Molecular Mechanisms behind the Physiological Resistance to Intense Transient Warming in an Iconic Marine Plant

Abstract

The endemic Mediterranean seagrass Posidonia oceanica is highly threatened by the increased frequency and intensity of heatwaves. Meadows of the species offer a unique opportunity to unravel mechanisms marine plants activate to cope transient warming, since their wide depth distribution impose divergent heat-tolerance. Understanding these mechanisms is imperative for their conservation. Shallow and deep genotypes within the same population were exposed to a simulated heatwave in mesocosms, to analyze their transcriptomic and photo-physiological responses during and after the exposure. Shallow plants, living in a more unstable thermal environment, optimized phenotype variation in response to warming. These plants showed a pre-adaptation of genes in anticipation of stress. Shallow plants also showed a stronger activation of heat-responsive genes and the exclusive activation of genes involved in epigenetic mechanisms and in molecular mechanisms that are behind their higher photosynthetic stability and respiratory acclimation. Deep plants experienced higher heat-induced damage and activated metabolic processes for obtaining extra energy from sugars and amino acids, likely to support the higher protein turnover induced by heat. In this study we identify transcriptomic mechanisms that may facilitate persistence of seagrasses to anomalous warming events and we discovered that P. oceanica plants from above and below the mean depth of the summer thermocline have differential resilience to heat.

Heat‐stress induced flowering can be a potential adaptive response to ocean warming for the iconic seagrass Posidonia oceanica

“…Functional enrichment analysis showed that the early (T1) response of C‐plants to temperature increase included the activation of biological processes previously reported in the short‐term heat response of P. oceanica (Marín‐Guirao et al, ), and encompassed the modification of primary and secondary metabolism, protein folding and cell wall reorganization (Figure , Table a). The response was more intense after 6 weeks of heat exposure (T2) as reflected by the number of DEGs.…”

“…The newly assembled transcriptome was combined with three previously published P. oceanica transcriptomes using Trinity to generate a comprehensive and representative transcriptome of the species. A whole description of methods and bioinformatic analysis of these three de novo assemblies can be found elsewhere (D'Esposito et al, ; Entrambasaguas et al, ; Marín‐Guirao et al, ). In order to remove intra‐assembly redundancy, each individual assembly was firstly processed by cd‐hit‐est v4.6.7 (Huang, Niu, Gao, Fu, & Li, ) with 100% identity to remove identical contigs with a word size of 10.…”

“…DE analysis was confirmed using real‐time PCR (RT‐PCR, Figure , Table ), as described in Marín‐Guirao et al (). Briefly, seven randomly selected genes were analyzed through RT‐qPCR on the same samples used in the study.…”

“…A whole description of methods and bioinformatic analysis of these three de novo assemblies can be found elsewhere (D'Esposito et al, 2016;Entrambasaguas et al, 2017;Marín-Guirao et al, 2017). In order to remove intra-assembly redundancy, each individual assembly was firstly processed by cd-hit-est v4.6.7 (Huang, Niu, Gao, Fu, & Li, 2010) with 100% identity to remove identical contigs with a word size of 10.…”

“…Despite this pessimistic scenario, plants adapted to warm thermal environments have shown better different capability to acclimate to temperature changes, in respect to plants from different latitudes. Warm adapted populations were able to activate a suite of physiological and molecular mechanisms to tolerate simulated heatwave exposures (Marín‐Guirao, Entrambasaguas, Dattolo, Ruiz, & Procaccini, ; Marín‐Guirao, Ruiz, Dattolo, Garcia‐Muñoz, & Procaccini, ; Tutar, Marín‐Guirao, Ruiz, & Procaccini, ). Cold‐adapted plants, instead, showed clear physiological symptoms of heat stress and reduced fitness (Beca‐Carretero et al, ; Marín‐Guirao et al, ), which might point to a greater risk of local extinction.…”