Extremely thick cell walls and low mesophyll conductance: Welcome to the world of ancient living!

Journal of Experimental Botany

Volumn 68, Issue 7, 2017, Pages 1639-1653

  Veromann Jürgenson, Linda Liisa ^a   Tosens, Tiina ^a   Laanisto, Lauri ^a   Niinemets, Ülo ^a,b  

^a ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^b ESTONIAN ACADEMY OF SCIENCES   (Estonia)

Author keywords

Conifer; Gm; Gymnosperm; LES; LMA; Nitrogen; Photosynthesis

Indexed keywords

CARBON DIOXIDE;

CELL WALL; CYCADOPHYTA; CYTOLOGY; MESOPHYLL CELL; METABOLISM; PHOTOSYNTHESIS; PLANT LEAF; SELAGINELLACEAE; ULTRASTRUCTURE;

CARBON DIOXIDE; CELL WALL; CYCADOPSIDA; MESOPHYLL CELLS; PHOTOSYNTHESIS; PLANT LEAVES; SELAGINELLACEAE;

EID: 85020174965     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erx045     Document Type: Article

References (81)

1. Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP. 2001. Improved temperature response functions for models of Rubiscolimited photosynthesis. Plant, Cell and Environment 24, 253-259.
2. Biffin E, Brodribb TJ, Hill RS, Thomas P, Lowe AJ. 2012. Leaf evolution in Southern Hemisphere conifers tracks the angiosperm ecological radiation. Proceedings of the Royal Society B. Biological Sciences 279, 341-348.
3. Black K, Davis P, McGrath J, Doherty P, Osborne B. 2005. Interactive effects of irradiance and water availability on the photosynthetic performance of Picea sitchensis seedlings: implications for seedling establishment under different management practices. Annals of Forest Science 62, 413-422.
4. Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B. 2005. Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. The New Phytologist 165, 839-846.
5. 2 and optimization of water-use efficiency among land plants. The New Phytologist 183, 839-847.
6. Carnicer J, Barbeta A, Sperlich D, Coll M, Peñuelas J. 2013. Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale. Frontiers in Plant Science 4, 409.
7. Carriquí M, Cabrera HM, Conesa MÀ, et al. 2015. Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study. Plant, Cell and Environment 38, 448-460.
8. Cheng Y, Nicolson RG, Tripp K, Chaw SM. 2000. Phylogeny of Taxaceae and Cephalotaxaceae genera inferred from chloroplast matK gene and nuclear rDNA ITS region. Molecular Phylogenetics and Evolution 14, 353-365.
9. De Lucia EH, Whitehead D, Clearwater MJ. 2003. The relative limitation of photosynthesis by mesophyll conductance in co-occurring species in a temperate rainforest dominated by the conifer Dacrydium cupressinum. Functional Plant Biology 30, 1197-1204.
10. Equiza MA, Day ME, Jagels R. 2006. Physiological responses of three deciduous conifers (Metasequoia glyptostroboides, Taxodium distichum and Larix laricina) to continuous light: adaptive implications for the early Tertiary polar summer. Tree Physiology 26, 353-364.
11. 2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell and Environment 27, 137-153.
12. 2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235-2248.
13. 2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Plant Environmental Biology 21, 475-495.
14. Fini A, Loreto F, Tattini M, Giordano C, Ferrini F, Brunetti C, Centritto M. 2016. Mesophyll conductance plays a central role in leaf functioning of Oleaceae species exposed to contrasting sunlight irradiance. Physiologia Plantarum 157, 54-68.
15. 2: an unappreciated central player in photosynthesis. Plant Science 193-194, 70-84.
16. Flexas J, Díaz-Espejo A, Berry JA, Cifre J, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbó M. 2007a. Analysis of leakage in IRGA's leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. Journal of Experimental Botany 58, 1533-1543.
17. 2 concentration around leaves. Plant, Cell and Environment 30, 1284-1298.
18. 2 as a target for increasing photosynthesis and photosynthetic wateruse efficiency. Photosynthesis Research 117, 45-59.
19. 2: current knowledge and future prospects. Plant, Cell and Environment 31, 602-621.
