Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Summary: Cycads are the most ancient lineage of living seed plants, but the design of their leaves has received little study. We tested whether cycad leaves are governed by the same fundamental design principles previously established for ferns, conifers and angiosperms, and characterized the uniqueness of this relict lineage in foliar trait relationships. Leaf structure, photosynthesis, hydraulics and nutrient composition were studied in 33 cycad species from nine genera and three families growing in two botanical gardens. Cycads varied greatly in leaf structure and physiology. Similarly to other lineages, light-saturated photosynthetic rate per mass (Am) was related negatively to leaf mass per area and positively to foliar concentrations of chlorophyll, nitrogen (N), phosphorus and iron, but unlike angiosperms, leaf photosynthetic rate was not associated with leaf hydraulic conductance. Cycads had lower photosynthetic N use efficiency and higher photosynthetic performance relative to hydraulic capacity compared with other lineages. These findings extend the relationships shown for foliar traits in angiosperms to the cycads. This functional convergence supports the modern synthetic understanding of leaf design, with common constraints operating across lineages, even as they highlight exceptional aspects of the biology of this key relict lineage. © 2015 New Phytologist Trust.

Registro:

Documento: Artículo
Título:Extending the generality of leaf economic design principles in the cycads, an ancient lineage
Autor:Zhang, Y.-J.; Cao, K.-F.; Sack, L.; Li, N.; Wei, X.-M.; Goldstein, G.
Filiación:Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, United States
State Key Lab for Cons. and Util. of Subtropical Agro-biores. and College of Forestry, Guangxi University, Nanning, Guangxi, 530004, China
Department of Ecology and Evolutionary Biology, University of California, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, United States
National Cycad Germplasm Conservation Center, Fairylake Botanical Garden, Shenzhen and Chinese Academy of Sciences, 160 Xianhu Rd., Liantang, Shenzhen, 518004, China
Department of Biology, University of Miami, PO Box 249118, Coral Gables, FL 33124, United States
Departamento de Ecologia Genetica y Evolucion, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Nuñez, Buenos Aires, Argentina
Palabras clave:Cycas; Cycadales; Functional convergence; Gymnosperms; Leaf economic spectrum; Leaf hydraulic conductance; Photosynthetic capacity; Trade-off; concentration (composition); hydraulic conductivity; leaf morphology; nutrient dynamics; photosynthesis; physiology; vascular plant; Coniferophyta; Cycadales; Cycadopsida; Cycas; Filicophyta; Gymnospermae; Magnoliophyta; Spermatophyta; chlorophyll; nitrogen; phosphorus; anatomy and histology; angiosperm; comparative study; Cycadophyta; Cycas; evapotranspiration; gymnosperm; light; metabolism; phenotype; photosynthesis; physiology; plant leaf; Angiosperms; Chlorophyll; Cycadophyta; Cycas; Gymnosperms; Light; Nitrogen; Phenotype; Phosphorus; Photosynthesis; Plant Leaves; Plant Transpiration
Año:2015
Volumen:206
Número:2
Página de inicio:817
Página de fin:829
DOI: http://dx.doi.org/10.1111/nph.13274
Título revista:New Phytologist
Título revista abreviado:New Phytol.
