Download Photosynthesis in reproductive structures: costs and benefits

Journal of Experimental Botany, Vol. 66, No. 7 pp. 1699–1705, 2015
doi:10.1093/jxb/erv009 Advance Access publication 20 February 2015
Commentary
Photosynthesis in reproductive structures: costs and benefits
John A. Raven1,* and Howard Griffiths2
1 Division of Plant Sciences, University of Dundee at the James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK†, and School of
Plant Biology, University of Western Australia, M048, 35 Stirling Highway, Crawley, WA 6009, Australia
2 Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK
* To whom correspondence should be addressed. E-mail: [email protected]
Permanent address of JAR.
†
Received 20 October 2014; Revised 16 December 2014; Accepted 19 December 2014
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 grainfilling. 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.
Key words: Carbon on isotope composition, fruit and seed dispersal, oxidative damage, pollination, reproductive structure
photosynthesis, resource allocation.
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
Abbreviations: CAM, crassulacean acid metabolism; WSC, water-soluble compounds.
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1700 | Raven and Griffiths
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 SanchezBragado 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
13
C: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).
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
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
Leaf blade
Leaf sheath
Stem
Xylem sap
Phloem sap
–26.7o/ooa
–29.8o/ooa
–28.3o/ooa
–26.8o/ooa
–28.4o/oo
–28.4o/oo
–28.8o/oo
–30.9o/oo
–30.6o/oo
–28.1o/oo
–28.4o/oo
–28.4o/oo
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.
Photosynthesis in reproductive structures: costs and benefits | 1701
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
13
C 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
1702 | Raven and Griffiths
‘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.
rest of the plan, which might be more important for iteroparous rather than semelparous organisms.
Embryophytes at the bryophyte grade of organization
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 42 mol m–3 Ca2+ (Table 8.2 in Raven, 1984), at maximum
dry matter accumulation (57 mg) 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.
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
Transpiration drives the supply of phloem-immobile
nutrients and photosynthesis offers a low-cost carbon
benefit
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
Photosynthesis in reproductive structures: costs and benefits | 1703
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 shorterlived (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 4 h 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
1704 | Raven and Griffiths
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.
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