Maternal Plants Research Articles

Phenotypic differentiation among native, expansive and introduced populations influences invasion success

AbstractAimHumans influence species distributions by modifying the environment and by dispersing species beyond their natural ranges. Populations of species that have established in disjunct regions of the world may exhibit trait differentiation from native populations due to founder effects and adaptations to selection pressures in each distributional region. We compared multiple native, expansive and introduced populations of a single species across the world, considering the influence of environmental stressors and transgenerational effects.LocationUnited States Gulf and Atlantic coasts, United States interior, European Atlantic and Mediterranean coasts, east coast of Australia.TaxonBaccharis halimifolia L. (eastern baccharis).MethodsWe monitored seed germination, seedling emergence, survival and early growth in a common garden experiment, conducted with over 18,200 seeds from 80 populations. We also evaluated the influence of environmental stress and maternal traits on progeny performance.ResultsIntroduced European Atlantic populations had faster germination and early growth than native populations. However, this was not the case for the more recently naturalized European Mediterranean populations. Introduced Australian populations grew faster than native populations in non‐saline environments but had lower survival in saline conditions commonly encountered in the native range. Similarly, expansive inland US populations germinated faster than coastal native populations in non‐saline environments but grew and germinated more slowly in saline environments. Maternal inflorescence and plant size were positively related with seed germination and seedling survival, whereas flower abundance was positively correlated with seedling early growth and survival. However, maternal traits explained a much lower fraction of the total variation in early demographic stages of B. halimifolia than did distributional range.Main conclusionsPhenotypic differentiation could allow B. halimifolia to adapt to different biotic and abiotic selection pressures found in each distributional range, potentially contributing to its success in introduced and expansive ranges.

Warming during maternal generations delays offspring germination in native and nonnative species

As environmental conditions shift due to global warming and other human‐caused environmental changes, plastic responses in phenological traits like germination or flowering time may become increasingly important. While phenological plasticity is a common response to global warming, with many populations exhibiting earlier germination or flowering in warmer years, warming may also result in transgenerational plasticity, especially on early life stages. In other words, seeds produced by mothers inhabiting warmer environments may germinate faster (or slower) than seeds produced by mothers inhabiting ambient or cooler environments. Here, we use seeds collected from a field warming experiment to examine how germination and early growth differ in response to ambient versus warmed (+3°C) temperatures experienced by both maternal and offspring generations. Because nonnative species are often more phenotypically plastic than native species and because a variety of life‐history traits and environmental factors affect the evolution of both within‐ and transgenerational plasticity, we include multiple invasive and native plant species in our study. On average, warming experienced during maternal generations delayed germination by ~0.2 days °C−1, although species varied in the magnitude of response. In contrast, warming during the offspring generation tended to advance germination by ~0.1 days °C−1. Nonnative species demonstrated higher germination success than native species, but we detected no differences in germination timing between native and nonnative species or that native and nonnative species differed in either within‐ or transgenerational plasticity, although species (independent of native status) did exhibit differing degrees of within‐ and transgenerational plasticity in germination timing and early growth. This study suggests that temperatures experienced by maternal plants can influence their offspring's germination phenology, potentially even more so than temperatures experienced in the offspring's immediate environment.

The Effect of Environment and Maternal Plant on Germination Traits of Sugar Beet Seeds and an Approach to Select the Superior Genotype

The Effect of Environment and Maternal Plant on Germination Traits of Sugar Beet Seeds and an Approach to Select the Superior Genotype

The implication of leaf anatomical structure for the selective breeding of lilacs.

