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Journal ArticleDOI

Sequence and pattern of lateral root formation in five selected species

01 Aug 1970-American Journal of Botany (John Wiley & Sons, Ltd)-Vol. 57, Iss: 7, pp 800-809
TL;DR: In the angiosperms studied, the pattern of lateral root distribution seemed to depend primarily upon a rather strict longitudinal relationship between the lateral root primordia formed opposite any one protoxylem pole.
Abstract: A B S T R A C T The proximal-distal distribution of the lateral roots of five species was studied. A detailed investigation was carried out on two of the five species, Ceratopteris thalictroides and Cucurbita maxima. A definite pattern of lateral root arrangement, with a degree of variability related to the number of protoxylem poles, was found in all of the species studied. In the fern Ceratopteris, lateral root initiation was found to be related to the segmentation of the apical cell, which in turn determines the distribution of the laterals. In this species the lateral roots occur in a predictable sequence and they are grouped in pairs. In the angiosperms studied, the pattern of lateral root distribution seemed to depend primarily upon a rather strict longitudinal relationship between the lateral root primordia formed opposite any one protoxylem pole. In Cucurbita maxima, 93.7 i 5.02% of the lateral root primordia observed were in a specific sequence. The laterals of this species are also arranged in groups. In the other plants studied, Arachis hypogaea, Victoria trickeri, and Eichhornia crassipes, the laterals were not as regularly arranged, but nevertheless they were found to be arranged in groups along the main root axis and not randomly dispersed. Factors controlling the spacing of lateral root primordia include their relationship with the developing vascular system, a direct effect of the parent root apex, and an effect of older lateral root pri
Citations
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Journal ArticleDOI
TL;DR: Evidence is found that the priming of pericycle cells for lateral root initiation might take place in the basal meristem, correlating with elevated auxin sensitivity in this part of the root, and auxin responsiveness oscillates with peaks of expression at regular intervals of 15 hours.
Abstract: In plants, the developmental mechanisms that regulate the positioning of lateral organs along the primary root are currently unknown. We present evidence on how lateral root initiation is controlled in a spatiotemporal manner in the model plant Arabidopsis thaliana. First, lateral roots are spaced along the main axis in a regular left-right alternating pattern that correlates with gravity-induced waving and depends on AUX1, an auxin influx carrier essential for gravitropic response. Second, we found evidence that the priming of pericycle cells for lateral root initiation might take place in the basal meristem, correlating with elevated auxin sensitivity in this part of the root. This local auxin responsiveness oscillates with peaks of expression at regular intervals of 15 hours. Each peak in the auxin-reporter maximum correlates with the formation of a consecutive lateral root. Third, auxin signaling in the basal meristem triggers pericycle cells for lateral root initiation prior to the action of INDOLE-3-ACETIC ACID14 (SOLITARY ROOT).

585 citations


Cites background from "Sequence and pattern of lateral roo..."

  • ...In several plant species, lateral roots along the main root axis seem to be formed according to a regular pattern (Mallory et al., 1970; Charlton, 1983; Barlow and Adam, 1988)....

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Journal ArticleDOI
TL;DR: An alternative, topological model is outlined, in which the link is the basic unit of classification of root systems, and it is shown that resource cost, transport efficiency and exploration efficiency cannot be simultaneously minimized and that optimum form may vary with the mobility of the resource.
Abstract: Summary Although plants devote a large proportion of their resources to roots, we have a poor understanding of the constraints under which root systems function. Roots are much less variable morphologically than leaves and it is likely that root systems rather than individual roots are the focus of natural selection. In other words, architecture is more important than morphology. Existing classifications of root systems, based on the developmental model, have failed to provide much insight into their functioning and an alternative, topological model is outlined, in which the link is the basic unit of classification. Other components of the architecture of root systems, including link lengths, branching angles and diameters, are considered and the ecological implications of variation in each is discussed. Simulation models of transport and space exploration are discussed and it is shown that resource cost, transport efficiency and exploration efficiency cannot be simultaneously minimized and that optimum form may vary with the mobility of the resource. In general, a ‘herringbone’ structure seems to be the most efficient at exploration of space but the least transport-efficient and the most expensive.

