Geometric analysis of intrusive growth of wood fibres in Robinia pseudoacacia

Abstract

All cell types of the secondary xylem arise from the meristematic cells (initials) of the vascular cambium and grow under mechanical constraints emerging from the circular-symmetrical geometry that characterises many tree trunks. The course of intrusive growth of cambial initials has been elucidated, but is yet to be described in the case of xylem fibres. This study explains the geometry of intrusive growth of the secondary xylem fibres in the trunk ofRobinia pseudoacacia.Long series of serial semi-thin sections of the vascular cambium and the differentiating secondary xylem were analysed. Since fibres grow in close vicinity to expanding cells of the derivatives of the vascular cambium, we assumed that they have similar growth conditions. Dealing with the cylindrical tissue of the vascular cambium in a previous study, we used a circularly symmetrical equation for describing the growth mechanism of cambial initials. Like the cambial initials, some of the cambial derivatives differentiating into the various cell types composing the secondary xylem also exhibit intrusive growth between the tangential walls of adjacent cells. As seen in cross sections of the cambium, intrusively growing initials form slanted walls by a gradual transformation of tangential (periclinal) walls into radial (anticlinal) walls. Similarly, the intrusive growth of xylem fibres manifests initially as slants, which are formed due to axial growth of the growing cell tips along the tangential walls of adjacent cells. During this process, the tangential walls of adjacent cells are partly separated and dislocated from the tangential plane. The final shape of xylem fibres, or that of vessel elements and axial parenchyma cells, depends upon the ratio of their intrusiveversussymplastic growths in the axial, circumferential and radial directions.

Elongation of wood fibers combines features of diffuse and tip growth

“…The shape of mature xylem fibers determined by our AFM analysis (Figs 2, S3b) and three‐dimensional (3D) reconstructions from serial transverse sections of wood (Fujiwara et al ., 1988; Yahya et al ., 2015) clearly allow distinction of the main body (the wide part with pit connections to adjacent cells) and the extensions (the narrower tapering parts, which are typically devoid of pits) (Larson, 1994; Chaffey et al ., 1999; Evert, 2006). The border between the body and extensions is sometimes marked by the presence of structures called ‘knees’ (Gorshkova et al ., 2012; Wilczek et al ., 2018). The length of the body corresponds to the length of xylem vessel elements and axial strands of parenchyma cells (Wenham & Cusick, 1975; Yahya et al ., 2015) that do not elongate during differentiation, and thus represents the length of xylem mother cells in the cambium (Larson, 1994; Mellerowicz, 2006).…”

“…2; S3b) and 3D reconstructions from serial transverse sections of wood (Fujiwara et al, 1988;Yahya et al, 2015) clearly allow distinction of the main body (the wide part with pit connections to adjacent cells) and the extensions -the narrower tapering parts, which are typically devoid of pits (Larson, 1994;Chaffey et al, 1999;Evert, 2006). The border between the body and extensions is sometimes marked by the presence of structures called 'knees' (Gorshkova et al, 2012;Wilczek et al, 2018).…”

“…Phloem fibers of flax and hemp elongate at the primary wall stage by diffuse rather than tip growth (Gorshkova et al ., 2003; Ageeva et al ., 2005; Snegireva et al ., 2015). Three‐dimensional reconstructions of elongating xylem fibers have shown that the tips frequently grow between tangential walls, starting at the three‐ or four‐way junctions between the fibers which undergo radial expansion (Wenham & Cusick, 1975; Włoch et al ., 2009; Wilczek et al ., 2018). It is unknown what drives the cell separation where the tips intrude.…”

How Do Trees Grow in Girth? Controversy on the Role of Cellular Events in the Vascular Cambium

“…Here we focus only on the intrusive growth of the cambial initials. However, recent reports suggest that the same mechanical conditions are likely involved in the intrusive growth of cambial initials, vessel-element mother cells (Wilczek et al 2011b ; Gizińska et al 2021 ) and fibres (Miodek et al 2013 ; Wilczek et al 2018 ).…”

“…Studies undertaken on the cambial cell growth during the last two decades (Karczewska et al 2009 ; Kojs 2012 ; Kojs et al 2004a , b ; Jura et al 2006 ; Włoch et al 2009 , 2013 ; Wilczek et al 2011a , 2018 ; Miodek et al 2021 ) have led to a new hypothesis on the mechanism of intrusive growth of the cambial initials. These studies have elucidated certain characteristic features of the cambium from new angles, suggesting that the mechanical strains in the cambial tissue likely affect the processes involved in the formation of wood and the consequent increase in the cambial circumference.…”