Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Apical intrusive growth of cambial fusiform initials along the tangential walls of adjacent fusiform initials: evidence for a new concept

Joanna Jura A , Paweł Kojs A B , Muhammad Iqbal C , Joanna Szymanowska-Pułka D and Wiesław Włoch A B E

A Botanical Garden—Centre for Biological Diversity Conservation of the Polish Academy of Sciences, Prawdziwka 2, 02-973 Warszawa 76, Poland.

B Department of Biosystematics, University of Opole, Oleska 22, 40-052 Opole, Poland.

C Department of Botany, Jamia Hamdard (Hamdard University), Tughlaqabad, New Delhi-110062, India.

D Department of Biophysics and Cell Biology, Silesian University, Jagiellońska 28, 40-032 Katowice, Poland.

E Corresponding author. Email: wwloch@op.pl

Australian Journal of Botany 54(5) 493-504 http://dx.doi.org/10.1071/BT05130
Submitted: 27 July 2005  Accepted: 2 February 2006   Published: 3 August 2006

Abstract

A new study of cambium of Pinus sylvestris L., Tilia cordata Mill. and Wisteria floribunda (Willd.) DC provides fresh clues on the cambial dynamics, rejecting the hitherto held concept that intrusive growth of the fusiform initial occurs between the radial walls of adjacent initials. It demonstrates that intrusion of the elongating initial in fact takes place along tangential walls of adjacent fusiform initials and their immediate derivatives. It also suggests a new mechanism for ‘elimination of initials’. Intrusive growth of the fusiform initial was found to begin with development of characteristic slants, representing a transitional stage of the process of transformation of periclinal walls of fusiform initial cells into radial walls, as observed in transverse sections of active cambium. The gradually progressing event comprised (a) appearance of either a triangular microspace limited by two periclinal walls of a fusiform initial and its derivative and one radial wall of another fusiform initial in the adjacent radial file, or a rhomboidal microspace enclosed by four periclinal walls of two laterally adjacent fusiform initials and their immediate derivatives, (b) intrusion of elongating tip of fusiform initial from neighbouring file into the microspace thus formed, (c) symplastic growth of the cambial cell walls in radial direction, (d) unequal periclinal divisions of fusiform initial cells while growing intrusively, and (e) unequal periclinal divisions of derivative cells not growing intrusively. Intrusive growth between periclinal walls affected rearrangement of the fusiform initials but did not add to the cambial circumference. The existing concepts of (a) intrusion of the fusiform initial between radial walls of neighbouring initials and (b) elimination of fusiform initials from cambial surface have been reassessed and redefined.


References

Bannan MW 1951 The annual cycle of size changes in the fusiform cambial cells of Chamaecyparis and Thuja. Canadian Journal of Botany 29 421 437

Bannan MW 1953 Further observations on the reduction of fusiform cambial cells in Thuja occidentalis L. Canadian Journal of Botany 31 63 74


Bannan MW 1956 Some aspects of the elongation of fusiform cambial cells in Thuja occidentalis. Canadian Journal of Botany 34 175 194


Bannan MW 1964 Tracheid size and anticlinal divisions in the cambium of Pseudotsuga. Canadian Journal of Botany 42 603 631


Bannan MW Bayly IL 1956 Cell size and survival in conifer cambium. Canadian Journal of Botany 34 769 776


Bannan MW Whalley BE 1950 The elongation of fusiform cambial cells in Chamaecyparis. Canadian Journal of Research 28C 341 355


Barghoorn ES Jr 1940 a Origin and development of the uniseriate ray in the Coniferae. Bulletin of the Torrey Botanical Club 67 303 328


Barghoorn ES Jr 1940 b The ontogenetic development and phylogenetic specialization of ray in the xylem of dicotyledons. I. The promitive ray structure. American Journal of Botany 27 918 928


Brański JM 1970 Relations between anticlinal divisions, intrusive growth and loss of fusiform initials in the cambium of Pinus silvestris. Acta Societatis Botanicorum Poloniae 39 593 615


Brown CL 1970 Physiology of wood formation in conifers. Wood Science 3 8 22


Butterfield BG 1975 Terminology used for describing the cambium. IAWA Bulletin XXX 13 14


Cumbie BG 1967 Developmental changes in the vascular cambium of Leitneria floridana. American Journal of Botany 54 414 424


Cumbie BG 1969 a Developmental changes in the vascular cambium of Polygonum lapathifolium. American Journal of Botany 56 139 146