ISSN:0028646X
CODEN:NEPHA
CAS:chlorophyll, 1406-65-1, 15611-43-5; nitrogen, 7727-37-9; phosphorus, 7723-14-0; Chlorophyll; Nitrogen; Phosphorus
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0028646X_v206_n2_p817_Zhang

Referencias:

  • Ares, A., Burner, D.M., Brauer, D.K., Soil phosphorus and water effects on growth, nutrient and carbohydrate concentrations, delta C13, and nodulation of mimosa (Albizia julibrissin Durz.) on a highly weathered soil (2009) Agroforestry Systems, 76, pp. 317-325
  • Berendse, F., Scheffer, M., The angiosperm radiation revisited, an ecological explanation for Darwin's 'abominable mystery' (2009) Ecology Letters, 12, pp. 865-872
  • Blonder, B., Violle, C., Bentley, L.P., Enquist, B.J., Venation networks and the origin of the leaf economics spectrum (2011) Ecology Letters, 14, pp. 91-100
  • Blonder, B., Violle, C., Bentley, L.P., Enquist, B.J., Inclusion of vein traits improves predictive power for the leaf economic spectrum: a response to Sack (2013) (2014) Journal of Experimental Botany, 65, pp. 5109-5114
  • Blonder, B., Violle, C., Enquist, B.J., Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides (2013) Journal of Ecology, 101, pp. 981-989
  • Bond, W.J., The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence (1989) Biological Journal of the Linnean Society, 36, pp. 227-249
  • Boyce, C.K., Brodribb, T.J., Feild, T.S., Zwieniecki, M.A., Angiosperm leaf vein evolution was physiologically and environmentally transformative (2009) Proceedings of the Royal Society B, 276, pp. 1771-1776
  • Brenner, E.D., Stevenson, D.W., Twigg, R.W., Cycads: evolutionary innovations and the role of plant-derived neurotoxins (2003) Trends in Plant Science, 8, pp. 446-452
  • Brodribb, T.J., Feild, T.S., Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification (2010) Ecology Letters, 13, pp. 175-183
  • Brodribb, T.J., Feild, T.S., Jordan, G.J., Leaf maximum photosynthetic rate and venation are linked by hydraulics (2007) Plant Physiology, 144, pp. 1890-1898
  • Campanello, P.I., Gatti, M.G., Goldstein, G., Coordination between water-transport efficiency and photosynthetic capacity in canopy tree species at different growth irradiances (2008) Tree Physiology, 28, pp. 85-94
  • Castelli, F., Contillo, R., Miceli, F., Non-destructive determination of leaf chlorophyll content in four crop species (1996) Journal of Agronomy and Crop Science, 177, pp. 275-283
  • Chaw, S.M., Walters, T.W., Chang, C.C., Hu, S.H., Chen, S.H., A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region (2005) Molecular Phylogenetics and Evolution, 37, pp. 214-234
  • Clark, D.B., Clark, D.A., Leaf production and the cost of reproduction in the neotropical rainforest cycad, Zamia skinneri (1988) Journal of Ecology, 76, pp. 1153-1163
  • Cramer, M.D., Hawkins, H.J., Verboom, G.A., The importance of nutritional regulation of plant water flux (2009) Oecologia, 161, pp. 15-24
  • Crane, P.R., Friis, E.M., Pedersen, K.R., The origin and early diversification of angiosperms (1995) Nature, 374, pp. 27-33
  • Fanizza, G., Gatta, C.D., Bagnulo, C., A non-destructive determination of leaf chlorophyll in Vitis vinifera (1991) The Annals of Applied Biology, 119, pp. 203-205
  • Feild, T.S., Brodribb, T.J., Iglesias, A., Chatelet, D.S., Baresch, A., Upchurch, G.R., Gomez, B., Kvacek, J., Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution (2011) Proceedings of the National Academy of Sciences, USA, 108, pp. 8363-8366
  • Feild, T.S., Upchurch, G.R., Chatelet, D.S., Brodribb, T.J., Grubbs, K.C., Samain, M.S., Wanke, S., Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves (2011) Paleobiology, 37, pp. 195-213
