Next Article in Journal
First Report of Fungal Pathogens Causing Leaf Spot on Sorghum–Sudangrass Hybrids and Their Interactions with Plants
Next Article in Special Issue
Ratoon Rice Cropping Mitigates the Greenhouse Effect by Reducing CH4 Emissions through Reduction of Biomass during the Ratoon Season
Previous Article in Journal
Monitoring Drought Tolerance in Oil Palm: Choline Monooxygenase as a Novel Molecular Marker
Previous Article in Special Issue
Increasing Planting Density and Reducing N Application Improves Yield and Grain Filling at Two Sowing Dates in Double-Cropping Rice Systems
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 17
10.3390/plants12173090
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications

by
Marina López-Pozo
1,*,
William W. Adams III
2 and
Barbara Demmig-Adams
2
1
Department of Plant Biology & Ecology, University of the Basque Country, 48940 Leioa, Spain
2
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
*
Author to whom correspondence should be addressed.
Plants 2023, 12(17), 3090; https://doi.org/10.3390/plants12173090
Submission received: 24 July 2023 / Revised: 19 August 2023 / Accepted: 25 August 2023 / Published: 28 August 2023
(This article belongs to the Special Issue Crop Cultivation and Low Carbon Agriculture)
Browse Figures
Review Reports Versions Notes

Abstract

:
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.

1. Overview: Lemnaceae for CO2 Mitigation Coupled with Additional Attractive Features

Since the industrial revolution, human activity has resulted in increased levels of various atmospheric pollutants (including greenhouse gases), with atmospheric carbon dioxide (CO2) projected to be twice as high as the pre-industrial revolution level by 2050 [1,2]. As detailed below, duckweeds are efficient at removing CO2 from the atmosphere. In addition to CO2 mitigation, duckweed can provide food (for humans and livestock) of high nutritional quality at high yields with minimal input of light, space, and fertilizer supply (Figure 1). Moreover (Figure 1), duckweed can produce feedstock in the form of starch and lipid for production of biofuels [3,4] and can also serve in wastewater recycling and freshwater reclamation through the removal of nitrogen- and phosphate-based fertilizer run-off and other waste products [5].
Duckweed is also particularly suitable for hydroponic culture, which avoids CO2 release associated with soil tilling [6]. Under natural conditions, duckweed coverage has, furthermore, been shown to reduce or eliminate CO2 emissions from ponds [7].

1.1. Harvest Index

Unlike terrestrial crops, the entire duckweed plant is edible, which in turn reduces (or eliminates) post-harvest waste products. Much or all the plant (in rootless duckweeds) consists of one or several small green organs termed fronds. Figure 2 illustrates that duckweed fronds are unusual in simultaneously acting as the plant’s carbohydrate-source tissue (taking in light and CO2 as direct inputs into photosynthesis to produce sugars) as well as its major carbohydrate-sink tissue (because non-green/non-photosynthetic tissues are virtually absent). In contrast, land plants must invest in substantial non-photosynthetic support structures, including a root system, systems of long-distance vascular transport between roots and shoot, and structural support that allows leaves and stems to be displayed upright and withstand wind and a dry atmosphere. On the other hand, duckweed floating on water has minimal to no need for long-distance transport of nutrients or for structural support. As will be elaborated further in Section 5 below, the green frond is also chiefly responsible for nutrient uptake, especially under ample nutrient supply. Only under low nutrient supply do plants primarily rely on fine roots (with a superior surface-to-volume ratio) for nutrient uptake (except in species without roots).

1.2. The Plant Microbiome’s Multiple Roles

This section provides a brief background on plant-microbiome interactions based largely on the existing literature on terrestrial plants. The microbiome, in addition to maintaining or improving growth, is also responsible for other processes relevant to plant health and nutrition [8]. The microbiome contributes to bioavailability and plant absorption of nutrients (Figure 2), as well as production of various beneficial metabolites [9,10]. Specifically, the microbiome performs biological fixation of atmospheric nitrogen [11] and solubilization of phosphorus [12,13], potassium [10], and iron [14], as well as sulfur oxidation [15]. In addition, members of the microbiome synthesize compounds with structures and functions similar to those of plant hormones, as well as affect the regulation and synthesis of phytohormones produced by the plant itself [16]. The plant microbiome can thus influence plant growth and development [17] and nutrient uptake [18,19]. Additional impacts of the plant microbiome include induction of biotic defense [20], such as induced systemic resistance against pests, insects, and pathogenic fungi [21,22], and plant resistance to biotic stress [23]. Some members of the microbiome can also compete with pathogens for limiting nutrients, inhibit their growth, produce antibiotic compounds, or dissolve fungal cell walls [24,25]. Through these many impacts, the plant microbiome also modulates the plant responses to elevated CO2, which include phytohormone synthesis and signaling [26], as well as altered carbon allocation pathways [27], growth [28], senescence [29], and defenses [30]. In turn, the metabolic activity of the microbiome is supported by energy-rich carbohydrates supplied by the plant [31].

1.3. Growth Rate, Sink Strength, and Response to CO2

This section briefly summarizes literature on how plant growth and carbohydrate storage capacity affect the response to elevated CO2 across plant species and places the exceptionally high growth rate of Lemnaceae into this context. A plant’s sink strength, i.e., its capacity to either utilize or store photosynthetically produced sugar, plays a role in determining plant response to elevated CO2 [32,33,34]. Plants with a high sink strength tend to exhibit sustained new growth, storage, and/or reproductive output under elevated CO2 and otherwise favorable conditions (see Section 2). In contrast, plants with a low sink strength typically not only exhibit no sustained increases in photosynthetic productivity but can instead experience metabolic disruption [34] and accelerate senescence [35] under elevated CO2. Lemnaceae possess the highest relative growth rates among plants [36], which may be related to the fact that aquatic floating plants reinvest their photosynthetic income predominantly into additional productive infrastructure (additional photosynthetic tissue) while having minimal need to invest in non-productive (non-photosynthetic) support structures (see [37]). The resulting rapid frond growth, paired with a considerable starch-storage capacity of the frond itself [4,38], constitutes the major sinks within the plant, with carbohydrate consumption by the plant microbiome (Figure 2) acting as an additional sink [34,39,40] and serving to maintain high plant sink strength. Future research should address the capacity of duckweed to increase the allocation of any surplus sugar underutilized to polysaccharide synthesis (starch [32,41,42] but also cell wall material [43]). Maintenance of new growth under conditions of high carbohydrate supply is supported by matching input of mineral nutrients for an appropriate carbon-to-nitrogen ratio. The interaction of CO2 and nutrient supply is addressed for the case of duckweed (Section 2 below).

2. Context-Dependent Response of Duckweed to Elevated CO2: Role of Nutrients, Light, and Microbiome

This section briefly reviews the response of Lemnaceae to elevated CO2 in the context of different environmental conditions.

2.1. Effect of Nutrient Supply and Plant Microbiome under Moderate Light Supply

Under ample nutrient supply (Figure 3a), elevated CO2 did not inhibit growth (as relative growth rate, RGR, of frond area expansion) in Lemna minor, irrespective of whether the plant microbiome was absent (sanitized plants) or present (inoculated plants). In contrast, RGR was inhibited by elevated CO2 in plants transferred to low nutrient supply when the microbiome was absent but not when the microbiome was present (Figure 3b). Plant-microbiome interaction thus supported L. minor’s performance under elevated CO2 in combination with limiting nutrient supply. It should be noted that this was a snapshot in time upon transfer of duckweed from high to low nutrient supply and that responses may change after internal nitrogen sources [storage protein] become further depleted.
The fact that elevated CO2 did not increase RGR in L. minor under ample nutrient supply suggests that RGR was already maximal under these conditions, allowing no further stimulation by elevated CO2. These fronds were grown in a nutrient medium containing both nitrate and ammonium. The following section addresses the additional effect of high light (in combination with elevated CO2) and raises the possibility that duckweed responses to both elevated CO2 and inoculation may vary depending on the specific form of nitrogen supplied (nitrate versus ammonium).

