Light- and hormone-mediated development in non-flowering plants: An overview.

MAIN CONCLUSION: Light, hormones and their interaction regulate different aspects of development in non-flowering plants. They might have played a role in the evolution of different plant groups by conferring specific adaptive evolutionary changes. Plants are sessile organisms. Unlike animals, they lack the opportunity to abandon their habitat in unfavorable conditions. They respond to different environmental cues and adapt accordingly to control their growth and developmental pattern. While phytohormones are known to be internal regulators of plant development, light is a major environmental signal that shapes plant processes. It is plausible that light-hormone crosstalk might have played an important role in plant evolution. But how the crosstalk between light and phytohormone signaling pathways might have shaped the plant evolution is unclear. One of the possible reasons is that flowering plants have been studied extensively in context of plant development, which cannot serve the purpose of evolutionary comparisons. In order to elucidate the role of light, hormone and their crosstalk in the evolutionary adaptation in plant kingdom, one needs to understand various light- and hormone-mediated processes in diverse non-flowering plants. This review is an attempt to outline major light- and phytohormone-mediated responses in non-flowering plant groups such as algae, bryophytes, pteridophytes and gymnosperms.

Low assimilation efficiency of photorespiratory ammonia in conifer leaves.

Glutamine synthetase (GS) localized in the chloroplasts, GS2, is a key enzyme in the assimilation of ammonia (NH3) produced from the photorespiration pathway in angiosperms, but it is absent from some coniferous species belonging to Pinaceae such as Pinus. We examined whether the absence of GS2 is common in conifers (Pinidae) and also addressed the question of whether assimilation efficiency of photorespiratory NH3 differs between conifers that may potentially lack GS2 and angiosperms. Search of the expressed sequence tag database of Cryptomeria japonica, a conifer in Cupressaceae, and immunoblotting analyses of leaf GS proteins of 13 species from all family members in Pinidae revealed that all tested conifers exhibited only GS1 isoforms. We compared leaf NH3 compensation point (γNH3) and the increments in leaf ammonium content per unit photorespiratory activity (NH3 leakiness), i.e. inverse measures of the assimilation efficiency, between conifers (C. japonica and Pinus densiflora) and angiosperms (Phaseolus vulgaris and two Populus species). Both γNH3 and NH3 leakiness were higher in the two conifers than in the three angiosperms tested. Thus, we concluded that the absence of GS2 is common in conifers, and assimilation efficiency of photorespiratory NH3 is intrinsically lower in conifer leaves than in angiosperm leaves. These results imply that acquisition of GS2 in land plants is an adaptive mechanism for efficient NH3 assimilation under photorespiratory environments.

Hornwort stomata do not respond actively to exogenous and environmental cues.

Backgrounds and Aims: Because stomata in bryophytes occur on sporangia, they are subject to different developmental and evolutionary constraints from those on leaves of tracheophytes. No conclusive experimental evidence exists on the responses of hornwort stomata to exogenous stimulation. Methods: Responses of hornwort stomata to abscisic acid (ABA), desiccation, darkness and plasmolysis were compared with those in tracheophyte leaves. Potassium ion concentrations in the guard cells and adjacent cells were analysed by X-ray microanalysis, and the ontogeny of the sporophytic intercellular spaces was compared with those of tracheophytes by cryo-scanning electron microscopy. Key Results: The apertures in hornwort stomata open early in development and thereafter remain open. In hornworts, the experimental treatments, based on measurements of >9000 stomata, produced only a slight reduction in aperture dimensions after desiccation and plasmolysis, and no changes following ABA treatments and darkness. In tracheophytes, all these treatments resulted in complete stomatal closure. Potassium concentrations are similar in hornwort guard cells and epidermal cells under all treatments at all times. The small changes in hornwort stomatal dimensions in response to desiccation and plasmolysis are probably mechanical and/or stress responses of all the epidermal and spongy chlorophyllose cells, affecting the guard cells. In contrast to their nascent gas-filled counterparts across tracheophytes, sporophytic intercellular spaces in hornworts are initially liquid filled. Conclusions: Our experiments demonstrate a lack of physiological regulation of opening and closing of stomata in hornworts compared with tracheophytes, and support accumulating developmental and structural evidence that stomata in hornworts are primarily involved in sporophyte desiccation and spore discharge rather than the regulation of photosynthesis-related gaseous exchange. Our results run counter to the notion of the early acquisition of active control of stomatal movements in bryophytes as proposed from previous experiments on mosses.

Wind loads and competition for light sculpt trees into self-similar structures.

