Leaf venation: Structure, function, development, evolution, ecology and applications in the past, present and future

New Phytologist

Volumn 198, Issue 4, 2013, Pages 983-1000

  Sack, Lawren ^a   Scoffoni, Christine ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biological networks; Drought tolerance; Functional traits; Leaf hydraulics; Shade tolerance; Vasculature; Vein patterning

Indexed keywords

ADAPTATION; DROUGHT; ECOLOGY; EVOLUTION; GROWTH FORM; HABITAT; LEAF; PALEOBIOLOGY; PLANT; PLASTICITY; SHADE TOLERANCE;

ECOSYSTEM; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; EVOLUTION; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; PHYLOGEOGRAPHY; PHYSIOLOGY; PLANT LEAF; QUANTITATIVE TRAIT; REVIEW;

BIOLOGICAL EVOLUTION; ECOLOGICAL AND ENVIRONMENTAL PHENOMENA; ECOSYSTEM; PHYLOGEOGRAPHY; PLANT LEAVES; QUANTITATIVE TRAIT, HERITABLE;

EID: 84877602457     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12253     Document Type: Review

References (176)

1. Adams WW III, Watson AM, Mueh KE, Amiard V, Turgeon R, Ebbert V, Logan BA, Combs AF, Demmig-Adams B. 2007. Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynthesis Research 94: 455-466.
2. Alvin K, Chaloner WG. 1970. Parallel evolution in leaf venation: an alternative view of angiosperm origins. Nature 226: 662-663.
3. Arzee T. 1953. Morphology and ontogeny of foliar sclereids in Olea europaea. 2. Ontogeny. American Journal of Botany 40: 745-752.
4. Badeck F-W, Fontaine J-L, Dumas F, Ghashghaie J. 2009. Consistent patterns in leaf lamina and leaf vein carbon isotope composition across ten herbs and tree species. Rapid Communications in Mass Spectrometry 23: 2455-2460.
5. Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C. 2009. Integration of transport-based models for phyllotaxis and midvein formation. Genes & Development 23: 373-384.
6. Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 179: 975-986.
7. Beerling DJ, Fleming AJ. 2007. Zimmermann's telome theory of megaphyll leaf evolution: a molecular and cellular critique. Current Opinion in Plant Biology 10: 4-12.
8. Beerling DJ, Franks PJ. 2010. Plant science: the hidden cost of transpiration. Nature 464: 495-496.
9. 2 decline in the Late Palaeozoic era. Nature 410: 352-354.
10. Berner RA. 2008. Addendum to "Inclusion of the weathering of volcanic rocks in the GEOCARBSULF model" (vol 306, pg 295-302, 2006). American Journal of Science 308: 100-103.
11. Blackman CJ, Brodribb TJ. 2011. Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Functional Plant Biology 38: 118-126.
12. Blonder B, De Carlo F, Moore J, Rivers M, Enquist BJ. 2012. X-ray imaging of leaf venation networks. New Phytologist 196: 1274-1282.
13. Blonder B, Violle C, Bentley LP, Enquist BJ. 2011. Venation networks and the origin of the leaf economics spectrum. Ecology Letters 14: 91-100.
14. de Boer HJ, Eppinga MB, Wassen MJ, Dekker SC. 2012. A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. Nature Communications 3: 1221.
15. Bohn S, Andreotti B, Douady S, Munzinger J, Couder Y. 2002. Constitutive property of the local organization of leaf venation networks. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics 65: 061914.
16. Bohn S, Magnasco MO. 2007. Structure, scaling and phase transition in the optimal transport network. Physical Review Letters 98: 088702.
17. Bosabalidis AM, Evert RF, Russin WA. 1994. Ontogeny of the vascular bundles and contiguous tissues in the maize leaf blade. American Journal of Botany 81: 745-752.
18. Boyce CK. 2008. The fossil record of plant physiology and development: what leaves can tell us. Paleontological Society Papers 14: 133-146.
19. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B-Biological Sciences 276: 1771-1776.
20. Boyce CK, Lee JE. 2010. An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity. Proceedings of the Royal Society B-Biological Sciences 277: 3437-3443.
21. Boyce CK, Lee J-E, Feild TS, Brodribb TJ, Zwieniecki MA. 2010. Angiosperms helped put the rain in the rainforests: the impact of plant physiological evolution on tropical biodiversity. Annals of the Missouri Botanical Garden 97: 527-540.
