Within the plant microbiota, mutualistic fungal and bacterial symbionts are striking examples of microorganisms playing crucial roles in nutrient acquisition. They have coevolved with their hosts ...since initial plant adaptation to land. Despite the evolutionary distances that separate mycorrhizal and nitrogen-fixing symbioses, these associations share a number of highly conserved features, including specific plant symbiotic signaling pathways, root colonization strategies that circumvent plant immune responses, functional host-microbe interface formation, and the central role of phytohormones in symbiosis-associated root developmental pathways. We highlight recent and emerging areas of investigation relating to these evolutionarily conserved mechanisms, with an emphasis on the more ancestral mycorrhizal associations, and consider to what extent this knowledge can contribute to an understanding of plant-microbiota associations as a whole.
Summary
Microorganisms, or ‘microbes’, have formed intimate associations with plants throughout the length of their evolutionary history. In extant plant systems microbes still remain an integral ...part of the ecological landscape, impacting plant health, productivity and long‐term fitness. Therefore, to properly understand the genetic wiring of plants, we must first determine what perception systems plants have evolved to parse beneficial from commensal from pathogenic microbes. In this review, we consider some of the most recent advances in how plants respond at the molecular level to different microbial lifestyles. Further, we cover some of the means by which microbes are able to manipulate plant signaling pathways through altered destructiveness and nutrient sinks, as well as the use of effector proteins and micro‐RNAs (miRNAs). We conclude by highlighting some of the major questions still to be answered in the field of plant‐microbe research, and suggest some of the key areas that are in greatest need of further research investment. The results of these proposed studies will have impacts in a wide range of plant research disciplines and will, ultimately, translate into stronger agronomic crops and forestry stock, with immune perception and response systems bred to foster beneficial microbial symbioses while repudiating pathogenic symbioses.
Significance Statement
Ecological research is increasingly demonstrating that the microbes associated with plant tissues have as much, if not more, impact on plant physiology and fitness than the plant genome itself. Therefore, when studying plant systems, we must take into account the role of plant‐microbe symbioses. We review, here, recent advances in our understanding of how plants interact with their microbial community and highlight areas of pressing need for further research investment.
1406 I. 1407 II. 1408 III. 1410 IV. 1411 V. 1413 VI. 1416 VII. 1418 1418 References 1419 SUMMARY: Almost all land plants form symbiotic associations with mycorrhizal fungi. These below‐ground fungi ...play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi and many plant species depend on these symbionts for growth and survival. Estimates suggest that there are c. 50 000 fungal species that form mycorrhizal associations with c. 250 000 plant species. The development of high‐throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large‐scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant–fungal partners as complex underground multi‐species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.
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.
The concurrent development of high-throughput genotyping platforms and next generation sequencing (NGS) has increased the number and density of genetic markers, the efficiency of constructing ...detailed linkage maps, and our ability to overlay recombination and physical maps of the genome. We developed an array for tomato with 8,784 Single Nucleotide Polymorphisms (SNPs) mainly discovered based on NGS-derived transcriptome sequences. Of the SNPs, 7,720 (88%) passed manufacturing quality control and could be scored in tomato germplasm. The array was used to generate high-density linkage maps for three interspecific F(2) populations: EXPEN 2000 (Solanum lycopersicum LA0925 x S. pennellii LA0716, 79 individuals), EXPEN 2012 (S. lycopersicum Moneymaker x S. pennellii LA0716, 160 individuals), and EXPIM 2012 (S. lycopersicum Moneymaker x S. pimpinellifolium LA0121, 183 individuals). The EXPEN 2000-SNP and EXPEN 2012 maps consisted of 3,503 and 3,687 markers representing 1,076 and 1,229 unique map positions (genetic bins), respectively. The EXPEN 2000-SNP map had an average marker bin interval of 1.6 cM, while the EXPEN 2012 map had an average bin interval of 0.9 cM. The EXPIM 2012 map was constructed with 4,491 markers (1,358 bins) and an average bin interval of 0.8 cM. All three linkage maps revealed an uneven distribution of markers across the genome. The dense EXPEN 2012 and EXPIM 2012 maps showed high levels of colinearity across all 12 chromosomes, and also revealed evidence of small inversions between LA0716 and LA0121. Physical positions of 7,666 SNPs were identified relative to the tomato genome sequence. The genetic and physical positions were mostly consistent. Exceptions were observed for chromosomes 3, 10 and 12. Comparing genetic positions relative to physical positions revealed that genomic regions with high recombination rates were consistent with the known distribution of euchromatin across the 12 chromosomes, while very low recombination rates were observed in the heterochromatic regions.
The roots of Arabidopsis thaliana host diverse fungal communities that affect plant health and disease states. Here, we sequence the genomes of 41 fungal isolates representative of the A. thaliana ...root mycobiota for comparative analysis with other 79 plant-associated fungi. Our analyses indicate that root mycobiota members evolved from ancestors with diverse lifestyles and retain large repertoires of plant cell wall-degrading enzymes (PCWDEs) and effector-like small secreted proteins. We identify a set of 84 gene families associated with endophytism, including genes encoding PCWDEs acting on xylan (family GH10) and cellulose (family AA9). Transcripts encoding these enzymes are also part of a conserved transcriptional program activated by phylogenetically-distant mycobiota members upon host contact. Recolonization experiments with individual fungi indicate that strains with detrimental effects in mono-association with the host colonize roots more aggressively than those with beneficial activities, and dominate in natural root samples. Furthermore, we show that the pectin-degrading enzyme family PL1_7 links aggressiveness of endophytic colonization to plant health.
