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Sex-specific physiology and source-sink relations in the dioecious plant Silene latifolia

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Abstract

Differences in reproductive demands between the sexes of dioecious plants could cause divergence in physiology between the sexes. We found that the reproductive effort of female Silene latifolia plants increased to more than twice that of male plants or female plants that were prevented from setting fruit by lack of pollination after 4 weeks of flowering. Whole-plant source/sink ratios of pollinated females were significantly lower than those of males or unpollinated females because of investment in fruit. We hypothesized that these differences in source/sink ratio between the sexes and within females, depending on pollination, would lead to differences in leaf photosynthetic rates. Within females, we found that photosynthetic capacity was consistent with measurement of whole-plant source/sink ratio. Females that were setting fruit had 30% higher light-saturated photosynthetic rates by 28 days after flowering than females that were not setting fruit. Males, however, had consistently higher photosynthetic rates than females from 10 days after flowering onwards. Males also had approximately twice the dark respiration rates of fruiting females. We found that female reproductive structures are longer-lived and contribute more carbon to their own support than male reproductive structures. Despite the higher rates of leaf dark respiration and lower calyx photosynthetic rates, males fix more carbon than do females. We conclude that females have a sink-regulated mechanism of photosynthesis that allows them to respond to variations in fruit set. This mechanism is not, however, sufficient to explain why male S. latifolia plants have higher rates of photosynthesis, higher source/sink ratios, and lower reproductive allocation, but fail to grow larger than female plants.

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References

  • Adams WW, Winter K, Schreiber U, Schramel P (1990) Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal leaf senescence. Plant Physiol 92:1184–1190

    Google Scholar 

  • Ågren J (1988) Sexual differences in biomass and nutrient allocation in the dioecious Rubus chamaemorus. Ecology 69:962–973

    Google Scholar 

  • Allen GA, Antos JA (1988) Relative reproductive effort in males and females of the dioecious shrub, Oemleria cerasiformis. Oecologia 76:111–118

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in chloroplasts. Plant Physiol 24:1–15

    Google Scholar 

  • Ashman TL, Baker I (1992) Variation in floral sex allocation with time of season and currency. Ecology 73:1237–1243

    Google Scholar 

  • Azcón-Bieto J (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol 73:681–686

    Google Scholar 

  • Barrett JE III, Amling HJ (1978) Effects of developing fruits on production and translocation of 14C-labeled assimilates in cucumber. Hort Sci 13:545–547

    Google Scholar 

  • Bazzaz FA, Carlson RW (1979) Photosynthetic contribution of flowers and seeds to reproductive effort of an annual colonizer. New Phytol 82:223–232

    Google Scholar 

  • Bazzaz FA, Carlson RW, Harper JL (1979) Contribution to reproductive effort by photosynthesis of flowers and fruits. Nature 279:554–555

    Google Scholar 

  • Boussingault JB (1868) Agronomie chimie agricole et physiologie, 2d edn. Mellet Bachelier, Paris

    Google Scholar 

  • Carroll SB, Delph LF (in press) The effects of gender and plant architecture on allocation to flowers in dioecious Silene latifolia (Caryophyllaceae). Int J Plant Sci

  • Carroll SB, Mulcahy DL (1993) Progeny sex ratios in dioecious Silene latifolia (Caryophyllaceae). Am J Bot 80:551–556

    Google Scholar 

  • Cipollini ML, Whigham DF (1994) Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae). Am J Bot 81:65–75

    Google Scholar 

  • Cody ML (1966) A general theory of clutch size. Evolution 20:174–184

    Google Scholar 

  • Conn JS (1981) Phenological differentiation between the sexes of Rumex hastalulus: niche partitioning or different optimal reproductive strategies? Bull Torrey Bot Club 108:374–378

    Google Scholar 

  • Correns C (1928) Bestimmung, Vererbung und Verteilung des Geschlechtes bei den hoheren Pflanzen. Handb Vererbungswiss 2:1–138

    Google Scholar 

  • Dawson TE, Bliss LC (1989) Patterns of water use and the tissue water relations in the dioecious shrub, Salix arctica: the physiological basis for habitat partitioning between the sexes. Oecologia 79:332–343

    Google Scholar 

  • Dawson TE, Bliss LC (1993) Plants as mosaics: leaf-, ramet- and gender-level variation in the physiology of the dwarf willow, Salix arctica. Funct Ecol 7:293–304

    Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815

    Google Scholar 

  • Delph LF (1990) Sex-differential resource allocation patterns in the subdioecious shrub Hebe subalpina. Ecology 71:1342–1351

    Google Scholar 

  • Delph LF, Meagher TR (1995) Sexual dimorphism masks life history trade-offs in the dioecious plant Silene latifolia. Ecology 76:775–785

