The Paradox of Clonality and the Evolution of Self-Incompatibility

In the January issue of New Phytologist Vallejo-Marín and O''Brien¹ documented that in the genus Solanum (Solanaceae) clonality and self-incompatibility, a common genetic mechanism enforcing cross-fertilization, co-occur more often than expected by chance. Using a phylogenetic approach the authors showed that the statistical association between clonality and self-incompatibility persists even after taking into account phylogenetic relationships among species, uncertainty in the phylogenetic reconstruction, and associations between clonality and life history (annual/perennial). Vallejo-Marín and O''Brien¹ suggest that clonality and self-incompatibility tend to co-occur because clonality, by allowing the persistence and propagation of a genotype in environments with limited pollinator or mate availability, reduces the selective pressure favoring the breakdown of self-incompatibility. In addition to promoting the maintenance of self-incompatibility, when clonality results in the spatial aggregation of genetically identical individuals, clonality may promote its breakdown by restricting pollen transfer between different genotypes. Here I call attention to these contradictory predictions of the effects of clonality on the evolution of self-incompatibility, and suggest that the outcome of this paradox depend on both the extent to which clonal propagation compensates for limited seed production, and on the extent to which clonality reduces pollen transfer between genotypes.Key Words: asexual reproduction, clonality, mating system, pollen limitation, reproductive assurance, reproductive compensation, SolanumFlowering plants display a variety of mechanisms preventing self-fertilization, among which self-incompatibility is one of the best studied.^2,3 In the genus Solanum (Solanaceae) ancestrally present self-incompatibility has broken down multiple independent times through out the evolutionary history of this group to give rise to self-compatible lineages.^4,5 The breakdown of outcrossing mechanisms, including self-incompatibility, is one of the most common and best studied evolutionary transitions in flowering plants.⁶Self-incompatibility is a genetic mechanism by which the maternal plant can recognize and reject pollen grains expressing alleles in common with the maternal genotype.⁷ The reproductive advantages of self-incompatibility can be understood as a balance between two forces. On one hand the rejection of pollen grains is a mechanism for the preferential support of outbred progeny which, generally, is of higher genetic quality. On the other hand, if pollen or pollinator availability is low, pollen grains that are rejected by the self-incompatibility mechanism may not be substituted, and thus some ovules would go unfertilized. The evolutionary maintenance of self-incompatibility depends on the relative benefit of producing higher quality offspring and the relative costs incurred by potential reduction in offspring number⁸Plant clonality can affect the relative benefits and costs of self-incompatibility through its effects on the persistence and spatial distribution of genotypes. For instance, Vallejo-Marín and O''Brien¹ suggest that clonality provides reproductive assurance in colonizing taxa by allowing genotypes to persist and propagate even in the absence of conditions conducive to seed production. The reproductive assurance conferred by clonality would then relief the evolutionary costs of self-incompatibility incurred through reduced seed number, favoring the maintenance of self-incompatibility (Fig. 1).^1,9,10 In contrast, clonality may increase the evolutionary costs of self-incompatibility, by restricting pollen transfer between genotypes.^11,12 In some forms of clonal growth, dispersal of asexual propagules is very localized, resulting in an aggregation or clumping of genotypes. If spatial clumping restricts pollen flow between distinct genetic individuals, plants may not receive enough compatible pollen to fertilize all ovules (incomplete reproductive compensation) thus resulting in reduced seed set, which may favor the breakdown of self-incompatibility (Fig. 1).^8,12,13 It is important to note that both the maintenance and the breakdown effects mentioned above are expected to occur in the same ecological conditions, namely when the availability of pollen, pollinators, or compatible mates limit seed set (collectively known as pollen limitation).Open in a separate windowFigure 1Potential consequences of clonality for the evolutionary maintenance of self-incompatibility (SI). Full reproductive compensation occurs when pollen grains rejected by the SI system can be replaced with other compatible pollen grains. Under full reproductive compensation, seed set is independent of the level of SI expression.⁸ When pollen receipt is limited, rejected pollen grains cannot be always substituted (incomplete reproductive compensation) and consequently seed set is negatively related to the level of SI expression.⁸ Notice that under similar ecological conditions, e.g., when pollen receipt is limited (outside arrows), clonality may both favor the maintenance of SI through reproductive assurance, and facilitate its breakdown through increasing within-genotype pollen transfer and reducing seed set.A contrasting ecological scenario, may in turn favor the maintenance of self-incompatibility in clonal taxa. When pollen is abundant, and pollinators transport pollen through larger distances, enough pollen might still be received to fertilize all ovules even after accounting for pollen rejected by the self-incompatibility system (full reproductive compensation; Fig. 1). In this case, seed number will not be affected by the expression of self-incompatibility, but seed quality may be increased through the rejection of inbred pollen.¹⁴ In other words, when pollen receipt does not limit seed number, the presence of clonality is expected to favor self-incompatibility as a mechanism to successfully screen inbred pollen originated from different individuals of the same genotype or clone.To summarize, under the same ecological conditions (i.e., pollen limitation) the co-occurrence of clonality and self-incompatibility may have contrasting effects (Fig. 1). On one hand clonality favors the maintenance of self-incompatibility by providing reproductive assurance. On the other hand clonality may favor the breakdown of self-incompatibility, because rejected pollen cannot be compensated for, ensuing in a reduction in seed number. The resolution of the paradox of clonality for the evolution of self-incompatibility is likely to depend on the degree to which clonal propagation compensates for limited reproduction through seeds (e.g., during population establishment), as well as on the extent to which clonality reduces pollen flow between established genotypes, which in turn is affected by characteristics such as clonal architecture, plant density, and pollinator type and availability.^12,15,16Vallejo-Marín and O''Brien''s data¹ suggest that in the colonizing genus Solanum, which is expected to experience pollen limiting conditions, clonality reduces the costs of self-incompatibility through reproductive assurance (maintenance effect) more than it increases the costs of self-incompatibility due to pollen flow within spatially clumped genotypes (breakdown effect). Future comparative studies of the association between self-incompatibility and clonality in other groups could help us determine the general conditions in which the maintenance effect outweighs the breakdown effect.     