2.2. Response of Inoculated Lemna Plants under High Light and Ample Nutrient Supply

Figure 4a illustrates that RGR was unaffected by elevated CO2 even in combination with continuous high light (700 µmol photons m−2 s−1) input in inoculated L. minor plants (with their microbiome) growing with ample nutrient supply. Such a combination of high inputs from both light and CO2 can trigger detrimental effects in some plants because of extreme surplus sugar accumulation and resulting metabolic disruption [34]. The ability of duckweed to maintain its high RGR under such circumstances (Figure 4a) is consistent with early reports for duckweed by other authors (see, e.g., [45,46]) that elevated CO2 had no effect on RGR.
A somewhat different response of duckweed to elevated CO2 was reported by Toyama et al. [47], who grew plants in nutrient-replete nitrate-only medium (without ammonium) and reported that plant inoculation with beneficial microbes caused RGR to increase from ~0.36 to ~0.55 with concomitant changes in plant nitrogen metabolism and amino acid profile. Future research should compare responses side-by-side for duckweed grown in ammonium-containing versus ammonium-free media. Figure 4 compares responses under high light supply (Figure 4a,c,e,g,i) with those under moderate light supply (Figure 4b,d,f,h,j), all in nutrient-replete medium. Area RGR was just below 0.5 under 200 µmol photons m−2 s−1 (Figure 4b) and just above 0.5 under 700 µmol photons m−2 s−1 in either ambient or elevated CO2 in ammonium-containing medium (Figure 4a). Section 5 provides further detail on the preference of aquatic floating plants for ammonium.
For the sets of plants with their microbiome shown in Figure 4, dry biomass accumulation was unaffected by elevated CO2 under continuous high growth light intensity (700 µmol photons m−2 s−1) but was stimulated somewhat (from just below to just above half of that in very high light) under moderate light of 200 µmol photons m−2 s−1. This finding is consistent with the notion that elevated CO2 can have a stimulatory effect when plant productivity is not already saturated. One would consequently predict a subsequent downregulation of photosynthesis (affecting various chloroplast constituents) by elevated CO2 under the condition (very high light) where productivity is already saturated but not under the condition (lower light) where productivity can still increase.
Pioneering work by Gale et al. [48] demonstrated this effect for duckweed—with an initial increase in photosynthesis rate upon increasing CO2 quickly, giving rise to a pronounced decrease in photosynthesis rate under high growth light intensity with a long photoperiod but not under low growth light intensity and/or a short photoperiod. The data in Figure 4 illustrates the results of this secondary downregulation of photosynthesis. Total chlorophyll content was downregulated in plants exposed to elevated versus ambient CO2 under 700 µmol photons m−2 s−1 with more surplus sugar, but not in plants growing under 200 µmol photons m−2 s−1 with less surplus sugar (Figure 4e,f). This photosynthetic downregulation but unimpeded growth under elevated CO2 reflects the general ability of plants (including duckweed) to support the same growth rate with a lesser investment in photosynthetic machinery in the presence of elevated CO2 by virtue of acclimatory downsizing of the photosynthetic apparatus to counteract surplus sugar production [34,37,49]. This downsizing of the photosynthetic apparatus includes downregulation of chlorophyll in the plants grown under continuous high light in the presence of elevated CO2 (Figure 4g) as well as downregulation of carotenoids (Figure 4h) bound to the same light-harvesting protein complexes as chlorophyll (see [37]). Such effects, as documented in Figure 4 for duckweed, are also observed in other plants. Because these carotenoids serve as important human micronutrients [50], their decline constitutes a cost to plant nutritional quality for the human (or livestock) consumer [51,52]. However, as Figure 4 illustrates, this cost can be prevented by growing plants under a lower light intensity (Figure 4g,h).
Overall frond protein content was also lower under elevated CO2 in the presence of continuous high light (Figure 4j), albeit to a lesser extent than chlorophyll or carotenoid levels. This finding is likely unique to duckweed and is consistent with the role of Ribulose 1,5-bisphosphate Carboxylase/Oxygenase (RuBisCO), the predominant protein in fronds, not only in photosynthesis but also as a vegetative storage protein in duckweed [53] that is maintained at high levels across a wide range of growth light environments [54,55]. This welcome finding thus illustrates the unique ability of duckweed to maintain high protein content under elevated CO2. Moreover, Figure 4 illustrates that any negative effects of elevated CO2 on both protein and carotenoid micronutrient content can be prevented by growing plants under a lower light supply (Figure 4j) with ample nutrient supply. It is noteworthy that when the same relatively low light supply was paired with limiting nutrient supply, downregulation of carotenoid content was observed in sanitized plants [39,40]. In contrast, plants inoculated with their microbiome exhibited less or no such downregulation [39].

3. Multiple Advantages of Growing Duckweed under Low Light Intensity

This section compares key features of plant responses to light quality in land plants with those of Lemnaceae. As stated above, plant carotenoid content—with respect to the important human micronutrients lutein and provitamin A (β-carotene)—is highest under low growth light intensity in duckweed [38,56] as well as other plants. However, unlike terrestrial plants, duckweed can be grown under low light without a decline in RGR and with a maximally high protein content per dry mass [55]. In contrast to land plants, Lemna thus grew similarly fast, with the same light- and CO2-saturated photosynthetic capacity and as much protein per frond area (and more per dry biomass), under low versus high growth light intensity [56,57]. Such a high maximal photosynthetic capacity even in low-light-grown plants is consistent with duckweeds’ high RuBisCO content [55,58]. Overall, these findings indicate that the accumulation of desirable products relative to the required light energy input is most favorable in duckweed grown under low light intensity [56].
Moreover, unlike land plants with multiple layers of leaves, duckweeds have no fixed plant tiers and possess relatively thin leaves, resulting in minimal self-shading and the ability to saturate the whole plant even at low levels of incident light intensity. This scenario may also explain the fact that duckweeds accumulate exceptionally large amounts of antioxidants that serve as essential (= must be acquired from the diet) human micronutrients with antioxidative and anti-inflammatory effects (antioxidant vitamins A, C, E, carotenoids, and phenolics) [37,53,55,59,60]. In contrast, land plants have lower average levels of antioxidants per leaf dry mass, with relatively low antioxidant levels in the lower versus upper portions of individual leaves [61,62] as well as lower versus upper leaves in a tiered plant canopy [61]. In addition, land plants downsize their pools of various antioxidants and other essential human micronutrients under low growth light intensity more strongly than duckweed [54]. This difference between duckweeds and land plants, along with duckweed’s high RGR under low light [54], is advantageous for energy-efficient cultivation of duckweed in controlled environments with relatively low light supply (see also Section 7 and Section 8).

4. Light Quality Effects

The upper versus lower portions of leaves, as well as whole upper versus lower leaves, of most land plants absorb most of the blue and red fractions of incident sunlight and dissipate much of this as heat (via a photoprotective process [63]) at peak irradiance in natural settings, even in fast-growing plants (e.g., [64]). In tiered land plants, only little blue and red light penetrates down to the lower layers of leaves or canopies. In those lower levels, green and far-red portions of the solar spectrum thus represent most of the available energy [65]. These lower layers may require additional support from photosynthate supplied by the upper layers of the leaf or plant. Plants with such tiered structures may benefit from inclusion of wavelengths other than blue and red in their growth light supply. On the other hand, duckweeds (without fixed tiered layers and relatively thin fronds) may reach photosynthetic saturation with just the blue and red portions of the light spectrum, with little to no additional stimulation by the green and far-red regions of the solar spectrum.

5. Duckweed Preference for Ammonium versus Nitrate

Because ammonium is the most common form of nitrogenous waste produced by heterotrophic aquatic organisms, it is not surprising that aquatic duckweeds are highly efficient at nitrogen uptake in the form of ammonium (Figure 5a,b) and prefer ammonium over nitrate [66]. Lemna minor, transferred from ample to low nutrient supply, preferentially removed ammonium from the medium and only started drawing down the nitrate pool after the ammonium pool had been depleted (Figure 5d). Over the first two days following transfer from ample to limiting nutrient supply (Figure 5a,c; phase 1), there was no draw-down of nitrate and the draw-down of ammonium was much less pronounced compared to the next several days (Figure 5b,d, phase 2). This result suggests that new fronds growing during phase 1 were supported by internal nitrogen stores (vegetative storage protein). For the relatively low light intensities used here, a longer photoperiod led to more pronounced uptake of nitrogen compounds than a shorter photoperiod (Figure 5). A similar scenario, with nitrate uptake commencing only after ammonium had been consumed, was also seen in the duckweed genus Landoltia [67,68]. Duckweeds thus have a high fertilizer-use efficiency and capacity for phytoremediation [5] such as removal of fertilizer runoff from freshwater bodies and fertilizer retention in, e.g., rice paddies [69].
In closed photobioreactors, increased CO2 supply enhanced removal of nitrate and phosphate from the medium by duckweed [4], along with increasing RGR and starch content, indicating that higher nutrient removal efficiency was likely due to a higher growth rate under elevated CO2. In duckweeds, unlike in land plants, fronds and roots are both active in nutrient uptake, and both organs are more efficient at taking up ammonium compared to nitrate [70,71,72]. Whereas frond activity accounted for the majority of nutrient update under high nutrient supply, roots were responsible for most of both ammonium and nitrate uptake at low nutrient supply [70]. The ability to take up high levels of ammonium without experiencing the toxicity effects commonly observed in land plants [73,74] is related to duckweeds’ ability to rapidly convert ammonium to protein via an expanded glutamine oxoglutarate aminotransferase (involved in synthesis of glutamate from glutamine and α-ketoglutarate) gene family [75] and storage of large quantities of protein throughout the plant [76]. In this respect, duckweeds are like legumes—land plants capable of using ammonium and storing high protein levels in their seeds (rather than throughout the plant as in duckweeds). Both soybean and duckweed have a proclivity for taking up ammonium as well as accepting ammonium from their endogenous N2-fixing Rhizobium symbionts.

6. Interactions among Nutrient Transporters, Hormones, Elevated CO2, and the Microbiome

This section highlights interactions between elevated CO2 and transport/metabolism of nitrogen compounds while comparing the response of duckweeds with that of various terrestrial plants. Duckweeds can form thin, slender root-like appendices and increase their length, and thus the plant’s surface-to-volume area, for nutrient uptake under low nitrogen supply [70]. “Nitrate and hormonal signaling crosstalk” (for a review, see Vega et al. [77]) has been characterized in Arabidopsis thaliana, where a high-affinity nitrate transporter was linked to regulation of lateral root growth and increased access to mineral nutrients under limiting nutrient supply [77]. Elevated CO2 has been shown to alter the expression of transporters for nitrogen compounds in a manner that depends on nutrient concentration, plant species, and overall plant response to elevated CO2 [78]. In tall fescue, elevated CO2 increased root growth and did so even more under moderate versus low nitrate supply [79]. In other scenarios, elevated CO2 decreased, and thus interfered with, high-affinity uptake of nitrogen compounds under limiting nitrogen supply [78]. The plant microbiome can stimulate root growth and nutrient uptake in various species [80], including rice [81,82], maize [83], and soybean [82]. Duckweeds [84] and soybean [85] can thrive under low nitrogen supply due to partnerships with N2-fixing endophytic microbial symbionts, such as Rhizobium lemnae for Lemna species [86] and various rhizobia species for soybean [87]. The ability to metabolize large amounts of ammonium thus presumably allows duckweeds to take advantage of plant-microbe interaction to restore carbon-nitrogen balance under elevated CO2 in combination with low nitrogen supply (see Figure 3 above). In such situations, the microbiome (i) acts as a carbon sink that helps remove surplus sugar, (ii) supports nitrogen use for new growth, and (iii) supports a plant hormone balance conducive to continued new growth, all of which counteract feedback downregulation of the photosynthetic apparatus and the associated aspects of plant nutritional quality.
Whether or not elevated CO2 stimulates plant productivity can also depend on interaction between the plant microbiome and plant developmental stage. A stimulation of soybean seed yield by elevated CO2 was only seen in nodulated soybean lines (with endophytic N2-fixing symbionts) but not in non-nodulated mutant lines of soybean and only during the reproductive phase—with no growth stimulation during the vegetative phase of plant growth [88]. Developmental effects should play a minor role in duckweeds that mainly reproduce by vegetative cloning and rarely flower [89]. No additional improvement in soybean productivity was obtained when using bacteria with higher N2-fixation rates for inoculation [90]. Moreover, inoculation with bacterial strains isolated from soybeans grown under elevated CO2 caused metabolic disruption in plants grown under ambient CO2 [91].

