Adaptive transgenerational plasticity in the perennial Plantago lanceolata

Phenotypes of plants, and thus their ecology and evolution, can be affected by the environmental conditions experienced by their parents, a phenomenon called parental effects or transgenerational plasticity. However, whether such effects are just passive responses or represent a special type of adaptive plasticity remains controversial because of a lack of solid tests of their adaptive significance. Here, we investigated transgenerational effects of different nutrient environments on the productivity, carbon storage and flowering phenology of the perennial plant Plantago lanceolata, and whether these effects are influenced by seasonal variation in the maternal environment. We found that maternal environments significantly affected the offspring phenotype, and that plants consistently produced more biomass and had greater root carbohydrate storage if grown under the same environmental conditions as experienced by their mothers. The observed transgenerational effects were independent of the season in which seeds had matured. We therefore conclude that transgenerational effects on biomass and carbon storage in P. lanceolata are adaptive regardless of the season of seed maturation.     

The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

Maternal warming affects early life stages of an invasive thistle

Maternal environment can influence plant offspring performance. Understanding maternal environmental effects will help to bridge a key gap in the knowledge of plant life cycles, and provide important insights for species’ responses under climate change. Here we show that maternal warming significantly affected the early life stages of an invasive thistle, Carduus nutans. Seeds produced by plants grown in warmed conditions had higher germination percentages and shorter mean germination times than those produced by plants under ambient conditions; this difference was most evident at suboptimal germination temperatures. Subsequent seedling emergence was also faster with maternal warming, with no cost to seedling emergence percentage and seedling growth. Our results suggest that maternal warming may accelerate the life cycle of this species via enhanced early life‐history stages. These maternal effects on offspring performance, together with the positive responses of the maternal generation, may exacerbate invasions of this species under climate change.     

Geographical variation in offspring size effects across generations

Offspring size is thought to strongly affect offspring fitness and many studies have shown strong offspring size/fitness relationships in marine and terrestrial organisms. This relationship is strongly mitigated by local environmental conditions and the optimal offspring size that mothers should produce will vary among different environments. It is assumed that offspring size will consistently affect the same traits among populations but this assumption has not been tested. Here I use a common garden experiment to examine the effects of offspring size on subsequent performance for the marine bryozoan Bugula neritina using larvae from two very different populations. The local conditions at one population (Williamstown) favour early reproduction whereas the other population (Pt. Wilson) favours early growth. Despite being placed in the same habitat, the effects of parental larval size were extremely variable and crossed generations. For larvae from Williamstown, parental larval size positively affected initial colony growth and larval size in the next generation. For larvae from the other population, parental larval size positively affected colony fecundity and negatively affected larval size in the next generation. Traditionally, exogenous factors have been viewed as the sole source of variation in offspring size/fitness relationship but these results show that endogenous factors (maternal source population) can also cause variation in this crucial relationship. It appears offspring size effects can be highly variable among populations and organisms can adapt to local conditions without changing the size of their offspring.     

Generation carryover of a fraction of population members as an animal adaptation to unstable environmental conditions

A heterogeneous life cycle of individuals in a population was examined on its adaptive significance to an unstable environmental condition. The trend of population growth was simulated by a simple mathematical model in which a part of population in a certain generation was carried over to the next generation without participating in the reproduction. With the increase of the rate of carryover of individuals to the next generation the population fluctuation tended to be stabilized. A minute fraction of population is carried over, the effect is very large to prevent the population decline at a sequence of adverse environmental conditions. The population level increased greatly depending upon the extent of environmental change as far as the rate of carryover took an intermediate value. The optimum proportion of members to be carried over to the next generation was determined by the extent of environmental change and its frequency of occurrence.     

Testing population differentiation in plant species – how important are environmental maternal effects

The maternal environment may contribute to population differentiation in offspring traits if growing conditions of mother plants are different. However, the magnitude of such environmental maternal effects compared with genetic differentiation is often not clear. We tested the importance of environmental maternal effects by comparing population differentiation in parental seed directly collected in the field and in F₁ seed grown under homogeneous conditions. The F₁ seeds were obtained by random crosses within populations. We used five populations in each of four plant species to analyse seed mass and growth chamber germination of both generations at the same time. In two species, we additionally tested offspring performance in the field. We found a significant population differentiation in all species and for nearly all measured traits. Population‐by‐generation interactions indicating environmental maternal effects were significant for germination (three species) and for seed mass (two species) but not for growth and reproduction. The significant interaction was partly due to a reduction of among‐population differentiation from the parental to the F₁ generation that can be explained by a decrease of maternal provisioning effects. However, in some species by trait combinations a change in population ranking and not a decrease of variation was responsible for significant population‐by‐generation interactions indicating environmental maternal effects beyond maternal provisioning. Fitting of seed mass as covariate was not successful in reducing environmental maternal effects on population differentiation in germination. We discuss alternative methods to account for environmental maternal effects in studies on genetic differentiation among populations.     

