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Specialty Grand Challenge ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Plant Sci. | doi: 10.3389/fpls.2019.01545

Marine and freshwater plants: challenges and expectations

  • 1iRTSV, CEA Grenoble, UMR5168 Laboratoire de Physiologie Cellulaire Vegetale (LPCV), France

identified by their photosynthetic pigments: the green lineage, comprising green algae and embryophytes forming together the Viridiplanta, the red lineage, consisting of red algae, and the glaucophytes, comprising few species (Marechal, 2018). In addition, a more recent cyanobacterial endosymbiosis has occurred in Paullinellida, at the origin of a photosynthetic organelle called the chromatophore (Archibald, 2017). The vast majority of photosynthetic eukaryotes populating aquatic ecosystems are neither Archaeplastida nor Paullinellida, as they derive from secondary endosymbiosis events that have occurred later, after the engulfment and reduction of a green or a red alga inside a secondary eukaryotic host cell (de Vargas et al., 2015). Some organelles have also been 'stolen' from one cell to another by a process known as kleptoplasty (Hehenberger et al., 2019). The green and red lineages can, therefore, be traced in secondary endosymbionts, for instance in Euglenida and Heterokonta, respectively. In all cases, massive endosymbiotic and horizontal gene transfers have occurred, indicating the contribution of multiple prokaryotes, eukaryotes and possibly viruses in the emergence of novel clades. Genomes have a mosaic organization resulting from this complex history (Obornik, 2018). Major phyla of photosynthetic eukaryotes have nonphotosynthetic, and even plastid-free relatives. In the red lineage, Chromera velia is close to Apicomplexa, such as the malaria causative agent Plasmodium falciparum, containing a non-green plastid. In the green lineage, Euglena gracilis is close to human parasites such as Trypanosoma cruzi, the causative agent of Chagas disease, devoid of any plastid. Although a rough estimate of more than two thirds of the biodiversity of photosynthetic eukaryotes derive from a secondary endosymbiosis (de Vargas et al., 2015), Euglenophyta, Chlorarachniophyta, Cryptophyta, Haptophyta, Heterokontophyta, Dinophyta, etc., have been far less studied than green algae and vascular plants. A fascinating but really challenging task is, therefore, to trace, reconstruct and refine missing events. The mosaic architecture of genomes needs to be characterized with care. The definition and positioning of clades in the Tree of Life and the refining of taxonomy are also crucial for large-scale studies at ecosystems' level. Environmental DNA and/or RNA, analyzed with barcoding, metagenomic and/or meta-transcriptomic methods, are used to define 'operational taxonomic units ', or OTUs (de Vargas et al., 2015). Better characterizations of species and their mosaic genomes are therefore necessary to improve the assignment and interpretation of OTUs, and address the structure and dynamics of natural populations and communities in water ecosystems.Propagation of unicellular, colonial and multicellular organisms, ecotypes and cryptic species, life cycles, genetic diversification and adaptation mechanisms.Schematically, cell and organism propagation is less constrained in water. Simple cell division is actually the basis of cyanobacteria propagation in all environments, developing resisting forms, spores and cysts to cope with adverse periods. In water, mitotic divisions of phytoplankton, in haploid or diploid states, can be sufficient to populate large biogeographic areas. By contrast, a fixed lifestyle marks some major clades of macroalgae, most spectacular being kelp forests. Although vegetative reproduction occurs in land plants as well, breeding is a major process for the expansion of terrestrial species and it coincides with the acquisition of genetic variations. In aquatic ecosystems, it seems that all reproductive processes exist and allow genetic diversification. Sexual reproduction of some eukaryotic algae may be minor, undemonstrated or even absent, leading to the possible existence of cryptic species (Grimsley et al., 2010). Genetic variations can be acquired by a multitude of processes other than recombination during meiosis. These mechanisms include spontaneous mutations, permanent exposure to free or viral DNA in the water environment, and numerous mechanisms of horizontal gene transfers. The importance of transposable elements needs to be evaluated in aquatic photosynthetic organisms, compared to the role they have as drivers of genome evolution in numerous terrestrial plants. Emergence of allopolyploidy, combining parental genomes from distinct species, has been little described in marine algae, with noticeable exceptions such as the hybrid diatom Fistulifera solaris (Nomaguchi et al., 2018). Vegetative reproduction is also a key to the existence of longer generations in life cycles of unparalleled variety and complexity. The alternation of diploid and haploid generations and sex determination can follow schemes that are often very sophisticated and unique to some algal and protist phyla (Umen and Coelho, 2019). A second challenge is, therefore, to combine our efforts to characterize the diverse and complex life cycles of marine and freshwater plants. Molecular and cellular mechanisms of mitosis and meiosis, genetic determinants of sexual dimorphism in haploid and/or diploid