Symplasmic networks in secondary vascular tissues: Parenchyma distribution and activity supporting long-distance transport

Journal of Experimental Botany

Volumn 65, Issue 7, 2014, Pages 1829-1848

  Spicer, Rachel ^a  

^a The Holleran Center for Community Action and Public Policy   (United States)

Author keywords

Cambium; contact cells; parenchyma; phloem; rays; xylem.

Indexed keywords

CYTOLOGY; MESOPHYLL CELL; METABOLISM; PHLOEM; PLANT; PLANT STEM; TRANSPORT AT THE CELLULAR LEVEL; XYLEM;

BIOLOGICAL TRANSPORT; MESOPHYLL CELLS; PHLOEM; PLANT STEMS; PLANTS; XYLEM;

EID: 84898848273     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert459     Document Type: Review

References (222)

1. Alferi FJ, Evert RF. 1968. Seasonal development of the secondary phloem in Pinus. American Journal of Botany 55, 518-528.
2. Alferi FJ, Kemp RI. 1983. The seasonal cycle of phloem development in Juniperus californica. American Journal of Botany 70, 891-896.
3. Alferi FJ, Mottola PM. 1983. Seasonal-changes in the phloem of Ephedra californica Wats. Botanical Gazette 144, 240-246.
4. Allen RM, Hiatt EN. 1994. Tissue culture of secondary xylem parenchyma of four species of southern pines. Wood and Fiber Science 26, 294-302.
5. +-ATPase of vessel-associated cells. Tree Physiology 24, 99-105.
6. +-ATPase in stem xylem of walnut during dormancy and growth resumption. Tree Physiology 27, 1471-1480.
7. +-ATPase, succinate and isocitrate dehydrogenases activities of vessel-associated cells in walnut trees. Journal of Plant Physiology 158, 1263-1271.
8. Angyalossy V, Angeles G, Pace MR, Lima AC, Dias-Leme CL, Lohmann LG, Madero-Vega C. 2012. An overview of the anatomy, development and evolution of the vascular system of lianas. Plant Ecology and Diversity 5, 167-182.
9. Apfel RE. 1972. The tensile strength of liquids. Scientifc American 227, 58-71.
10. +-ATPase of the wood ray parenchyma in poplar. Plant, Cell and Environment 27, 1288-1296.
11. +-ATPase and endogenous ion current during cambial growth in poplar plants. Plant Physiology 129, 1651-1663.
12. Bamber RK, Fukazawa K. 1985. Sapwood and heartwood: a review. Forest Products Abstracts 8, 265-278.
13. Barbaroux C, Breda N. 2002. Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiology 22, 1201-1210.
14. Barlow PW, Lueck J. 2006. Patterned cell development in the secondary phloem of dicotyledonous trees: a review and a hypothesis. Journal of Plant Research 119, 271-291.
15. Barnard DM, Lachenbruch B, McCulloh KA, Kitin P, Meinzer FC. 2013. Do ray cells provide a pathway for radial water movement in the stems of conifer trees? American Journal of Botany 100, 322-331.
16. Barnett JR, Cooper P, Bonner LJ. 1993. The protective layer as an extension of the apoplast. IAWA Bulletin 14, 163-171.
17. Bazot S, Barthes L, Blanot D, Fresneau C. 2013. Distribution of non-structural nitrogen and carbohydrate compounds in mature oak trees in a temperate forest at four key phenological stages. Trees 27, 1023-1034.
18. Bonsen KJM, Kucera LJ. 1990. Vessel occlusions in plants: morphological, functional and evolutionary aspects. IAWA Bulletin 11, 393-399.
19. Borchert R. 1994. Water status and development of tropical trees during seasonal drought. Trees 8, 115-125.
20. Boyce CK, Zwieniecki MA, Cody GD, Jacobsen C, Wirick S, Knoll AH, Holbrook NM. 2004. Evolution of xylem lignifcation and hydrogel transport regulation. Proceedings of the National Academy of Sciences, USA 101, 17555-17558.
21. Brandes A, Barros CF. 2008. Wood anatomy of eight liana species of Leguminosae family from Atlantic Rain Forest. Acta Botanica Brasilica 22, 465-480.
22. Braun HJ. 1970. Funktionelle histologie der sekundaaren sprossachse. I. Das Holz. Handbuch der Pfanzenanatomie (Encyclopedia of Plant Anatomy). Berlin: Borntraeger.
23. Braun HJ. 1984. The signifcance of the accessory tissues of the hydrosystem for osmotic water shifting as the 2nd principle of water ascent, with some thoughts concerning the evolution of trees. IAWA Bulletin 5, 275-294.
24. Brodersen C, McElrone A. 2013. Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in Plant Science 4, 108.
25. Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA. 2010. The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiology 154, 1088-1095.
26. Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDL. 2003. Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the reflling of embolized vessels. Plant, Cell and Environment 26, 1633-1645.