    Google Scholar 

  • Delph LF, Lu Y, Jayne LD (1993) Patterns of resource-allocation in a dioecious Carex (Cyperaceae). Am J Bot 80:607–615

    Google Scholar 

  • Evans AS (1991) Whole-plant responses of Brassica campestris (Cruciferae) to altered sink-source relations. Am J Bot 78:394–400

    Google Scholar 

  • Evans LT, Rawson HM (1970) Photosynthesis and respiration by the flag leaf and components of the ear during grain development in wheat. Aust J Biol Sci 23:245–254

    Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Google Scholar 

  • Farrar JF (ed) (1993) Sink strength: what is it and how do we measure it? Plant Cell Environ 16:1013–1046

    Google Scholar 

  • Fox JF, Stevens GC (1991) Costs of reproduction in a willow: experimental responses versus natural variation. Ecology 72:1013–1023

    Google Scholar 

  • Fujii JA, Kennedy RA (1985) Seasonal changes in the photosynthetic rate in apple trees: A comparison between fruiting and nonfruiting trees. Plant Physiol 78:519–524

    Google Scholar 

  • Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1–24

    Google Scholar 

  • Galen C, Dawson TE, Stanton ML (1993) Carpels as leaves: meeting the carbon cost of reproduction in an alpine buttercup. Oecologia 95:187–193

    Google Scholar 

  • Gehring JL (1993) Temporal patterns in the development of sexual dimorphisms in Silene latifolia (Caryophyllaceae). Bull Torrey Bot Club 120:405–416

    Google Scholar 

  • Gehring JL, Linhart YB (1993) Sexual dimorphisms and response to low resources in the dioecious plant, Silene latifolia (Caryophyllaceae). Int J Plant Sci 154:152–162

    Google Scholar 

  • Gehring JL, Monson RK (1994) Sexual differences in gas exchange and response to environmental stress in dioecious Silene latifolia (Caryophyllaceae). Am J Bot 81:166–174

    Google Scholar 

  • Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448

    Google Scholar 

  • Hansen P (1970) 14C-Studies on apple trees. VI. The influence of the fruit on the photosynthesis of the leaves, and the relative photosynthetic yields of fruits and leaves. Physiol Plant 23:805–810

    Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity-the missing link. New Phytol 86:131–144

    Google Scholar 

  • Herold A, McGee EEM, Lewis DH (1980) The effect of orthophosphate concentration and exogenously supplied sugars on the distribution of newly fixed carbon in sugar beet leaf discs. New Phytol 85:1–13

    Google Scholar 

  • Houssard C, Thompson JD, Escarre J (1994) Do sex-related differences in response to environmental variation influence the sex-ratio in the dioecious Rumex acetosella? Oikos 70:80–90

    Google Scholar 

  • Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4:59–69

    Google Scholar 

  • Kapp A, Stitt M (1994) Influence of high carbohydrate content on the activity of plastidic and cytosolic isoenzyme pairs in photosynthetic tissues. Plant Cell Environ 17:861–866

    Google Scholar 

  • Krapp A, Hofmann B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the “sink regulation” of photosynthesis? Plant J 3:817–828

    Google Scholar 

  • Laporte MM (1994) Sex-specific physiology and source-sink relations in Silene latifolia. M.A. Thesis. Indiana University, Bloomington, Indiana, USA

  • Lawrence CW (1963) Genetic studies of wild populations of Melandrium. II. Flowering time and plant height. Heredity 18:149–163

    Google Scholar 

  • Lokker C, Susko D, Lovett Doust L, Lovett Doust J (1994) Population genetic structure of Vallisneria americana, a dioecious clonal macrophyte. Am J Bot 81:1004–1012

    Google Scholar 

  • Lovett Doust J, Lovett Doust L (1987) Leaf demography and clonal growth in female and male Rumex acetosella. Ecology 68:2056–2058

    Google Scholar 

  • Lovett Doust J, O'Brien G, Lovett Doust L (1987) Effect of density on secondary sex characteristics and sex ratio in Silene alba (Caryophyllaceae). Am J Bot 74:40–46

    Google Scholar 

  • Lyons EE, Miller D, Meagher TR (1994) Evolutionary dynamics of sex ratio and gender dimorphism in Silene latifolia. I. Environmental effects. J Hered 85:196–203

    Google Scholar 

  • Marshall C, Watson MA (1992) Ecological and physiological aspects of reproductive allocation. In: Marshall C, Grace J (eds) Fruit and seed production. Cambridge University Press, Cambridge, pp 173–202

    Google Scholar 

  • Marshall JD, Dawson TE, Ehleringer JR (1993) Gender-related differences in gas exchange are not related to host quality in the xylem-tapping mistletoe, Phoradendron juniperum (Viscaceae). Am J Bot 80:641–645

