Plant Physiology and Development

J.G. Dubrovsky , M. Laskowski , in Encyclopedia of Applied Plant Sciences (Second Edition), 2017

Abstract

Lateral roots increase the volume of soil reached by the root, provide anchorage, and participate in water and nutrient uptake and transport. The number and location of lateral roots depends on their continued initiation and, collectively, is a major determinant of root system architecture. In seed plants, lateral root initiation (LRI) typically takes place close to the meristematic region in the root tip in an internal cell layer called the pericycle. Current hypotheses as to how pericycle cells become committed to forming lateral roots are discussed, along with the cellular basis and genetic control of LRI. Examples of the ecological, agricultural, and economic importance of LRI are also presented.

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Nitric oxide (NO) and lateral root development in plants under stress

R. Wimalasekera , G.F.E. Scherer , in Nitric Oxide in Plant Biology, 2022

3.1 Nitric oxide in lateral root development

Lateral root (LR) primordia origination from pericycle founder cells and emergence is essentially auxin-controlled. Auxin promotes LR initiation through the expression of cell-cycle regulatory genes in the pericycle cells ( Casimiro et al., 2003). Experimental evidences support that NO is implicated in the auxin-mediated signaling pathways during lateral root growth and development including adventitious root development (Pagnussat et al., 2002) and LR formation (Correa-Aragunde et al., 2004).

Treatment of tomato seedlings with the NO-donor SNP induced LR emergence and elongation in a dose-dependent manner (Correa-Aragunde et al., 2004). Further, treating roots with NO scavenger cPTIO resulted in reduction of NO biosynthesis and abolition of LR emergence (Correa-Aragunde et al., 2004) suggesting a role of NO in the regulation of root system growth and development. In another study, treatment of Arabidopsis seedlings with NO-donor enhanced LR primordia formation (Méndez-Bravo et al., 2015). In the process of LR development, NO is shown to affect cell-cycle regulatory genes and modulate cellulose synthesis (Correa-Aragunde et al., 2006, 2008).

During all the stages of LR development, endogenous NO biosynthesis as detected by DAF-2 DA, could be observed in the LR primordia (Correa-Aragunde et al., 2004). The molecular mechanism underlying the role of NO in LR initiation and elongation is not known. Studies on LR root formation in tomato shows NO modulation of cell-cycle regulatory genes is involved in G1-to-S phase transition.

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ROOT DEVELOPMENT | Lateral Root Initiation

J.G. Dubrovsky , T.L. Rost , in Encyclopedia of Applied Plant Sciences, 2003

When Does Initiation Start?

LRP initiation usually starts in the primary root after seed germination. However, in some plants LRP initiation actually starts during the development of the radicle in the embryo axis; cucumber (Cucumis sativum) is an example. In the radicle of mature cucumber embryos, LRPs are well developed and each consists of a few hundred cells. These primordia are initiated during embryo development opposite prospective protoxylem strands (Figure 1 ). In these species, lateral root emergence occurs within two to three days of germination.

Figure 1. Mature embryo of cucumber plant (Cucumus sativum cv Muromsky) 12   h after the start of seed imbibition. At this stage no cell division occurred. The 7-μm thick section was made in the plane of the cotyledons. Arrowheads indicate embryonic LRPs in the radicle that are located along the prospective protoxylem strands. In the upper part of the embryo, shoot apical meristem, leaf primordium and parts of cotyledons (to the right and to the left from the embryo) can be seen. Scale=200   μm. Photograph courtesy of Dr J.G. Dubrovsky.

In peas (Pisum sativum), preformed lateral roots also exist, but they cannot be observed unless the seeds are treated with a cell division inhibitor such as colchicine. Once treated, the emerging radicle can be seen to have up to 10 preformed lateral root primordia.

