Growth and Cell Pattern Formation on an Axis: Critique of Concepts, Terminology, and Modes of Study

Green, Paul B.

doi:10.1086/336858

Cited by 231 publications

(167 citation statements)

References 12 publications

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“…2). Within each domain, different relationships between relative elongation and cell division rates (Green, 1976) or DLPs cause a change in the mean cell length. We have found that on average the PD DLP is equal to zero and the TD DLP is greater than zero (Table 3).…”

Section: Discussionmentioning

confidence: 99%

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Pacheco-Escobedo

Ivanov

Ransom-Rodríguez

et al. 2016

Ann Bot

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Background and Aims The Arabidopsis thaliana root is a key experimental system in developmental biology. Despite its importance, we are still lacking an objective and broadly applicable approach for identification of number and position of developmental domains or zones along the longitudinal axis of the root apex or boundaries between them, which is essential for understanding the mechanisms underlying cell proliferation, elongation and differentiation dynamics during root development.Methods We used a statistics approach, the multiple structural change algorithm (MSC), for estimating the number and position of developmental transitions in the growing portion of the root apex. Once the positions of the transitions between domains and zones were determined, linear models were used to estimate the critical size of dividing cells (L critD ) and other parameters.Key Results The MSC approach enabled identification of three discrete regions in the growing parts of the root that correspond to the proliferation domain (PD), the transition domain (TD) and the elongation zone (EZ). Simultaneous application of the MSC approach and G2-to-M transition (CycB1;1DB:GFP) and endoreduplication (pCCS52A1:GUS) molecular markers confirmed the presence and position of the TD. We also found that the MADS-box gene XAANTAL1 (XAL1) is required for the wild-type (wt) PD increase in length during the first 2 weeks of growth. Contrary to wt, in the xal1 loss-of-function mutant the increase and acceleration of root growth were not detected. We also found alterations in L critD in xal1 compared with wt, which was associated with longer cell cycle duration in the mutant.Conclusions The MSC approach is a useful, objective and versatile tool for identification of the PD, TD and EZ and boundaries between them in the root apices and can be used for the phenotyping of different genetic backgrounds, experimental treatments or developmental changes within a genotype. The tool is publicly available at www.ibiologia.com.mx/MSC_analysis.

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Section: Discussionmentioning

confidence: 99%

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Pacheco-Escobedo

Ivanov

Ransom-Rodríguez

et al. 2016

Ann Bot

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“…In principle, either parameter could have been reduced by phosphorus stress or maintained by ethylene; however, indirect evidence implicates the number of cells rather than their division rate. Under steady-state conditions, cell division rate must be in equilibrium with relative elongation rate, otherwise cell size would progressively increase or decrease, leading to non-steady-state behavior (Green, 1976). Relative elongation rate in the meristem was not changed by phosphorus stress, and roots grew at steady state for days; consequently, we deduce that cell division rate was unchanged by phosphorus stress and that the effects of phosphorus availability and ethylene action on cell flux were mediated by the number of dividing epidermal cells.…”

Section: Discussionmentioning

confidence: 99%

Regulation of Root Elongation under Phosphorus Stress Involves Changes in Ethylene Responsiveness

