Botanic Gardens and Parks Authority

Here, the coevolution of mycorrhizal fungi and roots is assessed in the light of evidence now available, from palaeobotanical and morphological studies and the analysis of DNA-based phylogenies. The first bryophyte-like land plants, in the early Devonian (400 million years ago), had endophytic associations resembling vesicular-arbuscular mycorrhizas (VAM) even before roots evolved. Mycorrhizal evolution would have progressed from endophytic hyphae towards balanced associations where partners were interdependent due to the exchange of limiting energy and nutrient resources. Most mycorrhizas are mutualistic, but in some cases the trend for increasing plant control of fungi culminates in the exploitative mycorrhizas of achlorophyllous, mycoheterotrophic plants. Ectomycorrhizal, ericoid and orchid mycorrhizas, as well as nonmycorrhizal roots, evolved during the period of rapid angiosperm radiation in the Cretaceous. It is hypothesised that roots gradually evolved from rhizomes to provide more suitable habitats for mycorrhizal fungi and provide plants with complex branching and leaves with water and nutrients. Selection pressures have caused the morphological divergence of roots with different types of mycorrizas. Root cortex thickness and exodermis suberization are greatest in obllgately mycorrhizal plants, while nonmycorrhizal plants tend to have fine roots, with more roots hairs and relatively advanced chemical defences. Major coevolutionary trends and the relative success of plants with different root types are discussed. Contents Summary 275 I. Introduction 276 II. Mycorrhizal Fungi 276 III. The Dawn of Mycorrhizas 279 IV. Mycorrhizal Associations of Living and Extinct Plants 282 V. Evolution of Roots 288 VI. The Root as a Habitat for Fungi 290 VII. Mycorrhizal Evolution Trends 295 Acknowledgements 298 References 298.

At the core of plant regeneration, temperature and water supply are critical drivers for seed dormancy (initiation, break) and germination. Hence, global climate change is altering these environmental cues and will preclude, delay, or enhance regeneration from seeds, as already documented in some cases. Along with compromised seedling emergence and vigour, shifts in germination phenology will influence population dynamics, and thus, species composition and diversity of communities. Altered seed maturation (including consequences for dispersal) and seed mass will have ramifications on life history traits of plants. Predicted changes in temperature and precipitation, and thus in soil moisture, will affect many components of seed persistence in soil, e.g. seed longevity, dormancy release and germination, and soil pathogen activity. More/less equitable climate will alter geographic distribution for species, but restricted migratory capacity in some will greatly limit their response. Seed traits for weedy species could evolve relatively quickly to keep pace with climate change enhancing their negative environmental and economic impact. Thus, increased research in understudied ecosystems, on key issues related to seed ecology, and on evolution of seed traits in nonweedy species is needed to more fully comprehend and plan for plant responses to global warming.

▪ Abstract Like South Africa's Greater Cape Floristic Region, the Southwest Australian Floristic Region (SWAFR) is species rich, with a Mediterranean climate and old, weathered, nutrient-deficient landscapes. This region has 7380 native vascular plants (species/subspecies): one third described since 1970, 49% endemic, and 2500 of conservation concern. Origins are complex. Molecular phylogenies suggest multiple dispersal events into, out of, and within the SWAFR throughout the Cretaceous and Cenozoic; in many phylogenetically unrelated clades; and from many directions. Either explosive speciation or steady cladogenesis occurred among some woody sclerophyll and herbaceous families from the mid-Tertiary in response to progressive aridity. Genomic coalescence was sometimes involved. Rainforest taxa went extinct by the Pleistocene. Old lineages nevertheless persist as one endemic order (Dasypogonales) and 6–11 endemic families. Such a rich flora on old landscapes that have been exposed to European land-use practices is highly threatened. Conservation programs must minimize soil removal and use local germplasm in restoration programs.

