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. 2015 Feb 20;66(7):1699–1705. doi: 10.1093/jxb/erv009

Photosynthesis in reproductive structures: costs and benefits

John A Raven 1,*, Howard Griffiths 2
PMCID: PMC4669558  PMID: 25871648

Highlight

Photosynthesis in the reproductive structures of algae and plants is common but by no means universal and has evolutionary and agricultural, e.g. in the grain filling of cereals, significance.

Key words: Carbon on isotope composition, fruit and seed dispersal, oxidative damage, pollination, reproductive structure photosynthesis, resource allocation.

Abstract

The role of photosynthesis by reproductive structures during grain-filling has important implications for cereal breeding, but the methods for assessing the contribution by reproductive structures to grain-filling are invasive and prone to compensatory changes elsewhere in the plant. A technique analysing the natural abundance of stable carbon isotopes in soluble carbohydrates has significant promise. However, it depends crucially on there being no more than two sources of organic carbon (leaf and ear/awn), with significantly different 13C:12C ratios and no secondary fractionation during grain-filling. The role of additional peduncle carbohydrate reserves represents a potential means for N remobilization, as well as for hydraulic continuity during grain-filling. The natural abundance of the stable isotopes of carbon and oxygen are also useful for exploring the influence of reproduction on whole plant carbon and water relations and have been used to examine the resource costs of reproduction in females and males of dioecious plants. Photosynthesis in reproductive structures is widespread among oxygenic photosynthetic organisms, including many clades of algae and embryophytes of different levels of complexity. The possible evolutionary benefits of photosynthesis in reproductive structures include decreasing the carbon cost of reproduction and ‘use’ of transpiratory loss of water to deliver phloem-immobile calcium Ca2+ and silicon [Si(OH)4] via the xylem. The possible costs of photosynthesis in reproductive structures are increasing damage to DNA from photosynthetically active, and hence UV-B, radiation and the production of reactive oxygen species.

Introduction

Photosynthesis in reproductive structures of photosynthetic organisms is phylogenetically widespread but the extent varies within clades, with many organisms having no photosynthesis in their reproductive structures. This topic has attracted the attention of plant physiologists, ecologists, and evolutionary biologists (Whittaker, 1931; Bazzaz et al., 1979; Kenzo et al., 2003). Photosynthesis in reproductive structures is also of importance to plant breeders, especially those cereal breeders concerned with the Triticeae (Hordeum, Secale, Triticum) where trait selection must be considered in relation to photosynthate allocation from various sources to the grain (Carr and Wardlaw, 1965; Evans et al., 1972, 1975; Teare et al., 1972). Many of the methods used to quantify organic carbon sources for grain-filling are invasive, limited by any compensation for excised or shaded source structures by the remaining source structures (Carr and Wardlaw, 1965; Evans et al., 1972, 1975; Teare et al, 1972; Sanchez-Bragado et al., 2014). These problems led Sanchez-Bragado et al. (2014) to explore the use of the natural abundance of stable carbon isotopes to partition organic carbon supply to grain-filling. This commentary discusses the limitations and significance of the work of Sanchez-Bragado et al. (2014), and goes on to consider photosynthesis in reproductive structures more generally from a phylogenetic and functional perspective.

The use of the natural abundance of stable carbon isotopes in determining the quantitative significance of photosynthesis in reproductive structures

Sanchez-Bragado et al. (2014) use the natural abundance of stable carbon isotopes to estimate the contribution of photosynthesis in the ear and that in other parts of the plant. This method depends on (i) their being only two sources (or sets of sources) of photosynthate for grain-filling; (ii) that the photosynthate from these two sources have a significantly different natural abundance 13C:12C ratio and that the 13C:12C ratio of each source is constant over the grain-filling period; and (iii) that secondary fractionations during storage and mobilization to sinks are minimal (Cernusak et al., 2009).

