Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Sugars and the speed of life-Metabolic signals that determine plant growth, development and death.

Plant growth and development depend on the availability of carbohydrates synthesised in photosynthesis (source activity) and utilisation of these carbohydrates for growth (sink activity). External conditions, such as temperature, nutrient availability and stress, can affect source as well as sink activity. Optimal utilisation of resources is under circadian clock control. This molecular timekeeper ensures that growth responses are adjusted to different photoperiod and temperature settings by modulating starch accumulation and degradation accordingly. For example, during the night, starch degradation is required to provide sugars for growth. Under favourable growth conditions, high sugar availability stimulates growth and development, resulting in an overall accelerated life cycle of annual plants. Key signalling components include trehalose-6-phosphate (Tre6P), which reflects sucrose availability and stimulates growth and branching when the conditions are favourable. Under sink limitation, Tre6P does, however, inhibit night-time starch degradation. Tre6P interacts with Sucrose-non-fermenting1-Related Kinase1 (SnRK1), a protein kinase that inhibits growth under starvation and stress conditions and delays development (including flowering and senescence). Tre6P inhibits SnRK1 activity, but SnRK1 increases the Tre6P to sucrose ratio under favourable conditions. Alongside Tre6P, Target of Rapamycin (TOR) stimulates processes such as protein synthesis and growth when sugar availability is high. In annual plants, an accelerated life cycle results in early leaf and plant senescence, thus shortening the lifespan. While the availability of carbohydrates in the form of sucrose and other sugars also plays an important role in seasonal life cycle events (phenology) of perennial plants, the sugar signalling pathways in perennials are less well understood.

Interactions between sucrose and jasmonate signalling in the response to cold stress.

BACKGROUND: Jasmonates play an important role in plant stress and defence responses and are also involved in the regulation of anthocyanin synthesis in response to sucrose availability. Here we explore the signalling interactions between sucrose and jasmonates in response to cold stress in Arabidopsis. RESULTS: Sucrose and cold treatments increased anthocyanin content additively. Comprehensive profiling of phytohormone contents demonstrated that jasmonates, salicylic acid and abscisic acid contents increased in response to sucrose treatment in plants grown on agar, but remained considerably lower than in plants grown in compost. The gibberellin GA3 accumulated in response to sucrose treatment but only at warm temperature. The role of jasmonate signalling was explored using the jasmonate response mutants jar1-1 and coi1-16. While the jar1-1 mutant lacked jasmonate-isoleucine and jasmonate-leucine, it accumulated 12-oxo-phytodienoic acid at low temperature on agar medium. Altered patterns of abscisic acid accumulation and higher sugar contents were found in the coi1-16 mutant when grown in compost. Both mutants were able to accumulate anthocyanin and to cold acclimate, but the jar-1-1 mutant showed a larger initial drop in whole-rosette photosystem II efficiency upon transfer to low temperature. CONCLUSIONS: Hormone contents are determined by interactions between temperature and sucrose supply. Some of these effects may be caused indirectly through senescence initiation in response to sucrose availability. During cold stress, the adjustments of hormone contents may compensate for impaired jasmonate signalling, enabling cold acclimation and anthocyanin accumulation in Arabidopsis jasmonate response mutants, e.g. through antagonistic interactions between gibberellin and jasmonate signalling.

Floral uniformity through evolutionary time in a species-rich tree lineage.

Changes in floral morphology are expected across evolutionary time and are often promoted as important drivers in angiosperm diversification. Such a statement, however, is in contrast to empirical observations of species-rich lineages that show apparent conservative floral morphologies even under strong selective pressure to change from their environments. Here, we provide quantitative evidence for prolific speciation despite uniform floral morphology in a tropical species-rich tree lineage. We analyse floral disparity in the environmental and phylogenetic context of Myrcia (Myrtaceae), one of the most diverse and abundant tree genera in Neotropical biomes. Variation in floral morphology among Myrcia clades is exceptionally low, even among distantly related species. Discrete floral specialisations do occur, but these are few, present low phylogenetic signal, have no strong correlation with abiotic factors, and do not affect overall macroevolutionary dynamics in the lineage. Results show that floral form and function may be conserved over large evolutionary time scales even in environments full of opportunities for ecological interactions and niche specialisation. Species accumulation in diverse lineages with uniform flowers apparently does not result from shifts in pollination strategies, but from speciation mechanisms that involve other, nonfloral plant traits.