Novel carbohydrate specificity of the 16-kDa galectin from Caenorhabditis elegans: binding to blood group precursor oligosaccharides (type 1, type 2, Talpha,and Tbeta) and gangliosides

Galectins, a family of soluble beta-galactosyl-binding lectins, are believed to mediate cell-cell and cell-extracellular matrix interactions during development, inflammation, apoptosis, and tumor metastasis. However, neither the detailed mechanisms of their function(s) nor the identities of their natural ligands have been unequivocally elucidated. Of the several galectins present in the nematode Caenorhabditis elegans, the 16-kDa "proto" type and the 32-kDa "tandem-repeat" type are the best characterized so far, but their carbohydrate specificities have not been examined in detail. Here, we report the carbohydrate-binding specificity of the recombinant C. elegans 16-kDa galectin and the structural analysis of its binding site by homology modeling. Our results indicate that unlike the galectins characterized so far, the C. elegans 16-kDa galectin interacts with most blood group precursor oligosaccharides (type 1, Galbeta1,3GlcNAc, and type 2, Galbeta1,4GlcNAc; Talpha, Galbeta1,3GalNAcalpha; Tbeta, Galbeta1,3GalNAcbeta) and gangliosides containing the Tbeta structure. Homology modeling of the C. elegans 16-kDa galectin CRD revealed that a shorter loop containing residues 66-69, which enables interactions of Glu(67) with both axial and equatorial -OH at C-3 of GlcNAc (in Galbeta1,4GlcNAc) or at C-4 of GalNAc (in Galbeta1,3GalNAc), provides the structural basis for this novel carbohydrate specificity.     

