Terrestrial and Floating Aquatic Plants Differ in Acclimation to Light Environment.

The ability of plants to respond to environmental fluctuations is supported by acclimatory adjustments in plant form and function that may require several days and development of a new leaf. We review adjustments in photosynthetic, photoprotective, and foliar vascular capacity in response to variation in light and temperature in terrestrial plants. The requirement for extensive acclimation to these environmental conditions in terrestrial plants is contrasted with an apparent lesser need for acclimation to different light environments, including rapid light fluctuations, in floating aquatic plants for the duckweed Lemna minor. Relevant features of L. minor include unusually high growth rates and photosynthetic capacities coupled with the ability to produce high levels of photoprotective xanthophylls across a wide range of growth light environments without compromising photosynthetic efficiency. These features also allow L. minor to maximize productivity and avoid problems during an abrupt experimental transfer of low-light-grown plants to high light. The contrasting responses of land plants and floating aquatic plants to the light environment further emphasize the need of land plants to, e.g., experience light fluctuations in their growth environment before they induce acclimatory adjustments that allow them to take full advantage of natural settings with such fluctuations.

Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications.

Atmospheric carbon dioxide (CO2) is projected to be twice as high as the pre-industrial level by 2050. This review briefly highlights key responses of terrestrial plants to elevated CO2 and compares these with the responses of aquatic floating plants of the family Lemnaceae (duckweeds). Duckweeds are efficient at removing CO2 from the atmosphere, which we discuss in the context of their exceptionally high growth rates and capacity for starch storage in green tissue. In contrast to cultivation of terrestrial crops, duckweeds do not contribute to CO2 release from soils. We briefly review how this potential for contributions to stabilizing atmospheric CO2 levels is paired with multiple additional applications and services of duckweeds. These additional roles include wastewater phytoremediation, feedstock for biofuel production, and superior nutritional quality (for humans and livestock), while requiring minimal space and input of light and fertilizer. We, furthermore, elaborate on other environmental factors, such as nutrient availability, light supply, and the presence of a microbiome, that impact the response of duckweed to elevated CO2. Under a combination of elevated CO2 with low nutrient availability and moderate light supply, duckweeds' microbiome helps maintain CO2 sequestration and relative growth rate. When incident light intensity increases (in the presence of elevated CO2), the microbiome minimizes negative feedback on photosynthesis from increased sugar accumulation. In addition, duckweed shows a clear propensity for absorption of ammonium over nitrate, accepting ammonium from their endogenous N2-fixing Rhizobium symbionts, and production of large amounts of vegetative storage protein. Finally, cultivation of duckweed could be further optimized using hydroponic vertical farms where nutrients and water are recirculated, saving both resources, space, and energy to produce high-value products.

Growth and Nutritional Quality of Lemnaceae Viewed Comparatively in an Ecological and Evolutionary Context.

This review focuses on recently characterized traits of the aquatic floating plant Lemna with an emphasis on its capacity to combine rapid growth with the accumulation of high levels of the essential human micronutrient zeaxanthin due to an unusual pigment composition not seen in other fast-growing plants. In addition, Lemna's response to elevated CO2 was evaluated in the context of the source-sink balance between plant sugar production and consumption. These and other traits of Lemnaceae are compared with those of other floating aquatic plants as well as terrestrial plants adapted to different environments. It was concluded that the unique features of aquatic plants reflect adaptations to the freshwater environment, including rapid growth, high productivity, and exceptionally strong accumulation of high-quality vegetative storage protein and human antioxidant micronutrients. It was further concluded that the insensitivity of growth rate to environmental conditions and plant source-sink imbalance may allow duckweeds to take advantage of elevated atmospheric CO2 levels via particularly strong stimulation of biomass production and only minor declines in the growth of new tissue. It is proposed that declines in nutritional quality under elevated CO2 (due to regulatory adjustments in photosynthetic metabolism) may be mitigated by plant-microbe interaction, for which duckweeds have a high propensity.

Features of the Duckweed Lemna That Support Rapid Growth under Extremes of Light Intensity.

This study addresses the unique functional features of duckweed via comparison of Lemna gibba grown under controlled conditions of 50 versus 1000 µmol photons m-2 s-1 and of a L. minor population in a local pond with a nearby population of the biennial weed Malva neglecta. Principal component analysis of foliar pigment composition revealed that Malva was similar to fast-growing annuals, while Lemna was similar to slow-growing evergreens. Overall, Lemna exhibited traits reminiscent of those of its close relatives in the family Araceae, with a remarkable ability to acclimate to both deep shade and full sunlight. Specific features contributing to duckweed's shade tolerance included a foliar pigment composition indicative of large peripheral light-harvesting complexes. Conversely, features contributing to duckweed's tolerance of high light included the ability to convert a large fraction of the xanthophyll cycle pool to zeaxanthin and dissipate a large fraction of absorbed light non-photochemically. Overall, duckweed exhibited a combination of traits of fast-growing annuals and slow-growing evergreens with foliar pigment features that represented an exaggerated version of that of terrestrial perennials combined with an unusually high growth rate. Duckweed's ability to thrive under a wide range of light intensities can support success in a dynamic light environment with periodic cycles of rapid expansion.

