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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
+ Author Affiliations
- Author Affiliations

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 https://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. open url image1

Bannan MW (1953) Further observations on the reduction of fusiform cambial cells in Thuja occidentalis L. Canadian Journal of Botany 31, 63–74. open url image1

Bannan MW (1956) Some aspects of the elongation of fusiform cambial cells in Thuja occidentalis. Canadian Journal of Botany 34, 175–194. open url image1

Bannan MW (1964) Tracheid size and anticlinal divisions in the cambium of Pseudotsuga. Canadian Journal of Botany 42, 603–631. open url image1

Bannan MW, Bayly IL (1956) Cell size and survival in conifer cambium. Canadian Journal of Botany 34, 769–776. open url image1

Bannan MW, Whalley BE (1950) The elongation of fusiform cambial cells in Chamaecyparis. Canadian Journal of Research 28C, 341–355. open url image1

Barghoorn ES (1940a) Origin and development of the uniseriate ray in the Coniferae. Bulletin of the Torrey Botanical Club 67, 303–328.
Crossref | Crossref | Crossref |
open url image1

Barghoorn ES (1940b) 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.
Crossref | Crossref |
open url image1

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. open url image1

Brown CL (1970) Physiology of wood formation in conifers. Wood Science 3, 8–22. open url image1

Butterfield BG (1975) Terminology used for describing the cambium. IAWA Bulletin XXX, 13–14. open url image1

Cumbie BG (1967) Developmental changes in the vascular cambium of Leitneria floridana. American Journal of Botany 54, 414–424.
Crossref | Crossref | Crossref |
open url image1

Cumbie BG (1969a) Developmental changes in the vascular cambium of Polygonum lapathifolium. American Journal of Botany 56, 139–146.
Crossref | Crossref | Crossref |
open url image1

Cumbie BG (1969b) Developmental changes in the xylem and vascular cambium of Apocynum sybiricum. Bulletin of the Torrey Botanical Club 96, 629–640.
Crossref | Crossref | Crossref |
open url image1

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.
PubMed | | PubMed |
open url image1

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.
Crossref | Crossref | Crossref |
open url image1

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. open url image1

Hejnowicz Z (1961) Anticlinal divisions, intrusive growth, and loss of fusiform initials in nonstoreyed cambium. Acta Societatis Botanicorum Poloniae 30, 729–758. open url image1

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. open url image1

Hejnowicz Z (1975) A model for morphogenetic map and clock. Journal of Theoretical Biology 54, 345–362.
Crossref | Crossref | PubMed | PubMed |
open url image1

Hejnowicz Z (1980) Tensional stress in the cambium and its developmental significance. American Journal of Botany 67, 1–5.
Crossref | Crossref | Crossref |
open url image1

Hejnowicz Z, Brański S (1966) Quantitative analysis of cambium growth in Thuja. Acta Societatis Botanicorum Poloniae 35, 395–400. open url image1

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. open url image1

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. open url image1

Kojs P, Włoch W, Rusin A (2004a) 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kojs P, Włoch W, Iqbal M, Rusin A, Jura J (2004b) Readjustment of cambial initials in Wisteria floribunda (Willd.) DC to ensure the development of storeyed structure. New Phytologist 163, 287–297.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kramer EM (2002) A mathematical model of pattern formation in the vascular cambium of trees. Journal of Theoretical Biology 216, 147–158.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Kramer EM, Groves JV (2003) Defect coarsening in a biological system: the vascular cambium of cottonwood trees. Physical Review E article no. 041914 67,
Crossref | Crossref | Crossref |
open url image1

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. open url image1

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. open url image1

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. open url image1

Neeff F (1914) Über die Zellumlagerung. Ein Beitrag zur experimentallen Anatomie. Zeitschrift für Botanik 6, 465–547. open url image1

Neeff F (1920) Über die Umlagerung der Kambiumzellen beim Dickenwachstum der Dikotylen. Zeitschrift für Botanik 12, 225–252. open url image1

Newman IV (1956) Pattern in the meristems of vascular plants. Phytomorphology 6, 1–19. open url image1

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.
Crossref | Crossref | Crossref |
open url image1

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. open url image1

Schmid R (1976) The elusive cambium—another terminological contribution. IAWA Bulletin 4, 51–59. open url image1

Schoch-Bodmer H, Huber P (1952) Local apical growth and forking in secondary fibres. Proceedings of the Leeds Philosophical and Literary Society (Scientific Section) Part 1 6, 25–32. open url image1

Sinnott EW, Bloch R (1941) Division in vacuolated plant cells. American Journal of Botany 28, 225–232.
Crossref | Crossref |
open url image1

Timell TE (1980) Organization and ultrastructure of the dormant cambial zone in compression wood of Picea abies. Wood Science and Technology 14, 161–179. open url image1

Wenham MW, Cusick F (1975) The growth of secondary wood fibers. New Phytologist 74, 247–261.
Crossref | Crossref | Crossref |
open url image1

Whalley BE (1950) Increase in girth of the cambium in Thuja occidentalis L. Canadian Journal of Research Section C 28, 331–340. open url image1

Wilson BF, Wodzicki TJ, Zahner R (1966) Differentiation of cambial derivatives, proposed terminology. Forest Science 12, 438–440. open url image1

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. open url image1

Włoch W (1981) Nonparallelism of cambium cells in neighbouring rows. Acta Societatis Botanicorum Poloniae 50, 625–636. open url image1

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. open url image1

Włoch W, Zagórska-Marek B (1982) Reconstruction of storeyed cambium in the linden. Acta Societatis Botanicorum Poloniae 51, 215–228. open url image1

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. open url image1

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. open url image1

Zagórska-Marek B (1975) Growth activity of fusiform initials in storeyed cambium. Acta Societatis Botanicorum Poloniae 44, 537–552. open url image1

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. open url image1

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. open url image1