Cycads show no stomatal-density and index response to elevated carbon dioxide and subambient oxygen

Australian Journal of Botany

Volumn 59, Issue 7, 2011, Pages 629-638

  Haworth, Matthew ^a   Fitzgerald, Annmarie ^b   McElwain, Jennifer C ^b  

^a CNR   (Italy)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; FOSSIL RECORD; MESOZOIC; OXYGEN; PALEOATMOSPHERE; PALEOBOTANY; PALEOENVIRONMENT; PHOTOSYNTHESIS; PROXY CLIMATE RECORD; RECONSTRUCTION; STOMATA;

CYCADOPHYTA; CYCADOPSIDA; CYCAS; CYCAS REVOLUTA; DIOON MEROLAE; LEPIDOZAMIA HOPEI; LEPIDOZAMIA PEROFFSKYANA; MACROZAMIA; MACROZAMIA MIQUELII; ZAMIA; ZAMIA INTEGRIFOLIA;

EID: 82055184160     PISSN: 00671924     EISSN: None     Source Type: Journal    
DOI: 10.1071/BT11009     Document Type: Article

References (89)

1. Ainsworth EA, Rogers A, Nelson R, LongSP (2004) Testing the 'source-sink' hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agricultural and Forest Meteorology 122, 85-94. doi:10.1016/j.agrformet.2003.09.002 (Pubitemid 38362134)
2. Archangelsky S, de Seoane LV (2004) Cycadean diversity in the Cretaceous of Patagonia, Argentina. Three new Androstrobus species from the Baquero Group. Review of Palaeobotany and Palynology 131, 1-28. doi:10.1016/j.revpalbo.2004.01. 008 (Pubitemid 38871573)
3. Bacon KL, Belcher CM, Hesselbo SP, McElwain JC (2011) The Triassic-Jurassic boundary carbon-isotope excursions expressed in taxonomically identified leaf cuticles. Palaios 26, 461-469. doi:10.2110/palo.2010.p10-120r
4. Beerling DJ, Chaloner WG (1993) Evolutionary responses of stomatal density to global CO2 change. Biological Journal of the Linnean Society. Linnean Society of London 48, 343-353.
5. Beerling DJ, Franks PJ (2010) The hidden cost of transpiration. Nature 464, 495-496. doi:10.1038/464495a
6. Beerling DJ, Kelly CK (1997) Stomatal density responses of temperate woodland pants over the past seven decades of CO2 increase: A comparison of Salisbury (1927) with contemporary data. American Journal of Botany 84, 1572-1583. doi:10.2307/2446619 (Pubitemid 27513939)
7. Beerling DJ, Woodward FI (1996) Palaeo-ecophysiological perspectives on plant responses to global change. Trends in Ecology & Evolution 11, 20-23. doi:10.1016/0169-5347(96)81060-3 (Pubitemid 3017998)
8. Beerling DJ, Woodward FI (1997) Changes in land plant function over the Phanerozoic: Reconstructions based onthe fossil record. Botanical Journal of the Linnean Society 124, 137-153. (Pubitemid 27288637)
9. Beerling DJ, McElwain JC, Osborne CP (1998a) Stomatal responses of the 'living fossil' Ginkgo biloba L. to changes in atmospheric CO2 concentrations. Journal of Experimental Botany 49, 1603-1607. doi:10.1093/jexbot/49.326.1603 (Pubitemid 28395546)
10. Beerling DJ, Woodward FI, Lomas MR, Wills MA, Quick WP, Valdes PJ (1998b) The influence of carboniferous palaeoatmospheres on plant function: An experimental and modelling assessment. Philosophical Transactions of the Royal Society B-Biological Sciences 353, 131-140. doi:10.1098/rstb.1998.0196 (Pubitemid 28094396)
11. Belcher CM, Mander L, Rein G, Jervis FX, Haworth M, Hesselbo SP, Glasspool IJ, McElwain JC (2010) Increased fire activity at the Triassic/Jurassic boundary in Greenland due to climate-driven floral change. Nature Geoscience 3, 426-429. doi:10.1038/ngeo871
