Conserved and variable responses of the HEAT SHOCK FACTOR transcription factor family in maize and Setaria viridis

Abstract

Responding to the environment is a core aspect of plant growth and development. Mounting an effective response is important for plants to balance growth and survival. The HEAT SHOCK FACTOR (HSF) transcription factor family is a central and required component of plant heat stress responses and acquired thermotolerance. The HSF family has dramatically expanded in plant lineages, often including a repertoire of 20 or more genes. Here we assess the composition and heat responsiveness of the HSF family in Setaria viridis (Setaria), a model C4 panicoid grass, and make targeted comparisons between the HSF families of Setaria and maize. Examples of both conserved and variable expression responses to a heat stress event were observed when comparing the two species. Novel and existing data on chromatin accessibility, histone modifications, and genome-wide DNA binding profiles were utilized to assess the chromatin of HSF family members with distinct responses to heat stress. We observed significant variability for both expression and chromatin state within syntenic and orthologous sets of HSFs between Setaria and maize, as well as between syntenic pairs of maize HSFs retained following its most recent genome duplication event. These observations collectively support a complex scenario of expansion and sub-functionalization within this transcription factor family that has significant untapped potential for better understanding the evolution of large gene families.Significance StatementA comparison of the Heat Shock Factor transcription factors in maize and Setaria reveals examples of consistent and variable expression responses to heat stress and provides insights into the role of chromatin in predicting expression responses.

cis-Regulatory Elements in Plant Development, Adaptation, and Evolution

“…This study also included profiles of samples with a 24-hour recovery period following the stress, revealing that chromatin accessibility often reverts to prestress configurations (110). An analysis of heat shock factors in maize and Setaria indicated that while many genes are strongly induced by heat stress, chromatin accessibility variation in response to heat stress is limited (94). However, a combined analysis of three-dimensional spatial organization and chromatin accessibility uncovered dynamic changes in the response to heat stress in rice (72).…”

Mapping Responsive Genomic Elements to Heat Stress in a Maize Diversity Panel

“…Prior studies have found evidence for enrichment of the HSF binding site motif at up-regulated genes in Arabidopsis 13 , maize 14 and rice 15 . Some HSFs are stably expressed and become activated in response to heat stress, while many other members of this family are themselves transcriptionally activated in response to heat stress 12,16,17 . Several other transcription factors and cis -regulatory elements have also been implicated in the response to heat stress 18 .…”

Mapping responsive genomic elements to heat stress in a maize diversity panel

“…Prior studies have found evidence for enrichment of the HSF binding site motif at upregulated genes in Arabidopsis [13], maize [14], and rice [15]. Some HSFs are stably expressed and become activated in response to heat stress, while many other members of this family are themselves transcriptionally activated in response to heat stress [12,16,17]. Several other transcription factors and cis-regulatory elements have also been implicated in the response to heat stress [18].…”