Transgenerational transmission of induced defenses

Transgenerational defense induction denotes a change in offspring phenotype guided by the environmental signal in the parental generation. This is a form of priming spanning across two generations. To assess the transmission of a priming signal, it is important to study parental environmental effects for different offspring traits (e.g., time of germination, resource allocation, plant architecture, and chemistry, etc.) (Verhoeven and van Gurp 2012; Liza M. Holeski et al. 2012). Plants in each generation can face combinations of different environmental challenges or stress and can often increase the resistance, growth, and reproduction success of their offspring under similar conditions (Karban et al. 1999; Herman and Sultan 2011).

A recent meta-analysis suggested that transgenerational transmission is also influenced by the developmental stage of parental and offspring during stress exposure, such that the transgenerational effect is stronger if the stress was experienced during the early development of the parental plants (Yin et al. 2019). Stress-relevant features like stress occurrence and its predictability in the parental environment can enhance the defense in offspring for the same stress and thus transmit as transgenerational defense (Yin et al. 2019). For example, Arabidopsis thaliana plants showed enhanced performance when exposed to single parental stress treatment (temperature shock or clipping), but not when two different treatments were combined, suggesting that environmental complexity is an important driver of efficient transgenerational defense (Lampei 2019).

Current studies reported that the transgenerational transmission of stress defense includes specific growth variations that are functionally adaptive to the parental conditions, but there are strong differences between the typical laboratory conditions to the complex environment of natural plant populations (Herman and Sultan 2011). However, first evidence exists that the required predictable environmental conditions for the selection of transgenerational effects indeed exist in nature. Lampei et al. (2017) showed in a recent study with a Mediterranean annual plant that winter precipitation predicted the following winter's seedling densities. In order to reduce competition in the offspring generation (avoidance strategy), plants from high water treatments reduced offspring germination (stronger seed dormancy) proportional to the long-term correlation between precipitation and the following winter's seedling density (Lampei et al. 2017). This example demonstrates the high complexity of the natural environments in which the plants live, but at the same time, it also demonstrates how seemingly random and very noisy variables, such as weather, can produce strong environmental correlations between generations that select for transgenerational plasticity.

But how does the transgenerational defense transmission work on the molecular scale? There are several possible mechanisms, including components of seed provisioning. But epigenetic mechanisms are often indicated as one of the most significant underlying mechanisms of transgenerational stress response (Boyko and Kovalchuk 2010; Luna et al. 2012). There are three major reasons supporting this suggestion.

1. The state of epigenetic modifications can be heritably transmitted, it is principally reversible, and the transition can take place rapidly (see Chapters 6, 7, and 8).

2. Epigenetic modifications are known to shape ecologically meaningful traits that also could be stably inherited. For example, histone modifications have been reported to be responsible for priming and transgenerational plant defense (Bej & Basak 2017; Jablonka and Raz 2009).

3. Epigenetic modifications can keep the memory potentially for a longer time than other types of transgenerational phenotype transmitters, such as components of seed provisioning.

Therefore, it is not unlikely that epigenetic modifications play a role also in the phenotype transition to the next generation. For a more detailed discussion of the molecular transmission of transgenerational plant defenses, refer to Chapter 1.