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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.
Highlights
Higher plants are characterized by a flexible capacity to adapt to multiple environmental conditions
Gene expression data from RNA sequencing (RNA-seq) experiments in A. thaliana, S. lycopersicum, P. patens, and C. reinhardtii were obtained from the Gene Expression Omnibus, and gene co-expression networks were inferred for each species from transcriptomic data as described in section “Materials and Methods.”
The four species were represented unequally, as both A. thaliana and S. lycopersicum genes were present in ca. 70% of the groups, while P. patens genes were found in little more than 50% of them, and only ca. 30% of the groups contained genes from C. reinhardtii
Summary
Higher plants are characterized by a flexible capacity to adapt to multiple environmental conditions. It has become evident that hormone pathways share common components with the pathways that transduce light and other environmental signals (Jaillais and Chory, 2010); and, on the other hand, hormones have been shown to participate in the regulation of developmental processes all throughout a plant’s life cycle (Alabadi et al, 2009) In this context, gibberellins (GAs) and DELLA proteins are a paradigmatic example of the mechanisms that allow environmental signal integration. DELLA proteins constitute a small clade within the GRAS family of loosely defined plant specific nuclear proteins (Vera-Sirera et al, 2015) Their name was coined on the basis of a short stretch of amino acids (D-E-L-L-A) in their N-terminal region, which is tightly conserved among all higher plant species. The promiscuous interaction with TFs, and the observation that A. thaliana dellaKO mutants display constitutive growth even under stress, and suffer from increased sensitivity to several types of stress factors such as salinity, cold, or fungal attacks (Alabadí et al, 2004; Achard et al, 2006, 2007, 2008a,b; Cheminant et al, 2011) suggests that DELLAs are potentially important ‘hubs’ in the transcriptional network that regulates the balance between growth and stress tolerance in higher plants
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