  • Field, C., Mooney, H.A., The photosynthesis-nitrogen relationship in wild plants (1986) On the economy of plant form and function, pp. 25-55. , In: Givnish T, ed. . London, UK: Cambridge University Press
  • Gao, Z., Thomas, B.A., A review of fossil cycad megasporophylls, with new evidence of crossozamia pomel and its associated leaves from the Lower Permian of Taiyuan, China (1989) Review of Palaeobotany and Palynology, 60, pp. 205-223
  • Gratani, L., A nondestructive method to determine chlorophyll content of leaves (1992) Photosynthetica, 26, pp. 469-473
  • Haworth, M., Fitzgerald, A., McElwain, J.C., Cycads show no stomatal-density and index response to elevated carbon dioxide and subambient oxygen (2011) Australian Journal of Botany, 59, pp. 629-638
  • Hikosaka, K., Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance (2004) Journal of Plant Research, 117, pp. 481-494
  • Hou, X.Y., (1982) Chinese vegetable geography and chemical elements: analyses of the dominant plant species, , Beijing, China: Science Press
  • Hu, Y.-S., Yao, B.-J., Transfusion tissue in gymnosperm leaves (1981) Botanical Journal of the Linnean Society, 83, pp. 263-272
  • Huang, Y.-Y., Zhang, H.-D., The brief report on first discovery of vessel in cycads (1999) Journal of Agricultural and Biological Science, 18, pp. 99-100
  • Karst, A.L., Lechowicz, M.J., Are correlations among foliar traits in ferns consistent with those in the seed plants? (2007) New Phytologist, 173, pp. 306-312
  • Kuppers, M., Carbon relations and competition between woody species in a central European hedgerow. 2. Stomatal responses, water-use, and hydraulic conductivity in the root leaf pathway (1984) Oecologia, 64, pp. 344-354
  • Lloyd, J., Bloomfield, K., Domingues, T.F., Farquhar, G.D., Photosynthetically relevant foliar traits correlating better on a mass vs an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand? (2013) New Phytologist, 199, pp. 311-321
  • Mamay, S.H., Cycads: fossil evidence of late Paleozoic origin (1969) Science, 164, pp. 295-296
  • Manetas, Y., Grammatikopoulos, G., Kyparissis, A., The use of the portable, non-destructive, SPAD-502 (Minolta) chlorophyll meter with leaves of varying trichome density and anthocyanin content (1998) Journal of Plant Physiology, 153, pp. 513-516
  • Marenco, R.A., Antezana-Vera, S.A., Nascimento, H.C.S., Relationship between specific leaf area, leaf thickness, leaf water content and SPAD-502 readings in six Amazonian tree species (2009) Photosynthetica, 47, pp. 184-190
  • Markwell, J., Osterman, J.C., Mitchell, J.L., Calibration of the Minolta SPAD-502 leaf chlorophyll meter (1995) Photosynthesis Research, 46, pp. 467-472
  • Marquard, R., Tipton, J., Relationship between extractable chlorophyll and an in situ method to estimate leaf greenness (1987) HortScience, 22, p. 1327
  • Meinzer, F.C., Functional convergence in plant responses to the environment (2003) Oecologia, 134, pp. 1-11
  • Meinzer, F.C., Grantz, D.A., Stomatal and hydraulic conductance in growing sugarcane - stomatal adjustment to water transport capacity (1990) Plant, Cell & Environment, 13, pp. 383-388
  • Melcher, P.J., Michele Holbrook, N., Burns, M.J., Zwieniecki, M.A., Cobb, A.R., Brodribb, T.J., Choat, B., Sack, L., Measurements of stem xylem hydraulic conductivity in the laboratory and field (2012) Methods in Ecology and Evolution, 3, pp. 685-694
  • Mencuccini, M., The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms (2003) Plant, Cell & Environment, 26, pp. 163-182
  • Monson, R.K., The use of phylogenetic perspective in comparative plant physiology and development biology (1996) Annals of the Missouri Botanical Garden, 83, pp. 3-16
  • Nagalingum, N.S., Marshall, C.R., Quental, T.B., Rai, H.S., Little, D.P., Mathews, S., Recent synchronous radiation of a living fossil (2011) Science, 334, pp. 796-799