The cultivars of the common lilac (Syringa vulgaris) grown in the south of the Russian Far East are not always winter-hardy and are often damaged by fungal diseases due to a very humid climate. A promising trend in the selective breeding of lilacs in Russia is the creation of new breeding material based on the gene pool of the broadleaf lilac (S. oblata) and its hybrids in order to introduce valuable adaptive traits into cultivars. The present work aimed to identify the traits of leaf anatomy in species and cultivars of Syringa resistant and susceptible to Pseudocercospora lilacis, the causative agent of brown leaf spot disease. The study was carried out on the living collection of the Botanical Garden-Institute, Far Eastern Branch, Russian Academy of Sciences (Vladivostok). The leaf anatomical structure of two Syringa species showing different degrees of resistance to P. lilacis in the monsoon climate of the Far East (resistant S. oblata and weakly resistant S. vulgaris, and also their hybrid cultivars) has been analyzed. The differences between species, subspecies, and cultivars are quantitative: they differ in the number of spongy mesophyll layers, the cell height in the f irst layer of palisade mesophyll, the cell height in the upper and lower epidermises, and the thickness of both mesophylls. The interspecif ic hybrids resistant or weakly resistant to P. lilacis (brown leaf spot disease) mainly retain the leaf anatomy structure of the maternal plant. One of the traits determining the resistance of hybrid lilac cultivars is an increased number of spongy mesophyll layers in the leaf blade. The study of leaf anatomy has shown that the four-layered spongy mesophyll leaf parenchyma correlates with the resistance of lilacs from the subsection Euvulgaris to P. lilacis. In S. oblata, this trait is inherited down the maternal line. To establish lilac cultivars resistant to fungal diseases, it is advisable to cross the two species (S. oblata and S. vulgaris) or their cultivars using one of S. oblata subspecies as a maternal plant.

Effect of Water Deficit Stress and Foliar Application of Maternal Plant on Germination Characteristics of Three Barley (Hordeum vulgare) Cultivars

Effect of Water Deficit Stress and Foliar Application of Maternal Plant on Germination Characteristics of Three Barley (Hordeum vulgare) Cultivars

The 'black box' of plant demography: how do seed type, climate and seed fungal communities affect grass seed germination?

Demographic studies measure drivers of plant fecundity including seed production and survival, but few address both abiotic and biotic drivers of germination such as variation in climate among sites, population density, maternal plants, seed type and fungal pathogen abundance. We examined germination and microbial communities of seeds of Danthonia californica, which are either chasmogamous (external, wind-pollinated) or cleistogamous (internal, self-fertilized) and Festuca roemeri, which are solely chasmogamous. Seed populations were sourced across environmental gradients. We tested germination and used high-throughput sequencing to characterize seed fungal community structure. For F.roemeri, maternal plants significantly influenced germination as did climate and pathogens; germination increased from wetter, cooler sites. For D.californica, the main drivers of germination were maternal plant, seed type and pathogens; on average, more chasmogamous seeds germinated. Fungal communities depended largely on seed type, with fewer fungi associated with cleistogamous seeds, but the communities also depended on site factors such as vapor pressure deficit, plant density and whether the seeds had germinated. Putative pathogens that were negatively correlated with germination were more abundant for both D.californica and F.roemeri chasmogamous seeds than D.californica cleistogamous seeds. In D.californica, cleistogamous and chasmogamous seeds contain vastly different fungal communities.

Quantitative dissection of color patterning in the foliar ornamental coleus.

Coleus (Coleus scutellarioides) is a popular ornamental plant that exhibits a diverse array of foliar color patterns. New cultivars are currently hand selected by both amateur and experienced plant breeders. In this study, we reimagine breeding for color patterning using a quantitative color analysis framework. Despite impressive advances in high-throughput data collection and processing, complex color patterns remain challenging to extract from image datasets. Using a phenotyping approach called “ColourQuant,” we extract and analyze pigmentation patterns from one of the largest coleus breeding populations in the world. Working with this massive dataset, we can analyze quantitative relationships between maternal plants and their progeny, identify features that underlie breeder-selections, and collect and compare public input on trait preferences. This study is one of the most comprehensive explorations into complex color patterning in plant biology and provides insights and tools for exploring the color pallet of the plant kingdom.

