Papers by Roberto Ligrone
Bulletin of Regional Natural Sciences, 2022
Extant eukaryotes are a monophyletic lineage sharing a set of unique cellular and molecular trait... more Extant eukaryotes are a monophyletic lineage sharing a set of unique cellular and molecular traits inherited from a last common ancestor (LECA). There are no known intermediates between the eukaryotic and prokaryotic cellular organization. In contrast, the eukaryote pangenome has a chimeric structure combining eukaryote-specific genes and genes with homologs in bacteria and archaea, with bacterial genes only in part acquired via the mitochondrial symbiosis. At odd with the longheld view of a sister relationship between the archaea and eukaryotes, more recent phylogenomic work places the eukaryotes within the archaea and the root of the tree of life between the archaea and bacteria, thus supporting a 2-Domain tree of life. Challenging the traditional endosymbiotic scenario of eukaryogenesis, this novel phylogenetic paradigm has prompted hypotheses of archaeal-bacterial symbiosis with emphasis on the timing and impact of mitochondrial evolution (mitochondrion-first vs. mitochondrion-later models). Phylogenomic analysis has resolved the extant eukaryotic diversity into two major clades, the Amorphea and Diaphoretickes, leaving out several minor taxa listed as incertae sedis. The root of the eukaryote tree is still undefined. The chloroplast primarily evolved in the unicellular ancestor of Archaeplastida (Plantae) from a cyanobacterial endosymbiont, and was then transferred horizontally to other eukaryotic lineages by further events of endosymbiosis. Molecular-clock analysis integrated with paleontological evidence dates the appearance of eukaryotes to at least 1.6 billion years ago. LECA is consistently dated to about 1.2 billion years ago, and extant lineages from about 1 billion years ago onwards. The BORNH Review ; 1
Moving to the Light: The Evolution of Photosynthesis
Biological Innovations that Built the World, 2019
Photosynthesis enabled early life to severe its ancestral dependence on geochemistry. The paleoge... more Photosynthesis enabled early life to severe its ancestral dependence on geochemistry. The paleogeochemical record suggests that photosynthetic life colonized the planet photic zone as early as 3.4 GYA. Photosynthesis evolved in the Bacteria domain, and initially utilized compounds of geochemical origin such as ferrous iron or hydrogen as sources of electrons, without producing oxygen. Several variants of anoxygenic photosynthesis are present in extant bacteria. The cyanobacteria evolved oxygenic photosynthesis, a pathway that deploys two types of photosystem working in series to sum the energy of two photons for each electron transported from water to carbon dioxide. Multiple sources of evidence suggest that the cyanobacteria and oxygenic photosynthesis appeared at least 2.7 GYA, viz. 300 MY before the stable oxygenation of the planet. Endosymbiosis horizontally transferred oxygenic photosynthesis to the eukaryotes. Major similarities in the molecular architecture of photosystems in...
DNA is intrinsically unstable due to spontaneous mutation and degradation. Yet, life has thrived ... more DNA is intrinsically unstable due to spontaneous mutation and degradation. Yet, life has thrived for about four billion years, adapting to most diverse environmental conditions. The ultimate reason for the striking resilience and versatility of life is sex, here defined as any mechanism that recombines DNA from separate organisms. Sex is a universal property of life that originally emerged as a spontaneous by-product of the machinery for gene duplication and repair. Sex counteracts genetic erosion (Muller's ratchet), thus stabilizing biological information across time. Concurrently, sex builds novel genes and novel genomes, thus fostering genetic innovation and evolution. Bacterial sex is independent of reproduction, generally involves short DNA sequences, and encompasses a relatively high frequency of horizontal gene transfer between distantly related taxa. Because of this, bacterial sex produces large pangenomes, fosters population ecological flexibility, and blurs species dem...