Cumbie BG 1969 b Developmental changes in the xylem and vascular cambium of Apocynum sybiricum. Bulletin of the Torrey Botanical Club 96 629 640


Eames AJ , Mac Daniels LH (1947) ‘An introduction to plant anatomy.’ (McGraw-Hill: New York and London)

Erickson RO 1986 Symplastic growth and symplasmic transport. Plant Physiology 82 1153


Esau K (1965) ‘Plant anatomy.’ 2nd edn. (John Wiley and Sons: New York)

Esau K (1977) ‘The anatomy of seed plants.’ 2nd edn. (John Wiley and Sons: New York)

Evert RF 1961 Some aspects of cambial development of Pyrus communis. American Journal of Botany 48 479 488


Harris JM (1989) ‘Spiral grain and wave phenomena in wood formation.’ (Springer-Verlag: Berlin, Heidelberg, New York)

Harris JM 1973 Spiral grain and xylem polarity in radiata pine: microscopy of cambial reorientation. New Zealand Journal of Forestry Science 3 363 378


Hejnowicz Z 1961 Anticlinal divisions, intrusive growth, and loss of fusiform initials in nonstoreyed cambium. Acta Societatis Botanicorum Poloniae 30 729 758


Hejnowicz Z 1967 Interrelationship between mean length, rate of intrusive elongation, frequency of anticlinal divisions and survival of fusiform initials in cambium. Acta Societatis Botanicorum Poloniae 36 367 378


Hejnowicz Z 1975 A model for morphogenetic map and clock. Journal of Theoretical Biology 54 345 362


Hejnowicz Z 1980 Tensional stress in the cambium and its developmental significance. American Journal of Botany 67 1 5


Hejnowicz Z Brański S 1966 Quantitative analysis of cambium growth in Thuja. Acta Societatis Botanicorum Poloniae 35 395 400


Hejnowicz Z Zagórska-Marek B 1974 Mechanism of changes in grain inclination in wood produced by storeyed cambium. Acta Societatis Botanicorum Poloniae 43 381 398


Iqbal M (1990) ‘The vascular cambium.’ (Research Studies Press/John Wiley and Sons Inc.: Taunton, UK)

Iqbal M (1994) Structural and operational specializations of the vascular cambium of seed plants. In ‘Growth patterns in vascular plants’. (Ed. M Iqbal) pp. 211–271. (Dioscorides Press: Portland, OR)

Iqbal M (1995) Structure and behaviour of vascular cambium and the mechanism and control of cambial growth. In ‘The cambial derivatives’. (Ed. M Iqbal) pp. 1–67. (Gebrüder Borntraeger: Stuttgart, Germany)

Kojs P Włoch W Rusin A Szendera W Duda J Jura J Rusin T 2002 From non-functional to functional storeyed arrangement in the cambium. Models of storeyed arrangement. [In Polish] Biuletyn Ogrodów Botanicznych 11 93 104


Kojs P Włoch W Rusin A 2004 a Rearrangement of cells in storeyed cambium of Lonchocarpus sericeus (Pior.) DC. connected with formation of interlocked grain in the xylem. Trees—Structure and Function 18 136 144
doi:10.1007/s00468-003-0292-9

Kojs P Włoch W Iqbal M Rusin A Jura J 2004 b Readjustment of cambial initials in Wisteria floribunda (Willd.) DC to ensure the development of storeyed structure. New Phytologist 163 287 297 doi:10.1111/j.1469-8137.2004.01120.x

Kojs P , Iqbal M , Włoch W , Wilczek A (2005). Is the control of the cambial cells readjustment based on the negative feedback? In ‘XVII international botanical congress-abstracts, 17–23 July 2005, Vienna’. Abstract No. P0464. p. 313. (Robidruck: Vienna)

Krabbe G (1886) ‘Das gleitende Wachsthum bei der Gewebebildung der Gefässpflanzen.’ (Gebrüder Borntraeger: Berlin)

Kramer EM 1999 Observation of topological defects in the xylem of Populus deltoides and implifications for the vascular cambium. Journal of Theoretical Biology 200 223 230 doi:10.1006/jtbi.1999.0989

Kramer EM 2002 A mathematical model of pattern formation in the vascular cambium of trees. Journal of Theoretical Biology 216 147 158 doi:10.1006/jtbi.2002.2551

Kramer EM Groves JV 2003 Defect coarsening in a biological system: the vascular cambium of cottonwood trees. Physical Review E 67 article no. 041914