BACKGROUND: Conservation through reserves alone is now considered unlikely to achieve protection of plant species necessary to mitigate direct losses of habitat and the pervasive impact of global climate change. Assisted translocation/migration represent new challenges in the face of climate change; species, particularly orchids, will need artificial assistance to migrate from hostile environments, across ecological barriers (alienated lands such as farmlands and built infrastructure) to new climatically buffered sites. The technology and science to underpin assisted migration concepts are in their infancy for plants in general, and orchids, with their high degree of rarity, represent a particularly challenging group for which these principles need to be developed. It is likely that orchids, more than any other plant family, will be in the front-line of species to suffer large-scale extinction events as a result of climate change. SCOPE: The South West Australian Floristic Region (SWAFR) is the only global biodiversity hotspot in Australia and represents an ideal test-bed for development of orchid conservation principles. Orchids comprise 6 % of all threatened vascular plants in the SWAFR, with 76 out of the 407 species known for the region having a high level of conservation risk. The situation in the SWAFR is a portent of the global crisis in terrestrial orchid conservation, and it is a region where innovative conservation solutions will be required if the impending wave of extinction is to be averted. Major threatening processes are varied, and include land clearance, salinity, burning, weed encroachment, disease and pests. This is compounded by highly specialized pollinators (locally endemic native invertebrates) and, in the most threatened groups such as hammer orchids (Drakaea) and spider orchids (Caladenia), high levels of mycorrhizal specialization. Management and development of effective conservation strategies for SWAFR orchids require a wide range of integrated scientific approaches to mitigate impacts that directly influence ecological traits critical for survival. CONCLUSIONS: In response to threats to orchid species, integrated conservation approaches have been adopted (including ex situ and translocation principles) in the SWAFR with the result that a significant, multidisciplinary approach is under development to facilitate conservation of some of the most threatened taxa and build expertise to carry out assisted migration to new sites. Here the past two decades of orchid conservation research in the SWAFR and the role of research-based approaches for managing effective orchid conservation in a global biodiversity hotspot are reviewed.

Exposure of seeds to aerosol smoke or crude smoke extracts stimulates the germination of a number of fire-dependent and fire-independent plant species. We now report the identity of a germination-promoting compound present in plant- and cellulose-derived smoke. The structure of this compound, deduced from spectroscopic analysis and confirmed by synthesis, was shown to be that of the butenolide 3-methyl-2 H -furo[2,3- c ]pyran-2-one ( 1 ). Here we show that 1 promotes germination of a number of plant species at a level similar to that observed with plant-derived smoke water.

Coevolutionary interactions are thought to have spurred the evolution of key innovations and driven the diversification of much of life on Earth. However, the genetic and evolutionary basis of the innovations that facilitate such interactions remains poorly understood. We examined the coevolutionary interactions between plants (Brassicales) and butterflies (Pieridae), and uncovered evidence for an escalating evolutionary arms-race. Although gradual changes in trait complexity appear to have been facilitated by allelic turnover, key innovations are associated with gene and genome duplications. Furthermore, we show that the origins of both chemical defenses and of molecular counter adaptations were associated with shifts in diversification rates during the arms-race. These findings provide an important connection between the origins of biodiversity, coevolution, and the role of gene and genome duplications as a substrate for novel traits.

