Review of cellular and subcellular changes in the cambium

IAWA Journal

Volumn 34, Issue 4, 2013, Pages 391-407

  Schmitt, Uwe ^c   Koch, Gerald ^c   Gričar, Jožica ^a   Čufar, Katarina ^b   Prislan, Peter ^a,b  

^a SLOVENIAN FORESTRY INSTITUTE   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c Thuenen Institute of Wood Research   (Germany)

Author keywords

Cambial activity; cambial cells; Fagus sylvatica; light microscopy; transmission electron microscopy; ultrastructural changes

Indexed keywords

EID: 84890012171     PISSN: 09281541     EISSN: 22941932     Source Type: Journal    
DOI: 10.1163/22941932-00000032     Document Type: Article

References (76)

1. Antonova GF & Stasova VV. 1993. Effects of environmental factors on wood formation in Scots pine stems. Trees 7: 214-219.
2. Bailey IW. 1919. Phenomena of cell division in the cambium of arborescent gymnosperms and their cytological significance. Proceedings of the National Academy of Sciences of the USA 5: 283-285.
3. Barnett Jr. 1992. Reactivation of the cambium in Aesculus hippocastanum L.-a transmission electron microscopy study. Ann. Bot. 70: 169-177.
4. Begum S, Nakaba S, Oribe Y, Kubo T & Funada R. 2010a. Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann. Bot. 106: 885-895.
5. Begum S, Nakaba S, Oribe Y, Kubo T & Funada R. 2010b. Cambial sensitivity to rising temperatures by natural condition and artificial heating from late winter to early spring in the evergreen conifer Cryptomeria japonica. Trees 24: 43-52.
6. 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. Physiol. Plantarum 147: 46-54.
7. Bozzola JJ & Russell LD. 1999. Electron microscopy: Principles and techniques for biologists. Jones and Bartlett Publishers, Boston.
8. Callado CH, Roig FA, Tomazello-Filho M & Barrow CF. 2013. Cambial growth periodicity studies of South American woody species-A review. IAWA J. 34: 213-230.
9. Catesson A-M. 1994. Cambial ultrastructure and biochemistry: Changes in relation to vascular tissue differentiation and the seasonal cycle. Int. J. Plant Sci. 155: 251-261.
10. Chaffey NJ. 2002. Wood formation in trees: Cell and molecular biology techniques. Taylor & Francis, London, New York.
11. Chaffey NJ, Barlow PW & Barnett Jr. 1998. A seasonal cycle of cell wall structure is accompanied by a cyclical rearrangement of cortical microtubules in fusiform cambial cells within taproots of Aesculus hippocastanum (Hippocastanaceae). New Phytol. 139: 623-635. (Pubitemid 28422342)
12. Chen HM, Han JJ, Cui KM & He XQ. 2010. Modification of cambial cell wall architecture during cambium periodicity in Populus tomentosa Carr. Trees 24: 533-540.
13. 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.
14. Ufar K, De Luis M, Saz M, repinšek Z & Kajfež-Bogataj L. 2012. Temporal shifts in leaf phenology of beech (Fagus sylvatica) depend on elevation. Trees 26: 1091-1100.
15. Ufar K, Prislan P, De Luis M & Griar J. 2008. Tree-ring variation, wood formation and phenology of beech (Fagus sylvatica) from a representative site in Slovenia, SE Central Europe. Trees 22: 749-758.
16. De Luis M, Ufar K, Saz M, Longares L, Ceglar A & Kajfež- Bogataj L. 2012. Trends in seasonal precipitation and temperature in Slovenia during 1951-2007. Reg. Environ. Change. DOI: 10.1007/s10113-012-0365-7.
17. Deslauriers A, Morin H & Begin Y. 2003. Cellular phenology of annual ring formation of Abies balsamea in the Quebec boreal forest (Canada). Can. J. Forest Res. 33: 190-200. (Pubitemid 36453074)
18. Deslauriers A, Rossi S, Anfodillo T & Saracino A. 2008. Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiol. 28: 863-871. (Pubitemid 351967849)
19. Di Filippo A, Biondi F, Ufar K, De Luis M, Grabner M, Maugeri M, Presutti Saba E, Schirone B & Piovesan G. 2007. Bioclimatology of beech (Fagus sylvatica L.) in the Eastern Alps: Spatial and altitudinal climatic signals identified through a tree-ring network. J. Biogeogr. 34: 1873-1892. (Pubitemid 47609719)
20. Evert RF. 2006. Esau's Plant anatomy. Meristems, cells, and tissues of the plant body: Their structure, function, and development. Wiley-Interscience, Hoboken, New Jersey.
21. Farrar JJ & Evert RF. 1997a. Ultrastructure of cell division in the fusiform cells of the vascular cambium of Robinia pseudoacacia. Trees 11: 203-215. (Pubitemid 27140697)
