EARLYWOOD VESSELS in RING-POROUS TREES BECOME FUNCTIONAL for WATER TRANSPORT after BUD BURST and before the MATURATION of the CURRENT-YEAR LEAVES

IAWA Journal

Volumn 37, Issue 2, 2016, Pages 315-331

  Kitin, Peter ^a,b   Funada, Ryo ^c  

^a FOREST PRODUCTS LABORATORY   (United States)

^b Madison Area Technical College   (United States)

^c TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Deciduous; earlywood; functional ecology; Kalopanax; phenology; ring porous; tree ring; vessel maturation; xylem formation

Indexed keywords

EID: 84977265970     PISSN: 09281541     EISSN: 22941932     Source Type: Journal    
DOI: 10.1163/22941932-20160136     Document Type: Article

References (76)

1. Aloni R & Peterson CA. 1997. Auxin promotes dormancy callose removal from the phloem of Magnolia kobus and callose accumulation and earlywood vessel differentiation in Quercus robur. J. Plant Research 110: 37-44.
2. Atkinson CJ & Denne MP. 1988. Reactivation of vessel production in ash (Fraxinus excelsior L.) trees. Ann. Bot. 61: 679-688.
3. Baas P. 1976. Some functional and adaptive aspects of vessel member morphology. In: Baas P, Bolton AJ & Catling DM (eds.), Wood structure in biological and technological research. Leiden Botanical Series No 3: 157-181. Leiden University Press.
4. Barnett JR. 1992. Reactivation of the cambium in Aesculus hippocastanum L.: a transmission electron microscope study. Ann. Bot. 70: 169-177.
5. Beeckman H. 2016. Wood anatomy and trait-based ecology. IAWA J. 37: 127-151.
6. Begum S, Nakaba S, Oribe Y, Kubo T & Funada R. 2007. Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann. Bot. 100: 439-447.
7. Begum S, Nakaba S, Yamagishi Y, Oribe Y & Funada R. 2013. Regulation of cambial activity in relation to environmental conditions: understanding the role of temperature in wood formation of trees. Physiologia Plantarum 147: 46-54.
8. Bräuning A, De Ridder M, Zafirov N, García-González I, Dimitrov DP & Gärtner H. 2016. Tree-ring features-indicators of extreme event impacts. IAWA J. 37: 206-231.
9. Butterfield BG & Meylan BA. 1982. Cell wall hydrolysis in the tracheary elements of the secondary xylem. In: Baas P (ed.), New perspectives in wood anatomy: 71-84. Nijhoff, Junk, The Hague.
10. Buvat R. 1989. Ontogeny, cell differentiation, and structure of vascular plants. Springer-Verlag, Berlin.
11. Carlquist S. 1980. Further concepts in ecological wood anatomy, with comments on recent work in wood anatomy and evolution. Aliso 9: 499-553.
12. Catesson AM. 1994. Cambial ultrastructure and biochemistry: changes in relation to vascular tissue differentiation and the seasonal cycle. Int. J. Plant Sci. 155: 251-261.
13. Cochard H & Tyree MT. 1990. Xylem dysfunction in Quercus: vessel size, tyloses, cavitation and seasonal changes in embolism. Tree Physiology 6: 393-407.
14. Costa MS, De Vasconcellos TJ, Barros CF & Callado CH. 2013. Does growth rhythm of a widespread species change in distinct growth sites? IAWA J. 34: 498-509.
15. De Micco V, Balzano A, Wheeler EA & Baas P. 2016. Tyloses and gums: a review of structure, function and occurrence of vessel occlusions. IAWA J. 37: 186-205.
16. Delvaux C, Sinsin B, Damme P & Beeckman H. 2010. Wound reaction after bark harvesting: microscopic and macroscopic phenomena in ten medicinal tree species. Trees 24: 941-951.
17. Dié A, Kitin P, Kouamé FNG, Van den Bulcke J, Van Acker J & Beeckman H. 2012. Fluctuations of cambial activity in relation to precipitation result in annual rings and intra-annual growth zones of xylem and phloem in teak (Tectona grandis) in Ivory Coast. Ann. Bot. 110: 861-873.
18. Dünisch O, Bauch J & Gasparotto L. 2002. Formation of increment zones and intra-annual growth dynamics in the xylem of Swietenia macrophylla, Carapa guianensis, and Cedrela odorata (Meliaceae). IAWA J. 23: 101-119.