7. Commercial Applications of Duckweed

7.1. Human and Livestock Nutrition

Based on its nutritional composition, duckweed can provide adequate nutrition for both humans and livestock. Due to accumulation of large amounts of vegetative storage protein throughout the plant, duckweed can produce between 20 and 30% of crude protein, which is equivalent to 20× the amount of protein produced by soybeans (per unit cultivated area) [92] and even much higher amounts than those produced by cereals [93]. A key factor in the superior protein production by duckweed is protein accumulation in all its tissues compared to only in the seeds of land plants. Furthermore, duckweed protein quality is the same as that of soybean or milk—with all essential amino acids humans must obtain from their diet [94]. The quantity and quality (amino acid profile) of crude protein are directly related to the amount of nitrogen in the medium (see Section 5) [95]. The main protein in duckweed is RuBisCO, a non-allergenic source of all nine essential amino acids with high digestibility, making it an ideal candidate for animal feed [96]. Duckweed also contains large amounts of the non-essential amino acid glutamic acid, which has health benefits for humans and other animals [97]. However, similar to other plants (e.g., spinach or beet greens [98]), some duckweeds (e.g., genus Lemna) can contain high levels of anti-nutritive compounds such as oxalic acid [99]. This compound chelates calcium ions and other micronutrients, hindering their absorption in the intestine and compromising human health [100,101]. In contrast, duckweeds in the genus Wolffia contain minimal and thus safe amounts of anti-nutrients, which makes this genus suitable as a safe source of human food and highly recommended due to its superior nutritional characteristics regarding proteins, vitamins, and other micronutrients mentioned above. There are other potentially anti-nutritive compounds (nitrates, tannins, phytates, dioxins, and cyanogenic glycosides [102]) that require further investigation in duckweeds. Wolffia globosa (Mankai) has long been consumed as a high-protein source in Japan [103].
Sufficient intake of protein and other micronutrients (such as vitamins and antioxidants) is essential for optimal body function [50] and one of the current global challenges [104] facing human society and science. Currently, more than 15% of people worldwide cannot achieve the recommended daily protein intake and fall behind even further with respect to micronutrients (up to a 25% deficit), leading to malnutrition [105,106]. The WHO “Global Strategy for Food Safety (2022–2030)” program (https://www.who.int/publications/i/item/9789240057685; URL accessed on 27 August 2023) aims to “ensure that all people, everywhere, consume safe and healthy food so as to reduce the burden of foodborne diseases” [107]. A resilient food system is thus needed that is fit for the future, with concomitant benefits for the health of individual people and societies as well as for the physical and natural environment, including climate.
Plant–microbe interaction in duckweed also has additional nutritional benefits beyond minimizing the loss of photosynthesis-associated micronutrients under elevated CO2 (see above; [39,40]). In contrast to edible products from other plants, Mankai contains high levels of vitamin B12—even after plants have been surface sterilized [108]. The synthesis of vitamin B12 is carried out by bacteria and archaea absent in other vegetable food products [109]. Presence of vitamin B12 in Mankai is thus apparently due to as-yet undefined B12-producing bacteria that must be endophytic and produce high levels of vitamin B12 even in otherwise axenic Mankai cultures [94,108]. Because other plants are not a source of vitamin B12, this vitamin is currently obtained mainly from animal products (clams and beef liver are rich in vitamin B12; [110]). The current trend towards greater consumption of plant versus animal products [111] increases the risk of deficiencies in vitamin B12 and associated health problems [112]. To meet the need for B12 intake in diets low in animal products, algae had been suggested as a source for this compound, but recent studies showed that vitamin B12 occurs in algae in a form (pseudo B12) not usable by humans and even capable of competing with the usable forms of B12 [113]. In contrast, Makai can be considered a good addition to meat-free diets. However, the benefits of Mankai go farther because Mankai intake also positively modified the gut microbiota and increased the diversity of genes (as assessed via 16S rRNA) related to the absorption of vitamin B12 [108]. A recent series of human clinical trials provided a comprehensive summary of these health benefits, including improved serum levels of vitamin B12, iron, and phenolics, gut microbiome composition, brain function, blood glucose control/insulin sensitivity, cardiovascular health, weight management, and decreased fat accumulation resulting from supplementation with a combination of Mankai and green tea [108,114,115,116,117,118,119,120,121].

7.2. Feedstock for Biofuels

This section highlights plant use as feedstock for biofuels while comparing relevant features of Lemnaceae and terrestrial plants. Problems with current production systems for biofuel feedstocks include food–fuel conflict and undesirable environmental impacts, both due to the use of staple food crops with relatively high requirements for irrigation and fertilization. Production of maize, yucca, or sweet potato for biofuel increased the price of basic foods and threatened food security [122]. In association with these crops’ high fertilizer requirement, excessive nutrient runoff caused environmental problems [123]. Therefore, it is urgent to identify new, sustainable feedstocks for biofuel production.
Due to its high starch content (see, e.g., [38]), duckweed is suitable for bioethanol production via starch hydrolysis and subsequent alcoholic fermentation. The yield of bioethanol from duckweed has been estimated to potentially reach 6420 L ha−1, which is about 50% above that obtained for ethanol based on corn [3,123,124] and production could continue throughout the year. The ability of Lemna to accumulate starch without needing large amounts of light [38] and to respond to elevated CO2 with increased starch accumulation would support high biofuel production yields [4]. Biofuel production could thus be paired with wastewater treatment, as previously shown for systems that combine wastewater recycling with livestock feed production [92]. Moreover, effective sequestration of atmospheric CO2 into starch by duckweed would contribute to CO2 mitigation and climate control. Such systems could serve as a model for future regenerative life support systems, providing both food and fuel.
Additional mechanisms have been documented through which starch accumulation by Lemna can be enhanced through restriction of nutrient supply with minimal impact on growth rate [123,125,126]. Restriction of sulfur supply showed the greatest promise with respect to stimulation of starch accumulation with negligible growth impact [125], while nitrogen limitation increased starch yield at the expense of growth and overall biomass production [125]. Recent progress has also been reported in engineering duckweed for enhanced accumulation of lipids [127] that could be used to produce biodiesel.

8. Agricultural Technology: Hydroponics and Vertical Farming

This section highlights plant use in vertical and hydroponic farming while again comparing relevant features of Lemnaceae and terrestrial plants. Documented advantages of hydroponic crops include the highly efficient use of water and nutrients [6] by crops such as tomatoes, cucumbers, and other vegetables [6,72]. Recirculating hydroponic systems further increase resource-use efficiency [128]. Duckweed has a high potential for use in closed hydroponic systems consisting of multiple vertical layers (Figure 6), with controlled temperature, CO2, light intensity, quality, and photoperiod, as well as nutrient composition [129]. Vertical design would further optimize use of space [72,105,130] when using a diminutive, 100% edible plant like duckweed. Control of environmental factors allows optimization of biomass quality, i.e., micronutrients (vitamins, antioxidants) and proteins for use as food [131] or either starch or lipid content for use as biofuel feedstock. Recirculation of nutrients and water prevents nutrients release into the environment and resulting land and water pollution [132], as well as minimizes water loss [128] by reducing evaporation (proximity between different vertical levels could act as “semi-closed lids”). Duckweed, furthermore, thrives on a film of water [133]. Vertical, hydroponics-based farming is also suitable for continuous production throughout the year.
Figure 6 depicts a system where layers of duckweed are interspersed with layers of light-emitting diodes (LEDs), resulting in illumination of duckweed layers from both below and above, a design first suggested by Gale et al. [48]. Figure 6 features a mix of blue and red LEDs that, due to minimal self-shading within a single layer of fronds, may support maximal productivity with minimal energy input. We suggest using both red and blue wavelengths to support not only photosynthesis but also plant morphogenesis [134] and blue-light-triggered phenolic production [135].

9. Conclusions

Duckweed is an attractive candidate to sequester atmospheric CO2 while at the same time producing multiple products and services of human interest. In addition, the aquatic cultivation of Lemna avoids releasing CO2 into the atmosphere from the soil, as can occur during terrestrial plant cultivation.
Due to its high lipid- and starch-storage capacity, duckweed is a promising crop for production of biofuels, and its exceptionally high protein and human micronutrient content makes it a food with high nutritional value. Duckweed’s outstanding ability to absorb ammonium (and turn it into protein), furthermore, serves in wastewater treatment. Its ability to sequester CO2 is enhanced by presence of a microbiome that counteracts the accumulation of surplus sugars and resulting feedback inhibition of photosynthesis (and associated loss of human micronutrients).
All these characteristics make duckweed unusually productive in small cultivation areas or volumes. The combination of its diminutive size with exceptionally high relative growth rates, harvest index (no inedible parts), and nutrient density makes this plant ideal for vertical growth in multiple stacked layers (Figure 6). Whereas multi-layer cultivation may also be attractive with terrestrial plants, it offers clear advantages in duckweed with highly efficient use of space, energy, nutrient supply, and gas exchange with the atmosphere.