• Endogonales (Mucoromycotina), composed of Endogonaceae and Densosporaceae, is the only known non-Dikarya order with ectomycorrhizal members. They also form mycorrhizallike association with some ...nonspermatophyte plants. It has been recently proposed that Endogonales were among the earliest mycorrhizal partners with land plants. It remains unknown whether Endogonales possess genomes with mycorrhizal-lifestyle signatures and whether Endogonales originated around the same time as land plants did.
• We sampled sporocarp tissue from four Endogonaceae collections and performed shotgun genome sequencing. After binning the metagenome data, we assembled and annotated the Endogonaceae genomes. We performed comparative analysis on plant-cell-wall-degrading enzymes (PCWDEs) and small secreted proteins (SSPs). We inferred phylogenetic placement of Endogonaceae and estimated the ages of Endogonaceae and Endogonales with expanded taxon sampling.
• Endogonaceae have large genomes with high repeat content, low diversity of PCWDEs, but without elevated SSP/secretome ratios. Dating analysis estimated that Endogonaceae originated in the Permian–Triassic boundary and Endogonales originated in the mid–late Silurian. Mycoplasma-related endobacterium sequences were identified in three Endogonaceae genomes.
• Endogonaceae genomes possess typical signatures of mycorrhizal lifestyle. The early origin of Endogonales suggests that the mycorrhizal association between Endogonales and plants might have played an important role during the colonization of land by plants.
Glomeromycotina is a lineage of early diverging fungi that establish arbuscular mycorrhizal (AM) symbiosis with land plants. Despite their major ecological role, the genetic basis of their obligate ...mutualism remains largely unknown, hindering our understanding of their evolution and biology.
We compared the genomes of Glomerales (Rhizophagus irregularis, Rhizophagus diaphanus, Rhizophagus cerebriforme) and Diversisporales (Gigaspora rosea) species, together with those of saprotrophic Mucoromycota, to identify gene families and processes associated with these lineages and to understand the molecular underpinning of their symbiotic lifestyle.
Genomic features in Glomeromycotina appear to be very similar with a very high content in transposons and protein-coding genes, extensive duplications of protein kinase genes, and loss of genes coding for lignocellulose degradation, thiamin biosynthesis and cytosolic fatty acid synthase. Most symbiosis-related genes in R. irregularis and G. rosea are specific to Glomeromycotina. We also confirmed that the present species have a homokaryotic genome organisation.
The high interspecific diversity of Glomeromycotina gene repertoires, affecting all known protein domains, as well as symbiosis-related orphan genes, may explain the known adaptation of Glomeromycotina to a wide range of environmental settings. Our findings contribute to an increasingly detailed portrait of genomic features defining the biology of AM fungi.
Changing diet and physical activity behaviour is one of the cornerstones of type 2 diabetes treatment, but changing behaviour is challenging. The objective of this study was to identify behaviour ...change techniques (BCTs) and intervention features of dietary and physical activity interventions for patients with type 2 diabetes that are associated with changes in HbA
and body weight.
We performed a systematic review of papers published between 1975-2015 describing randomised controlled trials (RCTs) that focused exclusively on both diet and physical activity. The constituent BCTs, intervention features and methodological rigour of these interventions were evaluated. Changes in HbA
and body weight were meta-analysed and examined in relation to use of BCTs.
Thirteen RCTs were identified. Meta-analyses revealed reductions in HbA
at 3, 6, 12 and 24 months of -1.11 % (12 mmol/mol), -0.67 % (7 mmol/mol), -0.28 % (3 mmol/mol) and -0.26 % (2 mmol/mol) with an overall reduction of -0.53 % (6 mmol/mol 95 % CI -0.74 to -0.32, P < 0.00001) in intervention groups compared to control groups. Meta-analyses also showed a reduction in body weight of -2.7 kg, -3.64 kg, -3.77 kg and -3.18 kg at 3, 6, 12 and 24 months, overall reduction was -3.73 kg (95 % CI -6.09 to -1.37 kg, P = 0.002). Four of 46 BCTs identified were associated with >0.3 % reduction in HbA
: 'instruction on how to perform a behaviour', 'behavioural practice/rehearsal', 'demonstration of the behaviour' and 'action planning', as were intervention features 'supervised physical activity', 'group sessions', 'contact with an exercise physiologist', 'contact with an exercise physiologist and a dietitian', 'baseline HbA
>8 %' and interventions of greater frequency and intensity.
Diet and physical activity interventions achieved clinically significant reductions in HbA
at three and six months, but not at 12 and 24 months. Specific BCTs and intervention features identified may inform more effective structured lifestyle intervention treatment strategies for type 2 diabetes.
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