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Heterotrimeric G-protein-mediated signaling is a key mechanism to transduce a multitude of endogenous and environmental signals in diverse organisms. The scope and expectations of plant G-protein research were set by pioneering work in metazoans. Given the similarity of the core constituents, G-protein-signaling mechanisms were presumed to be universally conserved. However, because of the enormous diversity of survival strategies and endless forms among eukaryotes, the signal, its interpretation, and responses vary even among different plant groups. Earlier G-protein research in arabidopsis (Arabidopsis thaliana) has emphasized its divergence from Metazoa. Here, we compare recent evidence from diverse plant lineages with the available arabidopsis G-protein model and discuss the conserved and novel protein components, signaling mechanisms, and response regulation.more » « less
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Abstract Plants perceive a multitude of environmental signals and stresses, and integrate their response to them in ways that culminate in modified phenotypes, optimized for plant survival. This ability of plants, known as phenotypic plasticity, is found throughout evolution, in all plant lineages. For any given environment, the specifics of the response to a particular signal may vary depending on the plants’ unique physiology and ecological niche. The bryophyte lineage, including mosses, which diverged from the vascular plants ~450–430 million years ago, represent a unique ecological and phylogenetic group in plant evolution. Several aspects of the moss life cycle, their morphology including the presence of specialized tissue types and distinct anatomical features, gene repertoires and networks, as well as the habitat differ significantly from those of vascular plants. To evaluate the outcomes of these differences, we explore the phenotypic responses of mosses to environmental signals such as light, temperature, CO2, water, nutrients, and gravity, and compare those with what is known in vascular plants. We also outline knowledge gaps and formulate testable hypotheses based on the contribution of anatomical and molecular factors to specific phenotypic responses.more » « less
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Summary Mosses hold a unique position in plant evolution and are crucial for protecting natural, long‐term carbon storage systems such as permafrost and bogs. Due to small stature, mosses grow close to the soil surface and are exposed to high levels of CO2, produced by soil respiration. However, the impact of elevated CO2(eCO2) levels on mosses remains underexplored.We determined the growth responses of the mossPhyscomitrium patensto eCO2in combination with different nitrogen levels and characterized the underlying physiological and metabolic changes.Three distinct growth characteristics, an early transition to caulonema, the development of longer, highly pigmented rhizoids, and increased biomass, define the phenotypic responses ofP. patensto eCO2. Elevated CO2impacts growth by enhancing the level of a sugar signaling metabolite, T6P. The quantity and form of nitrogen source influences these metabolic and phenotypic changes. Under eCO2,P. patensexhibits a diffused growth pattern in the presence of nitrate, but ammonium supplementation results in dense growth with tall gametophores, demonstrating high phenotypic plasticity under different environments.These results provide a framework for comparing the eCO2responses ofP. patenswith other plant groups and provide crucial insights into moss growth that may benefit climate change models.more » « less
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Abstract Heterotrimeric G-proteins modulate multiple signaling pathways in many eukaryotes. In plants, G-proteins have been characterized primarily from a few model angiosperms and a moss. Even within this small group, they seem to affect plant phenotypes differently: G-proteins are essential for survival in monocots, needed for adaptation but are nonessential in eudicots, and are required for life cycle completion and transition from the gametophytic to sporophytic phase in the moss Physcomitrium (Physcomitrella) patens. The classic G-protein heterotrimer consists of three subunits: one Gα, one Gβ and one Gγ. The Gα protein is a catalytically active GTPase and, in its active conformation, interacts with downstream effectors to transduce signals. Gα proteins across the plant evolutionary lineage show a high degree of sequence conservation. To explore the extent to which this sequence conservation translates to their function, we complemented the well-characterized Arabidopsis Gα protein mutant, gpa1, with Gα proteins from different plant lineages and with the yeast Gpa1 and evaluated the transgenic plants for different phenotypes controlled by AtGPA1. Our results show that the Gα protein from a eudicot or a monocot, represented by Arabidopsis and Brachypodium, respectively, can fully complement all gpa1 phenotypes. However, the basal plant Gα failed to complement the developmental phenotypes exhibited by gpa1 mutants, although the phenotypes that are exhibited in response to various exogenous signals were partially or fully complemented by all Gα proteins. Our results offer a unique perspective on the evolutionarily conserved functions of G-proteins in plants.more » « less
