Photosynthetic activity increases with leaf size and intercellular spaces in an allomorphic lianescent aroid Rhodospatha oblongata
Dulce Mantuano A E , Thales Ornellas B , Marcos P. M. Aidar C and André Mantovani DA Laboratório de Ecofisiologia Vegetal, Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho 373, Bloco A, sala A1-118, CCS, Cidade Universitária, 21941-590, Rio de Janeiro, RJ, Brazil.
B Escola Nacional de Botânica Tropical; Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, Jardim Botânico, 22460-030, Rio de Janeiro, Brazil.
C Centro de Pesquisas em Ecologia e Fisiologia, Núcleo de Pesquisa em Fisiologia e Bioquímica, Instituto de Botânica de São Paulo, São Paulo, SP, Brazil.
D Laboratório de Botânica Estrutural, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, Jardim Botânico, 22460-030, Rio de Janeiro, Brazil.
E Corresponding author. Email: dulcemantuano.ufrj@gmail.com
Functional Plant Biology 48(6) 557-566 https://doi.org/10.1071/FP20215
Submitted: 24 July 2020 Accepted: 17 December 2020 Published: 9 February 2021
Abstract
This study aimed to investigate leaf anatomy, as well as photosynthetic gas exchange, that underlie the improvement in light foraging capacity, which appears to occur in aroid vines seeking light exposure. Three levels of plant height (soil level, 3 m and 6 m) were categorised for the aroid vine Rhodospatha oblongata Poepp. to represent the transition from ground to canopy. Compared with shaded leaves, leaves exposed to high light conditions were thicker, presenting a larger, spongy parenchyma characterised by a larger transversal area of intercellular spaces. In addition to the increase in maximum CO2 assimilation (Amax) and thicker and larger leaf lamina, we found an increased light saturation point, light compensation point and water use efficiency at 500 µmol PPFD. Nitrogen content per leaf dry mass remained constant across habitats, but Amax/N was 1.5-times greater in the canopy position than in the leaves at soil level, suggesting that CO2 gain did not rely on an N-related biochemical apparatus. The lower δ13C discrimination observed at high canopy leaves corroborated the higher photosynthesis. Altogether, these results suggest that the large and exposed aroid leaves maintained carbon gain coupled with light gain through investing in a more efficient proportion of intercellular spaces and photosynthetic cell surface, which likely allowed a less pronounced CO2 gradient in substomatal-intercellular space.
Keywords: aroid vines, canopy height, CO2 absorption, leaf morpho-physiology, leaf thickness, light foraging, mesophyll conductance, Rhodospatha oblongata Poepp.
References
Ackerly DD (1992) Light, leaf age, and leaf nitrogen concentration in a tropical vine. Oecologia 89, 596–600.| Light, leaf age, and leaf nitrogen concentration in a tropical vine.Crossref | GoogleScholarGoogle Scholar | 28311893PubMed |
Berghuijs HNC, Yin X, Tri Ho Q, van der Putten PEL, Verboven P, Retta MA, Nicolaï BM, Struik PC (2015) Modelling the relationship between CO2 assimilation and leaf anatomical properties in tomato leaves. Plant Science 238, 297–311.
| Modelling the relationship between CO2 assimilation and leaf anatomical properties in tomato leaves.Crossref | GoogleScholarGoogle Scholar |
Brodersen CR, Vogelmann TJ (2010) Do changes in light direction affect absorption profiles in leaves? Functional Plant Biology 37, 403–412.
| Do changes in light direction affect absorption profiles in leaves?Crossref | GoogleScholarGoogle Scholar |
Brodersen CR, Vogelmann TC, Williams WE, Gorton HL (2008) A new paradigm in leaf-level photosynthesis: direct and diffuse lights are not equal. Plant, Cell & Environment 31, 159–164.