27. Bullock SH. 1992. Seasonal differences in nonstructural carbohydrates in two dioecious monsoon-climate trees. Biotropica 24, 140-145.
28. Butterfield BG, Meylan BA. 1982. Cell wall hydrolysis in the tracheary elements of the secondary xylem. In: Baas P, editor, New perspectives in wood anatomy. The Hague, Netherlands: Martinus Nijhoff Publishers, pp 71-84.
29. Canny MJ. 1995. A new theory for the ascent of sap-cohesion supported by tissue pressure. Annals of Botany 75, 343-357.
30. Canny MA. 1997. Vessel contents during transpiration-embolisms and reflling. American Journal of Botany 84, 1223-1230.
31. Canny MJ. 1998. Applications of the compensating pressure theory of water transport. American Journal of Botany 85, 897-909.
32. Canny MJ, Sparks JP, Huang CX, Roderick ML. 2007. Air embolisms exsolving in the transpiration water-the effect of constrictions in the xylem pipes. Functional Plant Biology 34, 95-111.
33. Carlquist S. 1991. Anatomy of vine and liana stems: a review and synthesis. In: Putz FE, Mooney HA, editors, The biology of vines. Cambridge, UK: Cambridge University Press, pp 53-71.
34. Carlquist S. 1998. Wood and bark anatomy of Caricaceae: correlations with systematics and habit. IAWA Journal 19, 191-206.
35. Carlquist S. 2001a. Axial parenchyma. In: Timell TW, editor, Comparative wood anatomy. Berlin: Springer-Verlag, pp 157-181.
36. Carlquist S. 2001b. Cambial variants (anomalous secondary growth). In: Timell TW, editor, Comparative wood anatomy. Berlin: Springer-Verlag, pp 271-295.
37. Carlquist S. 2007. Successive cambia revisited: ontogeny, histology diversity, and functional signifcance. Journal of the Torrey Botanical Society 134, 301-332.
38. Castro MA, Apostolo NM, De Magistris AA. 2005. Bark anatomy of Nothofagus species (Nothofagaceae) indigenous to the Andean-Patagonian forest, Argentina. Australian Journal of Botany 53, 69-79.
39. Castro MA, Apostolo NM, Navarro LE. 2006. Bark anatomy of three indigenous conifers from southern South America. Australian Journal of Botany 54, 73-82.
40. Chafe SC. 1974. Cell wall formation and 'protective layer' development in the xylem parenchyma of trembling aspen. Protoplasm 80, 335-354.
41. Chaffey N, Barlow P. 2001. The cytoskeleton facilitates a three-dimensional symplasmic continuum in the long-lived ray and axial parenchyma cells of angiosperm trees. Planta 213, 811-823.
42. Chapotin SM, Razanameharizaka JH, Holbrook NM. 2006a. Baobab trees (Adansonia) in Madagascar use stored water to fush new leaves but not to support stomatal opening before the rainy season. New Phytologist 169, 549-559.
43. Chapotin SM, Razanameharizaka JH, Holbrook NM. 2006b. A biomechanical perspective on the role of large stem volume and high water content in baobab trees (Adansonia spp.; Bombacaceae). American Journal of Botany 93, 1251-1264.
44. Chapotin SM, Razanameharizaka JH, Holbrook NM. 2006c. Water relations of baobab trees (Adansonia spp. L.) during the rainy season: does stem water buffer daily water defcits? Plant, Cell and Environment 29, 1021-1032.
45. Chattaway MM. 1949. The development of tyloses and secretion of gum in heartwood formation. Australian Journal of Scientifc Research B 2, 227-240.
46. Chattaway M. 1951. Morphological and functional variations in the rays of pored timbers. Australian Journal of Biological Sciences 4, 12-27.
47. Chattaway M. 1952. The sapwood-heartwood transition. Australian Forestry 16, 25-34.
48. Choat B, Cobb AR, Jansen S. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytologist 177, 608-625.
49. Chowdhury KA. 1936. Terminal and initial parenchyma cells in the wood of Terminalia tomentosa W. A. New Phytologist 35, 351-358.
50. Comstock JP. 1999. Why Canny's theory doesn't hold water. American Journal of Botany 86, 1077-1081.
51. Czaninski Y. 1977. Vessel-associated cells. IAWA Bulletin 3, 51-55.
52. Decourteix M, Alves G, Bonhomme M, et al. 2008. Sucrose (JrSUT1) and hexose (JrHT1 and JrHT2) transporters in walnut xylem parenchyma cells: their potential role in early events of growth resumption. Tree Physiology 28, 215-224.
53. Decourteix M, Alves G, Brunel N, Ameglio T, Guilliot A, Lemoine R, Petel G, Sakr S. 2006. JrSUT1, a putative xylem sucrose transporter, could mediate sucrose infux into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.). Plant, Cell and Environment 29, 36-47.
54. den Outer RW. 1983. Comparative-study of the secondary phloem of some woody dicotyledons Acta Botanica Neerlandica 32, 29-38.