22. Farrar JJ & Evert RF. 1997b. Seasonal changes in the ultrastructure of the vascular cambium of Robinia pseudoacacia. Trees 11: 191-202. (Pubitemid 27140696)
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. (Pubitemid 30427835)
24. Frankenstein C, Eckstein D & Schmitt U. 2005. The onset of cambium activity-A matter of agreement Dendrochronologia 23: 57-62. (Pubitemid 41338422)
25. Fromm J. 2013. Xylem development in trees: From cambial divisions to mature wood cells. In: Fromm J (ed.), Cellular aspects of wood formation: 3-39. Springer, Berlin, Heidelberg.
26. Fuchs M, van Bel AJE & Ehlers K. 2010. Season-associated modifications in symplasmic organization of the cambium in Populus nigra. Ann. Bot. 105: 375-387.
27. Goodhew PJ, Humphreys J & Beanland R. 2000. Electron microscopy and analysis. Taylor and Francis, London, New York.
28. Griar J. 2007. Xylo-and phloemogenesis in silver fir (Abies alba Mill.) and Norway spruce (Picea abies (L.) Karst.). Slovenian Forestry Institute, Ljubljana.
29. Griar J & Ufar K. 2008. Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought. Russ. J. Plant Physiol. 55: 538-543.
30. Griar J, Ufar K, Oven P & Schmitt U. 2005. Differentiation of terminal latewood tracheids in silver fir trees during autumn. Ann. Bot. 95: 959-965. (Pubitemid 41214408)
31. Griar J, Zupani M, Ufar K, Koch G, Schmitt U & Oven P. 2006. Effect of local heating and cooling on cambial activity and cell differentiation in the stem of Norway spruce (Picea abies). Ann. Bot. 97: 943-951. (Pubitemid 44447289)
32. Griar J, Zupani M, Ufar K & Oven P. 2007a. Wood formation in Norway spruce (Picea abies) studied by pinning and intact tissue sampling method. Wood Res. 52: 1-10. (Pubitemid 47173025)
33. Griar J, Zupani M, Ufar K & Oven P. 2007b. Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci. Technol. 41: 463-475. (Pubitemid 47197888)
34. Itoh T. 1971. On the ultrastructure of dormant and active cambium of conifers. Bull. Wood Res. Inst. Kyoto Univ. 51: 33-45.
35. Jyske T, Manner M, Mäkinen H, Nöjd P, Peltola H & Repo T. 2011. The effects of artificial soil frost on cambial activity and xylem formation in Norway spruce. Trees 26: 1-15.
36. Kirdyanov A, Hughes M, Vaganov E, Schweingruber F & Silkin P. 2003. The importance of early summer temperature and date of snow melt for tree growth in the Siberian Subarctic. Trees 17: 61-69. (Pubitemid 36028954)
37. Lachaud S, Catesson AM & Bonnemain JL. 1999. Structure and functions of the vascular cambium. Life Sci. 322: 633-650.
38. Larson PR. 1994. The vascular cambium: Development and structure. Springer, Berlin.
39. Li WF, Ding Q, Chen JJ, Cui KM & He XQ. 2009. Induction of PtoCDKB and PtoCYCB transcription by temperature during cambium reactivation in Populus tomentosa Carr. J. Exp. Bot. 60: 2621-2630.
40. Liang EY, Eckstein D & Shao XM. 2009. Seasonal cambial activity of relict Chinese pine at the northern limit of its natural distribution in north China-Exploratory results. IAWA J. 30: 371-378.
41. Lupi C, Morin H, Deslauriers A & Rossi S. 2010. Xylem phenology and wood production: Resolving the chicken-or-egg dilemma. Plant Cell Environ. 33: 1721-1730.
42. Mauseth JD. 2009. Botany: An introduction to plant biology. Jones & Bartlett Publ., Sudbury.
43. Mellerowicz EJ, Baucher M, Sundberg B & Boerjan W. 2001. Unravelling cell wall formation in woody dicot stem. Plant Mol. Biol. 47: 239-274. (Pubitemid 32804507)
44. 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 Physiol. 32: 1033-1045.
45. Moser L, Fonti P, Büntgen U, Esper J, Luterbacher J, Franzen J & Frank D. 2010. Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiol. 30: 225-233.
46. Oberhuber W & Gruber A. 2010. Climatic influences on intra-annual stem radial increment of Pinus sylvestris (L.) exposed to drought. Trees 24: 887-898.
47. Plomion C, LeProvost G & Stokes A. 2001. Wood formation in trees. Plant Physiol. 127: 1513-1523. (Pubitemid 34050021)
48. Pomeroy MK & Siminovitch D. 1971. Seasonal cytological changes in secondary phloem parenchyma cells in Robinia pseudoacacia in relation to cold hardiness. Can. J. Bot. 49: 787-795.
49. Prislan P, Griar J, De Luis M, Smith KT & Ufar K. 2013. Phenological variation in xylem and phloem formation in Fagus sylvatica from two contrasting sites. Agr. Forest Meteorol. 180: 142-151.
50. Prislan P, Schmitt U, Koch G, Griar J & Ufar K. 2011. Seasonal ultrastructural changes in the cambial zone of beech (Fagus sylvatica) grown at two different altitudes. IAWA J. 32: 443-459.
