Leaf Vasculature and the Upper Limit of Photosynthesis

  • William W. AdamsIIIEmail author
  • Jared J. Stewart
  • Stephanie K. Polutchko
  • Barbara Demmig-Adams
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)


The foliar vascular network is responsible for (1) structural support of the lamina as a platform for absorbing photons of light to drive photosynthesis, (2) transfer of information carriers like hormones and other signaling molecules between the leaf and other parts of the plant, (3) distribution of water and nutrients to leaf tissues via the xylem, and (4) movement of photosynthetic products, as well as chemical components remobilized during senescence, from mesophyll tissue into the phloem, and from source leaves to the plant’s many sinks. Foliar venation is thus central to the leaf’s primary role as a photosynthetic organ. Positive relationships between hydraulic conductance of the xylem, foliar vein density, and photosynthesis have been studied, and close links between foliar phloem capacity and intrinsic photosynthetic capacity were identified more recently. In this chapter, the relationship between various features of the foliar vasculature and photosynthetic capacity in mesophytic species with high rates of photosynthesis is explored. These metrics include foliar vein density, numbers and/or cross-sectional areas of xylem, phloem, and companion (including intermediary) cells, tracheary and sieve elements, and expansion of cell membrane area due to cell wall ingrowths in phloem transfer cells. Total xylem conduit volume per leaf area (the product of vein density and xylem cell metrics) of minor foliar veins exhibited a strong positive relationship with photosynthetic capacity per leaf area among multiple summer annuals. In the winter annual Arabidopsis thaliana, acclimation to contrasting growth temperatures involves differential acclimation of photosynthesis versus transpiration and is matched by similar differential acclimation of phloem versus xylem features. Photosynthetic capacity was positively correlated with various phloem metrics among all species and conditions examined, including summer annuals, winter annuals, and biennial species under various temperature and light conditions during growth. Given the essential role of vasculature in leaf functioning, it is not surprising that foliar vascular metrics are adjusted in response to environmental conditions (temperature, light levels, etc.). The vascular grid of the leaf and its xylem and phloem components thus underlies efficient leaf and plant functioning by facilitating the exchange of water, nutrients, and energy and information carriers between photosynthetic and non-photosynthetic parts of the plant. Recognition of this centrality of the foliar vasculature is critical to the effective selection, breeding, and engineering of crop plants to meet the nutritional, energy, fiber, material, and pharmaceutical needs of an expanding human population.



C-repeat binding factor (a transcription factor)


companion cell


intermediary cell


phloem parenchyma cell


sieve element


tracheary element


vein density (vein length per leaf area)


xylem parenchyma cell



The research of BD-A and WWA was supported by the National Science Foundation (Award Numbers IOS-0841546 and DEB-1022236) and the University of Colorado at Boulder. We remain indebted to Profs. D. Schemske and J. Ågren for the invitation to study the Swedish and Italian ecotypes of Arabidopsis thaliana.


