American Journal of Botany最新文献

Premise: Advances in transcriptomic and reduced representation genomic sequencing are deepening our understanding of how hybridization, reticulation, and environmental variation impact species diversification and genome size. Leucaena is a useful system for exploring the genomic basis of allopatric and allopolyploid speciation events and the effect of environmental pressures on genome size across 30° of latitude. We investigate phylogenetic relationships, the roles of polyploidy and hybridization in speciation, and genome size evolution in the genus.

Methods: Using newly generated RNA-sequencing data for Leucaena, we applied reference-guided and de novo phylotranscriptomics to reconstruct nuclear and organellar phylogenies. We then used comparative genome sizes from 252 samples and phylogenetic methods to investigate genome size evolution broadly and the impacts of environmental variables specifically.

Results: The phylogenetic results supported cladogenetic, rather than reticulate/hybrid, origins for most of the 19 paleotetraploid species. By contrast, gene tree data supported hybrid origins for octoploid Leucaena. The ancestral paleotetraploid genome size (1.52 pg/2 C) is relatively conserved among the paleotetraploids, rejecting our hypothesis associated with environmental variables significantly impacting genome sizes.

Conclusions: The phylogenetic results illustrate the complex interplay of intrinsic and external factors that impact speciation, including ancient whole-genome duplication (WGD), cladogenesis, secondary contact, and allopolyploidy. A weak relationship between genome size and environmental variables suggests that other factors, including paleotetraploid genomic stability, have constrained genome size variation following a WGD 16+ million years ago. The findings are consistent with a small but growing number of studies identifying groups with ancient WGDs that resist diploidization associated with gene and DNA loss.

Desiccation tolerance (DT), the ability to survive near-complete cellular dehydration, is widespread in diaspores but rare in the vegetative tissues of land plants. The patchy and punctuated phylogenetic distribution of vegetative desiccation tolerance (VDT) suggests that the trait is both ancient and recurrent, yet the evolutionary trajectories remain unresolved. Here, we synthesize evidence across land plants to propose a framework for the evolution of VDT in embryophytes. We build on the current understanding of VDT as an ancestral trait, present in the gametophyte of early land plants. The transition to sporophyte dominance and resulting homiohydry in vascular plants coincides with the widespread loss of VDT, likely driven by relaxed selection for VDT, coupled with new structural constraints and anatomical innovations that facilitated water acquisition, transport, and retention. The core molecular modules of DT were retained in the diaspores of most land plants, where they served as evolutionary refugia for the essential building blocks of the trait. Some species later reestablished VDT by co-opting deeply conserved diaspore modules and evolving key anatomical innovations to support them. We argue that such reestablishments of VDT are dependent on both anatomical predispositions as well as exposure to key selective pressures and ecological filters. We conclude that VDT is not a simple presence-absence trait, but rather a modular system, subject to anatomical constraints and contingent on the ecological context. Ultimately, we suggest that VDT serves as an elegant example of how complex traits emerge, persist, and shift across time.

Premise: Shoot and root apical meristems (SAMs and RAMs, respectively) drive primary vascular plant growth, yet their 2-D profile geometries remain poorly quantified. Shoot and root apical meristems differ in evolutionary origin, cellular organization, and developmental context, prompting investigation into whether their shapes differ within and across angiosperms, gymnosperms, and representative seedless vascular plants.

Methods: SAM and RAM profiles from 11 representative taxa were extracted from histological images. Six nonlinear equations (the catenary, parabolic, hybrid catenary-parabolic, performance, superparabolic, and superellipse equations) were fitted to normalized profile coordinates. Model performance was evaluated using the Akaike information criterion (AIC).

Results: The superparabolic equation provided the best fit for eight of 16 of the SAM and RAM profiles, as evidenced by the lowest AIC values, whereas the hybrid catenary-parabolic equation performed best for five profiles. These two equations outperformed the other four, though no single model was universally superior across all profiles. Although meristem shapes differed, SAM and RAM geometries showed no consistent differences across the three plant groupings.

Conclusions: Both the superparabolic and hybrid catenary-parabolic equations provide robust descriptions of SAM and RAM profiles, perhaps reflecting a convergence in apical meristem geometry across otherwise divergent vascular plant lineages. This quantitative approach offers a potential tool for comparing meristem geometry and shape that can be extended to the study of nonvascular plants to increase our understanding of plant form, evolution, and meristem functionality.