Brodribb TJ, Field TS, Jordan GJ (2007) Leaf maximum photosynthesis rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| Leaf maximum photosynthesis rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 17556506PubMed |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
| Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |
Chazdon RL, Pearcy RW, Lee DW, Fetcher N (1996) Photosynthetic responses of tropical forest plants to contrasting light environments. In ‘Tropical Forest Plant Ecophysiology’. (Eds S. S. Mulkey, R. L. Chazdon and A. P. Smith) pp. 5–55. (Springer: Boston, MA, USA)
Domec J-C, Berghoff H, Way DA, Moshelion M, Palmroth S, Kets K, Huang C-W, Oren R (2019) Mechanisms for minimizing height‐related stomatal conductance declines in tall vines. Plant, Cell & Environment 42, 3121–3139.
| Mechanisms for minimizing height‐related stomatal conductance declines in tall vines.Crossref | GoogleScholarGoogle Scholar |
Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H, Diallo A, Grace J, Lloyd J (2010) Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33, 959–980.
| Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands.Crossref | GoogleScholarGoogle Scholar |
Domingues TF, Martinelli LA, Ehleringer JR (2014) Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest. Plant Ecology & Diversity 7, 189–203.
| Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest.Crossref | GoogleScholarGoogle Scholar |
Duarte HM, Jakovlejevic I, Kaiser F, Lüttge U (2005) Lateral diffusion of CO2 in leaves of the crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perrier. Planta 220, 809–816.
| Lateral diffusion of CO2 in leaves of the crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perrier.Crossref | GoogleScholarGoogle Scholar | 15843962PubMed |
Evans JR, Seemann JR (1989) The allocation of protein N in the photosynthetic apparatus: costs, consequences and control. In ‘Photoynthesis’. (Ed. W. R. Briggs) pp. 183–205. (Alan R Liss: New York. USA)
Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281–292.
Evans JR, Terashima I, Hanba YT, Loreto F (2004) CO2 capture by the leaf. In ‘Photosynthetic Adaptation from the Chloroplast to the Landscape’. (Eds W. K. Smith, T. Vogelmann and C. Critchley.) pp. 107–132. (Springer-Verlag: New York, USA)
Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235–2248.
| Resistances along the CO2 diffusion pathway inside leaves.Crossref | GoogleScholarGoogle Scholar | 19395390PubMed |
Farquhar GD, Ehleringer R, Hubic KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Filartiga ALP, Vieira RC, Mantovani A (2014) Size-correlated morpho-physiology of the aroid vine Rhodospatha oblongata along a vertical gradient in a Brazilian rain forest. Plant Biology 16, 155–165.
| Size-correlated morpho-physiology of the aroid vine Rhodospatha oblongata along a vertical gradient in a Brazilian rain forest.Crossref | GoogleScholarGoogle Scholar |
Filartiga ALP, Vieira RC, Mantovani A (2018) Aerial root hydraulic conductivity increases with plant size for the aroid vine Rhodospatha oblongata (Araceae). The Journal of Plant Hydraulics 4, e006
| Aerial root hydraulic conductivity increases with plant size for the aroid vine Rhodospatha oblongata (Araceae).Crossref | GoogleScholarGoogle Scholar |
Filartiga AL, Mantuano D, Vieira RC, Gama de Toni KL, Vasques GM, Mantovani A (2020) Root morphophysiology changes during the habitat transition from soil to canopy of the aroid vine Rhodospatha oblongata. Annals of Botany
| Root morphophysiology changes during the habitat transition from soil to canopy of the aroid vine Rhodospatha oblongata.Crossref | GoogleScholarGoogle Scholar |
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
| Mesophyll conductance to CO2: current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar |
Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriqui M, Diaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Galle A, Galmes J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomas M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Science 193–194, 70–84.
| Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 22794920PubMed |
Flexas J, Niinemets Ü, Gallé A, Barbour MM, Centritto M, Diaz-Espejo A, Douthe C, Galmés J, Ribas-Carbo M, Rodriguez PL, Rosselló F, Soolanayakanahally R, Tomas M, Wright IJ, Farquhar GD, Medrano H (2013) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water use efficiency. Photosynthesis Research 117, 45–59.
| Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water use efficiency.Crossref | GoogleScholarGoogle Scholar | 23670217PubMed |
Freiberg M (1997) Spatial and temporal pattern of temperature and humidity of a tropical premontane rain forest tree in Costa Rica. Selbyana 18, 77–84.