Karrikins are butenolides derived from burnt vegetation that stimulate seed germination and enhance seedling responses to light. Strigolactones are endogenous butenolide hormones that regulate shoot and root architecture, and stimulate the branching of arbuscular mycorrhizal fungi. Thus, karrikins and strigolactones are structurally similar but physiologically distinct plant growth regulators. In Arabidopsis thaliana, responses to both classes of butenolides require the F-box protein MAX2, but it remains unclear how discrete responses to karrikins and strigolactones are achieved. In rice, the DWARF14 protein is required for strigolactone-dependent inhibition of shoot branching. Here, we show that the Arabidopsis DWARF14 orthologue, AtD14, is also necessary for normal strigolactone responses in seedlings and adult plants. However, the AtD14 paralogue KARRIKIN INSENSITIVE 2 (KAI2) is specifically required for responses to karrikins, and not to strigolactones. Phylogenetic analysis indicates that KAI2 is ancestral and that AtD14 functional specialisation has evolved subsequently. Atd14 and kai2 mutants exhibit distinct subsets of max2 phenotypes, and expression patterns of AtD14 and KAI2 are consistent with the capacity to respond to either strigolactones or karrikins at different stages of plant development. We propose that AtD14 and KAI2 define a class of proteins that permit the separate regulation of karrikin and strigolactone signalling by MAX2. Our results support the existence of an endogenous, butenolide-based signalling mechanism that is distinct from the strigolactone pathway, providing a molecular basis for the adaptive response of plants to smoke.

Simultaneous environmental changes challenge biodiversity persistence and human wellbeing. The science and practice of restoration ecology, in collaboration with other disciplines, can contribute to overcoming these challenges. This endeavor requires a solid conceptual foundation based in empirical research which confronts, tests and influences theoretical developments. We review conceptual developments in restoration ecology over the last 30 years. We frame our review in the context of changing restoration goals which reflect increased societal awareness of the scale of environmental degradation and the recognition that inter‐disciplinary approaches are needed to tackle environmental problems. Restoration ecology now encompasses facilitative interactions and network dynamics, trophic cascades, and above‐ and belowground linkages. It operates in a non‐equilibrium, alternative states framework, at the landscape scale, and in response to changing environmental, economic and social conditions. Progress has been marked by conceptual advances in the fields of trait‐environment relationships, community assembly, and understanding the links between biodiversity and ecosystem functioning. Conceptual and practical advances have been enhanced by applying evolving technologies, including treatments to increase seed germination and overcome recruitment bottlenecks, high throughput DNA sequencing to elucidate soil community structure and function, and advances in satellite technology and GPS tracking to monitor habitat use. The synthesis of these technologies with systematic reviews of context dependencies in restoration success, model based analyses and consideration of complex socio‐ecological systems will allow generalizations to inform evidence based interventions. Ongoing challenges include setting realistic, socially acceptable goals for restoration under changing environmental conditions, and prioritizing actions in an increasingly space‐competitive world. Ethical questions also surround the use of genetically modified material, translocations, taxon substitutions, and de‐extinction, in restoration ecology. Addressing these issues, as the Ecological Society of America looks to its next century, will require current and future generations of researchers and practitioners, including economists, engineers, philosophers, landscape architects, social scientists and restoration ecologists, to work together with communities and governments to rise to the environmental challenges of the coming decades.

Accumulating evidence highlights increased mortality risks for trees during severe drought, particularly under warmer temperatures and increasing vapour pressure deficit (VPD). Resulting forest die-off events have severe consequences for ecosystem services, biophysical and biogeochemical land-atmosphere processes. Despite advances in monitoring, modelling and experimental studies of the causes and consequences of tree death from individual tree to ecosystem and global scale, a general mechanistic understanding and realistic predictions of drought mortality under future climate conditions are still lacking. We update a global tree mortality map and present a roadmap to a more holistic understanding of forest mortality across scales. We highlight priority research frontiers that promote: (1) new avenues for research on key tree ecophysiological responses to drought; (2) scaling from the tree/plot level to the ecosystem and region; (3) improvements of mortality risk predictions based on both empirical and mechanistic insights; and (4) a global monitoring network of forest mortality. In light of recent and anticipated large forest die-off events such a research agenda is timely and needed to achieve scientific understanding for realistic predictions of drought-induced tree mortality. The implementation of a sustainable network will require support by stakeholders and political authorities at the international level.