22. 2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences of the United States of America 109: 10403-10408.
23. Brodersen CR, Roark LC, Pittermann J. 2012. The physiological implications of primary xylem organization in two ferns. Plant, Cell & Environment 35: 1898-1911.
24. Brodribb TJ. 2009. Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Science 177: 245-251.
25. Brodribb TJ, Feild TS. 2008. Evolutionary significance of a flat-leaved Pinus in Vietnamese rainforest. New Phytologist 178: 201-209.
26. Brodribb TJ, Feild TS. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13: 175-183.
27. Brodribb TJ, Feild TS, Jordan GJ. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144: 1890-1898.
28. Brodribb TJ, Feild TS, Sack L. 2010. Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37: 488-498.
29. Brodribb TJ, Holbrook NM. 2003. Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest. New Phytologist 158: 295-303.
30. Brodribb TJ, Jordan GJ. 2011. Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192: 437-448.
31. Buckley TN, Sack L, Gilbert ME. 2011. The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156: 962-973.
32. Candela H, Martinez-Laborda A, Micol JL. 1999. Venation pattern formation in Arabidopsis thaliana vegetative leaves. Developmental Biology 205: 205-216.
33. Choong MF, Lucas PW, Ong JSY, Pereira B, Tan HTW, Turner IM. 1992. Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytologist 121: 597-610.
34. Cochard H, Nardini A, Coll L. 2004. Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell & Environment 27: 1257-1267.
35. Cooley AM, Reich A, Rundel P. 2004. Leaf support biomechanics of neotropical understory herbs. American Journal of Botany 91: 573-581.
36. Coomes DA, Heathcote S, Godfrey ER, Shepherd JJ, Sack L. 2008. Scaling of xylem vessels and veins within the leaves of oak species. Biology Letters 4: 302-306.
37. Corson F. 2010. Fluctuations and redundancy in optimal transport networks. Physical Review Letters 104: 048703.
38. Couturier E, Brunel N, Douady S, Nakayama N. 2012. Abaxial growth and steric constraints guide leaf folding and shape in Acer pseudoplatanus. American Journal of Botany 2012: 1289-1299.
39. Crane PR, Kenrick P. 1997. Diverted development of reproductive organs: a source of morphological innovation in land plants. Plant Systematics and Evolution 206: 161-174.
40. Cutler DF. 2005 Design in plants. In: Collins MW, Atherton MA, Bryant JA, eds. Nature and Design. Southampton, Boston: WIT Press, 95-124.
41. Dannenhoffer JM, Ebert W, Evert RF. 1990. Leaf vasculature in barley, Hordeum vulgare (Poaceae). American Journal of Botany 77: 636-652.
42. Denne MP. 1960. Leaf development in Narcissus pseudonarcissus L. II. The comparative development of scale and foliage leaves. Annals of Botany 24: 32-47.
43. Dhondt S, Van Haerenborgh D, Van Cauwenbergh C, Merks RMH, Philips W, Beemster GTS, Inze D. 2012. Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis. Plant Journal 69: 553-563.
44. Doyle JA. 1998. Phylogeny of vascular plants. Annual Review of Ecology and Systematics 29: 567-599.
45. Doyle JA, Hickey LJ. 1976. Pollen and leaves from the mid-Cretaceous Potomac Group and their bearing on early angiosperm evolution. In: Beck CB, ed. Origin and early evolution of angiosperms. Columbia, New York, NY, USA: Columbia University Press, 139-206.
46. Dunbar-Co S, Sporck MJ, Sack L. 2009. Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. International Journal of Plant Sciences 170: 61-75.
47. Durand M. 2006. Architecture of optimal transport networks. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics 73: 016116.
48. 4 grasslands: integrating evolutionary and ecosystem science. Science 328: 587-591.
49. Ellis B, Daly DC, Hickey LJ, Mitchell JD, Johnson KR, Wilf P, Wing SL. 2009 Manual of Leaf Architecture. Ithaca, NY: Cornell University Press.
50. Esau K. 1977. Anatomy of seed plants, 2nd edn. New York, NY, USA: John Wiley & Sons.
51. Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR, Gomez B, Mohr BAR, Coiffard C, Kvacek J et al. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, USA 108: 8363-8366.
