Stress Memory in Seagrasses: First Insight Into the Effects of Thermal Priming and the Role of Epigenetic Modifications

Abstract

While thermal priming and the relative role of epigenetic modifications have been widely studied in terrestrial plants, their roles remain unexplored in seagrasses so far. Here, we experimentally compared the ability of two different functional types of seagrass species, dominant in the Southern hemisphere, climax species Posidonia australis and pioneer species Zostera muelleri, to acquire thermal-stress memory to better survive successive stressful thermal events. To this end, a two-heatwave experimental design was conducted in a mesocosm setup. Findings across levels of biological organization including the molecular (gene expression), physiological (photosynthetic performances and pigments content) and organismal (growth) levels provided the first evidence of thermal priming in seagrasses. Non-preheated plants suffered a significant reduction in photosynthetic capacity, leaf growth and chlorophyll a content, while preheated plants were able to cope better with the recurrent stressful event. Gene expression results demonstrated significant regulation of methylation-related genes in response to thermal stress, suggesting that epigenetic modifications could play a central role in seagrass thermal stress memory. In addition, we revealed some interspecific differences in thermal responses between the two different functional types of seagrass species. These results provide the first insights into thermal priming and relative epigenetic modifications in seagrasses paving the way for more comprehensive forecasting and management of thermal stress in these marine foundation species in an era of rapid environmental change.

The Seagrass Methylome Is Associated With Variation in Photosynthetic Performance Among Clonal Shoots

“…Molecular mechanisms involved in forming a stress memory include stalled RNA polymerase II, storage of chemical signaling factors, accumulation and phosphorylation of transcription factors, and epigenetic mechanisms such as microRNAs, histone modifications, and DNA methylation ( Iwasaki and Paszkowski, 2014 ; Crisp et al, 2016 ; Hilker et al, 2016 ; Gallusci et al, 2017 ; Lämke and Bäurle, 2017 ). Heat-priming has only very recently been described in seagrasses ( Nguyen et al, 2020 ). Zostera muelleri and Posidonia australis both performed better under a second heat-wave, in terms of photosynthetic capacity, leaf growth, and chlorophyll a content, when they had been previously exposed to a first heat-wave as compared with naïve controls ( Nguyen et al, 2020 ).…”

“…Heat-priming has only very recently been described in seagrasses (Nguyen et al, 2020). Zostera muelleri and Posidonia australis both performed better under a second heat-wave, in terms of photosynthetic capacity, leaf growth, and chlorophyll a content, when they had been previously exposed to a first heat-wave as compared with naïve controls (Nguyen et al, 2020). This could explain why no mortality was reported for the seagrass Posidoinia oceanica after intense and long-lasting heat-waves in 2012, 2015, and 2017 (Darmaraki et al, 2019), although it had suffered high mortality rates after the 2006 heatwave ( (Marbà and Duarte, 2010), as discussed in Nguyen et al (2020).…”

Priming of Marine Macrophytes for Enhanced Restoration Success and Food Security in Future Oceans

“…• C above natural conditions) of the seagrass species Zostera muelleri and Posidonia australis showed significantly enhanced photosynthetic capacity, leaf growth, and chlorophyll a content after exposure to heat stress (32 • C for 9 days) compared with naïve plants (Nguyen et al, 2020). Moreover, previous exposure of Zostera marina to simulated warming (15 • C for 45 days, 2 • C above control temperature) resulted in an increase in clonal shoot production and shoot length, as well as a decrease in leaf growth rates and in the ratio of below to above ground biomass (DuBois et al, 2020).…”

“…The changes, which lasted for several years across multiple clonal generations after the stress was removed, would likely be adaptive in a warmer environment by reducing the respiratory burden of non-photosynthetic tissues. As discussed in Nguyen et al (2020), heat priming may explain why the Mediterranean seagrass Posidonia oceanica did not suffer high mortality rates after intense and long-lasting heat-waves in 2012, 2015, and 2017 (Darmaraki et al, 2019), in contrast to an extensive die-off after the 2006 heatwave (Marbà and Duarte, 2010).…”

“…Evidence that epigenetic modifications contribute to form a thermal stress memory in seagrass is suggested by significant stress-induced regulation of methylation-related genes, in particular histone methyltransferases (Nguyen et al, 2020), and a change in DNA-methylation patterns that lasted for at least 5 weeks following exposure to heat stress (Jueterbock et al, 2020). A 5-week heat-stress memory is potentially long enough to heatharden the same generation of previously exposed shoots.…”