The Phylogenetic Association Between Salt Tolerance and Heavy Metal Hyperaccumulation in Angiosperms

Salt tolerance and heavy metal hyperaccumulation are two rare plant abilities that are heavily studied for their potential to contribute to agricultural sustainability and phytoremediation in response to anthropogenic environmental change. Several observations suggest that it is worth investigating the link between the abilities to tolerate high levels of soil salinity or accumulate more of a particular heavy metal from the soil than most plants. Firstly, several angiosperm families are known to contain both salt tolerant plants (halophytes) and heavy metal hyperaccumulators. Secondly, some halophytes can also accumulate heavy metals. Thirdly, although salinity tolerance and heavy metal hyperaccumulation typically require many physiological or anatomical changes, both have apparently evolved many times in angiosperms and among closely related species. We test for a significant relationship between halophytes and hyperaccumulators in angiosperms using taxonomic and phylogenetic analyses. We test whether there are more angiosperm families with both halophytes and hyperaccumulators than expected by chance, and whether there are more species identified as both halophyte and hyperaccumulator than if the abilities were unconnected. We also test whether halophytes and hyperaccumulators are phylogenetically clustered among species in seven angiosperm families. We find a significant association between halophytes and hyperaccumulators among angiosperm families and that there are significantly more species identified as both halophytes and hyperaccumulators than expected. Halophytes and hyperaccumulators each show low phylogenetic clustering, suggesting these abilities can vary among closely related species. In Asteraceae, Amaranthaceae, Fabaceae, and Poaceae, halophytes and hyperaccumulators are more closely related than if the two traits evolved independently.     

Salt tolerance evolves more frequently in C4 grass lineages

Salt tolerance has evolved many times in the grass family, and yet few cereal crops are salt tolerant. Why has it been so difficult to develop crops tolerant of saline soils when salt tolerance has evolved so frequently in nature? One possible explanation is that some grass lineages have traits that predispose them to developing salt tolerance and that without these background traits, salt tolerance is harder to achieve. One candidate background trait is photosynthetic pathway, which has also been remarkably labile in grasses. At least 22 independent origins of the C₄ photosynthetic pathway have been suggested to occur within the grass family. It is possible that the evolution of C₄ photosynthesis aids exploitation of saline environments, because it reduces transpiration, increases water‐use efficiency and limits the uptake of toxic ions. But the observed link between the evolution of C₄ photosynthesis and salt tolerance could simply be due to biases in phylogenetic distribution of halophytes or C₄ species. Here, we use a phylogenetic analysis to investigate the association between photosynthetic pathway and salt tolerance in the grass family Poaceae. We find that salt tolerance is significantly more likely to occur in lineages with C₄ photosynthesis than in C₃ lineages. We discuss the possible links between C₄ photosynthesis and salt tolerance and consider the limitations of inferring the direction of causality of this relationship.     

Plant salt tolerance: adaptations in halophytes

Background Most of the water on Earth is seawater, each kilogram of which contains about 35 g of salts, and yet most plants cannot grow in this solution; less than 0·2 % of species can develop and reproduce with repeated exposure to seawater. These ‘extremophiles’ are called halophytes.Scope Improved knowledge of halophytes is of importance to understanding our natural world and to enable the use of some of these fascinating plants in land re-vegetation, as forages for livestock, and to develop salt-tolerant crops. In this Preface to a Special Issue on halophytes and saline adaptations, the evolution of salt tolerance in halophytes, their life-history traits and progress in understanding the molecular, biochemical and physiological mechanisms contributing to salt tolerance are summarized. In particular, cellular processes that underpin the ability of halophytes to tolerate high tissue concentrations of Na⁺ and Cl⁻, including regulation of membrane transport, their ability to synthesize compatible solutes and to deal with reactive oxygen species, are highlighted. Interacting stress factors in addition to salinity, such as heavy metals and flooding, are also topics gaining increased attention in the search to understand the biology of halophytes.Conclusions Halophytes will play increasingly important roles as models for understanding plant salt tolerance, as genetic resources contributing towards the goal of improvement of salt tolerance in some crops, for re-vegetation of saline lands, and as ‘niche crops’ in their own right for landscapes with saline soils.     