52. Feild TS, Wilson JP. 2012. Evolutionary voyage of angiosperm vessel structure-function and its significance for early angiosperm success. International Journal of Plant Sciences 173: 596-609.
53. Fisher DG, Evert RF. 1982. Studies on the leaf of Amaranthus retroflexus (Amaranthaceae): quantitative aspects, and solute concentration in the phloem. American Journal of Botany 69: 1375-1388.
54. Floyd SK, Bowman JL. 2006. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Current Biology 16: 1911-1917.
55. Franck DH. 1976. Comparative morphology and early life histogenesis of adult and juvenile leaves of Darlingtonia californica and their bearing on the concept of heterophylly. Botanical Gazette 137: 20-34.
56. 2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, USA 106: 10343-10347.
57. Givnish TJ. 1979 On the adaptive significance of leaf form. In: Solbrig OT, Jain S, Johnson GB, Raven PH, eds. Topics in Plant Population Biology. New York: Columbia University Press, 375-407.
58. 4 plants. Plant, Cell & Environment 36: 249-261.
59. Grubb PJ. 1998. A reassessment of the strategies of plants which cope with shortages of resources. Perspectives in Plant Ecology, Evolution and Systematics 1: 3-31.
60. Guyot G, Scoffoni C, Sack L. 2012. Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control. Plant, Cell & Environment 35: 857-871.
61. Haberlandt G. 1914. Physiological plant anatomy, 4th edn. London, UK: MacMillan.
62. Haritatos E, Ayre BG, Turgeon R. 2000a. Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter. Plant Physiology 123: 929-937.
63. Haritatos E, Medville R, Turgeon R. 2000b. Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211: 105-111.
64. Hickey LJ. 1973. Classification of architecture of dicotyledonous leaves. American Journal of Botany 60: 17-33.
65. Horn JW, Fisher JB, Tomlinson PB, Lewis CE, Laubengayer K. 2009. Evolution of lamina anatomy in the palm family (Arecaceae). American Journal of Botany 96: 1462-1486.
66. Jover-Gil S, Candela H, Robles P, Aguilera V, Barrero JM, Micol JL, Ponce MR. 2012. The microRNA pathway genes AGO1, HEN1 and HYL1 participate in leaf proximal-distal, venation and stomatal patterning in Arabidopsis. Plant and Cell Physiology 53: 1322-1333.
67. Kang J, Dengler N. 2004. Vein pattern development in adult leaves of Arabidopsis thaliana. International Journal of Plant Sciences 165: 231-242.
68. Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG. 2007. Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226: 1207-1218.
69. Karabourniotis G. 1998. Light-guiding function of foliar sclereids in the evergreen sclerophyll Phillyrea latifolia: a quantitative approach. Journal of Experimental Botany 49: 739-746.
70. Katifori E, Magnasco M. 2012. Quantifying loopy network architectures. PLoS ONE 7: e37994.
71. Katifori E, Szollosi GJ, Magnasco MO. 2010. Damage and fluctuations induce loops in optimal transport networks. Physical Review Letters 104: 048704.
72. King MJ, Vincent JFV, Harris W. 1996. Curling and folding of leaves of monocotyledons: a strategy for structural stiffness. New Zealand Journal of Botany 34: 411-416.
73. Kinsman EA, Pyke KA. 1998. Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125: 1815-1822.
74. Kobayashi H, Kresling B, Vincent JFV. 1998. The geometry of unfolding tree leaves. Proceedings of the Royal Society of London Series B-Biological Sciences 265: 147-154.
75. Korn RW. 2011. Window patterns in Lithops. International Journal of Plant Sciences 172: 1101-1109.
76. 3 plants. Journal of Experimental Botany 59: 1663-1673.
77. Liakoura V, Fotelli MN, Rennenberg H, Karabourniotis G. 2009. Should structure-function relations be considered separately for homobaric vs. heterobaric leaves? American Journal of Botany 96: 612-619.
78. Lucas PW, Pereira B. 1990. Estimation of the fracture-toughness of leaves. Functional Ecology 4: 819-822.
79. Lucas PW, Choong MF, Tan HTW, Turner IM, Berrick AJ. 1991. The fracture-toughness of the leaf of the dicotyledon Calophyllum inophyllum L. (Guttiferae). Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 334: 95-106.