Trees are self-similar structures: their branch lengths and diameters vary allometrically within the tree architecture, with longer and thicker branches near the ground. These tree allometries are often attributed to optimisation of hydraulic sap transport and safety against elastic buckling. Here, we show that these allometries also emerge from a model that includes competition for light, wind biomechanics and no hydraulics. We have developed MECHATREE, a numerical model of trees growing and evolving on a virtual island. With this model, we identify the fittest growth strategy when trees compete for light and allocate their photosynthates to grow seeds, create new branches or reinforce existing ones in response to wind-induced loads. Strikingly, we find that selected trees species are self-similar and follow allometric scalings similar to those observed on dicots and conifers. This result suggests that resistance to wind and competition for light play an essential role in determining tree allometries.

Plasticity in seedling morphology, biomass allocation and physiology among ten temperate tree species in response to shade is related to shade tolerance and not leaf habit.

Mechanisms of shade tolerance in tree seedlings, and thus growth in shade, may differ by leaf habit and vary with ontogeny following seed germination. To examine early responses of seedlings to shade in relation to morphological, physiological and biomass allocation traits, we compared seedlings of 10 temperate species, varying in their leaf habit (broadleaved versus needle-leaved) and observed tolerance to shade, when growing in two contrasting light treatments - open (about 20% of full sunlight) and shade (about 5% of full sunlight). We analyzed biomass allocation and its response to shade using allometric relationships. We also measured leaf gas exchange rates and leaf N in the two light treatments. Compared to the open treatment, shading significantly increased traits typically associated with high relative growth rate (RGR) - leaf area ratio (LAR), specific leaf area (SLA), and allocation of biomass into leaves, and reduced seedling mass and allocation to roots, and net assimilation rate (NAR). Interestingly, RGR was not affected by light treatment, likely because of morphological and physiological adjustments in shaded plants that offset reductions of in situ net assimilation of carbon in shade. Leaf area-based rates of light-saturated leaf gas exchange differed among species groups, but not between light treatments, as leaf N concentration increased in concert with increased SLA in shade. We found little evidence to support the hypothesis of a increased plasticity of broadleaved species compared to needle-leaved conifers in response to shade. However, an expectation of higher plasticity in shade-intolerant species than in shade-tolerant ones, and in leaf and plant morphology than in biomass allocation was supported across species of contrasting leaf habit.

Establishing a Wild, Ex Situ Population of a Critically Endangered Shade-Tolerant Rainforest Conifer: A Translocation Experiment.

Translocation can reduce extinction risk by increasing population size and geographic range, and is increasingly being used in the management of rare and threatened plant species. A critical determinant of successful plant establishment is light environment. Wollemia nobilis (Wollemi pine) is a critically endangered conifer, with a wild population of 83 mature trees and a highly restricted distribution of less than 10 km2. We used under-planting to establish a population of W. nobilis in a new rainforest site. Because its optimal establishment conditions were unknown, we conducted an experimental translocation, planting in a range of different light conditions from deeply shaded to high light gaps. Two years after the experimental translocation, 85% of plants had survived. There were two distinct responses: very high survival (94%) but very low growth, and lower survival (69%) and higher growth, associated with initial plant condition. Overall survival of translocated W. nobilis was strongly increased in planting sites with higher light, in contrast to previous studies demonstrating long-term survival of wild W. nobilis juveniles in deep shade. Translocation by under-planting may be useful in establishing new populations of shade-tolerant plant species, not least by utilizing the range of light conditions that occur in forest understories.

A comparison of methods to estimate photosynthetic light absorption in leaves with contrasting morphology.

Accurate temporal and spatial measurements of leaf optical traits (i.e., absorption, reflectance and transmittance) are paramount to photosynthetic studies. These optical traits are also needed to couple radiative transfer and physiological models to facilitate the interpretation of optical data. However, estimating leaf optical traits in leaves with complex morphologies remains a challenge. Leaf optical traits can be measured using integrating spheres, either by placing the leaf sample in one of the measuring ports (External Method) or by placing the sample inside the sphere (Internal Method). However, in leaves with complex morphology (e.g., needles), the External Method presents limitations associated with gaps between the leaves, and the Internal Method presents uncertainties related to the estimation of total leaf area. We introduce a modified version of the Internal Method, which bypasses the effect of gaps and the need to estimate total leaf area, by painting the leaves black and measuring them before and after painting. We assess and compare the new method with the External Method using a broadleaf and two conifer species. Both methods yielded similar leaf absorption estimates for the broadleaf, but absorption estimates were higher with the External Method for the conifer species. Factors explaining the differences between methods, their trade-offs and their advantages and limitations are also discussed. We suggest that the new method can be used to estimate leaf absorption in any type of leaf independently of its morphology, and be used to study further the impact of gap fraction in the External Method.

