Light Response Curves in Land Plants.

Light is the driving force for photosynthesis. Two techniques are commonly employed to help characterize the relationship between the light environment and photosynthesis in plants.Chlorophyll a fluorescence analysis is used to examine both the capacity for and the efficiency of the conversion of absorbed light into energy for photosynthesis. Additionally, gas exchange analysis is used to assess the utilization of that energy for carbon fixation. These techniques are used either in isolation or in combination to acquire light response curves that measure the response of the plant to sequential changes in irradiance. Light response curves can help users understand photosynthetic mechanisms, evaluate how plants respond to light conditions, or assess the extent of physiological plasticity within plants. In this chapter, we provide a generalized method for acquiring light response curves suitable for both chlorophyll a fluorescence and gas exchange techniques using commercially available apparatus. Depending on the equipment available, these methods can be applied individually or combined to acquire data simultaneously. The methods are broadly applicable to most land plants but are ideally suited to help those that are unfamiliar with these techniques.

Evolution of endosymbiosis-mediated nuclear calcium signaling in land plants.

The ability of fungi to establish mycorrhizal associations with plants and enhance the acquisition of mineral nutrients stands out as a key feature of terrestrial life. Evidence indicates that arbuscular mycorrhizal (AM) association is a trait present in the common ancestor of land plants,1,2,3,4 suggesting that AM symbiosis was an important adaptation for plants in terrestrial environments.5 The activation of nuclear calcium signaling in roots is essential for AM within flowering plants.6 Given that the earliest land plants lacked roots, whether nuclear calcium signals are required for AM in non-flowering plants is unknown. To address this question, we explored the functional conservation of symbiont-induced nuclear calcium signals between the liverwort Marchantia paleacea and the legume Medicago truncatula. In M. paleacea, AM fungi penetrate the rhizoids and form arbuscules in the thalli.7 Here, we demonstrate that AM germinating spore exudate (GSE) activates nuclear calcium signals in the rhizoids of M. paleacea and that this activation is dependent on the nuclear-localized ion channel DOES NOT MAKE INFECTIONS 1 (MpaDMI1). However, unlike flowering plants, MpaDMI1-mediated calcium signaling is only required for the thalli colonization but not for the AM penetration within rhizoids. We further demonstrate that the mechanism of regulation of DMI1 has diverged between M. paleacea and M. truncatula, including a key amino acid residue essential to sustain DMI1 in an inactive state. Our study reveals functional evolution of nuclear calcium signaling between liverworts and flowering plants and opens new avenues of research into the mechanism of endosymbiosis signaling.

Evolution of immunity networks across embryophytes.

Land plants (embryophytes), including vascular (tracheophytes) and non-vascular plants (bryophytes), co-evolved with microorganisms since descendants of an algal ancestor colonized terrestrial habitats around 500 million years ago. To cope with microbial pathogen infections, embryophytes evolved a complex immune system for pathogen perception and activation of defenses. With the growing number of sequenced genomes and transcriptome datasets from algae, bryophytes, tracheophytes, and available plant models, comparative analyses are increasing our understanding of the evolution of molecular mechanisms underpinning immune responses in different plant lineages. In this review, recent progress on plant immunity networks is highlighted with emphasis on the identification of key components that shaped immunity against pathogens in bryophytes compared to angiosperms during plant evolution.

Reproductive innovations and pulsed rise in plant complexity.

Morphological complexity is a notable feature of multicellular life, although whether it evolves gradually or in early bursts is unclear. Vascular plant reproductive structures, such as flowers, are familiar examples of complex morphology. In this study, we use a simple approach based on the number of part types to analyze changes in complexity over time. We find that reproductive complexity increased in two pulses separated by ~250 million years of stasis, including an initial rise in the Devonian with the radiation of vascular plants and a pronounced increase in the Late Cretaceous that reflects flowering plant diversification. These pulses are associated with innovations that increased functional diversity, suggesting that shifts in complexity are linked to changes in function regardless of whether they occur early or late in the history of vascular plants.

Optimization can provide the fundamental link between leaf photosynthesis, gas exchange and water relations.

Tight coordination in the photosynthetic, gas exchange and water supply capacities of leaves is a globally conserved trend across land plants. Strong selective constraints on leaf carbon gain create the opportunity to use quantitative optimization theory to understand the connected evolution of leaf photosynthesis and water relations. We developed an analytical optimization model that maximizes the long-term rate of leaf carbon gain, given the carbon costs in building and maintaining stomata, leaf hydraulics and osmotic pressure. Our model demonstrates that selection for optimal gain should drive coordination between key photosynthetic, gas exchange and water relations traits. It also provides predictions of adaptation to drought and the relative costs of key leaf functional traits. Our results show that optimization in terms of carbon gain, given the carbon costs of physiological traits, successfully unites leaf photosynthesis and water relations and provides a quantitative framework to consider leaf functional evolution and adaptation.