Author Contributions

Conceptualized the review, B.D.-A. with contributions from W.W.A.III and M.L.-P.; conducted the experiments resulting in data shown in Figure 4j and Figure 5, M.L.-P.; prepared other figures based on data from previously published studies, M.L.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This research is based on data from research funded by the Translational Research Institute for Space Health through Cooperative Agreement NNX16AO69A and the University of Colorado.

Data Availability Statement

The data discussed in this review are shown here and/or in previously published studies.

Acknowledgments

We thank Madeleine Zenir for help with experimental development and nitrogen analyses shown in Figure 5.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Stocker, T.F.; Qin, D.; Plattner, G.-K.; Tignor, M.; Allen, S.K.; Boschung, J.; Nauels, A.; Xia, Y.; Bex, V.; Midgley, P.M. (Eds.) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In IPCC, 2013: Climate Change 2013: The Physical Science Basis; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2013; p. 1535. [Google Scholar] [CrossRef]
  2. Liu, K.; Harrison, M.T.; Yan, H.; Liu, D.L.; Meinke, H.; Hoogenboom, G.; Wang, B.; Peng, B.; Guan, K.; Jaegermeyr, J.; et al. Silver lining to a climate crisis in multiple prospects for alleviating crop waterlogging under future climates. Nat. Commun. 2023, 14, 765. [Google Scholar] [CrossRef] [PubMed]
  3. Cheng, J.J.; Stomp, A.M. Growing duckweed to recover nutrients from wastewaters and for production of fuel ethanol and animal feed. Clean—Soil Air Water 2009, 37, 17–26. [Google Scholar] [CrossRef]
  4. Mohedano, R.A.; Costa, R.H.R.; Filho, P.B. Effects of CO2 concentration on nutrient uptake and starch accumulation by duckweed used for wastewater treatment and bioethanol production. Rev. Latinoam. Biotecnol. Ambient. Algal 2016, 7, 30–41. [Google Scholar] [CrossRef]
  5. Baek, G.Y.; Saeed, M.; Choi, H.K. Duckweeds: Their utilization, metabolites and cultivation. Appl. Biol. Chem. 2021, 64, 73. [Google Scholar] [CrossRef]
  6. Sharma, N.; Acharya, S.; Kumar, K.; Singh, N.; Chaurasia, O.P. Hydroponics as an advanced technique for vegetable production: An overview. J. Soil Water Conserv. 2018, 17, 364–371. [Google Scholar] [CrossRef]
  7. Rabaey, J.; Cotner, J. Pond greenhouse gas emissions controlled by duckweed coverage. Front. Environ. Sci. 2022, 10, 889289. [Google Scholar] [CrossRef]
  8. Valenzuela-Aragon, B.; Parra-Cota, F.I.; Santoyo, G.; Arellano-Wattenbarger, G.L.; de los Santos-Villalobos, S. Plant-assisted selection: A promising alternative for in vivo identification of wheat (Triticum turgidum L. subsp. Durum) growth promoting bacteria. Plant Soil 2019, 435, 367–384. [Google Scholar] [CrossRef]
  9. Kong, Z.; Glick, B.R. The role of bacteria in phytoremediation. In Applied Bioengineering: Innovations and Future Directions; Yoshida, T., Ed.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2017; pp. 327–353. [Google Scholar] [CrossRef]
  10. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef] [PubMed]
  11. Mukherjee, R.; Sen, S. Role of biological nitrogen fixation (BNF) in sustainable agriculture: A Review. Int. J. Adv. Life Sci. Res. 2021, 4, 1–7. [Google Scholar] [CrossRef]
  12. Alori, E.T.; Dare, M.O.; Babalola, O.O. Microbial inoculants for soil quality and plant health. In Sustainable Agriculture Reviews; Lichtfouse, E., Ed.; Springer: Cham, Switzerland, 2017; Volume 22, pp. 281–307. [Google Scholar] [CrossRef]
  13. Emami, S.; Alikhani, H.A.; Pourbabaee, A.A.; Etesami, H.; Motasharezadeh, B.; Sarmadian, F. Consortium of endophyte and rhizosphere phosphate solubilizing bacteria improves phosphorous use efficiency in wheat cultivars in phosphorus deficient soils. Rhizosphere 2020, 14, 100196. [Google Scholar] [CrossRef]
  14. Kramer, J.; Özkaya, Ö.; Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 2020, 18, 152–163. [Google Scholar] [CrossRef]
  15. Roy, S.; Roy, M. Bioleaching of heavy metals by sulfur oxidizing bacteria: A Review. Int. Res. J. Environ. Sci. 2015, 4, 75–79. [Google Scholar]
  16. Oleńska, E.; Małek, W.; Wójcik, M.; Swiecicka, I.; Thijs, S.; Vangronsveld, J. Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: A methodical review. Sci. Total Environ. 2020, 743, 140682. [Google Scholar] [CrossRef] [PubMed]
  17. Shah, V.; Daverey, A. Phytoremediation: A multidisciplinary approach to clean up heavy metal contaminated soil. Environ. Technol. Innov. 2020, 18, 100774. [Google Scholar] [CrossRef]
  18. Krouk, G.; Lacombe, B.; Bielach, A.; Perrine-Walker, F.; Malinska, K.; Mounier, E.; Hoyerova, K.; Tillard, P.; Leon, S.; Ljung, K.; et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 2010, 18, 927–937. [Google Scholar] [CrossRef]
  19. Anfang, M.; Shani, E. Transport mechanisms of plant hormones. Curr. Opin. Plant Biol. 2021, 63, 102055. [Google Scholar] [CrossRef] [PubMed]
  20. Romero-Contreras, Y.J.; Ramírez-Valdespino, C.A.; Guzmán-Guzmán, P.; Macías-Segoviano, J.I.; Villagómez-Castro, J.C.; Olmedo-Monfil, V. Tal6 from Trichoderma atroviride is a LysM effector involved in mycoparasitism and plant association. Front. Microbiol. 2019, 10, 2231. [Google Scholar] [CrossRef]
  21. Akhtar, S.S.; Mekureyaw, M.F.; Pandey, C.; Roitsch, T. Role of cytokinins for interactions of plants with microbial pathogens and pest insects. Front. Plant Sci. 2020, 10, 1777. [Google Scholar] [CrossRef]
  22. Pieterse, C.M.J.; Zamioudis, C.; Berendsen, R.L.; Weller, D.M.; Van Wees, S.C.M.; Bakker, P.A.H.M. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 2014, 52, 347–375. [Google Scholar] [CrossRef]
  23. Pathania, P.; Rajta, A.; Singh, P.C.; Bhatia, R. Role of plant growth-promoting bacteria in sustainable agriculture. Biocatal. Agric. Biotechnol. 2020, 30, 101842. [Google Scholar] [CrossRef]
  24. Glick, B.R. Beneficial Plant-Bacterial Interactions, 2nd ed.; Springer Nature: Cham, Switzerland, 2020. [Google Scholar] [CrossRef]
  25. Ma, Y.; Oliveira, R.S.; Freitas, H.; Zhang, C. Biochemical and molecular mechanisms of plant-microbe-metal interactions: Relevance for phytoremediation. Front. Plant Sci. 2016, 7, 918. [Google Scholar] [CrossRef] [PubMed]
  26. Yang, H.; Wang, T.; Yu, X.; Yang, Y.; Wang, C.; Yang, Q.; Wang, X. Enhanced sugar accumulation and regulated plant hormone signalling genes contribute to cold tolerance in hypoploid Saccharum spontaneum. BMC Genom. 2020, 21, 507. [Google Scholar] [CrossRef]
  27. Ainsworth, E.A.; Rogers, A.; Nelson, R.; Long, S.P. Testing the “source-sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agric. For. Meteorol. 2004, 122, 85–94. [Google Scholar] [CrossRef]
  28. Asha, A.D.; Nivetha, N.; Krishna, G.K.; Thakur, J.K.; Rathi, M.S.; Manjunatha, B.S.; Chinnusamy, V.; Paul, S. Amelioration of short-term drought stress during different growth stages in Brassica juncea by rhizobacteria mediated maintenance of ROS homeostasis. Physiol. Plant. 2021, 172, 1880–1893. [Google Scholar] [CrossRef] [PubMed]
  29. Poupin, M.J.; Timmermann, T.; Vega, A.; Zuñiga, A.; González, B. Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS ONE 2013, 8, e69435. [Google Scholar] [CrossRef] [PubMed]
  30. Salwan, R.; Sharma, M.; Sharma, A.; Sharma, V. Insights into plant beneficial microorganism-triggered induced systemic resistance. Plant Stress 2023, 7, 100140. [Google Scholar] [CrossRef]
  31. Glick, B.R. Soil microbes and sustainable agriculture. Pedosphere 2018, 28, 167–169. [Google Scholar] [CrossRef]
  32. Körner, C. Carbon limitation in trees. J. Ecol. 2003, 91, 4–17. [Google Scholar] [CrossRef]
  33. Aranjuelo, I.; Cabrera-Bosquet, L.; Morcuende, R.; Avice, J.C.; Nogués, S.; Araus, J.L.; Martínez-Carrasco, R.; Pérez, P. Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? J. Exp. Bot. 2011, 62, 3957–3969. [Google Scholar] [CrossRef]
  34. Demmig-Adams, B.; Polutchko, S.K.; Zenir, M.C.; Fourounjian, P.; Stewart, J.J.; López-Pozo, M.; Adams, W.W., III. Intersections: Photosynthesis, abiotic stress, and the plant microbiome. Photosynthetica 2022, 60, 59–69. [Google Scholar] [CrossRef]
  35. Pourtau, N.; Jennings, R.; Pelzer, E.; Pallas, J.; Wingler, A. Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 2006, 224, 556–568. [Google Scholar] [CrossRef] [PubMed]