Myrteae phylogeny, calibration, biogeography and diversification patterns: Increased understanding in the most species rich tribe of Myrtaceae.

Myrteae (c. 2500 species; 51 genera) is the largest tribe of Myrtaceae and an ecologically important groups of angiosperms in the Neotropics. Systematic relationships in Myrteae are complex, hindering conservation initiatives and jeopardizing evolutionary modelling. A well-supported and robust phylogenetic hypothesis was here targeted towards a comprehensive understanding of the relationships within the tribe. The resultant topology was used as a base for key evolutionary analyses such as age estimation, historical biogeography and diversification rate patterns. One nuclear (ITS) and seven chloroplast (psbA-trnH, matK, ndhF, trnl-trnF, trnQ-rps16, rpl16 and rpl32-trnL) DNA regions for 115 taxa representing 46 out of the 51 genera in the tribe were accessed and analysed using maximum likelihood and Bayesian inference tools for phylogenetic reconstruction. Dates of diversification events were estimated and contrasted using two distinct fossil sets (macro and pollen) in BEAST. The subsequent dated phylogenies were compared and analysed for biogeographical patterns using BioGeoBEARS and diversification rates using BAMM. Myrteae phylogeny presents strong statistical support for three major clades within the tribe: Australasian group, Myrtus group and Main Neotropical Lineage. Dating results from calibration using macrofossil are an average of 20 million years older and show an early Paleocene origin of Myrteae, against a mid-Eocene one from the pollen fossil calibration. Biogeographic analysis shows the origin of Myrteae in Zealandia in both calibration approaches, followed by a widespread distribution throughout the still-linked Gondwana continents and diversification of Neotropical endemic lineages by later vicariance. Best configuration shift indicates three points of acceleration in diversification rates, all of them occurring in the Main Neotropical Lineage. Based on the reconstructed topology, several new taxonomic placements were recovered, including: the relative position of Myrtus communis, the placement of the Blepharocalyx group, the absence of generic endemism in the Caribbean, and the paraphyletism of the former Pimenta group. Distinct calibration approaches affect biogeography interpretation, increasing the number of necessary long distance dispersal events in the topology with older nodes. It is hypothesised that biological intrinsic factors such as modifications of embryo type and polyploidy might have played a role in accelerating shifts of diversification rates in Neotropical lineages. Future perspectives include formal subtribal classification, standardization of fossil calibration approaches and better links between diversification shifts and trait evolution.

Classification of intra-specific variation in plant functional strategies reveals adaptation to climate.

Background and Aims: In plants, extensive intra-specific variation exists in the allocation of resources between vegetative growth and reproduction, reflecting different functional strategies. A simple method for the classification of intra-specific variation in these strategies would enable characterization of evolutionary and ecological processes. Methods: C-S-R theory can be applied to classify functional strategies (competitive C; stress tolerant, S; ruderal, R) in different plant species. Using a diverse set of arabidopsis ( Arabidopsis thaliana ) accessions grown under common conditions, it was tested whether a simple approach designed for allocating C-S-R strategies at the species level can also be used to analyse intra-specific variation. Key Results: Substantial intra-specific variation between arabidopsis accessions was found along the S-R axis. There was a positive correlation of temperature at the geographical origin with the dimension of S and a negative correlation with the dimension of R. Flowering time in a natural annual cycle and leaf dry matter content were identified as the main determinants of this adaptation, with plants originating from warmer climates having a higher leaf dry matter content and flowering earlier in a common garden. Conclusions: It was shown that functional strategies reflect adaptation to climate, with consequences for important traits such as fecundity and total plant dry weight. The approach could be used in genome-wide association studies to determine the genetic basis of functional strategies in wild species or crops.