Premise: Insect herbivory is a major biotic factor shaping plant populations and driving the evolution of defensive traits. Polyploidy (whole-genome duplication) often induces substantial phenotypic and genotypic changes that may affect species interactions, including herbivory. However, natural variation in herbivory responses and the drivers of resistance and tolerance across heteroploid lineages remain poorly understood.

Methods: We conducted a bioassay to quantify variation in plant damage and tolerance to locust herbivory across multiple diploid and allotetraploid populations of the Brachypodium distachyon species complex, a model system comprising two diploid species (B. distachyon and B. stacei) and their allotetraploid derivative (B. hybridum). For each species, we also examined which plant functional traits were associated with resistance and tolerance to herbivory.

Results: Herbivory reduced maternal fitness across the species complex, although its magnitude depended on species and the fitness component considered. Our results do not support enhanced herbivory resistance or tolerance in the allotetraploid lineage: Levels of plant damage in B. hybridum were comparable to those of one diploid parent (B. distachyon), and diploid B. distachyon had higher tolerance than B. hybridum for two of three fitness estimators. Variation in resistance was associated with differences in plant traits, particularly C:N ratio and silica content. In B. distachyon, tolerance was negatively associated with silica and water content, suggesting allocation trade-offs between resistance- and tolerance-related traits.

Conclusions: Overall, our findings indicate that variation in herbivory responses across Brachypodium populations is more closely linked to population history and trait differentiation than to polyploid formation per se.

Premise: The parentage of the widespread allopolyploid Drosera anglica, a member of the carnivorous sundew genus, remains uncertain despite over 100 years of morphological, cytological, and, more recently, molecular study.

Methods: Using transcriptomic and genomic data from 12 species of Drosera sect. Drosera, including four D. anglica populations and a population sometimes identified as disjunct D. intermedia, we assembled genes in HybPiper and phased sequences in HybPhaser. We estimated species relationships with phylogenetic and pairwise genetic distance methods and ploidy with heterozygosity and flow cytometry measurements. Additionally, we expanded represented taxa by analyzing new and previously published rbcL sequences.

Results: Sequences from phased subgenomes of D. anglica were highly similar to D. rotundifolia (99.60-99.80%) and D. linearis (99.79-99.95%) and showed no evidence of multiple origins despite sampling across North America, Europe, and Hawaii. Additionally, the disjunct D. intermedia from Idaho had been misidentified and is D. anglica. Sequences from the nuclear ribosomal region and rbcL of D. anglica were nearly identical to D. linearis despite their chromosomes mispairing during meiosis and counter to interpretations of limited Sanger sequencing. Drosera anglica is intermediate between its parental lineages in leaf shape and microhabitat; however, across D. sect. Drosera, neither leaf shape nor biogeographic distribution was a reliable indicator of phylogenetic relationships.

Conclusions: Drosera anglica arose from allopolyploidy between the D. linearis lineage, representing the plastid and dominant ribosomal donor, and the D. rotundifolia lineage. Our study demonstrates the importance of taxon sampling and careful examination of complex phylogenomic data and presents an exemplar of analyzing allopolyploid relationships.

Premise: Seed longevity is critical for successful genebanking, but it is hard to detect or predict. We examined survival of genebanked seeds from species native to the United States to estimate longevity. We tested whether RNA integrity (RIN) can be used to detect aging and predict mortality.

Methods: Dry seeds from >100 species were stored for 28 ± 7 yr at -18°C. A recently harvested sample (cohort) from the same population provides a zero-time reference. Germination and RIN were assessed and differences between cohorts were used to distinguish short-lived seeds from long-lived seeds.

Results: No differences in germination or RIN were detected between cohorts in about one-fourth of the species. Viability and/or RIN was lower in the stored cohort than in the recently harvested cohort in most species, and the size of the difference was used to infer aging rates. Differences in germination and RIN were correlated among the 100 samples tested; moderate correlation coefficients indicate that additional factors are involved in seed aging and its detection.

Conclusions: Overall, longevity in the genebank appears to be similar for seeds from wild and domesticated species. We identified species that appeared to produce quite long-lived and short-lived seeds. Seeds from wild species tend to germinate slowly and asynchronously, and this confounds comparisons across storage times; deterioration is detected mostly after severe mortality. By contrast, RIN values decline before viability loss is detected and appear to be unaffected by wild seed traits. RIN tests during early storage can help predict seed longevity.