  36. Sree, K.S.; Sudakaran, S.; Appenroth, K.J. How fast can angiosperms grow? Species and clonal diversity of growth rates in the genus Wolffia (Lemnaceae). Acta Physiol. Plant. 2015, 37, 31–39. [Google Scholar] [CrossRef]
  37. Demmig-Adams, B.; López-Pozo, M.; Polutchko, S.K.; Fourounjian, P.; Stewart, J.J.; Zenir, M.C.; Adams, W.W., III. Growth and nutritional quality of Lemnaceae viewed comparatively in an ecological and evolutionary context. Plants 2022, 11, 145. [Google Scholar] [CrossRef]
  38. Stewart, J.J.; Adams, W.W., III; Escobar, C.M.; López-Pozo, M.; Demmig-Adams, B. Growth and essential carotenoid micronutrients in Lemna gibba as a function of growth light intensity. Front. Plant Sci. 2020, 11, 480. [Google Scholar] [CrossRef]
  39. Zenir, M.C.; López-Pozo, M.; Polutchko, S.K.; Stewart, J.J.; Adams, W.W., III; Escobar, A.; Demmig-Adams, B. Productivity and nutrient quality of Lemna minor as affected by microbiome, CO2 level, and nutrient supply. Stresses 2023, 3, 69–85. [Google Scholar] [CrossRef]
  40. López-Pozo, M.; Zenir, M.C.; Polutchko, S.K.; Stewart, J.J.; Adams, W.W., III; Escobar, A.; Demmig-Adams, B. Effects of growth environment on Lemna minor. E Sch. Community Encycl. 2023, 40481. Available online: https://encyclopedia.pub/entry/40481 (accessed on 24 August 2023).
  41. Agüera, E.; De la Haba, P. Leaf senescence in response to elevated atmospheric CO2 concentration and low nitrogen supply. Biol. Plant. 2018, 62, 401–408. [Google Scholar] [CrossRef]
  42. Poorter, H.; Van Berkel, Y.; Baxter, R.; Den Hertog, J.; Dijkstra, P.; Gifford, R.M.; Griffin, K.L.; Roumet, C.; Roy, J.; Wong, S.C. The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant Cell Environ. 1997, 20, 472–482. [Google Scholar] [CrossRef]
  43. Louback, E.; Batista, D.S.; Pereira, T.A.R.; Mamedes-Rodrigues, T.C.; Silva, T.D.; Felipe, S.H.S.; Rocha, D.I.; Steinmacher, D.A.; Otoni, W.C. CO2 enrichment leads to altered cell wall composition in plants of Pfaffia glomerata (Spreng.) Pedersen (Amaranthaceae). Plant Cell Tissue Organ Cult. 2021, 145, 603–613. [Google Scholar] [CrossRef]
  44. Schenk, R.U.; Hildebrandt, A.C. Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can. J. Bot. 1972, 50, 199–204. [Google Scholar] [CrossRef]
  45. Björndahl, G.; Nilsen, S. Growth potential of Lemna gibba: Effect of CO2 enrichment at high photon flux rate. Aquat. Bot. 1985, 22, 79–82. [Google Scholar] [CrossRef]
  46. Smernoff, D.T. Interactions between Carbon Assimilation and Nitrogen Metabolism at Elevated Carbon Dioxide in Duckweed Species and Aphanizomenon flos-aquae; Stanford University ProQuest Dissertations Publishing: Ann Arbor, MI, USA, 1992. [Google Scholar]
  47. Toyama, T.; Mori, K.; Tanaka, Y.; Ike, M.; Morikawa, M. Growth promotion of giant duckweed Spirodela polyrhiza (Lemnaceae) by Ensifer sp. SP4 through enhancement of nitrogen metabolism and photosynthesis. Mol. Plant-Microbe Interact. 2022, 35, 28–38. [Google Scholar] [CrossRef]
  48. Gale, J.; Smernoff, D.T.; Macler, B.A.; MacElroy, R.D. Carbon balance and productivity of Lemna gibba, a candidate plant for CELSS. Adv. Space Res. 1989, 9, 43–52. [Google Scholar] [CrossRef]
  49. Krapp, A.; Stitt, M. An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 1995, 195, 313–323. [Google Scholar] [CrossRef]
  50. Demmig-Adams, B.; López-Pozo, M.; Stewart, J.J.; Adams, W.W., III. Zeaxanthin and lutein: Photoprotectors, anti-inflammatories, and brain food. Molecules 2020, 25, 3607. [Google Scholar] [CrossRef] [PubMed]
  51. Dong, J.; Gruda, N.; Lam, S.K.; Li, X.; Duan, Z. Effects of elevated CO2 on nutritional quality of vegetables: A review. Front. Plant Sci. 2018, 9, 924. [Google Scholar] [CrossRef]
  52. Pal, M.; Karthikeyapandian, V.; Jain, V.; Srivastava, A.C.; Raj, A.; Sengupta, U.K. Biomass production and nutritional levels of berseem (Trifolium alexandrium) grown under elevated CO2. Agric. Ecosyst. Environ. 2004, 101, 37–38. [Google Scholar] [CrossRef]
  53. Appenroth, K.J.; Sree, K.S.; Böhm, V.; Hammann, S.; Vetter, W.; Leiterer, M.; Jahreis, G. Nutritional value of duckweeds (Lemnaceae) as human food. Food Chem. 2017, 217, 266–273. [Google Scholar] [CrossRef]
  54. López-Pozo, M.; Adams, W.W., III; Polutchko, S.K.; Demmig-Adams, B. Terrestrial and floating aquatic plants differ in acclimation to light environment. Plants 2023, 12, 1928. [Google Scholar] [CrossRef]
  55. Polutchko, S.K.; Stewart, J.J.; Mcnamara, M.; Garcia, N.D.; López-Pozo, M.; Adams, W.W., III; Demmig-Adams, B. Lemna as a sustainable, highly nutritious crop: Nutrient production in different light environments. Nutraceuticals 2022, 2, 350–364. [Google Scholar] [CrossRef]
  56. Polutchko, S.K.; Stewart, J.J.; Demmig-Adams, B. Integrative view of the nutrition of the eye. In Nutraceuticals and Functional Foods in Human Health and Disease Prevention; CRC Press: Boca Raton, FL, USA, 2015; pp. 407–418. [Google Scholar] [CrossRef]
  57. Stewart, J.J.; Adams, W.W., III; López-Pozo, M.; Doherty Garcia, N.; McNamara, M.; Escobar, C.M.; Demmig-Adams, B. Features of the duckweed Lemna that support rapid growth under extremes of light intensity. Cells 2021, 10, 1481. [Google Scholar] [CrossRef]
  58. Martindale, W.; Bowes, G. The effects of irradiance and CO2 on the activity and activation of ribulose-1,5-bisphosphate carboxylase/oxygenase in the aquatic plant Spirodela polyrhiza. J. Exp. Bot. 1996, 47, 781–784. [Google Scholar] [CrossRef]
  59. Polutchko, S.K.; Adams, W.W., III; Escobar, C.M.; Demmig-Adams, B. Conquering space with crops that produce ample oxygen and antioxidants. Oxygen 2022, 2, 211–226. [Google Scholar] [CrossRef]
  60. Sree, K.S.; Dahse, H.M.; Chandran, J.N.; Schneider, B.; Jahreis, G.; Appenroth, K.J. Duckweed for human nutrition: No cytotoxic and no anti-proliferative effects on human cell lines. Plant Foods Hum. Nutr. 2019, 74, 223–224. [Google Scholar] [CrossRef] [PubMed]
  61. Adams, W.W., III; Demmig-Adams, B.; Barker, D.H.; Kiley, S. Carotenoids and photosystem II characteristics of upper and lower halves of leaves acclimated to high light. Aust. J. Plant Physiol. 1996, 23, 669–677. [Google Scholar] [CrossRef]
  62. Terashima, I.; Inoue, Y. Vertical gradient in photosynthetic properties of spinach chloroplast dependent on intra-leaf light environment. Plant Cell Physiol. 1985, 26, 781–785. [Google Scholar] [CrossRef]
  63. Hommel, E.; Liebers, M.; Offermann, S.; Pfannschmidt, T. Effectiveness of light-quality and dark-white growth light shifts in short-term light acclimation of photosynthesis in Arabidopsis. Front. Plant Sci. 2022, 12, 615253. [Google Scholar] [CrossRef] [PubMed]
  64. Demmig-Adams, B.; Stewart, J.J.; López-Pozo, M.; Polutchko, S.K.; Adams, W.W., III. Zeaxanthin, a molecule for photoprotection in many different environments. Molecules 2020, 25, 5825. [Google Scholar] [CrossRef]
  65. Parker, G.G.; Fitzjarrald, D.R.; Gonçalves Sampaio, I.C. Consequences of environmental heterogeneity for the photosynthetic light environment of a tropical forest. Agric. For. Meteorol. 2019, 278, 107661. [Google Scholar] [CrossRef]
  66. Zhou, Y.; Kishchenko, O.; Stepanenko, A.; Chen, G.; Wang, W.; Zhou, J.; Pan, C.; Borisjuk, N. The dynamics of NO3− and NH4+ uptake in duckweed are coordinated with the expression of major nitrogen assimilation genes. Plants 2022, 11, 11. [Google Scholar] [CrossRef]
  67. Fang, Y.Y.; Babourina, O.; Rengel, Z.; Yang, X.E.; Pu, P.M. Ammonium and nitrate uptake by the floating plant Landoltia punctata. Ann. Bot. 2007, 99, 365–370. [Google Scholar] [CrossRef]
  68. Gallego, L.M.; Chien, Y.H.; Angeles, I.P. Effects of light source and photoperiod on growth of duckweed Landoltia punctata and its water quality. Aquac. Res. 2022, 53, 398–408. [Google Scholar] [CrossRef]
  69. Wang, Y.; Chen, X.; Guo, B.; Liu, C.; Liu, J.; Qiu, G.; Fu, Q.; Li, H. Alleviation of aqueous nitrogen loss from paddy fields by growth and decomposition of duckweed (Lemna minor L.) after fertilization. Chemosphere 2023, 311, 137073. [Google Scholar] [CrossRef] [PubMed]
  70. Cedergreen, N.; Madsen, T.V. Nitrogen uptake by the floating macrophyte Lemna minor. New Phytol. 2002, 155, 285–292. [Google Scholar] [CrossRef]