55. den Outer RW. 1993. Evolutionary trends in secondary phloem anatomy of trees, shrubs and climbers from Africa (mainly Ivory Coast). Acta Botanica Neerlandica 42, 269-287.
56. De Schepper V, Steppe K. 2010. Development and verifcation of a water and sugar transport model using measured stem diameter variations. Journal of Experimental Botany 61, 2083-2099.
57. De Schepper V, Steppe K, Van Labeke MC, Lemeur R. 2010. Detailed analysis of double girdling effects on stem diameter variations and sap fow in young oak trees. Environmental and Experimental Botany 68, 149-156.
58. DeSmidt WJ. 1922. Studies of the distribution and volume of the wood rays in slippery elm (Ulmus fulva Michx.). Journal of Forestry 20, 352-362.
59. Dickson RE, Vogelmann TC, Larson PR. 1985. Glutamine transfer from xylem to phloem and translocation to developing leaves of Populus deltoides. Plant Physiology 77, 412-417.
60. Dobbins DR, Fisher JB. 1986. Wound responses in girdled stems of lianas. Botanical Gazette 147, 278-289.
61. Dute R, Patel J, Jansen S. 2010. Torus-bearing pit membranes in Cercocarpus. IAWA Journal 31, 53-66.
62. Eames AJ, MacDaniels LH. 1947. Secondary phloem. In: Sinnott EW, editor, An introduction to plant anatomy. New York: McGraw-Hill Book Company, pp 231-247.
63. Ehlers K, van Bel AJE. 2010. Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231, 371-385.
64. Esau K. 1948. Phloem structure in grapevine, and its seasonal changes. Hilgardia 18, 217-296.
65. Esau K. 1950. Development and structure of the phloem tissue. II. Botanical Review 16, 67-114.
66. Esau K. 1964. Structure and development of bark in dicotyledons. In: Zimmermann MH, editor, The formation of wood in forest trees. New York: Academic Press, pp 37-50.
67. Evert RF. 1961. Seasonal changes in phloem of Pyrus malus. American Journal of Botany 48, 533 et seq.
68. Evert RF. 1963a. The cambium and seasonal development of the phloem in Pyrus malus. American Journal of Botany 50, 149-159.
69. Evert RF. 1963b. Ontogeny and structure of the secondary phloem in Pyrus malus. American Journal of Botany 50, 8-37.
70. Evert RF. 2006. Phloem: secondary phloem and variations in its structure. Esau's plant anatomy. Hoboken, New Jersey: John Wiley and Sons, pp 407-445.
71. Fahn A, Zimmermann MH. 1982. Development of the successive cambia in Atriplex halimus (Chenopodiaceae). Botanical Gazette 143, 353-357.
72. Fink VS. 1982. Histochemical investigations on starch-distribution and activity of acid phosphatases in the xylem of some tropical tree species. Holzforschung 36, 295-302.
73. Fischer C, Höll W. 1991. Food reserves of Scots pine (Pinus sylvestris L.) I. Seasonal changes in the carbohydrate and fat reserves of pine needles. Trees 5, 187-195.
74. Fischer C, Höll W. 1992. Food reserves of scots pine (Pinus sylvestris L.) II. Seasonal changes and radial distribution of carbohydrate and fall reserves in pine wood. Trees 6, 147-155.
75. Fisher JB. 1981. Wound healing by exposed secondary xylem in Adansonia (Bombacaceae). IAWA Bulletin 2, 193-199.
76. Fisher JB, Ewers FW. 1989. Wound healing in stems of lianas after twisting and girdling injuries. Botanical Gazette 150, 251-265.
77. Fisher JB, Ewers FW. 1991. Structural responses to stem injury in vines. In: Putz FE, Mooney HA, editors, The biology of vines. Cambridge, UK: Cambridge University Press, pp 99-124.
78. Foster RC. 1967. Fine structure of tyloses in three species of the Myrtaceae. Australian Journal of Botany 15, 25-34.
79. Fromard L, Babin V, Fleurat-Lessard P, Fromont J-C, Serrano R, Bonnemain J-L. 1995. Control of vascular sap pH by the vessel-associated cells in woody species. Plant Physiology 108, 913-918.
80. Fu QS, Cheng LL, Guo YD, Turgeon R. 2011. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiology 157, 1518-1527.
81. Fuchs M, Ehlers K, Will T, van Bel AJE. 2010a. Immunolocalization indicates plasmodesmal traffcking of storage proteins during cambial reactivation in Populus nigra. Annals of Botany 106, 385-394.
82. Fuchs M, van Bel AJE, Ehlers K. 2010b. Season-associated modifcations in symplasmic organization of the cambium in Populus nigra. Annals of Botany 105, 375-387.
83. Fuchs M, van Bel AJE, Ehlers K. 2011. Do symplasmic networks in cambial zones correspond with secondary growth patterns? Protoplasma 248, 141-151.