    Google Scholar 

  • Meagher TR (1992) The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae). I. Genetic variation. Evolution 46:445–457

    Google Scholar 

  • Mitton and Grant (1980) Observations on the ecology and evolution of quaking aspen, Populus tremuloides, in the Colorado Front Range. Am J Bot 67:202–209

    Google Scholar 

  • Nigtevecht G van (1966) Genetic studies in dioecious Melandrium I. Sex-linked and sex influenced inheritance in M. album and M. dioicum. Genetica 37:281–306

    Google Scholar 

  • Neales TF, Incoll LD (1968) The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: a review of the hypothesis. Bot Rev 34:107–125

    Google Scholar 

  • Popp JW, Reinartz IA (1988) Sexual dimorphism in biomass allocation and clonal growth of Xanthoxylum americanum. Am J Bot 75:1732–1741

    Google Scholar 

  • Primack RB, Miao SL, Becker KR (1994) Costs of reproduction in the pink lady's slipper orchid (Cypripedium acaule): Defoliation, increased fruit production, and fire. Am J Bot 81:1083–1090

    Google Scholar 

  • Putwain PD, Harper JL (1972) Studies in the dynamics of plant populations. V. Mechanisms governing the sex ratio in Rumex acetosa and R. acetosella. J Ecol 60:113–129

    Google Scholar 

  • Reekie EG, Bazzaz FA (1987) Reproductive effort in plants. II. Does carbon reflect the allocation of other resources? Am Nat 129:897–906

    Google Scholar 

  • Reznick D (1983) The structure of guppy life histories: the trade-off between growth and reproduction. Ecology 64:862–873

    Google Scholar 

  • Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84:658–664

    Google Scholar 

  • Sakai AK, Burris TA (1985) Growth in male and female bigtooth aspen (Populus grandidentata). Ecology 68:2031–2033

    Google Scholar 

  • Sawada S, Hasegawa Y, Kasai M, Sasaki M (1989) Photosynthetic electron transport and carbon metabolism during altered source/sink balance in single-rooted soybean leaves. Plant Cell Physiol 30:691–698

    Google Scholar 

  • Schecter I, Proctor JTA, Elfving DC (1994) Carbon exchange rate and accumulation in limbs of fruiting and nonfruiting apple trees. J Am Soc Hort Sci 119:150–156

    Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot Rev 51:53–105

    Google Scholar 

  • Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91:679–684

    Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038

    Google Scholar 

  • Sonnewald U, Willmitzer L (1992) Molecular approaches to sink-source interactions. Plant Physiol 99:1267–1270

    Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, New York

    Google Scholar 

  • Stitt M, Schaewen A von, Willmitzer L (1990) “Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes. Planta 183:40–50

    Google Scholar 

  • Tennessen DJ, Singsaas EL, Sharkey TD (1994) Light-emitting diodes as a light source of photosynthesis research. Photosynth Res 39:85–92

    Google Scholar 

  • Tuomi J, Hakala T, Haukioja E (1983) Alternative concepts of reproductive effort, costs of reproduction, and sclection in life-history evolution. Am Zool 23:25–34

    Google Scholar 

  • Walker DA, Herold A (1977) Can the chloroplast support photosynthesis unaided? Plant Cell Physiol 51:295–310

    Google Scholar 

  • Wallace CS, Rundel PW (1979) Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia 44:34–39

    Google Scholar 

  • Watson MA (1984) Developmental constraints: Effect on population growth and patterns of resource allocation in a clonal plant. Am Nat 123:411–426

    Google Scholar 

  • Watson MA, Casper BB (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annu Rev Ecol Syst 15:233–258

    Google Scholar 

  • Willson MF (1986) On the costs of reproduction in plants: Acer negundo. Am Midland Nat 115:204–207

    Google Scholar 

  • Ye D, Oliveira M, Veuskens J, Wu Y, Installe P, Hinnisdaels S, Truong AT, Brown S, Mouras A, Negrutiu I (1991) Sex determination in the dioecious Melandrium. The X/Y chromosome system allows complementary cloning strategies. Plant Sci 80:93–106

    Google Scholar 

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  1. Marianne M. Laporte

    Present address: Botany Department, University of Wisconsin, 430 Lincoln Drive, 53706, Madison, Wisconsin, USA

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  1. Department of Biology, Indiana University, 47405, Bloomington, Indiana, USA

    Marianne M. Laporte & Lynda F. Delph

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  1. Marianne M. Laporte
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Laporte, M.M., Delph, L.F. Sex-specific physiology and source-sink relations in the dioecious plant Silene latifolia . Oecologia 106, 63–72 (1996). https://doi.org/10.1007/BF00334408

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