Predicting species’ tolerance to salinity and alkalinity using distribution data and geochemical modelling: a case study using Australian grasses

Background and Aims Salt tolerance has evolved many times independently in different plant groups. One possible explanation for this pattern is that it builds upon a general suite of stress-tolerance traits. If this is the case, then we might expect a correlation between salt tolerance and other tolerances to different environmental stresses. This association has been hypothesized for salt and alkalinity tolerance. However, a major limitation in investigating large-scale patterns of these tolerances is that lists of known tolerant species are incomplete. This study explores whether species’ salt and alkalinity tolerance can be predicted using geochemical modelling for Australian grasses. The correlation between taxa found in conditions of high predicted salinity and alkalinity is then assessed.Methods Extensive occurrence data for Australian grasses is used together with geochemical modelling to predict values of pH and electrical conductivity to which species are exposed in their natural distributions. Using parametric and phylogeny-corrected tests, the geochemical predictions are evaluated using a list of known halophytes as a control, and it is determined whether taxa that occur in conditions of high predicted salinity are also found in conditions of high predicted alkalinity.Key Results It is shown that genera containing known halophytes have higher predicted salinity conditions than those not containing known halophytes. Additionally, taxa occurring in high predicted salinity tend to also occur in high predicted alkalinity.Conclusions Geochemical modelling using species’ occurrence data is a potentially useful approach to predict species’ relative natural tolerance to challenging environmental conditions. The findings also demonstrate a correlation between salinity tolerance and alkalinity tolerance. Further investigations can consider the phylogenetic distribution of specific traits involved in these ecophysiological strategies, ideally by incorporating more complete, finer-scale geochemical information, as well as laboratory experiments.     

Convergent evolution of seed dispersal by ants,and phylogeny and biogeography in flowering plants: A global survey

Seed dispersal is a fundamental life history trait in plants. Although the recent surge of interest in seed dispersal by ants (myrmecochory) has added greatly to knowledge on the ecology of seed dispersal and ant–plant mutualisms, myrmecochory also represents a unique opportunity to examine the links between seed dispersal and evolution in flowering plants. Here we review the taxonomic, phylogenetic and biogeographic distribution of myrmecochory in flowering plants. Myrmecochory is mediated by elaiosomes, i.e., lipid-rich seed appendages that attract ants and serve as rewards for dispersal. We surveyed the literature for evidence of elaiosomes in angiosperm plants to estimate the global prevalence of myrmecochory. We then searched the literature for phylogenetic reconstructions to identify myrmecochorous lineages and to estimate the minimum number of independent evolutionary origins of myrmecochory. We found that myrmecochory is present in at least 11 000 species or 4.5% of all species, in 334 genera or 2.5% of all genera and in 77 families or 17% of all families of angiosperm plants. We identified at least 101, but possibly up to 147, independent origins of myrmecochory. We estimated three or more origins in 13 families and found that at least half the genera are myrmecochorous in 10 families. Most myrmecochorous lineages were Australian, South African or northern temperate (Holarctic). A mapping of families containing myrmecochorous genera on a dated angiosperm supertree showed that myrmecochory has evolved in most of the major angiosperm lineages and that it is more frequent in younger families (crown group age <80 million years) than in older ones. We suggest that the relatively low physiological and energetic costs of producing an elaiosome and the consistent selective benefits of myrmecochory (dispersal, protection from seed predators and fire, safe and nutrient-rich microsites) explain the numerous evolutionary and developmental origins of myrmecochory in angiosperm plants, and we propose that elaiosomes thus provide one of the most dramatic examples of convergent evolution in biology.     