19. Dünisch O & Moraes RR. 2002. Regulation of xylem sap flow in an evergreen, a semi-deciduous, and a deciduous Meliaceae species from the Amazon. Trees 16: 404-416.
20. Ellmore GS & Ewers FW. 1986. Fluid flow in the outermost xylem increment of a ring-porous tree, Ulmus americana. Amer. J. Bot. 73: 1771-1774.
21. Fahn A & Werker E. 1990. Seasonal cambial activity. In: Iqbal M (ed.), The vascular cambium: 1-36. Research Studies Press, Taunton.
22. Fonti P, Solomonoff N & García-González I. 2007. Earlywood vessels of Castanea sativa record temperature before their formation. New Phytol. 173: 562-570. DOI:10.1111/j. 1469-8137.2006.01945.x.PMID:17244050.
23. Forster T, Schweingruber FH & Denneler B. 2000. Increment puncher - a tool for extracting small cores of wood and bark from living trees. IAWA J. 21: 169-180.
24. Frankenstein C, Eckstein D & Schmitt U. 2005. The onset of cambium activity - a matter of agreement? Dendrochronologia 23: 57-62.
25. Funada R, Iwatate-Suzuki T, Utsumi Y, Suzuki T, Kitin P & Sano Y. 2001. Formation of new vessel elements in the ring-porous hardwoods in springtime in relation to water transport. Tree Rings and People-International Conference on the Future of Dendrochronology.-A tribute to Fritz Hans Schweingruber, Davos, Switzerland, September (2001).
26. García-González I, Souto-Herrero M & Campelo F. 2016. Ring porosity and earlywood vessels: a review on extracting environmental information through time. IAWA J. 37: 295-314.
27. González-González BD, García-González I & Vázquez-Ruiz RA. 2013. Comparative cambial dynamics and phenology of Quercus robur L. and Q. pyrenaica Willd. in an Atlantic forest of the northwestern Iberian Peninsula. Trees 27: 1571-1585.
28. Hacke UG & Sperry JS. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4: 97-115.
29. Haggerty BP & Mazer SJ. 2008. The phenology handbook. A guide to phenological monitoring to students, teachers, families, and nature enthusiasts. University of California Santa Barbara Phenology Stewardship Program. (Last accessed online on Feb 27, 2016 at https://ndep. nv.gov/tribe/docs/env-mgr-ref-docs/Climate%20Change/Phenology-Handbook-2nd-ed- Abridged.pdf).
30. Iliev I, Kitin P & Funada R. 2001. Morphological and anatomical study of in vitro root formation of silver birch (Betula pendula Roth). Propagation of Ornamental Plants 1: 10-19.
31. Imagawa H & Ishida S. 1972. Study on the wood formation in trees. III. Occurrence of overwintering cells in cambial zone of several ring-porous trees. Research Bulletin of the College Experimental Forests. College of Agriculture, Hokkaido University 39: 207-221.
32. Kitin P. 1990. Dynamics of the cambial divisions in the early and late flushing forms of pedunculate oak (Quercus robur L. f. praecox Czern. and Q. robur L. f. tardiflora Czern.) grown in Sofia. Nauka za gorata (Forest Science) 30: 10-21.
33. Kitin P. 2001. Three-dimensional analysis of cambium and differentiating xylem cells in the ringporous hardwood Kalopanax pictus. PhD thesis. Hokkaido University, Sapporo, Japan.
34. Kitin P, Beeckman H, Fujii T, Funada R, Noshiro S & Abe H. 2009. What is disjunctive xylem parenchyma? A case study of the African tropical hardwood Okoubaka aubrevillei (Santalaceae). Amer. J. Bot. 96: 1399-1408.
35. Kitin PB, Fujii T, Abe H & Funada R. 2004. Anatomy of the vessel network within and between tree rings of Fraxinus lanuginosa (Oleaceae). Amer. J. Bot. 91: 779-788.
36. Kitin P, Funada R, Sano Y, Beeckman H & Ohtani J. 1999. Variations in the lengths of fusiform cambial cells and vessel elements in Kalopanax pictus. Ann. Bot. 84: 621-632.