12. Berner RA (2006) GEOCARBSULF: A combined model for Phanerozoic atmospheric O2 and CO2. Geochimica et Cosmochimica Acta 70, 5653-5664. doi:10.1016/j.gca.2005.11.032 (Pubitemid 44712462)
13. Berner RA (2009) Phanerozoic atmospheric oxygen: New results using the Geocarbsulf Model. American Journal of Science 309, 603-606. doi:10.2475/07.2009.03
14. Bonis NR, Van Konijnenburg-Van Cittert JHA, Kürschner WM (2010) Changing CO2 conditions during the end-Triassic inferred from stomatal frequency analysis on Lepidopteris ottonis (Goeppert) Schimper and Ginkgoites taeniatus (Braun) Harris. Palaeogeography, Palaeoclimatology, Palaeoecology 295, 146-161. doi:10.1016/j.palaeo.2010.05.034
15. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings. Biological Sciences 276, 1771-1776. doi:10.1098/rspb.2008.1919
16. Brodribb TJ, Jordan GJ (2008) Internal coordination between hydraulics and stomatal control in leaves. Plant, Cell & Environment 31, 1557-1564. doi:10.1111/j.1365-3040.2008.01865.x
17. Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331, 582-585. doi:10.1126/science.1197985
18. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890-1898. doi:10.1104/pp.107.101352 (Pubitemid 47258112)
19. Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytologist 183, 839-847. doi:10.1111/j.1469-8137.2009.02844.x
20. ChenLQ,Li CS, ChalonerWG,Beerling DJ, SunQG,CollinsonME,Mitchell PL (2001) Assessing the potential for the stomatal characters of extant and fossil ginkgo leaves to signal atmosphericCO2 change. American Journal of Botany 88, 1309-1315. doi:10.2307/3558342 (Pubitemid 33645039)
21. Cowan I (1977) Stomatal behaviour and environment. Advances in Botanical Research 4, 117-219.
22. Delevoryas T (1982) Perspectives on the origin of cycads and cycadeoids. Review of Palaeobotany and Palynology 37, 115-132. doi:10.1016/0034-6667(82) 90040-9
23. Doi M, Shimazaki K-i (2008) The stomata of the fern Adiantum capillusveneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiology 147, 922-930. doi:10.1104/pp.108.118950 (Pubitemid 352844329)
24. Falkowski PG, Katz ME, Milligan AJ, Fennel K, Cramer BS, Aubry MP, Berner RA, Novacek MJ, ZapolWM(2005) The rise of oxygen over the past 205 million years and the evolution of large placental mammals. Science 309, 2202-2204. doi:10.1126/science.1116047 (Pubitemid 41396066)
25. Farquhar GD, Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78-90. doi:10.1007/BF00386231
26. 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, USA 106, 10343-10347. doi:10.1073/pnas.0904209106
27. Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: An analysis using Eucalyptus globulus. Plant, Cell & Environment 32, 1737-1748. doi:10.1111/j.1365-3040.2009.002031.x
28. Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, HeteringtonAM(2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature 408, 302-305. doi:10.1038/35042663
29. Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457-461. doi:10.1007/s004420100628 (Pubitemid 32442682)
30. Hammer PA, Hopper DA (1997) Experimental design. In 'Plant growth chamber handbook'. (Eds RW Langhans, TW Tibbitts) pp. 177-187. (Iowa State University: Ames, IA)
