Leaf shape influences spatial variation in photosynthetic function in Lomatia tinctoria
Andrea Leigh A D , Ross Hill B and Marilyn C. Ball C
+ Author Affiliations
- Author Affiliations
A School of the Environment, University of Technology, Sydney, PO Box 123, Broadway, NSW 2007, Australia.
B Centre for Marine Bio-Innovation and Sydney Institute of Marine Science, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW 2052, Australia.
C Plant Science Division, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
D Corresponding author. Email: andrea.leigh@uts.edu.au
Functional Plant Biology 41(8) 833-842 https://doi.org/10.1071/FP13334
Submitted: 14 November 2013 Accepted: 25 February 2014 Published: 22 April 2014
Abstract
A relationship exists between the two-dimensional shape of leaves and their venation architecture, such that broad or broad-lobed leaves can have leaf tissue far from major veins, potentially creating stronger gradients in water potential – and associated photosynthetic function – than found across narrow counterparts. We examined the spatial patterns of photosynthetic efficiency (ΔF/Fm′) and non-photochemical quenching (NPQ) in response to increased vapour pressure deficit (VPD) using two morphs of Lomatia tinctoria (Labill.) R.Br: those with broad-lobed and those with narrow-lobed leaves. Stomatal conductance (gs), instantaneous water use efficiency (WUE), stomatal and minor veins density also were measured. ΔF/Fm′ decreased with stress but was higher and less spatially heterogeneous across broad than narrow lobes. The strongest depression in ΔF/Fm′ in broad lobes was at the edges and in narrow lobes, the tips. Non-photochemical quenching was spatially more varied in broad lobes, increasing at the edges and tips. Variation in photosynthetic function could not be explained by gs, WUE or minor vein density, whereas proximity to major veins appeared to mitigate water stress at the tips only for broad lobes. Our findings indicate that the relationship between venation architecture and water delivery alone can partially explain the spatial pattern of photosynthetic function.
Additional keywords: chlorophyll fluorescence, leaf morphology, leaf shape, leaf venation, photoprotection, water stress.
References
Barradas VL, Jones HG, Clark JA (1994) Stomatal responses to changing irradiance in Phaseolus vulgaris L. Journal of Experimental Botany 45, 931–936.| Stomatal responses to changing irradiance in Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtVWju78%3D&md5=07b8c90298b962d30b4ef0997e8030efCAS |
Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist 188, 1113–1123.
| Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 20738785PubMed |
Blackman CJ, Brodribb TJ, Jordan GJ (2012) Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168, 1–10.
| Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 21744163PubMed |
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575–584.
| Hydraulic failure defines the recovery and point of death in water-stressed conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Wqtb4%3D&md5=2442d1e9d742838003d24f6613ac2fdfCAS | 19011001PubMed |
Brodribb TJ, Holbrook NM (2005) Leaf physiology does not predict leaf habit; examples from tropical dry forest. Trees – Structure and Function 19, 290–295.
| Leaf physiology does not predict leaf habit; examples from tropical dry forest.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=af12f58caacd925d16035eea3ba3533dCAS | 17556506PubMed |
Buckley TN, Mott KA (2000) Stomatal responses to non-local changes in PFD: evidence for long-distance hydraulic interactions. Plant, Cell & Environment 23, 301–309.
| Stomatal responses to non-local changes in PFD: evidence for long-distance hydraulic interactions.Crossref | GoogleScholarGoogle Scholar |
Cardon ZG, Mott KA, Berry JA (1994) Dynamics of patchy stomatal movements, and their contribution to steady state and oscillating stomatal conductance calculated using gas exchange techniques. Plant, Cell & Environment 17, 995–1007.
| Dynamics of patchy stomatal movements, and their contribution to steady state and oscillating stomatal conductance calculated using gas exchange techniques.Crossref | GoogleScholarGoogle Scholar |
Cochard H, Nardini A, Coll L (2004) Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell & Environment 27, 1257–1267.
| Hydraulic architecture of leaf blades: where is the main resistance?Crossref | GoogleScholarGoogle Scholar |
Csintalan Z, Proctor MCF, Tuba Z (1999) Chlorophyll fluorescence during drying and rehydration in the mosses Rhytidiadelphus loreus (Hedw.) Warnst., Anomodon viticulosus (Hedw.) Hook. & Tayl. and Grimmia pulvinata (Hedw.) Sm. Annals of Botany 84, 235–244.
| Chlorophyll fluorescence during drying and rehydration in the mosses Rhytidiadelphus loreus (Hedw.) Warnst., Anomodon viticulosus (Hedw.) Hook. & Tayl. and Grimmia pulvinata (Hedw.) Sm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCgtL0%3D&md5=e1c523a34813c8f9cf68331450185632CAS |
Deltoro VI, Calatayud A, Gimeno C, Barreno E (1998) Water relations, chlorophyll fluorescence, and membrane permeability during desiccation in bryophytes from xeric, mesic, and hydric environments. Canadian Journal of Botany 76, 1923–1929.
| Water relations, chlorophyll fluorescence, and membrane permeability during desiccation in bryophytes from xeric, mesic, and hydric environments.Crossref | GoogleScholarGoogle Scholar |
Demmig B, Winter K, Kruger A, Czygan FC (1988) Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water-stress. Plant Physiology 87, 17–24.
| Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water-stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXksFWqs7c%3D&md5=9a48fad507f2a5605554a36330b5e46aCAS | 16666096PubMed |
Iio A, Fukasawa H, Nose Y, Kakubari Y (2004) Stomatal closure induced by high vapor pressure deficit limited midday photosynthesis at the canopy top of Fagus crenata Blume on Naeba mountain in Japan. Trees – Structure and Function 18, 510–517.