Microheterogeneity of bovine myelin basic protein studied by nuclear magnetic resonance spectroscopy

Myelin basic protein isolated from bovine white matter is known to consist of a mixture of three or more “charge isomers”, which can be separated by cation-exchange chromatography. We are using 360-MHz ¹H-nmr spectroscopy to establish the chemical and structural differences among them. Preliminary studies by difference spectroscopy between two of the isomers suggest (a) all aromatic residues, and probably their nearest-neighbors, are unchanged; (b) the less cationic isomer lacks one (or two) of its C-terminal Arg residues; and (c) a significant fraction of the two Met residues in the less cationic isomer is present as methionine sulfoxide.     

Signaling by FGF4 and FGF8 is required for axial elongation of the mouse embryo

Fibroblast growth factor (FGF) signaling has been shown to play critical roles in vertebrate segmentation and elongation of the embryonic axis. Neither the exact roles of FGF signaling, nor the identity of the FGF ligands involved in these processes, has been conclusively determined. Fgf8 is required for cell migration away from the primitive streak when gastrulation initiates, but previous studies have shown that drastically reducing the level of FGF8 later in gastrulation has no apparent effect on somitogenesis or elongation of the embryo. In this study, we demonstrate that loss of both Fgf8 and Fgf4 expression during late gastrulation resulted in a dramatic skeletal phenotype. Thoracic vertebrae and ribs had abnormal morphology, lumbar and sacral vertebrae were malformed or completely absent, and no tail vertebrae were present. The expression of Wnt3a in the tail and the amount of nascent mesoderm expressing Brachyury were both severely reduced. Expression of genes in the NOTCH signaling pathway involved in segmentation was significantly affected, and somite formation ceased after the production of about 15-20 somites. Defects seen in the mutants appear to result from a failure to produce sufficient paraxial mesoderm, rather than a failure of mesoderm precursors to migrate away from the primitive streak. Although the epiblast prematurely decreases in size, we did not detect evidence of a change in the proliferation rate of cells in the tail region or excessive apoptosis of epiblast or mesoderm cells. We propose that FGF4 and FGF8 are required to maintain a population of progenitor cells in the epiblast that generates mesoderm and contributes to the stem cell population that is incorporated in the tailbud and required for axial elongation of the mouse embryo after gastrulation.     

Risk factors and outcomes of candidemia caused by biofilm-forming isolates in a tertiary care hospital

Background

Very few data exist on risk factors for developing biofilm-forming Candida bloodstream infection (CBSI) or on variables associated with the outcome of patients treated for this infection.

Methods and Findings

We identified 207 patients with CBSI, from whom 84 biofilm-forming and 123 non biofilm-forming Candida isolates were recovered. A case-case-control study to identify risk factors and a cohort study to analyze outcomes were conducted. In addition, two sub-groups of case patients were analyzed after matching for age, sex, APACHE III score, and receipt of adequate antifungal therapy. Independent predictors of biofilm-forming CBSI were presence of central venous catheter (odds ratio [OR], 6.44; 95% confidence interval [95% CI], 3.21–12.92) or urinary catheter (OR, 2.40; 95% CI, 1.18–4.91), use of total parenteral nutrition (OR, 5.21; 95% CI, 2.59–10.48), and diabetes mellitus (OR, 4.47; 95% CI, 2.03–9.83). Hospital mortality, post-CBSI hospital length of stay (LOS) (calculated only among survivors), and costs of antifungal therapy were significantly greater among patients infected by biofilm-forming isolates than those infected by non-biofilm-forming isolates. Among biofilm-forming CBSI patients receiving adequate antifungal therapy, those treated with highly active anti-biofilm (HAAB) agents (e.g., caspofungin) had significantly shorter post-CBSI hospital LOS than those treated with non-HAAB antifungal agents (e.g., fluconazole); this difference was confirmed when this analysis was conducted only among survivors. After matching, all the outcomes were still favorable for patients with non-biofilm-forming CBSI. Furthermore, the biofilm-forming CBSI was significantly associated with a matched excess risk for hospital death of 1.77 compared to non-biofilm-forming CBSI.

Conclusions

Our data show that biofilm growth by Candida has an adverse impact on clinical and economic outcomes of CBSI. Of note, better outcomes were seen for those CBSI patients who received HAAB antifungal therapy.     

Habitat loss of a rainforest specialist pollinator fly as an indicator of conservation status of the South American Temperate Rainforests

We estimate habitat loss and fragmentation in a hoverfly, Aneriophora aureorufa, used as a representative forest specialist species. This species is a pollinator specialist of two native trees, forming a triad endemic to the South American Temperate Rainforest (SATR). We combine species distribution models with species-specific requirements to estimate the habitat range of A. aureorufa over two non-overlapping time periods (before human settlement to 2000, and from 2000 to 2014). We analyzed the predicted distribution range of A. aureorufa in Chile, quantifying habitat loss in both periods and fragmentation in the latter. In addition, we evaluated the representativeness of the Chilean protected areas system in relation to the current habitat of the species. We found that the total habitat of A. aureorufa decreased by 68.3% compared to historic pre-settlement levels; in the period 2000–2014 the loss was 4.9%. The northern zone was the most affected by habitat loss and fragmentation, with an estimated total loss of 89.9% from the historic period to 2014, with the loss of 238.2 km² per year between 2000 and 2014. Eighteen percent of the habitat of A. aureorufa occurs within protected areas. We found an overrepresentation in the southern zone (24.79%) and an underrepresentation in the northern zone (3.44%). We propose that forest specialist species of the northern zone of the SATR could be threatened due to the high pressure of habitat loss and the underrepresentation of the Chilean protected areas systems.     

Cytokine Profiles at Admission Can Be Related to Outcome in AIDS Patients with Cryptococcal Meningitis

Cryptococcal meningitis (CM) remains as common life-threatening AIDS-defining illness mainly in resource-limited settings. Previous reports suggested that baseline cytokine profiles can be associated to fungal burden and clinical outcome. This study aimed to evaluate the baseline cytokine profiles in AIDS patients with CM and its relation with the outcome at weeks 2 and 10. Thirty AIDS patients with CM diagnosed by cerebrospinal fluid (CSF) Cryptococcus neoformans positive culture, India ink stain and cryptococcal antigen test were prospectively evaluated. As controls, 56 HIV-infected patients without CM and 48 non-HIV individuals were included. Baseline CSF and sera levels of IL-2, IL-4, IL-8, IL-10, IL-12p40, IL-17A, INF-γ and TNF-α were measured by ELISA. Of 30 CM patients, 24 (80%) were male, median age of 38.1. The baseline CSF high fungal burden and positive blood culture were associated with a positive CSF culture at week 2 (p = 0.043 and 0.029). Most CSF and sera cytokines presented higher levels in CM patients than control subjects (p < 0.05). CSF levels of IL-8, IL-12p40, IL-17A, TNF-α, INF-γ and sera TNF-α were significantly higher among survivors at weeks 2 and 10 (p < 0.05). Patients with increased intracranial pression exhibited CSF IL-10 high levels and poor outcome at week 10 (p = 0.032). Otherwise, baseline CSF log10 IFN-γ and IL-17A were negatively correlated with fungal burden (r = -0.47 and -0.50; p = 0.0175 and 0.0094, respectively). The mortality rate was 33% (10/30) at week 2 and 57% (17/30) at week 10. The severity of CM and the advanced immunodeficiency at admission were related to a poor outcome in these patients. Otherwise, the predominant Th1 cytokines profile among survivors confirms its pivotal role to infection control and would be a prognostic marker in cryptococcal meningitis.