  1. Adams WW III, Hoehn A, Demmig-Adams B (1995) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22: 75–85Google Scholar
  2. Adams WW III, Demmig-Adams B, Rosenstiel TN, Ebbert V, Brightwell AK, Barker DH, Zarter CR (2001a) Photosynthesis, xanthophylls, and D1 phosphorylation under winter stress. In: PS2001, Vol 3, Number 1. Proceedings of the 12th International Congress on Photosynthesis. CSIRO Publishing, Melbourne, Australia.;
  3. Adams WW III, Demmig-Adams B, Rosenstiel RN, Ebbert V (2001b) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res 67:51–62PubMedCrossRefPubMedCentralGoogle Scholar
  4. Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biol 4:545–557CrossRefGoogle Scholar
  5. Adams WW III, Zarter CF, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49CrossRefGoogle Scholar
  6. Adams WW III, Amiard VSE, Mueh KE, Turgeon R, Demmig-Adams B (2005) Phloem loading type and photosynthetic acclimation to light. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspectives. Allen Press, Lawrence, pp 814–816Google Scholar
  7. 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. Photosynth Res 94:455–466PubMedCrossRefPubMedCentralGoogle Scholar
  8. Adams WW III, Cohu CM, Muller O, Demmig-Adams B (2013a) Foliar phloem infrastructure in support of photosynthesis. Front Plant Sci 4:194PubMedPubMedCentralGoogle Scholar
  9. Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2013b) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117:31–44PubMedCrossRefPubMedCentralGoogle Scholar
  10. Adams WW III, Cohu CM, Amiard V, Demmig-Adams B (2014a) Associations between phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate. Front Plant Sci 5:24Google Scholar
  11. Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2014b) Photosystem II efficiency and non-photochemical quenching in the context of source-sink balance. In: Demmig-Adams B, Garab G, Adams WW III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht, pp 503–529Google Scholar
  12. Adams WW III, Stewart JJ, Cohu CM, Muller O, Demmig-Adams B (2016) Habitat temperature and precipitation of Arabidopsis thaliana ecotypes determine the response of foliar vasculature, photosynthesis, and transpiration to growth temperature. Front Plant Sci 7:1026PubMedPubMedCentralCrossRefGoogle Scholar
  13. Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM (2005) Genetic and molecular analyses of natural variation indicate CBF2 as a candidate for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139:1304–1312PubMedPubMedCentralCrossRefGoogle Scholar
  14. Amiard V, Mueh KE, Demmig-Adams B, Ebbert V, Turgeon R, Adams WW III (2005) Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proc Natl Acad Sci U S A 102:12968–12973PubMedPubMedCentralCrossRefGoogle Scholar
  15. Amiard V, Demmig-Adams B, Mueh KE, Turgeon R, Combs AF, Adams WW III (2007) Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development. New Phytol 173:722–731PubMedCrossRefGoogle Scholar
  16. Bailey IW, Sinnott EW (1916) The climatic distribution of certain types of angiosperm leaves. Am J Bot 3:24–39CrossRefGoogle Scholar
  17. Beerling DJ, Franks PJ (2010) The hidden cost of transpiration. Nature 464:495–496PubMedCrossRefGoogle Scholar
  18. Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecol Lett 14:91–100PubMedCrossRefGoogle Scholar
  19. Boersma L, Lindstrom FT, Childs SW (1991) Model for steady-state coupled transport in xylem and phloem. Agron J 83:401–408CrossRefGoogle Scholar
  20. Boese SR, Huner NPA (1990) Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. Plant Physiol 94:1830–1836PubMedPubMedCentralCrossRefGoogle Scholar
  21. Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187:348–358PubMedGoogle Scholar
  22. Bower FO (1884) On the comparative morphology of the leaf in the vascular cryptogams and gymnosperms. Phil Trans R Soc Lond 175:565–615CrossRefGoogle Scholar
  23. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc R Soc B-Biol Sci 276:1771–1776CrossRefGoogle Scholar
  24. Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183CrossRefGoogle Scholar