一年生盐生植物耐盐机制研究进展

盐生植物是一类能够在盐土上完成生活史的天然植物, 在与盐土协同演化过程中形成了一系列适应盐生环境的特殊生存策略。其中一年生盐生植物因其生活史短、方便培养和观察、易于基因转化和后代繁殖, 已成为耐盐机制研究的主要对象。一年生盐生植物面临多变的生境胁迫, 具有更大的生存风险, 所以具有不同于多年生盐生植物的更稳妥的适应机制, 主要体现在种子的高盐休眠、复水速萌、形态和萌发的多态性、存在持久种子库及调节资源分配等方面。种子萌发后的生长、发育和繁殖等生活史的各阶段都要经受严峻的盐生胁迫环境。通常所说的耐盐机理是指成株对盐分的调控, 按照植物种类不同而分为稀盐、泌盐和拒盐3种耐盐形式。该文在对国内外相关文献进行分析归纳的基础上, 首先介绍了一年生盐生植物的常见类型, 然后分别从种子特征、形态结构、生理生化和生态习性等方面综述了一年生盐生植物的耐盐机制。     

Halophyte Improvement for a Salinized World

It is more important to improve the salt tolerance of crops in a salinized world with the situations of increasing populations, declining crop yields, and a decrease in agricultural lands. Attempts to produce salt-tolerant crops have involved the manipulation of existing crops through conventional breeding, genetic engineering and marker-assisted selection (MAS). However, these have, so far, not produced lines growing on highly saline water. Hence, the domestication of wild halophytes as crops appears to be a feasible way to develop agriculture in highly saline environments. In this review, at first, the assessment criteria of salt tolerance for halophytes are discussed. The traditional criteria for the classification of salinity in crops are less applicable to strong halophytes with cubic growth curves at higher salinities. Thus, realistic assessment criteria for halophytes should be evaluated at low and high salinity levels. Moreover, absolute growth rather than relative growth in fields during a crop's life cycle should be considered. Secondly, the use of metabolomics to understand the mechanisms by which halophytes respond to salt tolerance is highlighted as is the potential for metabolomics-assisted breeding of this group of plants. Metabolomics provides a better understanding of the changes in cellular metabolism induced by salt stress. Identification of metabolic quantitative trait loci (QTL) associated with salt tolerance might provide a new method to aid the selection of halophyte improvement. Thirdly, the identification of germplasm-regression-combined (GRC) marker-trait association and its potential to identifying markers associated with salt tolerance is outlined. Results of MAS/linkage map-QTL have been modest because of the absence of QTLs with tight linkage, the non-availability of mapping populations and the substantial time needed to develop such populations. To overcome these limitations, identification by GRC-based marker-trait association has been successfully applied to many plant traits, including salt tolerance. Finally, we provide a prospect on the challenges and opportunities for halophyte improvement, especially in the integration of metabolomics- and GRC-marker-assisted selection towards new or unstudied halophyte breeding, for which no other genetic information, such as linkage maps and QTL, are available.     

Transcriptome Analysis of the Heritable Salt Tolerance of Prairie Cordgrass (<Emphasis Type="Italic">Spartina pectinata Link</Emphasis>)

The salt-tolerant capability of the candidate bioenergy crop prairie cordgrass greatly surpasses that of previously characterized prairie grass species and most other plants. To understand the mechanism of inherited salt tolerance, we compared phenotypic and genetic qualities in half-sib families of prairie cordgrass after salt treatment. Each family was treated with a 400 mM NaCl solution or a water control and then measured for various health phenotypes. Phenotypes associated with salt tolerance were shown to be moderately heritable between parent and offspring. RNA-seq analysis revealed differential regulation in unique pathways including metabolism, signaling, photosynthesis, and the circadian rhythm. The studies herein suggest that alternative regulation of the photosynthetic pathway could confer increased salt resistance in halophytes and can be monitored phenotypically or genetically in breeding programs. The improvement of salt-tolerant traits in prairie cordgrass would increase its potential to be grown as a bioenergy crop on lands that are not suitable for the growth of food crops.     

