant step in ergot alkaloid biosynthesis by an endophyte of perennial ryegrass. Fungal Genetics and Biology 41: 189-198 (see abstract) (USDA Support)

2003

Craven KD, Schardl CL (2003). Tall fescue - systematics and morphology. in: Fribourg HA (ed)Tall fescue information system: Tall fescue book on-line. Oregon State University, Corvallis, Oregon. (see paper)

Schardl CL, and Craven KD. 2003. Interspecific hybridization in plant-associated fungi and oomycetes: a review. Molecular Ecology 12: 2861–2873. (see abstract) 

2002

Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160: S99-S127

Heist EP, Nesmith WC, Schardl CL (2002) Interactions of Peronospora tabacina with roots of Nicotiana species in gnotobiotic associations. Phytopathology: 92: 400-405

Moon CD, Miles CO, Jarlfors U, Schardl CL (2002) The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere.Mycologia 94: 694-711. (NSF Support)

Spiering MJ, Wilkinson HH, Blankenship JD, Schardl CL (2002) Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum. Fungal Genetics and Biology 36: 242–254. (see abstract)(NSF Support)

2001

Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL (2001) Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media.Phytochemistry 58: 395–401. (see abstract) (NSF Support)

Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL (2001) Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia 53: 44-73. (NSF Support)

Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL (2001) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden 88:14-34. (NSF Support)

Heist EP, Nesmith WC, Schardl CL (2001) Cocultures of Peronospora tabacina and Nicotiana species to study host-pathogen interactions. Phytopathology 91: 1224-1230

Panaccione DG, Johnson RD, Wang JH, Young CA, Damrongkool P, Scott B, Schardl CL (2001) Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proceedings of the National Academy of Sciences of the United States of America 98: 12820-12825. (see abstract) (USDA Support)

Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genetics & Biology 33: 69-82. (see abstract) 

2000

Moon CD, Scott B, Schardl CL, Christensen MJ (2000) Evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92:1103-1118.

Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL (2000): Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions 13: 1027-1033. (see abstract) (USDA Support)

1999

Kuldau GA, Tsai H-F, Schardl CL (1999) Genome sizes of Epichloë species and anamorphic hybrids. Mycologia 91: 776-782. (NSF Support)

Schardl CL, Leuchtmann A (1999) Three new species of Epichloë symbiotic with North American grasses. Mycologia 91: 95-107. (NSF Support)

1998

Leuchtmann A, Schardl CL (1998) Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species. Mycological Research 102:1169-1182. (NSF Support)

1997

Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology 114: 1-7. (see paper)

Chung K-R, Hollin W, Siegel MR, Schardl CL (1997) Genetics of host specificity in Epichloë typhina. Phytopathology 87: 599-605. (NSF Support)

Chung K-R, Schardl CL (1997) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycological Research 101: 295-301. (NSF Support)

Chung K-R, Schardl CL (1997) Vegetative compatibility between and within Epichloë species.Mycologia 89: 558-565. (NSF Support)

Kuldau, GA, Liu J-S, White JF, Siegel MR, Schardl CL (1997) Molecular systematics of Clavicipitaceae supporting monophyly of genus Epichloë and form genus Ephelis. Mycologia 89:431-441. (NSF Support)

Schardl CL, Leuchtmann A, Chung K-R, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Molecular Biology and Evolution 14: 133-143. (NSF Support)

Schardl CL, Phillips TD (1997) Protective grass endophytes: Where are they from and where are they going? Plant Disease 81: 430-438.

1996

Chung K-R, Leuchtmann A, Schardl CL (1996) Inheritance of mitochondrial DNA and plasmids in the ascomycetous fungus, Epichloë typhina. Genetics 142: 259-265. (NSF Support)

Schardl CL (1996) Epichloë species: fungal symbionts of grasses. Annual Review of Phytopathology 34: 109-130

1995

Tsai H-F, Wang H, Gebler JC, Poulter CD, Schardl CL (1995) The Claviceps purpurea gene encoding dimethylallyltryptophan synthase, the committed step for ergot alkaloid biosynthesis.Biochemical and Biophysical Research Communications 216: 119-125. (see abstract) (USDA Support)

Li D, Chung K-R, Smith DA, Schardl CL (1995) The Fusarium solani gene encoding kievitone hydratase, a secreted enzyme that catalyzes detoxification of a bean phytoalexin. Molecular Plant-Microbe Interactions 8: 388-397. (USDA Support)

Siegel MR, Schardl CL, Phillips TD (1995) Incidence and compatibility of non-clavicipitaceous fungal endophytes in Festuca and Lolium grass species. Mycologia 87: 196-202. (USDA Support)

1994

Finkel RA, Bent S, Schardl CL (1994) Determining the probability of obtaining a desired clone in an amplified or shuttle library. Biotechniques 16: 580-583.

Leuchtmann A, Schardl CL, Siegel MR (1994) Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia 86: 802-812. (USDA Support)

Schardl CL, Leuchtmann A, Tsai H-F, Collett M, Watt DM, Scott DB (1994) Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics 136: 1307-1317. (see abstract) 

Tsai H-F, Liu J-S, Staben C, Christensen MJ, Latch GCM, Siegel MR, Schardl CL (1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proceedings of the National Academy of Sciences of the United States of America 91: 2542-2546. (see abstract) 

1992

Tsai H-F, Siegel MR, Schardl CL (1992) Transformation of Acremonium coenophialum, a protective mycosymbiont of the grass Festuca arundinacea. Current Genetics 22: 399-406