Different water relations between flowering and leaf periods: a case study in flower-before-leaf-emergence Magnolia species
Hui Liu A B , Qiu-Yuan Xu A C , Marjorie R. Lundgren D and Qing Ye A B EA Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Xingke Road 723, Tianhe District, Guangzhou 510650, China.
B Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China.
C University of Chinese Academy of Sciences, Yuquan Road 19A, Beijing 100049, China.
D Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
E Corresponding author. Email: qye@scbg.ac.cn
Functional Plant Biology 44(11) 1098-1110 https://doi.org/10.1071/FP16429
Submitted: 8 December 2016 Accepted: 11 July 2017 Published: 11 August 2017
Abstract
The differing water relations between flowers and leaves on a plant reflect the lack of co-ordination between reproductive and vegetative organs during the evolution of angiosperm species. The amount of water that flowers consume has been reported to vary across species, and compared with studies of leaves, accurate measurements of flower water relations at the branch level are lacking. Further, the mechanisms by which flowers regulate their hydraulic function and structure to maintain water balance remain unclear. To explore the ecophysiological basis underpinning the differences between flowers and leaves, we measured hydraulic and morphological traits and monitored sap flow in flowers and leaves from the same branches of two Magnoliaceae species that flower before leaf emergence (Magnolia denudata Desr. and Magnolia soulangeana Soul.-Bod.). Sap flux density (JS) of flowers was 22% and 55% of that predicted for leaves in M. denudata and M. soulangeana respectively. JS of flowers commenced before predawn and ceased early in the afternoon, reflecting their night-time flowering pattern and a dramatic decrease of JS with increasing vapour pressure deficit (D) under the high light of midday. Relative to leaves, tepals were thicker and more hydrated, and had bigger but scarcer stomata, leading to lower stomatal conductance (gs) and transpiration rate (E), less negative water potential (Ψtepal) and lower hydraulic conductance. This study revealed different hydraulic patterns in the flowers and leaves of the two Magnolia species. Although flowers consumed less than half the water that leaves did, they used different strategies to maintain sufficiently high Ψ to sustain hydraulic safety. Magnolia flowers retained more hydrated tepals by exhibiting less water loss than leaves via lower hydraulic conductance. In contrast, Magnolia leaves maintained high transpiration rates through efficient stomatal responses to environmental changes compared with flowers.
Additional keywords: floral hydraulics, flowering stage, gas exchange, leaf hydraulic conductance, Magnoliaceae, sap flow, stomata, water potential, xylem hydraulic conductivity.
References
Azad AK, Sawa Y, Ishikawa T, Shibata H (2007) Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower opening and closing. Annals of Applied Biology 150, 81–87.| Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower opening and closing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtF2isbc%3D&md5=0fe1b1355e6daf141b1f57ffbd6ea562CAS |
Azuma H, Thien LB, Kawano S (1999) Floral scents, leaf volatiles and thermogenic flowers in Magnoliaceae. Plant Species Biology 14, 121–127.
| Floral scents, leaf volatiles and thermogenic flowers in Magnoliaceae.Crossref | GoogleScholarGoogle Scholar |
Azuma H, García-Franco JG, Rico-Gray V, Thien LB (2001) Molecular phylogeny of the Magnoliaceae: the biogeography of tropical and temperate disjunctions. American Journal of Botany 88, 2275–2285.
| Molecular phylogeny of the Magnoliaceae: the biogeography of tropical and temperate disjunctions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFyitw%3D%3D&md5=8bd234445662ed5dd353ca4b31a473b4CAS |
Blanke MM, Lovatt CJ (1993) Anatomy and transpiration of the avocado inflorescence. Annals of Botany 71, 543–547.
| Anatomy and transpiration of the avocado inflorescence.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175–183.
| Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Holbrook NM (2003) Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest. New Phytologist 158, 295–303.
| Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest.Crossref | GoogleScholarGoogle Scholar |
Brodribb T, Holbrook NM (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant, Cell & Environment 27, 820–827.
| Diurnal depression of leaf hydraulic conductance in a tropical tree species.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=4f04ed96d6b9423f9048f7253d491de9CAS |
Brown HT, Escombe F (1900) Static diffusion of gases and liquids in relation to the assimilation of carbon and translocation in plants. Proceedings of the Royal Society of London 67, 124–128.
| Static diffusion of gases and liquids in relation to the assimilation of carbon and translocation in plants.Crossref | GoogleScholarGoogle Scholar |
Chambers JL, Hinckley TM, Cox GS, Metcalf C, Aslin R (1985) Boundary-line analysis and models of leaf conductance for 4 oak-hickory forest species. Forest Science 31, 437–450.
