Epigenetic stress memory in gymnosperms.

Gymnosperms are long-lived, cone-bearing seed plants that include some of the most ancient extant plant species. These relict land plants have evolved to survive in habitats marked by chronic or episodic stress. Their ability to thrive in these environments is partly due to their phenotypic flexibility, and epigenetic regulation likely plays a crucial part in this plasticity. We review the current knowledge on abiotic and biotic stress memory in gymnosperms and the possible epigenetic mechanisms underlying long-term phenotypic adaptations. We also discuss recent technological improvements and new experimental possibilities that likely will advance our understanding of epigenetic regulation in these ancient and hard-to-study plants.

Middle Jurassic insect mines on gymnosperms provide missing links to early mining evolution.

We investigated the mining mode of insect feeding, involving larval consumption of a plant's internal tissues, from the Middle Jurassic (165 million years ago) Daohugou locality of Northeastern China. Documentation of mining from the Jurassic Period is virtually unknown, and results from this time interval would address mining evolution during the temporal gap of mine-seed plant diversifications from the previous Late Triassic to the subsequent Early Cretaceous. Plant fossils were examined with standard microscopic procedures for herbivory and used the standard functional feeding group-damage-type system of categorizing damage. All fossil mines were photographed and databased. We examined 2014 plant specimens, of which 27 occurrences on 14 specimens resulted in eight, new, mine damage types (DTs) present on six genera of bennettitalean, ginkgoalean, and pinalean gymnosperms. Three conclusions emerge from this study. First, these mid-Mesozoic mines are morphologically conservative and track plant host anatomical structure rather than plant phylogeny. Second, likely insect fabricators of these mines were three basal lineages of polyphagan beetles, four basal lineages of monotrysian moths, and a basal lineage tenthredinoid sawflies. Third, the nutrition hypothesis, indicating that miners had greater access to nutritious, inner tissues of new plant lineages, best explains mine evolution during the mid-Mesozoic.

Limited effects of xylem anatomy on embolism resistance in cycad leaves.

Drought-induced xylem embolism is a primary cause of plant mortality. Although c. 70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked. We quantified the vulnerability to drought-induced embolism, pressure-volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads. Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads. Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits - particularly vessels - may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.

Conserved autophagy and diverse cell wall composition: unifying features of vascular tissues in evolutionarily distinct plants.

BACKGROUND AND AIMS: The formation of multifunctional vascular tissues represents a significant advancement in plant evolution. Differentiation of conductive cells is specific, involving two main pathways, namely protoplast clearance and cell wall modification. In xylogenesis, autophagy is a crucial process for complete protoplast elimination in tracheary elements, whose cell wall also undergoes strong changes. Knowledge pertaining to living sieve elements, which lose most of their protoplast during phloemogenesis, remains limited. We hypothesized that autophagy plays a crucial role, not only in complete cytoplasmic clearance in xylem but also in partial degradation in phloem. Cell wall elaborations of mature sieve elements are not so extensive. These analyses performed on evolutionarily diverse model species potentially make it possible to understand phloemogenesis to an equal extent to xylogenesis. METHODS: We investigated the distribution of ATG8 protein, which is an autophagy marker, and cell wall components in the roots of ferns, gymnosperms and angiosperms (monocots, dicot herbaceous plants and trees). Furthermore, we conducted a bioinformatic analysis of complete data on ATG8 isoforms for Ceratopteris richardii. KEY RESULTS: The presence of ATG8 protein was confirmed in both tracheary elements and sieve elements; however, the composition of cell wall components varied considerably among vascular tissues in the selected plants. Arabinogalactan proteins and ß-1,4-galactan were detected in the roots of all studied species, suggesting their potential importance in phloem formation or function. In contrast, no evolutionary pattern was observed for xyloglucan, arabinan or homogalacturonan. CONCLUSIONS: Our findings indicate that the involvement of autophagy in plants is universal during the development of tracheary elements that are dead at maturity and sieve elements that remain alive. Given the conserved nature of autophagy and its function in protoplast degradation for uninterrupted flow, autophagy might have played a vital role in the development of increasingly complex biological organizations, including the formation of vascular tissues. However, different cell wall compositions of xylem and phloem in different species might indicate diverse functionality and potential for substance transport, which is crucial in plant evolution.

