The chloroplast redox-responsive transcriptome of solanaceous plants reveals significant nuclear gene regulatory motifs associated to stress acclimation

Plastid functions depend on the coordinated expression of nuclear genes, many of them associated to developmental and stress response pathways. Plastid-generated signals mediate this coordination via retrograde signaling, which includes sensing of chloroplast redox state and levels of reactive oxygen species (ROS), although it remains a poorly understood process. Chloroplast redox poise and ROS build-up can be modified by recombinant expression of a plastid-targeted antioxidant protein, i.e., cyanobacterial flavodoxin, with the resulting plants displaying increased tolerance to multiple environmental challenges. Here we analysed the transcriptomes of these flavodoxin-expressing plants to study the coordinated transcriptional responses of the nucleus to the chloroplast redox status and ROS levels during normal growth and stress responses (drought or biotic stress) in tobacco and potato, members of the economically important Solanaceae family. We compared their transcriptomes against those from stressed and mutant plants accumulating ROS in different subcellular compartments and found distinct ROS-related imprints modulated by flavodoxin expression and/or stress. By introducing our datasets in a large-scale interaction network, we identified transcriptional factors related to ROS and stress responses potentially involved in flavodoxin-associated signaling. Finally, we discovered identical cis elements in the promoters of many genes that respond to flavodoxin in the same direction as in wild-type plants under stress, suggesting a priming effect of flavodoxin before stress manifestation. The results provide a genome-wide picture illustrating the relevance of chloroplast redox status on biotic and abiotic stress responses and suggest new cis and trans targets to generate stress-tolerant solanaceous crops.Fil: Arce, Rocio Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Pierella Karlusich, Juan José. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentin

Environmental selection pressures related to iron utilization are involved in the loss of the Flavodoxin Gene from the plant genome

Oxidative stress and iron limitation represent the grim side of life in an oxygen-rich atmosphere. The versatile electron transfer shuttle ferredoxin,aniron-sulfurprotein,isparticularlysensitivetothesehardships,anditsdownregulationunderadverseconditionsseverely compromises survival of phototrophs. Replacement of ferredoxin by a stress-resistant isofunctional carrier, flavin-containing flavodoxin, is a widespread strategy employed by photosynthetic microorganisms to overcome environmental adversities. The flavodoxin gene was lostin the course ofplantevolution, but its reintroduction in transgenicplants confers increased tolerance to environmental stress and iron starvation, raising the question as to whya genetic asset with obvious adaptive value was not kept by natural selection. Phylogenetic analyses reveal that the evolutionary history of flavodoxin is intricate, with several horizontal gene transfer events between distant organisms, including Eukarya, Bacteria, and Archaea. The flavodoxin gene is unevenly distributed in most algal lineages, with flavodoxin-containing species being overrepresented in iron-limited regions and scarce or absent in iron-rich environments. Evaluation of cyanobacterial genomic and metagenomic data yielded essentially the same results, indicating that there was little selection pressure to retain flavodoxin in iron-rich coastal/freshwater phototrophs. Our results show a highly dynamic evolution pattern of flavodoxin tightly connected to the bioavailability of iron. Evidence presented here also indicates that the high concentration of iron in coastal and freshwater habitats may have facilitated the loss of flavodoxin in the freshwater ancestor of modern plants during the transition of photosynthetic organisms from the open oceans to the firm land.Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina. Universidad Nacional de Rosario; ArgentinaFil: Ceccoli, Romina Denis. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas; ArgentinaFil: Graña, Martín. Instituto Pasteur de Montevideo; UruguayFil: Romero, Héctor. Universidad de la Republica; UruguayFil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina. Universidad Nacional de Rosario; Argentin

