Evolutionary Analysis of DELLA-Associated Transcriptional Networks

Abstract

DELLA proteins are transcriptional regulators present in all land plants which have been shown to modulate the activity of over 100 transcription factors in Arabidopsis, involved in multiple physiological and developmental processes. It has been proposed that DELLAs transduce environmental information to pre-wired transcriptional circuits because their stability is regulated by gibberellins (GAs), whose homeostasis largely depends on environmental signals. The ability of GAs to promote DELLA degradation coincides with the origin of vascular plants, but the presence of DELLAs in other land plants poses at least two questions: what regulatory properties have DELLAs provided to the behavior of transcriptional networks in land plants, and how has the recruitment of DELLAs by GA signaling affected this regulation. To address these issues, we have constructed gene co-expression networks of four different organisms within the green lineage with different properties regarding DELLAs: Arabidopsis thaliana and Solanum lycopersicum (both with GA-regulated DELLA proteins), Physcomitrella patens (with GA-independent DELLA proteins) and Chlamydomonas reinhardtii (a green alga without DELLA), and we have examined the relative evolution of the subnetworks containing the potential DELLA-dependent transcriptomes. Network analysis indicates a relative increase in parameters associated with the degree of interconnectivity in the DELLA-associated subnetworks of land plants, with a stronger effect in species with GA-regulated DELLA proteins. These results suggest that DELLAs may have played a role in the coordination of multiple transcriptional programs along evolution, and the function of DELLAs as regulatory ‘hubs’ became further consolidated after their recruitment by GA signaling in higher plants.

Photoperiodic Signaling and Senescence, an Ancient Solution to a Modern Problem?

“…The correct response to external physical stimuli such as light or temperature is critical for the survival of any organism, and early plants developed a complex gene network to respond successfully to them ( Serrano-Bueno et al, 2017 ; Cheng et al, 2019 ). With the increasing signaling complexity of the new aerial habitats and the production of new organs ( Bowman et al, 2017 ; de Vries and Archibald, 2018 ), land plants developed new forms of regulation that included transportable signals such as florigens, tuberigens, signal peptides, and hormones, among other mobile effectors ( Thomas et al, 2009 ; Wang et al, 2015 ; Briones-Moreno et al, 2017 ; Figure 1 ). This may explain why evolutionarily modern and complex developmental programs, such as flower formation or senescence, are deeply intertwined with hormonal signals ( Thomas et al, 2009 ), whereas ancient physiological responses, such as photosynthesis modulation or photoperiodic signaling in the leaf or algae, often respond to more physical stimuli such as changes in light or temperature ( Serrano-Bueno et al, 2017 ).…”

AnHB40-Jungbrunnen1-GA 2-OXIDASEregulatory module for gibberellin homeostasis in Arabidopsis

“…Binding of GA to its receptor GID1 (GIBBERELLIN INSENSITIVE DWARF1) enhances the interaction between GID1 and DELLA proteins, leading to the rapid degradation of DELLA proteins via the ubiquitin/proteasome pathway (Sun 2010; Davière and Achard 2013; Thomas et al 2016). DELLA proteins are master suppressors of plant growth by inhibiting cell proliferation and elongation (Willige et al 2007), and their function is highly conserved across angiosperm land plants (Gao et al 2008; Briones-Moreno et al 2017; Hernández-García et al 2019). In addition to repressing GA responses, DELLA proteins act as a central node to integrate inputs from light and temperature (Li et al 2016; Zhou et al 2017) as well as from other hormone signaling pathways involving brassinosteroids (BRs), auxin, abscisic acid (ABA) and jasmonic acid (JA) (Davière and Achard 2016).…”

Regulation of DELLA Proteins by Post-translational Modifications

“…Thanks to the ability of DELLAs to interact with other proteins and to the high sensitivity of the GA metabolism to environmental changes ( Sun 2011 ), it is thought that DELLAs act as signaling hubs, connecting the transcriptional pathways regulating growth and defense with the environment ( Claeys et al 2014 ). Indeed, in silico analyses of DELLA-associated gene coexpression networks suggest that DELLAs coordinate transcriptional programs ( Briones-Moreno et al. 2017 ).…”