The phylogeny of Syntrichia: An ecologically diverse clade of mosses with an origin in South America.

PREMISE: To address the biodiversity crisis, we need to understand the evolution of all organisms and how they fill geographic and ecological space. Syntrichia is one of the most diverse and dominant genera of mosses, ranging from alpine habitats to desert biocrusts, yet its evolutionary history remains unclear. METHODS: We present a comprehensive phylogenetic analysis of Syntrichia, based on both molecular and morphological data, with most of the named species and closest outgroups represented. In addition, we provide ancestral-state reconstructions of water-related traits and a global biogeographic analysis. RESULTS: We found 10 major well-resolved subclades of Syntrichia that possess geographical or morphological coherence, in some cases representing previously accepted genera. We infer that the extant species diversity of Syntrichia likely originated in South America in the early Eocene (56.5-43.8 million years ago [Mya]), subsequently expanded its distribution to the neotropics, and finally dispersed to the northern hemisphere. There, the clade experienced a recent diversification (15-12 Mya) into a broad set of ecological niches (e.g., the S. caninervis and S. ruralis complexes). The transition from terricolous to either saxicolous or epiphytic habitats occurred more than once and was associated with changes in water-related traits. CONCLUSIONS: Our study provides a framework for understanding the evolutionary history of Syntrichia through the combination of morphological and molecular characters, revealing that migration events that shaped the current distribution of the clade have implications for morphological character evolution in relation to niche diversity.

To dry perchance to live: Insights from the genome of the desiccation-tolerant biocrust moss Syntrichia caninervis.

With global climate change, water scarcity threatens whole agro/ecosystems. The desert moss Syntrichia caninervis, an extremophile, offers novel insights into surviving desiccation and heat. The sequenced S. caninervis genome consists of 13 chromosomes containing 16 545 protein-coding genes and 2666 unplaced scaffolds. Syntenic relationships within the S. caninervis and Physcomitrella patens genomes indicate the S. caninervis genome has undergone a single whole genome duplication event (compared to two for P. patens) and evidence suggests chromosomal or segmental losses in the evolutionary history of S. caninervis. The genome contains a large sex chromosome composed primarily of repetitive sequences with a large number of Copia and Gypsy elements. Orthogroup analyses revealed an expansion of ELIP genes encoding proteins important in photoprotection. The transcriptomic response to desiccation identified four structural clusters of novel genes. The genomic resources established for this extremophile offer new perspectives for understanding the evolution of desiccation tolerance in plants.

Strategies of desiccation tolerance vary across life phases in the moss Syntrichia caninervis.

PREMISE: Desiccation tolerance (DT) is a widespread phenomenon among land plants, and variable ecological strategies for DT are likely to exist. Using Syntrichia caninervis, a dryland moss and model system used in DT studies, we hypothesized that DT is lowest in juvenile (protonemal) tissues, highest in asexual reproductive propagules (gemmae), and intermediate in adults (shoots). We tested the long-standing hypothesis of an inherent constitutive strategy of DT in this species. METHODS: Plants were rapidly dried to levels of equilibrating relative humidity (RHeq) ranging from 0 to 93%. Postrehydration recovery was assessed using chlorophyll fluorescence, regeneration rates, and visual tissue damage. For each life phase, we estimated the minimum rate of drying (RoDmin ) at RHeq = 42% that did not elicit damage 24 h postrehydration. RESULTS: DT strategy varied with life phase, with adult shoots having the lowest RoDmin (10-25 min), followed by gemmae (3-10 h) and protonema (14-20 h). Adult shoots exhibited no detectable damage 24 h postrehydration following a rapid-dry only at the highest RHeq used (93%), but when dried to lower RHs the response declined to <50% of control fluorescence values. Notably, immediately following rehydration (0 h postrehydration), shoots were damaged below control levels of fluorescence regardless of the RHeq, thus implicating damage. CONCLUSIONS: Life phases of the moss S. caninervis had a range of strategies from near constitutive (adult shoots) to demonstrably inducible (protonema). A new response variable for assessing degree of DT is introduced as the minimum rate of drying from which full recovery occurs.

Embryos of a moss can be hardened to desiccation tolerance: effects of rate of drying on the timeline of recovery and dehardening in Aloina ambigua (Pottiaceae).

BACKGROUND AND AIMS: Embryonic sporophytes of the moss Aloina ambigua are inducibly desiccation tolerant (DT). Hardening to DT describes a condition of temporary tolerance to a rapid-drying event conferred by a previous slow-drying event. This paper aimed to determine whether sporophytic embryos of a moss can be hardened to DT, to assess how the rate of desiccation influences the post-rehydration dynamics of recovery, hardening and dehardening, and to determine the minimum rate of drying for embryos and shoots. METHODS: Embryos were exposed to a range of drying rates using wetted filter paper in enclosed Petri dishes, monitoring relative humidity (RH) inside the dish and equilibrating tissues with 50% RH. Rehydrated embryos and shoots were subjected to a rapid-drying event at intervals, allowing assessments of recovery, hardening and dehardening times. KEY RESULTS: The minimum rate of slow drying for embryonic survival was ∼3·5 h and for shoots ∼9 h. Hardening to DT was dependent upon the prior rate of drying. When the rate of drying was extended to 22 h, embryonic hardening was strong (>50% survival) with survival directly proportional to the post-rehydration interval preceding rapid drying. The recovery time (repair/reassembly) was so short as to be undetectable in embryos and shoots desiccated gradually; however, embryos dried in <3·5 h exhibited a lag time in development of ∼4 d, consistent with recovery. Dehardening resulted in embryos incapable of surviving a rapid-drying event. CONCLUSIONS: The ability of moss embryos to harden to DT and the influence of prior rate of drying on the dynamics of hardening are shown for the first time. The minimum rate of drying is introduced as a new metric for assessing ecological DT, defined as the minimum duration at sub-turgor during a drying event in which upon rehydration the plant organ of interest survives relatively undamaged from the desiccating event.

Developing sporophytes transition from an inducible to a constitutive ecological strategy of desiccation tolerance in the moss Aloina ambigua: effects of desiccation on fitness.

BACKGROUND AND AIMS: Two ecological strategies of desiccation tolerance exist in plants, constitutive and inducible. Because of difficulties in culturing sporophytes, very little is known about desiccation tolerance in this generation and how desiccation affects sexual fitness. METHODS: Cultured sporophytes and vegetative shoots from a single genotype of the moss Aloina ambigua raised in the laboratory were tested for their strategy of desiccation tolerance by desiccating the shoot-sporophyte complex and vegetative shoots at different intensities, and comparing outcomes with those of undried shoot-sporophyte complexes and vegetative shoots. By using a dehardened clonal line, the effects of field, age and genetic variance among plants were removed. KEY RESULTS: The gametophyte and embryonic sporophyte were found to employ a predominantly inducible strategy of desiccation tolerance, while the post-embryonic sporophyte was found to employ a moderately constitutive strategy of desiccation tolerance. Further, desiccation reduced sporophyte fitness, as measured by sporophyte mass, seta length and capsule size. However, the effects of desiccation on sporophyte fitness were reduced if the stress occurred during embryonic development as opposed to postembryonic desiccation. CONCLUSIONS: The effects of desiccation on dehardened sporophytes of a bryophyte are shown for the first time. The transition from one desiccation tolerance strategy to the other in a single structure or generation is shown for only the second time in plants and for the first time in bryophytes. Finding degrees of inducible strategies of desiccation tolerance in different life phases prompts the formulation of a continuum hypothesis of ecological desiccation tolerance in mosses, where desiccation tolerance is not an either/or phenomenon, but varies in degree along a gradient of ecological inducibility.

The desert moss Pterygoneurum lamellatum (Pottiaceae) exhibits an inducible ecological strategy of desiccation tolerance: effects of rate of drying on shoot damage and regeneration.

PREMISE OF THE STUDY: Bryophytes include clades that incorporate constitutive desiccation tolerance, especially terrestrial species. Here we test the hypothesis that the opposing ecological strategy of desiccation tolerance, inducibility, is present in a desert moss, and address this hypothesis by varying rates of drying in a laboratory study. Desiccation tolerance is arguably the most important evolutionary innovation relevant to the colonization of land by plants; increased understanding of the ecological drivers of this trait will eventually illuminate the responsible mechanisms and ultimately open doors to the potential for the application of this trait in cultivated plants. METHODS: Plants were cloned, grown in continuous culture (dehardened) for several months, and subjected to rates of drying (drying times) ranging from 30 min to 53 h, rehydrated and tested for recovery using chlorophyll fluorescence, leaf damage, and regeneration of protonema and shoots. KEY RESULTS: Rate of drying significantly affected all recovery responses, with very rapid drying rates severely damaging the entire shoot except the shoot apex and resulting in slower growth rates, fewer regenerative shoots produced, and a compromised photosynthetic system as inferred from fluorescence parameters. CONCLUSIONS: For the first time, a desert moss is shown to exhibit an ecological strategy of desiccation tolerance that is inducible, challenging the assumption that arid-land bryophytes rely exclusively on constitutive protection. Results indicate that previous considerations defining a slow-dry event in bryophytes need reevaluation, and that the ecological strategy of inducible desiccation tolerance is probably more common than currently understood among terrestrial bryophytes.