Biological Innovations that Built the World, 2019
The eukaryote pangenome has a chimeric structure encompassing genes unique to eukaryotes (~41%), ... more The eukaryote pangenome has a chimeric structure encompassing genes unique to eukaryotes (~41%), and genes of bacterial (~50% of total) and archaeal ancestry (~9%). Crucially, bacterial sequences far exceed the set acquired from the proteobacterial ancestor of mitochondria. Extant eukaryotic lineages share a common ancestor (LECA) that had all the fundamental traits of eukaryotes including the mitochondrion. The current debate about eukaryote origins revolves around two competing scenarios. The fusion model posits that the eukaryotes derive from the "fusion" of an archaeon and a bacterium, and that the acquisition of the mitochondrion was pivotal to the evolution of other eukaryotic traits. The neomuran model maintains that the archaea and eukaryotes are sister groups devived from a bacterial ancestor, and that fundamental eukaryotic traits including phagocytosis were already in place before the evolution of the mitochondrion by endosymbiosis. Eukaryote placement within the archaea in phylogenomic analysis supports the fusion scenario. The predominance of bacterial sequences in the eukaryote pangenome, the bacterial stereochemistry of eukaryote membrane lipids, and similar trajectories in mitochondrial and chloroplast evolution favour the neomuran scenario. Phylogenomic analysis resolves two major eukaryotic domains, the Amorphea and Diaphoretika, with traditional Excavata being probably paraphyletic. The root of the eukaryote tree remains elusive. Paleontological evidence and molecular clock analysis date the eukaryote lineage to at least 1.5 GYA, the concestor of extant eukaryotes to about 1.2 GYA, and major extant lineages to 900 MYA or less. The chapter includes a review of mitochondrial properties and of locomotor organelles in bacteria, archaea and eukaryotes.
The eukaryote pangenome has a chimeric structure encompassing genes unique to eukaryotes (~41%), ... more The eukaryote pangenome has a chimeric structure encompassing genes unique to eukaryotes (~41%), and genes of bacterial (~50% of total) and archaeal ancestry (~9%). Crucially, bacterial sequences far exceed the set acquired from the proteobacterial ancestor of mitochondria. Extant eukaryotic lineages share a common ancestor (LECA) that had all the fundamental traits of eukaryotes including the mitochondrion. The current debate about eukaryote origins revolves around two competing scenarios. The fusion model posits that the eukaryotes derive from the "fusion" of an archaeon and a bacterium, and that the acquisition of the mitochondrion was pivotal to the evolution of other eukaryotic traits. The neomuran model maintains that the archaea and eukaryotes are sister groups devived from a bacterial ancestor, and that fundamental eukaryotic traits including phagocytosis were already in place before the evolution of the mitochondrion by endosymbiosis. Eukaryote placement within the archaea in phylogenomic analysis supports the fusion scenario. The predominance of bacterial sequences in the eukaryote pangenome, the bacterial stereochemistry of eukaryote membrane lipids, and similar trajectories in mitochondrial and chloroplast evolution favour the neomuran scenario. Phylogenomic analysis resolves two major eukaryotic domains, the Amorphea and Diaphoretika, with traditional Excavata being probably paraphyletic. The root of the eukaryote tree remains elusive. Paleontological evidence and molecular clock analysis date the eukaryote lineage to at least 1.5 GYA, the concestor of extant eukaryotes to about 1.2 GYA, and major extant lineages to 900 MYA or less. The chapter includes a review of mitochondrial properties and of locomotor organelles in bacteria, archaea and eukaryotes.
The Birth of Life
Biological Innovations that Built the World, 2019
Life was most likely present on Earth as early as 3.5 GYA and probably made its first appearance ... more Life was most likely present on Earth as early as 3.5 GYA and probably made its first appearance around 4 GYA. Alkaline hydrothermal vents discovered in 2000 are presently considered a likely setting for the origin of life because they could provide organic matter, chemical disequilibria and compartmentation. Simulation experiments show that the synthesis of simple organic molecules from CO2 and H2 and of peptides from free amino acids is thermodynamically favoured under hydrothermal vent conditions. Abiotic synthesis of nucleotides and RNA is more problematic due to intrinsic instability of RNA and ribose under alkaline conditions. Association with abiotic peptides might have stabilized abiotic RNA, leading to the emergence of self-replicating ribonucleoprotein complexes (RNPs). It is suggested that a crucial step towards life was the appearance of “protoribosomes”, viz. RNPs capable of making peptides with a sequence determined by cognate RNAs under the rules of a primordial genet...
The Emergence of Humanity
Adaptation to the savanna and transition to bipedality probably triggered the divergence of the h... more Adaptation to the savanna and transition to bipedality probably triggered the divergence of the hominins from other apes in Central-Eastern or Southern Africa between 5 and 7 MYA. The human lineage (here identified with the genus Homo) appeared between 3 and 2 MYA, its earliest distinctive traits being increased brain size, the loss of fur, improved thermoregulation, and arm/torso anatomy adapted to high-energy throwing. Coercive suppression of conflict of interest probably favoured kinship-independent aggregation into cooperative groups. Cooperative hunting and social rearing improved the diet, thus providing the extra resources necessary for the development of larger and metabolically more active brains under selection pressure for higher cognition. In a complex network of mutual interactions, kinship-independent cooperation paved the way to the evolution of language and the emergence of culture, a body of shared knowledge and beliefs transmitted across generations. Culture accumu...
