Optimal concentration for sugar transport in plants

Journal of the Royal Society Interface

Volumn 10, Issue 83, 2013, Pages

  Jensen, Kaare H ^a   Savage, Jessica A ^a   Holbrook, N Michele ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Optimal concentration theory; Phloem transport; Sugar translocation

Indexed keywords

CARDIOVASCULAR SYSTEM; LOADING; PLANTS (BOTANY); SUGARS;

AVERAGE CONCENTRATION; CONSTANT PRESSURES; FLOW AND TRANSPORT; OPTIMAL CONCENTRATION; PHLOEM TRANSPORT; PRESSURE DIFFERENTIAL; SUGAR CONCENTRATION; TRANSPORT EFFICIENCY;

OPTIMIZATION;

CARBOHYDRATE;

ARTICLE; CONCENTRATION (PARAMETERS); ENERGY YIELD; FLOW RATE; MATHEMATICAL MODEL; NONHUMAN; PHLOEM; PHOTOSYNTHESIS; PLANT; SAP FLOW; SUGAR TRANSPORT; VASCULARIZATION; VISCOSITY; CARBOHYDRATE METABOLISM; CHEMISTRY; METABOLISM; PHYSIOLOGY; PRESSURE; REGRESSION ANALYSIS; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CARBOHYDRATE METABOLISM; CARBOHYDRATES; LEAST-SQUARES ANALYSIS; PHLOEM; PLANTS; PRESSURE; VISCOSITY;

EID: 84877251604     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.0055     Document Type: Article

References (92)