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Brassinosteroids' regulation of plant architecture

Xuewei Song , ... Xiaojian Xia , in Brassinosteroids in Plant Developmental Biology and Stress Tolerance, 2022

5.2 Role in the lateral root development

Lateral root development plays a crucial role in enhancing the ability of the root system to acquire water and nutrients from the soil. In most eudicot plants such as Arabidopsis and tomato, lateral roots are derived from the xylem pole pericycle cells of the primary root (Van Norman et al., 2013). The development of lateral roots comprises several distinct phases (Ivanchenko et al., 2015). First, some of the xylem pole pericycle cells in the transition zone undergo "priming." In the differentiation zone of the root, some pericycle cells become specified as lateral root founder cells. The stage I primordium forms as a result of the asymmetric anticlinal division of founder cells. Then, a two-cell layered primordium (stage II) forms, following periclinal cell division. Further development generates a dome-shaped primordium. Finally, the new lateral root establishes its own meristem and emerges through the overlying tissues of the parent root.

BR signaling is essential for lateral root development. Mutants with defects in BR perception displayed less lateral roots, and a reduced auxin response as indicated by the expression of DR5::GUS. Auxins are involved in different stages of lateral root development, including initiation, outgrowth, and emergence (Benkova et al., 2003; Lavenus et al., 2013). BRs are thought to promote the initiation of lateral root primordia through interacting with auxins (Bao et al., 2004). However, high BR levels suppress lateral root formation, possibly by inducing the expression of Aux/IAA genes, which encode suppressors of auxin signaling (Gupta et al., 2015). Intriguingly, BR biosynthesis in root tips and lateral roots was induced by auxins (Chung et al., 2011), suggesting that BRs acts downstream of auxins to promote lateral root development. Furthermore, auxins are found to induce the expression of BREVIS RADIX (BRX), which influences the expression of genes for rate-limiting enzymes in BR biosynthesis (Mouchel et al., 2006). However, the roles of BRX-mediated interaction between BRs and auxins in lateral root development need further studies.

The cysteine-rich peptides rapid alkalinization factors (RALFs) play a key role in cell-cell communications. Silencing of RALF1 resulted in an increase in the number of lateral roots, whereas RALF1 overexpression produced the opposite effect. Intriguingly, RALF1 and BR antagonistically regulate lateral root development (Bergonci et al., 2014). BAK1 as the coreceptor for multiple ligands is shared by both RALF and BR signaling pathways. The competition between BR and RALF signaling for BAK1 may account in part for the antagonistic interaction of BR and RALF (Dressano et al., 2017). The negative regulator of BR signaling BIN2 has been shown to be recruited by the TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF)-TDIF RECEPTOR (TDR) module to promote lateral root development (Cho et al., 2014). BIN2-mediated phosphorylation relieved suppression of ARF7 and ARF19 by AUX/IAAs, leading to their enhanced transcriptional activity toward marker genes of lateral root initiation.

Beside peptide signals, BRs also interact with sugar signals to coordinately control lateral root development. Glucose and BRs coordinately promote lateral root development at lower concentrations (Gupta et al., 2015). This study also provides genetic and physiological evidence indicating that BR signaling acts downstream of sugar signaling in regulating lateral root development. Sugar sensing by Target-of-rapamycin (TOR) plays a central role in reprogramming metabolic, cellular, and signaling processes in root development (Xiong et al., 2013). Recently, the TOR-mediated autophagy pathway was found to control the stability of BZR1 protein (Zhang et al., 2016). Further studies are required to reveal the mechanism of how BR signaling is regulated by sugar signal during lateral root development.

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Plant Development

Tom Bennett , Ben Scheres , in Current Topics in Developmental Biology, 2010

3.3 Lateral root formation

Lateral roots form as completely de novo organs, from divisions in the mature pericycle layer, although it has been suggested that certain pericycle cells are preconditioned to do this while residing in the basal MZ (de Smet et al., 2007). Auxin is well established as acting in several steps during lateral root formation, including the initial specification of the new primordium (recently reviewed in Péret et al., 2009). Once a new lateral root is specified, the characteristic pattern of auxin transport seen in primary roots is set-up in the developing primordium and this drives formation and growth of the new root (Benková et al., 2003). Recent attempts to model lateral root formation suggest that small differences in auxin levels in the pericycle could be sufficient to trigger formation of a lateral auxin reflux loop, which could couple lateral root specification, formation and growth (Laskowski et al., 2008).

