Mum is always right: Environmental effects on plant biology across generations

This guest post is reposted from Gabriela Auge’s original post, with permission. Read Gabriela’s Tansley insight: Adjusting phenotypes via within- and across-generational plasticity.

Living organisms change their behaviour in response to their environment. But they can also change their behaviour because of the environment that their mothers experienced. Plants perceive seasonal changes and modify their growth and development accordingly, to increase their chances of survival. Many plants shed their leaves during the fall and flower during the spring, giving us amazing and colourful views during both seasons. They become dormant during the winter when it is too cold to grow, and slowly resume growth at the beginning of the spring when the warmer temperatures and longer days allow them to start producing more leaves. Plants know “where” they are and “when” they are.

Plants have developed fine perception mechanisms that allow them to take in information about their environments: how rich in nutrients the soil is, how long the days are and what time of the day it is, how many neighbours they have around, whether it is a hot summer day or a cool winter day. These perception mechanisms drive a concerted developmental program that allows plants to grow when conditions are good for survival, by matching processes like flowering, leaf shedding, and seed dispersal to the seasons.

Of all the transitions that need to be matched to a season, the process of going from a quiescent seed to a young plant (called germination) is most critical, because the timing will determine the environment that the growing plant will face in the future. It’s not safe for a seed to germinate in the fall if this means the seedling will have to survive the freezing winter. Or if germination happens too late during the spring, the seedling would have to survive the upcoming hot dry summer. So a latent seed waits until the conditions are best for germination and subsequent plant growth.

Image: Figure 1 from Auge, G., et al.
Figure 1 from Auge, G., et al.

Seeds get information from different sources in order to decide whether to germinate or not. They inherit genetic information that will influence the process. They get to know the seasonal context by taking in information about their own environment. And, lastly, seeds receive information from the mother plant about the environment that was experienced in the previous generation. These are known as “maternal environment effects.”

Maternal effects have been shown to affect the behaviour of new generations in a wide variety of living organisms, including humans. These widespread effects influence the next generation in many ways, including the ability to reproduce, susceptibility to diseases, and the development of body parts. One of the mechanisms that might enable these effects is known as epigenetic marking. We now know that experience alters the DNA of living organisms—not in the DNA sequence itself, but through chemical modifications to the DNA that can have enormous impacts on how the genes are expressed.

We would expect seeds to respond most strongly to their own environment—it should be a more accurate indicator of the current and future conditions for the offspring than the mother plant’s experience of the environment. We would also expect the impact of the maternal environment, if any, to get weaker with time: as more time passes between the mother plant experiencing a cue and the present conditions the offspring is perceiving, the maternal effects should have declining power to predict the future environment.

Contrary to expectation, maternal effects in plants are sometimes even stronger than the effect of the progeny’s own environment. Seeds from mother plants that experienced different environments can display different response patterns when facing the same germination conditions. The effects of events in the maternal environment can affect germination of the next generation, even when these events occurred before the seeds developed. That is, a change in the conditions when the mother plant was as young as a seedling (right after her own germination) can influence the germination response of the next generation.

Maternal effects can also be persistent across time, modifying the responses of seeds after they have remained dormant or quiescent for long periods. These strong, long-lasting effects imposed at any time of the mother plant’s life cycle have been observed with respect to predictable cues that are associated to seasons (such as temperature, day length and water availability changes) but also with others that have little association with the seasons (like herbivory, soil disturbance, and plant disease). Maternal effects can influence much more than simply the timing of germination. They can also affect key developmental traits in the next generation, such as the transition from juvenile to adult plant, flowering timing, biomass accumulation, and the production and allocation of phytochemicals.

Why would plants respond to changes that occurred in previous generations if there weren’t a reliable way to predict the future environment? It may be that the maternal environment (experienced across the whole lifespan of the mother plant) actually provides a better guess at the future environment than the progeny’s own limited experience does. Combining present cues with information from the last generation may be the optimal strategy. There’s also a chance that the strength of maternal environment effects are not optimal—there is evidence of this in some species, due to an inherent conflict between the reproductive strategies of the mother and the progeny.

