Evolution of the B3 DNA Binding Superfamily: New Insights into REM Family Gene Diversification

Background: The B3 DNA binding domain includes five families: auxin response factor (ARF), abscisic acid-insensitive3 (ABI3), high level expression of sugar inducible (HSI), related to ABI3/VP1 (RAV) and reproductive meristem (REM). The release of the complete genomes of the angiosperm eudicots Arabidopsis thaliana and Populus trichocarpa, the monocot Orysa sativa, the bryophyte Physcomitrella patens,the green algae Chlamydomonas reinhardtii and Volvox carteri and the red algae Cyanidioschyzon melorae provided an exceptional opportunity to study the evolution of this superfamily. Methodology: In order to better understand the origin and the diversification of B3 domains in plants, we combined comparative phylogenetic analysis with exon/intron structure and duplication events. In addition, we investigated the conservation and divergence of the B3 domain during the origin and evolution of each family. Conclusions: Our data indicate that showed that the B3 containing genes have undergone extensive duplication events, and that the REM family B3 domain has a highly diverged DNA binding. Our results also indicate that the founding member of the B3 gene family is likely to be similar to the ABI3/HSI genes found in C. reinhardtii and V. carteri. Among the B3 families, ABI3, HSI, RAV and ARF are most structurally conserved, whereas the REM family has experienced a rapid divergence. Thes

The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes

BACKGROUND: Transcription factors of the basic leucine zipper (bZIP) family control important processes in all eukaryotes. In plants, bZIPs are regulators of many central developmental and physiological processes including photomorphogenesis, leaf and seed formation, energy homeostasis, and abiotic and biotic stress responses. Here we performed a comprehensive phylogenetic analysis of bZIP genes from algae, mosses, ferns, gymnosperms and angiosperms. METHODOLOGY/PRINCIPAL FINDINGS: We identified 13 groups of bZIP homologues in angiosperms, three more than known before, that represent 34 Possible Groups of Orthologues (PoGOs). The 34 PoGOs may correspond to the complete set of ancestral angiosperm bZIP genes that participated in the diversification of flowering plants. Homologous genes dedicated to seed-related processes and ABA-mediated stress responses originated in the common ancestor of seed plants, and three groups of homologues emerged in the angiosperm lineage, of which one group plays a role in optimizing the use of energy. CONCLUSIONS/SIGNIFICANCE: Our data suggest that the ancestor of green plants possessed four bZIP genes functionally involved in oxidative stress and unfolded protein responses that are bZIP-mediated processes in all eukaryotes, but also in light-dependent regulations. The four founder genes amplified and diverged significantly, generating traits that benefited the colonization of new environments

SnRK2 protein kinases represent an ancient system in plants for adaptation to a terrestrial environment

The SNF1-related protein kinase 2 (SnRK2) family includes key regulators of osmostress and abscisic acid (ABA) responses in angiosperms and can be classified into three subclasses. Subclass III SnRK2s act in the ABA response while ABA-nonresponsive subclass I SnRK2s are regulated through osmostress. Here we report that an ancient subclass III SnRK2-based signalling module including ABA and an upstream Raf-like kinase (ARK) exclusively protects the moss Physcomitrella patens from drought. Subclass III SnRK2s from both Arabidopsis and from the semiterrestrial alga Klebsormidium nitens, which contains all the components of ABA signalling except ABA receptors, complement Physcomitrella snrk2− mutants, whereas Arabidopsis subclass I SnRK2 cannot. We propose that the earliest land plants developed the ABA/ARK/subclass III SnRK2 signalling module by recruiting ABA to regulate a pre-existing dehydration response and that subsequently a novel subclass I SnRK2 system evolved in vascular plants conferring osmostress protection independently from the ancient system

Regulation of the ABA-responsive Em promoter by ABI3 in the moss Physcomitrella patens: Role of the ABA response element and the RY element

The plant-specific transcription factor ABSCISIC ACID IN SENSITIVE3 (ABI3) or the maize ortholog VIVIPAROUS1 (VP1) is known to regulate seed maturation and germination in concert with the phytohormone abscisic acid (ABA) but is also evolutionarily conserved among land plants including non-seed plants. An ABI3/VP1 ortholog (PpABI3A) from the moss Physcomitrella patens can activate ABA-responsive gene promoters in the moss and angiosperms; however, it failed to fully complement the phenotypes of the Arabidopsis abi3-6 mutant, suggesting that some aspects of ABI3/VP1 functions have diverged during the evolution of land plants. To gain insights into the evolution of ABI3/VP1 function, we performed a comparative analysis of the regulatory elements required for ABI3 activation in Physcomitrella using a wheat Em gene promoter, which is induced by ABA and ABI3/VP1 both in Physcomitrella and in angiosperms. Elimination of either the ACGT core motif in the ABA response element (ABRE) or the RY element, to which ABI3/VP1 binds directly, resulted in a drastic reduction of the ABA response in Physcomitrella. Arabidopsis ABI3 could effectively activate the Em promoter either in an ABRE- or RY-dependent manner, as observed in angiosperms. On the other hand, PpABI3A failed to activate an Em promoter lacking the RY element but not the ABRE. These results suggest that RY-mediated transcriptional regulation of ABI3/VP1 is evolutionarily conserved between the moss and angiosperms, whereas angiosperm ABI3/VP1 has evolved to activate ABA-inducible promoters via the ABRE sequence independently from the RY element