Elongation of wood fibers combines features of diffuse and tip growth

Abstract

 Xylem fibers are highly elongated cells that are key constituents of wood, play major physiological roles in plants, comprise an important terrestrial carbon reservoir, and thus have enormous ecological and economic importance. As they develop, from fusiform initials, their bodies remain the same length while their tips elongate and intrude into intercellular spaces.  To elucidate mechanisms of tip elongation, we studied the cell wall along the length of isolated elongating aspen xylem fibers and used computer simulations to predict the forces driving the intercellular space formation required for their growth.  We found pectin matrix epitopes (JIM5, LM7) concentrated at the tips where cellulose microfibrils have transverse orientation, and xyloglucan epitopes (CCRC-M89, CCRC-M58) in fiber bodies where microfibrils are disordered. These features are accompanied by changes in cell wall thickness, indicating that while the cell wall elongates strictly at the tips, it is deposited all over fibers. Computer modeling revealed that the intercellular space formation needed for intrusive growth may only require targeted release of cell adhesion, which allows turgor pressure in neighboring fiber cells to "round" the cells creating spaces.  These characteristics show that xylem fibers' elongation involves a distinct mechanism that combines features of both diffuse and tip growth.

Laticifer growth pattern is guided by cytoskeleton organization

“…In that case, the region of the cell which is intrusively growing detaches from the neighboring walls. That process was observed, for instance, during xylary fiber tip growth ( Majda et al, 2021 ). In phloem bast fibers, a higher rate of elongation in comparison with the neighboring cells has been also observed.…”

“…Two concurrent hypotheses based on observations from anatomical and developmental studies have been debated to explain their mode of growth in the plant body: (1) Laticifers grow through apical intrusive growth in meristematic regions, dissolving the middle lamella through enzymatic activity and growing intrusively between cells (Mahlberg, 1993;Canaveze and Machado, 2016;Castelblanque et al, 2016;Canaveze et al, 2019). In this case laticifers might combine two types of cell expansion, diffuse growth followed by polarized growth, as described for some fibers (Snegireva et al, 2010;Gorshkova et al, 2012;Majda et al, 2021);…”

“…Two concurrent hypotheses based on observations from anatomical and developmental studies have been debated to explain their mode of growth in the plant body: (1) Laticifers grow through apical intrusive growth in meristematic regions, dissolving the middle lamella through enzymatic activity and growing intrusively between cells ( Mahlberg, 1993 ; Canaveze and Machado, 2016 ; Castelblanque et al, 2016 ; Canaveze et al, 2019 ). In this case laticifers might combine two types of cell expansion, diffuse growth followed by polarized growth, as described for some fibers ( Snegireva et al, 2010 ; Gorshkova et al, 2012 ; Majda et al, 2021 ); (2) Laticifers may grow through the addition of new cells in the laticifer system followed by cell expansion, thus not through apical growth. Evidence supporting this view is the fact that laticifer apices (the region of the laticifer system where new cells that have just differentiated are added to the system) are found close to the shoot apical meristem but never penetrate this tissue ( Milanez, 1960 , 1977 , 1978 ; Demarco and Castro, 2008 ; Demarco et al, 2013 ; Gama et al, 2017 ; Ramos et al, 2019 ; Naidoo et al, 2020 ).…”

“…Additionally, some plant cells display an apical intrusive growth where the plant cell grows differentially at its tip. Intrusive growth implies that a part of the cell maintains cell-to-cell contact with their neighboring cells, and another part of the cell (the tip) invades new locations ( Lev-Yadun, 2001 ), provoking changes not only in cytoskeleton patterns but also in the middle lamella of the surrounding cells, as well as disrupting their plasmodesmata connections ( Lev-Yadun, 2001 ; Majda et al, 2021 ; Box 1). The apical intrusive growth has also been used to explain the way laticifers might grow within the plant, i.e., combining an initial phase of diffuse growth and then a phase of apical growth during their development, as is observed in vascular fibers ( Ageeva et al, 2005 ; Snegireva et al, 2010 ; Gorshkova et al, 2018 ; Gorshkov et al, 2019 ; Majda et al, 2021 ; Sousa-Baena and Onyenedum, 2022 ).…”

Riddled with holes: Understanding air space formation in plant leaves

“…In all species studied, leaf air spaces initially form at multicellular junctions [ 7 , 14 , 17 , 18 ] before subsequently expanding. TEM imaging has shown that localised wall breakdown happens at the site of future air space formation in Phaseolus vulgaris [ 17 ], and modelling of intercellular space formation in xylem fibres suggests that localised loss of adhesion combined with turgor pressure is sufficient to initialise small intercellular air spaces without the need for differential growth between the internal tissues and epidermis [ 19 ]. However, it is not clear whether localised changes in cell wall properties are necessary to initialise air spaces or whether stresses due to turgor pressure are highest at multicellular junctions and induce cell separation there despite equal adhesion on all walls.…”