Adaptation of the gymnosperms to the conditions of irradiation in Chornobyl zone: from morphological anomalies to the molecular genetic consequences.

It is known that the most suitable plant indicator targets for radiation pollution biomonitoring are conifers, because they have high radiosensitivity. In this review are briefly considered previously accumulated information about the genetic nature of morphological abnormalities in gymnosperms, induced by acute and chronic irradiation in the exclusion zone of the Chornobyl nuclear power plant. Since in the last decade appeared additional number of important research results, dedicated to the analysis of molecular biological and molecular genetic effects of chronic irradiation on the coniferous plants growing in the exclusion zone of the Chornobyl disaster, all these results are also analyzed in current review.

Seedling growth and biomass allocation in relation to leaf habit and shade tolerance among 10 temperate tree species.

Initial growth of germinated seeds is an important life history stage, critical for establishment and succession in forests. Important questions remain regarding the differences among species in early growth potential arising from shade tolerance. In addition, the role of leaf habit in shaping relationships underlying shade tolerance-related differences in seedling growth remains unresolved. In this study we examined variation in morphological and physiological traits among seedlings of 10 forest tree species of the European temperate zone varying in shade tolerance and leaf habit (broadleaved winter-deciduous species vs needle-leaved conifers) during a 10-week period. Seeds were germinated and grown in a controlled environment simulating an intermediate forest understory light environment to resolve species differences in initial growth and biomass allocation. In the high-resource experimental conditions during the study, seedlings increased biomass allocation to roots at the cost of leaf biomass independent of shade tolerance and leaf habit. Strong correlations between relative growth rate (RGR), net assimilation rate (NAR), leaf area ratio (LAR), specific leaf area (SLA) and leaf mass fraction (LMF) indicate that physiology and biomass allocation were equally important determinants of RGR as plant structure and leaf morphology among these species. Our findings highlight the importance of seed mass- and seed size-related root morphology (specific root length-SRL) for shade tolerance during early ontogeny. Leaf and plant morphology (SLA, LAR) were more successful in explaining variation among species due to leaf habit than shade tolerance. In both broadleaves and conifers, shade-tolerant species had lower SRL and greater allocation of biomass to stems (stem mass fraction). Light-seeded shade-intolerant species with greater SRL had greater RGR in both leaf habit groups. However, the greatest plant mass was accumulated in the group of heavy-seeded shade-tolerant broadleaves. The results of our study suggest that the combinations of plant attributes enhancing growth under high light vary with shade tolerance, but differ between leaf habit groups.

[Estimation of light-use efficiency of China' s mid-subtropical planted coniferous forest based on flux measurements and spectral observations].

The photochemical reflectance index (PRI) calculated from spectral reflectance has universally become a proxy for the light-use efficiency (LUE), which significantly improves the LUE-based estimation of ecosystem gross primary productivity on a large scale through upscaling. In this study, we observed the vegetation spectral reflectance of a planted subtropical coniferous forest from the top of a flux tower at Qianyanzhou Station, one of the ChinaFLUX sites, in September and December 2013, and simultaneously measured CO2 flux and meteorological variables for correlation and regression analysis. Results showed that PRI had a better correlation with LUE (R2 = 0.20, P< 0.001) than that of normalized difference vegetation index (NDVI), i.e., PRI was preferred in LUE retrieval. During the whole observation period, PRI and soil water content (SWC)-based bivariate regression model correlated well with LUE (R2 = 0.29, P < 0.001 and R2 = 0.30, P < 0.01 for daytime and midday observation, respectively), but in autumn the bivariate regression model of PRI and vapor pressure deficit (VPD) had a higher correlation with LUE (R2 = 0.448, P < 0.001) for midday observation, which showed that environmental factors, i.e., SWC and VPD, had a potential in improving the LUE retrieval from PRI, but the choice of appropriate environmental factors depended on season.

Growth, allometry and shade tolerance of understory saplings of four subalpine conifers in central Japan.