Multigenerational consequences of aphid size on offspring phenotype and reproduction

AbstractIn many organisms, phenotype and fitness are strongly influenced by both current environmental factors and maternal effects. The low genetic variation, high phenotypic plasticity, and telescoping generations seen in aphids permit us to investigate the relative importance and potential interaction of maternal and current environments on phenotype. Although past studies have identified an influence of maternal host plant on offspring phenotype and reproduction in aphids, few have demonstrated the potential for these maternal effects to also interact with the aphid's current environment. By rearing multiple generations ofAphis nerii(Fonscolombe) (Hemiptera: Aphididae) on their host common milkweed,Asclepias syriaca(L.) (Apocynaceae), we tested the relative influence and interaction of both maternal and current environmental effects of crowding and plant quality on aphid body size and reproduction. Our results indicate that aphid body size increased with current plant quality and decreased with aphid density in both generations, with an additional direct, positive relationship between body size and fecundity. We did not find evidence for adaptive maternal effects, e.g., production of fewer, larger, offspring by stressed mothers. Instead, poor maternal environments constrained aphid body size and reproduction. Importantly, these adverse maternal effects were only seen in offspring where subsequent nymph population growth was allowed to increase unchecked, likely reducing available resources. Our study thus demonstrates that the significance of maternal effects in aphid development and reproduction can depend on current resource availability, shaping the phenotype and fecundity of offspring under stressful conditions. Incorporating this framework for how aphid body size and reproduction respond to current and maternal environments may improve predictions for how aphid population growth is impacted by resource limitation across generations.

Inheritance of DNA methylation differences in the mangrove Rhizophora mangle.

The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and nongenetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the nongenetic contributions to variation. Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions and is potentially threatened by anthropogenic environmental changes. Several studies have documented landscape-level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of nongenetic variation. To assess one type of nongenetic variation, we examined the patterns of DNA sequence and DNA methylation in maternal plants and offspring from natural populations of R. mangle from the Gulf Coast of Florida. We used a reduced representation bisulfite sequencing approach (epi-genotyping by sequencing; epiGBS) to address the following questions: (a) What are the levels of genetic and epigenetic diversity in natural populations of R. mangle? (b) How are genetic and epigenetic variation structured within and among populations? (c) How faithfully is epigenetic variation inherited? We found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field. In addition, a large portion (up to ~25%) of epigenetic differences among offspring grown in common garden was explained by maternal family. Therefore, epigenetic variation could be an important source of response to challenging environments in the genetically depauperate populations of this foundation species.

Benefits to the germination of seeds provided by birds that mandibulate fleshy fruits

The effect of fruit removal and passage through the digestive tract of frugivorous birds on seed germination has been mostly studied in species that swallow the whole fruit without mandibulating (“gulpers”), and defecate or regurgitate seeds without pulp away from the maternal plant. Functional groups with other fruit-handling methods, while often quantitatively important in removing fruits, are presumed to provide lower quality seed dispersal due to their tendency to damage seeds with the beak or discard seeds with pulp still attached under the maternal plant. We conducted a series of experiments with five bird species that mandibulate fruits with the beak before swallowing (“mashers”). They were fed with fruits of one to five plant species to test the effect of handling on their germination. We compared germination probabilities and times of seeds defecated or dropped from the bill with seeds with pulp removed by hand. Overall, bird processed seeds germinated in equal proportions than manually extracted seeds (69.9 vs 70.2%, respectively). However, depending on the bird-fruit species pair considered, the proportion and germination time of seeds processed by masher birds were equal to or less than those of manually extracted seeds. Most of the retrieved seeds processed by these birds were defecated (94%), and a large percentage of them germinated (70.3%), which confirms that they are important for the seed dispersal process. Our results provide new insights on aspects of the qualitative component of seed dispersal by masher birds. We discuss the possible implications of these findings on seed dispersal in the rest of the Neotropical region.