Chapotin S, Holbrook N, Morse S, Gutierrez M (2003) Water relations of tropical dry forest flowers: pathways for water entry and the role of extracellular polysaccharides. Plant, Cell & Environment 26, 623–630.
| Water relations of tropical dry forest flowers: pathways for water entry and the role of extracellular polysaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsl2rurY%3D&md5=6e3d47f7f7515539b8bd944d46671d73CAS |
Dandy JE (1927) The genera of Magnoliaceae. Kew Bulletin 7, 257–264.
Dieringer G (1999) Beetle pollination and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae). International Journal of Plant Sciences 160, 64–71.
| Beetle pollination and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae).Crossref | GoogleScholarGoogle Scholar |
Ewers B, Gower S, Bond-Lamberty B, Wang C (2005) Effects of stand age and tree species on canopy transpiration and average stomatal conductance of boreal forests. Plant, Cell & Environment 28, 660–678.
| Effects of stand age and tree species on canopy transpiration and average stomatal conductance of boreal forests.Crossref | GoogleScholarGoogle Scholar |
Feild TS, Chatelet DS, Brodribb TJ (2009a) Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7, 237–264.
| Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3ltFagsg%3D%3D&md5=dcadfe35b3134e1492455caf002bccb1CAS |
Feild TS, Chatelet DS, Brodribb TJ (2009b) Giant flowers of Southern magnolia are hydrated by the xylem. Plant Physiology 150, 1587–1597.
| Giant flowers of Southern magnolia are hydrated by the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFeru7g%3D&md5=bb5cc4924e0ff0e2a629f31256588027CAS |
Figlar RB, Nooteboom HP (2004) Notes on Magnoliaceae IV. Blumea 49, 87–100.
| Notes on Magnoliaceae IV.Crossref | GoogleScholarGoogle Scholar |
Franks PJ (2004) Stomatal control and hydraulic conductance, with special reference to tall trees. Tree Physiology 24, 865–878.
| Stomatal control and hydraulic conductance, with special reference to tall trees.Crossref | GoogleScholarGoogle Scholar |
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 10343–10347.
| Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1Giurg%3D&md5=8952cb3c20c1fb52b33e8e134eb8827bCAS |
Galen C, Sherry RA, Carroll AB (1999) Are flowers physiological sinks or faucets? Costs and correlates of water use by flowers of Polemonium viscosum. Oecologia 118, 461–470.
| Are flowers physiological sinks or faucets? Costs and correlates of water use by flowers of Polemonium viscosum.Crossref | GoogleScholarGoogle Scholar |
Gottsberger G, Silberbauer-Gottsberger I, Seymour RS, Dötterl S (2012) Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus. Flora – Morphology, Distribution, Functional Ecology of Plants 207, 107–118.
| Pollination ecology of Magnolia ovata may explain the overall large flower size of the genus.Crossref | GoogleScholarGoogle Scholar |
Granier A, Loustau D (1994) Measuring and modelling the transpiration of a maritime pine canopy from sap-flow data. Agricultural and Forest Meteorology 71, 61–81.
| Measuring and modelling the transpiration of a maritime pine canopy from sap-flow data.Crossref | GoogleScholarGoogle Scholar |
Gross KL, Soule JD (1981) Differences in biomass allocation to reproductive and vegetative structures of male and female plants of a dioecious, perennial herb, Silene alba (Miller) Krause. American Journal of Botany 68, 801–807.
| Differences in biomass allocation to reproductive and vegetative structures of male and female plants of a dioecious, perennial herb, Silene alba (Miller) Krause.Crossref | GoogleScholarGoogle Scholar |
Hew CS, Lee GL, Wong SC (1980) Occurrence of non-functional stomata in the flowers of tropical orchids. Annals of Botany 46, 195–201.
| Occurrence of non-functional stomata in the flowers of tropical orchids.Crossref | GoogleScholarGoogle Scholar |
Higuchi H, Sakuratani T (2005) The sap flow in the peduncle of the mango (Mangifera indica L.) inflorescence as measured by the stem heat balance method. Journal of the Japanese Society for Horticultural Science 74, 109–114.
| The sap flow in the peduncle of the mango (Mangifera indica L.) inflorescence as measured by the stem heat balance method.Crossref | GoogleScholarGoogle Scholar |
Kim S, Suh Y (2013) Phylogeny of Magnoliaceae based on ten chloroplast DNA regions. Journal of Plant Biology 56, 290–305.
| Phylogeny of Magnoliaceae based on ten chloroplast DNA regions.Crossref | GoogleScholarGoogle Scholar |
Lambrecht SC (2013) Floral water costs and size variation in the highly selfing Leptosiphon bicolor (Polemoniaceae). International Journal of Plant Sciences 174, 74–84.
| Floral water costs and size variation in the highly selfing Leptosiphon bicolor (Polemoniaceae).Crossref | GoogleScholarGoogle Scholar |
Lambrecht S, Dawson T (2007) Correlated variation of floral and leaf traits along a moisture availability gradient. Oecologia 151, 574–583.