  25. Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846PubMedCrossRefGoogle Scholar
  26. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brodribb TJ, Feild TS, Sack L (2010) Viewing leaf structure and evolution from a hydraulic perspective. Funct Plant Biol 37:488–498CrossRefGoogle Scholar
  28. Buckley TN, Sack L, Gilbert ME (2011) The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiol 156:962–973PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cabrita P, Thorpe M, Huber G (2013) Hydrodynamics of steady state phloem transport with radial leakage of solute. Front Plant Sci 4:531PubMedPubMedCentralCrossRefGoogle Scholar
  30. Canny MJ (1993) The transpiration stream in the leaf apoplast: water and solutes. Phil Trans R Soc Lond B 341:87–100CrossRefGoogle Scholar
  31. Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211CrossRefGoogle Scholar
  32. Cohu CM, Muller O, Demmig-Adams B, Adams WW III (2013a) Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes. Front Plant Sci 4:240PubMedPubMedCentralGoogle Scholar
  33. Cohu CM, Muller O, Stewart JJ, Demmig-Adams B, Adams WWIII (2013b) Association between minor loading vein architecture and light- and CO2-saturated photosynthetic oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes. Front Plant Sci 4:264PubMedPubMedCentralGoogle Scholar
  34. Cohu CM, Muller O, Adams WW III, Demmig-Adams B (2014) Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals. Physiol Plant 152:164–173PubMedCrossRefPubMedCentralGoogle Scholar
  35. Dahal K, Gadapati W, Savitch LV, Singh J, Hüner NPA (2012) Cold acclimation and BnCBF17-over-expression enhance photosynthetic performance and energy conversion efficiency during long-term growth of Brassica napus under elevated CO2 conditions. Planta 236:1639–1652PubMedCrossRefPubMedCentralGoogle Scholar
  36. Davidson A, Keller F, Turgeon R (2011) Phloem loading, plant growth form, and climate. Protoplasma 248:153–163PubMedCrossRefPubMedCentralGoogle Scholar
  37. Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372PubMedCrossRefPubMedCentralGoogle Scholar
  38. Duan Z, Homma A, Kobayashi M, Nagata N, Kaneko Y, Fujiki Y, Nishida I (2014) Photoassimilation, assimilate translocation and plasmodesmal biogenesis in the source leaves of Arabidopsis thaliana grown under an increased atmospheric CO2 concentration. Plant Cell Physiol 55:358–369PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dumlao MR, Darehshouri A, Cohu CM, Muller O, Mathias J, Adams WW III, Demmig-Adams B (2012) Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type. Photosynth Res 113:181–189PubMedCrossRefPubMedCentralGoogle Scholar
  40. Efroni I, Eshed Y, Lifschitz E (2010) Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22:1019–1032PubMedPubMedCentralCrossRefGoogle Scholar
  41. Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin IW, Qu X-Q, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Cur Opin Plant Biol 25:53–62CrossRefGoogle Scholar
  42. Esau K (1934) Ontogeny of phloem in the sugar beet (Beta vulgaris L.). Am J Bot 21:632–644CrossRefGoogle Scholar
  43. Esau K (1967) Minor veins in Beta leaves: structure related to function. Proc Am Phil Soc 111:219–233Google Scholar
  44. Esau K, Cheadle VI (1958) Wall thickening in sieve elements. Proc Natl Acad Sci U S A 44:546–553PubMedPubMedCentralCrossRefGoogle Scholar
  45. Falhof J, Pedersen JT, Fuglsang AT, Palmgren M (2016) Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol Plant 9:323–337PubMedCrossRefPubMedCentralGoogle Scholar
  46. Fatichi S, Leuzinger S, Körner C (2014) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201:1086–1095PubMedCrossRefPubMedCentralGoogle Scholar
  47. Fischer A (1884) Untersuchungen über das Siebröhren-System der Cucurbitaceen. Gebrüder Borntraeger, BerlinGoogle Scholar
  48. Fischer A (1885) Studien über die Siebröhren der Dikotylenblätter. Ber Verhanl Kön Sächsische Gesell der Wiss Leipzig. Math Phys Cl 37:245–290Google Scholar
  49. Foster AS (1936) Leaf differentiation in angiosperms. Bot Rev 2:349–372CrossRefGoogle Scholar