  • Niinemets, U., Sack, L., Structural determinants of leaf light-harvesting capacity and photosynthetic potentials (2006) Progress in botany, pp. 385-419. , In: Esser K, Lüttge U, Beyschlag W, Murata J, eds. . Berlin/Heidelberg, Germany: Springer
  • Norstog, K., Nicholls, T.J., (1997) The biology of the cycads, , Ithaca, NY, USA: Comstock Publishing Associates/ Cornell University Press
  • Osnas, J.L.D., Lichstein, J.W., Reich, P.B., Pacala, S.W., Global leaf trait relationships: mass, area, and the leaf economics spectrum (2013) Science, 340, pp. 741-744
  • Parkhurst, D.F., Diffusion of CO2 and other gases inside leaves (1994) New Phytologist, 126, pp. 449-479
  • Pearson, K., On lines and planes of closest fit to systems of points in space (1901) Philosophical Magazine, 2, pp. 559-572
  • Prado, A., Sierra, A., Windsor, D., Bede, J.C., Leaf traits and herbivory levels in a tropical gymnosperm, Zamia stevensonii (Zamiaceae) (2014) American Journal of Botany, 101, pp. 437-447
  • Randall, P.J., Bouma, D., Zinc deficiency, carbonic-anhydrase, and photosynthesis in leaves of spinach (1973) Plant Physiology, 52, pp. 229-232
  • Reich, P.B., Ellsworth, D.S., Walters, M.B., Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups (1998) Functional Ecology, 12, pp. 948-958
  • Reich, P.B., Walters, M.B., Ellsworth, D.S., From tropics to tundra: global convergence in plant functioning (1997) Proceedings of the National Academy of Sciences, USA, 94, pp. 13730-13734
  • Roderick, M.L., Berry, S.L., Noble, I.R., Farquhar, G.D., A theoretical approach to linking the composition and morphology with the function of leaves (1999) Functional Ecology, 13, pp. 683-695
  • Roderick, M.L., Berry, S.L., Saunders, A.R., Noble, I.R., On the relationship between the composition, morphology and function of leaves (1999) Functional Ecology, 13, pp. 696-710
  • Sack, L., Frole, K., Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees (2006) Ecology, 87, pp. 483-491
  • Sack, L., Melcher, P.J., Zwieniecki, M.A., Holbrook, N.M., The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods (2002) Journal of Experimental Botany, 53, pp. 2177-2184
  • Sack, L., Scoffoni, C., Measurement of leaf hydraulic conductance and stomatal conductance and their responses to irradiance and dehydration using the evaporative flux method (EFM) (2012) Journal of Visualized Experiments: JoVE, 70, p. e4179
  • Sack, L., Scoffoni, C., Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future (2013) New Phytologist, 198, pp. 983-1000
  • Sack, L., Scoffoni, C., John, G.P., Poorter, H., Mason, C.M., Mendez-Alonzo, R., Donovan, L.A., How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis (2013) Journal of Experimental Botany, 64, pp. 4053-4080
  • Sack, L., Scoffoni, C., John, G.P., Poorter, H., Mason, C.M., Mendez-Alonzo, R., Donovan, L.A., Leaf mass per area is independent of vein length per area: avoiding pitfalls when modelling phenotypic integration (reply to Blonder 2014) (2014) Journal of Experimental Botany, 65, pp. 5115-5123
  • Sack, L., Tyree, M.T., Holbrook, N.M., Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees (2005) New Phytologist, 167, pp. 403-413
  • Sage, R.F., Pearcy, R.W., Seemann, J.R., The nitrogen use efficiency of C3 and C4 plants III. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.) (1987) Plant Physiology, 85, pp. 355-359
  • Santiago, L.S., Goldstein, G., Meinzer, F.C., Fisher, J.B., Machado, K., Woodruff, D., Jones, T., Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees (2004) Oecologia, 140, pp. 543-550
  • Shipley, B., Lechowicz, M.J., Wright, I., Reich, P.B., Fundamental trade-offs generating the worldwide leaf economics spectrum (2006) Ecology, 87, pp. 535-541