et al. 2003

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We characterized the growth of the primary root of Arabidopsis under phosphorus sufficiency (1 mm phosphate) and deficiency (1 m phosphate), focusing on the role of ethylene. We quantified the spatial profile of relative elongation with a novel method based on image processing, as well as the production rates of cortical cells, trichoblasts, and atrichoblasts. Phosphorus deficiency moderately decreased the maximal rate of relative elongation, shortened the growth zone, and decreased the production rate of both epidermal cell types but not of cortical cells. Inhibiting ethylene production (with aminoethoxyvinyl-glycine) or action (with 1-methylcyclopropene) increased elongation in high phosphorus and decreased it in low phosphorus. That these effects were specific to ethylene was confirmed by negating the effect of inhibited ethylene production with simultaneous treatment with an ethylene precursor (1-aminocyclopropane-1-carboxylic acid). Under both phosphorus regimes, ethylene regulated the maximal rate of relative elongation rather than the size of the growth zone. In addition, inhibiting ethylene action in high versus low phosphorus elicited opposite responses for the position of root hair initiation and for the production rates of cortex cells and atrichoblasts. We conclude that the root system acclimates to phosphorus deficiency by changing the signal transduction pathway connecting ethylene levels to growth and division.Plant root systems display an array of physiological, morphological, and architectural responses to low phosphorus availability. These responses enhance the ability of the root to explore the soil and include changes in branching patterns, in elongation rate, and in root hair length and density (Bates and Lynch, 1996;Bonser et al., 1996;Borch et al., 1999; Lynch and Brown, 2001; Ma et al., 2001a). These changes accompany changes in biochemical and metabolic processes and both together presumably represent adaptive responses to assist growth during phosphorus deficiency. In particular, the growth of root hairs and their response to phosphorus availability is important in the acquisition of this highly immobile nutrient (Lewis and Quirk, 1967;Bhat and Nye, 1974;Gahoonia and Nielsen, 1997; Lynch, 2000a, 2000b; Ma et al., 2001b).In response to low phosphorus, adaptive changes in roots may be mediated through the plant hormone ethylene. Both phosphorus deficiency and ethylene cause similar changes in root systems, such as aerenchyma formation, altered root growth angle, and stimulated root hair development (He et al., 1992;Lynch and Brown, 1997;Borch et al., 1999; Lynch and Brown, 2001). In bean (Phaseolus vulgaris), ethylene inhibits root elongation in phosphorus-sufficient conditions but maintains elongation under phosphorus deficiency (Borch et al., 1999). This finding suggests that roots respond to phosphorus stress by changing ethylene signal transduction pathways involved in regulating growth.In this report, we focus on the role of ethylene in mediating growth responses to low phosphoru...

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“…Bichet et al, 2001). Cell shape is formed by division as well as expansion; therefore, static images of meristem cell shape reveal nothing about expansion anisotropy (Green, 1976;Baskin and Beemster, 1998).…”

Section: Growth Patternsmentioning

confidence: 99%

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

et al. 2004

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To test the role of cortical microtubules in aligning cellulose microfibrils and controlling anisotropic expansion, we exposed Arabidopsis thaliana roots to moderate levels of the microtubule inhibitor, oryzalin. After 2 d of treatment, roots grow at approximately steady state. At that time, the spatial profiles of relative expansion rate in length and diameter were quantified, and roots were cryofixed, freeze-substituted, embedded in plastic, and sectioned. The angular distribution of microtubules as a function of distance from the tip was quantified from antitubulin immunofluorescence images. In alternate sections, the overall amount of alignment among microfibrils and their mean orientation as a function of position was quantified with polarized-light microscopy. The spatial profiles of relative expansion show that the drug affects relative elongation and tangential expansion rates independently. The microtubule distributions averaged to transverse in the growth zone for all treatments, but on oryzalin the distributions became broad, indicating poorly organized arrays. At a subcellular scale, cellulose microfibrils in oryzalin-treated roots were as well aligned as in controls; however, the mean alignment direction, while consistently transverse in the controls, was increasingly variable with oryzalin concentration, meaning that microfibril orientation in one location tended to differ from that of a neighboring location. This conclusion was confirmed by direct observations of microfibrils with field-emission scanning electron microscopy. Taken together, these results suggest that cortical microtubules ensure microfibrils are aligned consistently across the organ, thereby endowing the organ with a uniform mechanical structure.How do plants build organs with specific and heritable shapes? A part of the answer to this question lies in the control of growth. It is not growth rate per se that is crucial for morphogenesis but the directionality of growth. If growth rate were the same in all directions, i.e. isotropic, plant organs would be spherical; organs attain shapes other than spherical because their component cells grow at different rates in different directions, i.e. anisotropically. Understanding how cells control the anisotropy of their expansion is essential for understanding morphogenesis.Expansion anisotropy is characterized by the direction in which the maximal growth rate occurs and by the degree to which the maximum differs from the minimum. The direction of maximal expansion rate is known to be controlled by the direction of net alignment of cellulose microfibrils. Within a growing cell wall, microfibrils are aligned, on average, perpendicularly to the direction of maximal expansion rate, and the aligned cellulose microfibrils confer a mechanical anisotropy on the cell wall, which translates into expansion anisotropy (Green, 1980;Taiz, 1984). The wall can be considered a composite material with strong, rod-shaped particles (microfibrils) embedded in a compliant matrix. Such materials deform perpendic...

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Growth and Cell Pattern Formation on an Axis: Critique of Concepts, Terminology, and Modes of Study

Cited by 231 publications

References 12 publications

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

Regulation of Root Elongation under Phosphorus Stress Involves Changes in Ethylene Responsiveness

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

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