Cell wall composition strongly influences mesophyll conductance in gymnosperms.

Cell wall thickness is widely recognized as one of the main determinants of mesophyll conductance to CO2 (gm ). However, little is known about the components that regulate effective CO2 diffusivity in the cell wall (i.e. the ratio between actual porosity and tortuosity, the other two biophysical diffusion properties of cell walls). The aim of this study was to assess, at the interspecific level, potential relationships between cell wall composition, cell wall thickness (Tcw ) and gm . Gymnosperms constitute an ideal group to deepen these relationships, as they present, on average, the thickest cell walls within spermatophytes. We characterized the foliar gas exchange, the morphoanatomical traits related with gm , the leaf fraction constituted by cell walls and three main components of primary cell walls (hemicelluloses, cellulose and pectins) in seven gymnosperm species. We found that, although the relatively low gm of gymnosperms was mainly determined by their elevated Tcw , gm was also strongly correlated with cell wall composition, which presumably sets the final effective CO2 diffusivity. The data presented here suggest that (i) differences in gm are strongly correlated to the pectins to hemicelluloses and cellulose ratio in gymnosperms, and (ii) variations in cell wall composition may modify effective CO2 diffusivity in the cell wall to compensate the negative impact of thickened walls. We speculate that higher relative pectin content allows higher gm because pectins increase cell wall hydrophilicity and CO2 molecules cross the wall dissolved in water.

Mehler reaction plays a role in C3 and C4 photosynthesis under shade and low CO2.

Alternative electron fluxes such as the cyclic electron flux (CEF) around photosystem I (PSI) and Mehler reaction (Me) are essential for efficient photosynthesis because they generate additional ATP and protect both photosystems against photoinhibition. The capacity for Me can be estimated by measuring O2 exchange rate under varying irradiance and CO2 concentration. In this study, mass spectrometric measurements of O2 exchange were made using leaves of representative species of C3 and C4 grasses grown under natural light (control; PAR ~ 800 µmol quanta m-2 s-1) and shade (~ 300 µmol quanta m-2 s-1), and in representative species of gymnosperm, liverwort and fern grown under natural light. For all control grown plants measured at high CO2, O2 uptake rates were similar between the light and dark, and the ratio of Rubisco oxygenation to carboxylation (Vo/Vc) was low, which suggests little potential for Me, and that O2 uptake was mainly due to photorespiration or mitochondrial respiration under these conditions. Low CO2 stimulated O2 uptake in the light, Vo/Vc and Me in all species. The C3 species had similar Vo/Vc, but Me was highest in the grass and lowest in the fern. Among the C4 grasses, shade increased O2 uptake in the light, Vo/Vc and the assimilation quotient (AQ), particularly at low CO2, whilst Me was only substantial at low CO2 where it may contribute 20-50% of maximum electron flow under high light.

Alternative Oxidase Capacity of Mitochondria in Microsporophylls May Function in Cycad Thermogenesis.

Cone thermogenesis is a widespread phenomenon in cycads and may function to promote volatile emissions that affect pollinator behavior. Given their large population size and intense and durable heat-producing effects, cycads are important organisms for comprehensive studies of plant thermogenesis. However, knowledge of mitochondrial morphology and function in cone thermogenesis is limited. Therefore, we investigated these mitochondrial properties in the thermogenic cycad species Cycas revoluta Male cones generated heat even in cool weather conditions. Female cones produced heat, but to a lesser extent than male cones. Ultrastructural analyses of the two major tissues of male cones, microsporophylls and microsporangia, revealed the existence of a population of mitochondria with a distinct morphology in the microsporophylls. In these cells, we observed large mitochondria (cross-sectional area of 2 µm2 or more) with a uniform matrix density that occupied >10% of the total mitochondrial volume. Despite the size difference, many nonlarge mitochondria (cross-sectional area <2 µm2) also exhibited a shape and a matrix density similar to those of large mitochondria. Alternative oxidase (AOX) capacity and expression levels in microsporophylls were much higher than those in microsporangia. The AOX genes expressed in male cones revealed two different AOX complementary DNA sequences: CrAOX1 and CrAOX2 The expression level of CrAOX1 mRNA in the microsporophylls was 100 times greater than that of CrAOX2 mRNA. Collectively, these results suggest that distinctive mitochondrial morphology and CrAOX1-mediated respiration in microsporophylls might play a role in cycad cone thermogenesis.