INDEPENDENT EVOLUTION OF TERRESTRIALITY IN ATLANTIC TRUNCATELLID GASTROPODS

Phylogenetic analysis of truncatellid gastropods using comparative anatomy and ribosomal RNA sequences shows that terrestrial truncatellids likely evolved three times independently in the Caribbean. The terrestrial subfamily Geomelaniinae, characterized in part by pallial fertilization and uniquely derived features of radula and protoconch, occurs in the Greater Antilles and Cayman Islands. Truncatellinae, with renopericardial fertilization, has several widespread amphibious species and two terrestrial species restricted to Trinidad and Barbados. The species in Barbados may be the most recent animal species to evolve full terrestriality; Barbados emerged above sea level only about one million years ago. By the mid-Cenozoic, truncatellids had traits enabling them to colonize land in appropriate tectonic settings. Parallel trends in character evolution occurred in the terrestrial lineages. In older terrestrial radiations, transitional character states would likely be lost, potentially allowing parallelism to confound phylogenetic analysis of morphological characters.     

不同类型盐生植物适应盐胁迫的生理生长机制及Na+逆向转运研究进展

盐生植物是指能在离子浓度至少200 mmol/L以上的生境中生长并完成生活史的植物。盐生植物可分为稀盐盐生植物、泌盐盐生植物、拒盐盐生植物三类。本文从生长形态、生理和分子3个方面总结三类盐生植物响应盐胁迫的不同策略及研究进展,发现盐生植物在分子水平上主要通过Na⁺转运蛋白和为其提供能量的两类基因应对体内过高Na⁺,这可能是引起盐生植物生理和生长形态异于非盐生植物的重要因素。其中稀盐盐生植物主要通过液泡离子区隔化应对盐胁迫,并表现出肉质化生长形态;泌盐盐生植物通过将体内盐分排出体外应对盐胁迫,并进化出特有的生理结构——盐腺或盐囊泡;拒盐盐生植物通过将盐离子积累在皮层细胞液泡和根部木质部薄壁细胞中减少向上运输Na⁺,同时根部多栓质化减少Na⁺吸收。本综述旨在为今后研究盐生植物及其耐盐机制提供相关依据,为植物耐盐分子育种奠定基础。     

Species, types, distribution, and economic potential of halophytes in China

According to a survey conducted from 1995 to 2004 in the eight regions with salinized soils, China contains 587 halophytes representing 242 genera and 71 families: apart from three species of ferns, all are angiosperms. Physiologically, Chinese halophytes include salt-secreting halophytes, euhalophytes, and pseudohalophytes. Ecologically, Chinese halophytes include zerohalophytes, mesohalophytes, and hydrohalophytes. Chinese halophytes represent a salt-tolerant gene pool that might be used to increase the salt tolerance of conventional crops through breeding, but also have considerable potential as salt-tolerant economic crops providing food, forage, medicine, and industrial material in salinized soils.     

Physiological and molecular mechanisms of plant salt tolerance

Salt tolerance is an important economic trait for crops growing in both irrigated fields and marginal lands. The plant kingdom contains plant species that possess highly distinctive capacities for salt tolerance as a result of evolutionary adaptation to their environments. Yet, the cellular mechanisms contributing to salt tolerance seem to be conserved to some extent in plants although some highly salt-tolerant plants have unique structures that can actively excrete salts. In this review, we begin by summarizing the research in Arabidopsis with a focus on the findings of three membrane transporters that are important for salt tolerance: SOS1, AtHKT1, and AtNHX1. We then review the recent studies in salt tolerance in crops and halophytes. Molecular and physiological mechanisms of salt tolerance in plants revealed by the studies in the model plant, crops, and halophytes are emphasized. Utilization of the Na⁺ transporters to improve salt tolerance in plants is also summarized. Perspectives are provided at the end of this review.     

How Can Stomata Contribute to Salt Tolerance?