Origins and Evolution of Cuticle Biosynthetic Machinery in Land Plants.

The aerial epidermis of land plants is covered with a hydrophobic cuticle that protects the plant against environmental stresses. Although the mechanisms of cuticle biosynthesis have been extensively studied in model plants, particularly in seed plants, the origins and evolution of cuticle biosynthesis are not well understood. In this study, we performed a comparative genomic analysis of core components that mediate cuticle biosynthesis and characterized the chemical compositions and physiological parameters of cuticles from a broad set of embryophytes. Phylogenomic analysis revealed that the cuticle biosynthetic machinery originated in the last common ancestor of embryophytes. Coexpansion and coordinated expression are evident in core genes involved in the biosynthesis of two major cuticle components: the polymer cutin and cuticular waxes. Multispecies analyses of cuticle chemistry and physiology further revealed higher loads of both cutin and cuticular waxes in seed plants than in bryophytes as well as greater proportions of dihydroxy and trihydroxy acids, dicarboxylic acids, very-long-chain alkanes, and >C28 lipophilic compounds. This can be associated with land colonization and the formation of cuticles with enhanced hydrophobicity and moisture retention capacity. These findings provide insights into the evolution of plant cuticle biosynthetic mechanisms.

Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts.

Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole-genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomatal function are conserved in Anthoceros and upregulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

Life History Variation as a Model for Understanding Trade-Offs in Plant-Environment Interactions.

All plants must allocate limited resources to survival, growth, and reproduction. In natural species, allocation strategies reflect trade-offs between survivorship risk and subsequent fitness benefits and are therefore central to a species' ecology. Artificial selection on allocation has generated high-yielding crops that often invest the bare minimum in defense or longevity. Ecological, genetic, and evolutionary analyses of plant life history - particularly with respect to longevity and resource allocation along an axis from annual to perennial species - provides a framework to evaluate trade-offs in plant-environment interactions in natural and managed systems. Recent efforts to develop new model plant systems for research and to increase agricultural resilience and efficiency by developing herbaceous perennial crops motivates our critical assessment of traditional assumptions regarding differences between annual and perennial plant species. Here, we review our present understanding of the genetic basis of physiological, developmental, and anatomical differences in wild and crop species and reach two broad conclusions. First, that perenniality and annuality should be considered syndromes comprised of many interacting traits, and that elucidating the genetic basis of these traits is required to assess models of evolution and to develop successful breeding strategies. Modern phenomic and biotechnology tools will facilitate these enquiries. Second, many classic assumptions about the difference between the two syndromes are supported by limited evidence. Throughout this Review, we highlight key knowledge gaps in the proximate and ultimate mechanisms driving life history variation, and suggest empirical approaches to parameterize trade-offs and to make progress in this critical area of direct relevance to ecology and plant performance in a changing world.

A General Model for Seed and Seedling Respiratory Metabolism.

The ontogeny of seed plants usually involves a dormant dehydrated state and the breaking of dormancy and germination, which distinguishes it from that of most organisms. Seed germination and seedling establishment are critical ontogenetic stages in the plant life cycle, and both are fueled by respiratory metabolism. However, the scaling of metabolic rate with respect to individual traits remains poorly understood. Here, we tested metabolic scaling theory during seed germination and early establishment growth using a recently developed model and empirical data collected from 41 species. The results show that (i) the mass-specific respiration rate (Rm) was weakly correlated with body mass, mass-specific N content, and mass-specific C content; (ii) Rm conformed to a single Michaelis-Menten curve as a function of tissue water content; and (iii) the central parameters in the model were highly correlated with DNA content and critical enzyme activities. The model offers new insights and a more integrative scaling theory that quantifies the combined effects of tissue water content and body mass on respiratory metabolism during early plant ontogeny.

Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin.