Day length regulates seasonal patterns of stomatal conductance in Quercus species.

Vapour pressure deficit is a major driver of seasonal changes in transpiration, but photoperiod also modulates leaf responses. Climate warming might enhance transpiration by increasing atmospheric water demand and the length of the growing season, but photoperiod-sensitive species could show dampened responses. Here, we document that day length is a significant driver of the seasonal variation in stomatal conductance. We performed weekly gas exchange measurements across a common garden experiment with 12 oak species from contrasting geographical origins, and we observed that the influence of day length was of similar strength to that of vapour pressure deficit in driving the seasonal pattern. We then examined the generality of our findings by incorporating day-length regulation into well-known stomatal models. For both angiosperm and gymnosperm species, the models improved significantly when adding day-length dependences. Photoperiod control over stomatal conductance could play a large yet underexplored role on the plant and ecosystem water balances.

Fossil evidence reveals how plants responded to cooling during the Cretaceous-Paleogene transition.

BACKGROUND: Around the Cretaceous-Paleogene (K-Pg) boundary, an obvious global cooling occurred, which resulted in dramatic changes in terrestrial ecosystems and the evolutionary trends of numerous organisms. However, how plant lineages responded to the cooling has remained unknown until now. Between ca. 70-60 Ma Mesocyparis McIver & Basinger (Cupressaceae), an extinct conifer genus, was distributed from eastern Asia to western North America and provides an excellent opportunity to solve this riddle. RESULTS: Here we report a new species, Mesocyparis sinica from the early Paleocene of Jiayin, Heilongjiang, northeastern China. By integrating lines of evidence from phylogeny and comparative morphology of Mesocyparis, we found that during ca.70-60 Ma, the size of seed cone of Mesocyparis more than doubled, probably driven by the cooling during the K-Pg transition, which might be an effective adaptation for seed dispersal by animals. More importantly, we discovered that the northern limit of this genus, as well as those of two other arboreal taxa Metasequoia Miki ex Hu et Cheng (gymnosperm) and Nordenskioldia Heer (angiosperm), migrated ca.4-5° southward in paleolatitude during this time interval. CONCLUSIONS: Our results suggest that the cooling during the K-Pg transition may have been responsible for the increase in size of the seed cone of Mesocyparis and have driven the migration of plants southwards.

Differential responses of stomatal kinetics and steady-state conductance to abscisic acid in a fern: comparison with a gymnosperm and an angiosperm.

Origins of abscisic acid (ABA)-mediated metabolic control of stomatal conductance have been suggested to be recent, based on a gradualistic model of stomatal evolution. In ferns, steady-state stomatal conductance (gs ) was unresponsive to ABA in some studies, supporting this model. Stomatal kinetic responses to ABA have not been considered. We used dynamic gas exchange methods to characterise half times of stomatal opening and closing in response to step changes in light, across a range of ABA exposures in three diverse taxa. All taxa had asymmetric kinetics, with closure slower than opening in fern and cedar, but faster than opening in soybean. Closing was fastest in soybean but opening was slowest. Stomatal kinetics, particularly for closure, responded to ABA in all three taxa. Steady-state gs did not respond significantly to ABA in fern or cedar but responded strongly in soybean. Stomatal kinetics were responsive to ABA in fern. This finding supports a contrasting, single origin model, with ABA-mediated regulation of stomata arising early, in conjunction with stomata themselves. Stomatal kinetics are underutilised. Differential responses of opening and closing rates to environmental and hormonal stimuli may provide insights into phylogeny and stomatal regulatory strategies with potential application to selection for crop improvement.