| Correlated variation of floral and leaf traits along a moisture availability gradient.Crossref | GoogleScholarGoogle Scholar |
Lambrecht SC, Santiago LS, DeVan CM, Cervera JC, Stripe CM, Buckingham LA, Pasquini SC (2011) Plant water status and hydraulic conductance during flowering in the southern California coastal sage shrub Salvia mellifera (Lamiaceae). American Journal of Botany 98, 1286–1292.
| Plant water status and hydraulic conductance during flowering in the southern California coastal sage shrub Salvia mellifera (Lamiaceae).Crossref | GoogleScholarGoogle Scholar |
Law YW (2004) ‘Magnolias of China.’ (Beijing Sciences & Technology Press: Beijing)
Liu YH, Zhou RZ, Zeng QW (1997) Ex situ conservation of Magnoliaceae including its area and endangered species. Redai Yaredai Zhiwu Xuebao 5, 1–12. [In Chinese].
Liu H, Lundgren MR, Freckleton RP, Xu QY, Ye Q (2016) Uncovering the spatio-temporal drivers of species trait variances: a case study of Magnoliaceae in China. Journal of Biogeography 43, 1179–1191.
| Uncovering the spatio-temporal drivers of species trait variances: a case study of Magnoliaceae in China.Crossref | GoogleScholarGoogle Scholar |
Lohammar T, Larsson S, Linder S, Falk SO (1980) FAST: simulation models of gaseous exchange in Scots pine. Ecological Bulletins 32, 505–523.
Meinzer F, Grantz D (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant, Cell & Environment 13, 383–388.
| Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity.Crossref | GoogleScholarGoogle Scholar |
Meinzer FC, James SA, Goldstein G (2004) Dynamics of transpiration, sap flow and use of stored water in tropical forest canopy trees. Tree Physiology 24, 901–909.
| Dynamics of transpiration, sap flow and use of stored water in tropical forest canopy trees.Crossref | GoogleScholarGoogle Scholar |
Munguía-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14, 511–521.
| Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured.Crossref | GoogleScholarGoogle Scholar |
Nardini A, Pedà G, Rocca NL (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist 196, 788–798.
| Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.Crossref | GoogleScholarGoogle Scholar |
Oren R, Sperry J, Katul G, Pataki D, Ewers B, Phillips N, Schäfer K (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant, Cell & Environment 22, 1515–1526.
| Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit.Crossref | GoogleScholarGoogle Scholar |
Oren R, Sperry J, Ewers B, Pataki D, Phillips N, Megonigal J (2001) Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in a flooded Taxodium distichum L. forest: hydraulic and non-hydraulic effects. Oecologia 126, 21–29.
| Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in a flooded Taxodium distichum L. forest: hydraulic and non-hydraulic effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cnhsFymsg%3D%3D&md5=573958eda0a21abc9b224ca123c8a5d3CAS |
Ortuño MF, García-Orellana Y, Conejero W, Ruiz-Sánchez MC, Alarcón JJ, Torrecillas A (2006) Stem and leaf water potentials, gas exchange, sap flow, and trunk diameter fluctuations for detecting water stress in lemon trees. Trees 20, 1–8.
| Stem and leaf water potentials, gas exchange, sap flow, and trunk diameter fluctuations for detecting water stress in lemon trees.Crossref | GoogleScholarGoogle Scholar |
Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (1999) The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404–407.
| The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2Flt1WlsA%3D%3D&md5=01bea02cc527e9e84000511e6721c96eCAS |
R Development Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at http://www.R-project.org/ [Verified 6 May 2017].
Reekie E, Bazzaz F (1987) Reproductive effort in plants. 3. Effect of reproduction on vegetative activity. The American Naturalist 129, 907–919.
| Reproductive effort in plants. 3. Effect of reproduction on vegetative activity.Crossref | GoogleScholarGoogle Scholar |
Roddy A, Dawson T (2012) Determining the water dynamics of flowering using miniature sap flow sensors. Acta Horticulturae 47–53.
| Determining the water dynamics of flowering using miniature sap flow sensors.Crossref | GoogleScholarGoogle Scholar |
Roddy AB, Guilliams CM, Lilittham T, Farmer J, Wormser V, Pham T, Fine PV, Feild TS, Dawson TE (2013) Uncorrelated evolution of leaf and petal venation patterns across the angiosperm phylogeny. Journal of Experimental Botany 64, 4081–4088.
| Uncorrelated evolution of leaf and petal venation patterns across the angiosperm phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SmtLbF&md5=0de09dc6b7b747c32d320cc966121f6aCAS |
Roddy AB, Brodersen CR, Dawson TE (2016) Hydraulic conductance and the maintenance of water balance in flowers. Plant, Cell & Environment 39, 2123–2132.