84. Gamalei Y. 1989. Structure and function of leaf minor veins in trees and herbs: a taxonomic review. Trees 3, 96-110.
85. Gartner BL. 1991. Structural stability and architecture of vines vs. shrubs of poison oak, Toxicodendron diversilobum. Ecology 72, 2005-2015.
86. Gasco A, Nardini A, Gortan E, Salleo S. 2006. Ion-mediated increase in the hydraulic conductivity of laurel stems: role of pits and consequences for the impact of cavitation on water transport. Plant, Cell and Environment 29, 1946-1955.
87. Goodsman DW, Lusebrink I, Landhausser SM, Erbilgin N, Lieffers VJ. 2013. Variation in carbon availability, defense chemistry and susceptibility to fungal invasion along the stems of mature trees. New Phytologist 197, 586-594.
88. Gregory RA, Wargo PM. 1986. Timing of defoliation and its effect on bud development, starch reserves, and sap sugar concentration in sugar maple. Canadian Journal of Forest Research 16, 10-17.
89. Grillos SJ, Smith FH. 1959. The secondary phloem of Douglas fr. Forest Science 5, 377-388.
90. Hafke JB, van Amerongen JK, Kelling F, Furch ACU, Gaupels F, van Bel AJE. 2005. Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiology 138, 1527-1537.
91. Harms U, Sauter JJ. 1991. Storage proteins in the wood of Taxodiaceae and of Taxus. Journal of Plant Physiology 138, 497-499.
92. Harms U, Sauter JJ. 1992. Localization of a storage protein in the wood ray parenchyma cells of Taxodium distichum (l) Rich, l.c. by immunogold labeling. Trees 6, 37-40.
93. Hearn DJ. 2009a. Descriptive anatomy and evolutionary patterns of anatomical diversifcation in Adenia (Passiforaceae). Aliso 27, 13-38.
94. Hearn DJ. 2009b. Developmental patterns in anatomy are shared among separate evolutionary origins of stem succulent and storage root-bearing growth habits in Adenia (Passiforaceae). American Journal of Botany 96, 1941-1956.
95. Hearn DJ, Poulsen T, Spicer R. 2013. The evolution of growth forms with expanded root and shoot parenchymatous storage is correlated across the eudicots. International Journal of Plant Sciences 174, 1049-1061.
96. Hoch G, Popp M, Korner C. 2002. Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98, 361-374.
97. Hoch G, Richter A, Korner C. 2003. Non-structural carbon compounds in temperate forest trees. Plant, Cell and Environment 26, 1067-1081.
98. Holbrook NM, Zwieniecki MA. 1999. Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120, 1-4.
99. Höll W. 1975. Radial transport in rays. In: Zimmermann MH, Milburn JA, editors, Transport in Plants I. Phloem Transport. Berlin, Heidelburg, New York: Springer-Verlag, pp 432-450.
100. Höll W. 1985. Seasonal fuctuation of reserve materials in the trunkwood of spruce [Picea abies (L.) Karst.]. Journal of Plant Physiology 117, 355-362.
101. Höll W. 2000. Distribution, fuctuation and metabolism of food reserves in the wood of trees. In: Savidge R, Barnett J, Napier R, editors, Cell and molecular biology of wood formation. Oxford: BIOS Scientifc Publishers, pp 347-362.
102. Holtta T, Vesala T, Sevanto S, Peramaki M, Nikinmaa E. 2006. Modeling xylem and phloem water fows in trees according to cohesion theory and Munch hypothesis. Trees 20, 67-78.
103. Imaji A, Seiwa K. 2010. Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species. Oecologia 162, 273-281.
104. Jane FW. 1934. Terminal and initial parenchyma in wood. Nature 133, 534.
105. Kasuga J, Arakawa K, Fujikawa S. 2007. High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytologist 174, 569-579.
106. Kim JK, Daniel G. 2013. Developmental localization of homogalacturonan and xyloglucan epitopes in pit membranes varies between pit types in two poplar species. IAWA Journal 34, 245-262.
107. Kozlowski TT. 1992. Carbohydrate sources and sinks in woody-plants. Botanical Review 58, 107-222.
108. Kuroda K, Kasuga J, Arakawa K, Fujikawa S. 2003. Xylem ray parenchyma cells in boreal hardwood species respond to subfreezing temperatures by deep supercooling that is accompanied by incomplete dessication. Plant Physiology 131, 736-744.
109. Lahr EC, Krokene P. 2013. Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PloS One 8, 8 e72405.
110. Landhausser SM, Lieffers VJ. 2003. Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees 17, 471-476.
111. Landhausser SM, Lieffers VJ. 2012. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26, 653-661.
112. Langheinrich U, Tischner R. 1991. Vegetative storage proteins in poplar-induction and characterization of a 32-kilodalton and a 36-kilodalton polypeptide. Plant Physiology 97, 1017-1025.