  50. Franks PJ (2006) Higher rates of leaf gas exchange area associated with higher leaf hydrodynamic pressure gradients. Plant Cell Environ 29:584–592PubMedCrossRefPubMedCentralGoogle Scholar
  51. Fu Q, Cheng L, Guo Y, Turgeon R (2011) Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol 157:1518–1527PubMedPubMedCentralCrossRefGoogle Scholar
  52. Gamalei YV (1989) Structure and function of leaf minor veins in trees and herbs. A taxonimical review. Trees 3:96–110CrossRefGoogle Scholar
  53. Gamalei YV, Pakhomova MV, Syutkina AV, Voitsekhovskaja OV (2000) Compartmentation of assimilate fluxes in leaves I. Ultrastructural response of mesophyll and companion cells to the alteration of assimilate export. Plant Biol 2:98–106CrossRefGoogle Scholar
  54. Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214PubMedCrossRefGoogle Scholar
  55. Gehan MA, Park S, Gilmour SJ, An C, Lee C-M, Thomashow MF (2015) Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes. Plant J 84:682–693PubMedCrossRefGoogle Scholar
  56. Gifford RM, Evans LT (1981) Photosynthesis, carbon partitioning, and yield. Ann Rev Plant Physiol 32:485–509CrossRefGoogle Scholar
  57. Gifford RM, Thorne JH, Hitz WD, Giaquinta RT (1984) Crop productivity and photoassimilate partitioning. Science 225:801–808PubMedCrossRefGoogle Scholar
  58. Giuliani R, Koteyeva N, Voznesenskaya E, Evans MA, Cousins AB, Edwards GE (2013) Coordination of leaf photosynthesis, transpiration, and structural traits in rice and wild relatives (genus Oryza). Plant Physiol 162:1632–1651PubMedPubMedCentralCrossRefGoogle Scholar
  59. Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92CrossRefGoogle Scholar
  60. Gorsuch PA, Pandey S, Atkin OK (2010) Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves. Plant Cell Environ 33:244–258PubMedCrossRefGoogle Scholar
  61. Gray A (1848) A manual of the botany of the Northern United States: from New England to Wisconsin and South to Ohio and Pennsylvania inclusive, (the mosses and liverworts by Wm. S. Sullivant), arranged according to the natural system. James Munroe, BostonGoogle Scholar
  62. Gunning BES, Pate JS (1969) “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes – their occurrence, structure, and development. Protoplasma 68:107–133CrossRefGoogle Scholar
  63. Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–115CrossRefGoogle Scholar
  64. Hacke UG, Jacobsen AL, Pratt RB (2009) Xylem function in arid-land shrubs from California, USA: an ecological and evolutionary analysis. Plant Cell Environ 32:1324–1333PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol 126:695–705CrossRefGoogle Scholar
  66. Haritatos E, Turgeon R (1995) Symplastic phloem loading by polymer trapping. In: Pontis HG, Salemo GL, Echeverria EJ (eds) Sucrose metabolism, biochemistry, physiology and molecular biology, current topics in plant physiology, vol 14. American Society of Plant Physiologists, Rockville, pp 216–224Google Scholar
  67. Holaday AS, Martindale W, Alred W, Brooks AL, Leedgood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98:1105–1114PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hölttä T, Nikinmaa E (2013) Modelling the effect of xylem and phloem transport on leaf gas exchange. Acta Hortic (991):351–358Google Scholar
  69. Hölttä T, Vesala T, Sevanto S, Perämäki M, Nikinmaa E (2006) Modeling xylem and phloem water flows in trees according to cohesion theory and Münch hypothesis. Trees 20:67–78CrossRefGoogle Scholar
  70. Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121CrossRefGoogle Scholar
  71. Hüner NPA, Bode R, Dahal K, Hollis L, Rosso D, Krol M, Ivanov AG (2012) Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Sci 3:255PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hüner NPA, Dahal K, Bode R, Kurepin LV, Ivanov AG (2016) Photosynthetic acclimation, vernalization, crop productivity and “the grand design of photosynthesis”. J Plant Physiol 203:29–43PubMedCrossRefGoogle Scholar
  73. Jarvis AJ, Davies WJ (1998) The coupled response of stomatal conductance to photosynthesis and transpiration. J Exp Bot 49:399–406CrossRefGoogle Scholar