Adaptation to altitude affects the senescence response to chilling in the perennial plant Arabis alpina.

In annual plants with determinate growth, sugar accumulation signals high carbon availability once growth has ceased, resulting in senescence-dependent nutrient recycling to the seeds. However, this senescence-inducing effect of sugars is abolished at cold temperature, where sugar accumulation is important for protection. Here, natural variation was exploited to analyse the effect of chilling on interactions between leaf senescence, sugars, and phytohormones in Arabis alpina, a perennial plant with indeterminate growth. Eight accessions of A. alpina originating from between 2090 and 3090 m above sea level in the French Alps were used to identify heritable adaptations in senescence, stress response, sugars, and phytohormones to altitude. Accessions from high altitudes showed an enhanced capacity for sucrose accumulation and a diminished loss of chlorophyll in response to chilling. At warm temperature, sucrose content was negatively correlated with chlorophyll content, and sucrose treatment induced leaf senescence. Chilling resulted in lower indole-3-acetic acid, but higher zeatin and jasmonic acid contents. Interactions between sugar and phytohormones included a positive correlation between sucrose and jasmonic acid contents that may be involved in promoting the stress-dependent decline in chlorophyll. These findings reveal regulatory interactions that underlie adaptation in the senescence and stress response to chilling.

The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation.

Trehalose 6-P (T6P) is a sugar signal in plants that inhibits SNF1-related protein kinase, SnRK1, thereby altering gene expression and promoting growth processes. This provides a model for the regulation of growth by sugar. However, it is not known how this model operates under sink-limited conditions when tissue sugar content is uncoupled from growth. To test the physiological importance of this model, T6P, SnRK1 activities, sugars, gene expression, and growth were measured in Arabidopsis (Arabidopsis thaliana) seedlings after transfer to cold or zero nitrogen compared with sugar feeding under optimal conditions. Maximum in vitro activities of SnRK1 changed little, but T6P accumulated up to 55-fold, correlating with tissue Suc content in all treatments. SnRK1-induced and -repressed marker gene expression strongly related to T6P above and below a threshold of 0.3 to 0.5 nmol T6P g(-1) fresh weight close to the dissociation constant (4 µm) of the T6P/ SnRK1 complex. This occurred irrespective of the growth response to Suc. This implies that T6P is not a growth signal per se, but through SnRK1, T6P primes gene expression for growth in response to Suc accumulation under sink-limited conditions. To test this hypothesis, plants with genetically decreased T6P content and SnRK1 overexpression were transferred from cold to warm to analyze the role of T6P/SnRK1 in relief of growth restriction. Compared with the wild type, these plants were impaired in immediate growth recovery. It is concluded that the T6P/SnRK1 signaling pathway responds to Suc induced by sink restriction that enables growth recovery following relief of limitations such as low temperature.

Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability.

Trehalose 6-phosphate (T6P) is an important regulator of plant metabolism and development. T6P content increases when carbon availability is high, and in young growing tissue, T6P inhibits the activity of Snf1-related protein kinase (SnRK1). Here, strong accumulation of T6P was found in senescing leaves of Arabidopsis (Arabidopsis thaliana), in parallel with a rise in sugar contents. To determine the role of T6P in senescence, T6P content was altered by expressing the bacterial T6P synthase gene, otsA (to increase T6P), or the T6P phosphatase gene, otsB (to decrease T6P). In otsB-expressing plants, T6P accumulated less strongly during senescence than in wild-type plants, while otsA-expressing plants contained more T6P throughout. Mature otsB-expressing plants showed a similar phenotype as described for plants overexpressing the SnRK1 gene, KIN10, including reduced anthocyanin accumulation and delayed senescence. This was confirmed by quantitative reverse transcription-polymerase chain reaction analysis of senescence-associated genes and genes involved in anthocyanin synthesis. To analyze if the senescence phenotype was due to decreased sugar sensitivity, the response to sugars was determined. In combination with low nitrogen supply, metabolizable sugars (glucose, fructose, or sucrose) induced senescence in wild-type and otsA-expressing plants but to a smaller extent in otsB-expressing plants. The sugar analog 3-O-methyl glucose, on the other hand, did not induce senescence in any of the lines. Transfer of plants to and from glucose-containing medium suggested that glucose determines senescence during late development but that the effects of T6P on senescence are established by the sugar response of young plants.

