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Open Larsen Thesis.Pdf The Pennsylvania State University The Graduate School College of Engineering ENGINEERING HIGH-LEVEL TRANSIENT EXPRESSION OF HETEROLOGOUS PROTEINS IN PLANT CELL SUSPENSIONS AND HAIRY ROOTS A Dissertation in Chemical Engineering by Jeffrey S. Larsen 2011 Jeffrey S. Larsen Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2011 ii The dissertation of Jeffrey S. Larsen was reviewed and approved* by the following: Wayne R. Curtis Professor of Chemical Engineering Dissertation Advisor Chair of Committee Esther W. Gomez Assistant Professor of Chemical Engineering Timothy W. McNellis Associate Professor of Plant Pathology C. Peter Romaine Professor of Plant Pathology Andrew L. Zydney Walter L. Robb Chair and Professor of Chemical Engineering Head of the Department of Chemical Engineering *Signatures are on file in the Graduate School iii ABSTRACT Low protein product titers have thus far limited the application of Agrobacterium tumefaciens for the transient expression of heterologous proteins in plant cell suspensions and hairy root cultures. The overall objectives of this work were to overcome this limitation by: (1) increasing protein product titers in cell suspensions and hairy root cultures by harnessing A. tumefaciens to efficiently deliver replicating RNA viral vectors, and (2) identifying the physical and physiological factors important for reproducible, high-level transient expression in cell suspensions. Replicating vectors derived from Potato virus X (PVX) and Tobacco rattle virus (TRV) were modified to contain the reporter gene beta-glucuronidase (GUS) with a plant intron to prevent bacterial expression. In cell suspensions, a minimal PVX construct retaining only the viral RNA polymerase gene yielded 6.6-fold more GUS than an analogous full-genome PVX vector. Co-delivery of the minimal PVX vector with p19 of Tomato bushy stunt virus and HC-Pro of Tobacco etch virus increased transient GUS expression by 40-80%. In hairy roots, a vector derived from TRV that was capable of systemic movement increased GUS accumulation by 150- fold relative to the analogous PVX vector. A modified TRV-based vector and a transgenic host with integrated suppression of post- transcriptional gene silencing were investigated as strategies to further increase transient expression in hairy roots. A TRV vector was modified to retain the viral helper protein 2b, which is required for nematode transmission. In N. benthamiana hairy roots, the modified TRV vector resulted in GUS expression levels comparable to the control vector without the 2b gene. In contrast, Nicotiana tabacum cv. Xanthi hairy roots transgenic for HC-Pro yielded 5-fold more GUS from the modified TRV vector than control roots. iv Prior to the development of the TRV vectors, a study was conducted to determine if movement-deficient PVX vectors could be complemented in trans by the Tobacco mosaic virus 30K movement protein (MP). Unexpectedly, transient co-delivery of TMV MP with the minimal PVX vector resulted in reduced transient GUS expression in cell suspensions and hairy roots of N. benthamiana. Improved productivity in plant cell suspensions was achieved by manipulating the host, co-culture environment, and non-replicating expression vectors to produce conditions more favorable for Agrobacterium-mediated transient GUS expression. Modification of the N. glutinosa cell suspension host by transformation with Agrobacterium rhizogenes did not have a significant effect on average transient GUS expression across multiple independent cell lines. In N. benthamiana, doubling the concentration of potassium phosphate resulted in a 5-fold increase in transient GUS expression. Removal of the plant selectable marker cassette from a non- replicating vector with a constitutive promoter decreased the T-DNA size by one-third and increased transient GUS expression by almost 50%. This work established the feasibility of utilizing Agrobacterium-mediated delivery of replicating RNA viral vectors for amplified heterologous protein expression in plant tissue cultures. A TRV vector capable of systemic movement represents the first and only vector to achieve transient GUS expression levels in hairy roots comparable to those observed in plant cell suspensions. Considering the inconsistent absolute transient expression levels intrinsic to plant cell suspensions, hairy root cultures may be a preferable host for reproducible transient protein expression. The advantages and limitations of this approach are discussed in the context of engineering a safe, cost-effective, and scalable protein production platform. v TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. viii LIST OF TABLES ................................................................................................................... xiii Chapter 1 Introduction ............................................................................................................. 1 1.1 Summary .................................................................................................................... 1 1.2 Heterologous protein expression in eukaryotic hosts ................................................. 2 1.2.1 Post-translational modifications ...................................................................... 5 1.3 Expression of human proteins in plants ..................................................................... 7 1.3.1 Commercial enterprises ................................................................................... 8 1.3.2 Economics, scalability and containment ......................................................... 13 1.4 Viral vectors for transient protein expression in ex vitro plants................................. 19 1.4.1 Viral gene replacement and deletion strategies ............................................... 23 1.4.2 Post-transcriptional gene silencing .................................................................. 29 1.5 Conclusions ................................................................................................................ 30 Chapter 2 RNA virus-amplified transient GUS expression in leaves, cell suspensions and hairy roots of Nicotiana benthamiana .............................................................................. 33 2.1 Summary .................................................................................................................... 33 2.2 Introduction ................................................................................................................ 34 2.3 Materials and methods ............................................................................................... 39 2.3.1 Plants and plant tissue cultures ........................................................................ 39 2.3.2 Co-culture of plant tissue cultures with Agrobacterium tumefaciens.............. 40 2.3.3 Histochemical GUS detection and quantification ........................................... 41 2.3.4 Leaf infiltrations .............................................................................................. 43 2.3.5 Vector construction ......................................................................................... 44 2.3.6 Statistical analysis ........................................................................................... 48 2.4 Results and discussion ............................................................................................... 49 2.4.1 In cell suspensions, a replicating PVX vector yielded 6.6-fold more GUS when non-essential viral gene functions were omitted ..................................... 49 2.4.2 Suppression of post-transcriptional gene silencing increased transient GUS expression from the minimal PVX vector in cell suspensions ................ 52 2.4.3 A non-replicating vector containing a leader sequence from Cowpea mosaic virus modified for enhanced translation led to 70% higher transient GUS expression in cell suspensions ................................................................. 54 2.4.4 Absolute GUS expression levels in cell suspensions were an order of magnitude lower than those measured for the same vectors in infiltrated leaves ................................................................................................................ 57 2.4.5 In hairy roots, a movement-enabled vector derived from TRV yielded 150-fold more GUS than the analogous PVX vector. ...................................... 60 2.4.6 Histochemical staining of TRV-infected hairy roots revealed the capacity for higher productivity per unit biomass .......................................................... 63 2.5 Conclusions ................................................................................................................ 64 2.6 Acknowledgements .................................................................................................... 65 vi Chapter 3 Factors affecting Agrobacterium-mediated transient GUS expression in Nicotiana cell suspensions ............................................................................................... 67 3.1 Summary .................................................................................................................... 67 3.2 Introduction ................................................................................................................ 68 3.3 Materials and methods ..............................................................................................
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