The conifers Abies veitchii, A. mariesii, Picea jezoensis var. hondoensis, Tsuga diversifolia dominate in subalpine forests in central Japan. We expected that species differences in shade tolerance and in aboveground and belowground architecture are important for their coexistence. We examined net production and carbon allocation of understory saplings. Although the four species allocated similar amounts of biomass to roots at a given trunk height, the root-zone area of T. diversifolia was greater than that of the three other species. T. diversifolia often dominates shallow soil sites, such as ridge and rocky slopes, and, therefore, a wide spread of lateral roots would be an adaptation to such edaphic conditions. Crown width and leaf and branch mass were greatest for T. diversifolia and A. mariesii, followed in order by A. veitchii and P. jezoensis var. hondoensis. Although leaf mass of P. jezoensis var. hondoensis was lowest among the four species, species differences were not found in the net production per sapling because net production per leaf mass was greatest for P. jezoensis var. hondoensis. The leaf lifespan was longer in the order A. mariesii, T. diversifolia, P. jezoensis var. hondoensis and A. veitchii. The minimum rate of net production per leaf mass required to maintain the current sapling leaf mass (MRNP(LM)) was lowest in A. mariesii and T. diversifolia, and increased in the order of A. veitchii and P. jezoensis var. hondoensis. A. mariesii and T. diversifolia may survive in shade conditions by a lower MRNP(LM) than the two other species. Therefore, species differences in aboveground and belowground architecture and MRNPLM reflected their shade tolerance and regeneration strategies, which contribute to their coexistence.

Mutation in Torenia fournieri Lind. UFO homolog confers loss of TfLFY interaction and results in a petal to sepal transformation.

We identified a Torenia fournieri Lind. mutant (no. 252) that exhibited a sepaloid phenotype in which the second whorls were changed to sepal-like organs. This mutant had no stamens, and the floral organs consisted of sepals and carpels. Although the expression of a torenia class B MADS-box gene, GLOBOSA (TfGLO), was abolished in the 252 mutant, no mutation of TfGLO was found. Among torenia homologs such as APETALA1 (AP1), LEAFY (LFY), and UNUSUAL FLORAL ORGANS (UFO), which regulate expression of class B genes in Arabidopsis, only accumulation of the TfUFO transcript was diminished in the 252 mutant. Furthermore, a missense mutation was found in the coding region of the mutant TfUFO. Intact TfUFO complemented the mutant phenotype whereas mutated TfUFO did not; in addition, the transgenic phenotype of TfUFO-knockdown torenias coincided with the mutant phenotype. Yeast two-hybrid analysis revealed that the mutated TfUFO lost its ability to interact with TfLFY protein. In situ hybridization analysis indicated that the transcripts of TfUFO and TfLFY were partially accumulated in the same region. These results clearly demonstrate that the defect in TfUFO caused the sepaloid phenotype in the 252 mutant due to the loss of interaction with TfLFY.

Vertical and seasonal variation in the δ¹³C of leaf-respired CO2 in a mixed conifer forest.

The C-isotopic composition (δ¹³C) of leaf respiration (δ(LR)) has previously been shown to vary among functional groups, plant organs and times of day. We here investigated vertical and seasonal variation in δ(LR) through deep (~35 m) forest canopies. We measured δ(LR), δ¹³C of leaf bulk organic matter (δ(LB)), specific leaf area, net photosynthesis (A) and dark respiration in shade, middle and sun foliage in four conifer species from May to August. We used Keeling plots to estimate δ(LR); we developed a novel technique for ensuring that the respiratory substrate was not changing over the course of the measurement. Variables δ(LR) and δ(LB) displayed a vertical pattern in Abies grandis, Pseudotsuga menziesii and Thuja plicata, but were independent of canopy position in Larix occidentalis. Vertical gradients in δ(LB) (3.6‰) and δ(LR) (2.8‰) were similar. The respiratory enrichment (δ(LR)-δ(LB)) was smaller in expanding (3‰) than mature (4-8‰) foliage. There was a linear relationship between the respiratory enrichment and A. Our data support the hypothesis that δ(LR) values are related to patterns of C allocation among metabolic pathways. We demonstrated that considerable variation in δ(LR) occurs vertically through the canopy (3‰ gradient) and seasonally (3-7‰). Understanding sources of variation in respiratory signals is fundamental to comprehending C dynamics and for global model applications.

Physiological responses of three deciduous conifers (Metasequoia glyptostroboides, Taxodium distichum and Larix laricina) to continuous light: adaptive implications for the early Tertiary polar summer.