20. Franks PJ. 2006. Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients. Plant, Cell and Environment 29, 584-592.
21. Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ. 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell and Environment 28, 571-579.
22. Genty B, Briantais J-M, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
23. 2 diffusion and C18OO discrimination in C3 leaves. Plant Physiology 123, 201-214.
24. Grassi G, Magnani F. 2005. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant, Cell and Environment 28, 834-849.
25. 2 transfer conductance and photosynthesis in tree species having different types of shoot phenology. Australian Journal of Plant Physiology 28, 1075-1084.
26. 2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Functional Ecology 13, 632-639.
27. 2. Plant Physiology 98, 1429-1436.
28. 2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60, 2303-2314.
29. Hemsley AR, Poole I. 2004. The evolution of plant physiology. London: Academic Press.
30. Hollingsworth PM, Forrest LL, Spouge JL, et al. 2009. A DNA barcode for land plants. Proceedings of the National Academy of Sciences of the United States of America 106, 12794-12797.
31. James JC, Grace J, Hoad SP. 1994. Growth and photosynthesis of Pinus sylvestris at its altitudinal limit in Scotland. Journal of Ecology 82, 297-306.
32. Knapp M, Mudaliar R, Havell D, Wagstaff SJ, Lockhart PJ. 2007. The drowning of New Zealand and the problem of Agathis. Systematic Biology 56, 862-870.
33. Lang D, Weiche B, Timmerhaus G, Richardt S, Riaño-Pachón DM, Corrêa LG, Reski R, Mueller-Roeber B, Rensing SA. 2010. Genomewide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biology and Evolution 2, 488-503.
34. La Porta N, Bertamini M, Nedunchezhian N, Muthuchelian K. 2006. Photosynthetic changes that occur during aging of cypress (Cupressus sempervirens L.) needles. Photosynthetica 44, 555-560.
35. McAdam SA, Brodribb TJ. 2015. The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiology 167, 833-843.
36. Magallón SA, Sanderson MJ. 2005. Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59, 1653-1670.
37. Manter DK, Kerrigan J. 2004. A/Ci curve analysis across a range of woody plant species: influence of regression analysis parameters and mesophyll conductance. Journal of Experimental Botany 55, 2581-2588.
38. Mullin LP, Sillett SC, Koch GW, Tu KP, Antoine ME. 2009. Physiological consequences of height-related morphological variation in Sequoia sempervirens foliage. Tree Physiology 29, 999-1010.
39. Niinemets Ü. 1999. Research review. Components of leaf dry mass per area-thickness and density -alter leaf photosynthetic capacity in reverse directions in woody plants. The New Phytologist 144, 35-47.
40. Niinemets Ü. 2016. Does the touch of cold make evergreen leaves tougher? Tree Physiology 36, 267-272.
41. Niinemets Ü, Cescatti A, Rodehiero M, Tosens T. 2005. Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant, Cell and Environment 28, 1552-1566.
42. Niinemets Ü, Cescatti A, Rodeghiero M, Tosens T. 2006. Complex adjustments of photosynthetic potentials and internal diffusion conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex. Plant, Cell and Environment 29, 1159-1178.
43. Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR. 2009a. Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. Journal of Experimental Botany 60, 2271-2282.
44. Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR. 2009b. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 60, 2249-2270.
45. 2. Trends in Ecology and Evolution 26, 136-142.
46. Niinemets Ü, Lukjanova A, Turnbull MH, Sparrow AD. 2007. Plasticity in mesophyll volume fraction modulates light-acclimation in needle photosynthesis in two pines. Tree Physiology 27, 1137-1151.
47. Niinemets Ü, Reichstein M. 2003. Controls on the emission of plant volatiles through stomata: Differential sensitivity of emission rates to stomatal closure explained. Journal of Geophysical Research 108, 4208.
