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1.
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics.
Strullu-Derrien, C, Selosse, MA, Kenrick, P, Martin, FM
The New phytologist. 2018;(4):1012-1030
Abstract
Contents Summary 1012 I. Introduction 1013 II. The mycorrhizal symbiosis at the dawn and rise of the land flora 1014 III. From early land plants to early trees: the origin of roots and true mycorrhizas 1016 IV. The diversification of the AM symbiosis 1019 V. The ECM symbiosis 1021 VI. The recently evolved ericoid and orchid mycorrhizas 1023 VII. Limits of paleontological vs genetic approaches and perspectives 1023 Acknowledgements 1025 References 1025 SUMMARY The ability of fungi to form mycorrhizas with plants is one of the most remarkable and enduring adaptations to life on land. The occurrence of mycorrhizas is now well established in c. 85% of extant plants, yet the geological record of these associations is sparse. Fossils preserved under exceptional conditions provide tantalizing glimpses into the evolutionary history of mycorrhizas, showing the extent of their occurrence and aspects of their evolution in extinct plants. The fossil record has important roles to play in establishing a chronology of when key fungal associations evolved and in understanding their importance in ecosystems through time. Together with calibrated phylogenetic trees, these approaches extend our understanding of when and how groups evolved in the context of major environmental change on a global scale. Phylogenomics furthers this understanding into the evolution of different types of mycorrhizal associations, and genomic studies of both plants and fungi are shedding light on how the complex set of symbiotic traits evolved. Here we present a review of the main phases of the evolution of mycorrhizal interactions from palaeontological, phylogenetic and genomic perspectives, with the aim of highlighting the potential of fossil material and a geological perspective in a cross-disciplinary approach.
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2.
Nitrate-mediated control of root nodule symbiosis.
Nishida, H, Suzaki, T
Current opinion in plant biology. 2018;:129-136
Abstract
Nitrogen is an indispensable inorganic nutrient that is required by plants throughout their life. Root nodule symbiosis (RNS) is an important strategy mainly adopted by legumes to enhance nitrogen acquisition, where several key processes required for the establishment of the symbiosis, are pleiotropically controlled by nitrate availability in soil. Although the autoregulation of nodulation (AON), a systemic long-range signaling, has been suggested to be implicated in nitrate-induced control of RNS, AON alone is insufficient to fully explain the pleiotropic regulation that is induced by nitrate. A recent elucidation of the function of a NIN-LIKE PROTEIN transcription factor has provided greater insights into the genetic mechanisms underlying nitrate-induced control of RNS in varying nitrate environments.
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3.
Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii.
Jiao, J, Ni, M, Zhang, B, Zhang, Z, Young, JPW, Chan, TF, Chen, WX, Lam, HM, Tian, CF
PLoS genetics. 2018;(5):e1007428
Abstract
Prokaryotes benefit from having accessory genes, but it is unclear how accessory genes can be linked with the core regulatory network when developing adaptations to new niches. Here we determined hierarchical core/accessory subsets in the multipartite pangenome (composed of genes from the chromosome, chromid and plasmids) of the soybean microsymbiont Sinorhizobium fredii by comparing twelve Sinorhizobium genomes. Transcriptomes of two S. fredii strains at mid-log and stationary growth phases and in symbiotic conditions were obtained. The average level of gene expression, variation of expression between different conditions, and gene connectivity within the co-expression network were positively correlated with the gene conservation level from strain-specific accessory genes to genus core. Condition-dependent transcriptomes exhibited adaptive transcriptional changes in pangenome subsets shared by the two strains, while strain-dependent transcriptomes were enriched with accessory genes on the chromid. Proportionally more chromid genes than plasmid genes were co-expressed with chromosomal genes, while plasmid genes had a higher within-replicon connectivity in expression than chromid ones. However, key nitrogen fixation genes on the symbiosis plasmid were characterized by high connectivity in both within- and between-replicon analyses. Among those genes with host-specific upregulation patterns, chromosomal znu and mdt operons, encoding a conserved high-affinity zinc transporter and an accessory multi-drug efflux system, respectively, were experimentally demonstrated to be involved in host-specific symbiotic adaptation. These findings highlight the importance of integrative regulation of hierarchical core/accessory components in the multipartite genome of bacteria during niche adaptation and in shaping the prokaryotic pangenome in the long run.
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4.
Engineering yeast endosymbionts as a step toward the evolution of mitochondria.