Genome packaging by nucleosomes is a hallmark of eukaryotes. Histones and the pathways that deposit, remove, and read histone modifications are deeply conserved. Yet, we lack information regarding chromatin landscapes in extant representatives of ancestors of the main groups of eukaryotes, and our knowledge of the evolution of chromatin-related processes is limited. We used the bryophyte Marchantia polymorpha, which diverged from vascular plants circa 400 mya, to obtain a whole chromosome genome assembly and explore the chromatin landscape and three-dimensional genome organization in an early diverging land plant lineage. Based on genomic profiles of ten chromatin marks, we conclude that the relationship between active marks and gene expression is conserved across land plants. In contrast, we observed distinctive features of transposons and other repetitive sequences in Marchantia compared with flowering plants. Silenced transposons and repeats did not accumulate around centromeres. Although a large fraction of constitutive heterochromatin was marked by H3K9 methylation as in flowering plants, a significant proportion of transposons were marked by H3K27me3, which is otherwise dedicated to the transcriptional repression of protein-coding genes in flowering plants. Chromatin compartmentalization analyses of Hi-C data revealed that repressed B compartments were densely decorated with H3K27me3 but not H3K9 or DNA methylation as reported in flowering plants. We conclude that, in early plants, H3K27me3 played an essential role in heterochromatin function, suggesting an ancestral role of this mark in transposon silencing.

Mid-Devonian Archaeopteris Roots Signal Revolutionary Change in Earliest Fossil Forests.

The origin of trees and forests in the Mid Devonian (393-383 Ma) was a turning point in Earth history, marking permanent changes to terrestrial ecology, geochemical cycles, atmospheric CO2 levels, and climate. However, how all these factors interrelate remains largely unknown. From a fossil soil (palaeosol) in the Catskill region near Cairo NY, USA, we report evidence of the oldest forest (mid Givetian) yet identified worldwide. Similar to the famous site at Gilboa, NY, we find treefern-like Eospermatopteris (Cladoxylopsida). However, the environment at Cairo appears to have been periodically drier. Along with a single enigmatic root system potentially belonging to a very early rhizomorphic lycopsid, we see spectacularly extensive root systems here assigned to the lignophyte group containing the genus Archaeopteris. This group appears pivotal to the subsequent evolutionary history of forests due to possession of multiple advanced features and likely relationship to subsequently dominant seed plants. Here we show that Archaeopteris had a highly advanced root system essentially comparable to modern seed plants. This suggests a unique ecological role for the group involving greatly expanded energy and resource utilization, with consequent influence on global processes much greater than expected from tree size or rooting depth alone.

A ligand-independent origin of abscisic acid perception.

Land plants are considered monophyletic, descending from a single successful colonization of land by an aquatic algal ancestor. The ability to survive dehydration to the point of desiccation is a key adaptive trait enabling terrestrialization. In extant land plants, desiccation tolerance depends on the action of the hormone abscisic acid (ABA) that acts through a receptor-signal transduction pathway comprising a PYRABACTIN RESISTANCE 1-like (PYL)-PROTEIN PHOSPHATASE 2C (PP2C)-SNF1-RELATED PROTEIN KINASE 2 (SnRK2) module. Early-diverging aeroterrestrial algae mount a dehydration response that is similar to that of land plants, but that does not depend on ABA: Although ABA synthesis is widespread among algal species, ABA-dependent responses are not detected, and algae lack an ABA-binding PYL homolog. This raises the key question of how ABA signaling arose in the earliest land plants. Here, we systematically characterized ABA receptor-like proteins from major land plant lineages, including a protein found in the algal sister lineage of land plants. We found that the algal PYL-homolog encoded by Zygnema circumcarinatum has basal, ligand-independent activity of PP2C repression, suggesting this to be an ancestral function. Similarly, a liverwort receptor possesses basal activity, but it is further activated by ABA. We propose that co-option of ABA to control a preexisting PP2C-SnRK2-dependent desiccation-tolerance pathway enabled transition from an all-or-nothing survival strategy to a hormone-modulated, competitive strategy by enabling continued growth of anatomically diversifying vascular plants in dehydrative conditions, enabling them to exploit their new environment more efficiently.

Posture control in land plants: growth, position sensing, proprioception, balance, and elasticity.

The colonization of the atmosphere by land plants was a major evolutionary step. The mechanisms that allow for vertical growth through air and the establishment and control of a stable erect habit are just starting to be understood. A key mechanism was found to be continuous posture control to counterbalance the mechanical and developmental challenges of maintaining a growing upright structure. An interdisciplinary systems biology approach was invaluable in understanding the underlying principles and in designing pertinent experiments. Since this discovery previously held views of gravitropic perception had to be reexamined and this has led to the description of proprioception in plants. In this review, we take a purposefully pedagogical approach to present the dynamics involved from the cellular to whole-plant level. We show how the textbook model of how plants sense gravitational force has been replaced by a model of position sensing, a clinometer mechanism that involves both passive avalanches and active motion of statoliths, granular starch-filled plastids, in statocytes. Moreover, there is a transmission of information between statocytes and other specialized cells that sense the degree of organ curvature and reset asymmetric growth to straighten and realign the structure. We give an overview of how plants have used the interplay of active posture control and elastic sagging to generate a whole range of spatial displays during their life cycles. Finally, a position-integrating mechanism has been discovered that prevents directional plant growth from being disrupted by wind-induced oscillations.