Givnish TJ (1984) Leaf and canopy adaptations in tropical forests. In ‘Physiological Ecology of Plants of the Wet Tropics’. (Eds E. Medina, H. A. Mooney and C. Vázquez-Yánes.) pp. 51–84. (Springer: Dordrecht, The Netherlands.)
Givnish TJ, Vermeij GJ (1976) Sizes and shapes of liane leaves. American Naturalist 110, 743–778.
| Sizes and shapes of liane leaves.Crossref | GoogleScholarGoogle Scholar |
Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2 and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60, 2303–2314.
| Influence of leaf dry mass per area, CO2 and irradiance on mesophyll conductance in sclerophylls.Crossref | GoogleScholarGoogle Scholar | 19286919PubMed |
Holtum JAM, Winter K, Weeks MA, Sexton TR (2007) Crassulacean acid metabolism in the ZZ plant, Zamioculcas zamiifolia (Araceae). American Journal of Botany 94, 1670–1676.
| Crassulacean acid metabolism in the ZZ plant, Zamioculcas zamiifolia (Araceae).Crossref | GoogleScholarGoogle Scholar |
Jácome J, Galeano G, Amaya M, Mora M (2004) Vertical distribution of epiphytic and hemiepiphytic Araceae in a Tropical Rain Forest in Chocó, Colombia. Selbyana 25, 118–125.
Lee DW, Richards JH (1991) Heteroblastic development in vines. In ‘The Biology of Vines’. (Eds F. E. Putz and H. A. Mooney) pp. 205–243. (Cambridge University Press: Cambridge, UK)
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
| Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar |
Lichtenthaler HK, Ač A, Marek MV, Kalina J, Urban O (2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiology and Biochemistry 45, 577–588.
| Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species.Crossref | GoogleScholarGoogle Scholar | 17587589PubMed |
López-Portillo J, Ewers FW, Angeles G, Fisher JB (2000) Hydraulic architecture of Monstera acuminata: evolutionary consequences of the hemiepiphytic growth form. New Phytologist 145, 289–299.
| Hydraulic architecture of Monstera acuminata: evolutionary consequences of the hemiepiphytic growth form.Crossref | GoogleScholarGoogle Scholar |
Lorenzo N, Mantuano D, Mantovani A (2010) Comparative leaf ecophysiology and anatomy of seedlings, young and adult individuals of the epiphytic aroid Anthurium scandens (Aubl.) Engl. Environmental and Experimental Botany 68, 314–322.
| Comparative leaf ecophysiology and anatomy of seedlings, young and adult individuals of the epiphytic aroid Anthurium scandens (Aubl.) Engl.Crossref | GoogleScholarGoogle Scholar |
MacKinney G (1941) Absorption of light by chlorophyll solutions. The Journal of Biological Chemistry 140, 315–322.
Mantovani A (1999) Leaf morpho-physiology and distribution of epiphytic aroids along a vertical gradient in a Brazilian rain forest. Selbyana 20, 241–249.
Mantovani A, Pereira TE, Mantuano D (2017a) Allomorphic growth of Epipremnum aureum (Araceae) as characterized by changes in leaf morphophysiology during the transition from ground to canopy. Brazilian Journal of Botany 40, 177–191.
| Allomorphic growth of Epipremnum aureum (Araceae) as characterized by changes in leaf morphophysiology during the transition from ground to canopy.Crossref | GoogleScholarGoogle Scholar |
Mantovani A, Mantuano D, de Mattos EA (2017b) Relationship between nitrogen resorption and leaf size in the aroid vine Rhodospatha oblongata (Araceae). Australian Journal of Botany 65, 431–437.