Polar regions were covered with extensive forests during the Cretaceous and early Tertiary, and supported trees comparable in size and productivity to those of present-day temperate forests. With a winter of total or near darkness and a summer of continuous, low-angle illumination, these temperate, high-latitude forests were characterized by a light regime without a contemporary counterpart. Although maximum irradiances were much lower than at mid-latitudes, the 24-h photoperiod provided similar integrated light flux. Taxodium, Larix and Metasequoia, three genera of deciduous conifers that occurred in paleoarctic wet forests, have extant, closely related descendents. However, the contemporary relative abundance of these genera differs greatly from that in the paleoarctic. To provide insight into attributes that favor competitive success in a continuous-light environment, we subjected saplings of these genera to a natural photoperiod or a 24-h photoperiod and measured gas exchange, chlorophyll fluorescence, non-structural carbohydrate concentrations, biomass production and carbon allocation. Exposure to continuous light significantly decreased photosynthetic capacity and quantum efficiency of photosystem II in Taxodium and Larix, but had minimal influence in Metasequoia. In midsummer, foliar starch concentration substantially increased in both Taxodium and Larix saplings grown in continuous light, which may have contributed to end-product down-regulation of photosynthetic capacity. In contrast, Metasequoia allocated photosynthate to continuous production of new foliar biomass. This difference in carbon allocation may have provided Metasequoia with a two fold advantage in the paleoarctic by minimizing depression of photosynthetic capacity and increasing photosynthetic surface.

Temperature stress tolerance of conifer seedlings after exposure to UV-B radiation.

Ground-level UV-B radiation has increased globally due to a thinning stratospheric ozone layer. We estimated the effects of increased UV-B on 10 conifer species grown in chambers in greenhouses with supplemental UV-B. Species were selected from a wide range of geographic locations. Plant material of two ages (germinants, first growing season; seedlings, second season) were exposed to three levels of UV-B from ambient (at Victoria, B.C., Canada) to three times ambient (12 kJ m(-2) d(-1)) for up to four months. Frost hardiness and heat tolerance of shoots were estimated from changes in chlorophyll fluorescence after exposure to test temperatures. There were no significant differences among seed sources from different elevations in their response to temperature stresses. When UV-B increased above the ambient level, three species (interior Douglas-fir, Engelmann spruce, and interior lodgepole pine) increased in frost hardiness and four (grand fir, interior spruce, yellow-cedar, and western redcedar) decreased. Two species (western redcedar and western hemlock) increased in heat tolerance when UV-B increased to the 12 kJ level. The main differences in stress tolerance were between the triple ambient and the other two treatments, not between ambient and double ambient, suggesting that any changes in UV-B would have to be large to elicit physiological changes in conifer seedlings.

The penalty of a long, hot summer. Photosynthetic acclimation to high CO2 and continuous light in "living fossil" conifers.

Deciduous forests covered the ice-free polar regions 280 to 40 million years ago under warm "greenhouse" climates and high atmospheric pCO2. Their deciduous habit is frequently interpreted as an adaptation for minimizing carbon losses during winter, but experiments with "living fossils" in a simulated warm polar environment refute this explanation. Measured carbon losses through leaf abscission of deciduous trees are significantly greater than losses through winter respiration in evergreens, yet annual rates of primary productivity are similar in all species. Here, we investigate mechanisms underlying this apparent paradox by measuring the seasonal patterns of leaf photosynthesis (A) under pCO2 enrichment in the same trees. During spring, A increased significantly in coastal redwood (Sequoia sempervirens), dawn redwood (Metasequoia glyptostroboides), and swamp cypress (Taxodium distichum) at an elevated pCO2 of 80 Pa compared with controls at 40 Pa. However, strong acclimation in Rubisco carboxylation capacity (Vc,max) completely offset the CO2 response of A in all species by the end of 6 weeks of continuous illumination in the simulated polar summer. Further measurements demonstrated the temporary nature of acclimation, with increases in Vc,max during autumn restoring the CO2 sensitivity of A. Contrary to expectations, the acclimation of Vc,max was not always accompanied by accumulation of leaf carbohydrates, but was associated with a decline in leaf nitrogen in summer, suggesting an alteration of the balance in plant sources and sinks for carbon and nitrogen. Preliminary calculations using A indicated that winter carbon losses through deciduous leaf abscission and respiration were recovered by 10 to 25 d of canopy carbon fixation during summer, thereby explaining the productivity paradox.

[Molecular-biological nature of morphological abnormalities induced by chronic irradiation in coniferous plants from the Chernobyl nuclear power plant exclusion zone: emphasis on a possible role of the cytoskeleton]. / Molekuliarno-biologicheskaia priroda morfologicheskikh anomalii sredi golosemennykh rastenii, indutsirovannykh khronicheskim oblucheniem v zone otchuzhdeniia Chernobyl'skoi AES: aktsent na vozmozhnuiu rol' tsitoskeleta.

Results of the analysis of morphological abnormalities in coniferous plants from the Chernobyl exclusion zone are described. It is shown that such features as total and individual protein content, genome organization and peculiarities of its expression, and karyotype are different for the control and morphologically abnormal needles. A possible role of the cytoskeleton structures in the abnormal morphogenesis in plants is discussed.