  71. Petersen, F.; Demann, J.; Restemeyer, D.; Ulbrich, A.; Olfs, H.W.; Westendarp, H.; Appenroth, K.J. Influence of the nitrate-N to ammonium-N ratio on relative growth rate and crude protein content in the duckweeds Lemna minor and Wolffiella hyalina. Plants 2021, 10, 1741. [Google Scholar] [CrossRef] [PubMed]
  72. Petersen, F.; Demann, J.; von Salzen, J.; Olfs, H.W.; Westendarp, H.; Wolf, P.; Appenroth, K.J.; Ulbrich, A. Re-circulating indoor vertical farm: Technicalities of an automated duckweed biomass production system and protein feed product quality evaluation. J. Clean. Prod. 2022, 380, 134894. [Google Scholar] [CrossRef]
  73. Mehrer, I.; Mohr, H. Ammonium toxicity: Description of the syndrome in Sinapis alba and the search for its causation. Physiol. Plant 1989, 77, 545–554. [Google Scholar] [CrossRef]
  74. Hecht, U.; Mohr, H. Factors controlling nitrate and ammonium accumulation in mustard (Sinapis alba) seedlings. Physiol. Plant. 1990, 78, 379–387. [Google Scholar] [CrossRef]
  75. Wang, W.; Haberer, G.; Gundlach, H.; Gläßer, C.; Nussbaumer, T.; Luo, M.C.; Lomsadze, A.; Borodovsky, M.; Kerstetter, R.A.; Shanklin, J.; et al. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nat. Commun. 2014, 5, 3311. [Google Scholar] [CrossRef]
  76. Ziegler, P.; Adelmann, K.; Zimmer, S.; Schmidt, C.; Appenroth, K.J. Relative in vitro growth rates of duckweeds (Lemnaceae)—The most rapidly growing higher plants. Plant Biol. 2015, 17, 33–41. [Google Scholar] [CrossRef]
  77. Vega, A.; O’Brien, J.A.; Gutiérrez, R.A. Nitrate and hormonal signaling crosstalk for plant growth and development. Curr. Opin. Plant Biol. 2019, 52, 155–163. [Google Scholar] [CrossRef]
  78. Cassan, O.; Pimparé, L.L.; Dubos, C.; Gojon, A.; Bach, L.; Lèbre, S.; Martin, A. A gene regulatory network in Arabidopsis roots reveals features and regulators of the plant response to elevated CO2. New Phytol. 2023, 239, 992–1004. [Google Scholar] [CrossRef] [PubMed]
  79. Fan, N.; Yang, Z.; Hao, T.; Zhuang, L.; Xu, Q.; Yu, J. Differential effects of elevated atmosphere CO2 concentration on root growth in association with regulation of auxin and cytokinins under different nitrate supply. Environ. Exp. Bot. 2022, 201, 104943. [Google Scholar] [CrossRef]
  80. Mantelin, S.; Touraine, B. Plant growth-promoting bacteria and nitrate availability: Impacts on root development and nitrate uptake. J. Exp. Bot. 2004, 394, 27–34. [Google Scholar] [CrossRef] [PubMed]
  81. Cook, J.; Degon, Z.; Ruiz, D.; Pope, J.; Rahmatallah, Y.; Mukherjee, A. The plant growth-promoting bacteria, Azospirillum brasilense, induce a diverse array of genes in rice shoots and promote their growth. Plant Growth Regul. 2022, 97, 143–155. [Google Scholar] [CrossRef]
  82. Saini, M.R.; Chandran, L.P.; Barbadikar, K.M.; Sevanthi, A.M.V.; Chawla, G.; Kaushik, M.; Mulani, E.; Phule, A.S.; Govindannagari, R.; Sonth, B.; et al. Understanding plant–microbe interaction of rice and soybean with two contrasting diazotrophic bacteria through comparative transcriptome analysis. Front. Plant Sci. 2022, 13, 939395. [Google Scholar] [CrossRef] [PubMed]
  83. Da Silva Irineu, L.E.S.; da Silva Irineu, C.; Soares, T.S.; de Almeida, F.A.; Almeida-Silva, F.; Gazara, R.K.; Meneses, C.H.S.G.; Canellas, L.P.; Silveira, V.; Venancio, T.M.; et al. Multiomic approaches reveal hormonal modulation and nitrogen uptake and assimilation in the initial growth of maize inoculated with Herbaspirillum seropedicae. Plants 2023, 12, 48. [Google Scholar] [CrossRef] [PubMed]
  84. Shuvro, S.K.; Jog, R.; Morikawa, M. Diazotrophic bacterium Azotobacter vinelandii as a mutualistic growth promoter of an aquatic plant: Lemna minor. Plant Growth Regul. 2023, 100, 171–180. [Google Scholar] [CrossRef]
  85. Friel, C.A.; Friesen, M.L. Legumes modulate allocation to rhizobial nitrogen fixation in response to factorial light and nitrogen manipulation. Front. Plant Sci. 2019, 10, 1316. [Google Scholar] [CrossRef]
  86. Kittiwongwattana, C.; Thawai, C. Rhizobium lemnae sp. nov., a bacterial endophyte of Lemna aequinoctialis. Int. J. Syst. Evol. Microbiol. 2014, 64, 2455–2460. [Google Scholar] [CrossRef]
  87. Nakei, M.D.; Venkataramana, P.B.; Ndakidemi, P.A. Soybean-nodulating rhizobia: Ecology, characterization, diversity, and growth promoting functions. Front. Sustain. Food Syst. 2022, 6, 824444. [Google Scholar] [CrossRef]
  88. Oikawa, S.; Miyagi, K.M.; Hikosaka, K.; Okada, M.; Matsunami, T.; Kokubun, M.; Kinugasa, T.; Hirose, T. Interactions between elevated CO2 and N2-fixation determine soybean yield-a test using a non-nodulated mutant. Plant Soil 2010, 330, 163–172. [Google Scholar] [CrossRef]
  89. Sree, K.S.; Maheshwari, S.C.; Boka, K.; Khurana, J.P.; Keresztes, Á.; Appenroth, K.J. The duckweed Wolffia microscopica: A unique aquatic monocot. Flora Morphol. Distrib. Funct. Ecol. Plants 2015, 210, 31–39. [Google Scholar] [CrossRef]
  90. Sanz-sáez, Á.; Heath, K.D.; Burke, P.V.; Ainsworth, E.A. Inoculation with an enhanced N2-fixing Bradyrhizobium japonicum strain (USDA110) does not alter soybean (Glycine max Merr.) response to elevated [CO2]. Plant Cell Environ. 2015, 38, 2589–2602. [Google Scholar] [CrossRef] [PubMed]
  91. Soba, D.; Aranjuelo, I.; Gakière, B.; Gilard, F.; Pérez-López, U.; Mena-Petite, A.; Muñoz-Rueda, A.; Lacuesta, M.; Sanz-Saez, A. Soybean inoculated with one Bradyrhizobium strain isolated at elevated [CO2] show an impaired C and N metabolism when grown at ambient [CO2]. Front. Plant Sci. 2021, 12, 656961. [Google Scholar] [CrossRef] [PubMed]
  92. Mohedano, R.A.; Costa, R.H.R.; Tavares, F.A.; Belli Filho, P. High nutrient removal rate from swine wastes and protein biomass production by full-scale duckweed ponds. Bioresour. Technol. 2012, 112, 98–104. [Google Scholar] [CrossRef] [PubMed]
  93. De Beukelaar, M.F.A.; Zeinstra, G.G.; Mes, J.J.; Fischer, A.R.H. Duckweed as human food. The influence of meal context and information on duckweed acceptability of Dutch consumers. Food Qual. Prefer. 2019, 71, 76–86. [Google Scholar] [CrossRef]
  94. Kaplan, A.; Zelicha, H.; Tsaban, G.; Meir, A.Y.; Rinott, E.; Kovsan, J.; Novack, L.; Thiery, J.; Ceglarek, U.; Burkhardt, R.; et al. Protein bioavailability of Wolffia globosa duckweed, a novel aquatic plant—A randomized controlled trial. Clin. Nutr. 2019, 38, 2576–2582. [Google Scholar] [CrossRef]
  95. Skillicorn, P.; Spira, W.; Journey, W. Duckweed Aquaculture: A New Aquatic Farming System for Developing Countries; World Bank: Washington, DC, USA, 1993. [Google Scholar]
  96. Chakrabarti, R.; Clark, W.D.; Sharma, J.G.; Goswami, R.K.; Shrivastav, A.K.; Tocher, D.R. Mass production of Lemna minor and its amino acid and fatty acid profiles. Front. Chem. 2018, 6, 479. [Google Scholar] [CrossRef]
  97. Yahaya, N.; Hamdan, N.H.; Zabidi, A.R.; Mohamad, A.M.; Suhaimi, M.L.H.; Johari, M.A.A.M.; Yahya, H.N.; Yahya, H. Duckweed as a future food: Evidence from metabolite profile, nutritional and microbial analyses. Futur. Foods 2022, 5, 100128. [Google Scholar] [CrossRef]
  98. Noonan, S.C. Oxalate content of foods and its effect on humans. Asia Pac. J. Clin. Nutr. 1999, 8, 64–74. [Google Scholar] [CrossRef]
  99. Hu, Z.; Fang, Y.; Yi, Z.; Tian, X.; Li, J.; Jin, Y.; He, K.; Liu, P.; Du, A.; Huang, Y.; et al. Determining the nutritional value and antioxidant capacity of duckweed (Wolffia arrhiza) under artificial conditions. LWT 2022, 153, 112477. [Google Scholar] [CrossRef]
  100. Kumar, V.; Irfan, M.; Datta, A. Manipulation of oxalate metabolism in plants for improving food quality and productivity. Phytochemistry 2019, 158, 103–109. [Google Scholar] [CrossRef]
  101. Yang, J.; Fu, M.; Ji, C.; Huang, Y.; Wu, Y. Maize oxalyl-coa decarboxylase1 degrades oxalate and affects the seed metabolome and nutritional quality. Plant Cell 2018, 30, 2447–2462. [Google Scholar] [CrossRef] [PubMed]
  102. Natesh, H.N.; Abbey, L.; Asiedu, S.K. An overview of nutritional and anti nutritional factors in green leafy vegetables. Hortic. Int. J. 2017, 1, 58–65. [Google Scholar] [CrossRef]
  103. Appenroth, K.J.; Sree, S.K.; Bog, M.; Ecker, J.; Seeliger, C.; Böhm, V.; Lorkowski, S.; Sommer, K.; Vetter, W.; Tolzin-Banasch, K.; et al. Nutritional value of the duckweed species of the genus Wolffia (Lemnaceae) as human food. Front. Chem. 2018, 6, 483. [Google Scholar] [CrossRef] [PubMed]