The method presented by Sanchez-Bragado et al. (2014) compares carbon isotopes in bulk organic material and water-soluble compounds (WSC) (Brugnoli et al., 1988), where carbohydrates, organic acids, and amino acids represent recent photosynthate. In the Triticum aestivum cultivars used by Sanchez-Bragado et al. (2014) the carbon isotope ratio (13C:12C, expressed as δ13C) is higher (δ13C less negative) in the awns than in flag leaves and possible mechanistic reasons for this difference are discussed. The 13C:12C value of the grain is closer to that of the awn WSC than those of the flag leaf. Linear relationships were used to infer the proportional contribution between the ranges of grain and (awn+peduncle) WSC isotopic signals, with up to 48% of grain carbon coming from lower leaves and peduncle under well-watered conditions (Fig. 4 in Sanchez-Bragado et al., 2014). A comparison of awn and flag leaf WSC pools is used to suggest that awns contribute 82–97% of organic matter to the grain, with the remaining 3–18% coming from flag leaves (Fig. 5 in Sanchez-Bragado et al.,2014); however, this estimate does not include a third potential source, carbohydrates in the peduncle.

The allocation from flag leaf to grain could also be controlled by the extent that the peduncle acts as a store of carbohydrates, acting as an additional source for remobilization during grain fill. In relative terms, the instantaneous concentration of WSC can be between ×5 and ×20 higher in the lower peduncle than in leaf or awn components (Fig. 2 in Sanchez-Bragado et al., 2014). The peduncle WSC pool is generally enriched in 13C relative to the flag leaf (2–3‰: Table 2 in Sanchez-Bragado et al., 2014), and closer to that of the awn, but is responsive to irrigation. One possibility might be secondary fractionation during (re)mobilization and storage of carbohydrates (e.g. from flag leaf to stem), as discussed in detail by Cernusak et al. (2009), who suggested a number of hypotheses which could account for potential source–sink fractionations.

One mechanism leading to an offset in stored WSC isotope composition is the extent that reserves are mobilized at night rather than during the day (Tcherkez et al., 2004; Gessler et al., 2008), and also fractionation during phloem transport caused by leakage (Gessler et al., 2007). A number of studies have reported the isotopic enrichment of stem WSC relative to that in leaves, in a range of crops and trees (Cernusak et al., 2009; Sanchez-Bragado et al., 2014). Other variations include the additional contribution from phosphoenolpyruvate carboxylase, as discussed below.

An additional process that might alter the carbon isotope ratio in wheat ears is organic matter entering the ear through the xylem. The influx of xylem sap into the ears is essential for calcium (Ca) supply to growing ears, and especially grains, as well as for photosynthesis. Xylem sap usually contains the anions of organic acids as well as amino acids (Raven and Smith, 1976) and synthesis of organic acids and amino-acids involving phosphoenolpyruvate carboxylase in the roots uses carbon dioxide from respiration with a significantly lower 13C:12C than that of atmospheric carbon dioxide (Raven and Farquhar, 1990; Gillon and Griffiths, 1997; Lin and Ehleringer, 1997; Duranceau et al., 2001; Ghashghaie et al., 2003; Lanigan et al., 2008; Sanchez-Bragado et al., 2014).

The expectation is that the13C:12C ratio in organic acids and amino acids synthesized in the roots of C3 plants is lower than of those synthesized in the leaves, as shown by Yoneyama et al. (1997) for xylem sap and phloem sap in the grain-filling stage of Triticum aestivum cv. SUN 9E (Table 1, derived from data in Yoneyama et al., 1997). A significant role for xylem or phloem supply of organic C and N during grain-filling, either from roots or peduncle during grain fill, would add additional sources and limit the applicability of the C stable isotope model of Sanchez-Bragado et al. (2014).

Table 1.

Comparison of the carbon isotope ratio of water-soluble organic matter and total organic carbon in parts of Triticum aestivum cv SUN 9E, recalculated from data in Yoneyama et al. (1997)

Plant part δ13C water-soluble compounds δ13C total carbon
Ear –26.7o/oo a –28.8o/oo
Leaf blade –29.8o/oo a –30.9o/oo
Leaf sheath –28.3o/oo a –30.6o/oo
Stem –26.8o/oo a –28.1o/oo
Xylem sap –28.4o/oo –28.4o/oo
Phloem sap –28.4o/oo –28.4o/oo
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a Calculated from values in Table 4 of Yoneyama et al. (2014) as the carbon mass-weighted δ13C values for dissolved sugars plus organic acids and for dissolved amino acids.