31. Harris TM (1961) The fossil cycads. Palaeontology 4, 313-323.
32. HarrisTM(1964) 'The Yorkshire Jurassic flora II. Caytoniales, cycadales and pteridosperms.' (British Museum of Natural History: London)
33. Haworth M, Hesselbo SP, McElwain JC, Robinson SA, Brunt JW (2005) Mid-Cretaceous pCO2 based on stomata of the extinct conifer Pseudofrenelopsis (Cheirolepidiaceae). Geology 33, 749-752. doi:10.1130/G21736.1 (Pubitemid 41269228)
34. Haworth M, Elliott-Kingston C, McElwain J (2011a) The stomatal CO2 proxy does not saturate at high atmosphericCO2 concentrations: Evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167, 11-19. doi:10.1007/s00442-011-1969-1
35. Haworth M, Elliott-Kingston C, McElwain JC (2011b) Stomatal control as a driver of plant evolution. Journal of Experimental Botany 62, 2419-2423. doi:10.1093/jxb/err086
36. Haworth M, Gallagher A, Elliott-Kingston C, Raschi A, Marandola D, McElwain JC (2010a) Stomatal index responses of Agrostis canina to carbon dioxide and sulphur dioxide: Implications for palaeo-[CO2] using the stomatal proxy. New Phytologist 188, 845-855. doi:10.1111/j.1469-8137.2010.03403.x
37. Haworth M, Heath J, McElwain JC (2010b) Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers. Annals of Botany 105, 411-418. doi:10.1093/aob/mcp309
38. Heath OVS (1949) Studies in stomatal behaviour. V. The role of carbon dioxide in the light response of stomata. Journal of Experimental Botany 1, 29-62. doi:10.1093/jxb/1.1.29
39. Hesselbo SP, Grocke DR, Jenkyns HC, Bjerrum CJ, Farrimond P, Bell HSM, Green OR (2000) Massive dissociation of gas hydrate during a Jurassic oceanic anoxic event. Nature 406, 392-395. doi:10.1038/35019044 (Pubitemid 30625555)
40. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901-908. doi:10.1038/nature01843 (Pubitemid 37051674)
41. Hovenden MJ, Brodribb T (2000) Altitude of origin influences stomatal conductance and therefore maximum assimilation rate in southern beech, Nothofagus cunninghamii. Australian Journal of Plant Physiology 27, 451-456. (Pubitemid 30351627)
42. Hovenden MJ, Vander Schoor JK (2004) Nature vs nurture in the leaf morphology of southern beech, Nothofagus cunninghamii (Nothofagaceae). New Phytologist 161, 585-594. doi:10.1046/j.1469-8137.2003.00931.x (Pubitemid 38126970)
43. Hu H, Boisson-Dernier A, Israelsson-Nordstrom M, Bohmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI (2010) Carbonic anhydrases are upstream regulators of CO2 controlled stomatal movements in guard cells. Nature Cell Biology 12, 87-93. doi:10.1038/ncb2009
44. Jenkyns HC (2003) Evidence for rapid climate change in the Mesozoic-Palaeogene greenhouse world. Philosophical Transactions of the Royal Society of London Series A - Mathematical Physical and Engineering Sciences 361, 1885-1916. doi:10.1098/rsta.2003.1240 (Pubitemid 37256172)
45. Jones DL (2002) 'Cycads of the world: Ancient plants in today's landscape.' (Smithsonian Books: Washington, DC)
46. Jones HG (1999) Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces. Plant, Cell & Environment 22, 1043-1055. doi:10.1046/j.1365-3040.1999.00468.x (Pubitemid 29411950)
47. Kaiser H (2009) The relation between stomatal aperture and gas exchange under consideration of pore geometry and diffusional resistance in the mesophyll. Plant, Cell & Environment 32, 1091-1098. doi:10.1111/j.1365-3040. 2009.01990.x
48. KochGW,Sillett SC, JenningsGM,DavisSD(2004) The limits to tree height. Nature 428, 851-854. doi:10.1038/nature02417 (Pubitemid 38529498)
49. Körner C, Scheel JA, Bauer H (1979) Maximum leaf diffusive conductance in vascular plants. Photosynthetica 13, 45-82.
50. Kouwenberg LLR, McElwain JC, Kurschner WM, Wagner F, Beerling DJ, Mayle FE, Visscher H (2003) Stomatal frequency adjustment of four conifer species to historical changes in atmospheric CO2. American Journal of Botany 90, 610-619. doi:10.3732/ajb.90.4.610 (Pubitemid 38161879)
51. Kouwenberg L, Wagner R, Kürschner W, Visscher H (2005) Atmospheric CO2 fluctuations during the last millennium reconstructed by stomatal frequency analysis of Tsuga heterophylla needles. Geology 33, 33-36. doi:10.1130/G20941.1 (Pubitemid 40171614)
52. KürschnerWM(1997) The anatomical diversity of recent and fossil leaves of the durmast oak (Quercus petraea Lieblein/Q. pseudocastanea Goeppert) - implications for their use as biosensors of palaeoatmosphericCO2 levels. Review of Palaeobotany and Palynology 96, 1-30. doi:10.1016/S0034-6667(96)00051- 6 (Pubitemid 27356316)