Seed persistence is the survival of seeds in the environment once they have reached maturity. Seed persistence allows a species, population or genotype to survive long after the death of parent plants, thus distributing genetic diversity through time. The ability to predict seed persistence accurately is critical to inform long-term weed management and flora rehabilitation programs, as well as to allow a greater understanding of plant community dynamics. Indeed, each of the 420000 seed-bearing plant species has a unique set of seed characteristics that determine its propensity to develop a persistent soil seed bank. The duration of seed persistence varies among species and populations, and depends on the physical and physiological characteristics of seeds and how they are affected by the biotic and abiotic environment. An integrated understanding of the ecophysiological mechanisms of seed persistence is essential if we are to improve our ability to predict how long seeds can survive in soils, both now and under future climatic conditions. In this review we present an holistic overview of the seed, species, climate, soil, and other site factors that contribute mechanistically to seed persistence, incorporating physiological, biochemical and ecological perspectives. We focus on current knowledge of the seed and species traits that influence seed longevity under ex situ controlled storage conditions, and explore how this inherent longevity is moderated by changeable biotic and abiotic conditions in situ, both before and after seeds are dispersed. We argue that the persistence of a given seed population in any environment depends on its resistance to exiting the seed bank via germination or death, and on its exposure to environmental conditions that are conducive to those fates. By synthesising knowledge of how the environment affects seeds to determine when and how they leave the soil seed bank into a resistance-exposure model, we provide a new framework for developing experimental and modelling approaches to predict how long seeds will persist in a range of environments.

Smoke is an important abiotic cue for plant regeneration in postfire landscapes. Karrikins are a class of compounds discovered in smoke that promote seed germination and influence early development of many plants by an unknown mechanism. A genetic screen for karrikin-insensitive mutants in Arabidopsis thaliana revealed that karrikin signaling requires the F-box protein MAX2, which also mediates responses to the structurally-related strigolactone family of phytohormones. Karrikins and the synthetic strigolactone GR24 trigger similar effects on seed germination, seedling photomorphogenesis, and expression of a small set of genes during these developmental stages. Karrikins also repress MAX4 and IAA1 transcripts, which show negative feedback regulation by strigolactone. We demonstrate that all of these common responses are abolished in max2 mutants. Unlike strigolactones, however, karrikins do not inhibit shoot branching in Arabidopsis or pea, indicating that plants can distinguish between these signals. These results suggest that a MAX2-dependent signal transduction mechanism was adapted to mediate responses to two chemical cues with distinct roles in plant ecology and development.

Gaps in knowledge must be identified, capacities developed, and research translated into policy and practice.

Seed banks must shift from being “stamp-collections” of species to collections that can provide tons of seeds and the expertise to improve restoration efforts.

BACKGROUND: Seedling recruitment is essential to the sustainability of any plant population. Due to the minute nature of seeds and early-stage seedlings, orchid germination in situ was for a long time practically impossible to observe, creating an obstacle towards understanding seedling site requirements and fluctuations in orchid populations. The introduction of seed packet techniques for sowing and retrieval in natural sites has brought with it important insights, but many aspects of orchid seed and germination biology remain largely unexplored. KEY CONSIDERATIONS: The germination niche for orchids is extremely complex, because it is defined by requirements not only for seed lodging and germination, but also for presence of a fungal host and its substrate. A mycobiont that the seedling can parasitize is considered an essential element, and a great diversity of Basidiomycota and Ascomycota have now been identified for their role in orchid seed germination, with fungi identifiable as imperfect Rhizoctonia species predominating. Specificity patterns vary from orchid species employing a single fungal lineage to species associating individually with a limited selection of distantly related fungi. A suitable organic carbon source for the mycobiont constitutes another key requirement. Orchid germination also relies on factors that generally influence the success of plant seeds, both abiotic, such as light/shade, moisture, substrate chemistry and texture, and biotic, such as competitors and antagonists. Complexity is furthermore increased when these factors influence seeds/seedling, fungi and fungal substrate differentially. CONCLUSIONS: A better understanding of germination and seedling establishment is needed for conservation of orchid populations. Due to the obligate association with a mycobiont, the germination niches in orchid species are extremely complex and varied. Microsites suitable for germination can be small and transient, and direct observation is difficult. An experimental approach using several levels of environmental manipulation/control is recommended.