| Relationship between nitrogen resorption and leaf size in the aroid vine Rhodospatha oblongata (Araceae).Crossref | GoogleScholarGoogle Scholar |
Mantovani A, Brito C, Mantuano D (2018) Does the same morphology mean the same physiology? Morphophysiological adjustments of Philodendron hederaceum (Jacq.) Schott, an isomorphic aroid, to ground-canopy transition. Theoretical and Experimental Plant Physiology 30, 89–101.
| Does the same morphology mean the same physiology? Morphophysiological adjustments of Philodendron hederaceum (Jacq.) Schott, an isomorphic aroid, to ground-canopy transition.Crossref | GoogleScholarGoogle Scholar |
Milla R, Reich PB (2007) The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proceedings. Biological Sciences 274, 2109–2114.
| The scaling of leaf area and mass: the cost of light interception increases with leaf size.Crossref | GoogleScholarGoogle Scholar | 17591590PubMed |
Montgomery RA, Chazdon RL (2001) Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology 82, 2707–2718.
| Forest structure, canopy architecture, and light transmittance in tropical wet forests.Crossref | GoogleScholarGoogle Scholar |
Nobel PS (1999) ‘Physicochemical and Environmental Plant Physiology.’ (Academic Press: California, USA)
Nobel PS, Zaragoza LJ, Smith WK (1975) Relation between mesophyll surface area, photosynthesis rate and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiology 55, 1067–1070.
| Relation between mesophyll surface area, photosynthesis rate and illumination level during development for leaves of Plectranthus parviflorus Henckel.Crossref | GoogleScholarGoogle Scholar | 16659211PubMed |
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.
| Polychromatic staining of plant cell walls by toluidine blue O.Crossref | GoogleScholarGoogle Scholar |
Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell & Environment 26, 505–512.
| Does the photosynthetic light-acclimation need change in leaf anatomy?Crossref | GoogleScholarGoogle Scholar |
Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell & Environment 28, 916–927.
| Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees.Crossref | GoogleScholarGoogle Scholar |
Pearcy RW (1987) Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments. Functional Ecology 1, 169–178.
| Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments.Crossref | GoogleScholarGoogle Scholar |
Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant, Cell & Environment 20, 411–424.
| An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes.Crossref | GoogleScholarGoogle Scholar |
Peguero-Pina JJ, Flexas J, Galmés J, Niinemets Ü, Sancho-Knapik D, Barredo G, Villarroya D, Gil-Pelegrín E (2012) Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species. Plant, Cell & Environment 35, 2121–2129.
| Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species.Crossref | GoogleScholarGoogle Scholar |
Peguero-Pina JJ, Sisó S, Flexas J, Galmés J, Niinemets Ü, Sancho-Knapik D, Gil-Pelegrín E (2017) Coordinated modifications in mesophyll conductance, photosynthetic potentials and leaf nitrogen contribute to explain the large variation in foliage net assimilation across Quercus ilex povenances. Tree Physiology 37, 1084–1094.
| Coordinated modifications in mesophyll conductance, photosynthetic potentials and leaf nitrogen contribute to explain the large variation in foliage net assimilation across Quercus ilex povenances.Crossref | GoogleScholarGoogle Scholar | 28541538PubMed |
Piel C, Frak E, Le Roux X, Genty B (2002) Effect of local irradiance on CO2 transfer conductance of mesophyll in walnut. Journal of Experimental Botany 53, 2423–2430.
| Effect of local irradiance on CO2 transfer conductance of mesophyll in walnut.Crossref | GoogleScholarGoogle Scholar | 12432034PubMed |
Ray TS (1990) Metamorphosis in the Araceae. American Journal of Botany 77, 1599–1609.
| Metamorphosis in the Araceae.Crossref | GoogleScholarGoogle Scholar |
Ray TS (1992) Foraging behavior in tropical herbaceous climbers (Araceae). Journal of Ecology 80, 189–203.