Mehta, AP, Supekova, L, Chen, JH, Pestonjamasp, K, Webster, P, Ko, Y, Henderson, SC, McDermott, G, Supek, F, Schultz, PG
Proceedings of the National Academy of Sciences of the United States of America. 2018;(46):11796-11801
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Abstract
It has been hypothesized that mitochondria evolved from a bacterial ancestor that initially became established in an archaeal host cell as an endosymbiont. Here we model this first stage of mitochondrial evolution by engineering endosymbiosis between Escherichia coli and Saccharomyces cerevisiae An ADP/ATP translocase-expressing E. coli provided ATP to a respiration-deficient cox2 yeast mutant and enabled growth of a yeast-E. coli chimera on a nonfermentable carbon source. In a reciprocal fashion, yeast provided thiamin to an endosymbiotic E. coli thiamin auxotroph. Expression of several SNARE-like proteins in E. coli was also required, likely to block lysosomal degradation of intracellular bacteria. This chimeric system was stable for more than 40 doublings, and GFP-expressing E. coli endosymbionts could be observed in the yeast by fluorescence microscopy and X-ray tomography. This readily manipulated system should allow experimental delineation of host-endosymbiont adaptations that occurred during evolution of the current, highly reduced mitochondrial genome.
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Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi.
Field, KJ, Pressel, S
The New phytologist. 2018;(4):996-1011
Abstract
Contents Summary 996 I. Introduction 996 II. An ancient, and diverse, symbiosis 998 III. Structural diversity in ancient plant-fungal partnerships 1000 IV. Mycorrhizal unity in host plant nutrition 1002 V. Plant-to-fungus carbon transfer 1003 VI. From individuals to networks 1003 VII. Diverse responses of mycorrhizal functioning to dynamic environments 1006 VIII. Summary of future research direction 1007 Acknowledgements 1006 References 1006 SUMMARY Mycorrhizal symbiosis is an ancient and widespread mutualism between plants and fungi that facilitated plant terrestrialisation > 500 million years ago, with key roles in ecosystem functioning at multiple scales. Central to the symbiosis is the bidirectional exchange of plant-fixed carbon for fungal-acquired nutrients. Within this unifying role of mycorrhizas, considerable diversity in structure and function reflects the diversity of the partners involved. Early diverging plants form mutualisms not only with arbuscular mycorrhizal Glomeromycotina fungi, but also with poorly characterised Mucoromycotina, which may also colonise the roots of 'higher' plants as fine root endophytes. Functional diversity in these symbioses depends on both fungal and plant life histories and is influenced by the environment. Recent studies have highlighted the roles of lipids/fatty acids in plant-to-fungus carbon transport and potential contributions of Glomeromycotina fungi to plant nitrogen nutrition. Together with emerging appreciation of mycorrhizal networks as multi-species resource-sharing systems, these insights are broadening our views on mycorrhizas and their roles in nutrient cycling. It is crucial that the diverse array of biotic and abiotic factors that together shape the dynamics of carbon-for-nutrient exchange between plants and fungi are integrated, in addition to embracing the unfolding and potentially key role of Mucoromycotina fungi in these processes.
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Evolution of bidirectional costly mutualism from byproduct consumption.
Harcombe, WR, Chacón, JM, Adamowicz, EM, Chubiz, LM, Marx, CJ
Proceedings of the National Academy of Sciences of the United States of America. 2018;(47):12000-12004
Abstract
Mutualisms are essential for life, yet it is unclear how they arise. A two-stage process has been proposed for the evolution of mutualisms that involve exchanges of two costly resources. First, costly provisioning by one species may be selected for if that species gains a benefit from costless byproducts generated by a second species, and cooperators get disproportionate access to byproducts. Selection could then drive the second species to provide costly resources in return. Previously, a synthetic consortium evolved the first stage of this scenario: Salmonella enterica evolved costly production of methionine in exchange for costless carbon byproducts generated by an auxotrophic Escherichia coli Growth on agar plates localized the benefits of cooperation around methionine-secreting S. enterica Here, we report that further evolution of these partners on plates led to hypercooperative E. coli that secrete the sugar galactose. Sugar secretion arose repeatedly across replicate communities and is costly to E. coli producers, but enhances the growth of S. enterica The tradeoff between individual costs and group benefits led to maintenance of both cooperative and efficient E. coli genotypes in this spatially structured environment. This study provides an experimental example of de novo, bidirectional costly mutualism evolving from byproduct consumption. The results validate the plausibility of costly cooperation emerging from initially costless exchange, a scenario widely used to explain the origin of the mutualistic species interactions that are central to life on Earth.
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Rhizobia: from saprophytes to endosymbionts.