How does genome size affect the evolution of pollen tube growth rate, a haploid performance trait?

PREMISE: Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (PTGRs) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially accelerate PTGR because increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plant PTGRs. METHODS: We assembled a phylogenetic tree of 451 species with known PTGRs. We then used comparative phylogenetic methods to detect effects of neo-polyploidy (within-genus origins), DNA content, and WGD history on PTGR, and correlated evolution of PTGR and DNA content. RESULTS: Gymnosperms had significantly higher DNA content and slower PTGR optima than angiosperms, and their PTGR and DNA content were negatively correlated. For angiosperms, 89% of model weight favored Ornstein-Uhlenbeck models with a faster PTGR optimum for neo-polyploids, whereas PTGR and DNA content were not correlated. For within-genus and intraspecific-cytotype pairs, PTGRs of neo-polyploids < paleo-polyploids. CONCLUSIONS: Genome size increases should negatively affect PTGR when genetic consequences of WGDs are minimized, as found in intra-specific autopolyploids (low heterosis) and gymnosperms (few WGDs). But in angiosperms, the higher PTGR optimum of neo-polyploids and non-negative PTGR-DNA content correlation suggest that recurrent WGDs have caused substantial PTGR evolution in a non-haploid state.

Forest resilience to drought varies across biomes.

Forecasted increase drought frequency and severity may drive worldwide declines in forest productivity. Species-level responses to a drier world are likely to be influenced by their functional traits. Here, we analyse forest resilience to drought using an extensive network of tree-ring width data and satellite imagery. We compiled proxies of forest growth and productivity (TRWi, absolutely dated ring-width indices; NDVI, Normalized Difference Vegetation Index) for 11 tree species and 502 forests in Spain corresponding to Mediterranean, temperate, and continental biomes. Four different components of forest resilience to drought were calculated based on TRWi and NDVI data before, during, and after four major droughts (1986, 1994-1995, 1999, and 2005), and pointed out that TRWi data were more sensitive metrics of forest resilience to drought than NDVI data. Resilience was related to both drought severity and forest composition. Evergreen gymnosperms dominating semi-arid Mediterranean forests showed the lowest resistance to drought, but higher recovery than deciduous angiosperms dominating humid temperate forests. Moreover, semi-arid gymnosperm forests presented a negative temporal trend in the resistance to drought, but this pattern was absent in continental and temperate forests. Although gymnosperms in dry Mediterranean forests showed a faster recovery after drought, their recovery potential could be constrained if droughts become more frequent. Conversely, angiosperms and gymnosperms inhabiting temperate and continental sites might have problems to recover after more intense droughts since they resist drought but are less able to recover afterwards.

Resin flow in conifers.

Resins are plant exudates of economic importance used by plants as defence. They flow out of resin ducts, open and long tube-like intercellular spaces lined by a layer of specialized parenchyma cells, called the epithelium, which secrete resin into the duct lumen. A model that describes resin flow in conifers is presented to investigate how duct structure, resin loading, crystallisation, and viscosity affect flow and could explain differences between species. Considering resin viscosity, the structure of resin ducts, and a pressure-driven resin loading through the duct wall, the unsteady Stokes equation was applied. There is an increase in flow towards the open end that is favoured by the duct geometry. Both flow and pressure depend on the loading mechanism and on the duct resistance, which depends on the duct geometry, viscosity and duct wall permeability to resin. These results confirm previous measurements and observations made on Pinaceae and seem to be physiologically advantageous for the defence role of resin. Understanding of how these physiological and morphological parameters affect resin flow might be useful for selecting varieties and species having a high resin yielding capacity. The model presented in this paper is also applicable to other external secretory systems in plants.