Additional implications for carbohydrate storage in the peduncle

The capacity of bread wheat to respond to late additions of nitrogenous fertilizer during grain-filling (HGCA, 2009; see below) also suggests an important role for xylem or phloem sap C:N delivery during grain-filling. Farmers routinely measure %N content during grain fill and historically would apply a late (foliar) urea application to boost protein content and attain the bread wheat grain price premium (WD Wallace, personal communication). More quantitative cost–benefit analyses are now used in precision agriculture to determine the rate and timing of nitrogen fertilization (Sylvester-Bradley and Kindred, 2009). As attempts are made to explore the genetic diversity in N remobilization and allocation in order to maximize wheat yields (Sylvester-Bradley and Kindred, 2009; Waters et al., 2009; Hawkesford, 2014), one area of research to be developed remains the interaction between current photosynthate and stored carbohydrate reserves in mobilizing amino acid transfer to grain.

Additional uses of carbohydrate reserves in cereal stems could also relate to the maintenance of hydraulic continuity and repair of cavitation. Between 50–80% of maize xylem elements cavitate on a daily basis, with recovery (refilling) occurring dynamically later in the photoperiod (McCully, 1999). From a methodological perspective, there has been considerable debate recently on the extent of dynamic cavitation repair in vivo, based upon the extent that embolisms may be promoted during leaf or stem excision in some species (Zwieniecki and Holbrook, 2009; Sperry, 2013). Carbohydrate reserves in leaves (Nardini et al., 2011; Johnson et al., 2012) as well as in the leaf sheath and peduncle, could also be used to repair cavitation either overnight (if root pressure was insufficient during drought), or dynamically by day. The development of a bundle sheath (Griffiths et al., 2013) and straw-shortening traits (characteristic of the ‘Green Revolution’), have perhaps both helped to improve hydraulic continuity. Additional field trials of the sort undertaken by Sanchez-Bragado et al. (2014) would be needed to test the extent that both water and nitrogen use efficiency have been enhanced by carbohydrate re-mobilization in the shorter stems of modern, elite wheat cultivars.

Other methods which could distinguish the leaf and ear contributions to grain-filling in cereals include the 18O isotopic signal in organic matter which depends on a detailed understanding of the relative balance between source water inputs and the pool of water evaporatively enriched in 18O at the site of transpiration (Helliker and Ehleringer, 2002; Farquhar et al., 2007; Song et al., 2013). Analysis of WSC again provides a more instantaneous, daily-weighted indicator of evaporative enrichment, and an offset in δ18O between the leaf and the grain kernel was consistent with overall water use traits in durum wheat (Cabrera-Bosquet et al., 2011). In conclusion, the use of stable isotopes to infer source–sink partitioning requires a good understanding of the contrasting physiologies between cereal leaf and ear, both in terms of 13C and 18O enrichment.

Phylogenetic distribution of photosynthesis in reproductive structures

The surface areas of flower parts and developing fruiting bodies provide an additional cost in terms of water loss. Stable isotopes of carbon and oxygen have provided a series of insights into the extent and magnitude of these processes and the implications for resource use between plant sexes, habitat preference, and responses to climate change (Dawson and Ehleringer, 1993; Tognetti, 2012; Hultine et al., 2013). In a well-studied system, Acer negundo (box elder) female plants have higher resource demands and require mesophytic conditions whereas male plants are more stress-tolerant (Dawson and Ehleringer, 1993; Hultine et al., 2013). To date, a study of photosynthetic rate and isotope composition has not been undertaken specifically for male and female reproductive parts within a dioecious species. In advance of such a comparison, the photosynthetic characteristics of reproductive structures is now reviewed from a phylogenetic perspective.

Flowering plants

Flowers of some flowering plants (Aschan and Pfanz, 2003), for example, Helleborus viridis (Aschan et al., 2005) and several members of the Orchidaceae (Goh, 1983; Antlfinger and Wendel, 1997; He et al., 1998), carry out significant (for whole plant carbon balance) photosynthesis. In these organisms the flower photosynthesis uses the same CO2 fixation pathway as the vegetative parts of the same plant, i.e. C3 in Helleborus and some orchids, and crassulacean acid metabolism (CAM) in other orchid (Goh, 1983; He and Teo, 2007). In the obligate CAM Clusia rosea, carbon isotope signals of fruits (C3-like) reflect direct photosynthesis and/or photosynthate partitioning from daytime C3 photosynthesis (Borland and Dodd, 2002). In the myco-organotrophic orchid Neottia nidus-avis the green chloroplasts only carry out cyclic photophosphorylation and so could, at least partly, substitute for respiration of organic carbon in generating ATP in the light (Menke and Schmid, 1976).

