PhD Final Oral Exam - Trevor Nolan - "To grow or survive: Plants modulate Brassinosteroid-regulated transcription factor BES1 during drought to balance growth and stress responses"

Event
Friday, November 16, 2018 - 10:00am to 12:00pm

Abstract:
Understanding how plants balance growth and stress responses is essential to optimize
crop yield in an ever-changing environment. Brassinosteroids (BRs) regulate plant growth and
stress responses, including that of drought. BRs signal to control the activities of the BES1/BZR1
family transcription factors (TFs), which in turn mediate the expression of more than 5,000 BRresponsive
genes. The network through which BES1 regulates the large number of target genes
and the factors that modulate BES1 during stress are only beginning to be understood. In this
thesis, I investigated several mechanisms that converge on BES1 to balance BR-regulated
growth and stress responses. First, BES1 is degraded by selective autophagy during stress. BES1
interacts with the ubiquitin receptor protein DSK2 and is targeted to the autophagy pathway
during stress via the interaction of DSK2 with ATG8, a ubiquitin-like protein directing
autophagosome formation and cargo recruitment. DSK2 is phosphorylated by the GSK3-like
kinase BIN2, a negative regulator in the BR pathway. BIN2 phosphorylation of DSK2 flanking its
ATG8 interacting motifs (AIMs) promotes the interaction of DSK2 with ATG8, thereby targeting
BES1 for degradation under stress conditions. Accordingly, loss-of-function dsk2 plants
accumulate BES1, have altered global gene expression profiles, and have compromised
responses to drought and fixed-carbon starvation stresses.
In addition, BES1 interacts with other TFs to coordinate growth and drought responses.
RD26 is induced by drought and inhibits the activity of BES1 on target gene promoters during
drought conditions. In contrast, under growth promoting conditions BES1 cooperates with a
large network of TFs including WRKY46/54/70 to inhibit drought responses, thereby enabling
BR-regulated growth. To more fully characterize the BR-regulatory network, we used genomewide
chromatin immunoprecipitation (ChIP), transcriptome and TF interactome datasets to
identify 657 BR-related Transcription Factors (BR-TFs). We then took an integrated approach
involving computational modeling, phenomics and functional genomics to study the networks
through which BRs, BES1/BZR1 and BR-TFs function. Initially, 11,760 publicly available
microarray datasets were used to build comprehensive gene regulatory networks (GRNs). BRTFs
are significantly enriched for BR and drought target genes in the GRNs, suggesting that
these TFs function in growth and stress responses. BR-TFs were prioritized for functional studies
using NEST (Network Essentiality Scoring Tool). Next, we developed BR response assays to
conduct BR phenomics experiments for over 300 BR-TFs using more than 1000 knockout or
overexpression lines. These studies identified numerous BR-TF mutants that displayed altered
BR responses, allowing us to characterize the function of PLATZ and ARID-HMG1 as A/T-rich
binding TFs that oppositely regulate BR-responsive gene expression. Finally, BR and drought
phenomics experiments in soil-grown plants using time-lapse imaging and a robotic
phenotyping system revealed that tcp11 mutants have increased BR-regulated growth and
improved survival during drought compared to wild-type. These studies provide a paradigm for
network-based discovery and characterization of hormone response pathways through the
integration of genomics, network analysis and phenomics. Taken together, BES1 is emerging as
a critical hub for BR-drought crosstalk, allowing plants to efficiently balance growth and stress
responses

Biography:
Trevor Nolan obtained his B.S. in Genetics from Iowa State University in 2013. In 2014, Trevor
joined Dr. Yanhai Yin’s laboratory where he has been studying the mechanisms by which plants
balance growth and stress response through modulation of the Brassinosteroid-regulated
transcription factor BES1.

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