483 citations

Journal ArticleDOI
TL;DR: This review aims to give an overview on the developmental events taking place from the very early specification of founder cells in the pericycle until the first anticlinal divisions by combining the knowledge originating from classical physiology studies with new insights from genetic-molecular analyses.
Abstract: Root branching happens through the formation of new meristems out of a limited number of pericycle cells inside the parent root. As opposed to shoot branching, the study of lateral root formation has been complicated due to its internal nature, and a lot of questions remain unanswered. However, due to the availability of new molecular tools and more complete genomic data in the model species Arabidopsis, the probability to find new and crucial elements in the lateral root formation pathway has increased. Increasingly more data are supporting the idea that lateral root founder cells become specified in young root parts before differentiation is accomplished. Next, pericycle founder cells undergo anticlinal asymmetric, divisions followed by an organized cell division pattern resulting in the formation of a new organ. The whole process of cell cycle progression and stimulation of the molecular pathway towards lateral root initiation is triggered by the plant hormone auxin. In this review, we aim to give an overview on the developmental events taking place from the very early specification of founder cells in the pericycle until the first anticlinal divisions by combining the knowledge originating from classical physiology studies with new insights from genetic-molecular analyses. Based on the current knowledge derived from recent genetic and developmental studies, we propose here a hypothetical model for LRI.

265 citations


Cites background from "Sequence and pattern of lateral roo..."

  • ...the protophloem (Mallory et al., 1970), or the differentiating or mature protoxylem (Charlton, 1996)....

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  • ...…the origin of LR primordia is distal to the main root apex in the differentiation , p y ; , p ; , y 874 zone, which seems to coincide with the appearance of the first vascular elements, i.e. the protophloem (Mallory et al., 1970), or the differentiating or mature protoxylem (Charlton, 1996)....

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  • ...Some species initiate spontaneously LR primordia in the meristem itself (Mallory et al., 1970)....

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Journal ArticleDOI
TL;DR: The observation that pericycle cells divide and lateral root primordia form without intervening mitotic quiescence suggests that lateral organ formation in roots and shoots might not be as fundamentally different as previously thought.
Abstract: In contrast with other cells generated by the root apical meristem in Arabidopsis, pericycle cells adjacent to the protoxylem poles of the vascular cylinder continue to cycle without interruption during passage through the elongation and differentiation zones. However, only some of the dividing pericycle cells are committed to the asymmetric, formative divisions that give rise to lateral root primordia (LRPs). This was demonstrated by direct observation and mapping of mitotic figures, cell-length measurements, and the histochemical analysis of a cyclin-GUS fusion protein in pericycle cells. The estimated duration of a pericycle cell cycle in the root apical meristem was similar to the interval between cell displacement from the meristem and the initiation of LRP formation. Developmentally controlled LRP initiation occurs early, 3 to 8 mm from the root tip. Thus the first growth control point in lateral root formation is defined by the initiation of primordia in stochastic patterns by cells passing through the elongation and young differentiation zones, up to where lateral roots begin to emerge from the primary root. Therefore, the first growth control point is not restricted to a narrow developmental window. We propose that late LRP initiation is developmentally unrelated to the root apical meristem and is operated by a second growth control point that can be activated by environmental cues. The observation that pericycle cells divide and lateral root primordia form without intervening mitotic quiescence suggests that lateral organ formation in roots and shoots might not be as fundamentally different as previously thought.