113. Larson PR. 1994. The vascular cambium: development and structure. Berlin: Springer-Verlag.
114. Latt CR, Nair PKR, Kang BT. 2001. Reserve carbohydrate levels in the boles and structural roots of fve multipurpose tree species in a seasonally dry tropical climate. Forest Ecology and Management 146, 145-158.
115. Lawrence SD, Greenwood JS, Korhnak TE, Davis JM. 1997. A vegetative storage protein homolog is expressed in the growing shoot apex of hybrid poplar. Planta 203, 237-244.
116. Magel EA. 2000. Biochemistry and physiology of heartwood formation. In: Savidge R, Barnett J, Napier R, editors, Cell and molecular biology of wood formation. Oxford: BIOS Scientifc Publishers, pp 363-376.
117. Mayr S, Sperry JS. 2010. Freeze-thaw-induced embolism in Pinus contorta: centrifuge experiments validate the 'thaw-expansion hypothesis' but confict with ultrasonic emission data. New Phytologist 185, 1016-1024.
118. McCulloh KA, Johnson DM, Meinzer FC, Lachenbruch B. 2011. An annual pattern of native embolism in upper branches of four tall conifer species. American Journal of Botany 98, 1007-1015.
119. Mencuccini M, Holtta T, Sevanto S, Nikinmaa E. 2013. Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal. New Phytologist 198, 1143-1154.
120. Meyer RW, Cote WG. 1968. Formation of the protective layer and its role in tylosis development. Wood Science and Technology 2, 84-94.
121. Mooney HA, Chu C, Bullock SH, Robichaux R. 1992. Carbohydrate, water and nitrogen storage in vines of a tropical deciduous forest. Biotropica 24, 134-139.
122. Murakami Y, Funada R, Sano Y, Ohtani J. 1999. The differentiation of contact cells and isolation cells in the xylem parenchyma of Populus maximowiczii. Annals of Botany 84, 429-435.
123. Myer JE. 1922. Ray volumes of the commercial woods of the United States and their signifcance. Journal of Forestry 20, 337-351.
124. 2+ in the sap. Journal of Experimental Botany 58, 2609-2615.
125. Newell EA, Mulkey SS, Wright SJ. 2002. Seasonal patterns of carbohydate storage in four tropical tree species. Oecologia 131, 333-342.
126. O'Brien T P. 1970. Further observations on hydrolysis of the cell wall in the xylem. Protoplasma 69, 1-14.
127. O'Brien TP, Thimann KV. 1967. Observations on the fne structure of the oat coleoptile III. Correlated light and electron microscopy of the vascular tissues. Protoplasma 63, 443-478.
128. Offer CE, McCurdy DW, Patrick JW, Talbot MJ. 2003. Transfer cells: cells specialized for a special purpose. Annual Review of Plant Biology 54, 431-454.
129. Pace MR, Lohmann LG, Angyalossy V. 2009. The rise and evolution of the cambial variant in Bignonieae (Bignoniaceae). Evolution and Development 11, 465-478.
130. Pace MR, Lohmann LG, Angyalossy V. 2011. Evolution of disparity between the regular and variant phloem in Bignonieae (Bignoniaceae). American Journal of Botany 98, 602-618.
131. Panshin AJ, de Zeeuw C. 1980. Textbook of wood technology. Part 1. Formation, anatomy, and properties of wood. New York: McGraw-Hill.
132. Pate JS. 1975. Exchange of solutes between phloem and xylem and circulation in the whole plant. In: Zimmermann MH, Milburn JA, editors, Transport in plants I. Phloem transport. Berlin, Heidelburg, New York: Springer-Verlag, pp 451-473.
133. Pate JS, Dixon KW. 1981. Plants with feshy underground storage organs-a Western Australia survey. In: Pate JS, McComb AJ, editors, The biology of Australian plants. Nedlands: University of Western Australia Press, pp 181-215.
134. Pate JS, Gunning BES. 1972. Transfer cells. Annual Review of Plant Physiology 23, 173-196.
135. Pate JS, Jeschke WD. 1995. The role of stems in transport, storage, and circulation of ions and metabolites by the whole plant. In: Gartner B, editor, Plant stems. San Diego, CA: Academic Press, pp 177-204.
136. Perrone I, Pagliarani C, Lovisolo C, Chitarra W, Roman F, Schubert A. 2012. Recovery from water stress affects grape leaf petiole transcriptome. Planta 235, 1383-1396.
137. Phillips EWJ. 1941. The identifcation of coniferous woods by their microscopic structure. Journal of the Linnean Society of London, Botany 52, 259-320.
138. Plavcova L, Hacke UG. 2011. Heterogeneous distribution of pectin epitopes and calcium in different pit types of four angiosperm species. New Phytologist 192, 885-897.
139. Putz FE, Holbrook NM. 1991. Biomechanical studies of vines. In: Putz FE, Mooney HA, editors, The biology of vines. Cambridge, UK: Cambridge University Press, pp 73-97.