generations, formation of monoor polynucleated cells, acquisition of multicellularity, differentiation of cell types and gametes, spores and cysts, etc., need to be characterized in all major clades of unicellular and colonial algae, photosynthetic protists and eventually seaweeds.The complexity of the intracellular compartmentalization deriving from secondary endosymbiosis, mentioned above, makes the cells of Chlamydomonas, Arabidopsis, yeast or any kind of popular animal cell model, frustratingly simple. Sequenced genomes and metagenomes reveal lists of genes with no homolog, or with homology restricted to some clades. A third challenge is to accept that we need to perform molecular and cellular dissections of unknown gene products, unknown subcellular structures, using the tools of cell fractionations and biochemistry widely available in the 1990's, one thought we would not need following the release of complete genome sequences of dominating study models. Fortunately, analytical methods for the determination of the proteome, lipidome, metabolome, etc., of isolated cells and cell fractions have a sensitivity requesting much lower amounts of starting material (e.g. ). Strategies can also help addressing the role of unknown genes, circumventing the biochemical characterization of cell extracts, by attempting to interpret gene expression levels in some physiological states or in response to environmental conditions, and by the use of genetic engineering and editing methods (e.g. (Kroth et al., 2018;Stukenberg et al., 2018)(Gachon et al., 2007). Each model is key to address questions in relation to specific clades of algae. None of them is perfect, but they have become more or less popular and distributed in different laboratories. Novel model or non-model species are also critical to address specific or novel questions, such as Galdieria sulphuraria, to study life in sulfuric acidic hot springs (Hirooka and Miyagishima, 2016), Chromera velia or Vitrella brassicaformis to address the origin of Apicomplexa parasites, etc (Fussy et al., 2019). Efforts should, therefore, be focused on well-selected organisms. The recent methodic explorations of aquatic ecosystems with new technologies, combining environmental DNA analysis (Carradec et al., 2018) with the collection of live samples may help us identifying novel study models. Specific tools for molecular engineering (vectors, transformation methods, RNA interference, genetic recombination, overexpression, etc.), gene editing (e.g. TALEN, Crispr-Cas9, etc.) and phenotype characterization (high-resolution imaging, single-cell analyses, etc.) need to be developed for these cell lines, sometimes difficult to genetically transform.Diversity of unicellular and multicellular architectures, cell compartments, photosynthetic processes and metabolic pathways, genetic regulation systems, signaling, and developmental processes.The most obvious gaps of knowledge concern the complexity of functional architectures, found for instance in 'exotic' cell structures (e.g. nucleomorph in Cryptophyta or Chlorarachniophyta, mineralized cell wall in Coccolitophores or Diatoms, chromatophore in Paullinelidae, ocelloid in some Dinoflagellates). The organization and origin of the secondary or complex plastid in Chromista, bounded by four membranes (e.g. (Flori et al., 2016;Cavalier-Smith, 2018)) is an essential question that needs to be addressed. Multicellularity acquired by fixed macroalgae, living in a vertically contrasted environment in terms of light, salinity, exposure to the air at low tides, etc (Smale, 2019) also seems to be guided by constrains differing from those found in terrestrial ecosystems, in which the acquisition of vascular tissues proved critical to link organs developing in the soil and in the air. Photosynthesis and carbon metabolism, which seem to unify photosynthetic taxa, combine in fact common and distinct machineries and pathways that need to be unraveled (e.g. (Giovagnetti and Ruban, 2018)). Pigmented photosystems, photoprotection mechanisms, CO2 concentration and capture systems, etc need to be structurally and functionally deciphered. The biology of the pyrenoid, the relation between autotrophy, heterotrophy, and mixotrophy, are critical questions. Concerning development and differentiation, the mechanisms controlling gene expression, by the action of specific transcription factors but also via poorly characterized epigenetic mechanisms, controlling gene regulatory networks, need to be addressed (Tirichine and Bowler, 2011). The fourth grand challenge we face is, therefore, to dissect and clarify functional organizations that are unique to clades of marine and freshwater plants, in relation to their environment.Predominance of water is not sufficient to characterize an aquatic ecosystem. Habitats can be marked by spatiotemporal variations in light intensity and chromatic quality, temperature, pH, concentrations of salts, of all kinds of nutrients such as nitrogen, phosphorus, sulfur, iron, silica, etc., of CO2, noxious gases, particles, pollutants, etc. Water can also have various states, from liquid to snow, ice and even droplets in aerosols. Connectivity between water habitats can provoke a brutal transfer from a physicochemical environment to another, such as in estuaries, mangroves, upwelling or any kind of displacement in a water column, during freezing and melting. Environmental changes can also be progressive between highly contrasted conditions. For