Is Amphistomy an Adaptation to High Light? Optimality Models of Stomatal Traits along Light Gradients.

Stomata regulate the supply of CO2 for photosynthesis and the rate of water loss out of the leaf. The presence of stomata on both leaf surfaces, termed amphistomy, increases photosynthetic rate, is common in plants from high light habitats, and rare otherwise. In this study I use optimality models based on leaf energy budget and photosynthetic models to ask why amphistomy is common in high light habitats. I developed an R package leafoptimizer to solve for stomatal traits that optimally balance carbon gain with water loss in a given environment. The model predicts that amphistomy is common in high light because its marginal effect on carbon gain is greater than in the shade, but only if the costs of amphistomy are also lower under high light than in the shade. More generally, covariation between costs and benefits may explain why stomatal and other traits form discrete phenotypic clusters.

Review: ABA, flavonols, and the evolvability of land plants.

There is evidence that the ABA signaling pathway has greatly contributed to increase the complexity of land plants, thereby sustaining their ability to adapt in an ever-changing environment. The regulatory functions of the ABA signaling pathway go well beyond the movements of stomata and the dormancy of seeds. For instance, the ABA signaling regulates the flavonoid biosynthesis, consistent with the high integration of ABA and light signaling pathways, which occurs at the level of key signaling components, such as the bZIP transcription factors HY5 and ABI5. Here we focus on the regulation of 'colorless' (UV-absorbing) flavonol biosynthesis by the ABA signaling and, about how flavonols may regulate, in turn, the ABA signaling network. We discuss very recent findings that quercetin regulates the ABA signaling pathway, and hypothesize this might occur at the level of second messenger and perhaps of primary signaling components as well. We critically review old and recent suggestions of the primary roles played by flavonols, the ancient class of flavonoids already present in bryophytes, in the evolution of terrestrial plants. Our reasoning strongly supports the view that the ABA-flavonol relationship may represent a robust trait of land plants, and might have contributed to their adaptation on land.

Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land.

Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3'-phosphoadenosine-5'-phosphate (PAP) metabolism, evolved in streptophyte algae-the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii, and the moss Physcomitrella patens Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these diverse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.

Importance of the vegetation-groundwater-stream continuum to understand transformation of biogenic carbon in aquatic systems - A case study based on a pine-maize comparison in a lowland sandy watershed (Landes de Gascogne, SW France).

During land-aquatic transfer, carbon (C) and inorganic nutrients (IN) are transformed in soils, groundwater, and at the groundwater-surface water interface as well as in stream channels and stream sediments. However, processes and factors controlling these transfers and transformations are not well constrained, particularly with respect to land use effect. We compared C and IN concentrations in shallow groundwater and first-order streams of a sandy lowland catchment dominated by two types of land use: pine forest and maize cropland. Contrary to forest groundwater, crop groundwater exhibited oxic conditions all-year round as a result of higher evapotranspiration and better lateral drainage that decreased the water table below the organic-rich soil horizon, prevented the leaching of soil-generated dissolved organic carbon (DOC) in groundwater, and thus limited consumption of dissolved oxygen (O2). In crop groundwater, oxic conditions inhibited denitrification and methanogenesis resulting in high nitrate (NO3-; on average 1140 ±â€¯485 µmol L-1) and low methane (CH4; 40 ±â€¯25 nmol L-1) concentrations. Conversely, anoxic conditions in forest groundwater led to lower NO3- (25 ±â€¯40 µmol L-1) and higher CH4 (1770 ±â€¯1830 nmol L-1) concentrations. The partial pressure of carbon dioxide (pCO2; 30,650 ±â€¯11,590 ppmv) in crop groundwater was significantly lower than in forest groundwater (50,630 ±â€¯26,070 ppmv), and was apparently caused by the deeper water table delaying downward diffusion of soil CO2 to the water table. In contrast, pCO2 was not significantly different in crop (4480 ±â€¯2680 ppmv) and forest (4900 ±â€¯4500 ppmv) streams, suggesting faster degassing in forest streams resulting from greater water turbulence. Although NO3-concentrations indicated that denitrification occurred in riparian-forest groundwater, crop streams nevertheless exhibited important signs of spring and summer eutrophication such as the development of macrophytes. Stream eutrophication favored development of anaerobic conditions in crop stream sediments, as evidenced by increased ammonia (NH4+) and CH4 in stream waters and concomitant decreased in NO3- concentrations as a result of sediment denitrification. In crop streams, dredging and erosion of streambed sediments during winter sustained high concentration of particulate organic C, NH4+ and CH4. In forest streams, dissolved iron (Fe2+), NH4+ and CH4 were negatively correlated with O2 reflecting the gradual oxygenation of stream water and associated oxidations of Fe2+, NH4+ and CH4. The results overall showed that forest groundwater behaved as source of CO2 and CH4 to streams, the intensity depending on the hydrological connectivity among soils, groundwater, and streams. CH4 production was prevented in cropland in soils and groundwater, however crop groundwater acted as a source of CO2 to streams (but less so than forest groundwater). Conversely, in streams, pCO2 was not significantly affected by land use while CH4 production was enhanced by cropland. At the catchment scale, this study found substantial biogeochemical heterogeneity in C and IN concentrations between forest and crop waters, demonstrating the importance of including the full vegetation-groundwater-stream continuum when estimating land-water fluxes of C (and nitrogen) and attempting to understand their spatial and temporal dynamics.