Maternal effects are a general pattern across plant species, and are seen in both short-lived ones (annuals and biennials) and long-lived ones (perennials). Perhaps of most importance to humans is the fact that offspring responses to the maternal environment can affect the final quality of plant-derived products. One way to mitigate this problem would be to establish growing protocols that are as strict as possible, stabilizing the environment across generations. This is obviously not as feasible in certain environments (such as outdoors), but knowing about the potential consequences of maternal effects might help in the development of better tools to predict crop outcomes more accurately. As variation in genetic information within a species can also affect how plants respond to the maternal environment, it should be possible to select for varieties that show a steady response to differing maternal cues. It may even be possible to optimize plant-derived products by learning how to manipulate the maternal environment in ways that predictably improve yield in the progeny.

Gabriela Auge

Further reading:

(This is not intended to be an exhaustive list of what’s out there about maternal effects, but rather a compendium of recent papers with examples regarding the topic of this post.)

Finch-Savage, W. E. and Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist, 171: 501–523. doi: 10.1111/j.1469-8137.2006.01787.x

Dominguez-Salas, P., et al. (2014) Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nature Communications, 3746. doi: 10.1038/ncomms4746

Quadrana, L. and Colot, V. (2016) Plant Transgenerational Epigenetics. Annual Review of Genetics, 50: 467–491. doi: 10.1146/annurev-genet-120215-035254

Leverett, D. et al. (2016) Contrasting germination responses to vegetative canopies experienced in pre- vs. post-dispersal environments. Annals of Botany, 118 (6): 1175–1186. doi: 10.1093/aob/mcw166

Chen, M., et al. (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. PNAS, 111 (52): 18787–18792. doi: 10.1073/pnas.1412274111

Burghardt, L. T. et al. (2016) Multiple paths to similar germination behavior in Arabidopsis thaliana. New Phytologist, 209: 1301–1312. doi: 10.1111/nph.13685

Edwards, B. R., et al. (2016) Maternal temperature effects on dormancy influence germination responses to water availability in Arabidopsis thaliana. Environmental and Experimental Botany, 126: 55–67. doi: 10.1016/j.envexpbot.2016.02.011

Vivas, M., et al. (2013) Environmental Maternal Effects Mediate the Resistance of Maritime Pine to Biotic Stress. PLoS ONE, 8 (7): e70148. doi: 10.1371/journal.pone.0070148

Akkerman, K. C., et al. (2016). Transgenerational plasticity is sex-dependent and persistent in yellow monkeyflower (Mimulus guttatus). Environmental Epigenetics, 2 (2): dvw003. doi: 10.1093/eep/dvw003

Latzel, V. and Klimešová, J. (2010). Year-to-year changes in expression of maternal effects in perennial plants. Basic and Applied Ecology, 11 (8): 702–708. doi: 10.1016/j.baae.2010.09.004

Lacey, E. P. (1996) Parental Effects in Plantago lanceolata L. I.: A Growth Chamber Experiment to Examine Pre- and Postzygotic Temperature Effects. Evolution, 50 (2): 865–878. doi: 10.2307/2410858

Walter J. et al. (2016). Transgenerational effects of extreme weather: perennial plant offspring show modified germination, growth and stoichiometry. Journal of Ecology, 104: 1032–1040. doi: 10.1111/1365-2745.12567

Latzel, V., et al. (2014). Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos, 123 (1): 41–46. doi: 10.1111/j.1600-0706.2013.00537.x

Karban, R., et al. (1999). Induced plant responses and information content about risk of herbivory. Trends in Ecology and Evolution, 14 (11): 443–447. doi: 10.1016/S0169-5347(99)01678-X

Ezard, T. H. G., et al. (2014) The fitness costs of adaptation via phenotypic plasticity and maternal effects. Functional Ecology, 28 (3): 693–701. doi: 10.1111/1365-2435.12207

English, S., et al. (2015). The Information Value of Non-Genetic Inheritance in Plants and Animals. PLoS ONE, 10 (1): e0116996. doi: 10.1371/journal.pone.0116996

Murren, C. J., et al. (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity, 115: 293–301. doi: 10.1038/hdy.2015.8