80. Manuel Perez-Perez J, Rubio-Diaz S, Dhondt S, Hernandez-Romero D, Sanchez-Soriano J, Beemster GTS, Rosa Ponce M, Luis MicolJ. 2011. Whole organ, venation and epidermal cell morphological variations are correlated in the leaves of Arabidopsis mutants. Plant, Cell & Environment 34: 2200-2211.
81. 4 photosynthesism. Plant Journal 51: 886-896.
82. Maximov NA. 1931. The physiological significance of the xeromorphic structure of plants. Journal of Ecology 19: 279-282.
83. McKown AD, Cochard H, Sack L. 2010. Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. American Naturalist 175: 447-460.
84. 4 vein pattern in Flaveria (Asteraceae). American Journal of Botany 94: 382-399.
85. Méndez-Alonzo R, Ewers FW, Sack L. 2013. Ecological variation in leaf biomechanics and its scaling with tissue structure across three mediterranean-climate plant communities. Functional Ecology. doi: 11/1365-2435.12059.
86. Metcalfe CR, Chalk L. 1950. Anatomy of the dicotyledons. Oxford, UK: Clarendon Press.
87. Mileyko Y, Edelsbrunner H, Price CA, Weitz JS. 2012. Hierarchical ordering of reticular networks. PLoS ONE 7: e36715.
88. Moulia B, Fournier M. 1997. Mechanics of the maize leaf: a composite beam model of the midrib. Journal of Materials Science 32: 2771-2780.
89. 4 eudicots. American Journal of Botany 94: 362-381.
90. Murphy MRC, Jordan GJ, Brodribb TJ. 2012. Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35: 1407-1418.
91. Nardini A, Gortan E, Ramani M, Salleo S. 2008. Heterogeneity of gas exchange rates over the leaf surface in tobacco: an effect of hydraulic architecture? Plant, Cell & Environment 31: 804-812.
92. Nardini A, Raimondo F, Lo Gullo MA, Salleo S. 2010. Leafminers help us understand leaf hydraulic design. Plant, Cell & Environment 33: 1091-1100.
93. Nelson T, Dengler N. 1997. Leaf vascular pattern formation. Plant Cell 9: 1121-1135.
94. Niinemets U, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F. 2007a. Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100: 283-303.
95. Niinemets U, Portsmuth A, Tobias M. 2007b. Leaf shape and venation pattern alter the support investments within leaf lamina in temperate species: a neglected source of leaf physiological differentiation? Functional Ecology 21: 28-40.
96. Niinemets U, Valladares F. 2006. Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecological Monographs 76: 521-547.
97. Niklas KJ. 1992. Plant biomechanics: an engineering approach to plant form and function. Chicago, IL, USA: University of Chicago Press.
98. Niklas KJ. 1999. A mechanical perspective on foliage leaf form and function. New Phytologist 143: 19-31.
99. Niklas KJ, Cobb ED, Niinemets U, Reich PB, Sellin A, Shipley B, Wright IJ. 2007. "Diminishing returns" in the scaling of functional leaf traits across and within species groups. Proceedings of the National Academy of Sciences, USA 104: 8891-8896.
100. Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243.
101. Ocheltree TW, Nippert JB, Prasad PVV. 2012. Changes in stomatal conductance along grass blades reflect changes in leaf structure. Plant, Cell & Environment 35: 1040-1049.
102. 4 grasses: a modeling and meta-analysis. Oecologia 136: 532-542.
103. Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Diaz S, Dominy NJ, Elgart A, Enrico L et al. 2011. Global patterns of leaf mechanical properties. Ecology Letters 14: 301-312.
104. Orians CM, Smith SDP, Sack L. 2005. How are leaves plumbed inside a branch? Differences in leaf-to-leaf hydraulic sectoriality among six temperate tree species. Journal of Experimental Botany 56: 2267-2273.
105. Osborne CP, Beerling DJ, Lomax BH, Chaloner WG. 2004. Biophysical constraints on the origin of leaves inferred from the fossil record. Proceedings of the National Academy of Sciences, USA 101: 10360-10362.
106. 2 and water relations mediated by plant hydraulics. Philosophical Transactions of the Royal Society B-Biological Sciences 367: 583-600.
107. Pantin F, Monnet F, Jannaud D, Costa JM, Renaud J, Muller B, Simmonneau T, Genty B. 2013. The dual effect of abscisic acid on stomata. New Phytologist 197: 65-72.
