Are plant traits drivers of endophytic communities in seasonally flooded tropical forests?

PREMISE: In the Amazon basin, seasonally flooded (SF) forests offer varying water constraints, providing an excellent way to investigate the role of habitat selection on microbial communities within plants. However, variations in the microbial community among host plants cannot solely be attributed to environmental factors, and how plant traits contribute to microbial assemblages remains an open question. METHODS: We described leaf- and root-associated microbial communities using ITS2 and 16 S high-throughput sequencing and investigated the stochastic-deterministic balance shaping these community assemblies using two null models. Plant ecophysiological functioning was evaluated by focusing on 10 leaf and root traits in 72 seedlings, belonging to seven tropical SF tree species in French Guiana. We then analyzed how root and leaf traits drove the assembly of endophytic communities. RESULTS: While both stochastic and deterministic processes governed the endophyte assembly in the leaves and roots, stochasticity prevailed. Discrepancies were found between fungi and bacteria, highlighting that these microorganisms have distinct ecological strategies within plants. Traits, especially leaf traits, host species and spatial predictors better explained diversity than composition, but they were modest predictors overall. CONCLUSIONS: This study widens our knowledge about tree species in SF forests, a habitat sensitive to climate change, through the combined analyses of their associated microbial communities with functional traits. We emphasize the need to investigate other plant traits to better disentangle the drivers of the relationship between seedlings and their associated microbiomes, ultimately enhancing their adaptive capacities to climate change.

Low-frequency somatic mutations are heritable in tropical trees Dicorynia guianensis and Sextonia rubra.

Somatic mutations potentially play a role in plant evolution, but common expectations pertaining to plant somatic mutations remain insufficiently tested. Unlike in most animals, the plant germline is assumed to be set aside late in development, leading to the expectation that plants accumulate somatic mutations along growth. Therefore, several predictions were made on the fate of somatic mutations: mutations have generally low frequency in plant tissues; mutations at high frequency have a higher chance of intergenerational transmission; branching topology of the tree dictates mutation distribution; and exposure to UV (ultraviolet) radiation increases mutagenesis. To provide insights into mutation accumulation and transmission in plants, we produced two high-quality reference genomes and a unique dataset of 60 high-coverage whole-genome sequences of two tropical tree species, Dicorynia guianensis (Fabaceae) and Sextonia rubra (Lauraceae). We identified 15,066 de novo somatic mutations in D. guianensis and 3,208 in S. rubra, surprisingly almost all found at low frequency. We demonstrate that 1) low-frequency mutations can be transmitted to the next generation; 2) mutation phylogenies deviate from the branching topology of the tree; and 3) mutation rates and mutation spectra are not demonstrably affected by differences in UV exposure. Altogether, our results suggest far more complex links between plant growth, aging, UV exposure, and mutation rates than commonly thought.

Venomics survey of six myrmicine ants provides insights into the molecular and structural diversity of their peptide toxins.

Among ants, Myrmicinae represents the most speciose subfamily. The venom composition previously described for these social insects is extremely variable, with alkaloids predominant in some genera while, conversely, proteomics studies have revealed that some myrmicine ant venoms are peptide-rich. Using integrated transcriptomic and proteomic approaches, we characterized the venom peptidomes of six ants belonging to the different tribes of Myrmicinae. We identified a total of 79 myrmicitoxins precursors which can be classified into 38 peptide families according to their mature sequences. Myrmicine ant venom peptidomes showed heterogeneous compositions, with linear and disulfide-bonded monomers as well as dimeric toxins. Several peptide families were exclusive to a single venom whereas some were retrieved in multiple species. A hierarchical clustering analysis of precursor signal sequences led us to divide the myrmicitoxins precursors into eight families, including some that have already been described in other aculeate hymenoptera such as secapin-like peptides and voltage-gated sodium channel (NaV) toxins. Evolutionary and structural analyses of two representatives of these families highlighted variation and conserved patterns that might be crucial to explain myrmicine venom peptide functional adaptations to biological targets.

Microgeographic local adaptation and ecotype distributions: The role of selective processes on early life-history traits in sympatric, ecologically divergent Symphonia populations.