  74. Jensen KH, Berg-Sørensen K, Bruus H, Holbrook NM, Liesche J, Schulz A, Zwieniecki MA, Bohr T (2016) Sap flow and sugar transport in plants. Rev Mod Phys 88:035007CrossRefGoogle Scholar
  75. Jones HG (1998) Stomatal control of photosynthesis and transpiration. J Exp Bot 49:387–398CrossRefGoogle Scholar
  76. Kang J, Zhang H, Sun T, Shi Y, Want J, Zhang B, Want Z, Zhou Y, Gu H (2013) Natural variation of C-repeat-binding factor (CBFs) genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China. New Phytol 199:1069–1080PubMedCrossRefGoogle Scholar
  77. Karabourniotis G, Booman JF, Nikolopoulos D (2000) A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant Cell Environ 23:423–430CrossRefGoogle Scholar
  78. Keller BA (1933) Über den anatomischen Bau dürre- und hitzeresistenter Blätter. Ber Deut Bot Ges 51:514–522Google Scholar
  79. Körner C (2013) Growth controls photosynthesis – mostly. Nova Acta Leopold 114:273–283Google Scholar
  80. Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195:313–323CrossRefGoogle Scholar
  81. Krapp A, Hofmann B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3:817–828CrossRefGoogle Scholar
  82. Kühn C (2003) A comparison of the sucrose transporter systems of different plant species. Plant Biol 5:215–232CrossRefGoogle Scholar
  83. Kurepin LV, Dahal KP, Savitch LV, Singh J, Bode R, Ivanov AG, Hurry V, Hüner NPA (2013) Role of CBFs as integrators of chloroplast redox, phytochrome, and plant hormone signaling during cold acclimation. Int J Mol Sci 14:12729–12763PubMedPubMedCentralCrossRefGoogle Scholar
  84. Langan SJ, Ewers FW, Davis SD (1997) Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell Environ 20:425–437CrossRefGoogle Scholar
  85. Lebedincev E (1927) Physiologische une anatomische Besonderheiten der in trockener und feuchter Luft gezogenen Pflanzen. Ber Deut Bot Ges 45:83–96Google Scholar
  86. Maherali H, Sherrard ME, Clifford MH, Latta RG (2008) Leaf hydraulic conductivity and photosynthesis are genetically correlated in an annual grass. New Phytol 180:240–247PubMedCrossRefGoogle Scholar
  87. Martindale W, Leegood RC (1997) Acclimation of photosynthesis to low temperature in Spinacia oleracea L. I. Effects of acclimation on CO2-assimilation and carbon partitioning. J Exp Bot 48:1865–1872CrossRefGoogle Scholar
  88. McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. Am Nat 175:447–460CrossRefGoogle Scholar
  89. Melville R (1969) Leaf venation patterns and the origin of angiosperms. Nature 224:121–125CrossRefGoogle Scholar
  90. Monroe JG, McGovern C, Lasky JR, Grogan K, Beck J, McKay JK (2016) Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana. Mol Evol 25:3632–3644Google Scholar
  91. Muller O, Cohu CM, Stewart JJ, Protheroe JA, Demmig-Adams B, Adams WW III (2014a) Association between photosynthesis and contrasting features of minor veins in leaves of summer annuals loading phloem via symplastic versus apoplastic routes. Physiol Plant 152:174–183PubMedCrossRefGoogle Scholar
  92. Muller O, Stewart JJ, Cohu CM, Polutchko SK, Demmig-Adams B, Adams WW III (2014b) Leaf architectural, vascular, and photosynthetic acclimation to temperature in two biennials. Physiol Plant 152:763–772PubMedCrossRefPubMedCentralGoogle Scholar
  93. Münch E (1930) Die Stoffbewegungen in der Pflanze. Gustav Fischer, JenaGoogle Scholar
  94. Nardini A, Gortan E, Salleo S (2005) Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species. Funct Plant Biol 32:953–961CrossRefGoogle Scholar
  95. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692PubMedCrossRefGoogle Scholar
  96. Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36:655–669PubMedCrossRefGoogle Scholar
  97. Niklas KJ (1992) Plant biomechanics. The University of Chicago Press, ChicagoGoogle Scholar
  98. Niklas KJ (1999) A mechanical perspective on foliage leaf form and function. New Phytol 143:19–31CrossRefGoogle Scholar
  99. Niklas KJ (2009) Functional adaptation and phenotypic plasticity at the cellular and whole plant level. J Biosci 34:613–620PubMedCrossRefGoogle Scholar
  100. Nobel PS (2009) Physicochemical and environmental plant physiology, 4th edn. Academic, AmsterdamGoogle Scholar
