Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium-and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.symbiosis | plant evolution | algae | plant-microbe interactions | phylogeny T he colonization of land by plants 450 Mya created a major transition on Earth, causing the burial of large amounts of carbon, with resultant decreases in atmospheric CO 2 leading to a dramatically altered climate. This transition provided the foundation for the majority of extant terrestrial ecosystems (1, 2). The terrestrial environment that these early plants colonized must have presented many challenges, primary among them being the acquisition of mineral nutrients. It has been suggested that the appearance of the arbuscular mycorrhizal (AM) symbiosis and other beneficial associations with fungi such as Mucoromycotina facilitated this colonization of land by improving plants' ability to capture nutrients.Based on recent phylogenetic analyses, Zygnematales, one of the paraphyletic "advanced charophytes" (i.e., Coleochaetales, Charales, and Zygnematales), has been identified as the closest green algal relative to land plants, whereas the chlorophytes diverged much earlier (Fig. 1A) (3, 4). On the other side of this transition, bryophyte lineages (i.e., liverworts, mosses, and hornworts) are considered to be the earliest diverging land plants, although their branching order remains debated (5-7). Key innovations present in bryophytes but not in advanced charophytes thus are good candidates for understanding the basis of land colonization by plants. In support of previous suppositions, one innovation that discriminates bryophytes from charophytes is the ability to develop beneficial ass...

Little is known about the genetic basis of convergent traits that originate repeatedly over broad taxonomic scales. The myogenic electric organ has evolved six times in fishes to produce electric fields used in communication, navigation, predation, or defense. We have examined the genomic basis of the convergent anatomical and physiological origins of these organs by assembling the genome of the electric eel (Electrophorus electricus) and sequencing electric organ and skeletal muscle transcriptomes from three lineages that have independently evolved electric organs. Our results indicate that, despite millions of years of evolution and large differences in the morphology of electric organ cells, independent lineages have leveraged similar transcription factors and developmental and cellular pathways in the evolution of electric organs.

Symbiotic associations between legumes and rhizobia usually commence with the perception of bacterial lipochitooligosaccharides, known as Nod factors (NF), which triggers rapid cellular and molecular responses in host plants. We report here deep untargeted tandem mass spectrometry-based measurements of rapid NF-induced changes in the phosphorylation status of 13,506 phosphosites in 7739 proteins from the model legume Medicago truncatula. To place these phosphorylation changes within a biological context, quantitative phosphoproteomic and RNA measurements in wild-type plants were compared with those observed in mutants, one defective in NF perception (nfp) and one defective in downstream signal transduction events (dmi3). Our study quantified the early phosphorylation and transcription dynamics that are specifically associated with NF-signaling, confirmed a dmi3-mediated feedback loop in the pathway, and suggested "cryptic" NF-signaling pathways, some of them being also involved in the response to symbiotic arbuscular mycorrhizal fungi. Legumes have the ability to form a very efficient symbiotic association with rhizobia to meet their nitrogen demand. This results in root nodule formation, inside which the rhizobia can fix atmospheric nitrogen efficiently and transfer it to the plants, in exchange for a carbon source. This interaction is often characterized by a high level of host specificity and generally requires an exchange of diffusible signals between legumes and rhizobia. Flavonoids and isoflavonoids present in the legume root exudates induce the expression of nod genes in rhizobia, and are responsible for the production and secretion of bacterial lipochitooligosaccharides (LCOs), known as Nod factors (NF) 1 (1, 2). NF are generally required for rhizobial infection and nodule development. Mere application of purified NF at low concentrations (10 Ϫ8 to 10 Ϫ12 M) is sufficient to trigger responses in host plants similar to those elicited by the rhizobia themselves (2, 3). Responses are elicited in root cells within a few seconds to minutes after NF application and include changes in ion fluxes across the plasma membrane, as well as accumulation of reactive oxygen species (4, 5). After 15-20 min, oscillations of the nuclear and perinuclear calcium concentration (calcium spiking) are initiated and trigger the expression of early nodulin genes (3). Within the first hour, legume root hairs undergo a cytoplasmic disorganization ,which leads to a transient swelling (6), followed by root hair deformations (7).Forward and reverse genetic approaches, in the model legumes Medicago truncatula (Medicago) and Lotus japonicus (Lotus), have identified several components controlling these events (Fig. 1). NF are perceived with high specificity by LysM receptor-like kinases residing on the plasma membrane. These kinases include nod factor perception (NFP), an essential component of a signaling receptor necessary for early responses to NF and rhizobial infection (8, 9). Mutants in NFP are affected in all known cellular respons...

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Legumes are essential components of agricultural systems because they enrich the soil in nitrogen and require little environmentally deleterious fertilizers. A complex symbiotic association between legumes and nitrogen-fixing soil bacteria called rhizobia culminates in the development of root nodules, where rhizobia fix atmospheric nitrogen and transfer it to their plant host. Here we describe a quantitative proteomic atlas of the model legume Medicago truncatula and its rhizobial symbiont Sinorhizobium meliloti, which includes more than 23,000 proteins, 20,000 phosphorylation sites, and 700 lysine acetylation sites. Our analysis provides insight into mechanisms regulating symbiosis. We identify a calmodulin-binding protein as a key regulator in the host and assign putative roles and targets to host factors (bioactive peptides) that control gene expression in the symbiont. Further mining of this proteomic resource may enable engineering of crops and their microbial partners to increase agricultural productivity and sustainability.