Although some of the physiological mechanisms which contributeto salt tolerance in plants are known, there are still somemajor gaps in understanding and it remains impossible to providea satisfactory integrated picture for the plant as a whole.The operation of stomata in halophytes has received little attentioneven though all of the salt present in the shoot (apart fromthat taken in during submergence) is thought to be carried inthe transpiration stream. In non-halophytes, stomatal functionis damaged by sodium ions, and disruption of the normal regulationof transpiration should be seen as a possible contributor totheir inability to survive in salt-laden soils. The developmentof salt-tolerant cultivars of crops may require attention tothe need for appropriate adaptations to the ionic relationsof stomatal guard cells. Despite the small amount of evidenceavailable, it is possible to identify two alternative adaptationsthat occur in the stomata of halophytes: (1) the guard cellscan utilize Na⁺instead of K⁺to achieve their normal regulationof turgor; (2) the guard cells continue to use K⁺and are ableto limit their intake of Na⁺. The second adaptation is worthyof further exploration because it may provide a means for ‘topdown’ control of transpiration and, therefore, of theamount of salt delivered to the shoot. This mechanism may bevery important in some of the glandless halophytes, and it couldbe of particular interest as a potential contributor to thedevelopment of salt tolerance in crops. Salt tolerance; stomata; transpiration; halophytes; ionic regulation; sodium ions     

Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis

Phylogenetic evidence for biological traits that increase the net diversification rate of lineages (key innovations) is most commonly drawn from comparisons of clade size. This can work well for ancient, unreversed traits and for correlating multiple trait origins with higher diversification rates, but it is less suitable for unique events, recently evolved innovations, and traits that exhibit homoplasy. Here I present a new method for detecting the phylogenetic signature of key innovations that tests whether the evolutionary history of the candidate trait is associated with shorter waiting times between cladogenesis events. The method employs stochastic models of character evolution and cladogenesis and integrates well into a Bayesian framework in which uncertainty in historical inferences (such as phylogenetic relationships) is allowed. Applied to a well-known example in plants, nectar spurs in columbines, the method gives much stronger support to the key innovation hypothesis than previous tests.     

Growing floricultural crops with brackish water

In the current review we focus on the opportunity to use brackish water in the cultivation of floricultural plants, plants for which, due to their high economic value, growers have traditionally used good quality water for irrigation. Now, even for these crops the use of alternative water sources for irrigating nursery plants is needed because of the limited supplies of fresh water in many countries; understanding how saline water can be used will also enhance sustainable development in floriculture. While salt stress usually reduces plant growth, any such reduction might not be negative for ornamentals, where shoot vigour is sometime undesirable, although on flower crops salt stress can delay flowering or decrease flower quality characteristics. However, a decrease in growth rate is not enough to characterize the salt tolerance of ornamental plants, but traits like tip and marginal leaf burn, as consequence of sodium and chlorine accumulation, have to be considered for their effects on aesthetical value. With this in mind, some halophytes should be considered for floriculture because of their ability to cope with saline environments; their potential to tolerate salt is an important factor in reducing production costs. Consequently, the identification of ornamental halophytes is important for producing a commercially acceptable crop when irrigated with brackish waters. Many aspects of a plant's reaction to salt are genetically determined, so selection of suitable genotypes or breeding for salt tolerance in ornamentals are interesting options. Developing salt-tolerant floricultural crops, together with typical management practices that avoid excessive salinity stress in the root media, will provide the grower with economically and environmentally sound wastewater reuse options.     