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Abstract Heterotrimeric G-protein complexes comprising Gα-, Gβ-, and Gγ-subunits and the regulator of G-protein signaling (RGS) are conserved across most eukaryotic lineages. Signaling pathways mediated by these proteins influence overall growth, development, and physiology. In plants, this protein complex has been characterized primarily from angiosperms with the exception of spreading-leaved earth moss (Physcomitrium patens) and Chara braunii (charophytic algae). Even within angiosperms, specific G-protein components are missing in certain species, whereas unique plant-specific variants—the extra-large Gα (XLGα) and the cysteine-rich Gγ proteins—also exist. The distribution and evolutionary history of G-proteins and their function in nonangiosperm lineages remain mostly unknown. We explored this using the wealth of available sequence data spanning algae to angiosperms representing extant species that diverged approximately 1,500 million years ago, using BLAST, synteny analysis, and custom-built Hidden Markov Model profile searches. We show that a minimal set of components forming the XLGαβγ trimer exists in the entire land plant lineage, but their presence is sporadic in algae. Additionally, individual components have distinct evolutionary histories. The XLGα exhibits many lineage-specific gene duplications, whereas Gα and RGS show several instances of gene loss. Similarly, Gβ remained constant in both number and structure, but Gγ diverged before the emergence of land plants and underwent changes in protein domains, which led to three distinct subtypes. These results highlight the evolutionary oddities and summarize the phyletic patterns of this conserved signaling pathway in plants. They also provide a framework to formulate pertinent questions on plant G-protein signaling within an evolutionary context.more » « less
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Summary The plant hormone abscisic acid (ABA) plays crucial roles in regulation of stress responses and growth modulation. Heterotrimeric G‐proteins are key mediators of ABA responses. Both ABA and G‐proteins have also been implicated in intracellular redox regulation; however, the extent to which reversible protein oxidation manipulates ABA and/or G‐protein signaling remains uncharacterized.To probe the role of reversible protein oxidation in plant stress response and its dependence on G‐proteins, we determined the ABA‐dependent reversible redoxome of wild‐type and Gβ‐protein null mutantagb1of Arabidopsis.We quantified 6891 uniquely oxidized cysteine‐containing peptides, 923 of which show significant changes in oxidation following ABA treatment. The majority of these changes required the presence of G‐proteins. Divergent pathways including primary metabolism, reactive oxygen species response, translation and photosynthesis exhibited both ABA‐ and G‐protein‐dependent redox changes, many of which occurred on proteins not previously linked to them.We report the most comprehensive ABA‐dependent plant redoxome and uncover a complex network of reversible oxidations that allow ABA and G‐proteins to rapidly adjust cellular signaling to adapt to changing environments. Physiological validation of a subset of these observations suggests that functional G‐proteins are required to maintain intracellular redox homeostasis and fully execute plant stress responses.more » « less
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Summary Plant responses to abiotic environmental challenges are known to have lasting effects on the plant beyond the initial stress exposure. Some of these lasting effects are transgenerational, affecting the next generation. The plant response to elevated carbon dioxide (CO2) levels has been well studied. However, these investigations are typically limited to plants grown for a single generation in a high CO2environment while transgenerational studies are rare.We aimed to determine transgenerational growth responses in plants after exposure to high CO2by investigating the direct progeny when returned to baseline CO2levels.We found that both the flowering plantArabidopsis thalianaand seedless nonvascular plantPhyscomitrium patenscontinue to display accelerated growth rates in the progeny of plants exposed to high CO2. We used the model species Arabidopsis to dissect the molecular mechanism and found that DNA methylation pathways are necessary for heritability of this growth response.More specifically, the pathway of RNA‐directed DNA methylation is required to initiate methylation and the proteins CMT2 and CMT3 are needed for the transgenerational propagation of this DNA methylation to the progeny plants. Together, these two DNA methylation pathways establish and then maintain a cellular memory to high CO2exposure.more » « less