Flowering in Pisum: Effect of the Parental Environment

The parental photoperiod appears to have no effect on the floweringnode of the progeny, provided the progeny seed is selected tobe of the same weight. However, the parental photoperiod doesinfluence the mean seed weight and seed weight is shown to causesignificant alterations in the flowering node and time as wellas causing alterations in vegetative characters like the internodelength and the rate of leaf expansion and node formation. Theeffect of seed weight on flowering is thought to result fromthe alterations in the growth rate. On the other hand, vernalization of the parents does appearto cause a small, but significant effect on the flowering nodeof the progeny (i.e. it could be transmitted through a meioticdivision). This effect disappears in the next generation andthe possible nature of this effect is discussed. Pisum sativum L, garden pea, flowering, photoperiod, vernalization     

INBREEDING DEPRESSION IN HYDROPHYLLUM APPENDICULATUM: ROLE OF MATERNAL EFFECTS,CROWDING, AND PARENTAL MATING HISTORY

This paper examines several aspects of the expression of inbreeding depression in an outcrossing, obligately biennial plant, Hydrophyllum appendiculatum (Hydrophyllaceae). The amount of inbreeding depression detected was small during the first year of life but increased with age and had significant effects on adult size and reproductive traits. The lack of significant inbreeding depression during early growth is likely due to the overriding influence of maternal environmental effects on seed size and seedling growth. However, as maternal effects decreased with age, the seedling's own genotype became a more important determinant of its fate. To examine whether the expression of inbreeding depression was sensitive to ecological conditions, selfed and outcrossed seedlings were grown alone or with other H. appendiculatum seedlings. No inbreeding depression was detected in the plants grown alone. In contrast, under competitive conditions, outcrossed seedlings were significantly larger than selfed seedlings by the end of the first growing season. To address whether parental mating history influences the amount of inbreeding depression expressed, I examined the consequences of two successive generations of selfing on seed set and seed weight. The amount of inbreeding depression increased following the second generation of selfing. In the first generation, seed set and seed weight differed by less than 5% between selfed and outcrossed progeny. However, both traits were 15% greater for outcrossed plants after two generations. These results indicate that the alleles responsible for the reductions in these traits were not purged and suggest the action of multiple loci with deleterious effects.     

Generation carryover of a fraction of population members as an animal adaptation to unstable environmental conditions

Summary A heterogeneous life cycle of individuals in a population was examined on its adaptive significance to an unstable environmental condition. The trend of population growth was simulated by a simple mathematical model in which a part of population in a certain generation was carried over to the next generation without participating in the reproduction. With the increase of the rate of carryover of individuals to the next generation the population fluctuation tended to be stabilized. A minute fraction of population is carried over, the effect is very large to prevent the population decline at a sequence of adverse environmental conditions. The population level increased greatly depending upon the extent of environmental change as far as the rate of carryover took an intermediate value. The optimum proportion of members to be carried over to the next generation was determined by the extent of environmental change and its frequency of occurrence. Contribution from the Entomological Laboratory, College of Agriculture, Kyoto University, No. 451.     

The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits

Offspring trait expression is determined by the combination of parental genes and parental environments. Although maternal environmental effects have been widely characterized, few studies have focused on paternal environmental effects. To determine whether light availability influences pollen and offspring traits in the woodland herb Campanula americana, we reared clones of 12 genotypes in two light levels. In the parental generation we measured pollen number and size. Plants grown under high light produced more pollen grains per flower than those grown under low light. However, the response was genotype specific; some individuals responded little to changes in light availability while others substantially reduced pollen production. As a consequence, paternity ratios may vary between light environments if more pollen is associated with greater siring success. We crossed a subset of these plants to produce the offspring generation. The paternal and maternal light environments influenced offspring seed mass, percentage germination, and days to germination, while only maternal light levels influenced later life traits, such as leaf number and size. Maternal and paternal environmental effects had opposite influences on seed mass, percentage germination and days to germination. Finally, there was no direct relationship between light effects on pollen production and offspring trait expression.     