Developing seeds and fruits of many flowering plants also carry out photosynthesis sufficient to supply some or almost all of the organic carbon used in their growth and photosynthesis (Bazzaz et al., 1979). Seagrass fruits and seeds are photosynthetic (Celdrán and Marin, 2011); since seagrass sexual reproduction occurs entirely under water, transpiratory water loss during photosynthesis is not a factor in determining the fitness contributions of fruit (see below).

Gymnosperms: mega- and micro-sporangiate strobili (cones) of some conifers

In the megasporangiate strobili of Pinus sylvestris, photosynthesis decreases yearly net respiration by 31% (Linder and Troeng, 1981) whilst in Picea abies photosynthesis decreased net respiration by 16–17% over the entire growth of the strobili (Koppel et al., 1987). Dick et al. (1990a, b ) showed that respiration by megasporangiate strobili of Pinus contorta accounted for about 3% of canopy photosynthesis; this percentage might increase to 3.5–4% if there was no photosynthesis in the strobili (Koppel et al., 1987; Dick et al., 1990a, b ).

Embryophytes at the pteridophyte grade of organization

Green spores occur in the euphyllophytes Equisetum (Lebkeucher, 1997), and Osmunda. Heterosporous ‘pteridophytes’ (both euphyllophytes and lycophytes) have their male gametophytes contained in the microspores (and are non-photosynthetic). Female gametophytes develop within megaspores and, upon germination in the light, they may develop chlorophyll, but there are no data on the photosynthetic characteristics of megagametophytes.

Embryophytes at the bryophyte grade of organization

The matrotrophic sporophytes of bryophytes are non-photosynthetic in liverworts and some mosses and so rely on the gametophyte for all resources, organic and inorganic (Bell and Hemsley, 2000). The other bryophytes have sporophytes that are photosynthetically active and so are only partially dependent on the gametophyte for organic carbon (Bell and Hemsley, 2000).

Algae

Many marine macroalgae have biphasic life cycles with an alternating haploid gametophyte and diploid sporophyte phase, as in embryophytes, although independently evolved in three clades of algae. In one such alga, the isomorphic Ulva (Ulvophyceae: Chlorophyta) both the spores and the gametes (differentiated into large and small gametes) have photosynthetic rates in excess of the rate of respiration (Haxo and Clendenning, 1953). Kelps (Laminariales: Ochrophyta) have a heteromorphic alternation of phases; the large sporophytes produce haploid zoospores with varying degrees of photosynthetic capacity, with some species able to sustain net carbon gain over a diel cycle (Amsler and Neuchul, 1991; Reed et al., 1992). Photosynthesis could increase the time for which these spores can remain motile (Amsler and Neuchul, 1991; Reed et al., 1992). The fucoid brown algae (Fucales: Ochrophyta) have a diplontic, oogamous life cycle, similar to that of most metazoans. The large (tens of μm radius) eggs are photosynthetically active, in some species exceeding the rate of respiration (Whittaker, 1931;Tarakovskaya and Masskov, 2005). By contrast, the ovoid eggs (up to 600 μm long) of the oogamous haplontic green algae of the Charales (Charophyceae: Streptophyta) are non-photosynthetic, with proplastids differentiated into amyloplasts (Leitch et al., 1990).

Conclusions

The ancestral state in algae is for photosynthesis in asexual and sexual reproductive cells, with subsequent losses of photosynthesis in male and some female gametes. In embryophytes, male and female gametes are non-photosynthetic, although some spores are photosynthetic. The surrounding structures have varying degrees of photosynthetic potential.

Benefits of photosynthesis in reproductive structures

Decreasing organic carbon demand from the rest of the plant

For macrophytes, photosynthesis in reproductive structures decreases the energy and carbon costs of reproduction to the rest of the plan, which might be more important for iteroparous rather than semelparous organisms.