108. Pantin F, Simonneau T, Muller B. 2012. Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytologist 196: 349-366.
109. Peppe DJ, Royer DL, Cariglino B, Oliver SY, Newman S, Leight E, Enikolopov G, Fernandez-Burgos M, Herrera F, Adams JM et al. 2011. Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist 190: 724-739.
110. Pietak AM. 2009. Describing long-range patterns in leaf vasculature by metaphoric fields. Journal of Theoretical Biology 261: 279-289.
111. Pittermann J. 2010. The evolution of water transport in plants: an integrated approach. Geobiology 8: 112-139.
112. Plymale EL, Wylie RB. 1944. The major veins of mesomorphic leaves. American Journal of Botany 31: 99-106.
113. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182: 565-588.
114. Prentice IC, Cramer W, Harrison SP, Leemans R, Monserud RA, Solomon AM. 1992. A global biome model based on plant physiology and dominance, soil properties and climate. Journal of Biogeography 19: 117-134.
115. Price CA, Symonova O, Mileyko Y, Hilley T, Weitz JS. 2011. Leaf extraction and analysis framework graphical user interface: segmenting and analyzing the structure of leaf veins and areoles. Plant Physiology 155: 236-245.
116. Raimondo F, Ghirardelli LA, Nardini A, Salleo S. 2003. Impact of the leaf miner Cameraria ohridella on photosynthesis, water relations and hydraulics of Aesculus hippocastanum leaves. Trees-Structure and Function 17: 376-382.
117. Ramji MV. 1967. Morphology and ontogeny of foliar venation of Calophyllum inophyllum L. Australian Journal of Botany 15: 437-443.
118. Read J, Stokes A. 2006. Plant biomechanics in an ecological context. American Journal of Botany 93: 1546-1565.
119. Rolland-Lagan AG, Amin M, Pakulska M. 2009. Quantifying leaf venation patterns: two-dimensional maps. Plant Journal 57: 195-205.
120. Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H. 2001. Evolution and function of leaf venation architecture: a review. Annals of Botany 87: 553-566.
121. 2-forced climate thresholds during the Phanerozoic. Geochimica Et Cosmochimica Acta 70: 5665-5675.
122. Russin WA, Evert RF. 1984. Studies on the leaf of Populus deltoides (Salicaceae): morphology and anatomy. American Journal of Botany 71: 1398-1415.
123. Russin WA, Evert RF. 1985a. Studies on the leaf of Populus deltoides (Salicaceae): quantitative aspects, and solute concentrations of the sieve tube members. American Journal of Botany 72: 487-500.
124. Russin WA, Evert RF. 1985b. Studies on the leaf of Populus deltoides (Salicaceae): ultrastructure, plasmodesmatal frequency, and solute concentrations. American Journal of Botany 72: 1232-1247.
125. Rutishauser R. 1999. Polymerous leaf whorls in vascular plants: developmental morphology and fuzziness of organ identities. International Journal of Plant Sciences 160: S81-S103.
126. Sack L, Cowan PD, Jaikumar N, Holbrook NM. 2003. The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26: 1343-1356.
127. Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM. 2008. Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proceedings of the National Academy of Sciences, USA 105: 1567-1572.
128. Sack L, Frole K. 2006. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87: 483-491.
129. Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57: 361-381.
130. Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC, Tran H, Tran T. 2012. Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications 3: 837.
131. Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM. 2002. The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53: 2177-2184.
132. Sack L, Streeter CM, Holbrook NM. 2004. Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 134: 1824-1833.
133. 4 photosynthesis. New Phytologist 161: 341-370.
134. Sawchuk MG, Head P, Donner TJ, Scarpella E. 2007. Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytologist 176: 560-571.
135. Sack L, Tyree MT. 2005 Leaf hydraulics and its implications in plant structure and function. In: Holbrook NM, Zweiniecki MA, eds. Vascular transport in plants. Oxford, UK: Elsevier/Academic Press.
136. Scarpella E, Barkoulas M, Tsiantis M. 2010. Control of leaf and vein development by auxin. Cold Spring Harbor Perspectives in Biology 2: a001511.
137. Scarpella E, Francis P, Berleth T. 2004. Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131: 3445-3455.
138. Scarpella E, Marcos D, Friml J, Berleth T. 2006. Control of leaf vascular patterning by polar auxin transport. Genes & Development 20: 1015-1027.