51. Rao KS & Dave YS. 1983. Ultrastructure of active and dormant cambial cells in teak (Tectona grandis L.f.). New Phytol. 93: 447-456.
52. Rathgeber CBK, Rossi S & Bontemps J-D. 2011. Cambial activity related to tree size in a mature silver-fir plantation. Ann. Bot. 108: 429-438.
53. Rensing KH & Samuels AL. 2004. Cellular changes associated with rest and quiescence in winter-dormant vascular cambium of Pinus contorta. Trees 18: 373-380. (Pubitemid 38947048)
54. Rensing KH, Samuels AL & Savidge RA. 2002. Ultrastructure of vascular cambial cell cytokinesis in pine seedlings preserved by cryofixation and substitution. Protoplasma 220: 39-49. (Pubitemid 35301756)
55. Riding RT & Little CHA. 1984. Anatomy and histochemistry of Abies balsamea cambial zone cells during the onset and breaking of dormancy. Can. J. Bot. 62: 2570-2579.
56. Risopatron JPM, Sun YQ & Jones BJ. 2010. The vascular cambium: Molecular control of cellular structure. Protoplasma 247: 145-161.
57. Robards AW & Kidwai P. 1969. A comparative study of the ultrastructure of resting and active cambium of Salix fragilis L. Planta 84: 239-224.
58. Rossi S, Anfodillo T & Menardi R. 2006. Trephor: A new tool for sampling microcores from tree stems. IAWA J. 27: 89-97. (Pubitemid 43329990)
59. Rossi S, Deslauriers A, Griar J, Seo JW, Rathgeber CWG, Anfodillo T, Morin H, Levani T, Oven P & Jalkanen R. 2008. Critical temperatures for xylogenesis in conifers of cold climates. Global Ecol. Biogeogr. 17: 696-707.
60. Rossi S, Morin H & Deslauriers A. 2011. Multi-scale influence of snowmelt on xylogenesis of black spruce. Arctic, Antarctic, and Alpine Research 43: 457-464.
61. Samuels AL, Kaneda M & Rensing KH. 2006. The cell biology of wood formation: From cambial divisions to mature secondary xylem. Can. J. Bot. 84: 631-639. (Pubitemid 44310417)
62. Savidge RA. 1996. Xylogenesis, genetic and environmental regulation-a review. IAWA J. 17: 269-310. (Pubitemid 26324895)
63. Savidge RA. 2000a. Intrinsic regulation of cambial growth. J. Plant Growth Regul. 20: 52-77.
64. Savidge RA. 2000b. Biochemistry of seasonal cambial growth and wood formation-an overview of the challenges. In: Savidge RA, Barnett JR, Napier R &Biggs A (eds.), Cell and molecular biology of wood formation: 1-30. BIOS Scientific Publishers Ltd, Oxford, UK.
65. Schmitt U, Möller R & Eckstein D. 2000. Seasonal wood formation dynamics of beech (Fagus sylvatica L.) and black locust (Robinia pseudoacacia L.) as determined by the pinning technique. J. Appl. Bot. 74: 10-16. (Pubitemid 30308209)
66. Seo JW, Eckstein D, Jalkanen R, Rickebusch S & Schmitt U. 2008. Estimating the onset of cambial activity in Scots pine in northern Finland by means of the heat-sum approach. Tree Physiol. 28: 105-112. (Pubitemid 351344924)
67. Seo JW, Eckstein D, Jalkanen R & Schmitt U. 2011. Climatic control of intra-and interannual wood-formation dynamics of Scots pine in northern Finland. Environ. Exp. Bot. 72: 422-431.
68. Spurr AR. 1969. A low viscosity embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31-43.
69. Srivastava LM & O'Brien TP. 1966. On the ultrastructure of cambium and its vascular derivatives. I. Cambium of Pinus strobus L. Protoplasma 61: 257-276.
70. Timell TE. 1986. Formation of compression wood. In: (ed.), Compression wood in gymnosperms 1: 623-636. Springer-Verlag, Berlin.
71. Uggla C, Mellerowicz EJ & Sundberg B. 1998. Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol. 117: 113-121. (Pubitemid 128652784)
72. Uggla C & Sundberg B. 2002. Sampling of cambial region tissues for high resolution analysis. In: Chaffey N (ed.), Wood formation in trees. Cell and molecular biology techniques: 215-228. Taylor & Francis, London, New York.
73. Ursache R, Nieminen K & Helariutta Y. 2013. Genetic and hormonal regulation of cambial development. Physiol. Plantarum 147: 36-45.
74. Van der Werf GW, Sass-Klaassen U & Mohren GMJ. 2007. The impact of the 2003 summer drought on the intra-annual growth pattern of beech (Fagus sylvatica L.) and oak (Quercus robur L.) on a dry site in the Netherlands. Dendrochronologia 25: 103-112. (Pubitemid 47284938)
75. Wodzicki TJ. 2001. Natural factors affecting wood structure. Wood Sci. Tech. 35: 5-26. (Pubitemid 32583983)
76. Zimmermann HM & Brown CL. 1971. Trees structure and function. Springer, Berlin, Heidelberg, New York.