Transpiration drives the supply of phloem-immobile nutrients and photosynthesis offers a low-cost carbon benefit

In terrestrial seed plants, the supply of the essential but phloem-immobile (Raven, 1977) calcium to growing fruits and seeds depends on transport in the xylem. The water budget of the pre-dehydration fruit or seed can only be balanced by water loss by guttation or, much more generally, transpiration, and the calcium content of developing Triticum caryopses has been used to estimate their transpiration (Sofield et al., 1977). However, assuming a xylem sap concentration of 42mol m–3 Ca2+ (Table 8.2 in Raven, 1984), at maximum dry matter accumulation (57mg) in a grain there is 0.55 μmol calcium which would have been associated with a minimum of 13.2×10–9 m3 water, which is three times lower than the water content of a grain (43×10–9 m3).

A similar argument can be made for silicon (Si), a ‘beneficial nutrient’ for cereals that is also phloem-immobile (Raven, 1983). The ear contains between 16% and 48% of the total Si at harvest in Triticum (Hutton and Norish, 1974; Schulz and French, 1976). It has been shown in Oryza (Yamaji and Ma, 2009) and Hordeum (Yamaji et al., 2012) that there are silicic acid transporters at stem nodes that can move silicic acid from xylem streams destined for leaves to streams destined for reproductive structures.

Possible costs of photosynthesis in reproductive structures

Photodamage by photosynthetically active and hence ultraviolet radiation and by reactive oxygen species resulting from the occurrence of photosynthesis in reproductive structures

Almost all flowers (except very short-lived flowers that open for a single night; see below) are exposed to solar radiation, either as modified solely by passage through the atmosphere or additionally by overlying vegetation (understorey plants) or by overlying seawater (seagrasses). This means they are exposed to varying fluxes of ultraviolet B radiation, with the possibility of mutation to the DNA in cells that ultimately produce the gametes. This occurs whether or not the flowers are photosynthetic. Photosynthetically active flowers also produce additional amounts of reactive oxygen species, including singlet oxygen that is mainly produced in photosynthesis; these reactive oxygen species can also cause mutation (Allen and Raven, 1996; Raven and Larkum, 2007). Damage to DNA by reactive oxygen species has been cited as an evolutionary reason for gene transfer from mitochondria and chloroplasts, the major sites of production of reactive oxygen species, to set against reasons for the retention of genes in the organelles, predominantly rapid gene regulation by organelle redox status (Allen and Raven, 1996). Later work showed that a very great range of mitochondrial nucleotide substitution rates can occur, even in the single flowering plant genus, Plantago (Cho et al., 2004), with extremely low rates in another flowering plant genus, Liriodendron (Richardson et al., 2013). Furthermore, the observed rates of synonymous and non-synonymous substitutions are subject to many influences subsequent to the original change (Allen and Raven, 1996; Eyre-Walker and Gaut, 1997), including repair by recombination. Despite this, ROS damage to DNA clearly occurs (Kumar et al., 2014): how does this apply to flowers and fruits?

Most flowers and fruits have dark respiration in the light that exceeds the rate of photosynthesis (Quebedaux and Chollet, 1975; Bazzaz et al., 1979), so mean intracellular oxygen is always less than the atmospheric equilibrium. However, some cells in such flowers and fruits, and a few flowers and fruits, may have photosynthesis in excess of dark respiration, increasing the chances of ROS damage to DNA. The mechanism found in some metazoans, ensuring that mitochondria with minimal damage (including damage to DNA) as a result of not having been used in respiratory metabolism are transmitted in sexual reproduction (de Paula et al., 2013), is also not available to plants.

Flower life-span in relation to the occurrence of photosynthesis

Flower life-spans vary with phylogeny, habitat, modes of pollination, and whether plants are self-fertile or obligately out-breeding, with a wide variation within each of these modes of classification (Primack, 1985). A number of evolutionary determinants of flower life-span have been suggested (Primack, 1985; Ashman and Schoen, 1994): while some species of Orchidaceae have flowers only lasting one day, those of Gammatophyllum multiflorum live up to 9 months.

Some flowers are very short-lived; an extreme case is the iteroparous perennial Cereus (Cactaceae) where flowers open for a single night, presumably limiting water loss. However, there are a number of plants that have flowers that only open for one day in daylight hours (Primack, 1985; Ashman and Schoen, 1994; Rathke, 2003) so there is the question of the whether 12 hours would be enough to allow sufficient energy and carbon gain to offset the cost of synthesis of the photosynthetic apparatus.