139. Scoffoni C, Pou A, Aasamaa K, Sack L. 2008. The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods. Plant, Cell & Environment 31: 1803-1812.
140. 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.
141. Shatil-Cohen A, Attia Z, Moshelion M. 2011. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant Journal 67: 72-80.
142. 2. International Journal of Plant Sciences 164: 71-75.
143. Shull CA. 1934. Lateral water transfer in leaves of Ginkgo biloba. Plant Physiology 9: 387-389.
144. Slewinski TL, Anderson AA, Zhang C, Turgeon R. 2012. Scarecrow plays a role in establishing Kranz anatomy in maize leaves. Plant and Cell Physiology 53: 2030-2037.
145. Smillie IRA, Pyke KA, Murchie EH. 2012. Variation in vein density and mesophyll cell architecture in a rice deletion mutant population. Journal of Experimental Botany 63: 4563-4570.
146. 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.
147. Sperry JS. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164: S115-S127.
148. 4 Hawaiian Euphorbia. Abstract presented to the Botanical Society of America. Providence, Rhode Island.
149. Strain RW. 1933. A study of vein endings in leaves. American Midland Naturalist 14: 367-375.
150. Taneda H, Terashima I. 2012. Co-ordinated development of the leaf midrib xylem with the lamina in Nicotiana tabacum. Annals of Botany 110: 35-45.
151. Terashima I. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research 31: 195-212.
152. Tomescu AMF. 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14: 5-12.
153. Tomlinson PB, Fisher JB. 2005. Development of nonlignified fibers in leaves of Gnetum gnemon (Gnetales). American Journal of Botany 92: 383-389.
154. Trivett CL, Evert RF. 1998. Ontogeny of the vascular bundles and contiguous tissues in the barley leaf blade. International Journal of Plant Sciences 159: 716-723.
155. Trivett ML, Pigg KB. 1996. A survey of reticulate venation among fossil and living land plants. In: Taylor DW, Hickey LJ, eds. Flowering plant origin, evolution & phylogeny. New York, NY, USA: Springer, 8-31.
156. Turgeon R. 2006. Phloem loading: how leaves gain their independence. BioScience 56: 15-24.
157. Turgeon R, Medville R. 2011. Amborella trichopoda, plasmodesmata, and the evolution of phloem loading. Protoplasma 248: 173-180.
158. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Berlin, Germany: Springer.
159. 4 grasses: a two-dimensional analysis. Annals of Botany 97: 611-621.
160. Uhl D, Mosbrugger V. 1999. Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography Palaeoclimatology Palaeoecology 149: 15-26.
161. Upchurch GR. 1984. Cuticular anatomy of angiosperm leaves from the Lower Cretaceous Potomac Group. 1. Zone I leaves. American Journal of Botany 71: 192-202.
162. Van Bel AJE. 1993. Strategies of phloem loading. Annual Review of Plant Physiology and Plant Molecular Biology 44: 253-281.
163. Van Volkenburgh E. 1999. Leaf expansion - an integrating plant behaviour. Plant, Cell & Environment 22: 1463-1473.
164. Vincent JFV. 1990. Fracture properties of plants. Advances in Botanical Research Incorporating Advances in Plant Pathology 17: 235-287.
165. Wagner WH. 1979. Reticulate veins in the systematics of modern ferns. Taxon 28: 87-95.
166. Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD. 2005. Many-to-one mapping of form to function: a general principle in organismal design? Integrative and Comparative Biology 45: 256-262.
167. Walls RL. 2011. Angiosperm leaf vein patterns are linked to leaf functions in a global scale data set. American Journal of Botany 98: 244-253.
168. Wilson CL. 1953. The telome theory. Botanical Review 19: 417-437.
169. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets U, Oleksyn J et al. 2005. Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14: 411-421.
170. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
171. Zhang S-B, Guan Z-J, Sun M, Zhang J-J, Cao K-F, Hu H. 2012. Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS ONE 7: e40080.
172. 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.
173. 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.
174. Zwieniecki MA, Brodribb TJ, Holbrook NM. 2007. Hydraulic design of leaves: insights from rehydration kinetics. Plant, Cell & Environment 30: 910-921.
175. 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.
176. 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.