Relationships of the competitor, stress tolerator, ruderal functional strategies of grass species with lifespan, photosynthetic type, naturalization and climate.

Grass species (family Poaceae) are globally distributed, adapted to a wide range of climates and express a diversity of functional strategies. We explored the functional strategies of grass species using the competitor, stress tolerator, ruderal (CSR) system and asked how a species' strategy relates to its functional traits, climatic distribution and propensity to become naturalized outside its native range. We used a global set of trait data for grass species to classify functional strategies according to the CSR system based on leaf traits. Differences in strategies in relation to lifespan (annual or perennial), photosynthetic type (C3 or C4), or naturalisation (native or introduced) were investigated. In addition, correlations with traits not included in the CSR classification were analyzed, and a model was fitted to predict a species' average mean annual temperature and annual precipitation across its range as a function of CSR scores. Values for competitiveness were higher in C4 species than in C3 species, values for stress tolerance were higher in perennials than in annuals, and introduced species had more pronounced competitive-ruderal strategies than native species. Relationships between the CSR classification, based on leaf traits, and other functional traits were analyzed. Competitiveness was positively correlated with height, while ruderality was correlated with specific root length, indicating that both above- and belowground traits underlying leaf and root economics contribute to realized CSR strategies. Further, relationships between climate and CSR classification showed that species with competitive strategies were more common in warm climates and at high precipitation, whereas species with stress tolerance strategies were more common in cold climates and at low precipitation. The findings presented here demonstrate that CSR classification of functional strategies based on leaf traits matches expectations for the adaptations of grass species that underlie lifespan, photosynthetic type, naturalization and climate.

Overexpression of GCN2-type protein kinase in wheat has profound effects on free amino acid concentration and gene expression.

A key point of regulation of protein synthesis and amino acid homoeostasis in eukaryotes is the phosphorylation of the α subunit of eukaryotic translation initiation factor 2 (eIF2α) by protein kinase general control nonderepressible (GCN)-2. In this study, a GCN2-type PCR product (TaGCN2) was amplified from wheat (Triticum aestivum) RNA, while a wheat eIF2α homologue was identified in wheat genome data and found to contain a conserved target site for phosphorylation by GCN2. TaGCN2 overexpression in transgenic wheat resulted in significant decreases in total free amino acid concentration in the grain, with free asparagine concentration in particular being much lower than in controls. There were significant increases in the expression of eIF2α and protein phosphatase PP2A, as well as a nitrate reductase gene and genes encoding phosphoserine phosphatase and dihydrodipicolinate synthase, while the expression of an asparagine synthetase (AS1) gene and genes encoding cystathionine gamma-synthase and sulphur-deficiency-induced-1 all decreased significantly. Sulphur deficiency-induced activation of these genes occurred in wild-type plants but not in TaGCN2 overexpressing lines. Under sulphur deprivation, the expression of genes encoding aspartate kinase/homoserine dehydrogenase and 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase was also lower than in controls. The study demonstrates that TaGCN2 plays an important role in the regulation of genes encoding enzymes of amino acid biosynthesis in wheat and is the first to implicate GCN2-type protein kinases so clearly in sulphur signalling in any organism. It shows that manipulation of TaGCN2 gene expression could be used to reduce free asparagine accumulation in wheat grain and the risk of acrylamide formation in wheat products.

Interactions between temperature and sugars in the regulation of leaf senescence in the perennial herb Arabis alpina L.

