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.
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- NSF-PAR ID:
- 10368496
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Plant Physiology
- Volume:
- 189
- Issue:
- 3
- ISSN:
- 0032-0889
- Format(s):
- Medium: X Size: p. 1519-1535
- Size(s):
- ["p. 1519-1535"]
- Sponsoring Org:
- National Science Foundation
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Summary Plants being sessile integrate information from a variety of endogenous and external cues simultaneously to optimize growth and development. This necessitates the signaling networks in plants to be highly dynamic and flexible. One such network involves heterotrimeric G‐proteins comprised of Gα, Gβ, and Gγ subunits, which influence many aspects of growth, development, and stress response pathways. In plants such as Arabidopsis, a relatively simple repertoire of G‐proteins comprised of one canonical and three extra‐large Gα, one Gβ and three Gγ subunits exists. Because the Gβ and Gγ proteins form obligate dimers, the phenotypes of plants lacking the sole
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Heterotrimeric GTP-binding proteins (G proteins), consisting of Gα, Gβ and Gγ subunits, transduce signals from a diverse range of extracellular stimuli, resulting in the regulation of numerous cellular and physiological functions in Eukaryotes. According to the classic G protein paradigm established in animal models, the bound guanine nucleotide on a Gα subunit, either guanosine diphosphate (GDP) or guanosine triphosphate (GTP) determines the inactive or active mode, respectively. In plants, there are two types of Gα subunits: canonical Gα subunits structurally similar to their animal counterparts and unconventional extra-large Gα subunits (XLGs) containing a C-terminal domain homologous to the canonical Gα along with an extended N-terminal domain. Both Gα and XLG subunits interact with Gβγ dimers and regulator of G protein signalling (RGS) protein. Plant G proteins are implicated directly or indirectly in developmental processes, stress responses, and innate immunity. It is established that despite the substantial overall similarity between plant and animal Gα subunits, they convey signalling differently including the mechanism by which they are activated. This review emphasizes the unique characteristics of plant Gα subunits and speculates on their unique signalling mechanisms.more » « less
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