37. Kitin P, Funada R, Sano Y & Ohtani J. 2000. Analysis by confocal microscopy of the structure of cambium in the hardwood Kalopanax pictus. Ann. Bot. 86: 1109-1117.
38. Kitin P, Sano Y & Funada R. 2001. Analysis of cambium and differentiating vessel elements in Kalopanax pictus using resin cast replicas. IAWA J. 22: 15-28.
39. Kitin P, Sano Y & Funada R. 2002. Fusiform cells in the cambium of Kalopanax pictus are exclusively mononucleate J. Experim. Bot. 53: 483-488.
40. Kitin P, Sano Y & Funada R. 2003. Three-dimensional imaging and analysis of differentiating secondary xylem by confocal microscopy. IAWA J. 24: 211-222.
41. Kitin P, Voelker SL, Meinzer FC, Beeckman H, Strauss SH & Lachenbruch B. 2010. Tyloses and phenolic deposits in xylem vessels impede water transport in low-lignin transgenic poplars: a study by cryo-fluorescence microscopy. Plant Physiol. 154: 874-886.
42. Kudo K, Nabeshima E, Begum S, Yamagishi Y, Nakaba S, Oribe Y, Yasue K & Funada R. 2014. The effects of localized heating and disbudding on cambial reactivation and formation of earlywood vessels in seedlings of the deciduous ring-porous hardwood, Quercus serrata. Ann. Bot. 113: 1021-1027.
43. Kudo K, Yasue K, Hosoo Y & Funada R. 2015. Relationship between formation of earlywood vessels and leaf phenology in two ring-porous hardwoods, Quercus serrata and Robinia pseudoacacia, in early spring. J. Wood Sci. 61: 455-464.
44. Larson PR. 1994. The vascular cambium: development and structure. Springer, Berlin.
45. Lo Gullo MA, Salleo S, Piaceri EC & Rosso R. 1995. Relations between vulnerability to xylem embolism and xylem conduit dimensions in young trees of Quercus cerris. Plant Cell Environ. 18: 661-669.
46. Marcati CR, Angyalossy V & Evert RF. 2006. Seasonal variation in wood formation of Cedrela fissilis (Meliaceae). IAWA J. 27: 199-211.
47. McCulloh KA, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB & Voelker S. 2010. Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous and diffuse-porous saplings from temperate and tropical forests. New Phytol. 186: 439-450.
48. Meylan BA & Butterfield BG. 1981. Perforation plate differentiation in the vessels of hardwoods. In: Barnett JR (ed.), Xylem cell development: 47-95. Castle House Publ., Tunbridge Wells.
49. Michelot A, Simard S, Rathgeber C, Dufrêne E & Damesin C. 2012. Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiology 32: 1033-1045. DOI:10.1093/treephys/tps052.
50. Murmanis L. 1978. Breakdown of end walls in differentiating vessels of secondary xylem in Quercus rubra L. Ann. Bot. 42: 679-682.
51. Nakaba S, Kitin P, Yamagishi Y, Begum S, Kudo K, Nugroho WD & Funada R. 2015. Threedimensional imaging of cambium and secondary xylem cells by confocal laser scanning microscopy. In: Yeung ECT, Stasolla C, Summer MJ & Huang BQ (eds.), Plant microtechniques: methods and protocols: 431-465. Springer, Heidelberg.
52. Pomerleau R. 1966. Relation of early cambial activity in white elm and infection by Ceratocystis ulmi (Buis.) C. Moreau. Canad. J. Bot. 44: 109-111.
53. Prislan P, Cufar K, Koch G, Schmitt U & Gricar J. 2013. Review of cellular and subcellular changes in the cambium. IAWA J. 34: 391-407.
54. Priya PB & Bhat KM. 1998. False ring formation in teak (Tectona grandis L.f.) and the influence of environmental factors. Forest Ecology and Management 108: 215-222.
55. Priya PB & Bhat KM. 1999. Influence of rainfall, irrigation and age on the growth periodicity and wood structure in teak (Tectona grandis). IAWA J. 20: 181-192.
56. Rossi S, Anfodillo T & Menardi R. 2006. Trephor: a new tool for sampling microcores from tree stems. IAWA J. 27: 89-97.
57. Rossi S, Deslauriers A, Gricar J, Seo JW, Rathgeber CBK, Anfodillo T, Morin H, Levanic T, Oven P & Jalkanen R. 2008. Critical temperatures for xylogenesis in conifers of cold climates. Global Ecol. Biogeogr. 17: 696-707.