Cracking the omega code: hydraulic architecture of the cycad leaf axis.

Background and Aims: The leaf axis of members of the order Cycadales ('cycads') has long been recognized by its configuration of independent vascular bundles that, in transverse section, resemble the Greek letter omega (hence the 'omega pattern'). This provides a useful diagnostic character for the order, especially when applied to paleobotany. The function of this pattern has never been elucidated. Here we provide a three-dimensional analysis and explain the pattern in terms of the hydraulic architecture of the pinnately compound cycad leaf. Methods: The genus Cycas was used as a simple model, because each leaflet is supplied by a single vascular bundle. Sequential sectioning was conducted throughout the leaf axis and photographed with a digital camera. Photographs were registered and converted to a cinematic format, which provided an objective method of analysis. Key Results: The omega pattern in the petiole can be sub-divided into three vascular components, an abaxial 'circle', a central 'column' and two adaxial 'wings', the last being the only direct source of vascular supply to the leaflets. Each leaflet is supplied by a vascular bundle that has divided or migrated directly from the closest wing bundle. There is neither multiplication nor anastomoses of vascular bundles in the other two components. Thus, as one proceeds from base to apex along the leaf axis, the number of vascular bundles in circle and column components is reduced distally by their uniform migration throughout all components. Consequently, the distal leaflets are irrigated by the more abaxial bundles, guaranteeing uniform water supply along the length of the axis. Conclusions: The omega pattern exemplifies one of the many solutions plants have achieved in supplying distal appendages of an axis with a uniform water supply. Our method presents a model that can be applied to other genera of cycads with more complex vascular organization.

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Cretaceous-Tertiary Foraminifera and Palynomorphs from Djega Section and Inferred Paleodepositional Environments, Rio Del Rey Basin, Cameroon, West Africa.

Late Cretaceous-Paleocene foraminiferans and palynomorphs were recovered from the upper section of the Djega outcrop in the Rio del Rey Basin. Only a few planktonic foraminiferan species of the genera Heterohelix and Hedbergella were recovered among an assemblage dominated by calcareous and agglutinated benthonics. Marine dinocysts are curiously absent from among the palynomorph assemblage, which consists dominantly of pollen grains from land plants (angiosperms and gymnosperms) and pteridophytic spores, together with a few fungal remains. Two benthonic foraminiferal assemblages that include the Campanian-Maastrichtian Bolivina afra-Haplophragmoides talokensis and the Paleocene Anomalinoides umboniferus-Eponides pseudoelevatus are well established at this outcrop. The palynomorphs include a few typical Late Cretaceous and typical Paleogene species, while the majority are long ranging forms that straddle the Cretaceous-Tertiary boundary. The foraminiferal and palynomorph biostratigraphic distributions permitted us to recognize the succession of Campanian-Maastrichtian and Paleocene strata and the Cretaceous-Tertiary boundary for the first time in this basin. Lithofacies change from a monotonous thick pile of shales below, succeeded by sandstones, frequently alternating with mudstone, above. This indicates a general fall in sea level during the Early Paleocene earlier reported within this subregion, and the boundary marks the start of the out building of the Niger Delta which the Tertiary Rio del Rey Basin is part of. Both microfossils and lithofacies analyses aided the reconstruction of an open marine, probably middle to inner neritic shallow and transitional intertidal paleodepositional environments for the sediments exposed at this outcrop.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Exploring the bark thickness-stem diameter relationship: clues from lianas, successive cambia, monocots and gymnosperms.