48. Niinemets Ü, Wright IJ, Evans JR. 2009c. Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. Journal of Experimental Botany 60, 2433-2449.
49. Nobel PS. 1991. Physicochemical and environmental plant physiology. San Diego, CA, USA: Academic Press.
50. Norstog K, Nicholls T. 1997. The biology of the cycads. Ithaca, NY, USA: Cornell University Press.
51. 2labelling technique. Rapid Communications in Mass Spectrometry 23, 282-290.
52. 2 and photosynthesis in two related Mediterranean Abies species. Plant, Cell and Environment 35, 2121-2129.
53. 2. Tree Physiology 36, 300-310.
54. 2 transfer conductance of mesophyll in walnut. Journal of Experimental Botany 53, 2423-2430.
55. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. 2009. Causes and consequences of variation in leaf mass per area (LMA): a metaanalysis. The New Phytologist 182, 565-588.
56. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91, 1582-1598.
57. Reich P, Kloeppel B, Ellsworth D, Walters M. 1995. Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104, 24-30.
58. Rodeghiero M, Niinemets U, Cescatti A. 2007. Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar et al. model parameters? Plant, Cell and Environment 30, 1006-1022.
59. Rydin C, Pedersen KR, Friis EM. 2004. On the evolutionary history of Ephedra: Cretaceous fossils and extant molecules. Proceedings of the National Academy of Sciences of the United States of America 101, 16571-16576.
60. Shipley B, Lechowicz MJ, Wright I, Reich PB. 2006. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87, 535-541.
61. Slaton MR, Smith WK. 2002. Mesophyll architecture and cell exposure to intercellular air space in alpine, desert, and forest species. International Journal of Plant Sciences 163, 937-948.
62. Stewart WN. 1993. Paleobotany and the evolution of plants. New York: Cambridge University Press.
63. 2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell and Environment 18, 149-157.
64. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512-526.
65. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America 101, 11030-11035.
66. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725-2729.
67. 2 diffusion. Journal of Experimental Botany 57, 343-354.
68. Terashima I, Hanba YT, Tholen D, Niinemets Ü. 2011. Leaf functional anatomy in relation to photosynthesis. Plant Physiology 155, 108-116.
69. Tholen D, Ethier G, Genty B, Pepin S, Zhu XG. 2012. Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant, Cell and Environment 35, 2087-2103.
70. 2 across species: quantitative limitations and scaling up by models. Journal of Experimental Botany 64, 2269-2281.
71. Tosens T, Niinemets U, Vislap V, Eichelmann H, Castro Díez P. 2012a. Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. Plant, Cell and Environment 35, 839-856.
72. Tosens T, Niinemets Ü, Westoby M, Wright IJ. 2012b. 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.
73. 2 diffusion as a key trait. The New Phytologist 209, 1576-1590.
74. Villar R, Held AA, Merino J. 1995. Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiology 107, 421-427.
75. von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376-387.
76. Wang XQ, Tank DC, Sang T. 2000. Phylogeny and divergence times in Pinaceae: evidence from three genomes. Molecular Biology and Evolution 17, 773-781.
77. 2 transfer. Journal of Experimental Botany 59, 1475-1487.
78. Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA. 2003. Transfer conductance in second growth Douglasfir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant, Cell and Environment 26, 1215-1227.
79. Wright IJ, Reich PB, Westoby M, et al. 2004. The worldwide leaf economics spectrum. Nature 428, 821-827.
80. Wright IJ, Westoby M, Reich PB. 2002. Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. Journal of Ecology 90, 534-543.
81. Zhang YJ, Cao KF, Sack L, Li N, Wei XM, Goldstein G. 2015. Extending the generality of leaf economic design principles in the cycads, an ancient lineage. The New Phytologist 206, 817-829.