Annual plants usually flower and set seed once before senescence results in the death of the whole plant (monocarpic senescence). Leaf senescence also occurs in polycarpic perennials; even in "evergreen" species individual leaves senesce. In the annual model Arabidopsis thaliana sugars accumulate in the senescent leaves and senescence is accelerated by high sugar availability. Similar to A. thaliana, sugar contents increased with leaf age in the perennial Arabis alpina grown under warm conditions (22 °C day/18 night). At 5 °C, sugar contents in non-senescent leaves were higher than at a warm temperature, but dependent on the accession, either sugars did not accumulate or their contents decreased in old leaves. In A. alpina plants grown in their natural habitat in the Alps, sugar contents declined with leaf age. Growth at a cold temperature slightly delayed senescence in A. alpina. In both warm and cold conditions, an external glucose supply accelerated senescence, but natural variation was found in this response. In conclusion, sugar accumulation under warm conditions could accelerate leaf senescence in A. alpina plants, but genotype-specific responses and interactions with growth temperature are likely to influence senescence under natural conditions.

Cytosolic pyruvate,orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content.

The protein content of seeds determines their nutritive value, downstream processing properties and market value. Up to 95% of seed protein is derived from amino acids that are exported to the seed after degradation of existing protein in leaves, but the pathways responsible for this nitrogen metabolism are poorly defined. The enzyme pyruvate,orthophosphate dikinase (PPDK) interconverts pyruvate and phosphoenolpyruvate, and is found in both plastids and the cytosol in plants. PPDK plays a cardinal role in C(4) photosynthesis, but its role in the leaves of C(3) species has remained unclear. We demonstrate that both the cytosolic and chloroplastic isoforms of PPDK are up-regulated in naturally senescing leaves. Cytosolic PPDK accumulates preferentially in the veins, while chloroplastic PPDK also accumulates in mesophyll cells. Analysis of microarrays and labelling patterns after feeding (13)C-labelled pyruvate indicated that PPDK functions in a pathway that generates the transport amino acid glutamine, which is then loaded into the phloem. In Arabidopsis thaliana, over-expression of PPDK during senescence can significantly accelerate nitrogen remobilization from leaves, and thereby increase rosette growth rate and the weight and nitrogen content of seeds. This indicates an important role for cytosolic PPDK in the leaves of C(3) plants, and allows us to propose a metabolic pathway that is responsible for production of transport amino acids during natural leaf senescence. Given that increased seed size and nitrogen content are desirable agronomic traits, and that efficient remobilization of nitrogen within the plant reduces the demand for fertiliser applications, PPDK and the pathway in which it operates are targets for crop improvement.

Crops for Carbon Farming.

Agricultural cropping systems and pasture comprise one third of the world's arable land and have the potential to draw down a considerable amount of atmospheric CO2 for storage as soil organic carbon (SOC) and improving the soil carbon budget. An improved soil carbon budget serves the dual purpose of promoting soil health, which supports crop productivity, and constituting a pool from which carbon can be converted to recalcitrant forms for long-term storage as a mitigation measure for global warming. In this perspective, we propose the design of crop ideotypes with the dual functionality of being highly productive for the purposes of food, feed, and fuel, while at the same time being able to facilitate higher contribution to soil carbon and improve the below ground ecology. We advocate a holistic approach of the integrated plant-microbe-soil system and suggest that significant improvements in soil carbon storage can be achieved by a three-pronged approach: (1) design plants with an increased root strength to further allocation of carbon belowground; (2) balance the increase in belowground carbon allocation with increased source strength for enhanced photosynthesis and biomass accumulation; and (3) design soil microbial consortia for increased rhizosphere sink strength and plant growth-promoting (PGP) properties.

QTL analysis for sugar-regulated leaf senescence supports flowering-dependent and -independent senescence pathways.