Combatiendo la sequía con flavodoxina

Los episodios de estrés ambiental, especialmente la limitación de agua, representan la principal causa de pérdida de rendimiento en cultivos.Las plantas responden a estas situaciones mediante la expresión diferencial de una red de genes cuyos productos participan en la percepción, señalización, regulación transcripcional y finalmente la defensa ante la situación hostil mediante cambios bioquímicos y fisiológicos. La estrategia de la genética molecular para el mejoramiento de la tolerancia a condiciones ambientales adversas en cultivos se ha basado mayoritariamente en la sobreexpresión de dichos genes endógenos. El grado de éxito ha sido variable ya que se trata de una respuesta multigénica y, en consecuencia, difícil depredecir y manipular. Las cianobacterias, de las que las plantas han evolucionado a través de un proceso de endosimbiosis,han desarrollado estrategias sustitutivas y unigénicas basadas en el reemplazo de proteínas sensibles al estrés por versionesisofuncionales resistentes. Un ejemplo notorio es ferredoxina, el último componente de la cadena transportadora fotosintética.Ferredoxina resulta particularmente susceptible a los desafíos ambientales y ante tales situaciones muchas cianobacterias son capaces de expresar flavodoxina, que sustituye funcionalmente a ferredoxina aunque con menor eficiencia. Aunque el gen de flavodoxina ha desaparecido de las plantas, la reintroducción de una flavodoxina cianobacteriana en cloroplastos de distintas especies vegetales produjo líneas transgénicas con tolerancia aumentada a diversas fuentes de estrés ambiental, incluyendo sequía. Por lo tanto, las estrategias sustitutivas de los microorganismos siguen siendo efectivas en las plantas y esto abre nuevas perspectivas biotecnológicas para combatir el problema de la deficiencia de agua.Environmental stresses, especially water limitation, represent the primary cause of crop yield losses. Plants respond to such situations through the differential expression of a gene network whose products are involved in stress perception, signaling, transcriptional regulation and finally the defense against the hostile situation via biochemical and physiological changes. The strategy of molecular genetics to strengthen stress tolerance in crops has been largely based on over expression of those endogenous genes. The success of this approach has been variable as it is a multigenic response and, consequently, difficult to manipulate. Cyanobacteria, from which plants evolved though a process of endosymbiosis, have developed unigenic, substitutive strategies based on the replacement of stress-vulnerable targets by resistant isofunctional proteins. A notable example is ferredoxin, the terminal acceptor of the photosynthetic electron transport chain. Ferredoxin is particularly susceptible to environmental challenges and, under such situations, many cyanobacteria are able to express flavodoxin which functionally substitutes ferredoxin but with less efficiency. Although the Fld coding gene has been lost from the plant genome, the reintroduction of a cyanobacterial flavodoxin in chloroplasts of different plant species gave rise to transgenic lines with enhanced tolerance to multiple sources of environmental stress, including drought. Therefore, the substitutive responses from microorganisms are still effective in plants and this situation opens new biotechnological perspectives to combat the water deficiency problem.Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentin

Evolution of the acceptor side of photosystem I: ferredoxin, flavodoxin, and ferredoxin-NADP+ oxidoreductase

The development of oxygenic photosynthesis by primordial cyanobacteria ~2.7 billion years ago led to major changes in the components and organization of photosynthetic electron transport to cope with the challenges of an oxygen-enriched atmosphere. We review herein, following the seminal contributions as reported by Jaganathan et al. (Functional genomics and evolution of photosynthetic systems, vol 33, advances in photosynthesis and respiration, Springer, Dordrecht, 2012), how these changes affected carriers and enzymes at the acceptor side of photosystem I (PSI): the electron shuttle ferredoxin (Fd), its isofunctional counterpart flavodoxin (Fld), their redox partner ferredoxin-NADP+ reductase (FNR), and the primary PSI acceptors Fx and FA/FB. Protection of the [4Fe–4S] centers of these proteins from oxidative damage was achieved by strengthening binding between the FA/FB polypeptide and the reaction center core containing Fx, therefore impairing O2 access to the clusters. Immobilization of FA/FB in the PSI complex led in turn to the recruitment of new soluble electron shuttles. This function was fulfilled by oxygen-insensitive [2Fe–2S] Fd, in which the reactive sulfide atoms of the cluster are shielded from solvent by the polypeptide backbone, and in some algae and cyanobacteria by Fld, which employs a flavin as prosthetic group and is tolerant to oxidants and iron limitation. Tight membrane binding of FNR allowed solid-state electron transfer from PSI bridged by Fd/Fld. Fine tuning of FNR catalytic mechanism led to formidable increases in turnover rates compared with FNRs acting in heterotrophic pathways, favoring Fd/Fld reduction instead of oxygen reduction.Fil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Carrillo, Nestor Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentin

Better together? Lessons on sociality from Trichodesmium

The N2-fixing cyanobacterium Trichodesmium is an important player in the oceanic nitrogen and carbon cycles. Trichodesmium occurs both as single trichomes and as colonies containing hundreds of trichomes. In this review, we explore the benefits and disadvantages of colony formation, considering physical, chemical, and biological effects from nanometer to kilometer scale. Showing that all major life challenges are affected by colony formation, we claim that Trichodesmium\u27s ecological success is tightly linked to its colonial lifestyle. Microbial interactions in the microbiome, chemical gradients within the colony, interactions with particles, and elevated mobility in the water column shape a highly dynamic microenvironment. We postulate that these dynamics are key to the resilience of Trichodesmium and other colony formers in our changing environment

Exploration of marine phytoplankton: From their historical appreciation to the omics era