Differences in biochemical, gas exchange and hydraulic response to water stress in desiccation tolerant and sensitive fronds of the fern Anemia caffrorum.

Desiccation tolerant plants can survive extreme water loss in their vegetative tissues. The fern Anemia caffrorum produces desiccation tolerant (DT) fronds in the dry season and desiccation sensitive (DS) fronds in the wet season, providing a unique opportunity to explore the physiological mechanisms associated with desiccation tolerance. Anemia caffrorum plants with either DT or DS fronds were acclimated in growth chambers. Photosynthesis, frond structure and anatomy, water relations and minimum conductance to water vapour were measured under well-watered conditions. Photosynthesis, hydraulics, frond pigments, antioxidants and abscisic acid contents were monitored under water deficit. A comparison between DT and DS fronds under well-watered conditions showed that the former presented higher leaf mass per area, minimum conductance, tissue elasticity and lower CO2 assimilation. Water deficit resulted in a similar induction of abscisic acid in both frond types, but DT fronds maintained higher stomatal conductance and upregulated more prominently lipophilic antioxidants. The seasonal alternation in production of DT and DS fronds in A. caffrorum represents a mechanism by which carbon gain can be maximized during the rainy season, and a greater investment in protective mechanisms occurs during the hot dry season, enabling the exploitation of episodic water availability.

Frozen in the dark: interplay of night-time activity of xanthophyll cycle, xylem attributes, and desiccation tolerance in fern resistance to winter.

While most ferns avoid freezing as they have a tropical distribution or shed their fronds, wintergreen species in temperate and boreoalpine ecosystems have to deal with sub-zero temperatures. Increasing evidence has revealed overlapping mechanisms of desiccation and freezing tolerance in angiosperms, but the physiological mechanisms behind freezing tolerance in ferns are far from clear. We evaluated photochemical and hydraulic parameters in five wintergreen fern species differing in their ability to tolerate desiccation. We assessed frond freezing tolerance, ice nucleation temperature and propagation pattern, and xylem anatomical traits. Dynamics of photochemical performance and xanthophyll cycle were evaluated during freeze-thaw events under controlled conditions and, in selected species, in the field. Only desiccation-tolerant species, which possessed a greater fraction of narrow tracheids (<18 µm) than sensitive species, tolerated freezing. Frond freezing occurred in the field at -3.4 ± 0.9 °C (SD) irrespective of freezing tolerance, freezable water content, or tracheid properties. Even in complete darkness, maximal photochemical efficiency of photosystem II was down-regulated concomitantly with zeaxanthin accumulation in response to freezing. This was reversible upon re-warming only in tolerant species. Our results suggest that adaptation for freezing tolerance is associated with desiccation tolerance through complementary xylem properties (which may prevent risk of irreversible cavitation) and effective photoprotection mechanisms. The latter includes de-epoxidation of xanthophylls in darkness, a process evidenced for the first time directly in the field.

Zeaxanthin, a Molecule for Photoprotection in Many Different Environments.

Conversion of sunlight into photochemistry depends on photoprotective processes that allow safe use of sunlight over a broad range of environmental conditions. This review focuses on the ubiquity of photoprotection associated with a group of interconvertible leaf carotenoids, the xanthophyll cycle. We survey the striking plasticity of this process observed in nature with respect to (1) xanthophyll cycle pool size, (2) degree and speed of interconversion of its components, and (3) flexibility in the association between xanthophyll cycle conversion state and photoprotective dissipation of excess excitation energy. It is concluded that the components of this system can be independently tuned with a high degree of flexibility to produce a fit for different environments with various combinations of light, temperature, and other factors. In addition, the role of genetic variation is apparent from variation in the response of different species growing side-by-side in the same environment. These findings illustrate how field studies can generate insight into the adjustable levers that allow xanthophyll cycle-associated photoprotection to support plant photosynthetic productivity and survival in environments with unique combinations of environmental factors.

Zeaxanthin and Lutein: Photoprotectors, Anti-Inflammatories, and Brain Food.