1. Stark H, Schuster S. 2012 Comparison of various approaches to calculating the optimal hematocrit invertebrates. J. Appl. Physiol. 113, 355-367. (doi:10. 1152/japplphysiol.00369.2012)
2. Kim W, Gilet T, Bush JWM. 2011 Optimal concentrations in nectar feeding. Proc. Natl Acad. Sci. USA 104, 20 167-20 172. (doi:10.1073/pnas. 1108642108)
3. Rennie EA, Turgeon R. 2009 A comprehensive picture of phloem loading strategies. Proc. Natl Acad. Sci. USA 106, 14 162-14 167. (doi:10.1073/ pnas.0902279106)
4. Windt CW, Vergeldt FJ, de Jager PA, van As H. 2006 MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ. 29, 1715-1729. (doi:10. 1111/j.1365-3040.2006.01544.x)
5. Jensen KH, Liesche J, Bohr T, Schulz A. 2012 Universality of phloem transport in seed plants. Plant Cell Environ. 35, 1065-1076. (doi:10.1111/ 1365-3040.2011.02472.x)
6. Pate J. 1976 Nutrients and metabolites of fluids recovered from xylem and phloem: significance in relation to long-distance transport in plants. In Transport and transfer processes in plants (eds IF Wardlaw, JB Passioura), pp. 253-281. New York, NY: Academic Press.
7. Munch E. 1930 Die Stoffbewegungen in der Pflanze. Jena: Gustav Fisher.
8. Knoblauch M, Peters WS. 2010 Munch, morphology, microfluidics: our structural problem with the phloem. Plant Cell Environ. 33, 1439-1452. (doi:10.1111/j.1365-3040.2010.02177.x)
9. Passioura JB. 1976 Translocation and the diffusion equation. In Transport and transfer processes in plants (eds IF Wardlaw, JB Passioura), pp. 357-361. New York, NY: Academic Press.
10. Lang A. 1978 A model of mass flow in the phloem. Aust. J. Plant Physiol. 5, 535-546. (doi:10.1071/ PP9780535)
11. Lide DR. 2012 CRC handbook of chemistry and physics. Boca Raton, FL: CRC Press.
12. MacRobbie EAC. 1971 Phloem translocation. Facts and mechanisms: a comparative survey. Biol. Rev. 46, 429-481. (doi:10.1111/j.1469-185X.1971. tb01053.x)
13. Horwitz L. 1958 Some simplified mathematical treatments of translocation in plants. Plant Physiol. 33, 81-93. (doi:10.1104/pp.33.2.81)
14. Minchin P, Thorpe M, Farrar J. 1993 A simple mechanistic model of phloem transport which explains sink priority. J. Exp. Bot. 44, 947-955. (doi:10.1093/jxb/44.5.947)
15. Thompson M, Holbrook NM. 2003 Application of a single-solute non-steady-state phloem model to the study of long-distance assimilate transport. J. Theor. Biol. 220, 419-455. (doi:10.1006/jtbi.2003.3115)
16. Pickard WF, Abraham-Shrauner B. 2009 A simplest steady-state Mu?nch-like model of phloem translocation, with source and pathway and sink. Func. Plant Biol. 36, 629-644. (doi:10.1071/ FP08278)
17. Lacointe A, Minchin PEH. 2008 Modelling phloem and xylem transport within a complex architecture. Func. Plant Biol. 35, 772-780. (doi:10.1071/ FP08085)
18. Pickard WF. 2012 Munch without tears: a steadystate Mu?nch-like model of phloem so simplified that it requires only algebra to predict the speed of translocation. Func. Plant Biol. 39, 531-537. (doi:10.1071/FP12004)
19. Jensen KH, Berg-Sørensen K, Friis SMM, Bohr T. 2012 Analytic solutions and universal properties of sugar loading models in Mu?nch phloem flow. J. Theor. Biol. 304, 286-296. (doi:10.1016/j.jtbi. 2012.03.012)
20. Murray CD. 1926 The physiological principle of minimum work: I. The vascular system and the cost of blood volume. Proc. Natl Acad. Sci. USA 12, 207-214. (doi:10.1073/pnas.12.3.207)
21. Sherman TF. 1981 On connecting large vessels to small. The meaning of Murray's law. J. Gen. Physiol. 78, 431-453. (doi:10.1085/jgp.78.4.431)
22. LaBarbera M. 1990 Principles of design of fluid transport systems in zoology. Science 249, 992-1000. (doi:10.1126/science.2396104)
23. Donato K, Hegsted DM. 1985 Efficiency of utilization of various sources of energy for growth. Proc. Natl Acad. Sci. USA 82, 4866-4870. (doi:10.1073/pnas.82.15.4866)
24. Ehlers K, Knoblauch M, van Bel AJE. 2000 Ultrastructural features of well-preserved and injured sieve elements: minute clamps keep the phloem transport conduits free for mass flow. Protoplasma 214, 80-92. (doi:10.1007/BF02524265)