  104. Sadhukhan, J.; Dugmore, T.I.J.; Matharu, A.; Martinez-Hernandez, E.; Aburto, J.; Rahman, P.K.S.M.; Lynch, J. Perspectives on “game changer” global challenges for sustainable 21st century: Plant-based diet, unavoidable food waste biorefining, and circular economy. Sustainability 2020, 12, 1976. [Google Scholar] [CrossRef]
  105. Coughlan, N.E.; Walsh, É.; Bolger, P.; Burnell, G.; O’Leary, N.; O’Mahoney, M.; Paolacci, S.; Wall, D.; Jansen, M.A.K. Duckweed bioreactors: Challenges and opportunities for large-scale indoor cultivation of Lemnaceae. J. Clean. Prod. 2022, 336, 130285. [Google Scholar] [CrossRef]
  106. Markou, G.; Wang, L.; Ye, J.; Unc, A. Using agro-industrial wastes for the cultivation of microalgae and duckweeds: Contamination risks and biomass safety concerns. Biotechnol. Adv. 2018, 36, 1238–1254. [Google Scholar] [CrossRef]
  107. World Health Organization. WHO Global Strategy for Food Safety 2022–2030—Towards Stronger Food Safety Systems and Global Cooperation; World Health Organization: Geneva, Switzerland, 2022; pp. 1–86. [Google Scholar]
  108. Sela, I.; Meir, A.Y.; Brandis, A.; Krajmalnik-Brown, R.; Zeibich, L.; Chang, D.; Dirks, B.; Tsaban, G.; Kaplan, A.; Rinott, E.; et al. Wolffia globosa–mankai plant-based protein contains bioactive vitamin B12 and is well absorbed in humans. Nutrients 2020, 12, 3067. [Google Scholar] [CrossRef]
  109. Green, R.; Miller, J.W. Vitamin B12 deficiency. In Vitamins and Hormones; Litwack, G., Ed.; Academic Press: Cambridge, MA, USA, 2022; Volume 119, pp. 405–439. [Google Scholar] [CrossRef]
  110. U.S. Department of Health & Human Services. National Institutes of Health. Division of Program Coordination, Planning, and S.I. Vitamin B12 Fact Sheet for Health Professionals. 2023. Available online: https://ods.od.nih.gov/factsheets/VitaminB12-HealthProfessional/ (accessed on 24 August 2023).
  111. Yokoyama, Y.; Levin, S.M.; Barnard, N.D. Association between plant-based diets and plasma lipids: A systematic review and meta-analysis. Nutr. Rev. 2017, 75, 683–698. [Google Scholar] [CrossRef]
  112. Sukumar, N.; Saravanan, P. Investigating vitamin B12 deficiency. BMJ 2019, 365, 1865. [Google Scholar] [CrossRef]
  113. Watanabe, F.; Takenaka, S.; Kittaka-Katsura, H.; Ebara, S.; Miyamoto, E. Characterization and bioavailability of vitamin B12-compounds from edible algae. J. Nutr. Sci. Vitaminol. 2002, 48, 325–331. [Google Scholar] [CrossRef]
  114. Meir, A.Y.; Rinott, E.; Tsaban, G.; Zelicha, H.; Kaplan, A.; Rosen, P.; Shelef, I.; Youngster, I.; Shalev, A.; Blüher, M.; et al. Effect of green-Mediterranean diet on intrahepatic fat: The DIRECT plus randomised controlled trial. Gut 2021, 70, 2085–2095. [Google Scholar] [CrossRef] [PubMed]
  115. Meir, A.Y.; Tsaban, G.; Zelicha, H.; Rinott, E.; Kaplan, A.; Youngster, I.; Rudich, A.; Shelef, I.; Tirosh, A.; Brikner, D.; et al. A Green-Mediterranean diet, supplemented with mankai duckweed, preserves iron-homeostasis in humans and is efficient in reversal of anemia in rats. J. Nutr. 2019, 149, 1004–1011. [Google Scholar] [CrossRef]
  116. Rinott, E.; Meir, A.Y.; Tsaban, G.; Zelicha, H.; Kaplan, A.; Knights, D.; Tuohy, K.; Scholz, M.U.; Koren, O.; Stampfer, M.J.; et al. The effects of the Green-Mediterranean diet on cardiometabolic health are linked to gut microbiome modifications: A randomized controlled trial. Genome Med. 2022, 14, 29. [Google Scholar] [CrossRef] [PubMed]
  117. Tsaban, G.; Yaskolka Meir, A.; Rinott, E.; Zelicha, H.; Kaplan, A.; Shalev, A.; Katz, A.; Rudich, A.; Tirosh, A.; Shelef, I.; et al. The effect of green Mediterranean diet on cardiometabolic risk; A randomised controlled trial. Heart 2021, 107, 1054–1061. [Google Scholar] [CrossRef]
  118. Zelicha, H.; Kaplan, A.; Meir, A.Y.; Tsaban, G.; Rinott, E.; Shelef, I.; Tirosh, A.; Brikner, D.; Pupkin, E.; Qi, L.; et al. The effect of Wolffia globosa mankai, a green aquatic plant, on postprandial glycemic response: A randomized crossover controlled trial. Diabetes Care 2019, 42, 1162–1169. [Google Scholar] [CrossRef]
  119. Kaplan, A.; Zelicha, H.; Yaskolka Meir, A.; Rinott, E.; Tsaban, G.; Levakov, G.; Prager, O.; Salti, M.; Yovell, Y.; Ofer, J.; et al. The effect of a high-polyphenol Mediterranean diet (Green-MED) combined with physical activity on age-related brain atrophy: The Dietary Intervention Randomized Controlled Trial Polyphenols Unprocessed Study (DIRECT PLUS). Am. J. Clin. Nutr. 2022, 115, 1270–1281. [Google Scholar] [CrossRef]
  120. Meir, A.Y.; Tuohy, K.; von Bergen, M.; Krajmalnik-Brown, R.; Heinig, U.; Zelicha, H.; Tsaban, G.; Rinott, E.; Kaplan, A.; Aharoni, A.; et al. The metabolomic-gut-clinical axis of mankai plant-derived dietary polyphenols. Nutrients 2021, 13, 1866. [Google Scholar] [CrossRef]
  121. Rinott, E.; Youngster, I.; Meir, A.Y.; Tsaban, G.; Zelicha, H.; Kaplan, A.; Knights, D.; Tuohy, K.; Fava, F.; Scholz, M.U.; et al. Effects of diet-modulated autologous fecal microbiota transplantation on weight gain. Gastroenterology 2021, 160, 158–173. [Google Scholar] [CrossRef]
  122. Papong, S.; Rewlay-ngoen, C.; Itsubo, N.; Malakul, P. Environmental life cycle assessment and social impacts of bioethanol production in Thailand. J. Clean. Prod. 2017, 157, 254–266. [Google Scholar] [CrossRef]
  123. Cui, W.; Cheng, J.J. Growing duckweed for biofuel production: A review. Plant Biol. 2015, 17, 16–23. [Google Scholar] [CrossRef] [PubMed]
  124. Xu, Y.L.; Fang, Y.; Li, Q.; Yang, G.L.; Guo, L.; Chen, G.K.; Tan, L.; He, K.Z.; Jin, Y.L.; Zhao, H. Turion, an innovative duckweed-based starch production system for economical biofuel manufacture. Ind. Crops Prod. 2018, 124, 108–114. [Google Scholar] [CrossRef]
  125. Sun, Z.; Guo, W.; Zhao, X.; Chen, Y.; Yang, J.; Xu, S.; Hou, H. Sulfur limitation boosts more starch accumulation than nitrogen or phosphorus limitation in duckweed (Spirodela polyrhiza). Ind. Crops Prod. 2022, 185, 115098. [Google Scholar] [CrossRef]
  126. Li, J.M.; Du, A.P.; Liu, P.H.; Tian, X.P.; Jin, Y.L.; Yi, Z.L.; He, K.Z.; Fang, J.; Zhao, H. High starch accumulation mechanism and phosphorus utilization efficiency of duckweed (Landoltia punctata) under phosphate starvation. Ind. Crops Prod. 2021, 167, 113529. [Google Scholar] [CrossRef]
  127. Liang, Y.; Yu, X.H.; Anaokar, S.; Shi, H.; Dahl, W.B.; Cai, Y.; Luo, G.; Chai, J.; Cai, Y.; Mollá-Morales, A.; et al. Engineering triacylglycerol accumulation in duckweed (Lemna japonica). Plant Biotechnol. J. 2023, 21, 317–330. [Google Scholar] [CrossRef] [PubMed]
  128. De la Rosa-Rodríguez, R.; Lara-Herrera, A.; Trejo-Téllez, L.I.; Padilla-Bernal, L.E.; Solis-Sánchez, L.O.; Ortiz-Rodríguez, J.M. Water and fertilizers use efficiency in two hydroponic systems for tomato production. Hortic. Bras. 2020, 38, 47–52. [Google Scholar] [CrossRef]
  129. Benke, K.; Tomkins, B. Future food-production systems: Vertical farming and controlled-environment agriculture. Sustain. Sci. Pract. Policy 2017, 13, 13–26. [Google Scholar] [CrossRef]
  130. Kozai, T.; Niu, G.; Takagaki, M. (Eds.) Plant Factory: An Indoor Vertical Farming System for Efficient Quality Food Production; Academic Press: Cambridge, MA, USA, 2015. [Google Scholar]
  131. AlShrouf, A. Hydroponics, aeroponic and aquaponic as compared with conventional farming. Am. Sci. Res. J. Eng. Technol. Sci. 2017, 27, 247–255. [Google Scholar] [CrossRef]
  132. Keuter, V.; Deck, S.; Giesenkamp, H.; Gonglach, D.; Katayama, V.T.; Liesegang, S.; Petersen, F.; Schwindenhammer, S.; Steinmetz, H.; Ulbrich, A. Significance and vision of nutrient recovery for sustainable city food systems in Germany by 2050. Sustainability 2021, 13, 10772. [Google Scholar] [CrossRef]
  133. Escobar, C.M.; Escobar, A.C.; Power, G.J.; Nabity, J.A. μG-LilyPondTM: Preliminary design of a floating plant pond for microgravity. Int. Conf. Environ. Syst. 2020, 1–12. [Google Scholar]
  134. Fan, C.; Manivannan, A.; Wei, H. Light quality-mediated influence of morphogenesis in micropropagated horticultural crops: A comprehensive overview. Biomed Res. Int. 2022, 2022, 4615079. [Google Scholar] [CrossRef]