53. Kürschner WM, Wagner F, Visscher EH, Visscher H (1997) Predicting the response of leaf stomatal frequency to a future CO2-enriched atmosphere: Constraints from historical observations. Geologische Rundschau 86, 512-517. doi:10.1007/s005310050158
54. Kürschner WM, Kvacek Z, Dilcher DL (2008) The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proceedings of the National Academy of Sciences, USA 105, 449-453. doi:10.1073/pnas.0708588105 (Pubitemid 351171728)
55. Lake JA, Woodward FI (2008) Response of stomatal numbers to CO2 and humidity: Control by transpiration rate and abscisic acid. New Phytologist 179, 397-404. doi:10.1111/j.1469-8137.2008.02485.x (Pubitemid 351991428)
56. Llorens L, Osborne CP, Beerling DJ (2009) Water-use responses of 'living fossil' conifers to CO2 enrichment in a simulated Cretaceous polar environment. Annals of Botany 104, 179-188. doi:10.1093/aob/mcp108
57. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54, 2393-2401. doi:10.1093/jxb/erg262 (Pubitemid 37379253)
58. Mansfield TA, Meidner H (1966) Stomatal opening in light of different wavelengths: Effects of blue light independent of carbon dioxide concentration. Journal of Experimental Botany 17, 510-521. doi:10.1093/jxb/17.3.510
59. Marler TE, Willis LE (1997) Leaf gas-exchange characteristics of sixteen cycad species. Journal of the American Society for Horticultural Science 122, 38-42. (Pubitemid 27134298)
60. Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866-870. doi:10.1038/nature03835 (Pubitemid 41160647)
61. McElwain JC (1998) Do fossil plants signal palaeoatmospheric CO2 concentration in the geological past? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 83-96. doi:10.1098/rstb.1998.0193 (Pubitemid 28094393)
62. McElwain JC, Beerling DJ, Woodward FI (1999) Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285, 1386-1390. doi:10.1126/science.285.5432.1386 (Pubitemid 29411667)
63. Meidner H (1968) The comparative effects of blue and red light on the stomata of Allium cepa L. and Xanthium pennsylvanicum. Journal of Experimental Botany 19, 146-151. doi:10.1093/jxb/19.1.146
64. Miller-Rushing AJ, Primack RB, Templer PH, Rathbone S, Mukunda S (2009) Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees. American Journal of Botany 96, 1779-1786. doi:10.3732/ajb.0800410
65. MiyazawaSI, Livingston NJ, TurpinDH(2006) Stomatal development innew leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa P. deltoides). Journal of Experimental Botany 57, 373-380. doi:10.1093/jxb/eri278 (Pubitemid 43063789)
66. Miziorko HM, Llorimer GH (1983) Ribulose-1,5-bisphosphate carboxylaseoxygenase. Annual Review of Biochemistry 52, 507-535. doi:10.1146/annurev.bi.52.070183.002451
67. Mott KA, Woodrow IE (2000) Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. Journal of Experimental Botany 51, 399-406. doi:10.1093/jexbot/51.suppl1.399 (Pubitemid 30104767)
68. Muchow RC, Sinclair TR (1989) Epidermal conductance, stomatal density and stomatal size among genotypes of Sorghum bicolor (L) Moench. Plant, Cell & Environment 12, 425-431. doi:10.1111/j.1365-3040.1989.tb01958.x
69. Oliveras I, Martinez-Vilata J, Jimenez-Ortiz T, Lledó MJ, Escarre A, Pinol J (2003) Hydraulic properties of Pinus halepensis, Pinus pinea and Tetraclinis articulata in a dune ecosystem of eastern Spain. Plant Ecology 169, 131-141. doi:10.1023/A:1026223516580 (Pubitemid 37365414)
70. Passalia MG (2009) Cretaceous pCO2 estimation from stomatal frequency analysis of gymnosperm leaves of Patagonia, Argentina. Palaeogeography, Palaeoclimatology, Palaeoecology 273, 17-24. doi:10.1016/j.palaeo.2008.11.010
71. Passalia MG, Del Fueyo G, Archangelsky S (2010) An Early Cretaceous zamiaceous cycad of south west Gondwana: Restrepophyllum nov gen. from Patagonia, Argentina. Review of Palaeobotany and Palynology 161, 137-150. doi:10.1016/j.revpalbo.2010.04.001
72. Poole I, Kürschner WM (1999) Stomatal density and Index: The practise. In 'Fossil plants and spores: Modern techniques'. (Eds TP Jones, NP Rowe) pp. 257-260. (Geological Society: London)
73. Pott C, Kerp H, Krings M (2007) Morphology and epidermal anatomy of Nilssonia (cycadalean foliage) from the Upper Triassic of Lunz (Lower Austria). Review of Palaeobotany and Palynology 143, 197-217. doi:10.1016/j.revpalbo.2006. 07.007 (Pubitemid 46240094)
74. Radoglou KM, Jarvis PG (1990) Effects of CO2 enrichment on 4 poplar clones. 2. Leaf surface-properties. Annals of Botany 65, 627-632.