256 citations

Journal ArticleDOI
TL;DR: Early observations on the cell biology of lateral root formation and emergence are summarized, and in the following two sections recent observations in Arabidopsis that led to the identification of the molecular mechanism regulating lateral root emergence are described.
Abstract: Lateral root initiation takes place deep within the parental root, requiring new primordia to break through the overlying tissues before they emerge into the soil. Lateral root emergence has been well described at the cellular level but, until recently, the molecular mechanisms involved were unclear. Scientists in the 19th and 20th centuries hypothesized that the cell wall of the overlying tissues was modified by enzymes released by cells within the primordium. Recent studies in the model plant Arabidopsis thaliana revealed the existence of a complex transcellular signalling network regulated by auxin that controls cell wall remodelling in cells overlying lateral root primordia. In the first part of this review, early observations on the cell biology of lateral root formation and emergence are summarized, and in the following two sections recent observations in Arabidopsis that led to the identification of the molecular mechanism regulating lateral root emergence are described.

177 citations


Cites background from "Sequence and pattern of lateral roo..."

  • ...In rice, the pericycle is surrounded by the endodermis, the mesodermis, the sclerenchyma layer, the exodermis, and the epidermis (Rebouillat et al., 2008) (Fig....

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  • ...In Cucurbita maxima, the endodermis appears to contribute to the cortex, the epidermis, the cap, and the vascular tissues of the lateral root (Mallory et al., 1970)....

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References
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Journal ArticleDOI
TL;DR: In this paper, a schedule is given for staining the cell walls of young plant tissues in tannic acid and iron alum after the protoplasts have been stained in safranin and orange G.
Abstract: A schedule is given for staining the cell walls of young plant tissues in tannic acid and iron alum after the protoplasts have been stained in safranin and orange G. Sections are placed for one minute in 2% aqueous ZnCl2, and are then stained in a 1/25,000 aqueous solution of safranin O. From this they are placed for five minutes in a bath consisting of orange G (2 g.), tannic acid (5 g.). water (up to 100 cc.) and HC1 (4 drops). This is followed by five minutes in 5% aqueous tannic acid and two minutes in a 1% solution of iron alum. A brief rinse in tap water is given between each stage; the slides are raised and lowered about a dozen times at each change to ensure that the new solution reaches the material quickly. The method was originated for shoot apices but it also works excellently on more mature tissues and on adult material. It has the advantage of allowing extremely easy detection of protophloem in the strands even at the very onset of vascular differentiation.

192 citations

Book ChapterDOI
01 Jan 1965
TL;DR: The Musterbildung is eines der Grundphanomene in der Entwicklungsphysiologie der Pflanzen und der Tiere as discussed by the authors.
Abstract: Die Musterbildung ist eines der Grundphanomene in der Entwicklungsphysiologie der Pflanzen und der Tiere. Dementsprechend wird zu ihm in verschiedenen Beitragen dieses Bandes direkt oder indirekt Stellung genommen Dieser Abschnitt hat die Aufgabe, die Ursachen und Regeln der Musterbildung vergleichend zu betrachten; die Einzelphanomene selber konnen hier jeweils nur angedeutet oder nur an wenigen, aus gewahlten Beispielen demonstriert werden.

49 citations

Book ChapterDOI
01 Jan 1965
TL;DR: Enough information has accumulated to warrant an examination of the subject and even to outline the broad areas in which the subject may expect to make progress in the immediate future, and physiological and biochemical information is brought together.
Abstract: The organization and development of roots have been well described in morphological and anatomical terms by many authors (v. Guttenberg 1940, 1941, Esau 1943b, 1953a, 1960, Foster 1949) and recent concepts and terminologies with respect to root development have been reviewed and consolidated by Esau (1953 b, 1954) and in vol. III of this encyclopedia1. It is not the purpose of the present chapter to repeat such information. Rather, its purpose is to bring together physiological and biochemical information which bears upon the broad subject of root development and to analyze root organization and development in terms of the physiological and biochemical processes upon which they depend. Our present state of knowledge of the intimate machinery of the cell which, through its intricate and complex workings, controls and directs the course of cellular development, is entirely inadequate to give any clear or definitive picture of the physiological basis of cell organization, let alone the further complexities of such an organized tissue system as the elongating root. However, at our present stage, sufficient information has accumulated to warrant an examination of the subject and even to outline the broad areas in which we may expect to make progress in the immediate future.

43 citations