| Foraging behavior in tropical herbaceous climbers (Araceae).Crossref | GoogleScholarGoogle Scholar |
Ruzin SE (1999) ‘Plant Microtechnique and Microscopy.’ (Oxford University Press: Oxford, UK)
Schuepp PH (1993) Tansley Review No. 59. Leaf boundary layers. New Phytologist 125, 477–507.
| Tansley Review No. 59. Leaf boundary layers.Crossref | GoogleScholarGoogle Scholar |
Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell & Environment 18, 149–157.
| On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves.Crossref | GoogleScholarGoogle Scholar |
Terashima I (1992) Anatomy of non-uniform leaf photosynthesis (mini-review). Photosynthesis Research 31, 195–212.
| Anatomy of non-uniform leaf photosynthesis (mini-review).Crossref | GoogleScholarGoogle Scholar | 24408060PubMed |
Terashima I, Miyazawa S-I, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. Journal of Plant Research 114, 93–105.
| Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf.Crossref | GoogleScholarGoogle Scholar |
Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. Journal of Experimental Botany 57, 343–354.
| Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion.Crossref | GoogleScholarGoogle Scholar | 16356943PubMed |
Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiology 155, 108–116.
| Leaf functional anatomy in relation to photosynthesis.Crossref | GoogleScholarGoogle Scholar | 21075960PubMed |
Thain JF (1983) Curvature correction factors in the measurement of cell surface areas in plant tissues. Journal of Experimental Botany 34, 87–94.
| Curvature correction factors in the measurement of cell surface areas in plant tissues.Crossref | GoogleScholarGoogle Scholar |
Thornley JHM (1976) ‘Mathematical Models in Plant Physiology. A Quantitative Approach to Problems in Plant and Crop Physiology.’ (Academic Press: New York, USA)
Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Ribas-Carbó M, Tosens T, Vislap V, Niinemets Ü (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up to models. Journal of Experimental Botany 64, 2269–2281.
| Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up to models.Crossref | GoogleScholarGoogle Scholar | 23564954PubMed |
Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. Journal of Experimental Botany 63, 5105–5119.
| Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path.Crossref | GoogleScholarGoogle Scholar | 22888123PubMed |
Tosens T, Nishida K, Gago J, Coopman E, Cabrera HM, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, Talts E, Tomas M, Hanba Y, Niinemets Ü, Flexas J (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytologist 209, 1576–1590.
| The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait.Crossref | GoogleScholarGoogle Scholar |
Vernon LP (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Analytical Chemistry 32, 1144–1150.
| Spectrophotometric determination of chlorophylls and pheophytins in plant extracts.Crossref | GoogleScholarGoogle Scholar |
Veromann-Jürgenson LL, Tosens T, Laanisto L, Niinemets Ü (2017) Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living! Journal of Experimental Botany 68, 1639–1653.
| Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!Crossref | GoogleScholarGoogle Scholar | 28419340PubMed |
Vogelmann C, Evans JR (2002) Profiles of light absorption within spinach leaves from chlorophyll fluorescence. Plant, Cell & Environment 25, 1313–1323.
| Profiles of light absorption within spinach leaves from chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |
von Caemmerer S, Quick WP (2000) Rubisco: physiology in vivo. In ‘Photosynthesis: Physiology and Metabolism’. (Eds R. C. Leegood, T. D. Sharkey, S. von Caemmerer) pp. 85–113. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. Journal of Experimental Botany 59, 1475–1487.
| Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer.Crossref | GoogleScholarGoogle Scholar | 17975206PubMed |
Warren CR, Adams M (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant, Cell & Environment 29, 192–201.
| Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282, 424–426.
| Stomatal conductance correlates with photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groon PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |
Zotz G (1997) Photosynthetic capacity increases with plant size. Plant Biology 110, 306–308.
Zotz G, Hietz P, Schmidt G (2001) Small plants, large plants: the importance of plant size for the physiological ecology. Journal of Experimental Botany 52, 2051–2056.
| Small plants, large plants: the importance of plant size for the physiological ecology.Crossref | GoogleScholarGoogle Scholar | 11559741PubMed |