Bark thickness is ecologically crucial, affecting functions from fire protection to photosynthesis. Bark thickness scales predictably with stem diameter, but there is little consensus on whether this scaling is a passive consequence of growth or an important adaptive phenomenon requiring explanation. With a comparative study across 913 species, we test the expectation that, if bark thickness-stem diameter scaling is adaptive, it should be possible to find ecological situations in which scaling is predictably altered, in this case between species with different types and deployments of phloem. 'Dicots' with successive cambia and monocots, which have phloem-free bark, had predictably thinner inner (mostly living) bark than plants with single cambia. Lianas, which supply large leaf areas with limited stem area, had much thicker inner bark than self-supporting plants. Gymnosperms had thicker outer bark than angiosperms. Inner bark probably scales with plant metabolic demands, for example with leaf area. Outer bark scales with stem diameter less predictably, probably reflecting diverse adaptive factors; for example, it tends to be thicker in fire-prone species and very thin when bark photosynthesis is favored. Predictable bark thickness-stem diameter scaling across plants with different photosynthate translocation demands and modes strongly supports the idea that this relationship is functionally important and adaptively significant.

Opposite domination of cyclic and pseudocyclic electron flows in short-illuminated dark-adapted leaves of angiosperms and gymnosperms.

The present work was aimed to explain the recently reported higher O2-dependent electron flow capacity in gymnosperms than in angiosperms and to search for other differences in the electron transport processes by simultaneous characterization of the relative capacities of pseudocyclic (direct or Flavodiiron proteins (Flv)-mediated O2-reduction, Mehler(-like) reactions) and cyclic electron flows around photosystem I (CEF-PSI). To this end, a comparative multicomponent analysis was performed on the fluorescence decay curves of dark-adapted leaves after illumination with a 1-s saturating light pulse. In both gymnosperms and angiosperms, two or three exponential decay components were resolved: fast (t 1/21 ~ 170-260 ms), middle (~1.0-2.3 s), and slow (>4.2 s). The sensitivity of the decay parameters (amplitudes A1-3, halftimes t 1/2 1-3) to the alternative electron flows was assessed using Arabidopsis pgr5 and ndhM mutants, defective in CEF-PSI, Synechocystis sp. PCC 6803 Δflv1 mutant, defective in Flv-mediated O2-photoreduction, different O2 concentrations, and methyl viologen treatment. A1 reflected the part of electrons involved in linear and O2-photoreduction pathways after PSI. The middle component appeared in pgr5 (but not in ndhM), in gymnosperms under low O2, and in Δflv1, and reflected limitations at the PSI acceptor side. The slow component was sensitive to CEF-PSI. The comparison of decay parameters provided evidence that Flv mediate O2-photoreduction in gymnosperms, which explains their higher O2-dependent electron flow capacity. The concomitant quantification of relative electrons branching in O2-photoreduction and CEF-PSI pathways under the applied non-steady-state photosynthetic conditions reveals that CEF-PSI capacity significantly exceeds that of O2-photoreduction in angiosperms while the opposite occurs in gymnosperms.

Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I.

In land plants, photosystem I (PSI) photoinhibition limits carbon fixation and causes growth defects. In addition, recovery from PSI photoinhibition takes much longer than PSII photoinhibition when the PSI core-complex is degraded by oxidative damage. Accordingly, PSI photoinhibition should be avoided in land plants, and land plants should have evolved mechanisms to prevent PSI photoinhibition. However, such protection mechanisms have not yet been identified, and it remains unclear whether all land plants suffer from PSI photoinhibition in the same way. In the present study, we focused on the susceptibility of PSI to photoinhibition and investigated whether mechanisms of preventing PSI photoinhibition varied among land plant species. To assess the susceptibility of PSI to photoinhibition, we used repetitive short-pulse (rSP) illumination, which specifically induces PSI photoinhibition. Subsequently, we found that land plants possess a wide variety of tolerance mechanisms against PSI photoinhibition. In particular, gymnosperms, ferns and mosses/liverworts exhibited higher tolerance to rSP illumination-induced PSI photoinhibition than angiosperms, and detailed analyses indicated that the tolerance of these groups could be partly attributed to flavodiiron proteins, which protected PSI from photoinhibition by oxidizing the PSI reaction center chlorophyll (P700) as an electron acceptor. Furthermore, we demonstrate, for the first time, that gymnosperms, ferns and mosses/liverworts possess a protection mechanism against photoinhibition of PSI that differs from that of angiosperms.