  • Simonin, K.A., Limm, E.B., Dawson, T.E., Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain (2012) New Phytologist, 193, pp. 939-947
  • Singha, A., Townsend, E., Relationship between chromaticity values and chlorophyll concentration in apple, grape, and peach leaves (1989) HortScience, 24, p. 1034
  • Sober, A., Hydraulic conductance, stomatal conductance, and maximal photosynthetic rate in bean leaves (1997) Photosynthetica, 34, pp. 599-603
  • Spiller, S., Terry, N., Limiting factors in photosynthesis: II. iron stress diminishes photochemical capacity by reducing the number of photosynthetic units (1980) Plant Physiology, 65, pp. 121-125
  • Stevenson, D.W., Norstog, K.J., Molsen, D.V., Midribs of cycad pinnae (1996) Brittonia, 48, pp. 67-74
  • Uddling, J., Gelang-Alfredsson, J., Piikki, K., Pleijel, H., Evaluating the relationship between leaf chlorophyll concentration and SPAD-502 chlorophyll meter readings (2007) Photosynthesis Research, 91, pp. 37-46
  • Vovides, A.P., Etherington, J.R., Dresser, P.Q., Groenhof, A., Iglesias, C., Ramirez, J.F., CAM-cycling in the cycad Dioon edule Lindl. in its natural tropical deciduous forest habitat in central Veracruz, Mexico (2002) Botanical Journal of the Linnean Society, 138, pp. 155-162
  • Waite, M., Sack, L., How does moss photosynthesis relate to leaf and canopy structure? Trait relationships for 10 Hawaiian species of contrasting light habitats (2010) New Phytologist, 185, pp. 156-172
  • Warton, D.I., Wright, I.J., Falster, D.S., Westoby, M., Bivariate line-fitting methods for allometry (2006) Biological Reviews of the Cambridge Philosophical Society, 81, pp. 259-291
  • Westoby, M., Reich, P.B., Wright, I.J., Understanding ecological variation across species: area-based vs mass-based expression of leaf traits (2013) New Phytologist, 199, pp. 322-323
  • Whitelock, L.M., (2002) The Cycads, , Portland, OR, USA: Timber Press
  • Witkowski, E.T.F., Lamont, B.B., Leaf specific mass confounds leaf density and thickness (1991) Oecologia, 88, pp. 486-493
  • Wright, I.J., Reich, P.B., Westoby, M., Least-cost input mixtures of water and nitrogen for photosynthesis (2003) The American Naturalist, 161, pp. 98-111
  • Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., Cavender-Bares, J., Diemer, M., The worldwide leaf economics spectrum (2004) Nature, 428, pp. 821-827
  • Zgurski, J.M., Rai, H.S., Fai, Q.M., Bogler, D.J., Francisco-Ortega, J., Graham, S.W., How well do we understand the overall backbone of cycad phylogeny? New insights from a large, multigene plastid data set (2008) Molecular Phylogenetics and Evolution, 47, pp. 1232-1237
  • Zhang, J.L., Cao, K.F., Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species (2009) Functional Ecology, 23, pp. 658-667

Citas:

---------- APA ----------
Zhang, Y.-J., Cao, K.-F., Sack, L., Li, N., Wei, X.-M. & Goldstein, G. (2015) . Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytologist, 206(2), 817-829.
http://dx.doi.org/10.1111/nph.13274
---------- CHICAGO ----------
Zhang, Y.-J., Cao, K.-F., Sack, L., Li, N., Wei, X.-M., Goldstein, G. "Extending the generality of leaf economic design principles in the cycads, an ancient lineage" . New Phytologist 206, no. 2 (2015) : 817-829.
http://dx.doi.org/10.1111/nph.13274
---------- MLA ----------
Zhang, Y.-J., Cao, K.-F., Sack, L., Li, N., Wei, X.-M., Goldstein, G. "Extending the generality of leaf economic design principles in the cycads, an ancient lineage" . New Phytologist, vol. 206, no. 2, 2015, pp. 817-829.
http://dx.doi.org/10.1111/nph.13274
---------- VANCOUVER ----------
Zhang, Y.-J., Cao, K.-F., Sack, L., Li, N., Wei, X.-M., Goldstein, G. Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytol. 2015;206(2):817-829.
http://dx.doi.org/10.1111/nph.13274