Need for split: integrative taxonomy reveals unnoticed diversity in the subaquatic species of Pseudohygrohypnum (Pylaisiaceae, Bryophyta).

We present an integrative molecular and morphological study of subaquatic representatives of the genus Pseudohygrohypnum (Pylaisiaceae, Bryophyta), supplemented by distribution modelling of the revealed phylogenetic lineages. Phylogenetic analyses of nuclear and plastid datasets combined with the assemble species by automatic partitioning (ASAP) algorithm revealed eight distinct species within the traditionally circumscribed P. eugyrium and P. subeugyrium. These species are therefore yet another example of seemingly widely distributed taxa that harbour molecularly well-differentiated lineages with narrower distribution ranges. Studied accessions that were previously assigned to P. eugyrium form three clearly allopatric lineages, associated with temperate regions of Europe, eastern North America and eastern Asia. Remarkably, accessions falling under the current morphological concept of P. subeugyrium were shown to be even more diverse, containing five phylogenetic lineages. Three of these lineages occur under harsh Asian continental climates from cool-temperate to Arctic regions, while the remaining two, referred to P. subeugyrium s.str. and P. purpurascens, have more oceanic North Atlantic and East Asian distributions. Niche identity and similarity tests suggested no similarity in the distributions of the phylogenetically related lineages but revealed the identity of two East Asian species and the similarity of two pairs of unrelated species. A morphological survey confirmed the distinctness of all eight phylogenetic lineages, requiring the description of five new species. Pseudohygrohypnum appalachianum and P. orientale are described for North American and East Asian plants of P. eugyrium s.l., while P. sibiricum, P. subarcticum and P. neglectum are described for the three continental, predominantly Asian lineages of P. subeugyrium s.l. Our results highlight the importance of nontropical Asia as a center of bryophyte diversity. Phylogenic dating suggests that the diversification of subaquatic Pseudohygrohypnum lineages appeared in late Miocene, while mesophilous species of the genus split before Miocene cooling, in climatic conditions close to those where the ancestor of Pseudohygrohypnum appeared. We speculate that radiation of the P. subeugyrium complex in temperate Asia might have been driven by progressive cooling, aridification, and increases in seasonality, temperature and humidity gradients. Our results parallel those of several integrative taxonomic studies of North Asian mosses, which have resulted in a number of newly revealed species. These include various endemics from continental areas of Asia suggesting that the so-called Rapoport's rule of low diversity and wide distribution range in subpolar regions might not be applicable to bryophytes. Rather, the strong climatic oscillations in these regions may have served as a driving force of speciation and niche divergence.

An experimental demonstration of the cost of sex and a potential resource limitation on reproduction in the moss Pterygoneurum (Pottiaceae).

The cost of sexual reproduction is incurred when the current reproductive episode contributes to a a decline in future plant performance. To test the hypotheses that a trade-off exists between current sexual reproduction and subsequent clonal regeneration and that resources limit reproduction and regeneration, plants of the widespread moss Pterygoneurum ovatum were subjected to induced sporophytic abortion, upper leaf removal, and nutrient amendment treatments. Sexually reproducing plants were slower or less likely to produce regenerative structures (protonemata or shoots) and produced fewer regenerative tissue areas or structures. The ability and the timeline to reproduce sexually and regenerate clonally were unaffected by an inorganic nutrient amendment. However, when leaves subtending the sporophyte were removed, the sporophytes were less likely to mature, tended to take a longer time to mature, and were smaller compared to sporophytes from shoots with a full complement of upper leaves. Our findings indicate that plants investing in sexual reproduction suffer a cost of decreased clonal regeneration and indicate that sporophyte maturation is resource-limited, with upper leaves contributing to the nutrition of the sporophyte. This study represents only the second explicit experimental demonstration of a trade-off between sexual and asexual reproduction in bryophytes.