Poole, P, Ramachandran, V, Terpolilli, J
Nature reviews. Microbiology. 2018;(5):291-303
Abstract
Rhizobia are some of the best-studied plant microbiota. These oligotrophic Alphaproteobacteria or Betaproteobacteria form symbioses with their legume hosts. Rhizobia must exist in soil and compete with other members of the microbiota before infecting legumes and forming N2-fixing bacteroids. These dramatic lifestyle and developmental changes are underpinned by large genomes and even more complex pan-genomes, which encompass the whole population and are subject to rapid genetic exchange. The ability to respond to plant signals and chemoattractants and to colonize nutrient-rich roots are crucial for the competitive success of these bacteria. The availability of a large body of genomic, physiological, biochemical and ecological studies makes rhizobia unique models for investigating community interactions and plant colonization.
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Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond.
Keymer, A, Gutjahr, C
Current opinion in plant biology. 2018;:137-144
Abstract
Arbuscular mycorrhiza (AM) is a widespread symbiosis between most land plants and fungi of the Glomeromycotina, which has existed for more than 400million years. AM fungi (AMF) improve plant nutrition with mineral nutrients and conversely, their growth and development is fueled by organic carbon supplied from their host. Recent studies demonstrated independently and with different experimental approaches that lipids are transferred from plants to fungi in addition to sugars, and that AMF are dependent on this lipid supply because they lack genes encoding fatty acid synthase I subunits. Dependence on host lipids or lipid parasitism occur in a range of interorganismic associations with participants from almost all kingdoms. Thus, these phenomena seem rather common in mutualistic and parasitic interactions.
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First record of in vitro formation of ectomycorrhizae in Psidium cattleianum Sabine, a native Myrtaceae of the Brazilian Atlantic Forest.
Freire, CG, Giachini, AJ, Gardin, JPP, Rodrigues, AC, Vieira, RL, Baratto, CM, Werner, SS, Abreu, BH
PloS one. 2018;(5):e0196984
Abstract
Like many other species of trees native to the Brazilian Mata Atlântica (Atlantic Forest), the Myrtaceae, such as the Red Araza (Psidium cattleianum Sabine), are widely cited as arbuscular mycorrhizal formers. Nevertheless, recent studies show evidence that Myrtaceae from different tropical, subtropical and neotropical ecosystems can also prompt the formation of ectomycorrhizae, indicating that this species' ectomycorrhizal status should be further explored. Because of this, this research effort studied the in vitro interaction between the Red Araza and two ectomycorrhizal fungi isolates, belonging to the Pisolithus microcarpus (D17) and Scleroderma citrinum (UFSC-Sc133) species. An analysis was performed to determine the formation of ectomycorrhizal structures, or lack thereof, and the developmental differences between the in vitro mycorrhized and non-mycorrhized plants. The analysis proved that indeed an ectomycorrhizal association was developed between the Red Araza, and the D17 and UFSC-Sc133 isolates, a fact never before registered in the existing literature. After an in vitro period of 110 days, it was confirmed that the D17 and UFSC-Sc133 isolates formed mycorrhizal colonization of 91.6% and 15.7%, respectively. Furthermore, both isolates also promoted root thickening, and the formation of a fungal mantle and a Hartig net. However, when compared to the Control plants, the fungal isolates did not contribute to an increase in the development of the subject plants, possibly due to the specific experimental conditions used, such as a high humidity environment and high availability of nutrients in the symbiotic substrate.
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10.
Marchantia liverworts as a proxy to plants' basal microbiomes.
Alcaraz, LD, Peimbert, M, Barajas, HR, Dorantes-Acosta, AE, Bowman, JL, Arteaga-Vázquez, MA
Scientific reports. 2018;(1):12712
Abstract
Microbiomes influence plant establishment, development, nutrient acquisition, pathogen defense, and health. Plant microbiomes are shaped by interactions between the microbes and a selection process of host plants that distinguishes between pathogens, commensals, symbionts and transient bacteria. In this work, we explore the microbiomes through massive sequencing of the 16S rRNA genes of microbiomes two Marchantia species of liverworts. We compared microbiomes from M. polymorpha and M. paleacea plants collected in the wild relative to their soils substrates and from plants grown in vitro that were established from gemmae obtained from the same populations of wild plants. Our experimental setup allowed identification of microbes found in both native and in vitro Marchantia species. The main OTUs (97% identity) in Marchantia microbiomes were assigned to the following genera: Methylobacterium, Rhizobium, Paenibacillus, Lysobacter, Pirellula, Steroidobacter, and Bryobacter. The assigned genera correspond to bacteria capable of plant-growth promotion, complex exudate degradation, nitrogen fixation, methylotrophs, and disease-suppressive bacteria, all hosted in the relatively simple anatomy of the plant. Based on their long evolutionary history Marchantia is a promising model to study not only long-term relationships between plants and their microbes but also the transgenerational contribution of microbiomes to plant development and their response to environmental changes.