140. Rajput KS, Fiamengui MB, Marcati CR. 2012a. Stem anatomy and development of successive cambia in the neotropical liana Securidaca rivinifolia (Polygalaceae). IAWA Journal 33, 391-402.
141. Rajput KS, Nunes OM, Brandes AFN, Tamaio N. 2012b. Development of successive cambia and pattern of secondary growth in the stem of the neotropical liana Rhynchosia phaseoloides (SW.) DC. (Fabaceae). Flora 207, 607-614.
142. Rajput KS, Raole VM, Gandhi D. 2008. Radial secondary growth and formation of successive cambia and their products in Ipomoea hederifolia L. (Convolvulaceae). Botanical Journal of the Linnean Society 158, 30-40.
143. Rajput KS, Romeiro D, Longui EL, Marcati CR. 2012c. Development of successive cambia and structure of wood in Gallesia integrifolia (Spreng.) Harms (Phytolaccaceae). Trees 26, 1943-1950.
144. Rennie EA, Turgeon R. 2009. A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences, USA 106, 14162-14167.
145. Rioux D, Nicole M, Simard M, Ouellette GB. 1988. Immunocytochemical evidence that secretion of pectin occurs during gel (gum) and tylosis formation in trees. Phytopathology 88, 494-505.
146. Robert EMR, Schmitz N, Boeren I, Driessens T, Herremans K, De Mey J, Van de Casteele E, Beeckman H, Koedam N. 2011. Successive cambia: a developmental oddity or an adaptive structure? Plos One 6.
147. Rudelle J, Octave S, Kaid-Harche M, Roblin G, Fleurat-Lessard P. 2005. Structural modifcations induced by Eutypa lata in the xylem of trunk and canes of Vitis vinifera. Functional Plant Biology 32, 537-547.
148. Sakr S, Alves G, Morillon RL, Maurel K, Decourteix M, Guilliot A, Fleurat-Lessard P, Julien JL, Chrispeels MJ. 2003. Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiology 133, 630-641.
149. Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186, 274-281.
150. Salleo S, Lo Gullo MA, De Paoli D, Zippo M. 1996. Xylem recovery from cavitation-induced embolism plants of Laurus nobilis: a possible mechanism. New Phytologist 132, 47-56.
151. Salleo S, Lo Gullo MA, Triflo P, Nardini A. 2004. New evidence for a role of vessel-associated cells and phloem in the rapid xylem reflling of cavitated stems of Lauris nobilis, L. Plant, Cell and Environment 27, 1065-1076.
152. Salleo S, Triflo P, Esposito S, Nardini A, Lo Gullo MA. 2009. Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Functional Plant Biology 36, 815-825.
153. Salleo S, Triflo P, Lo Gullo MA. 2006. Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel). Functional Plant Biology 33, 1063-1074.
154. Santiago M, Pagay V, Stroock AD. 2013. Impact of electroviscosity on the hydraulic conductance of the bordered pit membrane: a theoretical investigation. Plant Physiology 163, 999-1011.
155. Sauter JJ. 1980. The Strasburger cells-equivalents of companion cells. Berichte der Deutschen Botanischen Gesellschaft 93, 29-42.
156. Sauter JJ. 2000. Photosynthate allocation to the vascular cambium: facts and problems. In: Savidge R, Barnett J, Napier R, editors, Cell and molecular biology of wood formation. Oxford: BIOS Scientifc Publishers, pp 71-83.
157. Sauter JJ, Dorr I, Kollmann R. 1976. Ultrastructure of Strasburger cells (= albuminous cells) in secondary phloem of Pinus nigra var. austriaca (Hoess) Badoux. Protoplasma 88, 31-49.
158. Sauter JJ, Kloth S. 1986. Plasmodesmatal frequency and radial translocation rates in ray cells of popular (Populus × Canadensis Moench 'robusta'). Planta 168, 337-380.
159. Sauter JJ, Kloth S. 1987. Changes in carbohydrates and ultrastructure in xylem ray cells of Populus in response to chilling. Protoplasma 137, 45-55.
160. Sauter JJ, Neumann U. 1994. The accumulation of storage materials in ray cells of poplar wood (Populus × canadensis robusta)-effect of ringing and defoliation. Journal of Plant Physiology 143, 21-26.
161. Sauter JJ, van Cleve B. 1989. Immunochemical localization of a willow storage protein with a poplar storage protein antibody. Protoplasma 149, 175-177.
162. Sauter JJ, van Cleve B. 1994. Storage, mobilization and interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees 8, 297-304.
163. Sauter JJ, van Cleve B, Apel K. 1988. Protein bodies in ray cells of Populus × canadensis Moench robusta. Planta 173, 31-34.
164. Sauter JJ, van Cleve B, Wellenkamp S. 1989. Ultrastructural and biochemical results on the localization and distribution of storage proteins in a poplar tree and in twigs of other tree species. Holzforschung 43, 1-6.
165. Sauter JJ, Wellenkamp S. 1998. Seasonal changes in content of starch, protein and sugars in the twig wood of Salix caprea L. Holzforschung 52, 255-262.