25. Knoblauch M, Stubenrauch M, van Bel AJE, Peters WS. 2012 Forisome performance in artificial sieve tubes. Plant Cell Environ. 35, 1419-1427. (doi:10. 1111/j.1365-3040.2012.02499.x)
26. Hartig T. 1860 Beitrage zur physiologischen forstbotanik. Forst und Jagdzeitung 36, 257-263.
27. Crafts AS. 1939 The relation between structure and function of the phloem. Am. J. Bot. 26, 172-177. (doi:10.2307/2436534)
28. Hall SM, Baker DA, Milburn JA. 1971 Phloem transport of 14C-labelled assimilates in Ricinus. Planta 100, 200-207. (doi:10.1007/BF00387036)
29. Moose C. 1938 Chemical and spectroscopic analysis of phloem exudate and parenchyma sap from several species of plants. Plant Physiol. 13, 365-380. (doi:10.1104/pp.13.2.365)
30. Atkins C. 1999 Spontaneous phloem exudation accompanying abscission in Lupinus mutabilis (Sweet). J. Exp. Bot. 50, 805-812. (doi:10.1093/ jexbot/50.335.805)
31. Amiard V, Morvan-Bertrand A, Cliquet J-B, Billard J-P, Huault C, Sandstro?m JP, Prud'homme M-P. 2004 Carbohydrate and amino acid composition in phloem sap of Lolium perenne L. before and after defoliation. Can. J. Bot. 82, 1594-1601. (doi:10. 1139/b04-117)
32. Helden M, Tjallingh WF, Beek TA. 1994 Phloem sap collection from lettuce (Lactuca sativa L.): chemical comparison among collection methods. J. Chem. Ecol. 20, 3191-3206. (doi:10.1007/ BF02033720)
33. Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O. 2010 Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. Proc. Natl Acad. Sci. USA 107, 13 532-13 537. (doi:10.1073/pnas.0910558107)
34. Zhang C, Yu X, Ayre BG, Turgeon R. 2012 The origin and composition of cucurbit 'phloem' exudate. Plant Physiol. 158, 1873-1882. (doi:10.1104/pp. 112.194431)
35. Fisher DB, Frame JM. 1984 A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161, 385-393. (doi:10.1007/BF00394567)
36. Mittler TE. 1958 Studies on the feeding and nutrition of Tuberolachnus Salignus (Gmelin) (Homoptera, Aphididae) II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. J. Exp. Biol. 35, 74-84.
37. Peel AJ, Weatherly PE. 1959 Composition of sievetube sap. Nature 184, 1955-1956. (doi:10.1038/ 1841955a0)
38. Fukumorita T, Chino M. 1982 Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol. 23, 273-283.
39. Hayashi H, Chino M. 1986 Collection of pure phloem sap from wheat and its chemical composition. Plant Cell Physiol. 27, 1387-1393.
40. Fisher DB. 1983 Year-round collection of willow sieve-tube exudate. Planta 159, 529-533. (doi:10. 1007/BF00409142)
41. Zimmermann MH. 1961 Movement of organic substances in trees: photosynthates are translocated in a layer of bark only a fraction of a millimeter thick. Science 133, 73-79. (doi:10.1126/science. 133.3446.73)
42. Turgeon R, Wolf S. 2009 Phloem transport: cellular pathways and molecular trafficking. Annu. Rev. Plant Biol. 60, 207-221. (doi:10.1146/annurev. arplant.043008.092045)
43. Zimmermann MH. 1957 Translocation of organic substances in trees. II. On the translocation mechanism in the phloem of white ash (Fraxinus americana L.). Plant Physiol. 32, 399-404. (doi:10. 1104/pp.32.5.399)
44. Sandstro?m J, Telang A, Moran N. 2000 Nutritional enhancement of host plants by aphids: a comparison of three aphid species on grasses. J. Insect Physiol. 46, 33-40. (doi:10.1016/S0022-1910(99)00098-0)
45. Kallarackal J, Bauer SN, Nowak H, Hajirezaei M-R, Komor E. 2012 Diurnal changes in assimilate concentrations and fluxes in the phloem of castor bean (Ricinus communis L.) and tansy (Tanacetum vulgare L.). Planta 236, 209-223. (doi:10.1007/ s00425-012-1600-7)
46. Pescod KV, Quick WP, Douglas AE. 2007 Aphid responses to plants with genetically manipulated phloem nutrient levels. Physiol. Entomol. 32, 253-258. (doi:10.1111/j.1365-3032.2007.00577.x)
47. Hewer A, Will T, van Bel AJE. 2010 Plant cues for aphid navigation in vascular tissues. J. Exp. Biol. 213, 4030-4042. (doi:10.1242/jeb.046326)