The placenta of hornworts is unique among bryophytes in the restriction of transfer cells that ar... more The placenta of hornworts is unique among bryophytes in the restriction of transfer cells that are characterized by elaborate wall labyrinths to the gametophyte generation. During development, cells around the periphery of the sporophyte foot elongate, forming smooth-walled haustorial cells that interdigitate with gametophyte cells. Using immunogold labeling with 22 antibodies to diverse cell wall polymers, we examined compositional differences in the developmentally and morphologically distinct cell walls of gametophyte transfer cells and sporophyte haustorial cells in the placenta of Phaeoceros. As detected by Calcofluor White fluorescence, cellulose forms the cell wall scaffolding in cells on both sides of the placenta. Homogalacturonan (HG) and rhamnogalacturonan I (RG-I) pectins are abundant in both cell types, and haustrorial cells are further enriched in methyl-esterified HGs. The abundance of pectins in placental cell walls is consistent with the postulated roles of these po...
The Chloroplast and Photosynthetic Eukaryotes
Biological Innovations that Built the World
The chloroplast primarily evolved in the unicellular ancestor of Archaeplastida (Plants) from a c... more The chloroplast primarily evolved in the unicellular ancestor of Archaeplastida (Plants) from a cyanobacterial endosymbiont around 900 MYA. A secondary chloroplast independently evolved in the Chlorarachniophytes (Rhizaria) and Euglenophytes (Excavata) from two different green algal endosymbionts, and in the “chromoalveolate” lineage from a red algal endosymbiont. It is debated whether the chromoalveolate chloroplast was transmitted vertically across the Cryptophytes, Haptophytes, Chromista and Alveolata as the chromoalveolate hypothesis maintains, or by serial symbiosis. Chloroplast evolution involved massive gene transfer from the cyanobacterial endosymbiont to the host nucleus; a minor part of the original genome remained in the chloroplast and was never completely lost. Protein translocation from the host cytosol to different sites of the chloroplast depends on multiple translocation mechanisms derived in part from the host, in part of cyanobacterial ancestry. The evolution of secondary chloroplasts involved the transfer of genes for chloroplast maintenance from the nucleus of the primary host to that of the secondary host; mechanisms derived from the secondary-host endomembrane system mediate protein translocation across extra envelope membranes of secondary chloroplasts. Chloroplast division involves a divisome complex in part of cyanobacterial origin, in part eukaryotic. Photosynthetic eukaryotes replaced ancestral glycogen with starch, accumulated either in the host cytosol or in chloroplast stroma, or with β-glucans in cytoplasmic vesicles. Multiple chloroplast transfer is a common occurrence in eukaryotes. A novel primary chloroplast independently evolved in the cercozoan amoeba Paulinella chromatophora. By transferring photosynthesis from the prokaryotic to eukaryotic world, chloroplast evolution dramatically increased global productivity, thus probably being a major driver of the Late-Proterozoic transition from a low- to high-oxygen planet.
Annals of Botany, 2003
Placental morphology is remarkably diverse between major bryophyte groups, especially with regard... more Placental morphology is remarkably diverse between major bryophyte groups, especially with regard to the presence and distribution of transfer cells in the sporophyte and gametophyte. In contrast, with the exception of metzgerialean liverworts, placental morphology is highly conserved within major bryophyte groups. Here we examine the ultrastructure of the placenta in Monoclea forsteri and Treubia lacunosa, basal members of the marchantialean and metzgerialean liverwort lineages, respectively. In both species several layers of transfer cells are found on both sides of the placenta, with sporophytic transfer cells exhibiting prominent wall labyrinths. Consistent with previous reports of a similar placenta in other putatively basal and isolated liverwort genera such as Fossombronia, Haplomitrium, Blasia and Sphaerocarpos, this ®nding suggests that this type of placenta represents the plesiomorphic (primitive) condition in liverworts. Distinctive ultrastructural features of placental cells in Monoclea include branched plasmodesmata in the sporophyte and prominent arrays of smooth endoplasmic reticulum, seemingly active in secretion in the gametophyte. These arrays contain a core of narrow tubules interconnected by electron-opaque rods, structures with no precedent in plants. Analysis of the distribution of different types of placenta in major bryophyte groups provides valuable insights into their interrelationships and possible phylogeny.
