Trade-off between sex and growth in diatoms: Molecular mechanisms and demographic implications.

Diatoms are fast-growing and winning competitors in aquatic environments, possibly due to optimized growth performance. However, their life cycles are complex, heteromorphic, and not fully understood. Here, we report on the fine control of cell growth and physiology during the sexual phase of the marine diatom Pseudo-nitzschia multistriata. We found that mating, under nutrient replete conditions, induces a prolonged growth arrest in parental cells. Transcriptomic analyses revealed down-regulation of genes related to major metabolic functions from the early phases of mating. Single-cell photophysiology also pinpointed an inhibition of photosynthesis and storage lipids accumulated in the arrested population, especially in gametes and zygotes. Numerical simulations revealed that growth arrest affects the balance between parental cells and their siblings, possibly favoring the new generation. Thus, in addition to resources availability, life cycle traits contribute to shaping the species ecological niches and must be considered to describe and understand the structure of plankton communities.

Gene body DNA methylation in seagrasses: inter- and intraspecific differences and interaction with transcriptome plasticity under heat stress.

The role of DNA methylation and its interaction with gene expression and transcriptome plasticity is poorly understood, and current insight comes mainly from studies in very few model plant species. Here, we study gene body DNA methylation (gbM) and gene expression patterns in ecotypes from contrasting thermal environments of two marine plants with contrasting life history strategies in order to explore the potential role epigenetic mechanisms could play in gene plasticity and responsiveness to heat stress. In silico transcriptome analysis of CpGO/E ratios suggested that the bulk of Posidonia oceanica and Cymodocea nodosa genes possess high levels of intragenic methylation. We also observed a correlation between gbM and gene expression flexibility: genes with low DNA methylation tend to show flexible gene expression and plasticity under changing conditions. Furthermore, the empirical determination of global DNA methylation (5-mC) showed patterns of intra and inter-specific divergence that suggests a link between methylation level and the plants' latitude of origin and life history. Although we cannot discern whether gbM regulates gene expression or vice versa, or if other molecular mechanisms play a role in facilitating transcriptome responsiveness, our findings point to the existence of a relationship between gene responsiveness and gbM patterns in marine plants.

Exploring Molecular Signs of Sex in the Marine Diatom Skeletonema marinoi.

Sexual reproduction plays a fundamental role in diatom life cycles. It contributes to increasing genetic diversity through meiotic recombination and also represents the phase where large-sized cells are produced to counteract the cell size reduction process that characterizes these microalgae. With the aim to identify genes linked to the sexual phase of the centric planktonic diatom Skeletonemamarinoi, we carried out an RNA-seq experiment comparing the expression level of transcripts in sexualized cells with that of large cells not competent for sex. A set of genes involved in meiosis were found upregulated. Despite the fact that flagellate gametes were observed in the sample, we did not detect the expression of genes involved in the synthesis of flagella that were upregulated during sexual reproduction in another centric diatom. A comparison with the set of genes changing during the first phases of sexual reproduction of the pennate diatom Pseudo-nitzschiamultistriata revealed the existence of commonalities, including the strong upregulation of genes with an unknown function that we named Sex Induced Genes (SIG). Our results further broadened the panel of genes that can be used as a marker for sexual reproduction of diatoms, crucial for the interpretation of metatranscriptomic datasets.

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

The Mediterranean Sea is particularly vulnerable to warming and the abrupt declines experienced by the endemic Posidonia oceanica populations after recent heatwaves have forecasted severe consequences for the ecological functions and socio-economical services this habitat forming species provides. Nevertheless, this highly clonal and long-lived species could be more resilient to warming than commonly thought since heat-sensitive plants massively bloomed after a simulated heatwave, which provides the species with an opportunity to adapt to climate change. Taking advantage of this unexpected plant response, we investigated for the first time the molecular and physiological mechanisms involved in seagrass flowering through the transcriptomic analysis of bloomed plants. We also aimed to identify if flowering is a stress-induced response as suggested from the fact that heat-sensitive but not heat-tolerant plants flowered. The transcriptomic profiles of flowered plants showed a strong metabolic activation of sugars and hormones and indications of an active transport of these solutes within the plant, most likely to induce flower initiation in the apical meristem. Preflowered plants also activated numerous epigenetic-related genes commonly used by plants to regulate the expression of key floral genes and stress-tolerance genes, which could be interpreted as a mechanism to survive and optimize reproductive success under stress conditions. Furthermore, these plants provided numerous molecular clues suggesting that the factor responsible for the massive flowering of plants from cold environments (heat-sensitive) can be considered as a stress. Heat-stress induced flowering may thus be regarded as an ultimate response to survive extreme warming events with potential adaptive consequences for the species. Fitness implications of this unexpected stress-response and the potential consequences on the phenotypic plasticity (acclimation) and evolutionary (adaptation) opportunity of the species to ocean warming are finally discussed.

MRP3 is a sex determining gene in the diatom Pseudo-nitzschia multistriata.

A broad diversity of sex-determining systems has evolved in eukaryotes. However, information on the mechanisms of sex determination for unicellular microalgae is limited, including for diatoms, key-players of ocean food webs. Here we report the identification of a mating type (MT) determining gene for the diatom Pseudo-nitzschia multistriata. By comparing the expression profile of the two MTs, we find five MT-biased genes, of which one, MRP3, is expressed exclusively in MT+ strains in a monoallelic manner. A short tandem repeat of specific length in the region upstream of MRP3 is consistently present in MT+ and absent in MT- strains. MRP3 overexpression in an MT- strain induces sex reversal: the transgenic MT- can mate with another MT- strain and displays altered regulation of the other MT-biased genes, indicating that they lie downstream. Our data show that a relatively simple genetic program is involved in defining the MT in P. multistriata.

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

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.

Tissue-specific transcriptomic profiling provides new insights into the reproductive ecology and biology of the iconic seagrass species Posidonia oceanica.

Seagrasses form extensive meadows in shallow coastal waters and are among the world's most productive ecosystems. Seagrasses can produce both clonally and sexually, and flowering has long been considered infrequent, but important for maintaining genetically diverse stands. Here we investigate the molecular mechanisms involved in flowering of the seagrass Posidonia oceanica, an iconic species endemic to the Mediterranean. We generated a de novo transcriptome of this non-model species for leaf, male and female flower tissue of three individuals, and present molecular evidence for genes that may be involved in the flowering process and on the reproductive biology of the species. We present evidence that suggests that P. oceanica exhibits a strategy of protogyny, where the female part of the hermaphroditic flower develops before the male part, in order to avoid self-fertilization. We found photosynthetic genes to be up-regulated in the female flower tissues, indicating that this may be capable of photosynthesis. Finally, we detected a number of interesting genes, previously known to be involved in flowering pathways responding to light and temperature cues and in pathways involved in anthocyanin and exine synthesis. This first comparative transcriptomic approach of leaf, male and female tissue provides a basis for functional genomics research on flower development in P. oceanica and other seagrass species.