48. Hoad G, Peel A. 1964 Studies on the movement of solutes between the sieve tubes and surrounding tissues in willow I. Interference between solutes and rate of translocation measurements. J. Exp. Bot. 16, 433-451. (doi:10.1093/jxb/16.3.433)
49. Smith JAC, Milburn JA. 1980 Osmoregulation and the control of phloem-sap composition in Ricinus communis L. Planta 148, 28-34. (doi:10.1007/ BF00385438)
50. Lang A. 1983 Turgor-regulated translocation. Plant Cell Environ. 6, 683-689.
51. Thompson M, Zwieniecki M. 2005 The role of potassium in long distance transport in plants. In Vascular transport in plants (eds NM Holbrook, MA Zwieniecki), pp. 221-240. Burlington, MA: Elsevier Academic Press.
52. Turgeon R. 2010 The puzzle of phloem pressure. Plant Physiol. 154, 578-581. (doi:10.1104/pp. 110.161679)
53. Pate J. 1973 Uptake, assimilation and transport of nitrogen compounds by plants. Soil Biol. Biochem. 5, 109-119. (doi:10.1016/0038-0717(73)90097-7)
54. Gamalei Y. 1989 Structure and function of leaf minor veins in trees and herbs. Trees 3, 96-110. (doi:10.1007/BF01021073)
55. Canny M. 1961 Measurements of the velocity of translocation. Ann. Bot. 25, 153-167.
56. Turgeon R, Medville R. 1998 The absence of phloem loading in willow leaves. Proc. Natl Acad. Sci. USA 95, 12 055-12 060. (doi:10.1073/pnas.95. 20.12055)
57. Vreugdenhil D, Koot-Gronsveld EAM. 1989 Measurements of pH, sucrose and potassium ions in the phloem sap of castor bean (Ricinus communis) plants. Physiol. Plantarum 77, 385-388. (doi:10. 1111/j.1399-3054.1989.tb05657.x)
58. Braun DM, Slewinski TL. 2009 Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol. 149, 71-81. (doi:10.1104/pp.108.129049)
59. Fu Q, Cheng L, Guo Y, Turgeon R 2011 Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol. 157, 1518-1527. (doi:10.1104/pp.111.184820)
60. Smith JAC, Milburn JA. 1980 Phloem transport, solute flux and the kinetics of sap exudation in Ricinus communis L. Planta 148, 35-41. (doi:10. 1007/BF00385439)
61. Deeken R, Geiger D, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Sauer N, May ST, Hedrich R. 2002 Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216, 334-344. (doi:10.1007/s00425-002-0895-1)
62. DeWitt ND, Harper JF, Sussman MR. 1991 Evidence for a plasma membrane proton pump in phloem cells of higher plants. Plant J. 1, 121-128. (doi:10. 1111/j.1365-313X.1991.00121.x)
63. Girousse C, Bonnemain J-L, Delrot S, Bournoville R. 1991 Sugar and amino acid composition of phloem sap of Medicago sativa: a comparative study of two collecting methods. Plant Physiol. Biochem. 29, 41-48.
64. Ziegler H. 1956 Untersuchungen U?ber die Leitung und Sekretion der Assimilate. Planta 47, 447-500. (doi:10.1007/BF01935416)
65. Pate J, Atkins C, Hamel K. 1979 Transport of organic solutes in phloem and xylem of a nodulated legume. Plant Physiol. 63, 1082-1088. (doi:10. 1104/pp.63.6.1082)
66. Canny M. 1973 Phloem translocation. London, UK: Cambridge University Press.
67. Rogers S, Peel AJ. 1975 Some evidence for the existence of turgor pressure gradients in the sieve tubes of willow. Planta 126, 259-267. (doi:10. 1007/BF00388967)
68. Hocking P. 1980 The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauca Grah.). Ann. Bot. 45, 633-643.
69. Kawabe S, Fukumorita T, Chino M. 1980 Collection of rice phloem sap from stylets of homopterous insects severed by YAG laser. Plant Cell Physiol. 21, 1319-1327.
70. Eom J-S, Choi S-B, Ward JM, Jeon J-S. 2012 The mechanism of phloem loading in rice (Oryza sativa). Mol. Cells 33, 431-438. (doi:10.1007/s10059-012- 0071-9)
71. Fisher DB, Gifford RM. 1986 Accumulation and conversion of sugars by developing wheat grains VI. Gradients along the transport pathway from the peduncle to the endosperm cavity during grain filling. Plant Physiol. 82, 1024-1030. (doi:10.1104/ pp.82.4.1024)
72. Zimmermann MH. 1962 Translocation of organic substances in trees. V. Experimental double interruption of phloem in white ash (Fraxinus americana L.). Plant Physiol. 37, 527-530. (doi:10. 1104/pp.37.4.527)