58. Sass-Klaassen U, Sabajo CR & Den Ouden J. 2011. Vessel formation in relation to leaf phenology in pedunculate oak and European ash. Dendrochronologia 29: 171-175.
59. Schmitz N, Robert EMR, Verheyden A, Kairo JG, Beeckman H & Koedam N. 2008. A patchy growth via successive and simultaneous cambia: key to success of the most widespread mangrove species Avicennia marina? Ann. Bot. 101: 49-58.
60. Sperry JS, Nichols KL, Sullivan JEM & Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous and coniferous trees of northern Utah and interior Alaska. Ecology 75: 1736-1752.
61. Sundberg B, Uggla C & Tuominen H. 2000. Cambial growth and auxin gradient. In: Savidge R, Barnett J & Napier R (eds.), Cell and molecular biology of wood formation: 169-188. Bios Scientific Publishers, Oxford.
62. Suzuki M, Yoda K & Suzuki H. 1996. Phenological comparison of the onset of vessel formation between ring-porous and diffuse-porous deciduous trees in a Japanese temperate forest. IAWA J. 17: 413-444.
63. Takahashi S, Okada N & Nobuchi T. 2013. Relationship between the timing of vessel formation and leaf phenology in ten ring-porous and diffuse-porous deciduous tree species. Ecological Research 28: 615-624.
64. Takahashi S, Okada N & Nobuchi T. 2015. Relationship between vessel porosity and leaf emergence pattern in ring-and diffuse-porous deciduous trees in a temperate hardwood forest. Botany 93: 31-39.
65. Takahashi S & Takahashi E. 2016. Timing of vessel formation in twigs and trunks in relation to porosity and leaf flushing. IAWA J. 37: 16-27.
66. Taneda H & Sperry JS. 2008. A case-study of water transport in co-occurring ring-versus diffuseporous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiology 28: 1641-1651.
67. Tarelkin Y, Delvaux C, De Ridder M, De Cannière C & Beeckman H. 2016. Tree-ring distinctness based on IAWA's definition: variability and consequences for trait analysis. IAWA J. 37: 275-294.
68. Tepper HB & Hollis CA. 1967. Mitotic reactivation of the terminal bud and cambium of white ash. Science 156: 1635-1636.
69. Umebayashi T, Utsumi Y, Koga S, Inoue S, Fujikawa S, Arakawa K, Matsumura J & Oda K. 2008. Conducting pathways in north temperate deciduous broadleaved trees. IAWA J. 29: 247-263.
70. Utsumi Y, Sano Y, Funada R, Fujikawa S & Ohtani J. 1999. The progression of cavitation in earlywood vessels of Fraxinus mandshurica var. japonica during freezing and thawing. Plant Physiology 121: 897-904.
71. Utsumi Y, Sano Y, Ohtani J & Fujikawa S. 1996. Seasonal changes in the distribution of water in the outer growth rings in Fraxinus mandshurica var. japonica: a study by cryo-scanning electron microscopy. IAWA J. 17: 113-124.
72. Vilhar U, Beuker E, Mizunuma T, Skudnik M, Lebourgeois F, Soudani K & Wilkinson M. 2013. Tree phenology. In: Ferretti M & Fischer R (eds.), Forest monitoring. Developments in Environmental Science 12: 169-182. Elsevier Ltd., Amsterdam, The Netherlands. ISBN: 978-0-08-098222-9.
73. Wakuta R, Saiki H & Harada H. 1973. Enlarging of differentiating vessel element in Furmiana platanifolia Shott et Endl. Bull. Kyoto Univ. Forests 45: 204-216.
74. Yata S, Itoh T & Kishima T. 1970. Formation of perforation plates and bordered pits in differentiating vessel elements. Wood Research 50: 1-11.
75. Yin J, Fridley JD, Smith MS & Bauerle TL. 2015. Xylem vessel traits predict the leaf phenology of native and non-native understorey species of temperate deciduous forests. Functional Ecology. DOI: 10.1111/1365-2435.12476.
76. Zasada JC & Zahner R. 1969. Vessel element development in the earlywood of red oak (Quercus rubra L.). Canad. J. Bot. 47: 1965-1971.