  101. Oakley CG, Ågren J, Atchinson RA, Schemske DW (2014) QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. Mol Ecol 23:4304–4315PubMedCrossRefGoogle Scholar
  102. Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454PubMedCrossRefGoogle Scholar
  103. Palacio-López K, Beckage B, Scheiner S, Molofsky J (2015) The ubiquity of phenotypic plasticity in plants: a synthesis. Ecol Evol 5:3389–3400PubMedPubMedCentralCrossRefGoogle Scholar
  104. Pate JS, Gunning BES (1969) Vascular transfer cells in angiosperm leaves. A taxonomic and morphological survey. Protoplasma 68:135–156CrossRefGoogle Scholar
  105. Pate JS, Gunning BES (1972) Transfer cells. Annu Rev Plant Physiol 23:173–196CrossRefGoogle Scholar
  106. Patrick JW, Zhang WH, Tyerman SD, Offler CE, Walker NA (2001) Role of membrane transport in phloem translocation of assimilates and water. Aust J Plant Physiol 28:695–707Google Scholar
  107. Pino M-T, Skinner JS, Jeknic Z, Hayes PM, Soeldner AH, Thomashow MF, Chen THH (2008) Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant Cell Environ 31:393–406PubMedCrossRefGoogle Scholar
  108. Polutchko SK, Stewart JJ, Demmig-Adams B, Adams WW III (2018) Evaluating the link between photosynthetic capacity and leaf vascular organization with principal component analysis. Photosynthetica 56:392–403CrossRefGoogle Scholar
  109. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588PubMedCrossRefGoogle Scholar
  110. Pray TR (1954) Foliar venation of angiosperms. 1. Mature venation of Liriodendron. Am J Bot 41:663–670CrossRefGoogle Scholar
  111. Pray TR (1955) Foliar venation of angiosperms. 3. Pattern and histology of the venation of Hosta. Am J Bot 42:611–618CrossRefGoogle Scholar
  112. Rennie EA, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proc Natl Acad Sci U S A 106:14162–14167PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rishmawi L, Bühler J, Jaegle B, Hülskamp M, Koornneef M (2017) Quantitative trait loci controlling leaf venation in Arabidopsis. Plant Cell Environ 40:1429–1441Google Scholar
  114. Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H (2001) Evolution and function of leaf venation architecture: a review. Ann Bot 87:553–566CrossRefGoogle Scholar
  115. Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381CrossRefGoogle Scholar
  116. Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000CrossRefGoogle Scholar
  117. Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140:543–550PubMedCrossRefGoogle Scholar
  118. Savitch LV, Allard G, Seki M, Robert LS, Tinker NA, Huner NPA, Shinozaki K, Singh J (2005) The effect of overexpression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. Plant Cell Physiol 46:1525–1539PubMedCrossRefPubMedCentralGoogle Scholar
  119. Schuster W (1908) Die Blattaderung des Dicotylenblattes und ihre Abhängigkeit von äußeren Einflüssen. Ber Deut Bot Ges 26:194–237Google Scholar
  120. Sevanto S, Hölttä T, Holbrook NM (2011) Effects of hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. Plant Cell Environ 34:690–703PubMedCrossRefGoogle Scholar
  121. Slewinski TL, Zhang C, Turgeon R (2013) Structural and functional heterogeneity in phloem loading and transport. Front Plant Sci 4:244PubMedPubMedCentralGoogle Scholar
  122. Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482PubMedPubMedCentralCrossRefGoogle Scholar
  123. Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 sucrose/H+ symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148:200–211PubMedPubMedCentralCrossRefGoogle Scholar
  124. Sterck FJ, Martínez-Vilalta J, Mencuccini M, Cochard H, Gerrits P, Zweifel R, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U (2012) Understanding trait interactions and their impacts on growth in scots pine branches across Europe. Funct Ecol 26:541–549CrossRefGoogle Scholar
  125. Stewart JJ, Demmig-Adams B, Cohu CM, Wenzl CA, Muller O, Adams WW III (2016) Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe. Plant Cell Environ 39:1549–1558PubMedCrossRefPubMedCentralGoogle Scholar