Krawczyszyn J 1972 Movement of the cambial domain pattern and mechanism of formation of interlocked grain in Platanus. Acta Societatis Botanicorum Poloniae 41 443 461


Larson PR (1994) ‘The vascular cambium: Development and structure.’ Springer Series in Wood Science. (Ed. TE Timell) (Springer Verlag: Berlin, Heidelberg)

Majumdar GP 1941 The sliding, gliding, symplastic or the intrusive growth of the cambium cells and their derivatives in higher vascular plants. Journal of the Indian Botanical Society 20 161 171


Meek GA (1976) ‘Practical electron microscopy for biologists.’ (John Wiley and Sons: London, New York, Sydney, Toronto)

Meeuse ADJ 1942 A study of intercellular relationships among vegetable cells with special reference to ‘sliding growth’ and to cell shape. Recueil des Travaux Botaniques Néerlandais 38 18 140


Neeff F 1914 Über die Zellumlagerung. Ein Beitrag zur experimentallen Anatomie. Zeitschrift für Botanik 6 465 547


Neeff F 1920 Über die Umlagerung der Kambiumzellen beim Dickenwachstum der Dikotylen. Zeitschrift für Botanik 12 225 252


Newman IV 1956 Pattern in the meristems of vascular plants. Phytomorphology 6 1 19


Philipson WR , Ward JM , Butterfield BG (1971) ‘The vascular cambium, its development and activity.’ (Chapman and Hall Ltd: London)

Phillips IDJ (1976) The cambium. In ‘Cell division in higher plants’. (Ed. MM Yeoman) pp. 347–390. (Academic Press: New York)

Priestley JH 1930 II. The concept of sliding growth. New Phytologist 29 96 104


Romberger JA , Hejnowicz Z , Hill JF (1993) ‘Plant structure: function and development.’ (Springer-Verlag: Berlin, Heidelberg, New York)

Sanio K 1873 Anatomie der gemeinen Kiefer (Pinus sylvestris L.). Jahrbücher für Wissenschaftliche Botanik 9 50 126


Schmid R 1976 The elusive cambium—another terminological contribution. IAWA Bulletin 4 51 59


Schoch-Bodmer H Huber P 1952 Local apical growth and forking in secondary fibres. Proceedings of the Leeds Philosophical and Literary Society (Scientific Section) 6 25 32
Part 1

Sinnott EW Bloch R 1941 Division in vacuolated plant cells. American Journal of Botany 28 225 232


Timell TE 1980 Organization and ultrastructure of the dormant cambial zone in compression wood of Picea abies. Wood Science and Technology 14 161 179


Wenham MW Cusick F 1975 The growth of secondary wood fibers. New Phytologist 74 247 261


Whalley BE 1950 Increase in girth of the cambium in Thuja occidentalis L. Canadian Journal of Research Section C 28 331 340


Wilson BF Wodzicki TJ Zahner R 1966 Differentiation of cambial derivatives, proposed terminology. Forest Science 12 438 440


Włoch W 1976 Cell events in cambium, connected with the formation and existence of a whirled cell arrangement. Acta Societatis Botanicorum Poloniae 45 313 326


Włoch W 1981 Nonparallelism of cambium cells in neighbouring rows. Acta Societatis Botanicorum Poloniae 50 625 636


Włoch W Połap E 1994 The intrusive growth of initial cells in re-arrangement of cells in cambium of Tilia cordata Mill. Acta Societatis Botanicorum Poloniae 63 109 116


Włoch W Zagórska-Marek B 1982 Reconstruction of storeyed cambium in the linden. Acta Societatis Botanicorum Poloniae 51 215 228


Włoch W Mazur E Kojs P 2001 Intensive change of inclination of cambial initials in Picea abies (L.) Karst. Tumours. Trees—Structure and Function 15 498 502


Włoch W Mazur E Bełtowski M 2002 Formation of spiral grain in the wood of Pinus sylvestris L. Trees—Structure and Function 16 306 312


Zagórska-Marek B 1975 Growth activity of fusiform initials in storeyed cambium. Acta Societatis Botanicorum Poloniae 44 537 552


Zagórska-Marek B Little CHA 1986 Control of fusiform initial orientation in the vascular cambium of Abies balsamea stems by indolyl-3-hacetic acid. Canadian Journal of Botany 64 1120 1128


Zhang CH Fujita M Takabe K 2002 Extraction and analysis of the tangential arrangement of cambial cells in Japanese hardwood species. Journal of Wood Science 48 353 358




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