Bulletin of Regional Natural History, 2021
DNA is intrinsically unstable due to spontaneous mutation and degradation. Yet, life has thrived ... more DNA is intrinsically unstable due to spontaneous mutation and degradation. Yet, life has thrived for about four billion years, adapting to most diverse environmental conditions. The ultimate reason for the striking resilience and versatility of life is
Life probably appeared on Earth around 4 billion years ago and was globally diffused within the n... more Life probably appeared on Earth around 4 billion years ago and was globally diffused within the next 500 million years. It is debated whether life emerged in a superficial terrestrial environment, as generally maintained by "primordial-soup" models, or in association with submarine hydrothermal vents. Simulation experiments show that abiotic formation of simple organic molecules from CO 2 and H 2 , and of peptides from free amino acids is thermodynamically favoured under hydrothermal-vent conditions. In contrast, proposed pathways of abiotic synthesis of nucleotides and RNA fit better with superficial scenarios subject to wet/dry cycles. The "RNA World" hypothesis posits that a critical step towards life was the appearance of RNA enzymes (ribozymes) that catalysed RNA replication and random α-amino acid polymerization. The narrative presented here suggests that ribozyme interaction with peptides underpinned the emergence of populations of "protoribosomes" and virus-like RNA "protochromosomes" depending on each other for replication and subject to Darwinian evolution. The establishment of a genetic code coupled RNA and peptide evolution. RNA chaperoning of peptides positively selected self-folding peptide sequences, thus paving the way to the evolution of biologically active protein architectures. Association of informationally interlinked protoribosomes and protochromosomes with liquid-crystal bilayers produced the first protocells, self-replicating structures that evolved an increasingly complex metabolism by replacing ancestral ribozymes with more efficient protein enzymes. The addition of the Sec translocon machinery and of integral lipid-synthesizing enzymes converted self-assembled protomembranes into hereditary encoded membranes. The transition to DNA as the repository of genetic information established the genotype-ribotype-phenotype BORNH Review Article 12
International symposium on hunting "Modern aspects of sustainable management of game population" ... more International symposium on hunting "Modern aspects of sustainable management of game population" Publisher
Annals of Botany, 1986
Mucilage-secreting hairs of the moss Timmiella barbuloides develop at the base of young leaves an... more Mucilage-secreting hairs of the moss Timmiella barbuloides develop at the base of young leaves and differentiate three to four basal cells which form a non-secretory stalk, and five to nine distal secretory cells. In both cell types the external walls are covered by a thin cuticle, and connecting walls are traversed by numerous plasmodesmata. Young secretory cells develop extensive stacks of rough endoplasmic reticulum and numerous dictyosomes. Mucilage secretion is granulocrine and involves two morphologically and cytochemically distinct vesicle types: smaller, dictyosome-derived vesicles which are positive to the periodic acid/thiocarbohydrazide/silver proteinate (PATAg) test for carbohydrates; and larger, PATAg-negative vesicles of uncertain origin. Coated vesicles arising from dictyosomes are also present but they do not seem to participate in secretion. In the first phase of activity, the smaller vesicles discharge their contents by exocytosis and the secretion accumulates beneath the cuticle which becomes separated from the cell walls. Later, the massive discharge of the larger vesicles is followed by the bursting of the cuticle and the release of mucilage from the cells. Concomitant to this, extensive invaginations of the plasmalemma are formed along the external walls. The mucilage is rich in carbohydrates but no appreciable amounts of protein were detected. /?-Glycerophosphatase activity is found to be associated with dictyosomes and endoplasmic reticulum in actively secreting cells. Neither plastids nor endoplasmic reticulum appear to participate in secretion directly. Following the release of mucilage, the hair cells degenerate.
Novel features of the plastids in some deep-shade, antipodean thalloid liverworts
Cryptogamie Bryologie, 2006
Résumé/Abstract The chloroplasts in the inner thallus cells of Monoclea forsteri and Verdoornia s... more Résumé/Abstract The chloroplasts in the inner thallus cells of Monoclea forsteri and Verdoornia succulenta contain giant grana often with over 100 thylakoids, a feature shared with another deep-shade liverwort Dumortiera hirsuta and withnumerous extreme-shade ...
