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Isolation and Structural Characterization of the Active Molecule

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Isolation and Structural Characterization of the Active Molecule ISOLATION AND STRUCTURAL CHARACTERIZATION OF THE ACTIVE MOLECULE FROM SIREX NOCTILIO WOODWASP VENOM INDUCING PRIMARY PHYSIOLOGICAL SYMPTOMS IN ATTACKED PINE SPECIES by JOHN MICHAEL BORDEAUX (Under the Direction of Jeffrey F. D. Dean) ABSTRACT Sirex noctilio F., a non-native, invasive woodwasp recently introduced into North America, attacks and kills living pines, including economically important species. S. noctilio introduces phytotoxic venom and a pathogenic basidiomycete, Amylostereum areolatum, into trees during oviposition. S. noctilio venom alone induces pine needle chlorosis and abscission, phloem collapse, altered respiration, loss of carbohydrate translocation, and reduced growth rate. A 26,496-feature loblolly pine cDNA microarray was used to identify two genes useful as biomarkers in qRT-PCR bioassays for pine response to venom exposure, PR4 and TLP. Expression of both was strongly induced in response to venom, while expression of an apparent actin gene (ACT1) was stable in response to the venom. The S. noctilio venom gland transcriptome was assembled from >260 million Illumina HiSeq reads using a minimum length cutoff for assemblies of 100 nucleotides. This dataset is the first transcriptome-scale resource available for a basal-order species of Hymenoptera. Of the 68,887 transcripts generated from this dataset, 24,471 (35%) returned annotations with E- value < 1 x 10-10. No annotations were returned for the seven most abundant transcripts. The single most abundant transcript present encodes the molecule responsible for initial wilt and gene responses in pines. The eighth most highly-expressed sequence recovered was a transcript encoding a putative laccase-like multicopper oxidase. The bioassay above was utilized to isolate from S. noctilio venom an 11-amino acid peptide (SEGPROGTKRP) of 1850 Da. This peptide, noctilisin, induced the wilt phenotype in pine seedling explants. Primary sequence and structure were established using Edman degradation, NMR, and MS-MS. Post-translational modifications include O-glycosylation of serine and threonine, and hydroxylation of the 6th residue (proline). Two identical O-glycans present were characterized as N-acetylgalactose, modified by an O-linked phosphoethanolamine on the glycan C6. Noctilisin activity is glycan-dependent. Wide-scale screening for resistance to woodwasp attack across pine populations now is feasible. A further RNA-Seq experiment was performed to compare the effects of whole venom, noctilisin alone, and a biologically-inactive, non-glycosylated peptide on sensitive P. radiata explants. These results should elucidate suites of genes responding specifically to noctilisin and distinguish them from genes responding to other active factors in whole venom. INDEX WORDS: bioassay, forest health, glycopeptide, Hymenoptera, LMCO, loblolly, pine, Pinus radiata, Pinus taeda, woodwasp, Sirex noctilio, Symphyta, transcriptome, venom ISOLATION AND STRUCTURAL CHARACTERIZATION OF THE ACTIVE MOLECULE FROM SIREX NOCTILIO WOODWASP VENOM INDUCING PRIMARY PHYSIOLOGICAL SYMPTOMS IN ATTACKED PINE SPECIES by JOHN MICHAEL BORDEAUX Bachelor of Science, University of North Carolina at Chapel Hill, 1992 Master of Science, University of Georgia, 2008 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2014 © 2014 John Michael Bordeaux All Rights Reserved ISOLATION AND STRUCTURAL CHARACTERIZATION OF THE ACTIVE MOLECULE FROM SIREX NOCTILIO WOODWASP VENOM INDUCING PRIMARY PHYSIOLOGICAL SYMPTOMS IN ATTACKED PINE SPECIES by JOHN MICHAEL BORDEAUX Major Professor: Jeffrey F. D. Dean Committee: Claiborne V. C. Glover III Scott E. Gold Michael R. Strand Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia May 2014 ACKNOWLEDGEMENTS This work was made possible by the efforts of the following indispensable persons: Jeff Dean: perspective, tireless guidance and consistent enthusiasm for the endeavor; Walt Lorenz: critical analysis, hard scientific work, and daily assistance; Claiborne Glover, Scott Gold, Michael Strand, Kamal Gandhi: rigor, honest criticism, abiding scientific interest, substantial counsel, material support, and friendship; D.J. Johnson, Majors Badgett, Ron Orlando, John Glushka, Bernard Slippers, Raj Ayyampalayam, Dave Coyle: scientific collaboration and generous contributions during experimental sampling and analysis; Ujwal Bagal, Susan Wilde, Dick Daniels, Mark Brown, Scott Merkle, Giselle Dean, Alan Przybyla, Zac Wood, Nanda Menon, Gwen Hirsch, Martin Kallins, Valeria Coscia, Bruce Johnson, C.J. Tsai, Eileen Carroll, Jay Shelton, Kris Irwin, Diana