One of the most cited papers in arbuscular mycorrhizal (AM) research was published by Phillips and Hayman in 1970 describing an easy standard method to stain AM fungi (AMF) in roots. Since then, a number of other methods (destructive–non‐destructive; vital–non‐vital) on how to visualize AMF in roots have been published. Our review provides an overview on present techniques used to visualize AMF in roots and gives recommendations on their use. We hope that the present review will help the readers to choose an appropriate method to visualize AMF in roots for their specific experimental set‐up.

Discovery of the primary seed germination stimulant in smoke, 3-methyl-2H-furo[2,3-c]pyran-2-one (KAR1), has resulted in identification of a family of structurally related plant growth regulators, karrikins. KAR1 acts as a key germination trigger for many species from fire-prone, Mediterranean climates, but a molecular mechanism for this response remains unknown. We demonstrate that Arabidopsis (Arabidopsis thaliana), an ephemeral of the temperate northern hemisphere that has never, to our knowledge, been reported to be responsive to fire or smoke, rapidly and sensitively perceives karrikins. Thus, these signaling molecules may have greater significance among angiosperms than previously realized. Karrikins can trigger germination of primary dormant Arabidopsis seeds far more effectively than known phytohormones or the structurally related strigolactone GR-24. Natural variation and depth of seed dormancy affect the degree of KAR1 stimulation. Analysis of phytohormone mutant germination reveals suppression of KAR1 responses by abscisic acid and a requirement for gibberellin (GA) synthesis. The reduced germination of sleepy1 mutants is partially recovered by KAR1, which suggests that germination enhancement by karrikin is only partly DELLA dependent. While KAR1 has little effect on sensitivity to exogenous GA, it enhances expression of the GA biosynthetic genes GA3ox1 and GA3ox2 during seed imbibition. Neither abscisic acid nor GA levels in seed are appreciably affected by KAR1 treatment prior to radicle emergence, despite marked differences in germination outcome. KAR1 stimulation of Arabidopsis germination is light-dependent and reversible by far-red exposure, although limited induction of GA3ox1 still occurs in the dark. The observed requirements for light and GA biosynthesis provide the first insights into the karrikin mode of action.

Two α/β-fold hydrolases, KARRIKIN INSENSITIVE2 (KAI2) and Arabidopsis thaliana DWARF14 (AtD14), are necessary for responses to karrikins (KARs) and strigolactones (SLs) in Arabidopsis (Arabidopsis thaliana). Although KAI2 mediates responses to KARs and some SL analogs, AtD14 mediates SL but not KAR responses. To further determine the specificity of these proteins, we assessed the ability of naturally occurring deoxystrigolactones to inhibit Arabidopsis hypocotyl elongation, regulate seedling gene expression, suppress outgrowth of secondary inflorescences, and promote seed germination. Neither 5-deoxystrigol nor 4-deoxyorobanchol was active in KAI2-dependent seed germination or hypocotyl elongation, but both were active in AtD14-dependent hypocotyl elongation and secondary shoot growth. However, the nonnatural enantiomer of 5-deoxystrigol was active through KAI2 in growth and gene expression assays. We found that the four stereoisomers of the SL analog GR24 had similar activities to their deoxystrigolactone counterparts. The results suggest that AtD14 and KAI2 exhibit selectivity to the butenolide D ring in the 2'R and 2'S configurations, respectively. However, we found, for nitrile-debranone (CN-debranone, a simple SL analog), that the 2'R configuration is inactive but that the 2'S configuration is active through both AtD14 and KAI2. Our results support the conclusion that KAI2-dependent signaling does not respond to canonical SLs. Furthermore, racemic mixtures of chemically synthesized SLs and their analogs, such as GR24, should be used with caution because they can activate responses that are not specific to naturally occurring SLs. In contrast, the use of specific stereoisomers might provide valuable information about the specific perception systems operating in different plant tissues, parasitic weed seeds, and arbuscular mycorrhizae.