Turning down the heat: An enhanced understanding of the relationship between urban vegetation and surface temperature at the city scale.

Guiding urban planners on the cooling returns of different configurations of urban vegetation is important to protect urban dwellers from adverse heat impacts. To this end, we estimated statistical models that fused multi-temporal very fine spatial (20 cm) and vertical (1 mm) resolution imagery, that captures the complexity of urban vegetation, with remotely sensed temperature data to assess how urban vegetation configuration influences urban temperatures. Perth, Western Australia, was used as a case-study for this analysis. Panel regression models showed that within a location an increase in tree and shrub cover has a larger cooling effect than grass coverage. On average, holding all else equal, an approximate 1 km2 increase in shrub (tree) cover within a location reduces surface temperatures by 12 °C (5 °C). We included a range of robustness checks for the observed relationships between urban vegetation type and temperature. Geographically weighted regression models showed spatial variation in the cooling effect of different vegetation types; this indicates that i) unobserved factors moderate temperature-vegetation relationships across urban landscapes, and ii) that urban vegetation type and temperature relationships are complex. Machine learning models (Random Forests) were used to further explore complex and non-linear relationships between different urban vegetation configurations and temperature. The Random Forests showed that vegetation type explained 31.84% of the out-of-bag variance in summer surface temperatures, that increased cover of large vegetation within a location increases cooling, and that different configurations of urban vegetation structure can lead to cooling gains. The models in this study were trained with vegetation data capturing local detail, multiple time-periods, and entire city coverage. Thus, these models illustrate the potential to develop locally-detailed and spatially explicit tools to guide planning of vegetation configuration to optimise cooling at local- and city-scales.

Mechanistic basis for the evolution of chalcone synthase catalytic cysteine reactivity in land plants.

Flavonoids are important polyphenolic natural products, ubiquitous in land plants, that play diverse functions in plants' survival in their ecological niches, including UV protection, pigmentation for attracting pollinators, symbiotic nitrogen fixation, and defense against herbivores. Chalcone synthase (CHS) catalyzes the first committed step in plant flavonoid biosynthesis and is highly conserved in all land plants. In several previously reported crystal structures of CHSs from flowering plants, the catalytic cysteine is oxidized to sulfinic acid, indicating enhanced nucleophilicity in this residue associated with its increased susceptibility to oxidation. In this study, we report a set of new crystal structures of CHSs representing all five major lineages of land plants (bryophytes, lycophytes, monilophytes, gymnosperms, and angiosperms), spanning 500 million years of evolution. We reveal that the structures of CHS from a lycophyte and a moss species preserve the catalytic cysteine in a reduced state, in contrast to the cysteine sulfinic acid seen in all euphyllophyte CHS structures. In vivo complementation, in vitro biochemical and mutagenesis analyses, and molecular dynamics simulations identified a set of residues that differ between basal-plant and euphyllophyte CHSs and modulate catalytic cysteine reactivity. We propose that the CHS active-site environment has evolved in euphyllophytes to further enhance the nucleophilicity of the catalytic cysteine since the divergence of euphyllophytes from other vascular plant lineages 400 million years ago. These changes in CHS could have contributed to the diversification of flavonoid biosynthesis in euphyllophytes, which in turn contributed to their dominance in terrestrial ecosystems.