instance, in sub-polar areas, photosynthetic organisms are exposed to light during a few months, whereas the rest of the year consists of a long night. Connectivity with other habitats, such as sediments, soils, and air is also common. Interactions with the abiotic environment need therefore to be established in a broad variety of conditions, including various transitional gradients between highly contrasted conditions. Intra-and interspecies biotic interactions need also to be addressed, providing clues on the dynamics of populations and communities and helping to characterize natural associations of microbial species, or holobionts (e.g. (Lachnit et al., 2015;Arnaud-Haond et al., 2017;Decelle et al., 2019;Ziegler et al., 2019)). These include, and are not limited to, interactions with bacteria, grazers, viruses, the formation of photosymbiotic and/or parasitic associations. This fifth challenge, aiming at characterizing abiotic and biotic interactions, is based on molecular mechanisms, including intra-and intercellular signaling molecules (e.g. calcium, cyclic nucleotides, oxylipins, phosphoinositides, 'infochemicals', 'phytohormones', etc.), their receptors, the signaling cascades they trigger and responses from genetic reprogramming to metabolic remodeling, activation of immune mechanisms and cell differentiation. Gained knowledge will be essential to improve our understanding of the role(s) of marine and freshwater plants in geochemical cycles and trophic networks. Knowledge is also critically needed to address the proliferation of algae in phytoplankton blooms, including harmful cyanobacterial blooms (Alvarenga et al., 2017), and in seaweed blooms, such as green tides occurring with an increasing frequencies on coastal areas (Zhao et al., 2019), or sargassum blooms that are so huge that they are considered to form the so-called Great Atlantic Sargassum Belt . Photosynthetic algae benefit from increased CO2 availability and their proliferation can be considered as a marker of global climate change. In the case of blooms of green algae in the snow cover, forming so-called 'red snow' in polar area and high altitudes, the pigmentation increases the albedo and accelerates melting: algae are then actors of climate change by a positive feedback loop (Kintisch, 2017). Understanding abiotic and biotic relations is, therefore, necessary to address the impact on, and the role of marine and freshwater plants in the environmental crisis.Expectations for the development of algae-based technologies.Last and not least, aquatic photosynthetic organisms are seen as a still to be explored mine of biomolecules, such as lipids, carbohydrates, pigments, secondary metabolites, etc. for high-value applications, including feed, food, health or cosmetics. They are also a promising feedstock for green chemistry (sometimes called blue chemistry), biomaterials and bioenergies (Scaife and Smith, 2016;Lupette and Maréchal, 2018). Algae can also serve as cell factories after genetic engineering. Expectations are high, but numerous biological and technological issues need to be resolved. Some species have reached the status of industrial production strains. Efforts are put to characterize and improve the domestication of microalgae such as Spirulina spp., Chlorella spp., Haematococcus pluvialis, Nannochloropsis spp., non-photosynthetic Thraustochytrids, and seaweeds and kelp, such as Saccharina japonica, Undaria pinnatifida, Porphyra tenebra, etc. Search for valuable novel strains is critical. In this last challenge, it seems that two major obstacles need to be overcome at the level of the developed strains. The first one is the production of biomass that seems to depend on the limitations of photosynthesis efficiency. The second obstacle is to succeed controlling carbon partitioning in cultivated strain to produce valuable biomolecules, for instance oil, with an economically viable yield and quality. Other key questions include the development of appropriate cultivation systems, nutrient supplies complying with sustainability models, and low-energy harvesting and extracting methods. All these applied issues rely on the advance of fundamental research.In conclusion, the field of marine and freshwater plant science is immense and fascinating. The advancement of knowledge should benefit from cross-fertilization of disciplines, from environmental sciences to molecular and cell biology, from the biophysics of photosynthesis and biochemistry of metabolism to biotechnological developments. No doubt that this field will lead to important discoveries changing our views on eukaryotes' biodiversity and ecosystems and leading to the development of an alga-based economy. AcknowledgmentsThe author is supported by the Centre National de la Recherche Scientifique, the Commissariat à l'Energie Atomique et aux Energies Alternatives, the Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, the Université Grenoble Alpes, and by grants from the French National Research Agency (Oceanomics ANR-11-BTBR-0008, GlycoAlps ANR-15-IDEX-02, GRAL Labex ANR-10-LABEX-04, and EUR CBS ANR-17-EURE-0003).

Keywords: algae, Phytoplankton, Seaweed, Photosynthesis, endosymbiosis, bloom, holobiont, blue biotechnologies

Received: 16 Oct 2019; Accepted: 05 Nov 2019.

Copyright: © 2019 Marechal. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Eric Marechal, UMR5168 Laboratoire de Physiologie Cellulaire Vegetale (LPCV), iRTSV, CEA Grenoble, Grenoble, 38054, France,