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Auxin

Lawrence J. Hobbie , in Encyclopedia of Hormones, 2003

IV.D Auxin and Lateral Roots

Lateral roots are produced when cells in the pericycle, the layer of cells surrounding the central vascular cylinder, begin to divide, form additional cell layers that push through the outer cell layers of the primary root, and ultimately organize a second root meristem. Many lines of evidence indicate that lateral root development is promoted by transported auxin. Increasing the auxin concentration in roots causes increased lateral root formation. Approaches that have been used to increase auxin levels include mutations, transgene expression, and exogenous application of auxin to the entire root or to the stump of a severed root. Conversely, reducing auxin levels or response in the primary root leads to a decreased number of lateral roots. This is accomplished by inhibition of polar auxin transport at the root–shoot junction or by mutation-induced reductions in auxin response. Auxin appears to stimulate the division of the pericycle cells that initiate lateral root development and may also be required at the later stage of outgrowth.

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Root System Architecture

Paul A. Ingram , Jocelyn E. Malamy , in Advances in Botanical Research, 2010

2 Cell cycle control in the LRP

LRP formation involves the controlled progression of anti- and periclinal cell divisions and specific cell cycle components have been identified in the regulation of this process (de Jager et al., 2005; De Smet et al., 2006; Himanen et al., 2002; Malamy, 2005; Osmont et al., 2007 ). A detailed transcriptome study of lateral root initiation using a synchronised population of pericycle cells that were simultaneously activated to form LRP showed that all pericycle cells are initially held at the G1–S checkpoint ( Himanen et al., 2002). Consistent with this, the G1–S-specific CycD4;1 and CycD3;1 genes show expression associated with LRP initiation (De Veylder et al., 1999; Himanen et al., 2002). In addition, the G1–S-specific CDKA;1 is constitutively active in the xylem-pole pericycle cells (Himanen et al., 2002). Interestingly, over-expression of CycD3;1 in the pericycle did not lead to an increased number of LRP, showing that it is not sufficient to promote LRP initiation (de Jager et al., 2005). Certain xylem-pole pericycle cells then become competent to progress through the G1–S transition and on to the G2-M checkpoint (Casimiro et al., 2003). This is evidenced by later expression of the G2-M specific genes CycB1;1, CycB1;2, CDKB1;1 and CDKB2;2 in synchronised, initiating cells (Himanen et al., 2002). The CycB1;1 gene had been associated with LRP initiation previously (Doerner et al., 1996); however, ectopic expression of CycB1;1 with the CDKA;1 promoter failed to increase the number of LRP. This result shows that CycB1;1 alone is not sufficient to drive LRP initiation. Intriguingly, it was found that the CDK inhibitors KRP1 and KRP2 were initially highly expressed in synchronised, initiating pericycle cells and subsequently down-regulated within 4   h of lateral root initiation (Himanen et al., 2002). These results were corroborated later in a more extensive microarray study (Himanen et al., 2004). The down-regulation of these cell cycle inhibitors correlated with the progression of initiated pericycle cells through the cell cycle. Furthermore, over-expression of KRP2 resulted in the strong inhibition of LRP initiation. Therefore, a model has been proposed where: (1) KRP2 inhibits progression of xylem-pole pericycle cells through the cell cycle; (2) down-regulation of KRP2 in specific cells within a certain developmental window allows those cells to continue through the cell cycle and (3) other cells retain high KRP2 expression and are not competent to progress through the cell cycle (Casimiro et al., 2003; Himanen et al., 2002). The direct targets of KRP2 remain to be explored in greater detail, and one would propose that direct down-regulation of KRP2 targets would result in decreased LRP initiation, while the over-expression of those targets would overcome the LRP reduction in the KRP2 over-expressing background.

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Highlights in European Plant Biotechnology Research and Technology Transfer

Malcolm J. Bennett , ... Malcolm J. Bennett , in Developments in Plant Genetics and Breeding, 2000

Isolation of Arabidopsis root architectural mutants

Lateral root architecture directly influences the ability of a plant to colonise the soil, maximises nutrient acquisition and provides mechanical support. Adventitious roots derived from stem tissues and anchor roots emerging at the root-shoot junction likewise perform important mechanical and physiological roles in crops like maize. We describe below a series of screens to identify Arabidopsis mutants that modify adventitious, anchor and/or lateral root development.