A more typical minimal flower life-time is that of shorter-lived (annual and ephemeral) semelparous plants whose flowers senesce 5–6 d after anthesis (Primack, 1985; Ashman and Schoen, 1994, 1997). Based on the growth data for a diatom in Ichimi et al. (2012) with a 4h doubling time at 20 °C, there would be ample time for photosynthetic energy gain to recoup the costs of biosynthesis of the photosynthetic components for flowers that only live for a day, granted an adequate supply of photosynthetically active radiation and other resources. A shorter life-span of flowers than of leaves is a general phenomenon (Chabot and Hicks, 1982; Primack, 1985; Ashman and Schoen, 1994, 1997; Kikuzawa and Ackerly, 1999), and it would be useful to have further focused work to see if the ‘time to recoup costs’ holds for the minimum life-span of photosynthetic flowers.

Possible contradictions between maximizing flower, fruit, and seed photosynthesis and maximizing reproductive output

An additional factor is a contradiction between maximizing photosynthetic rate and maximizing reproductive success: for pollination or fruit and seed dispersal by animals, chlorophyll and other pigments might not be attractive or identified visually against a background of green vegetative structures.

Expression of pigments such as anthocyanins, betalains, and carotenoids can also be attractants and the occurrence of protein layers in epidermal cells which cause thin film birefringence (iridescence) can also yield in Eleaocarpus fruits an intense blue colour (Lee, 1991; Glover and Whitney, 2010).

A further possibility of a contradiction between photosynthesis and reproduction is that some aspects of the morphology of reproductive structures often seem to concern their compatibility with pollinating and dispersing animals, the aerodynamics of wind (Niklas 1985), the hydrodynamics of water pollination, and wind or water dispersal of seeds and fruits. There are variable photosynthetic rates and water-use characteristics in the case of wind dispersal, in terms of ‘wings’ on seeds and fruits in Betula, Ulmus, Acer, and Tilia (Bazzaz et al., 1979) and in the Diptercarpaceae (Kenzo et al., 2003).

Conclusions

The role of photosynthesis by reproductive structures in grain-filling has important implications for cereal breeding. The methods for assessing the contribution by reproductive structure to grain-filling are invasive and prone to problems of compensatory increases in photosynthesis by those structures that have not been manipulated in response to the decreased contribution from structures that have been prevented from photosynthesizing. A novel technique based on the natural abundance of stable carbon isotopes has significant promise. However, it depends crucially on there only being two sources of organic carbon for grain-filling and that these two sources have distinct 13C/12C ratios. There are also examples of the use, and opportunities for further use, of the natural abundance of stable isotopes of carbon and oxygen in exploring the influence of reproduction on whole plant carbon and water relations. A particularly under-explored area is that of dioecious plants, where both the relative effects of reproduction on female and male plants and the role of any photosynthetic contribution from reproductive structures to the carbon, water, and nutrient economy of female and male plants need further investigation.

Photosynthesis in reproductive structures is widespread among oxygenic photosynthetic organisms, including many clades of algae and embryophytes of different levels of complexity and the extent of dominance of the gametophyte and the sporophyte phase in the vegetative activities of a species. Among the possible evolutionary benefits of photosynthesis in reproductive structures is in decreasing the organic carbon cost to the rest of the plant of reproduction, and (in terrestrial plants) ‘using’ the transpiratory loss of water from reproductive structures related to the xylem delivery of the phloem-immobile Ca and Si. One possible cost of photosynthesis in reproductive structures are the increased damage DNA by the necessary exposure of reproductive structures to photosynthetically active, and hence (in nature) UV-B, radiation, and the increased potential for the production of reactive oxygen species. There is also the possibility of decreasing the reproductive potential if the reproductive structures have many structural and functional changes relating to increasing photosynthetic potential.

Acknowledgements

Discussions with John F. Allen, John Beardall, Jason Bragg, Mario Giordano, Linda L. Handley, Hans Lambers, Jessica Royles, Charlie Scrimgeour, and Mark Westoby have been very helpful. The University of Dundee is a registered Scottish Charity, No. SC 015096.

Glossary

Abbreviations:

CAM

crassulacean acid metabolism

WSC

water-soluble compounds.

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