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• W1990307997 abstract "‘The Summerfield team selected an elegant, new approach for exploring the sites of heterocyst differentiation and the areas of highest levels of nitrogen fixation within the cyanobacterial cell population of young and mature thalline areas.’ Most lichen-forming fungi form morphologically and anatomically simple, crustose, leprose, microfilamentous or microglobose thalli in close contact with the substratum. Approx. 25% differentiate scaly (squamulose) or obscurely lobed (effigurate) thalli with internal stratification, and c. 25%, the so-called macrolichens, form three-dimensional, band- or leaf-shaped or shrubby thalli, either erect or pendulous, which rise above the substratum. Some macrolichens achieve impressive dimensions; examples are the epiphytic lungworts (Lobaria spp.), which produce large, foliose thalli several decimetre square in diameter, or the fishnet lichen (Ramalina menziesii) of the coastal Pacific Northwest, whose several-metre-long thalli hang like curtains from the trees. These fast growing species benefit from a climate which allows growth all year long and achieve their large size by combined apical-marginal and intercalary growth. Patchy intercalary growth is typically found in rock tripes (Umbilicaria and Lasallia spp.), whose foliose thalli are fixed to the substratum by a central umbilicus (for review see Honegger, 1993). However, the majority of macrolichens reveal apical-marginal growth, with a marginal pseudomeristem with high cell turnover rates, a subapical elongation zone where the cells of the fungal and cyanobacterial or algal partner achieve their final dimensions, and a nongrowing basal/central zone with limited cell turnover rates in both partners. Pseudomeristems of lichen-forming ascomycetes are functionally analogous to the apical meristems of plants but differ in their ontogeny and structure; they are formed by groups of co-ordinately growing hyphal tips which stay active for long periods of time (up to centuries; for review see Honegger, 2009). This growth pattern is commonly found in foliose and fruticose thalli of numerous green algal and cyanobacterial lichens (Fig. 1; Hill, 1989; Honegger, 1993, 2009). The growth pattern and growth rates of Pseudocyphellaria crocata were not analysed in detail, but the light micrographs provided by Summerfield and co-workers leave no doubts about their model lichen belonging to this last type of development. Approx. 10% of extant lichen-forming fungal species associate with cyanobacterial photobionts, c. 85% with green algal and an estimated 4% of species simultaneously with both a green algal and a cyanobacterial photobiont, the latter being housed in cephalodia, gall-like structures, either within the thallus (internal) or on its upper or lower surface (external cephalodia). The most common cyanobacterial photobionts of lichen-forming fungi are Nostoc species from the Nostoc II clade sensu O'Brien et al. (2005), N. punctiforme genotypes being the favourites of many lichen-forming ascomycetes, of the enigmatic glomeromycete Geosiphon pyriforme, but also of liverworts, hornworts, cycads and angiosperms (Gunnera spp.; Rai et al., 2000; O'Brien et al., 2005). Based on 16S rRNA gene and tRNALeu (UAA) intron sequence analyses, Tina Summerfield and co-workers had previously investigated the taxonomic affiliation of the Nostoc cyanobionts of Pseudocyphellaria crocata specimens from various collecting sites. While all thalli of P. crocata from New Zealand contained the same Nostoc genotype (Summerfield et al., 2002) a higher genetic diversity was detected among the samples from Australia, Chile and Canada (Summerfield & Eaton-Rye, 2006). High selectivity but moderate specificity is a feature observed in many lichen symbioses (for example, Paulsrud et al., 2000; Rikkinen et al., 2002; O'Brien et al., 2005). Irrespective of whether Nostoc species are the primary or the secondary partner of Peltigerales, the mycobiont–cyanobiont interface appears to be always the same: the mycobiont forms finger-like intragelatinous protrusions into the gelatinous sheaths of the Nostoc colonies but does not penetrate the cyanobacterial cell wall (Fig. 2; Honegger, 1991). As in green algal macrolichens, the photobiont cell population has access to water and dissolved mineral nutrients exclusively via the fungal apoplast. A mycobiont-derived, hydrophobic wall surface lining seals the apoplastic continuum of the fungal and cyanobacterial partners in thalli with Nostoc as primary photobiont; this canalizes fluxes of water and prevents solutes, originating from the photoautotrophic or the heterotrophic partner, from leaking out into the space between hyphae. It prevents the air-filled thalline interior from getting waterlogged, a pre-requisite to maintain gas exchange in the fully hydrated state (Fig. 2b; Honegger, 1991, 2009). It is virtually impossible to mechanically separate the entire cyanobacterial cell population from lichen thalli; therefore Summerfield and co-workers used thallus homogenates and designed cyanobacteria-specific primers for their analyses of changes in cyanobacterial gene expression within Pseudocyphellaria crocata thalli (a cultured isolate of N. punctiforme serving as reference material). In all studies on growth and differentiation processes within foliose, green algal or cyanobacterial macrolichens with apical-marginal growth, a similar pattern was observed: an increasing cell size in the mycobiont and photobiont from the young towards the older parts, coupled with increasing photosynthetic activity in subapical thalline areas (measured either as CO2 uptake, 14CO2 assimilation or chlorophyll fluorescence yields), but a decline in the oldest, senescent zones; conversely a decreasing cell turnover rate in both partners was observed, leading to a high percentage of oversized photobiont cells in subapical areas, that is, cells having exceeded the size for autospore formation or cell division, respectively, their cell cycle being arrested (Hill, 1985, 1989; Honegger, 1993; Rai et al., 2000). The phenomenon of increasing cell size with increasing age of the interaction was also found in Geosiphon pyriforme and in cyanobacterial symbioses with photoautotrophic land plants; there, a decline in photosynthetic activity and an increase in heterocyst differentiation and thus nitrogen fixation was documented (Rai et al., 2000). In cyanobacterial lichens of the order Peltigerales some authors reported on increasing heterocyst numbers and concluded on increasing rates of nitrogen fixation from the youngest to mature parts of the thallus, which might indicate continuous heterocyst differentiation throughout the thallus, while others found no major differences. An exception are tripartite lichens with distinctly higher heterocyst numbers in the large, mature, yellowish cephalodia in nongrowing, subapical thalline areas than in the small, dark grey cephalodia near the growing edge of the thallus (Englund, 1977). The Summerfield team selected an elegant, new approach for exploring the sites of heterocyst differentiation and the areas of highest levels of nitrogen fixation within the cyanobacterial cell population of young and mature thalline areas. By means of differential display and quantitative reverse transcription polymerase chain reaction (qRT-PCR) techniques, the expression of the putative cytochrome c oxidase (coxB2; elevated cytochrome oxidase activity generates microaerobic conditions in heterocysts as required by the nitrogenase enzyme), of genes involved in heterocyst differentiation (ntcA, hetR) and nitrogen fixation (nifK, encoding part of the nitrogenase enzyme) was analysed in thallus fragments derived from either < 5 mm from the thalline margin (i.e. from the youngest, growing areas and elongation zone) or from nongrowing central areas (> 1 cm apart from thallus margin), three thalli being selected. Additionally, the expression of psbB (encoding a chlorophyll α-binding protein of Photosystem II) and of several other genes was analysed. The photosynthetic activity was fluorimetrically measured. Confocal laser scanning microscopy of cyanobacterial (chlorophyll) and fungal autofluorescence in 30-μm cryotome sections gave less than optimal resolution, but allowed estimation of the dimensions of the upper and lower cortex, the medullary and photobiont layers and the mean diameters of Nostoc cells in young and mature thallus areas. As in other foliose, cyanobacterial and green algal macrolichens the cell sizes of both partners of the symbiosis, and the thickness of the photobiont and medullary layers, increased from the growing margin towards the centre of Pseudocyphellaria crocata thalli. The photosynthetic activity was slightly higher in older than in the younger parts. Interestingly, all genes involved in heterocyst differentiation and nitrogen fixation were upregulated in the marginal area; the nifK gene expression was up to 27-fold higher in the margin than in the thallus centre, but considerable differences were evident among the three samples studied. Indeed, the growing zone at the thallus margin, that is, the apical pseudomeristem and adjacent elongation zone, are the sites where lots of fixed nitrogen is required, among others for building up the hyphal walls of the mycobiont. Distinctly higher amounts of chitin were found in the cell walls of a representative of Peltigerales than in Lecanorales (Boissière, 1987; Honegger & Bartnicki-Garcia, 1991). This may be linked to the fact that Peltigerales are always associated with diazotrophic cyanobacteria, either as the primary or as the secondary photobiont. It would be very interesting to see the elegant experimental approach of the Summerfield team applied to other lichens with Nostoc as the primary photobiont in either an internally stratified or a gelatinous, nonstratified thallus (e.g. Collema and Leptogium spp., whose growth patterns have not yet been analysed) and in tripartite associations with Nostoc in external or internal cephalodia. Are there any seasonal differences in growth and thus gene expression? Moreover it would be interesting to see the sites of elevated transcript levels at a higher resolution, ideally with in situ hybridization techniques. This approach was successfully used for visualizing the differential expression of hydrophobin genes (XPH1 or DGH1, DGH2, DGH3, respectively) in the thalli of the lichen-forming ascomycete Xanthoria parietina (Scherrer et al., 2002) and in the lichenized basidiocarp of the tropical basidiomycete Dictyonema glabratum (syn. Cora pavonia; Trembley et al., 2002). The inspiring study of the Summerfield team on differential gene expression in ontogenetic stages of symbiotic Nostoc punctiforme greatly improves our understanding of the biology of the symbiosis in cyanobacterial lichens." @default.
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• W1990307997 date "2012-10-09" @default.
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• W1990307997 title "Differential gene expression within the cyanobacterial cell population of a lichen thallus" @default.
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