73. Merritt SZ. 1996 Within-plant variation in concentrations of amino acids, sugar, and sinigrin in phloem sap of black mustard, Brassica nigra (L.) Koch (Cruciferae). J. Chem. Ecol. 22, 1133-1145. (doi:10.1007/BF02027950)
74. Kuo-Sell H-L. 1989 Aminosauren und Zucker im Phloemsaft verschiedener Pflanzenteile von Hafer (Avena sativa) in Beziehung zur Saugortpraferenz von Getreideblattlausen (Hom, Aphididae). J. Appl. Entomol. 108, 54-63. (doi:10.1111/j.1439-0418. 1989.tb00432.x)
75. Riens B, Lohaus G, Heineke D, Heldt H. 1991 Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol. 97, 227-233. (doi:10.1104/pp.97.1.227)
76. Lohaus G, Winter H, Riens B, Heldt HW. 1995 Further studies of the phloem loading process in leaves of barley and spinach: the comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes. Botanica Acta 108, 270-275.
77. Pate J, Shedley E, Arthur D, Adams M. 1998 Spatial and temporal variations in phloem sap composition of plantation-grown Eucalyptus globulus. Oecologia 117, 312-322. (doi:10.1007/s004420050664)
78. Merchant A, Peuke AD, Keitel C, Macfarlane C, Warren CR, Adams MA. 2010 Phloem sap and leaf d13C,carbohydrates, and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment. J. Exp. Bot. 61, 1785-1793. (doi:10.1093/jxb/erq045)
79. Lohaus G, Hussmann M, Pennewiss K, Schneider H, Zhu JJ, Sattelmacher B. 2000 Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. J. Exp. Bot. 51, 1721-1732. (doi:10.1093/jexbot/51.351.1721)
80. Evert RF, Eschrich W, Heyser W. 1978 Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138, 279-294. (doi:10.1007/ BF00386823)
81. Weiner H, Blechschmidt-Schneider S, Mohme H, Eschrich W, Heldt H. 1991 Phloem transport of amino acids. Comparison of amino acid contents of maize leaves and of the sieve tube exudate. Plant Physiol. Biochem. 29, 19-23. (doi:10.1104. 97.1.227)
82. Ohshima T, Hayashi H, Chino M. 1990 Collection and chemical composition of pure phloem sap from Zeamays L. Plant Cell Physiol. 31, 735-737.
83. Winter H, Lohaus G, Heldt HW. 1992 Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol. 99, 996-1004. (doi:10.1104/pp.99.3.996)
84. Botha CEJ, Cross RHM. 1997 Plasmodesmatal frequency in relation to short-distance transport and phloem loading in leaves of barley (Hordeum vulgare). Phloem is not loaded directly from the symplast. Physiologia Plantarum 99, 355-362. (doi:10.1111/j.1399-3054.1997.tb00547.x)
85. Berthier A, Desclos M, Amiard V, Morvan-Bertrand A, Demmig-Adams B, Adams WW, Turgeon R, Prud'homme M-P, Noiraud-Romy N. 2009 Activation of sucrose transport in defoliated Lolium perenne L.: an example of apoplastic phloem loading plasticity. Plant Cell Physiol. 50, 1329-1344. (doi:10.1093/ pcp/pcp081)
86. Moing A, Carbonne F, Rashad MH, Gaudille're JP. 1992 Carbon fluxes in mature peach leaves. Plant Physiol. 100, 1878-1884. (doi:10.1104/ pp.100.4.1878)
87. Kehr J, Hustiak F, Walz C, Willmitzer L, Fisahn J. 1998 Transgenic plants changed in carbon allocation pattern display a shift in diurnal growth pattern. Plant J. 16, 497-503. (doi:10.1046/j.1365-313x. 1998.00318.x)
88. Turgeon R. 2010 The role of phloem loading reconsidered. Plant Physiol. 152, 1817-1823. (doi:10.1104/pp.110.153023)
89. Davidson A, Keller F, Turgeon R. 2011 Phloem loading, plant growth form, and climate. Protoplasma 248, 153-163. (doi:10.1007/s00709-010-0240-7)
90. Hill GP. 1962 Exudation from aphid stylets during the period from dormancy to bud break in Tilia americana (L.). J. Exp. Bot. 13, 144-151. (doi:10. 1093/jxb/13.1.144)
91. Hoffmann-Thoma G, van Bel AJE, Ehlers K. 2001 Ultrastructure of minor-vein phloem and assimilate export in summer and winter leaves of the symplasmically loading evergreens Ajuga reptans L, Aucuba japonica Thunb, and Hedera helix L. Planta 212, 231-242. (doi:10.1007/s004250000382)
92. Bachmann M, Matile P, Keller F. 1994 Metabolism of the raffinose family oligosaccharides in leaves ofAjuga reptans L. Cold acclimation, translocation, and sink to source transition: discovery of chain elongation enzyme. Plant Physiol. 105, 1335-1345.