Award Abstract # 1546862
RESEARCH-PGR: Defining the Sumoylation System in Maize and Its Roles in Stress Protection

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: WASHINGTON UNIVERSITY, THE
Initial Amendment Date: August 12, 2016
Latest Amendment Date: August 12, 2016
Award Number: 1546862
Award Instrument: Standard Grant
Program Manager: Diane Jofuku Okamuro
dokamuro@nsf.gov
 (703)292-4508
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: August 15, 2016
End Date: July 31, 2020 (Estimated)
Total Intended Award Amount: $930,142.00
Total Awarded Amount to Date: $930,142.00
Funds Obligated to Date: FY 2016 = $930,142.00
History of Investigator:
  • Richard Vierstra (Principal Investigator)
    rdvierstra@wustl.edu
Recipient Sponsored Research Office: Washington University
1 BROOKINGS DR
SAINT LOUIS
MO  US  63130-4862
(314)747-4134
Sponsor Congressional District: 01
Primary Place of Performance: Washington University
St. Louis
MO  US  63130-4899
Primary Place of Performance
Congressional District:
01
Unique Entity Identifier (UEI): L6NFUM28LQM5
Parent UEI:
NSF Program(s): Plant Genome Research Project
Primary Program Source: 01001617DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 7577, 9109, 9178, 9179, 9251, BIOT
Program Element Code(s): 132900
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Crop plants require suitable mechanisms to survive and perform well under unfavorable environments in order to maintain high productivity. Recently, a small protein called SUMO was discovered, and it appears to protect plants against environmental stresses like heat and drought. Recent experiments with plants exposed to environmental stresses have shown that the SUMO protein may significantly affect how genes are expressed under those unfavorable conditions. The SUMO protein becomes rapidly and reversibly attached to a group of proteins that affect the pattern of gene expression during environmental stress. The goals of this project are to understand the functions of SUMO during stress and determine whether its manipulation in crops might provide novel approaches to improve stress tolerance. This project will characterize the mode of action of the SUMO protein, and identify all the other proteins that interact with SUMO under stress. To help understand how SUMO helps maize survive stress, we will also determine why maize mutants missing key components are now hypersensitive to stress. Collectively, this fundamental research will identify key points in maize SUMOylation that can be exploited to improve stress protection, not only in maize but in other crops as well. This project will train postdocs, graduate students, and undergraduates at Washington University in St. Louis. It will also develop patentable technologies related SUMO and stress tolerance that can sustainably enhance food and biofuel crop yield.


