How does plant memory work?

In my previous post, I talked about what plant memory is and how it is sparked via priming. This is fascinating because it implies that epigenetic marks may be passed on to the next generations without altering DNA sequences [1], which is quite different from the Mendelian inheritance model we learned in high school. I don’t know about you, but I still remember the thrilling feeling when I did my first Punnett square to see whether there would have been any chance I could have had curly hair based on my parents’ phenotypic traits. However, epigenetic marks aren’t as easy as Punnett squares and they involve complex mechanisms; thus, I think it is important to take the time to understand the general mechanisms that allow for this memory to happen, before diving into stress-specific responses.

DNA methylation

DNA methylation refers to the biochemical addition of a methyl group (-CH3) to the cytosine C5 via a methyltransferase (MET) enzyme. Unlike in animal organisms, the cytosine in plants can be methylated in 3 different ways – CG, CHG, and CHH (where H is A, C, or T) - and it can be either symmetrical or asymmetrical [2]. Since there are 3 methylation possibilities, various enzymes are involved in maintaining them. For instance, CG and CHH methylation is maintained by MET1 and CHROMOMETHYLASE 2 (CMT2), respectively. Both enzymes have orthologues in mammalian organisms [1], and DRM2 is responsible for de novo methylation in plant organisms [3]. The CHG is maintained by a plant-specific methyltransferase CHROMOMETHYLASE 3 (CMT3), adding to the uniqueness and complexity of plant organisms [1].

Methylation generally decreases gene expression, meaning that if a gene is methylated certain traits can be inhibited. In a whole-genome study, scientists observed that DNA methylation is densest at the repetitive elements around the centromere [4]. MET1 is also essential to enhance methylation around this region and can be essential in further understanding of how plant memory works.

Histone modifications

Histone tails are subject to many post-transcriptional modifications that can impact gene expression by altering chromatin structure [5]. They control important aspects of DNA processes such as transcription, replication, chromosome condensation, or DNA repair [1, 6]. Since DNA not completely unwound during replication, the modified histones may be carried into each new DNA copy [7]. Once there, these histones may act as templates initiating the surrounding histones to be shaped in the new manner.

Modifications of histones H3 and H4 are often studied as they seem to be hotspots for memory. A recent study looked at the genome-wide expression patterns of histone H3 lysine 27 trimethylation (H3K27m3) under salt stress in soybeans [8]. H3K27m3 is categorized as an epigenetic repressive mark and showed greater activity when exposed to salt stress. This suggests that stress caused changes in chromatin structure via methylation of H3 when exposed to environmental stressors. The salt-stressed soybeans also showed poor development compared to the control group, signifying that this process is energy expensive (Figure 1).

Figure 1. A comparison between the control group (no stress) and salt-stress group. The latter shows disturbed developmental phenotypes that correlate with an increase in methylation. Adapted from Sun and colleagues [8].

Soil salinity due to anthropogenic factors is becoming an increasing environmental concern [9,10]. With an increasing demand for road salt ever since the 1940s [11], it is estimated that more than 50% of current croplands may be lost within the 21st century [12]. This is concerning not only due to the impact it has on the environment but also because it may imply that food resources may become limited for our increasing population.

Epigenetic states mediated by either DNA methylation or histone modifications affect plant development and can often result in either adaptive or maladaptive phenotypes. However, recent studies show promising results that show that epigenetic changes can aid with stress tolerance and acclimation [13]. Therefore, understanding epigenetic marks relative to memory may hold hope for future biotechnological advances in agriculture.

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References

1. Hauser, M. T., W. Aufsatz, C. Jonak, and C. Luschnig. 2011. Transgenerational inheritance in plants. Biochim Biophys Acta 1809:459-468.

2. Chan, S. W., I. Henderson, and S. E. Jacobsen. 2005. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360.

3. Zhong, X., J. Du, C. J. Hale, J. Gallego-Bartolome, S. Feng, A.A. Vashisht, J. Chory, J. A. Wohlschlegel, D. J. Patel, and S. E. Jacobsen. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:1050-1060.

4. Zhang, X., J. Yazaki, A. Sundaresan, S. Cokus, S. Chan, H. Chen, I. Henderson, P Shinn, M. Pellegrini, S. Jacobsen, J. Ecker. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189-1201.

5. Bannister, A. J., and T. Kouzarides. 2011. Regulation of chromatin by histone modifications. Cell Res 21:381–395.

6. Pasque, V., J. Jullien, K. Miyamoto, R. P. Halley-Stott, and J. B. Gurdon. 2011. Epigenetic factors influencing resistance to nuclear reprogramming. Trends in genetics 27:516–525.

7. Iwasaki, M., and J. Paskowski. 2014. Epigenetic memory in plants. EMBO J 33:1987-1998.

8. Sun, L., G. Song, W. Guo, W. Wang, H. Zhao, T. Gao, Q. Lv, X. Yang, F. Xu, Y. Dong, and L. Pu. 2019. Dynamic changes in genome-wide histone3 lysine27 trimethylation and gene expression of soybean roots in response to salt stress. Front Plant Sci 10:1031. https://doi.org/10.3389/fpls.2019.01031

9. Shrivastava, P., and R. Kumar. 2015. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi journal of biological sciences 22:123-131.

10. Litalien, A., and B. Zeeb. 2020. Curing the earth: A review of anthropogenic soil salinization and plant-based strategies for sustainable mitigation. Science of The Total Environment 698:134235. https://doi.org/10.1016/j.scitotenv.2019.134235

11. Daley, M., J. D. Potter, and W. H. McDowell. 2009. Salinization of urbanizing New Hampshire streams and groundwater: effects of road salt and hydrologic variability. J. N. Am. Benthol. Soc. 28:929-940.

12. Mahajan, S., and N. Tuteja. 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444:139-158.

13. Chinnusamy, V., Z. Gong, and J. Zhu. 2008. Abscisic acid-mediated epigenetic processes in plant development and stress responses. Journal of integrative plant biology 50:1187–1195.