Adventitious root mutants. Adventitious roots rarely emerge from non-root, light grown tissues such as the hypocotyl in wild-type Arabidopsis. However, we have observed that wild-type hypocotyl tissues are capable of forming significant numbers of adventitious roots following a short period of etiolation. An initial three-day period of seedling etiolation was determined to be optimal to stimulate several adventitious roots per wild-type hypocotyl. These conditions provided the basis to screen the En-1 gene machine for mutants that either failed to develop or formed elevated numbers of adventitious roots.

Several mutants that formed elevated numbers of adventitious roots under our screening conditions were identified within the En-1 gene machine. The mutants were termed medusa1 (Fig. 1A) and medusa2 (figure 1B) because they preferentially formed a ring of adventitious roots close to the apex of the seedling following etiolation. Neither mutant formed elevated numbers of adventitious roots under either constant light or dark grown conditions (figure 1A & B). Crosses between medusa1 and medusa2 confirmed that they were not allelic with one another. However, crosses with two existing adventitious root mutants, sur1 [5] and sur2 [6], confirmed that medusa2 was allelic to sur2 [7]. The medusa1 mutant was not allelic to either sur1 or sur2 and so potentially represents a novel locus controlling adventitious root formation.

Figure 1. Phenotypes of the medusa1, medusa2 and tripod mutants. The medusa1 (A) and medusa2 (B) seedlings were grown on MS agar under the following regimes; L–grown for 15 days in constant white light; D/L–grown for 1 day in the light followed by 3 days in the dark and 11 days in the light; D–grown for 15 days in the dark. Arrowheads indicate the position of the junction between the hypocotyl and the root. Seedlings were moved to a single plate for photography. (C) Three examples of tripod mutant seedlings which have been grown for 15 days on MS agar under constant light conditions.

Anchor root mutants Arabidopsis is capable of initiating anchor roots at the hypocotyl-root junction (figure 1C). However, anchor roots rarely emerge from wild-type Arabidopsis seedlings (less than 0.5%; Harmston & Bennett, unpublished results). Anchor root mutants were therefore identified on the basis of their ability to form one or more anchor roots. One anchor root mutant, termed tripod (tpd), forms a significantly increased number of anchor roots (figure 1C). Preliminary studies have observed that tpd seedlings initially produce a short primary root which stops elongating after ten days, followed by a pair of anchors roots that elongate to a similar length as the primary root, to create the characteristic three pronged tripod root architecture (figure 1C).

Lateral root mutants To date, only a handful of mutants have been identified on the basis of their lateral root phenotype in Arabidopsis. Mutations like alf4 and sur1 either abolish or exhibit an over-proliferation of lateral roots, respectively [8,5,9]. Visual screens for mutants exhibiting more subtle alterations in their lateral root development, spacing and/or number within the En-1 gene machine have proved unsuccessful.

Mutants that exhibit subtle differences in their lateral root architecture, such as tir3 and pas1, were originally identified as a result of a phytohormone-related defect [10,11]. Such observations have prompted us to perform a selection of phytohormone-based screens in order to identify root elongation and lateral root mutants. The antagonistic effects of auxin and cytokinin have been well documented for lateral root initiation [12]. IAA acts by stimulating cell division within pericycle tissues [13], whereas cytokinin treatment blocks lateral root development (figure 2). A screen for mutants with reduced auxin sensitive root elongation was performed since several auxin response mutants have been described to form fewer lateral roots [14]. In parallel, a screen designed to identify mutants that continued to form lateral roots in the presence of cytokinin was also performed. The latter screen required the inclusion of silver in order to block the inhibitory effects caused by cytokinin-induced ethylene production on root elongation (figure 2). Several mutants were identified which were subsequently characterised at the molecular level.