Can J Bot, 1994
Monoplastidic meiosis is reported for the first time in three seemingly unrelated liverworts, nam... more Monoplastidic meiosis is reported for the first time in three seemingly unrelated liverworts, namely Blasia pusilla (Metzgeriales), Monoclea gottschei (Monocleales), and Haplornitrium blumei (Haplomitriales). A second species of Haplornitriurn, H. hookeri, is polyplastidic as previously reported. All three taxa represent isolated relicts of ancient liverwort lineages. Monoplastidy in these hepatics is evident in archesporial tissue and is maintained through successive sporogenous cell generations. In archesporial mitosis, the single plastid divides and the two resultant plastids are precisely positioned so that one is inherited by each daughter cell. In the nascent spore mother cell, the solitary plastid undergoes two successive divisions and the resulting four plastids become positioned in a tetrahedral arrangement. Concomitantly, the sporocyte assumes a quadrilobed shape, which is less exaggerated in Monoclea, and a single large plastid is situated in each lobe. Details of plastid ultrastructure and morphology vary slightly among the three taxa. Evidence is presented that Blasia and Monoclea share a common ancestry and represent pivotal taxa in the evolution of the two main lines of liverworts. Haplomitrium is suggested to occupy a more basal position in bryophyte phylogeny. Monoplastidy in meiosis of liverworts links the charophytes, the three bryophyte clades, and the lycopsid pteridophytes and supports a monophyletic interpretation of land plant phylogeny.
A light and electron microscope study of the fungal endophytes in the sporophyte and gametophyte of Lycopodium cernuum with observations on the gametophyte-sporophyte junction
Can J Bot, 1992
The ventral epidermal cells of the photosynthetic, surface-living gametophytes of Lycopodium cern... more The ventral epidermal cells of the photosynthetic, surface-living gametophytes of Lycopodium cernuum, collected from moist shaded banks in Peninsular Malaysia, contain an aseptate fungus. In some cells the hyphae are thick walled and form coils encapsulated by a thin layer of host wall material. In others the fungus is thin walled and shows limited differentiation into larger trunk hyphae and arbuscules. The adjacent host cytoplasm, separated from the fungus by a granular interfacial matrix, contains numerous chloroplasts, mitochondria, and microtubules. The hyphae contact the substratum via the ventral walls of the epidermal cells and the rhizoids are free from infection. In the protocorm and root nodules, aseptate hyphae initially colonize mucilage-filled schizogenous intercellular spaces. Subsequent invasion of the host cells is associated with the development of massive overgrowths of host wall material. The fungal associations in L. cernuum share a mixture of attributes otherwise found in different angiosperm mycorrhizae and in mycotrophic relationships in liverworts. Wall ingrowths are present in both the gametophyte and sporophyte cells in the placenta of L. cernuum. The very limited development of the placenta, compared with L. appressum, certain bryophytes and ferns, the diminutive size, and early senescence of the gametophytes of L. cernuum are all linked to the presence of the protocorm. This massive absorptive organ, homologous to a foot, in terms of its position in sporophyte ontogeny, but external to the parent gametophyte, derives its nutrition partly from photosynthesis and partly from its fungal endophyte. Key words: chloroplasts, Lycopodium, mycorrhiza, pteridophytes, root nodules, symbiosis, transfer cells.
Gametophyte and sporophyte ultrastructure in Buxbaumia piperi Best(Buxbaumiales,Musci)
Journal of the Hattori Botanical Laboratory, May 1, 1982
A comparative cytological analysis of fungal endophytes in the sporophyte rhizomes and vascularized gametophytes of Tmesipteris and Psilotum
Can J Bot, 2005
This article describes the results of a light and electron microscopic study of the fungal endoph... more This article describes the results of a light and electron microscopic study of the fungal endophytes and vascular anatomy in the rhizomes and gametophytes of Tmesipteris and Psilotum. The parenchymatous cortical cells of the rhizomes and subterranean gametophytes of Tmesipteris and Psilotum contain intracellular aseptate glomeromycotean fungi resembling the “Paris-type” of arbuscular mycorrhizas found in seed plants. The fungi differentiate into multinucleate vesicles and hyphal coils, both containing bacteria-like structures and accumulating lipid masses and crystals as they age. After several cycles of infection in the same cell, degenerate hyphae form amorphous masses encased by host wall material. Nearly identical host–fungus cytology between the autotrophic sporophytes and the heterotrophic gametophytes suggests that these psilophyte associations are exploitative of the fungus in both generations. Following the description of tracheids nearly 60 years ago in the gametophytes of Psilotum, vascular elements are described for the first time in the haploid generation of Tmesipteris. Close similarities between the water- and food-conducting elements in both generations, viz. vessel elements with scalariform perforation plates and sieve cells with refractive spherules and lacking callose at all stages in their develoment, add support to the homologous theory of the alternations of generations. Mitochondrial aggregations, cross-linked by small electron-opaque rods, are common in the stelar cells of both generations and appear to be a unique feature of the psilophyte clade.
Effects of the potential allelochemical a-asarone on growth, physiology and ultrastructure of two unicellular green algae
J Appl Phycol, 1993
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Papers by Roberto Ligrone