Trees are characterized by the large number of seeds they produce. Although most of those seeds will never germinate, plenty will. Of those which germinate, many die young, and eventually, only a minute fraction will grow to adult stage and reproduce. Is this just a random process? Do variations in germination and survival at very young stages rely on variations in adaptations to microgeographic heterogeneity? and do these processes matter at all in determining tree species distribution and abundance? We have studied these questions with the Neotropical Symphonia tree species. In the Guiana shield, Symphonia are represented by at least two sympatric taxa or ecotypes, Symphonia globulifera found almost exclusively in bottomlands, and a yet undescribed more generalist taxon/ecotype, Symphonia sp1. A reciprocal transplantation experiment (510 seeds, 16 conditions) was set up and followed over the course of 6 years to evaluate the survival and performance of individuals from different ecotypes and provenances. Germination, survival, growth, and herbivory showed signs of local adaptation, with some combinations of ecotypes and provenances growing faster and surviving better in their own habitat or provenance region. S. globulifera was strongly penalized when planted outside its home habitat but showed the fastest growth rates when planted in its home habitat, suggesting it is a specialist of a high-risk high-gain strategy. Conversely, S. sp1 behaved as a generalist, performing well in a variety of environments. The differential performance of seeds and seedlings in the different habitats matches the known distribution of both ecotypes, indicating that environmental filtering at the very early stages can be a key determinant of tree species distributions, even at the microgeographic level and among very closely related taxa. Furthermore, such differential performance also contributes to explain, in part, the maintenance of the different Symphonia ecotypes living in intimate sympatry despite occasional gene flow.

SNP Markers as a Successful Molecular Tool for Assessing Species Identity and Geographic Origin of Trees in the Economically Important South American Legume Genus Dipteryx.

Dipteryx timber has been heavily exploited in South America since 2000s due to the increasing international demand for hardwood. Developing tools for the genetic identification of Dipteryx species and their geographical origin can help to promote legal trading of timber. A collection of 800 individual trees, belonging to 6 different Dipteryx species, was genotyped based on 171 molecular markers. After the exclusion of markers out of Hardy-Weinberg equilibrium or with no polymorphism or low amplification, 83 nuclear, 29 chloroplast, 13 mitochondrial single nucleotide polymorphisms (SNPs), and 2 chloroplast and 5 mitochondrial INDELS remained. Six genetic groups were identified using Bayesian Structure analyses of the nuclear SNPs, which corresponded to the different Dipteryx species collected in the field. Seventeen highly informative markers were identified as suitable for species identification and obtained self-assignment success rates to species level of 78-96%. An additional set of 15 molecular markers was selected to determine the different genetic clusters found in Dipteryx odorata and Dipteryx ferrea, obtaining self-assignment success rates of 91-100%. The success to assign samples to the correct country of origin using all or only the informative markers improved when using the nearest neighbor approach (69-92%) compared to the Bayesian approach (33-80%). While nuclear and chloroplast SNPs were more suitable for differentiating the different Dipteryx species, mitochondrial SNPs were ideal for determining the genetic clusters of D. odorata and D. ferrea. These 32 selected SNPs will be invaluable genetic tools for the accurate identification of species and country of origin of Dipteryx timber.

Fine-scale genetic structure and gene dispersal inferences in 10 neotropical tree species.

The extent of gene dispersal is a fundamental factor of the population and evolutionary dynamics of tropical tree species, but directly monitoring seed and pollen movement is a difficult task. However, indirect estimates of historical gene dispersal can be obtained from the fine-scale spatial genetic structure of populations at drift-dispersal equilibrium. Using an approach that is based on the slope of the regression of pairwise kinship coefficients on spatial distance and estimates of the effective population density, we compare indirect gene dispersal estimates of sympatric populations of 10 tropical tree species. We re-analysed 26 data sets consisting of mapped allozyme, SSR (simple sequence repeat), RAPD (random amplified polymorphic DNA) or AFLP (amplified fragment length polymorphism) genotypes from two rainforest sites in French Guiana. Gene dispersal estimates were obtained for at least one marker in each species, although the estimation procedure failed under insufficient marker polymorphism, limited sample size, or inappropriate sampling area. Estimates generally suffered low precision and were affected by assumptions regarding the effective population density. Averaging estimates over data sets, the extent of gene dispersal ranged from 150 m to 1200 m according to species. Smaller gene dispersal estimates were obtained in species with heavy diaspores, which are presumably not well dispersed, and in populations with high local adult density. We suggest that limited seed dispersal could indirectly limit effective pollen dispersal by creating higher local tree densities, thereby increasing the positive correlation between pollen and seed dispersal distances. We discuss the potential and limitations of our indirect estimation procedure and suggest guidelines for future studies.