166. Sauter JJ, Wisniewski M, Witt W. 1996. Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus × canadensis Moench robusta) wood. Journal of Plant Physiology 149, 451-461.
167. Schaffer K, Wisniewski M. 1989. Development of the amorphous layer (protective layer) in xylem parenchyma of cv. Golden Delicious apple, cv. Loring peach, and willow. American Journal of Botany 76, 1569-1582.
168. Schmid R, Machado R. 1968. Pit membranes in hardwoods-fne structure and development. Protoplasma 66, 185-204.
169. Schneider H. 1955. Ontogeny of lemon tree bark. American Journal of Botany 42, 893-905.
170. Secchi F, Gilbert ME, Zwieniecki MA. 2011. Transcriptome response to embolism formation in stems of Populus trichocarpa provides insight into signaling and the biology of reflling. Plant Physiology 157, 1419-1429.
171. Secchi F, Zwieniecki MA. 2010. Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of reflling process. Plant, Cell and Environment 33, 1285-1297.
172. Secchi F, Zwieniecki MA. 2011. Sensing embolism in xylem vessels: the role of sucrose as a trigger for reflling. Plant, Cell and Environment 34, 514-524.
173. Secchi F, Zwieniecki MA. 2012. Analysis of xylem sap from functional (nonembolized) and nonfunctional (embolized) vessels of Populus nigra: chemistry of reflling. Plant Physiology 160, 955-964.
174. Sevanto S, Holtta T, Holbrook NM. 2011. Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. Plant, Cell and Environment 34, 690-703.
175. Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. 2013. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell and Environment 37, 153-161.
176. Shigo AL. 1984. Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Annual Review of Phytopathology 22, 189-214.
177. Sokolowska K, Zagorska-Marek B. 2012. Symplasmic, longdistance transport in xylem and cambial regions in branches of Acer pseudoplatanus (Aceraceae) and Populus tremula × P. tremuloides (Salicaceae). American Journal of Botany 99, 1745-1755.
178. Sperry J. 2013. Cutting-edge research or cutting-edge artefact? An overdue control experiment complicates the xylem reflling story. Plant, Cell and Environment 36, 1916-1918.
179. Sperry JS, Tyree MT. 1988. Mechanism of water stress-induced xylem embolism. Plant Physiology 88, 581-587.
180. Spicer R. 2005. Senescence in secondary xylem: heartwood formation as an active developmental program. In: Holbrook NM, Zwieniecki MA, editors, Vascular transport in plants. Boston: Elsevier, pp 457-475.
181. Spicer R, Holbrook NM. 2005. Within-stem oxygen concentration and sap fow in four temperate tree species: does long-lived xylem parenchyma experience hypoxia? Plant, Cell and Environment 28, 192-201.
182. Spicer R, Holbrook NM. 2007. Parenchyma cell respiration and survival in secondary xylem: does metabolic activity decline with cell age? Plant, Cell and Environment 30, 934-943.
183. Stepien V, Sauter JJ, Martin F. 1994. Vegetative storage proteins in woody-plants. Plant Physiology and Biochemistry 32, 185-192.
184. Stiller V, Sperry JS. 1999. Canny's compensating pressure theory fails a test. American Journal of Botany 86, 1082-1086.
185. Takata N, Kasuga J, Takezawa D, Arakawa K, Fujikawa S. 2007. Gene expression associated with increased supercooling capability in xylem parenchyma cells of larch (Larix kaempferi). Journal of Experimental Botany 58, 3731-3742.
186. Thompson MV. 2006. Phloem: the long and the short of it. Trends in Plant Science 11, 26-32.
187. Turgeon R. 2010. The puzzle of phloem pressure. Plant Physiology 154, 578-581.
188. Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 19-38.
189. Utsumi Y, Sano Y, Fujikawa S, Funada R, Ohtani J. 1998. Visualization of cavitated vessels in winter and reflled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy. Plant Physiology 117, 1463-1471.
190. van Bel AJE. 1990. Xylem-phloem exchange via the rays: the undervalued route of transport. Journal of Experimental Botany 41, 631-644.
191. van Bel AJE. 1995. The low profile directors of carbon and nitrogen economy in plants: parenchyma associated with translocation channels. In: Gartner B, editor, Plant stems. San Diego, CA: Academic Press, pp 205-222.
192. van Bel AJE. 1996. Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with associated physiological software packages in dicotyledons. Journal of Experimental Botany 47, 1129-1140.
193. van Bel AJE, Ehlers K. 2000. Symplasmic organization of the transport phloem and the implications for photosynthate transfer to the cambium. In: Savidge R, Barnett J, Napier R, editors, Cell and molecular biology of wood formation. Oxford: BIOS Scientifc Publishers, pp 85-99.
194. van Bel AJE, Kempers R. 1991. Symplastic isolation of the sieve element-companion cell complex in the phloem of Ricinus communis and Salix alba stems. Planta 183, 69-76.