Hartle, Amonae Dabbs-Brown, Joyce Black, Angie Callaway, Kate Dedufour, Judith Willis: advice, interest, support, friendship, encouragement; Matt Head, David Rutland, Carolyn and Calvin Monroe, Grady and Glenda Bordeaux, Chris and Ashely Bordeaux, Sheila and Steve Rains, Randy Lindstrom, Dan and Susanne Reeder: family support in word and deed. iv TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................... iv LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ....................................................................................................................... xi CHAPTER 1 INTRODUCTION .........................................................................................................1 1.1 Pine, Economic Importance, and Potential Threats to Pine Health ..................1 1.2 Siricid Woodwasps ...........................................................................................2 1.3 Significant Players in the Woodwasp/Pine Pathosystem ..................................2 1.4 Research Objectives ..........................................................................................2 References ................................................................................................................5 2 LITERATURE REVIEW: SUSCEPTIBILITY AND RESPONSE OF PINES TO SIREX NOCTILIO ........................................................................................................7 2.1 Introduction .......................................................................................................9 2.2 Factors Contributing to Tree Susceptibility ....................................................11 2.3 Tree Responses to Sirex noctilio Mucus .........................................................14 2.4 Tree Responses to Amylostereum areolatum ..................................................20 2.5 General Responses to Sirex Attack .................................................................23 2.6 Reducing Tree Susceptibility ..........................................................................24 References ..............................................................................................................29 v 3 BIOMARKER GENES HIGHLIGHT INTRASPECIFIC AND INTERSPECIFIC VARIATIONS IN THE RESPONSES OF PINUS TAEDA L. AND PINUS RADIATA D. DON TO SIREX NOCTILIO F. ACID GLAND SECRETIONS .......42 3.1 Introduction .....................................................................................................44 3.2 Materials and Methods ....................................................................................46 3.3 Results .............................................................................................................52 3.4 Discussion .......................................................................................................56 3.5 Conclusions .....................................................................................................60 References ..............................................................................................................71 4 CHARACTERIZATION OF THE VENOM GLAND TRANSCRIPTOME FROM THE WOODWASP, SIREX NOCTILIO F., IDENTIFIES HIGHLY EXPRESSED TRANSCRIPTS ENCODING A LACCASE-LIKE MULTICOPPER OXIDASE AND OTHER PROTEINS THAT MODULATE THE RESPONSE OF PINES TO INSECT ATTACK ......................................................................................................78 4.1 Introduction .....................................................................................................80 4.2 Materials and Methods ....................................................................................84 4.3 Results .............................................................................................................88 4.4 Discussion .......................................................................................................95 4.5 Conclusions ....................................................................................................100 References ............................................................................................................114 5 NOCTILISIN, A VENOM GLYCOPEPTIDE, IS THE HEAT-STABLE FACTOR THAT CAUSES NEEDLE WILT AND DEFENSE GENE RESPONSES IN PINES ATTACKED BY THE SIREX NOCTILIO WOODWASP ......................................130 vi 5.1 Introduction ...................................................................................................132 5.2 Experimental Procedures ..............................................................................134 5.3 Results ...........................................................................................................138
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