This review compares and contrasts the role of carotenoids across the taxa of life-with a focus on the xanthophyll zeaxanthin (and its structural isomer lutein) in plants and humans. Xanthophylls' multiple protective roles are summarized, with attention to the similarities and differences in the roles of zeaxanthin and lutein in plants versus animals, as well as the role of meso-zeaxanthin in humans. Detail is provided on the unique control of zeaxanthin function in photosynthesis, that results in its limited availability in leafy vegetables and the human diet. The question of an optimal dietary antioxidant supply is evaluated in the context of the dual roles of both oxidants and antioxidants, in all vital functions of living organisms, and the profound impact of individual and environmental context.

Growth and Essential Carotenoid Micronutrients in Lemna gibba as a Function of Growth Light Intensity.

Duckweed is a promising food crop with multiple benefits for space applications. Fresh duckweed could deliver synergistically acting essential antioxidant nutrients to a crew - but only if growth conditions provide the plant with the right cues to trigger antioxidant formation. We grew Lemna gibba under continuous growth light ranging from low to very high intensities (photosynthetic photon flux densities = PPFDs) in order to investigate the effect on plant growth, photosynthesis, and level of carotenoid antioxidants that are essential human micronutrients. Lemna gibba achieved remarkably high growth rates under modest growth PPFD by virtue of superior light absorption resulting from minimal self-shading and high chlorophyll levels. Conversely, L. gibba's growth rate remained high even under very high growth PPFDs. This notable ability of L. gibba to avoid inactivation of photosynthesis and diminished growth under very high growth PPFDs resulted from a combination of downregulation of chlorophyll synthesis and increased biochemical photoprotection that limited a build-up of excessive excitation energy. This biochemical photoprotection included accumulation of zeaxanthin (an essential human micronutrient) and high levels of zeaxanthin-catalyzed thermal energy dissipation of excess excitation. Compared to the light levels needed to saturate L. gibba photosynthesis and growth, higher light levels were thus required for strong induction of the essential antioxidant zeaxanthin. These results indicate a need for design of light protocols that achieve simultaneous optimization of plant yield, nutritional quality, and light-use efficiency to circumvent the fact that the light requirement to saturate plant growth is lower than that for production of high zeaxanthin levels. How this trade-off between light-use efficiency of growth and nutritional quality might be minimized or circumvented to co-optimize all desired features is discussed.

Born to revive: molecular and physiological mechanisms of double tolerance in a paleotropical and resurrection plant.

Resurrection plants recover physiological functions after complete desiccation. Almost all of them are native to tropical warm environments. However, the Gesneriaceae include four genera, remnant of the past palaeotropical flora, which inhabit temperate mountains. One of these species is additionally freezing-tolerant: Ramonda myconi. We hypothesise that this species has been able to persist in a colder climate thanks to some resurrection-linked traits. To disentangle the physiological mechanisms underpinning multistress tolerance to desiccation and freezing, we conducted an exhaustive seasonal assessment of photosynthesis (gas exchange, limitations to partitioning, photochemistry and galactolipids) and primary metabolism (through metabolomics) in two natural populations at different elevations. R. myconi displayed low rates of photosynthesis, largely due to mesophyll limitation. However, plants were photosynthetically active throughout the year, excluding a reversible desiccation period. Common responses to desiccation and low temperature involved chloroplast protection: enhanced thermal energy dissipation, higher carotenoid to Chl ratio and de-epoxidation of the xanthophyll cycle. As specific responses, antioxidants and secondary metabolic routes rose upon desiccation, while putrescine, proline and a variety of sugars rose in winter. The data suggest conserved mechanisms to cope with photo-oxidation during desiccation and cold events, while additional metabolic mechanisms may have evolved as specific adaptations to cold during recent glaciations.

Symbiosis at its limits: ecophysiological consequences of lichenization in the genus Prasiola in Antarctica.

BACKGROUND AND AIMS: Lichens represent a symbiotic relationship between at least one fungal and one photosynthetic partner. The association between the lichen-forming fungus Mastodia tessellata (Verrucariaceae) and different species of Prasiola (Trebouxiophyceae) has an amphipolar distribution and represents a unique case study for the understanding of lichen symbiosis because of the macroalgal nature of the photobiont, the flexibility of the symbiotic interaction and the co-existence of free-living and lichenized forms in the same microenvironment. In this context, we aimed to (1) characterize the photosynthetic performance of co-occurring populations of free-living and lichenized Prasiola and (2) assess the effect of the symbiosis on water relations in Prasiola, including its tolerance of desiccation and its survival and performance under sub-zero temperatures. METHODS: Photochemical responses to irradiance, desiccation and freezing temperature and pressure-volume curves of co-existing free-living and lichenized Prasiola thalli were measured in situ in Livingston Island (Maritime Antarctica). Analyses of photosynthetic pigment, glass transition and ice nucleation temperatures, surface hydrophobicity extent and molecular analyses were conducted in the laboratory. KEY RESULTS: Free-living and lichenized forms of Prasiola were identified as two different species: P. crispa and Prasiola sp., respectively. While lichenization appears to have no effect on the photochemical performance of the alga or its tolerance of desiccation (in the short term), the symbiotic lifestyle involves (1) changes in water relations, (2) a considerable decrease in the net carbon balance and (3) enhanced freezing tolerance. CONCLUSIONS: Our results support improved tolerance of sub-zero temperature as the main benefit of lichenization for the photobiont, but highlight that lichenization represents a delicate equilibrium between a mutualistic and a less reciprocal relationship. In a warmer climate scenario, the spread of the free-living Prasiola to the detriment of the lichen form would be likely, with unknown consequences for Maritime Antarctic ecosystems.