SUMO is an influential regulator in eukaryotes that works following its post-translation addition to other intracellular proteins. Recent studies with Arabidopsis discovered that SUMOylation selectively modifies a number of critical regulators during stress that impact chromatin accessibility, DNA/histone modification, transcription, nuclear pore function, and mRNA processing/export. Their combined activities imply that stress-induced SUMOylation helps plants reversibly adjust chromatin architecture and the resulting RNA landscape to better survive adverse conditions. Unfortunately, appreciation of SUMO is lacking for crops, thus precluding rational redesign for agricultural benefit. To overcome this knowledge gap, this project will define how SUMOylation works in maize (Zea mays), using as essential backdrops our recent success in creating germplasm to study SUMO via proteomic approaches. This project will: (i) describe how the maize SUMO system works biochemically and responds to various environmental challenges, (ii) combine transgenic lines expressing tagged SUMOs with established mass spectrometric methods to define the maize 'SUMOylome' and its linkage sites, (iii) determine quantitatively how the SUMOylation status of individual targets is impacted by stress, and (iv) understand how SUMO helps maize survive adverse environments through the phenotypic and biochemical analyses of system mutants generated by either Mu transposition or CRISPR/Cas9 gene editing technologies. Collectively, this project will generate much-needed reagents, techniques, and mutants that will help define how SUMO reorganizes maize chromatin and its transcriptome during stress, and identify key points in SUMOylation that can be manipulated to improve stress protection in many crop species.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Augustine, R.A., and Vierstra, R.D. "SUMOylation: rewiring the plant nucleus during stress and development" Current Opinions in Plant Biology , v.45 , 2018 , p.143 doi.org/10.1016/j.pbi.2018.06.006
Augustine, R.C., Rytz, T.C., York, S.L., and Vierstra, R.D. "Defining the SUMO system is maize: SUMOylation is up-regulated during endosperm development and rapidly induced by stress." Plant Physiology , v.171 , 2016 , p.2191 https://doi.org/10.1104/pp.16.00353
Augustine, R.S., and R.D. Vierstra "SUMOylation: rewiring the plant nucleus during stress and development." Current Opinions in Plant Biology , v.45 , 2018 , p.143 org/10.1016/j.pbi.2018.06.006
Augustine, R.S., and Vierstra, R.D. "SUMOylation: rewiring the plant nucleus during stress and development" Current Opinions in Plant Biology , v.45 , 2018 , p.143 doi: org/10.1016/j.pbi.2018.06.006
Castro, P.H., A. Bachmair, E.R. Bejarano, G. Coupland, L.M. Lois, A. Sadanandom, H.A. van den Burg, R.D. Vierstra, and H. Azevedo "A revised nomenclature and functional overview of the ULP gene family of plant deSUMOylating proteases." Journal of Experimental Botany , 2018
Castro, P.H., Bachmair, A., Bejarano, E.R., Coupland, G., Lois, L.M., Sadanandom, A., van den Burg, H.A., Vierstra, R.D., and Azevedo, H. "A revised nomenclature and functional overview of the ULP gene family of plant deSUMOylating proteases." Journal of Experimental Botany , v.69 , 2018 , p.4505 doi org/10.1093/jxb/ery301
Robert C. Augustine, Samuel L. York, Thérèse C. Rytz, and Richard D. Vierstra "Defining the SUMO System in Maize: SUMOylation Is Up-Regulated during Endosperm Development and Rapidly Induced by Stress" American Society of Plant Biologists , 2016
Rytz, T.C.,Miller, M.J., McLoughlin, F., Augustine, R.C., , Marshall, R.S., Juan, Y.T., Chung,Y.-Y., Scalf, M., Smith, L.M., and Vierstra, R.D. "SUMOylome profiling in Arabidopsis reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress." Plant Cell , v.30 , 2018 , p.1077 doi:10.1105/tpc.17.00993
Rytz, T.C, Miller, M.J., McLoughlin, F., Augustine, R.C, Marshall, R.S., Juan, Y.-T., Scalf, M., Smith, L.S, and Vierstra, R.D. "SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress" Plant Cell , v.30 , 2018 , p.1077 doi/10.1105/tpc.17.00993
Rytz, T.C., M.J. Miller, F. McLoughlin, R.C. Augustine, R.S. Marshall, Y.-T. Juan, Y.-Y. Chung, M. Scalf, L.M. Smith, and R.D. Vierstra "SUMOylome profiling in Arabidopsis reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress" Plant Cell , v.30 , 2018 , p.1077 10.1105/tpc.17.00993

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.

The research herein had a major impact on the field of plant biology, providing important inroads into the roles of the protein post-translational modifier - SUMO in protecting plants against stress and helping direct important developmental processes – especially with respect to cereals - the world’s most foremost crop species.  Importantly, this project developed a library of maize mutants within the pathway that now allow scientists to study SUMOylation in various tissue-specific and developmental contexts.  It also generated transgenic lines and strategies to help catalog proteins that are affected by SUMOylation, which should provide new insights to researchers about the post-translational regulation of their favorite proteins.  In particular, our observations that many proteins involved in epigenetic regulation, including DNA and histone methylation/acetylation, are targets of SUMOylation, indicates that much of this regulation is controlled by SUMO attachment and its response to stress.  We also discovered through study of the SUMO ligase MMS21, a role for SUMOylation in regulating the expression of seed storage proteins and in controlling DNA damage.  Collectively, this project generated germplasm that will be useful to the community, including mutant seed stocks useful for dissecting the role of the SUMO pathway, and SUMO purification lines to help any researchers interested in testing the role of SUMOylation on their maize protein-of-interest.

 

 


Last Modified: 01/07/2021
Modified by: Richard D Vierstra

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