Premise: Populations can locally adapt to the biotic and abiotic factors of environments. However, detecting adaptation to biotic factors can depend on the abiotic conditions in which the adaptation is tested, and vice versa. The microbiome is one important aspect of the biotic environment: Interactions between microbiomes and their hosts are critical for host fitness and trait expression. If hosts adapt to local microbiomes, they may therefore depend on interactions with local microbes to express trait values adapted to the local abiotic environment.

Methods: Using Lemna minor (duckweed) as a model host, we examined differences in host fitness when grown in local and nonlocal microbiomes and in local and nonlocal water. We experimentally recombined duckweeds, microbes, and water from four ponds around Durham, New Hampshire (United States) in well-plate microcosms in a growth chamber.

Results: The source of duckweeds, microbes, and water all affected microbial growth, duckweed growth, and duckweed traits. However, weak, marginally significant local adaptation resulted in higher frond area only when duckweeds were paired with their local water and local microbes. Microbial growth was also marginally reduced when duckweeds were paired with microbes and water from their local site.

Conclusions: While microbiome impacts on duckweed growth and traits varied across abiotic contexts, local microbiomes provided only limited growth benefits. Harnessing the effects of plant microbiomes is an exciting area of applied research. Despite our findings, bioprospecting in local microbiomes could still be fruitful: It may be ecologically safer, and other plants may locally adapt to microbiomes.

Premise: The defining life history strategy of spring ephemeral wildflowers is their avoidance of shading by trees during the brief, high-light period before canopy leaf out. Studies suggest that spring ephemerals will experience increased light competition because canopy leaf out is more sensitive to warming than is the phenology of spring ephemerals. However, it remains unclear how longer durations of shade will alter the population dynamics of spring ephemerals and whether all populations are at risk.

Methods: We experimentally shaded Erythronium umbilicatum for one to six additional weeks before canopy leaf out to test for immediate and lagged effects of early shading on the timing of senescence and the probability of survival and flowering. To predict the potential for earlier shading, we combined long-term time series of spring air temperature, remotely sensed tree leaf out, and E. umbilicatum flowering phenology in North Carolina, United States.

Results: Early shading did not alter E. umbilicatum until the following year, when more-shaded plants senesced later. Year-to-year survival did not change, and the probability of flowering was reduced only when plants experienced extremely early shading. Moreover, E. umbilicatum phenology was more sensitive than tree leaf out to warming temperatures. We project that, under climate warming, E. umbilicatum is unlikely to experience shortened periods of high light.

Conclusions: Our findings show that a plant species' defining life history strategy does not necessarily predict their sensitivity to phenological mismatches. This incongruity complicates, but also underscores the importance of identifying the most vulnerable species and directing our research efforts accordingly.

Premise: Calcium oxalate biomineralization in plants is phylogenetically widespread and morphologically diverse, but the function of these inorganic crystals is an area of active debate. The variety of environmental conditions that produce the crystals, as well as the inconsistent evidence that they provide antiherbivore defense across plant and herbivore species, suggests that different crystal morphologies might have different functions.

Methods: Using Vitis riparia, or riverbank grape, we experimentally investigated the environmental influence of excess calcium and simulated herbivory on the formation of calcium oxalate druse and raphide crystals in leaves. We also investigated the putative defensive function of these crystals by using a no-choice herbivore bioassay manipulating herbivore diet composition to test for impacts of crystal shape on herbivore growth, both on its own and with plant chemistry.

Results: We found that the addition of calcium to soil increased the density of both raphide and druse crystals in V. riparia leaves. Contrary to expectations, the herbivory treatment decreased the density of raphides in leaves, and V. riparia-derived crystals did not impact weight gain, time to pupation, or survival of moth larvae.

Conclusions: Our multifaceted test of the formation and function of calcium oxalate crystals in riverbank grape demonstrates that an abiotic factor (i.e., soil calcium) is a relatively stronger determinant of crystal production and that, contrary to hundreds of years of speculation on their function, these crystals do not seem to mediate plant-insect herbivory in all plant taxa. Instead, the alternative hypothesis of calcium regulation was supported by our experimental evidence.