Desiccation Tolerance in Chlorophyllous Fern Spores: Are Ecophysiological Features Related to Environmental Conditions?

Fern spores of most species are desiccation tolerant (DT) and, in some cases, are photosynthetic at maturation, the so-called chlorophyllous spores (CS). The lifespan of CS in the dry state is very variable among species. The physiological, biochemical, and biophysical mechanisms underpinning this variability remain understudied and their interpretation from an ecophysiological approach virtually unexplored. In this study, we aimed at fulfilling this gap by assessing photochemical, hydric, and biophysical properties of CS from three temperate species with contrasting biological strategies and longevity in the dry state: Equisetum telmateia (spore maturation and release in spring, ultrashort lifespan), Osmunda regalis (spore maturation and release in summer, medium lifespan), Matteuccia struthiopteris (spore maturation and release in winter, medium-long lifespan). After subjection of CS to controlled drying treatments, results showed that the three species displayed different extents of DT. CS of E. telmateia rapidly lost viability after desiccation, while the other two withstood several dehydration-rehydration cycles without compromising viability. The extent of DT was in concordance with water availability in the sporulation season of each species. CS of O. regalis and M. struthiopteris carried out the characteristic quenching of chlorophyll fluorescence, widely displayed by other DT cryptogams during drying, and had higher tocopherol and proline contents. The turgor loss point of CS is also related to the extent of DT and to the sporulation season: lowest values were found in CS of M. struthiopteris and O. regalis. The hydrophobicity of spores in these two species was higher and probably related to the prevention of water absorption under unfavorable conditions. Molecular mobility, estimated by dynamic mechanical thermal analysis, confirmed an unstable glassy state in the spores of E. telmateia, directly related to the low DT, while the DT species entered in a stable glassy state when dried. Overall, our data revealed a DT syndrome related to the season of sporulation that was characterized by higher photoprotective potential, specific hydric properties, and lower molecular mobility in the dry state. Being unicellular haploid structures, CS represent not only a challenge for germplasm preservation (e.g., as these spores are prone to photooxidation) but also an excellent opportunity for studying mechanisms of DT in photosynthetic cells.

A field portable method for the semi-quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants.

Desiccation tolerant (DT) plants withstand complete cellular dehydration, reaching relative water contents (RWC) below 30% in their photosynthetic tissues. Desiccation sensitive (DS) plants exhibit different degrees of dehydration tolerance (DHT), never surviving water loss >70%. To date, no procedure for the quantitative evaluation of DHT extent exists that is able to discriminate DS species with differing degrees of DHT from truly DT plants. We developed a simple, feasible and portable protocol to differentiate between DT and different degrees of DHT in the photosynthetic tissues of seed plants and between fast desiccation (< 24 h) tolerant (FDT) and sensitive (FDS) bryophytes. The protocol is based on (1) controlled desiccation inside Falcon tubes equilibrated at three different relative humidities that, consequently, induce three different speeds and extents of dehydration and (2) an evaluation of the average percentage of maximal photochemical efficiency of PSII (Fv /fm) recovery after rehydration. Applying the method to 10 bryophytes and 28 tracheophytes from various locations, we found that (1) imbibition of absorbent material with concentrated salt-solutions inside the tubes provides stable relative humidity and avoids direct contact with samples; (2) for 50 ml capacity tubes, the optimal plant amount is 50-200 mg fresh weight; (3) the method is useful in remote locations due to minimal instrumental requirements; and (4) a threshold of 30% recovery of the initial Fv /fm upon reaching RWC ≤ 30% correctly categorises DT species, with three exceptions: two poikilochlorophyllous species and one gymnosperm. The protocol provides a semi-quantitative expression of DHT that facilitates comparisons of species with different morpho-physiological traits and/or ecological attributes.