Marenco RA, Siebke K, Farquhar GD, Ball MC (2006) Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum. Functional Plant Biology 33, 1103–1113.
| Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum.Crossref | GoogleScholarGoogle Scholar |
Meinzer FC, Goldstein G, Jackson P, Holbrook NM, Gutierrez MV, Cavelier J (1995) Environmental and physiological regulation of transpiration in tropical forest gap species – the influence of boundary layer and hydraulic properties. Oecologia 101, 514–522.
| Environmental and physiological regulation of transpiration in tropical forest gap species – the influence of boundary layer and hydraulic properties.Crossref | GoogleScholarGoogle Scholar |
Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology 38, 535–552.
| The evolution and functional significance of leaf shape in the angiosperms.Crossref | GoogleScholarGoogle Scholar |
Omasa K, Takayama K (2003) Simultaneous measurement of stomatal conductance, non-photochemical quenching, and photochemical yield of photosystem II in intact leaves by thermal and chlorophyll fluorescence imaging. Plant & Cell Physiology 44, 1290–1300.
| Simultaneous measurement of stomatal conductance, non-photochemical quenching, and photochemical yield of photosystem II in intact leaves by thermal and chlorophyll fluorescence imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFKqsQ%3D%3D&md5=b79a9e735b394368fe796e346b22d785CAS |
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
| Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar | 16637372PubMed |
Sack L, Tyree MT, Holbrook NM (2005) Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167, 403–413.
| Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees.Crossref | GoogleScholarGoogle Scholar | 15998394PubMed |
Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156, 832–843.
| Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrk%3D&md5=035989dacb128ea1c13ecb51c3b0b58bCAS | 21511989PubMed |
Siebke K, Weis E (1995) Assimilation images of leaves of Glechoma hederacea: analysis of nonsynchronous stomata related oscillations. Planta 196, 155–165.
| Assimilation images of leaves of Glechoma hederacea: analysis of nonsynchronous stomata related oscillations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvVemsbw%3D&md5=ec1ae04ad81327f15c71d3fd799441d4CAS |
Sisó S, Camarero JJ, Gil-Pelegrin E (2001) Relationship between hydraulic resistance and leaf morphology in broadleaf Quercus species: a new interpretation of leaf lobation. Trees – Structure and Function 15, 341–345.
| Relationship between hydraulic resistance and leaf morphology in broadleaf Quercus species: a new interpretation of leaf lobation.Crossref | GoogleScholarGoogle Scholar |
Sommerville KE, Gimeno TE, Ball MC (2010) Primary nerve (vein) density influences spatial heterogeneity of photosynthetic response to drought in two Acacia species. Functional Plant Biology 37, 840–848.
| Primary nerve (vein) density influences spatial heterogeneity of photosynthetic response to drought in two Acacia species.Crossref | GoogleScholarGoogle Scholar |
Sommerville KE, Sack L, Ball MC (2012) Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density. Plant, Cell & Environment 35, 158–168.
| Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density.Crossref | GoogleScholarGoogle Scholar |
Tinoco-Ojanguren C, Pearcy RW (1993) Stomatal dynamics and its importance to carbon gain in 2 rainforest Piper species. 1. VPD effects on the transient stomatal response to lightflecks. Oecologia 94, 388–394.
| Stomatal dynamics and its importance to carbon gain in 2 rainforest Piper species. 1. VPD effects on the transient stomatal response to lightflecks.Crossref | GoogleScholarGoogle Scholar |
Zhang SR, Ma KP, Chen LZ (2002) Tempo-spatial variations in stomatal conductance, aperture and density of Ligustrum sinense acclimated to different light environments. Acta Botanica Sinica 44, 1225–1232.
Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM (2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25, 1445–1450.
| Hydraulic architecture of leaf venation in Laurus nobilis L.Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Boyce CK, Holbrook NM (2004a) Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape. Annals of Botany 94, 507–513.
| Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape.Crossref | GoogleScholarGoogle Scholar | 15319225PubMed |
Zwieniecki MA, Boyce CK, Holbrook NM (2004b) Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant, Cell & Environment 27, 357–365.
| Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves.Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Stone HA, Leigh A, Boyce CK, Holbrook NM (2006) Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant, Cell & Environment 29, 803–809.
| Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves.Crossref | GoogleScholarGoogle Scholar |