75. Robinson JM (1994) Speculations on carbon dioxide starvation, late tertiary evolution of stomatal regulation and floristic modernization. Plant, Cell & Environment 17, 345-354. doi:10.1111/j.1365-3040.1994.tb00303.x (Pubitemid 2060830)
76. Rogiers SY, Hardie WJ, Smith JP (2011) Stomatal density of grapevine leaves (Vitis vinifera L.) responds to soil temperature and atmospheric carbon dioxide. Australian Journal of Grape and Wine Research 17, 147-152. doi:10.1111/j.1755-0238.2011.00124.x
77. Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47, 235-242. doi:10.2307/1313077
78. Sager JC, McFarlane JC (1997) Radiation. In 'Plant growth chamber handbook'. (Eds RW Langhans, TW Tibbitts) pp. 1-30. (Iowa State University: Ames, IA)
79. Smith RY, Greenwood DR, Basinger JF (2010) Estimating paleoatmospheric pCO2 during the Early Eocene climatic optimum from stomatal frequency of Ginkgo, Okanagan Highlands, British Columbia, Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 293, 120-131. doi:10.1016/j.palaeo.2010.05.006
80. Stults DZ, Wagner-Cremer F, Axsmith BJ (2011) Atmospheric palaeo-CO2 estimates based on Taxodium distichum (Cupressaceae) fossils from the Miocene and Pliocene of eastern North America. Palaeogeography, Palaeoclimatology, Palaeoecology 309, 327-332. doi:10.1016/j.palaeo.2011.06.017
81. Van Oosten JJ, Wilkins D, BesfordRT (1994) Regulation of the expression of photosynthetic nuclear genes by CO2 is mimicked by regulation by carbohydrates - a mechanism for the acclimation of photosynthesis to high CO2. Plant, Cell & Environment 17, 913-923. doi:10.1111/j.1365-3040.1994.tb00320. x (Pubitemid 2121521)
82. Van Vuuren MMI, Robinson D, Fitter AH, Chasalow SD, Williamson L, Raven JA (1997) Effects of elevated atmospheric CO2 and soil water availability on root biomass, root length, and N, P andK uptake by wheat. New Phytologist 135, 455-465. doi:10.1046/j.1469-8137.1997.00682.x (Pubitemid 28016886)
83. Wagner F, Below R, DeKlerk P, Dilcher DL, Joosten H, Kurschner WM, Visscher H (1996) A natural experiment on plant acclimation: Lifetime stomatal frequency response of an individual tree to annual atmospheric CO2 increase. Proceedings of the National Academy of Sciences, USA 93, 11 705-11 708. doi:10.1073/pnas.93.21.11705 (Pubitemid 26347186)
84. Wagner F, Bohncke SJP, Dilcher DL, Kurschner WM, Geel Bv, Visscher H (1999) Century-scale shifts in early Holocene atmospheric CO2 concentration. Science 284, 1971-1973. doi:10.1126/science.284.5422.1971 (Pubitemid 29309440)
85. Wagner F, Visscher H, Kurschner WM, Dilcher DL (2007) Influence of ontogeny and atmospheric CO2 on stomata parameters of Osmunda regalis. Advances in Angiosperm Paleobotany and Paleoclimatic Reconstruction 258, 183-189. (Pubitemid 350284106)
86. Whitelock LM (2002) 'The cycads.' (Timber Press: Portland, OR) Woodward FI (1987) Stomatal numbers are sensitive to increases inCO2 from preindustrial levels. Nature 327, 617-618. doi:10.1038/327617a0
87. Woodward FI, Bazzaz FA (1988) The responses of stomatal density to CO2 partial pressure. Journal of Experimental Botany 39, 1771-1781. doi:10.1093/jxb/39.12.1771
88. Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytologist 131, 311-327. doi:10.1111/j.1469-8137.1995. tb03067.x
89. Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany 59, 3317-3325. doi:10.1093/jxb/ern185