  126. Stewart JJ, Polutchko SK, Adams WW III, Cohu CM, Wenzl CA, Demmig-Adams B (2017a) Light, temperature, and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana. Physiol Plant 160:98–110Google Scholar
  127. Stewart JJ, Polutchko SK, Adams WW III, Demmig-Adams B (2017b) Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity. Photosynth Res 134:215–229Google Scholar
  128. Strand Å, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12:605–614PubMedCrossRefPubMedCentralGoogle Scholar
  129. Strand Å, Hurry VM, Henkes S, Huner NPA, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperature: increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397PubMedPubMedCentralCrossRefGoogle Scholar
  130. Strasburger E (1891) Über den Bau und die Berrichtunger der Leitungsbahnen in den Pflanzen. Hitsologische Beiträge 3:1–1000Google Scholar
  131. Strasburger E (1894) Lehrbuch der Botanik für Hochschulen. Fischer, Jena (currently in its 37th edition as Lehrbuch der Pflanzenwissenschaften)Google Scholar
  132. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:527–542CrossRefGoogle Scholar
  133. Terashima I, Miyazawa SI, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105CrossRefGoogle Scholar
  134. Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold-response pathway. Plant Physiol 154:571–577PubMedPubMedCentralCrossRefGoogle Scholar
  135. Turgeon R (2010) The role of phloem loading reconsidered. Plant Physiol 152:1817–1823PubMedPubMedCentralCrossRefGoogle Scholar
  136. Turgeon R, Medville R, Nixon KC (2001) The evolution of minor vein phloem and phloem loading. Am J Bot 88:1331–1339PubMedCrossRefPubMedCentralGoogle Scholar
  137. Tuzet A, Perrier A, Leuning R (2003) A coupled model of stomatal conductance, photosynthesis and transpiration. Plant Cell Environ 26:1097–1116CrossRefGoogle Scholar
  138. Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763PubMedCrossRefGoogle Scholar
  139. Verhoeven AS, Adams WW III, Demmig-Adams B (1999) The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118:277–287PubMedCrossRefPubMedCentralGoogle Scholar
  140. Vogel S (1989) Drag and reconfiguration of broad leaves in high winds. J Exp Bot 40:941–948CrossRefGoogle Scholar
  141. von Ettingshausen G (1861) Die Blatt-Skelete der Dikotyledonen. Staatsdruckerei Wien, ViennaGoogle Scholar
  142. Walls RL (2011) Angiosperm leaf vein patterns are linked to leaf functions in global-scale data set. Am J Bot 98:244–253PubMedCrossRefGoogle Scholar
  143. Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381CrossRefGoogle Scholar
  144. Wimmers LW, Turgeon R (1991) Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta 186:2–12PubMedCrossRefGoogle Scholar
  145. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426CrossRefGoogle Scholar
  146. Wylie RB (1951) Principles of foliar organization shown by sun-shade leaves from ten species of deciduous dicotyledonous trees. Am J Bot 38:355–361CrossRefGoogle Scholar
  147. Wylie RB (1952) The bundle sheath extension in leaves of dicotyledons. Am J Bot 39:645–651CrossRefGoogle Scholar
  148. Zalenski W (1902) Über die Ausbildung der Nervation bei verschiedenen Pflanzen. Ber Deut Bot Ges 20:433–440Google Scholar
  149. Zalenski W (1904) Materials for the study of the quantitative anatomy of different leaves of the same plant. Memoires de l'Institut Polytechnique de Kiev 4:1–203Google Scholar
  150. Zhu S-D, Song J-J, Li R-H, Ye Q (2013) Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests. Plant Cell Environ 36:879–891PubMedCrossRefPubMedCentralGoogle Scholar
  151. Zhu JQ, van der Werf W, Anten NPR, Vos J, Evers JB (2015) The contribution of phenotypic plasticity to complementary light capture in plant mixtures. New Phytol 207:1213–1222CrossRefGoogle Scholar
  152. Zsögön A, Alves Negrini AC, Pereira Peres LE, Nguyen HT, Ball MC (2015) A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum). New Phytol 205:618–626PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • William W. AdamsIII
    • 1
    Email author
  • Jared J. Stewart
    • 1
  • Stephanie K. Polutchko
    • 1
  • Barbara Demmig-Adams
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations