Towards an integrated understanding of charophyte biology and paleobiology

Abstract

In this special issue, we present an overview of the presentations given at the 7th Meeting of the International Research Group on charophytes held in Astana in 2016. Charophytes, understood as the members of extant Charales and their direct ancestors (fossil orders Sycidiales and Moellerinales), represent a significant plant group that provides an iconic research system for many diverse fields, such as evolution, ecology, electrophysiology, phytoremediation and management of wetlands. Charophytes have been proposed as one of the closest ancestors of land plants. Their fossil record goes back to 425 Ma (million years ago), but the rise of the oldest living charophyte genera is dated from ca 155–125 Ma. An example of vegetations already dominated by early Characeae has been recently found in China, dating back to that time. The definition of charophyte species has been a matter of debate, since the morphology of these plants shows a great plasticity. The elucidation of charophyte taxonomy is of major importance for the definition of endangered species. New light is shed by the use of genetic coding for the distinction of problematic species within the Chara genus. Climate change is one of the major concerns in the present scenario of disturbance of charophyte habitats. Specific adaptations, including changes in thallus morphology, parthenogenesis and enhanced production of oospores, develop when charophyte habitats become unstable, desiccate or increase their salinity. Brackish charophytes are also a subject of special attention, since they include species highly specialized in particular niches and highly vulnerable to extreme salinities reached through habitat desiccation. The chemistry of water controls the distribution of species, even at the biogeographic scale. Experiments, related to the transport of ions across the charophyte cell membrane, provide an understanding of how charophytes adapt physiologically to those changes.

Keywords:

• Charophytes
• molecular genetics
• physiology
• ecology
• paleobotany

Introduction

The main aim of the International Research Group on Charophytes (IRGC), founded in 1989 in Montpellier, France, is to enhance the collaboration between charophyte specialists, scattered all around the World. With this objective, regular meetings are organized both at the continental scale and at the inter-continental scale. The seventh such inter-continental meeting was organized by Aizhan Zhamangara, Raikhan Beisenova, Sherim Tulegenov, Leyla Akbayeva and Saida Nigmatova in Astana and Almaty (Kazakhstan) in 2016, and the main results of the meeting, as well as new results, are presented here. Like other meetings of the IRGC, this meeting comprised a number of oral and poster presentations as well as workshops, exploring both the field and the laboratory practices, which allowed delegates to share their experiences and to plan future collaborations. These meetings led the associates to reach an integrated view on almost all aspects of charophyte research. This approach is well reflected in the multidisciplinary scope of almost all the articles presented in this volume, making it very difficult to separate them by sub-disciplines. In this editorial for the Special Issue “Advances in Charophyte Research”, we provide an overview of the state of the art of the main “hot topics” in charophyte research, their interconnection and focus.

An integrated approach in charophyte research

Charophytes are understood by most of the authors of this volume as the monophyletic group composed of extant Charales and their direct fossil ancestors (Orders Sycidiales and Moellerinales), thus avoiding the misuse of the taxon Charophyta in a paraphyletic sense, to indicate the ancestors of embryophytes (www.algaebase.org). The charophytes, as understood here, represent just one of the key groups in the research of the origin of land plants. This issue has been a matter of debate in previous years (Timme, Bachvaroff, and Delwiche 2012 and references herein). The elucidation of the Chara braunii genome (Nishiyama et al. submitted) will help to resolve an important question, i.e. which of the streptophyte branches, the charophytes, the coleochatophytes or the zygnematophytes, are closest to the origin of land plants.

The evolution of charophytes is fairly well known from the fossil record, thanks to the biocalcification of the fructifications, called gyrogonites and utricles, in the last 425 million years (Feist et al. 2005). The paleobotany research presents a view of the time when charophytes were much more diverse than in the present and provides an understanding of how they reached the present status of pioneer plants, competing successfully with other aquatic plants, such as the angiosperms. One of the main purposes of palaeobotany research, as applied to charophytes, is the dating of the main events in charophyte evolution (e.g. Riveline et al. 1996). Martín-Closas et al. (forthcoming) document the occurrence of Tolypella (section Tolypella) in a lacustrine bed of the Garraf Massif (Catalonia, Spain), dated in the Lower Cretaceous, ca 125.0 Ma. This find confirms that Tolypella is one of the most ancient characean genera and provides an age for the main nodes of the molecular phylogeny of the living Characeae, as presented recently by Perez et al. (2014). The splitting of Nitellae and the Chareae is dated to 163.5–157.3 Ma, and the extant Chara, Lamprothamnium, Nitellopsis and Lychnothamnus groups formed in the second radiation of the Characeae during the Upper Cretaceous (83.6–72.1 Ma). This hypothesis could be tested in the future with the help of molecular clocks.