| Hydraulic conductance and the maintenance of water balance in flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVCqtrnJ&md5=dcc34c2b13e239434f757fa817cd58d1CAS |
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53, 2177–2184.
| The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1KgtLg%3D&md5=baea30cd2af01a0e57090301387cc309CAS |
Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26, 1343–1356.
| The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species.Crossref | GoogleScholarGoogle Scholar |
Sakuratani T (1981) A heat balance method for measuring water flux in the stem of intact plants. Journal of Agricultural Meteorology 37, 9–17.
| A heat balance method for measuring water flux in the stem of intact plants.Crossref | GoogleScholarGoogle Scholar |
Schulte PJ, Hinckley TM (1985) A comparison of pressure-volume curve data analysis techniques. Journal of Experimental Botany 36, 1590–1602.
| A comparison of pressure-volume curve data analysis techniques.Crossref | GoogleScholarGoogle Scholar |
Seymour RS, White CR, Gibernau M (2003) Environmental biology: heat reward for insect pollinators. Nature 426, 243–244.
| Environmental biology: heat reward for insect pollinators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVOisr0%3D&md5=e086b4a6bb1ab822772846111a8ad12fCAS |
Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant, Cell & Environment 31, 632–645.
| Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees.Crossref | GoogleScholarGoogle Scholar |
Teixido AL, Valladares F (2014) Disproportionate carbon and water maintenance costs of large corollas in hot Mediterranean ecosystems. Perspectives in Plant Ecology, Evolution and Systematics 16, 83–92.
| Disproportionate carbon and water maintenance costs of large corollas in hot Mediterranean ecosystems.Crossref | GoogleScholarGoogle Scholar |
Thien LB (1974) Floral biology of Magnolia. American Journal of Botany 61, 1037–1045.
| Floral biology of Magnolia.Crossref | GoogleScholarGoogle Scholar |
Thien LB, Azuma H, Kawano S (2000) New perspectives on the pollination biology of basal angiosperms. International Journal of Plant Sciences 161, S225–S235.
| New perspectives on the pollination biology of basal angiosperms.Crossref | GoogleScholarGoogle Scholar |
Thien LB, Bernhardt P, Devall MS, Chen Z-d, Luo Y-b, Fan J-H, Yuan L-C, Williams JH (2009) Pollination biology of basal angiosperms (ANITA grade). American Journal of Botany 96, 166–182.
| Pollination biology of basal angiosperms (ANITA grade).Crossref | GoogleScholarGoogle Scholar |
Tyree M, Hammel H (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23, 267–282.
| The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Biology 40, 19–36.
| Vulnerability of xylem to cavitation and embolism.Crossref | GoogleScholarGoogle Scholar |
Wada H, Iwaya-Inoue M, Akita M, Nonami H (2004) Direct measurements of cell turgor and hydraulic conductance in expanding tulip (Tulipa gesneriana L.) tepals. Environment Control in Biology (Japan) 42, 205–215.
| Direct measurements of cell turgor and hydraulic conductance in expanding tulip (Tulipa gesneriana L.) tepals.Crossref | GoogleScholarGoogle Scholar |
Wang R, Xu S, Liu X, Zhang Y, Wang J, Zhang Z (2014) Thermogenesis, flowering and the association with variation in floral odour attractants in Magnolia sprengeri (Magnoliaceae). PLoS One 9, e99356
| Thermogenesis, flowering and the association with variation in floral odour attractants in Magnolia sprengeri (Magnoliaceae).Crossref | GoogleScholarGoogle Scholar |
Whiley A, Chapman K, Saranah J (1988) Water loss by floral structures of avocado (Persea americana cv. Fuerte) during flowering. Australian Journal of Agricultural Research 39, 457–467.
| Water loss by floral structures of avocado (Persea americana cv. Fuerte) during flowering.Crossref | GoogleScholarGoogle Scholar |
Xu F, Rudall P (2006) Comparative floral anatomy and ontogeny in Magnoliaceae. Plant Systematics and Evolution 258, 1–15.
| Comparative floral anatomy and ontogeny in Magnoliaceae.Crossref | GoogleScholarGoogle Scholar |
Zhang F-P, Brodribb TJ (2017) Are flowers vulnerable to xylem cavitation during drought? Proceedings. Biological Sciences 284, 20162642
| Are flowers vulnerable to xylem cavitation during drought?Crossref | GoogleScholarGoogle Scholar |
Zhang F-P, Yang Y-J, Yang Q-Y, Zhang W, Brodribb TJ, Hao G-Y, Hu H, Zhang S-B (2017) Floral mass per area and water maintenance traits are correlated with floral longevity in Paphiopedilum (Orchidaceae). Frontiers in Plant Science 8, 501