Leaf energy balance modelling as a tool to infer habitat preference in the early angiosperms

Despite more than a century of research, some key aspects of habitat preference and ecology of the earliest angiosperms remain poorly constrained. Proposed growth ecology has varied from opportunistic weedy species growing in full sun to slow-growing species limited to the shaded understorey of gymnosperm forests. Evidence suggests that the earliest angiosperms possessed low transpiration rates: gas exchange rates for extant basal angiosperms are low, as are the reconstructed gas exchange rates for the oldest known angiosperm leaf fossils. Leaves with low transpirational capacity are vulnerable to overheating in full sun, favouring the hypothesis that early angiosperms were limited to the shaded understorey. Here, modelled leaf temperatures are used to examine the thermal tolerance of some of the earliest angiosperms. Our results indicate that small leaf size could have mitigated the low transpirational cooling capacity of many early angiosperms, enabling many species to survive in full sun. We propose that during the earliest phases of the angiosperm leaf record, angiosperms may not have been limited to the understorey, and that some species were able to compete with ferns and gymnosperms in both shaded and sunny habitats, especially in the absence of competition from more rapidly growing and transpiring advanced lineages of angiosperms.     

Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika

A recent phylogenetic analysis of mitochondrial DNA sequences from eretmodine cichlids from Lake Tanganyika indicated independent origins of strikingly similar trophic specializations, such as dentition characters. Because genetic lineages with similar trophic morphologies were not monophyletic, but instead were grouped with lineages with different trophic phenotypes, raises the question of whether trophic morphology covaries with additional morphological characters. Here, we quantified morphological variation in body shape and trophically associated traits among eretmodine cichlids using linear measurements, meristic counts and landmark‐based geometric morphometrics. A canonical variates analysis (CVA) delineated groups consistent with dentition characters. Multivariate regression and partial least squares analyses indicated that body shape was significantly associated with trophic morphology. When the phylogenetic relationships among taxa were taken into account using comparative methods, the covariation of body shape and trophic morphology persisted, indicating that phylogenetic relationships were not wholly responsible for the observed pattern. We hypothesize that trophic ecology may be a key factor promoting morphological differentiation, and postulate that similar body shape and feeding structures have evolved multiple times in independent lineages, enabling taxa to invade similar adaptive zones.     

Why care? Inferring the evolution of complex social behaviour

Phylogenetic comparative analyses of complex traits often reduce the traits of interests into a single (or a few) component variables. Here, we show that this may be an over‐simplification, because components of a complex trait may evolve independently from each other. Using eight components of parental care in 400 bird species from 89 avian families that represent the relative contribution of male vs. female to a particular type of care, we show that some components evolve in a highly correlated manner, whereas others exhibit low (or no) phylogenetic correlation. Correlations were stronger within types of parental activity (brooding, feeding, guarding) than within stages of the breeding cycle (incubation, prefledging care, post‐fledging care). A phylogenetically corrected cluster analysis identified two groups of parental care components that evolved in a correlated fashion: one group included incubation and brooding, whereas the other group comprised of the remaining components. The two groups of components provide working hypotheses for follow‐up studies to test the underlying genetic, developmental and ecological co‐evolutionary mechanism between male and female care. Furthermore, the components within each group are expected to respond consistently to different ambient and social environments.     

NADPH oxidases and the evolution of plant salinity tolerance

Soil salinization is a major threat to global food security and the biodiversity of natural ecosystems. To adapt to salt stress, plants rely on ROS-mediated signalling networks that operate upstream of a broad array of physiological and genetic processes. A key player in ROS signalling is NADPH oxidase, a plasma-membrane-bound enzyme encoded by RBOH genes. In this study, we have conducted a comprehensive bioinformatic analysis of over 50 halophytic and glycophytic species to link the difference in the kinetics of ROS signalling between contrasting species with the abundance and/or structure of NADPH oxidases. The RBOH proteins were predicted in all the tested plant lineages except some algae species from the Rhodophyta, Chlorophyta and Streptophyta. Within the glycophytic group, the number of RBOH copies correlated negatively with salinity stress tolerance, suggesting that a reduction in the number of RBOH isoforms may be potentially related to the evolution of plant salinity tolerance. While halophytes did not develop unique protein families during evolution, they evolved additional phosphorylation target sites at the N-termini of NADPH oxidases, potentially modulating enzyme activity and allowing more control over their function, resulting in more efficient ROS signalling and adaptation to saline conditions.