Figure 2. Cytokinin inhibits the formation of lateral roots in wild-type Arabidopsis thaliana. Wild-type (Columbia) seedlings were grown in the presence of various concentrations of benzyladenine (BA) with or without the addition of 20mM Ag+. The seedlings were grown for 11 days after which time the number of emerged lateral roots per mm of primary root were counted. Error bars represent the standard deviation (n=20).

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Apical Dominance and Some Other Phenomena Illustrating Correlative Effects of Hormones

Lalit M. Srivastava , in Plant Growth and Development: Hormones and Environment, 2002

1. ORIGIN OF LATERAL AND ADVENTITIOUS ROOTS

Lateral root primordia arise by localized cell divisions in the pericycle, resulting in a mound of tissue. Further oriented divisions and cell enlargement in the mound give rise to an organized structure, the root primordium, which acquires its own root apex and root cap and grows through the parent root cortex, finally emerging as a lateral rootlet ( Fig. 14-8).

FIGURE 14-8. Development of a lateral root in Zea mays. (A) A transverse section of the parent root showing an early stage. Periclinal and anticlinal divisions in the pericycle (P) opposite a xylem pole (Xy) herald the development of a lateral primordium. Arrowheads indicate the extent of pericycle tissue involved. An endodermis (E) is indicated by arrows. External to it are large cortical cells. (B) A longitudinal section of the parent root through the center of a lateral primordium at a later stage. Cell divisions in the pericycle have given rise to a mound of tissue composed of small, densely cytoplasmic cells. An endodermis is seen external to it. (C) A transverse section of the parent root through the center of a lateral primordium at a still later stage. The primordium is about half-way through the parent cortex; it has acquired its own root apex and root cap (RC). Provascular tissue (stele, S) and cortex (C) are also demarcated. The lateral primordium is growing toward the top left corner. Bar: 50 μm.

 From Bell and McCully (1970).

Adventitious roots, likewise, are initiated by cell divisions in the deeper-lying parenchyma cells associated with vascular tissues (stems and leaves of seed plants generally do not have a pericycle). A root primordium is organized similarly and then grows out as a new root.

Formation of a lateral or adventitious root thus has at least three stages: (i) induction of cell divisions in the hitherto "quiescent" pericyclic cells or parenchyma cells of vascular tissues, (ii) organization of a root primordium with its own root apex, root cap, and histological zonation, and (iii) growth of the primordium and its emergence as a lateral root. As in other developmental phenomena, these stages, especially the latter two, are not sharply delineated and partially overlap.

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Vegetative growth

Eduardo Primo-Millo , Manuel Agustí , in The Genus Citrus, 2020

10.5.2 Lateral root development

The lateral roots develop at a certain distance from the apical meristem of a higher root and originate from the pericycle ( Plate 10.7B). During the initiation of a lateral root, a group of cells of the pericycle undergoes periclinal and anticlinal divisions, giving rise to the formation of a protuberance, which is the primordium of a lateral root. When growing, the incipient root crosses the cortex of the main one, but before it emerges to the surface, the apical meristem and the calyptra appear already differentiated. In this phase, the endodermis divides anticlinally and forms a layer of cells on the surface of the primordium; shortly before the new root comes out the tissue derived from the endodermis disintegrates.

The vascular systems of the main and lateral roots are not totally independent. When the second one begins in the pericycle of the first one, the space that separates both conductive tissues is small and there are intermediate cells derived from the pericycle which differentiate into conductive cells, communicating both vascular systems.

Auxins are involved in the formation of lateral roots and are specifically required for the initial asymmetric divisions that give rise to the root primordium. Thus, the initiation of the lateral roots is preceded by an increase of auxin content. In addition, the localized application of synthetic auxins, such as indolebutyric acid or naphthaleneacetic acid, favors rooting (Ferguson et al., 1985; Moore, 1986; Primo-Millo, 1976; Primo-Millo and Harada, 1976).

The development of lateral roots is partially mediated by the transcription factor NAC1, whose expression is induced by auxins.

The formation of lateral root primordia can be controlled by the apical root meristem. In fact, detaching it stimulates lateral roots initiation.

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