195. van Bel AJE, Mostert E, Borstlap AC. 1979. Kinetics of L-alanine escape from xylem vessels. Plant Physiology 63, 244-247.
196. van Bel AJE, van der Schoot C. 1979. Xylem-to-phloem and the primary distribution of amino-acids in tomato plants. Plant Physiology 63, 45-45.
197. van Bel AJE, van der Schoot C. 1988. Primary function of the protective layer in contact cells-buffer against oscillations in hydrostatic-pressure in the vessels. IAWA Journal 9, 285-288.
198. van Bel AJE, van Rijen HVM. 1994. Microelectrode-recorded development of the symplasmic autonomy of the sieve element companion cell complex in the stem phloem of Lupinus luteus. Planta 192, 165-175.
199. van Cleve B, Just J, Sauter JJ. 1991. Poplar storage protein in xylem sap. Journal of Plant Physiology 137, 763-764.
200. van der Schoot C, van Bel AJE. 1989a. Architecture of the internodal xylem of tomato (Solanum lycopersicum) with reference to longitudinal and lateral transfer. American Journal of Botany 76, 487-503.
201. van der Schoot C, van Bel AJE. 1989b. Morphogram-a novel diagram to organize the transitive secondary xylem elements of basal tomato (Solanum lycopersicum) internodes. American Journal of Botany 76, 475-486.
202. van der Schoot C, van Bel AJE. 1990. Mapping membrane-potential differences and dye-coupling in internodal tissues of tomato (Solanum lycopersicon L.). Planta 182, 9-21.
203. van Doorn WG, Hiemstra T, Fanourakis D. 2011. Hydrogel regulation of xylem water fow: an alternative hypothesis. Plant Physiology 157, 1642-1649.
204. van Ieperen W. 2007. Ion-mediated changes of xylem hydraulic resistance in planta: fact or fction? Trends in Plant Science 12, 137-142.
205. van Ieperen W, van Gelder A. 2006. Ion-mediated fow changes suppressed by minimal calcium presence in xylem sap in Chrysanthemum and Prunus laurocerasus. Journal of Experimental Botany 57, 2743-2750.
206. van Ieperen W, van Meeteren U, van Gelder H. 2000. Fluid ionic composition infuences hydraulic conductance of xylem conduits. Journal of Experimental Botany 51, 769-776.
207. Vogelmann TC, Dickson RE, Larson PR. 1985. Comparative distribution and metabolism of xylem-borne amino-compounds and sucrose in shoots of Populus deltoides. Plant Physiology 77, 418-428.
208. Wargo MP. 1977. Wound closure in sugar maples: adverse effects of defoliation. Canadian Journal of Forest Research 7, 410-414.
209. Wetzel S, Greenwood JS. 1991. The 32-kilodalton vegetative storage protein of Salix microstachya Turz-characterization and immunolocalizations. Plant Physiology 97, 771-777.
210. Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM. 2013. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell and Environment 36, 1938-1949.
211. Wisniewski M, Davis G. 1989. Evidence for the involvement of a specifc cell wall layer in regulation of deep supercooling of xylem parenchyma. Plant Physiology 91, 151-156.
212. Wisniewski M, Davis G, Arora R. 1991. Effect of macerase, oxalic-acid, and EGTA on deep supercooling and pit membrane-structure of xylem parenchyma of peach. Plant Physiology 96, 1354-1359.
213. Wong BL, Baggett KL, Rye AH. 2003. Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Canadian Journal of Botany-Revue Canadienne De Botanique 81, 780-788.
214. Wurth MKR, Pelaez-Riedl S, Wright SJ, Korner C. 2005. Non-structural carbohydrate pools in a tropical forest. Oecologia 143, 11-24.
215. Zahur MS. 1959. Comparative study of secondary phloem of 423 species of woody dicotyledons belonging to 85 families. Cornell University Agricultural Experiment Station, Memoir 358, 122-160.
216. Zimmermann MH. 1978. Hydraulic architecture of some diffuse-porous trees. Canadian Journal of Botany 56, 2286-2295.
217. Zwieniecki MA, Holbrook NM. 1998. Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant, Cell and Environment 21, 1173-1180.
218. Zwieniecki MA, Holbrook NM. 2009. Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends in Plant Science 14, 530-534.
219. Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM. 2000. Dynamic changes in petiole specifc conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca). Plant, Cell and Environment 23, 407-414.
220. Zwieniecki MA, Melcher PJ, Feild TS, Holbrook NM. 2004. A potential role for xylem-phloem interactions in the hydraulic architecture of trees: effects of phloem girdling on xylem hydraulic conductance. Tree Physiology 24, 911-917.
221. Zwieniecki MA, Melcher PJ, Holbrook NM. 2001. Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059-1062.
222. Zwieniecki MA, Orians CM, Melcher PJ, Holbrook NM. 2003. Ionic control of the lateral exchange of water between vascular bundles in tomato. Journal of Experimental Botany 54, 1399-1405.