The study of molecular genetics has been shown in the last decades to be very useful, not only for characterizing the phylogeny of extant charophytes (e.g. Karol et al. 2001; McCourt et al. 1996, 2000; Perez et al. 2014) but also, more recently, to establish the identity of problematic species. The characterization of species, based on morphological characteristics, has been a conflictive issue since the very beginning of the charophyte taxonomy. The polymorphism of charophyte thalli is, indeed, greatly influenced by the environment and produces different plant morphologies of similar species, or even the same species in different environments. For this purpose, the genetic confirmations of the species identity were used, such as the plastid rbcL or the matK gene in Chara (e.g. Nowak, Schubert et al. forthcoming; Saber et al. forthcoming).

Focusing on the differences and the similarities within the Chara genus, it has previously been shown that water movement can affect Chara morphology (Bociąg et al. 2013). In a similar approach, Nowak, Schubert et al. (forthcoming) studied the effect of light on Chara morphology and tested a hypothesis that C. liljebladii is a low-light phenotype of C. baltica. A decrease in irradiance significantly increased the growth of the cells of C. baltica, changing their morphology in the direction of the C. liljebladii morphotype. However, the increased irradiance did not change the morphology of C. liljebladii. As another example of the variable morphology and the life cycle, Saber et al. (forthcoming) found Chara vulgaris in a thermal spring in the Egyptian desert. The thalli were more delicate than the usual C. vulgaris, and the antheridia were shed early in the reproductive cycle, while oogonia persisted. Despite these differences from “normal” C. vulgaris, genetic analysis clearly confirmed the species identity as C. vulgaris. The morphological characteristics may be adaptations to the highly isolated and selective desert freshwater habitat.

The understanding of the characean growth and development is of topical importance. This research direction has gained importance in recent years, since charophytes are coming under increasing pressure from anthropogenic pollution, climate change and competing algae and macrophytes. The global climate change and the tendency towards increasing aridity in some parts of the world, such as in the central and southern Europe, is one such major concern for the conservation of wetlands, rich in charophytes. Calero and Rodrigo (forthcoming) studied the unique ability of Chara canescens to reproduce parthenogenetically in water-stressed environments. The C. canescens population was monitored in Albufera de València Natural Park (Spain) for a year. In early March, new shoots developed from the germinating oospores, and the first oogonia appeared already in April. Parthenogenetic reproduction lasted for 5 months. The population had a short life cycle from March to September, with only a few small shoots overwintering.

In lake Bois d’Avaz, in the French pre-Alps, Boissezon, Auderset Joye, and Garcia (forthcoming) followed the population structure of Nitellopsis obtusa from 2009 to 2014. The abundance of the species decreased with dropping water level, climatically determined. The fertility of N. obtusa is thought to arise in response to disturbances in external conditions, such as important changes in the water table or even desiccation, producing long-lived and drought-resistant oospores and gyrogonites. Alternatively, fertile and sterile populations may belong to different ecotypes.

Knowledge about species, considered endangered in each country, will result in better conservation strategies. Hence, Auderset Joye, and Boissezon (forthcoming) followed the ecology and life cycles of Nitella opaca and N. gracilis, in a Swiss wetland over several years. Both species are at risk of extinction in Switzerland. N. opaca plants appeared in March, reproduced sexually and disappeared in July, while N. gracilis was perennial, reproducing throughout the year. The relationship of the phenophases for both species to water levels, temperatures, accumulated heat energy (growing degree days) and light (day-length) was investigated.

Herkül, Torn, and Mölle (forthcoming) studied the niche overlap, or separation, for aquatic angiosperms and charophytes in the Northern Baltic Sea in the environments ranging from brackish to freshwater, the former being also very sensitive to environmental change. Some Characeae species had highly specialized ecological niches, while others were more tolerant to their environment. Focusing on another type of brackish environment, Soulié-Märsche, Baumhauer, and Schütt (forthcoming) studied Lamprothamnium papulosum and Chara galioides gyrogonites from surface sediment and cores from the inland salt lake Laguna de Gallocanta (Spain). The gyrogonites of L. papulosum show great differences from those growing in the coastal sites, probably due to the hydro-chemical conditions of the Laguna de Gallocanta, with a high sulfate content in the past decades to centuries. The Characeae were last observed growing in the lake in 1990s, but since disappeared due to periods of lake bed exposure and extreme salinity.

Indeed, Chara physiology is affected strongly by changes in water salinity, and the giant characean cells provide a very useful system for electrophysiology. Beilby, Shepherd and Absolonova (forthcoming) review H⁺/OH^– channels, which participate in the pH banding pattern in Chara and Nitella species. The pH variation along the cells acts as a carbon concentrating mechanism. At the time of saline stress, however, these channels might become a part of saline pathology. The chemical composition of lake waters, including salinity, may also affect the distribution of charophytes significantly. This was also one of the findings presented by Schubert et al. (forthcoming), who related the Chilean charophyte biogeographic distribution to a range of water-chemistry parameters. Species of the genera Chara and Nitella tended to be well separated by their preferences for a given pH and conductivity range. Interestingly, however, Chara braunii tended to have similar requirements to Nitella rather than to other Chara species.

Environmental restoration of charophyte habitats is another subject gaining interest. For instance, the arrival of alien species, both charophytes and angiosperms, endangers original communities worldwide (Bertrin et al. 2013; Karol et al. 2017; Soulié-Märsche et al. 2013). The restoration of human-disturbed aquatic environments is largely dependent on the capability of the diaspore banks to regenerate the ancient communities. In this sense, charophyte oospores and gyrogonites have been shown to be highly resistant to damage over time and permit the germination of oospores after as much as 50 years of burial (Rodrigo, Alonso-Guillén, and Soulié-Märsche 2010). Holzhausen, Porsche, and Schubert (forthcoming) investigated the germination potential of 10 Characeae species, gathering oospores straight from the growing plants or from diaspore banks from seven European locations. The study yields species-specific data both on the dormancy breaking and on the germination induction that can be employed in restoration of degraded water bodies. In a related study, Nowak, Steinhardt et al. (forthcoming) examined macrophyte communities at 10 sampling sites along the Baltic coastline and compared the extant species distribution to that found in sediment cores. They also tested the germination potential of the diaspore bank. In general, charophytes seem to be less common now than in the past. However, the oospores are still present and viable in the sediments, making the diaspore reservoir available for the ecosystem restoration.

Furthermore, the calcified part of the oosporangia, i.e. the gyrogonites, is also useful for the elucidation of past environments, much older in the geological record. Li et al. (forthcoming) found fossil gyrogonites from the early characeans Mesochara stipitata and Aclistochara huihuibaoensis in the Lower Cretaceous Chijinbao formation (Jiuquan Basin, Northwest China). Correlation of sedimentological, taphonomic and palaeoecological data suggests that there was a permanent shallow freshwater lake in the Xiagou area during the deposition of the Chijinbao formation and that the climate was warm. China was one of the first landmasses, where the ancestors of living Characeae became abundant. At the same time, the now extinct family, the clavatoraceans, were the dominant charophytes in the tropical latitudes (such as, for instance, Europe and North Africa (Martín-Closas 2015).

Notes on Contributors

Mary Beilby is Honorary Senior Lecturer in School of Physics, University of NSW. Her main interest is electrophysiology of characean cells. Contribution: writing the article.

Susanne C. Schneider is a senior scientist at the Norwegian Institute for Water Research and holds an additional part time position as professor at the Norwegian University of Life Sciences. Her main interest centres around the ecology of macrophytes and benthic algae. Contribution: writing the article.

Andrzej Puckacz is an aquatic ecologist and associate professor at the Adam Mickiewicz University in Poznań working with charophytes from freshwater ecosystems. Contribution: writing the article.

Carles Martín-Closas is professor at the University of Barcelona and his research is mainly devoted to the evolution and biostratigraphy of fossil charophytes. Contribution: writing the article.

Disclosure statement

No potential conflict of interests was reported by the authors.