Respiration hastens maturation and lowers yield in rice

Role of respiration in plant growth remains an enigma. Growth of meristematic cells, which are not photosynthetic, is entirely driven by endogenous respiration. Does respiration determine growth and size or does it merely burn off the carbon depleting the biomass? We show here that respiration of the germinating rice seed, which is contributed largely by the meristematic cells of the embryo, quantitatively correlates with the dynamics of much of plant growth, starting with the time for germination to the time for flowering and yield. Seed respiration appears to define the quantitative phenotype that contributes to yield via growth dynamics that could be discerned even in commercial varieties, which are biased towards higher yield, despite considerable susceptibility of the dynamics to environmental perturbations. Intrinsic variation, irreducible despite stringent growth conditions, required independent validation of relevant physiological variables both by critical sampling design and by constructing dendrograms for the interrelationships between variables that yield high consensus. More importantly, seed respiration, by mediating the generation clock time via variable time for maturation as seen in rice, directly offers the plausible basis for the phenotypic variation, a major ecological stratagem in a variable environment with uncertain water availability. Faster respiring rice plants appear to complete growth dynamics sooner, mature faster, resulting in a smaller plant with lower yield. Counter to the common allometric views, respiration appears to determine size in the rice plant, and offers a valid physiological means, within the limits of intrinsic variation, to help parental selection in breeding.Key words: Meristematic cells, allometry, flowering, branching     

The role of epigenetic processes in controlling flowering time in plants exposed to stress

Plants interact with their environment by modifying gene expression patterns. One mechanism for this interaction involves epigenetic modifications that affect a number of aspects of plant growth and development. Thus, the epigenome is highly dynamic in response to environmental cues and developmental changes. Flowering is controlled by a set of genes that are affected by environmental conditions through an alteration in their expression pattern. This ensures the production of flowers even when plants are growing under adverse conditions, and thereby enhances transgenerational seed production. In this review recent findings on the epigenetic changes associated with flowering in Arabidopsis thaliana grown under abiotic stress conditions such as cold, drought, and high salinity are discussed. These epigenetic modifications include DNA methylation, histone modifications, and the production of micro RNAs (miRNAs) that mediate epigenetic modifications. The roles played by the phytohormones abscisic acid (ABA) and auxin in chromatin remodelling are also discussed. It is shown that there is a crucial relationship between the epigenetic modifications associated with floral initiation and development and modifications associated with stress tolerance. This relationship is demonstrated by the common epigenetic pathways through which plants control both flowering and stress tolerance, and can be used to identify new epigenomic players.     

CONSEQUENCES OF EMERGENCE PHENOLOGY FOR REPRODUCTIVE SUCCESS IN RANUNCULUS ADONEUS (RANUNCULACEAE)

This study explores the effects of emergence time and reproductive phenology on seed number, seed size, and seedling survival in a population of the alpine buttercup, Ranunculus adoneus. Phenology in this snow bowl population is structured by snow depth. Plants in late melting interior portions of the bowl emerged and flowered 3 to 4 wk after those in early melting zones at the bowl perimeter during the summers of 1988 and 1989. Flowering time differences of buttercups across the bowl were consistent from one year to the next. In 1988, late flowering plants tended to set fewer seeds than early flowering ones; in 1989 no decrease in seed number accompanied flowering date. Path analysis showed that equal fecundity in early and late emerging portions of the bowl population during 1989 resulted from balancing spatial and temporal constraints on seed production. Spatial aspects of habitat quality improved toward the interior of the bowl, but temporal regimes deteriorated in these late melting sites. In both 1988 and 1989 seed size declined with delays in flowering. Path analysis of 1989 data showed that because of reduced time for seed growth, plants in late melting portions of the bowl set smaller seeds than those in earlier melting zones. Differences in seed size due to parental phenology are likely to influence fitness in snow buttercups. Under natural conditions, seedlings from large seeds (>;0.65 mg) have sixfold higher survival than do those from smaller seeds (<;0.65 mg). We conclude that seedling recruitment may be infrequent in late-melting portions of the snow bowl due to delayed parental phenology.     

Estimates of broad-sense heritability for seed yield and yield criteria in faba bean (Vicia faba L.)

Eight faba bean (Vicia faba L.) genotypes were grown at lowlands of the west-Mediterranean region of Turkey in order to estimate the broad-sense heritability for plant height, number of stems and pods per plant, seed yield, biological yield, 100-seed weight, days to flowering and maturity. The heritability for plant height, number of stems and pods per plant, seed yield, biological yield, 100-seed weight, days to flowering and maturity were estimated as 83%, 63%, 43%, 62%, 52%, 99%, 97% and 97%, respectively. It was found that seed weight was the least affected trait across changing environmental conditions and followed by days to flowering and maturity. On the other hand, number of pods per plant, biological and seed yields and number of stems per plant were the most affected traits versus environmental conditions.     