It is well known that burning of vegetation stimulates new plant growth and landscape regeneration. The discovery that char and smoke from such fires promote seed germination in many species indicates the presence of chemical stimulants. Nitrogen oxides stimulate seed germination, but their importance in post-fire germination has been questioned. Cyanohydrins have been recently identified in aqueous smoke solutions and shown to stimulate germination of some species through the slow release of cyanide. However, the most information is available for karrikins, a family of butenolides related to 3-methyl-2H-furo[2,3-c]pyran-2-one. Karrikins stimulate seed germination and influence seedling growth. They are active in species not normally associated with fire, and in Arabidopsis they require the F-box protein MAX2, which also controls responses to strigolactone hormones. We hypothesize that chemical similarity between karrikins and strigolactones provided the opportunity for plants to employ a common signal transduction pathway to respond to both types of compound, while tailoring specific developmental responses to these distinct environmental signals.

Extreme climatic events can trigger abrupt and often lasting change in ecosystems via the reduction or elimination of foundation (i.e., habitat-forming) species. However, while the frequency/intensity of extreme events is predicted to increase under climate change, the impact of these events on many foundation species and the ecosystems they support remains poorly understood. Here, we use the iconic seagrass meadows of Shark Bay, Western Australia--a relatively pristine subtropical embayment whose dominant, canopy-forming seagrass, Amphibolis antarctica, is a temperate species growing near its low-latitude range limit--as a model system to investigate the impacts of extreme temperatures on ecosystems supported by thermally sensitive foundation species in a changing climate. Following an unprecedented marine heat wave in late summer 2010/11, A. antarctica experienced catastrophic (>90%) dieback in several regions of Shark Bay. Animal-borne video footage taken from the perspective of resident, seagrass-associated megafauna (sea turtles) revealed severe habitat degradation after the event compared with a decade earlier. This reduction in habitat quality corresponded with a decline in the health status of largely herbivorous green turtles (Chelonia mydas) in the 2 years following the heat wave, providing evidence of long-term, community-level impacts of the event. Based on these findings, and similar examples from diverse ecosystems, we argue that a generalized framework for assessing the vulnerability of ecosystems to abrupt change associated with the loss of foundation species is needed to accurately predict ecosystem trajectories in a changing climate. This includes seagrass meadows, which have received relatively little attention in this context. Novel research and monitoring methods, such as the analysis of habitat and environmental data from animal-borne video and data-logging systems, can make an important contribution to this framework.

• The mapping of functional traits onto chronograms is an emerging approach for the identification of how agents of natural selection have shaped the evolution of organisms. Recent research has reported fire-dependent traits appearing among flowering plants from 60 million yr ago (Ma). Although there are many records of fossil charcoal in the Cretaceous (65-145 Ma), evidence of fire-dependent traits evolving in that period is lacking. • We link the evolutionary trajectories for five fire-adapted traits in Pinaceae with paleoatmospheric conditions over the last 250 million yr to determine the time at which fire originated as a selective force in trait evolution among seed plants. • Fire-protective thick bark originated in Pinus c. 126 Ma in association with low-intensity surface fires. More intense crown fires emerged c. 89 Ma coincident with thicker bark and branch shedding, or serotiny with branch retention as an alternative strategy. These innovations appeared at the same time as the Earth's paleoatmosphere experienced elevated oxygen levels that led to high burn probabilities during the mid-Cretaceous. • The fiery environments of the Cretaceous strongly influenced trait evolution in Pinus. Our evidence for a strong correlation between the evolution of fire-response strategies and changes in fire regime 90-125 Ma greatly backdates the key role that fire has played in the evolution of seed plants.