Marine phytoplankton are believed to account for more than 45% of photosynthetic net primary production on Earth, and hence are at the base of marine food webs and have an enormous impact on the entire Earth system. Their members are found across many of the major clades of the tree of life, including bacteria (cyanobacteria) and multiple eukaryotic lineages that acquired photosynthesis through the process of endosymbiosis. Our understanding of their distribution in marine ecosystems and their contribution to biogeochemical cycles have increased since they were first described in the 18th century. Here, we review historical milestones in marine phytoplankton research and how their roles were gradually understood, with a particular focus on insights derived from large-scale ocean exploration. We start from the first observations made by explorers and naturalists, review the initial identification of the main phytoplankton groups and the appreciation of their function in the influential Kiel and Plymouth schools that established biological oceanography, to finally outline the contribution of modern large-scale initiatives to understand this fundamental biological component of the ocean.Fil: Pierella Karlusich, Juan José. Centre National de la Recherche Scientifique. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ibarbalz, Federico Matias. Centre National de la Recherche Scientifique. Ecole Normale Supérieure; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Centro de Investigaciones del Mar y la Atmósfera. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Centro de Investigaciones del Mar y la Atmósfera; ArgentinaFil: Bowler, Chris. Centre National de la Recherche Scientifique. Ecole Normale Supérieure; Francia. Centre National de la Recherche Scientifique; Franci

Coupling Imaging and Omics in Plankton Surveys: State-of-the-Art, Challenges, and Future Directions

International audienceA major challenge in characterizing plankton communities is the collection, identification and quantification of samples in a time-efficient way. The classical manual microscopy counts are gradually being replaced by high throughput imaging and nucleic acid sequencing. DNA sequencing allows deep taxonomic resolution (including cryptic species) as well as high detection power (detecting rare species), while RNA provides insights on function and potential activity. However, these methods are affected by database limitations, PCR bias, and copy number variability across taxa. Recent developments in high-throughput imaging applied in situ or on collected samples (high-throughput microscopy, Underwater Vision Profiler, FlowCam, ZooScan, etc) has enabled a rapid enumeration of morphologically-distinguished plankton populations, estimates of biovolume/biomass, and provides additional valuable phenotypic information. Although machine learning classifiers generate encouraging results to classify marine plankton images in a time efficient way, there is still a need for large training datasets of manually annotated images. Here we provide workflow examples that couple nucleic acid sequencing with high-throughput imaging for a more complete and robust analysis of microbial communities. We also describe the publicly available and collaborative web application EcoTaxa, which offers tools for the rapid validation of plankton by specialists with the help of automatic recognition algorithms. Finally, we describe how the field is moving with citizen science programs, unmanned autonomous platforms with in situ sensors, and sequencing and digitalization of historical plankton samples

Global drivers of eukaryotic plankton biogeography in the sunlit ocean

Eukaryotic plankton are a core component of marine ecosystems with exceptional taxonomic and ecological diversity, yet how their ecology interacts with the environment to drive global distribution patterns is poorly understood. In this work, we use Tara Oceans metabarcoding data, which cover all major ocean basins, combined with a probabilistic model of taxon co-occurrence to compare the biogeography of 70 major groups of eukaryotic plankton. We uncover two main axes of biogeographic variation. First, more-diverse groups display clearer biogeographic patterns. Second, large-bodied consumers are structured by oceanic basins, mostly through the main current systems, whereas small-bodied phototrophs are structured by latitude and follow local environmental conditions. Our study highlights notable differences in biogeographies across plankton groups and investigates their determinants at the global scale.Fil: Sommeria Klein, Guilhem. Centre National de la Recherche Scientifique; Francia. Université PSL. Institut de Biologie de l’École Normale Supérieure; FranciaFil: Watteaux, Romain. Stazione Zoologica Anton Dohrn; ItaliaFil: Ibarbalz, Federico Matias. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Centro de Investigaciones del Mar y la Atmósfera. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Centro de Investigaciones del Mar y la Atmósfera; Argentina. Centre National de la Recherche Scientifique; Francia. Université PSL. Institut de Biologie de l’École Normale Supérieure; FranciaFil: Pierella Karlusich, Juan José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. Centre National de la Recherche Scientifique; Francia. Université PSL. Institut de Biologie de l’École Normale Supérieure; FranciaFil: Iudicone, Daniele. Stazione Zoologica Anton Dohrn; ItaliaFil: Bowler, Chris. Centre National de la Recherche Scientifique; Francia. Université PSL. Institut de Biologie de l’École Normale Supérieure; FranciaFil: Morlon, Hélène. Centre National de la Recherche Scientifique; Francia. Université PSL. Institut de Biologie de l’École Normale Supérieure; Franci

Contribution of genome scale metabolic modeling to niche theory

Standard niche modeling is based on probabilistic inference from organismal occurrence data but does not benefit yet from genome-scale descriptions of these organisms. This study over-comes this shortcoming by proposing a new conceptual niche that encompasses the whole metabolic capabilities of an organism. The so-called metabolic niche resumes well-known traits such as nutrient needs and their dependencies for survival. Despite the computational challenge, its implementation allows the detection of traits and the formal comparison of niches of different organisms, emphasizing that the presence-absence of functional genes is not enough to approximate the phenotype. Further statistical exploration of an organism’s niche sheds light on genes essential for the metabolic niche and their role in understanding various biological experiments, such as transcriptomics, paving the way for incorporating better the genome-scale description in ecological studies