Maternal Dietary Protein Patterns During Pregnancy and the Risk of Infant Eczema: A Cohort Study.

Background: Previous studies have suggested that maternal dietary protein was associated with allergic diseases in offspring, but few studies have evaluated the influence of dietary protein patterns. This study aimed to explore the prospective association between maternal dietary protein patterns during pregnancy and the risk of infant eczema.Methods: A total of 713 mother-child pairs from a prospective cohort in Guangzhou, China were recruited. Maternal dietary protein was estimated using a validated face-to-face food frequency questionnaire at 20–28 weeks' gestation from 2017 to 2018. Dietary protein patterns were calculated based on the sources of protein. The data of infant eczema was assessed at 6 months of age using the symptom questionnaire of eczema. Logistic regression was carried out to examine the associations between maternal dietary protein patterns and infant eczema.Results: The cumulative incidence of infant eczema at 6 months of age was 51.19%. Mothers of infants with eczema consumed more protein from poultry source during pregnancy than mothers of infants without eczema, while no statistical differences were observed in maternal intakes of protein from cereals and tubers, vegetables, fruits, red meat, fish and seafood, eggs, dairy, soybean, and nuts and seeds. Four dietary protein patterns were identified and termed poultry, plant, dairy and eggs, and red meat and fish. The cumulative incidence of eczema was 61.2, 45.8, 48.0, 51.4% for these four patterns, respectively. Compared to the poultry dietary pattern, the plant pattern and the dairy and eggs pattern were associated with a reduced risk of infant eczema, and the adjusted odds ratios (95% confidence interval) were 0.572 (0.330–0.992), 0.478 (0.274–0.837), respectively. No such association was observed for the red meat and fish dietary protein pattern.Conclusion: This is the first study that focused on the association between maternal dietary protein during pregnancy from a whole-diet perspective and infant eczema. Compared with the poultry dietary protein pattern, the maternal plant pattern and the dairy and eggs pattern during pregnancy were associated with a reduced risk of infant eczema.

Maternal effects strengthen interactions of temperature and precipitation, determining seed germination of dominant alpine grass species.

Despite the existence of many studies on the responses of plant species to climate change, there is a knowledge gap on how specific climatic factors and their interactions regulate seed germination in alpine species. This understanding is complicated by the interplay between responses of seeds to the environment experienced during germination, the environment experienced by the maternal plant during seed development and genetic adaptations of the maternal plant to its environment of origin. The study species (Anthoxanthum alpinum, A. odoratum) originated from localities with factorial combinations of temperature and precipitation. Seed germination was tested in conditions simulating the extreme ends of the current field conditions and a climate change scenario. We compared the performance of field-collected seeds with that of garden-collected seeds. A change to warmer and wetter conditions resulted in the highest germination of A. alpinum, while A. odoratum germinated the most in colder temperature and with home moisture. The maternal environment did have an impact on plant performance of the study species. Field-collected seeds of A. alpinum tolerated warmer conditions better than those from the experimental garden. The results demonstrate how knowledge of responses to climate change can increase our ability to understand and predict the fate of alpine species. Studies that aim to understand the germination requirements of seeds under future climates should use experimental designs allowing the separation of genetic differentiation, plasticity and maternal effects and their interactions, since all these mechanisms play an important role in driving species' germination patterns.

The evolution of imprinting in plants: beyond the seed

Genomic imprinting results in the biased expression of alleles depending on if the allele was inherited from the mother or the father. Despite the prevalence of sexual reproduction across eukaryotes, imprinting is only found in placental mammals, flowering plants, and some insects, suggesting independent evolutionary origins. Numerous hypotheses have been proposed to explain the selective pressures that favour the innovation of imprinted gene expression and each differs in their experimental support and predictions. Due to the lack of investigation of imprinting in land plants, other than angiosperms with triploid endosperm, we do not know whether imprinting occurs in species lacking endosperm and with embryos developing on maternal plants. Here, we discuss the potential for uncovering additional examples of imprinting in land plants and how these observations may provide additional support for one or more existing imprinting hypotheses.

Unexpectedly low paternal diversity is associated with infrequent pollinator visitation for a bird-pollinated plant.

The behaviour of pollinators has important consequences for plant mating. Nectar-feeding birds often display behaviour that results in more pollen carryover than insect pollinators, which is predicted to result in frequent outcrossing and high paternal diversity for bird-pollinated plants. We tested this prediction by quantifying mating system parameters and bird visitation in three populations of an understory bird-pollinated herb, Anigozanthos humilis (Haemodoraceae). Microsatellite markers were used to genotype 131 adult plants, and 211 seeds from 23 maternal plants, from three populations. While outcrossing rates were high, estimates of paternal diversity were surprisingly low compared with other bird-pollinated plants. Despite nectar-feeding birds being common at the study sites, visits to A. humilis flowers were infrequent (62 visits over 21,552 recording hours from motion-triggered cameras, or equivalent to one visit per flower every 10days), and the majority (76%) were by a single species, the western spinebill Acanthorhynchus superciliosus (Meliphagidae). Pollen counts from 30 captured honeyeaters revealed that A. humilis comprised just 0.3% of the total pollen load. For 10 western spinebills, A. humilis pollen comprised only 4.1% of the pollen load, which equated to an average of 3.9 A. humilis pollen grains per bird. Taken together, our findings suggest that low visitation rates and low pollen loads of floral visitors have led to the low paternal diversity observed in this understory bird-pollinated herb. As such, we shed new light on the conditions that can lead to departures from high paternal diversity for plants competing for the pollination services of generalist nectar-feeding birds.

Functional packaging of seeds.

SummaryThe encapsulation of seeds in hard coats and fruit walls (pericarp layers) fulfils protective and dispersal functions in many plant families. In angiosperms, packaging structures possess a remarkable range of different morphologies and functionalities, as illustrated by thermo and hygro‐responsive seed pods and appendages, as well as mechanically strong and water‐impermeable shells. Key to these different functionalities are characteristic structural arrangements and chemical modifications of the underlying sclerenchymatous tissues. Although many ecological aspects of hard seed encapsulation have been well documented, a detailed understanding of the relationship between tissue structure and function only recently started to emerge, especially in the context of environmentally driven fruit opening and seed dispersal (responsive encapsulations) and the outstanding durability of some seed coats and indehiscent fruits (static encapsulations). In this review, we focus on the tissue properties of these two systems, with particular consideration of water interactions, mechanical resistance, and force generation. Common principles, as well as unique adaptations, are discussed in different plant species. Understanding how plants integrate a broad range of functions and properties for seed protection during storage and dispersal plays a central role for seed conservation, population dynamics, and plant‐based material developments.

Grain filling in barley relies on developmentally controlled programmed cell death

Cereal grains contribute substantially to the human diet. The maternal plant provides the carbohydrate and nitrogen sources deposited in the endosperm, but the basis for their spatial allocation during the grain filling process is obscure. Here, vacuolar processing enzymes have been shown to both mediate programmed cell death (PCD) in the maternal tissues of a barley grain and influence the delivery of assimilate to the endosperm. The proposed centrality of PCD has implications for cereal crop improvement.

Getting ready for the ozone battle: Vertically transmitted fungal endophytes have transgenerational positive effects in plants

Ground-level ozone is a global air pollutant with high toxicity and represents a threat to plants and microorganisms. Although beneficial microorganisms can improve host performance, their role in connecting environmentally induced maternal plant phenotypes to progeny (transgenerational effects [TGE]) is unknown. We evaluated fungal endophyte-mediated consequences of maternal plant exposure to ozone on performance of the progeny under contrasting scenarios of the same factor (high and low) at two stages: seedling and young plant. With no variation in biomass, maternal ozone-induced oxidative damage in the progeny that was lower in endophyte-symbiotic plants. This correlated with an endophyte-mediated higher concentration of proline, a defence compound associated with stress control. Interestingly, ozone-induced TGE was not associated with reductions in plant survival. On the contrary, there was an overall positive effect on seedling survival in the presence of endophytes. The positive effect of maternal ozone increasing young plant survival was irrespective of symbiosis and only expressed under high ozone condition. Our study shows that hereditary microorganisms can modulate the capacity of plants to transgenerationally adjust progeny phenotype to atmospheric change.

The effect of genotype on in vitro morphogenesis of blue- and purple-grained bread wheat

Bread wheat containing anthocyanins in grain is of great interest for in vitro cell selection. These compounds are antioxidants and help the plant cope with stress. For the first time, we have evaluated the regenerative potential of eight samples with purple and blue grain using mature and immature embryos as explants. The maternal plants grew in the field conditions in the south of Western Siberia (Russia). Colored wheat had an advantage over white-grained forms in the ability to in vitro morphogenesis and adaptation to ex vivo conditions. Samples Fioletovozernaya (k-55583) and Blue A (k-43091) showed an intense proliferation of callus (94-95%), a high morphogenic activity (74-100%) and a large yield of viable regenerants (4-6 from one callus). We consider these forms promising for the selection of cell and plant lines that are resistant to adverse environmental factors and are suitable for breeding programs.

No Effect of Selective Maturation on Fruit Traits for a Bird-Dispersed Species, Sambucus racemosa.

Selective abortion, also called selective maturation, is a phenomenon wherein maternal plants selectively mature ovules that have the potential to grow into higher-quality fruits, such as those that contain more seeds. We hypothesized that the effects of selective maturation on fruit traits could be influenced by the dispersal mechanism. However, to date, limited studies have been conducted on selective maturation in bird-dispersed fruits. Unlike self- or wind-dispersed species, bird-dispersed species would not selectively mature fruits that contain more seeds because they are not preferred by birds. Here, we investigated the effect of selective abortion on the fruit traits of a bird-dispersed species, elderberry (Sambucus racemosa L. subsp. kamtschatica). We performed a flower-removal experiment. Half of the inflorescences on each individual tree were removed for the treatment group, whereas the control group was not manipulated. We found that the flower-removed trees showed higher fruit sets, suggesting the existence of resource limitation. The number of seeds per fruit did not increase by the experimental treatment. Additionally, the control individuals did not produce larger fruits. The lack of effects on fruit traits supported our hypothesis that the effect of selective maturation on fruit traits may differ among species with different dispersal mechanisms.

The endosperm cavity of wheat grains contains a highly hydrated gel of arabinoxylan

Cereal grains provide a substantial part of the calories for humans and animals. The main quality determinants of grains are polysaccharides (mainly starch but also dietary fibers such as arabinoxylans, mixed-linkage glucans) and proteins synthesized and accumulated during grain development in a specialized storage tissue: the endosperm.In this study, the composition of a structure localized at the interface of the vascular tissues of the maternal plant and the seed endosperm was investigated. This structure is contained in the endosperm cavity where water and nutrients are transferred to support grain filling. While studying the wheat grain development, the cavity content was found to autofluoresce under UV light excitation. Combining multispectral analysis, Fourier-Transform infrared spectroscopy, immunolabeling and laser-dissection coupled with wet chemistry, we identified in the cavity arabinoxylans and hydroxycinnamic acids. The cavity content forms a “gel” in the developing grain, which persists in dry mature grain and during subsequent imbibition. Microscopic magnetic resonance imaging revealed that the gel is highly hydrated.Our results suggest that arabinoxylans are synthesized by the nucellar epidermis, released in the cavity where they form a highly hydrated gel which might contribute to regulate grain hydration.