*The aim of this work was to determine the genetic basis of sugar-regulated senescence and to explore the relationship with other traits, including flowering and nitrogen-use efficiency. *Quantitative trait loci (QTLs) for senescence were mapped in the Arabidopsis Bay-0 x Shahdara recombinant-inbred line (RIL) population after growth on glucose-containing medium, which accelerates senescence. The extent of whole-rosette senescence was determined by imaging the maximum quantum yield of photosystem II (F(v)/F(m)). *A major QTL on the top of chromosome 4 colocalized with FRI, a major determinant of flowering. This QTL interacted epistatically with a QTL on chromosome 5, where the floral repressor FLC localizes. Vernalization accelerated senescence in late-flowering lines with functional FRI and FLC alleles. Comparison with previous results using the Bay-0 x Shahdara population showed that rapid rosette senescence on glucose-containing medium was correlated with early flowering and high sugar content in compost-grown plants. In addition, correlation was found between the expression of flowering and senescence-associated genes in Arabidopsis accessions. However, an additional QTL on chromosome 3 was not linked to flowering, but to nitrogen-use efficiency. *The results show that whole-rosette senescence is genetically linked to the vernalization-dependent control of flowering, but is also controlled by flowering-independent pathways.

Sugars, senescence, and ageing in plants and heterotrophic organisms.

Although an involvement of metabolic signals in the regulation of plant senescence has been demonstrated in a range of studies, the exact signalling pathways remain largely unresolved. For leaves, evidence supports a role of sugar accumulation in the initiation and/or acceleration of senescence. However, regulation of senescence or ageing may respond to different metabolic signals in heterotrophic plant organs and heterotrophic organisms. In animals and yeast, dietary restriction results in increased lifespan. In this article, the metabolic regulation of leaf senescence is compared with the effects of dietary restriction. Similarities and differences in the signalling pathways are discussed, including the role of autophagy, TOR (target of rapamycin), Sir2 (silent information regulator-2), and SnRK1 (sucrose non-fermenting-1-related protein kinase-1).

Limitation of Grassland Productivity by Low Temperature and Seasonality of Growth.

The productivity of temperate grassland is limited by the response of plants to low temperature, affecting winter persistence and seasonal growth rates. During the winter, the growth of perennial grasses is restricted by a combination of low temperature and the lack of available light, but during early spring low ground temperature is the main limiting factor. Once temperature increases, growth is stimulated, resulting in a peak in growth in spring before growth rates decline later in the season. Growth is not primarily limited by the ability to photosynthesize, but controlled by active regulatory processes that, e.g., enable plants to restrict growth and conserve resources for cold acclimation and winter survival. An insufficient ability to cold acclimate can affect winter persistence, thereby also reducing grassland productivity. While some mechanistic knowledge is available that explains how low temperature limits plant growth, the seasonal mechanisms that promote growth in response to increasing spring temperatures but restrict growth later in the season are only partially understood. Here, we assess the available knowledge of the physiological and signaling processes that determine growth, including hormonal effects, on cellular growth and on carbohydrate metabolism. Using data for grass growth in Ireland, we identify environmental factors that limit growth at different times of the year. Ideas are proposed how developmental factors, e.g., epigenetic changes, can lead to seasonality of the growth response to temperature. We also discuss perspectives for modeling grass growth and breeding to improve grassland productivity in a changing climate.

Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicae.

Various microorganisms produce the disaccharide trehalose during their symbiotic and pathogenic interactions with plants. Trehalose has strong effects on plant metabolism and growth; therefore, we became interested to study its possible role in the interaction of Arabidopsis thaliana with Plasmodiophora brassicae, the causal agent of clubroot disease. We found that trehalose accumulated strongly in the infected organs (i.e., the roots and hypocotyls) and, to a lesser extent, in the leaves and stems of infected plants. This accumulation pattern of trehalose correlated with the expression of a putative trehalose-6-phosphate synthase (EC 2.4.1.15) gene from P. brassicae, PbTPS1. Clubroot formation also resulted in an induction of the Arabidopsis trehalase gene, ATTRE1, and in a concomitant increase in trehalase (EC 3.2.1.28) activity in the roots and hypocotyls, but not in the leaves and stems of infected plants. Thus, induction of ATTRE1 expression was probably responsible for the increased trehalase activity. Trehalase activity increased before trehalose accumulated; therefore, it is unlikely that trehalase was induced by its substrate. The induction of trehalase may be part of the plant's defense response and may prevent excess accumulation of trehalose in the plant cells, where it could interfere with the regulation of carbon metabolism.