Control of the Germination Responses of Amaranthus retroflexus L. Seeds by their Parental Photothermal Environment

Germination responses of the seeds of Amaranthus retroflexusL. were affected by the photoperiod, temperature, and levelof solar radiation experienced by their parent plants. Seedsfrom parents grown continuously in short days (SD, 8 h) lostpost-harvest dormancy more rapidly and had a higher dark germination,as well as a greater responsiveness (at 30?C) to pretreatmentsat low temperature (5 or 10?C) and to short illuminations, thanseeds from parents grown continuously in long days (LD, 16 h).Dark germination and responsiveness of the seeds to promotivetreatments were both higher when their parents were transferredat flowering from LD to SD than when grown continuously in LD.These responses were lower when their parents were similarlytransferred from SD to LD than when grown continuously in SD.The promotive effects of parental post-flowering SD on darkgermination (at 30?C) were enhanced by reduction of parentaltemperature (from 27/22?C to 22/17?C), but the responsivenessof the seeds to low temperature pretreatment was reduced. Inflorescencesdeveloping in LD produced seed with higher germinability whenfloweringwas not induced (LD throughout) than when it was induced (eitherby SD till flowering, or by three SD cycles when 4–5 leavesappeared). Reduced levels of solar radiation had opposite effectsin the different parental photoperiods: dark germination andthe responsiveness to low temperature pretreatments were reducedin LD, but were increased in SD. Differences in the germination responses resulting from differencesin the parental environment could not be correlated with differencesin seed coat thickness or seed dry weight.     

Anthropogenic edges,isolation and the flowering time and fruit set of Anadenanthera peregrina,a cerrado savanna tree

Fragmentation exposes plants to extreme environmental conditions with implications for species phenology and reproduction. We investigated whether isolation and edge effects influence size, flowering time, fruit set, and seedling establishment of Anadenanthera peregrina var. falcata. We compared trees in the interior (n?=?85), and on the edge (n?=?74) of a cerrado savanna fragment as well as in a pasture (n?=?26) with respect to size, flowering phenology, flower and fruit production, fruit and seed set, predispersal seed predation, and seedling establishment. Trees in the pasture were larger and produced a higher number of flowers and fruits than trees on the edge and interior, yet seed set did not differ across environments. The plant size structure explained the flower and fruit production, and the self-compatibility breeding system caused a similar seed set regardless of the environment. First flowering was later and fruit set higher in the interior. We argue that time of first flower influenced the fruit set of Anadenathera. Edge and isolated trees started to flower earlier as a response to microclimatic conditions—mainly temperature—reducing the fruit set. Predispersal seed predation was lower among pasture trees. Conversely, we found seedlings only on the edge and in the interior of cerrado, suggesting that the pasture was of poor quality habitat for Anadenanthera recruitment. Isolation affected the plant size structure and reproduction of Anadenanthera trees. Studies comparing plant phenology under contrasting environmental conditions may offer clues on how global change may affect plant reproduction in the tropics.     

Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences

? Seed longevity, which is essential for germplasm conservation and survival of many land plant species, can vary considerably within species and cultivars. Here, we explore the relationship between parental and offspring phenotypes to elucidate how pre-zygotic environment affects seed longevity. ? Plants of the wild species Plantago cunninghamii were exposed to wet or dry soil within a warm or cool glasshouse until flowering and then moved to a common environment. Seeds subsequently produced were collected at maturity, and longevity was assessed by controlled ageing at 45°C, 60% relative humidity. Multivariate analysis was used to examine relationships between the parental and offspring phenotypes. ? The pre-zygotic environment resulted in a highly plastic parental response which was passed on to offspring seeds and changed their longevity (p(50)) by more than a factor of 2. Seed longevity is a function of the seed population's distribution of deaths in time (σ) and quality (K(i)); σ was associated with plant size, and K(i) with reproductive plant traits. ? The pre-zygotic growth environment modulated seed longevity via a parental effect. Reproductive performance and seed quality (K(i)) were highly correlated with each other and unrelated to the maternal plant phenotype. Hence seed quality may be associated with the paternal plant response to the environment.     

PLEIOTROPY IN THE WILD: THE DORMANCY GENE DOG1 EXERTS CASCADING CONTROL ON LIFE CYCLES

In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental‐timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed‐dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental‐timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.