  135. Naoya Fukuda, M.E.; Yoshida, H.; Kusano, M. Effects of light quality, photoperiod, CO2 concentration, and air temperature on chlorogenic acid and rutin accumulation in young lettuce plants. Plant Physiol. Biochem. 2022, 186, 290–298. [Google Scholar] [CrossRef]
Plants 12 03090 g001
Figure 1. Schematic summary of the many applications of duckweed coupled with its high resource-use efficiency. Further detail is addressed in the different sections of this review.
Figure 1. Schematic summary of the many applications of duckweed coupled with its high resource-use efficiency. Further detail is addressed in the different sections of this review.
Plants 12 03090 g001
Plants 12 03090 g002
Figure 2. Schematic depiction of duckweed fronds serving as both source and main sink for photosynthetically produced sugar and the bidirectional interaction of the plant with its microbiome serving as a sugar sink and assisting with nutrient acquisition by increasing bioavailability and uptake by the plant. By modulating plant hormones, the microbiome may be able to modulate expression of high-affinity nitrate and/or ammonium transporters (that are also tied to regulation by phytohormones in plant roots).
Figure 2. Schematic depiction of duckweed fronds serving as both source and main sink for photosynthetically produced sugar and the bidirectional interaction of the plant with its microbiome serving as a sugar sink and assisting with nutrient acquisition by increasing bioavailability and uptake by the plant. By modulating plant hormones, the microbiome may be able to modulate expression of high-affinity nitrate and/or ammonium transporters (that are also tied to regulation by phytohormones in plant roots).
Plants 12 03090 g002
Plants 12 03090 g003
Figure 3. Relative growth rate (RGR; based on frond area expansion per day) of L. minor growing under either (a) ample nutrients (1/2 strength Schenk & Hildebrandt medium; [44]) with ambient (aCO2) or elevated (eCO2) CO2 and without (Sani) or with (Inoc) its microbiome or (b) low nutrients (1/20 strength Schenk & Hildebrandt medium) with ambient or elevated CO2 and without or with its microbiome. Mean values ± standard deviations, n = 3. * = significantly different at p < 0.05 (Student’s t-test); n.s. = not significantly different. Original data from Zenir et al. [39].
Figure 3. Relative growth rate (RGR; based on frond area expansion per day) of L. minor growing under either (a) ample nutrients (1/2 strength Schenk & Hildebrandt medium; [44]) with ambient (aCO2) or elevated (eCO2) CO2 and without (Sani) or with (Inoc) its microbiome or (b) low nutrients (1/20 strength Schenk & Hildebrandt medium) with ambient or elevated CO2 and without or with its microbiome. Mean values ± standard deviations, n = 3. * = significantly different at p < 0.05 (Student’s t-test); n.s. = not significantly different. Original data from Zenir et al. [39].
Plants 12 03090 g003
Plants 12 03090 g004
Figure 4. (a,b) Relative growth rate (RGR), (c,d) dry biomass, (e,f) and chlorophyll (g,h), carotenoid, and (i,j) protein content, all on a frond area basis, of L. minor growing under two light levels with ample nutrient supply and in the presence of either ambient (aCO2) or elevated (eCO2) CO2. Light supply was either very high, with 700 µmol photons m−2 s−1 (700 µE) for 24 h per day, or lower, with 200 µmol photons m−2 s−1 (200 µE) for 24 h per day. All plants were associated with their microbiomes. Ample nutrients were supplied as 1/2 strength Schenk & Hildebrandt medium [44]. Mean values ± standard deviations, n = 3. All paired sets of data were subjected to a Student’s t-test, with asterisks indicating the level of significant differences: n.s. = not significantly different; * = p < 0.05; ** = p < 0.01; *** = p < 0.001. For original data, growth conditions, and methods, see Demmig-Adams et al. [37] and Zenir et al. [39]. Previously unpublished data in panel j are from Marina López-Pozo.
Figure 4. (a,b) Relative growth rate (RGR), (c,d) dry biomass, (e,f) and chlorophyll (g,h), carotenoid, and (i,j) protein content, all on a frond area basis, of L. minor growing under two light levels with ample nutrient supply and in the presence of either ambient (aCO2) or elevated (eCO2) CO2. Light supply was either very high, with 700 µmol photons m−2 s−1 (700 µE) for 24 h per day, or lower, with 200 µmol photons m−2 s−1 (200 µE) for 24 h per day. All plants were associated with their microbiomes. Ample nutrients were supplied as 1/2 strength Schenk & Hildebrandt medium [44]. Mean values ± standard deviations, n = 3. All paired sets of data were subjected to a Student’s t-test, with asterisks indicating the level of significant differences: n.s. = not significantly different; * = p < 0.05; ** = p < 0.01; *** = p < 0.001. For original data, growth conditions, and methods, see Demmig-Adams et al. [37] and Zenir et al. [39]. Previously unpublished data in panel j are from Marina López-Pozo.
Plants 12 03090 g004
Plants 12 03090 g005
Figure 5. Ammonium (a,b) and nitrate (c,d) uptake by sanitized L. minor during phase 1 (48-h growing phase upon transfer of four fronds from ½ to 1/20 Schenk & Hildebrandt medium) and phase 2 (72-h second growing phase in 1/20 Schenk & Hildebrandt medium after transfer of fronds to fresh medium at time 0 of phase 2 and concomitantly reducing the number of fronds to four) under ambient CO2. This was performed under either a short (12 h light/12 h dark) photoperiod (green lines) or a long photoperiod (24 h light; yellow lines) with 200 µmol photons m−2 s−1 in each case. Ammonium and nitrate concentrations in the media were determined photometrically (photometers HI83314 and HI83300, respectively; Hanna Instruments, Woonsocket, RI, USA). At the time of sampling, 10 mL of media were collected for ammonium determination and an additional 1 mL for nitrate. n = 3 for each time point. Unpublished data from Madeleine Zenir and Marina López-Pozo. Plants were grown as described in Zenir et al. [39].
Figure 5. Ammonium (a,b) and nitrate (c,d) uptake by sanitized L. minor during phase 1 (48-h growing phase upon transfer of four fronds from ½ to 1/20 Schenk & Hildebrandt medium) and phase 2 (72-h second growing phase in 1/20 Schenk & Hildebrandt medium after transfer of fronds to fresh medium at time 0 of phase 2 and concomitantly reducing the number of fronds to four) under ambient CO2. This was performed under either a short (12 h light/12 h dark) photoperiod (green lines) or a long photoperiod (24 h light; yellow lines) with 200 µmol photons m−2 s−1 in each case. Ammonium and nitrate concentrations in the media were determined photometrically (photometers HI83314 and HI83300, respectively; Hanna Instruments, Woonsocket, RI, USA). At the time of sampling, 10 mL of media were collected for ammonium determination and an additional 1 mL for nitrate. n = 3 for each time point. Unpublished data from Madeleine Zenir and Marina López-Pozo. Plants were grown as described in Zenir et al. [39].
Plants 12 03090 g005
Plants 12 03090 g006
Figure 6. Schematic representation of a multi-level, closed, vertical production system for duckweed with interspersed blue and red light emitting diodes supplying the low level of light that is sufficient to saturate plant growth and food or biofuel feedstock production.
Figure 6. Schematic representation of a multi-level, closed, vertical production system for duckweed with interspersed blue and red light emitting diodes supplying the low level of light that is sufficient to saturate plant growth and food or biofuel feedstock production.
Plants 12 03090 g006
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

López-Pozo, M.; Adams, W.W., III; Demmig-Adams, B. Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications. Plants 2023, 12, 3090. https://doi.org/10.3390/plants12173090

AMA Style

López-Pozo M, Adams WW III, Demmig-Adams B. Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications. Plants. 2023; 12(17):3090. https://doi.org/10.3390/plants12173090

Chicago/Turabian Style

López-Pozo, Marina, William W. Adams, III, and Barbara Demmig-Adams. 2023. "Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications" Plants 12, no. 17: 3090. https://doi.org/10.3390/plants12173090

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop