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1.  The Production and Release of Living Root Cap Border Cells is a Function of Root Apical Meristem Type in Dicotyledonous Angiosperm Plants 
Annals of Botany  2006;97(5):917-923.
• Background and Aims The root apical meristems (RAM) of flowering plant roots are organized into recognizable pattern types. At present, there are no known ecological or physiological benefits to having one RAM organization type over another. Although there are phylogenetic distribution patterns in plant groups, the possible evolutionary advantages of different RAM organization patterns are not understood. Root caps of many flowering plant roots are known to release living border cells into the rhizosphere, where the cells are believed to have the capacity to alter conditions in the soil and to interact with soil micro-organisms. Consequently, high rates of border cell production may have the potential to benefit plant growth and development greatly, and to provide a selective advantage in certain soil environments. This study reports the use of several approaches to elucidate the anatomical and developmental relationships between RAM organization and border cell production.
• Methods RAM types from many species were compared with numbers of border cells released in those species. In addition, other species were grown, fixed and sectioned to verify their organization type and capacity to produce border cells. Root tips were examined microscopically to characterize their pattern and some were stained to determine the viability of root cap cells.
• Key Results The first report of a correlation between RAM organization type and the production and release of border cells is provided: species exhibiting open RAM organization produce significantly more border cells than species exhibiting closed apical organization. Roots with closed apical organization release peripheral root cap cells in sheets or large groups of dead cells, whereas root caps with open organization release individual living border cells.
• Conclusions This study, the first to document a relationship between RAM organization, root cap behaviour and a possible ecological benefit to the plant, may yield a framework to examine the evolutionary causes for the diversification of RAM organization types across taxa.
PMCID: PMC2803423  PMID: 16488922
Border cells; root caps; root apical organization; root meristem
2.  Differential spatial expression of A- and B-type CDKs, and distribution of auxins and cytokinins in the open transverse root apical meristem of Cucurbita maxima 
Annals of Botany  2010;107(7):1223-1234.
Background and Aims
Aside from those on Arabidopsis, very few studies have focused on spatial expression of cyclin-dependent kinases (CDKs) in root apical meristems (RAMs), and, indeed, none has been undertaken for open meristems. The extent of interfacing between cell cycle genes and plant growth regulators is also an increasingly important issue in plant cell cycle studies. Here spatial expression/localization of an A-type and B-type CDK, auxin and cytokinins are reported in relation to the hitherto unexplored anatomy of RAMs of Cucurbita maxima.
Median longitudinal sections were cut from 1-cm-long primary root tips of C. maxima. Full-length A-type CDKs and a B-type CDK were cloned from C. maxima using degenerate primers, probes of which were localized on sections of RAMs using in situ hybridization. Isopentenyladenine (iPA), trans-zeatin (t-Z) and indole-3yl-acetic acid (IAA) were identified on sections by immunolocalization.
Key Results
The C. cucurbita RAM conformed to an open transverse (OT) meristem typified by an absence of a clear boundary between the eumeristem and root cap columella, but with a distinctive longitudinally thickened epidermis. Cucma;CDKA;1 expression was detected strongly in the longitudinally thickened epidermis, a tissue with mitotic competence that contributes cells radially to the root cap of OT meristems. Cucma;CDKB2 was expressed mainly in proliferative regions of the RAM and in lateral root primordia. iPA and t-Z were mainly distributed in differentiated cells whilst IAA was distributed more uniformly in all tissues of the RAM.
Cucma;CDKA;1 was expressed most strongly in cells that have proliferative competence whereas Cucma;CDKB2 was confined mainly to mitotic cells. iPA and t-Z marked differentiated cells in the RAM, consistent with the known effect of cytokinins in promoting differentiation in root systems. iPA/t-Z were distributed in a converse pattern to Cucma;CDKB2 expression whereas IAA was detected in most cells in the RAM regardless of their proliferative potential.
PMCID: PMC3091794  PMID: 20601387
Auxin; cytokinins; CDKs; Cucurbita maxima; root apical meristems
3.  Influence of a Weak DC Electric Field on Root Meristem Architecture 
Annals of Botany  2007;100(4):791-796.
Background and Aims
Electric fields are an important environmental factor that can influence the development of plants organs. Such a field can either inhibit or stimulate root growth, and may also affect the direction of growth. Many developmental processes directly or indirectly depend upon the activity of the root apical meristem (RAM). The aim of this work was to examine the effects of a weak electric field on the organization of the RAM.
Roots of Zea mays seedlings, grown in liquid medium, were exposed to DC electric fields of different strengths from 0·5 to 1·5 V cm−1, with a frequency of 50 Hz, for 3 h. The roots were sampled for anatomical observation immediately after the treatment, and after 24 and 48 h of further undisturbed growth.
Key Results
DC fields of 1 and 1·5 V cm−1 resulted in noticeable changes in the cellular pattern of the RAM. The electric field activated the quiescent centre (QC): the cells of the QC penetrated the root cap junction, disturbing the organization of the closed meristem and changing it temporarily into the open type.
Even a weak electric field disturbs the pattern of cell divisions in plant root meristem. This in turn changes the global organization of the RAM. A field of slightly higher strength also damages root cap initials, terminating their division.
PMCID: PMC2749630  PMID: 17686761
Electric field; root apical meristem; quiescent centre; polar auxin transport; Zea mays
4.  Spatial and Directional Variation of Growth Rates in Arabidopsis Root Apex: A Modelling Study 
PLoS ONE  2013;8(12):e84337.
Growth and cellular organization of the Arabidopsis root apex are investigated in various aspects, but still little is known about spatial and directional variation of growth rates in very apical part of the apex, especially in 3D. The present paper aims to fill this gap with the aid of a computer modelling based on the growth tensor method. The root apex with a typical shape and cellular pattern is considered. Previously, on the basis of two types of empirical data: the published velocity profile along the root axis and dimensions of cell packets formed in the lateral part of the root cap, the displacement velocity field for the root apex was determined. Here this field is adopted to calculate the linear growth rate in different points and directions. The results are interpreted taking principal growth directions into account. The root apex manifests a significant anisotropy of the linear growth rate. The directional preferences depend on a position within the root apex. In the root proper the rate in the periclinal direction predominates everywhere, while in the root cap the predominating direction varies with distance from the quiescent centre. The rhizodermis is distinguished from the neighbouring tissues (cortex, root cap) by relatively high contribution of the growth rate in the anticlinal direction. The degree of growth anisotropy calculated for planes defined by principal growth directions and exemplary cell walls may be as high as 25. The changes in the growth rate variation are modelled.
PMCID: PMC3867472  PMID: 24367654
5.  ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1) is required for cell production, patterning, and morphogenesis in root development 
Journal of Experimental Botany  2014;65(22):6373-6384.
Methyltransferases maintain some genes in an active state. ATX1 regulates the timing of root development and is essential for stem cell niche maintenance and cell patterning during primary and lateral root development.
ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1/SDG27), a known regulator of flower development, encodes a H3K4histone methyltransferase that maintains a number of genes in an active state. In this study, the role of ATX1 in root development was evaluated. The loss-of-function mutant atx1-1 was impaired in primary root growth. The data suggest that ATX1 controls root growth by regulating cell cycle duration, cell production, and the transition from cell proliferation in the root apical meristem (RAM) to cell elongation. In atx1-1, the quiescent centre (QC) cells were irregular in shape and more expanded than those of the wild type. This feature, together with the atypical distribution of T-divisions, the presence of oblique divisions, and the abnormal cell patterning in the RAM, suggests a lack of coordination between cell division and cell growth in the mutant. The expression domain of QC-specific markers was expanded both in the primary RAM and in the developing lateral root primordia of atx1-1 plants. These abnormalities were independent of auxin-response gradients. ATX1 was also found to be required for lateral root initiation, morphogenesis, and emergence. The time from lateral root initiation to emergence was significantly extended in the atx1-1 mutant. Overall, these data suggest that ATX1 is involved in the timing of root development, stem cell niche maintenance, and cell patterning during primary and lateral root development. Thus, ATX1 emerges as an important player in root system architecture.
PMCID: PMC4246177  PMID: 25205583
Arabidopsis; lateral root development; patterning; root apical meristem; root development; root morphogenesis; root system.
6.  The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication 
The coordination of plant cell division and expansion controls plant morphogenesis, development, and growth. Cyclin-dependent kinases (CDKs) are not only key regulators of cell division but also play an important role in cell differentiation. In plants, CDK activity is modulated by the binding of INHIBITOR OF CDK/KIP-RELATED PROTEIN (ICK/KRP). Previously, ICK2/KRP2 has been shown to mediate auxin responses in lateral root initiation. Here are analysed the roles of all ICK/KRP genes in root growth. Analysis of ick/krp null-mutants revealed that only ick3/krp5 was affected in primary root growth. ICK3/KRP5 is strongly expressed in the root apical meristem (RAM), with lower expression in the expansion zone. ick3/krp5 roots grow more slowly than wildtype controls, and this results not from reduction of division in the proliferative region of the RAM but rather reduced expansion as cells exit the meristem. This leads to shorter final cell lengths in different tissues of the ick3/krp5 mutant root, particularly the epidermal non-hair cells, and this reduction in cell size correlates with reduced endoreduplication. Loss of ICK3/KRP5 also leads to delayed germination and in the mature embryo ICK3/KRP5 is specifically expressed in the transition zone between root and hypocotyl. Cells in the transition zone were smaller in the ick3/krp5 mutant, despite the absence of endoreduplication in the embryo suggesting a direct effect of ICK3/KRP5 on cell growth. It is concluded that ICK3/KRP5 is a positive regulator of both cell growth and endoreduplication.
PMCID: PMC3580825  PMID: 23440171
Arabidopsis; CDK; cell cycle; cell division; cell expansion; development; root growth
7.  Arabidopsis CULLIN3 Genes Regulate Primary Root Growth and Patterning by Ethylene-Dependent and -Independent Mechanisms 
PLoS Genetics  2009;5(1):e1000328.
CULLIN3 (CUL3) together with BTB-domain proteins form a class of Cullin-RING ubiquitin ligases (called CRL3s) that control the rapid and selective degradation of important regulatory proteins in all eukaryotes. Here, we report that in the model plant Arabidopsis thaliana, CUL3 regulates plant growth and development, not only during embryogenesis but also at post-embryonic stages. First, we show that CUL3 modulates the emission of ethylene, a gaseous plant hormone that is an important growth regulator. A CUL3 hypomorphic mutant accumulates ACS5, the rate-limiting enzyme in ethylene biosynthesis and as a consequence exhibits a constitutive ethylene response. Second, we provide evidence that CUL3 regulates primary root growth by a novel ethylene-dependant pathway. In particular, we show that CUL3 knockdown inhibits primary root growth by reducing root meristem size and cell number. This phenotype is suppressed by ethylene-insensitive or resistant mutations. Finally, we identify a function of CUL3 in distal root patterning, by a mechanism that is independent of ethylene. Thus, our work highlights that CUL3 is essential for the normal division and organisation of the root stem cell niche and columella root cap cells.
Author Summary
Ubiquitin-mediated proteolysis plays a central role in controlling intracellular levels of essential regulatory molecules in all eukaryotic organisms. This protein degradation pathway has a large number of components, including hundreds of ubiquitin protein ligases (E3s) that are predicted to have regulatory roles in cell homeostasis, cell cycle control, and development. Recent research revealed the molecular composition of CULLIN3 (CUL3)-based E3 ligases, which are essential enzymes in both metazoans and plants. Here, we report that in the model plant A. thaliana, CUL3 modulates the emission of ethylene, a gaseous plant hormone that controls a variety of processes such as fruit ripening and stress response. In particular, we provide evidence that CUL3 regulates root growth by a novel ethylene-dependant pathway. Thus, we showed that CUL3 knockdown inhibits primary root growth by reducing the root meristem size. Finally, we also identified a function of CUL3 in distal root patterning. Indeed, CUL3 function is required for normal division and organisation of the root stem cell niche and columella root cap cells. Overall, our results show that Arabidopsis CUL3 is essential for plant growth and development, not only during embryogenesis but also at post-embryonic stages.
PMCID: PMC2607017  PMID: 19132085
8.  Root System Architecture from Coupling Cell Shape to Auxin Transport 
PLoS Biology  2008;6(12):e307.
Lateral organ position along roots and shoots largely determines plant architecture, and depends on auxin distribution patterns. Determination of the underlying patterning mechanisms has hitherto been complicated because they operate during growth and division. Here, we show by experiments and computational modeling that curvature of the Arabidopsis root influences cell sizes, which, together with tissue properties that determine auxin transport, induces higher auxin levels in the pericycle cells on the outside of the curve. The abundance and position of the auxin transporters restricts this response to the zone competent for lateral root formation. The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation. Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition. Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.
Author Summary
Plant architecture is determined by where shoots or roots form along the main axis, but the mechanism responsible for lateral root initiation has long puzzled biologists. Here, we show that stretching root cells initiates changes in hormone transport, leading to lateral root initiation in plants, thereby solving a 120-year-old mystery: the mechanism of lateral root initiation. Our data reveal that physical tissue deformation is sufficient to induce chemical changes that unleash biological responses leading to new organ formation. When roots bend, concentrations of the plant hormone auxin increase along the outside of the bend. A complex auxin flux pattern is generated that further enhances auxin levels through localized reflux loops. Auxin importers—AUX1—and efflux carriers—PIN proteins—are known to be regulated by auxin. AUX1 up-regulation enhances the auxin maxima that specify the lateral root founder cells at the bend, while PIN down-regulation modulates the lateral spacing of the roots along the main root axis. This study shows that the biological regulation behind pattern formation can be a result of entangled hierarchies, explaining both the inner/outer spacing, lateral inhibition, and dynamics of lateral root initiation.
Experimental data and computer modeling show that lateral root positioning can be controlled by the physical stimulus of root curvature, which triggers self-organizing alterations in auxin transport.
PMCID: PMC2602721  PMID: 19090618
9.  A method to determine the displacement velocity field in the apical region of the Arabidopsis root 
Planta  2012;236(5):1547-1557.
In angiosperms, growth of the root apex is determined by the quiescent centre. All tissues of the root proper and the root cap are derived from initial cells that surround this zone. The diversity of cell lineages originated from these initials suggests an interesting variation of the displacement velocity within the root apex. However, little is known about this variation, especially in the most apical region including the root cap. This paper shows a method of determination of velocity field for this region taking the Arabidopsis root apex as example. Assuming the symplastic growth without a rotation around the root axis, the method combines mathematical modelling and two types of empirical data: the published velocity profile along the root axis above the quiescent centre, and dimensions of cell packet originated from the initials of epidermis and lateral root cap. The velocities, calculated for points of the axial section, vary in length and direction. Their length increases with distance from the quiescent centre, in the root cap at least twice slower than in the root proper, if points at similar distance from the quiescent centre are compared. The vector orientation depends on the position of a calculation point, the widest range of angular changes, reaching almost 90°, in the lateral root cap. It is demonstrated how the velocity field is related to both distribution of growth rates and growth-resulted deformation of the cell wall system. Also changes in the field due to cell pattern asymmetry and differences in slope of the velocity profile are modelled.
Electronic supplementary material
The online version of this article (doi:10.1007/s00425-012-1707-x) contains supplementary material, which is available to authorized users.
PMCID: PMC3481058  PMID: 22828709
Arabidopsis root apex; Displacement velocities; Mathematical modelling; Velocity field
10.  Influence of root-bed size on the response of tobacco to elevated CO2 as mediated by cytokinins 
AoB Plants  2014;6:plu010.
The effect of elevated CO2 on the growth of tobacco under high light (16 h), continuous water and nutrient supply was investigated. Biomass production depended strongly on the size of the root bed. Inhibition by a small root bed was higher at 700 than at 360 ppm CO2. Relative growth rates showed a head-start of the high-CO2 plants which gave rise to a persistently higher biomass production. Root-bed size and CO2 concentration were mirrored by the quantitative cytokinin patterns of the various plant parts. Amounts of the cytokinins moving from the root to the shoot were higher in high-CO2 plants.
The extent of growth stimulation of C3 plants by elevated CO2 is modulated by environmental factors. Under optimized environmental conditions (high light, continuous water and nutrient supply, and others), we analysed the effect of an elevated CO2 atmosphere (700 ppm, EC) and the importance of root-bed size on the growth of tobacco. Biomass production was consistently higher under EC. However, the stimulation was overridden by root-bed volumes that restricted root growth. Maximum growth and biomass production were obtained at a root bed of 15 L at ambient and elevated CO2 concentrations. Starting with seed germination, the plants were strictly maintained under ambient or elevated CO2 until flowering. Thus, the well-known acclimation effect of growth to enhanced CO2 did not occur. The relative growth rates of EC plants exceeded those of ambient-CO2 plants only during the initial phases of germination and seedling establishment. This was sufficient for a persistently higher absolute biomass production by EC plants in non-limiting root-bed volumes. Both the size of the root bed and the CO2 concentration influenced the quantitative cytokinin patterns, particularly in the meristematic tissues of shoots, but to a smaller extent in stems, leaves and roots. In spite of the generally low cytokinin concentrations in roots, the amounts of cytokinins moving from the root to the shoot were substantially higher in high-CO2 plants. Because the cytokinin patterns of the (xylem) fluid in the stems did not match those of the shoot meristems, it is assumed that cytokinins as long-distance signals from the roots stimulate meristematic activity in the shoot apex and the sink leaves. Subsequently, the meristems are able to synthesize those phytohormones that are required for the cell cycle. Root-borne cytokinins entering the shoot appear to be one of the major control points for the integration of various environmental cues into one signal for optimized growth.
PMCID: PMC4038427  PMID: 24790131
Biomass portioning; C/N ratio; cytokinins; elevated CO2; growth; root-bed volume; tobacco.
11.  Determinate Root Growth and Meristem Maintenance in Angiosperms 
Annals of Botany  2007;101(3):319-340.
The difference between indeterminate and determinate growth in plants consists of the presence or absence of an active meristem in the fully developed organ. Determinate root growth implies that the root apical meristem (RAM) becomes exhausted. As a consequence, all cells in the root tip differentiate. This type of growth is widely found in roots of many angiosperm taxa and might have evolved as a developmental adaptation to water deficit (in desert Cactaceae), or low mineral content in the soil (proteoid roots in various taxa).
Scope and Conclusions
This review considers the mechanisms of determinate root growth to better understand how the RAM is maintained, how it functions, and the cellular and genetic bases of these processes. The role of the quiescent centre in RAM maintenance and exhaustion will be analysed. During root ageing, the RAM becomes smaller and its organization changes; however, it remains unknown whether every root is truly determinate in the sense that its RAM becomes exhausted before senescence. We define two types of determinate growth: constitutive where determinacy is a natural part of root development; and non-constitutive where determinacy is induced usually by an environmental factor. Determinate root growth is proposed to include two phases: the indeterminate growth phase, when the RAM continuously produces new cells; and the termination growth phase, when cell production gradually decreases and eventually ceases. Finally, new concepts regarding stem cells and a stem cell niche are discussed to help comprehend how the meristem is maintained in a broad taxonomic context.
PMCID: PMC2701811  PMID: 17954472
Angiosperms; determinate root growth; indeterminate growth; meristem maintenance; quiescent centre; root apical meristem; root development; stem cells; stem cell niche
12.  Anatomical aspects of angiosperm root evolution 
Annals of Botany  2013;112(2):223-238.
Background and Aims
Anatomy had been one of the foundations in our understanding of plant evolutionary trends and, although recent evo-devo concepts are mostly based on molecular genetics, classical structural information remains useful as ever. Of the various plant organs, the roots have been the least studied, primarily because of the difficulty in obtaining materials, particularly from large woody species. Therefore, this review aims to provide an overview of the information that has accumulated on the anatomy of angiosperm roots and to present possible evolutionary trends between representatives of the major angiosperm clades.
This review covers an overview of the various aspects of the evolutionary origin of the root. The results and discussion focus on angiosperm root anatomy and evolution covering representatives from basal angiosperms, magnoliids, monocots and eudicots. We use information from the literature as well as new data from our own research.
Key Findings
The organization of the root apical meristem (RAM) of Nymphaeales allows for the ground meristem and protoderm to be derived from the same group of initials, similar to those of the monocots, whereas in Amborellales, magnoliids and eudicots, it is their protoderm and lateral rootcap which are derived from the same group of initials. Most members of Nymphaeales are similar to monocots in having ephemeral primary roots and so adventitious roots predominate, whereas Amborellales, Austrobaileyales, magnoliids and eudicots are generally characterized by having primary roots that give rise to a taproot system. Nymphaeales and monocots often have polyarch (heptarch or more) steles, whereas the rest of the basal angiosperms, magnoliids and eudicots usually have diarch to hexarch steles.
Angiosperms exhibit highly varied structural patterns in RAM organization; cortex, epidermis and rootcap origins; and stele patterns. Generally, however, Amborellales, magnoliids and, possibly, Austrobaileyales are more similar to eudicots, and the Nymphaeales are strongly structurally associated with the monocots, especially the Acorales.
PMCID: PMC3698381  PMID: 23299993
Anatomy; angiosperms; cortex; epidermis; evolution; roots; vascular tissue
13.  Structural Interaction Between GFP-Labeled Diazotrophic Endophytic Bacterium Herbaspirillum seropedicae RAM10 and Pineapple Plantlets ‘VitóRia’ 
Brazilian Journal of Microbiology  2011;42(1):114-125.
The events involved in the structural interaction between the diazotrophic endophytic bacterium Herbaspirillum seropedicae, strain RAM10, labeled with green fluorescent protein, and pineapple plantlets ‘Vitória’ were evaluated by means of bright-field and fluorescence microscopy, combined with scanning electron microscopy for 28 days after inoculation. After 6 hours of inoculation, H. seropedicae was already adhered to the roots, colonizing mainly root hair surface and bases, followed by epidermal cell wall junctions. Bacteria adherence in the initial periods occurred mainly in the form of solitary cells and small aggregates with pleomorphic cells. Bacteria infection of root tissue occurred through the cavities caused by the disruption of epidermal cells during the emergence of lateral roots and the endophytic establishment by the colonization of intercellular spaces of the cortical parenchyma. Moreover, within 1 day after inoculation the bacteria were colonizing the shoots. In this region, the preferred sites of epiphytic colonization were epidermal cell wall junctions, peltate scutiform trichomes and non-glandular trichomes. Subsequently, the bacteria occupied the outer periclinal walls of epidermal cells and stomata. The penetration into the shoot occurred passively through stoma aperture followed by the endophytic establishment on the substomatal chambers and spread to the intercellular spaces of spongy chlorenchyma. After 21 days of inoculation, bacterial biofilm were seen at the root hair base and on epidermal cell wall surface of root and leaf, also confirming the epiphytic nature of H. seropedicae.
PMCID: PMC3768922  PMID: 24031612
Ananas comosus; plant-growth promoting bacteria; microscopy
14.  Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases 
eLife  2014;3:e02525.
In Arabidopsis, root hair and non-hair cell fates are determined by a MYB-bHLH-WD40 transcriptional complex and are regulated by many internal and environmental cues. Brassinosteroids play important roles in regulating root hair specification by unknown mechanisms. Here, we systematically examined root hair phenotypes in brassinosteroid-related mutants, and found that brassinosteroid signaling inhibits root hair formation through GSK3-like kinases or upstream components. We found that with enhanced brassinosteroid signaling, GL2, a cell fate marker for non-hair cells, is ectopically expressed in hair cells, while its expression in non-hair cells is suppressed when brassinosteroid signaling is reduced. Genetic analysis demonstrated that brassinosteroid-regulated root epidermal cell patterning is dependent on the WER-GL3/EGL3-TTG1 transcriptional complex. One of the GSK3-like kinases, BIN2, interacted with and phosphorylated EGL3, and EGL3s mutated at phosphorylation sites were retained in hair cell nuclei. BIN2 phosphorylated TTG1 to inhibit the activity of the WER-GL3/EGL3-TTG1 complex. Thus, our study provides insights into the mechanism of brassinosteroid regulation of root hair patterning.
eLife digest
Roots anchor a plant into the ground, and allow the plant to absorb water and mineral nutrients from the soil. As roots grow and branch, they increase the surface area of root exposed to the soil—and many plant cells in the root's outer layer have a hair-like projection to further increase this surface area. Thus, root hairs are where most water and mineral nutrients are absorbed. Many factors affect whether, or not, a plant cell will develop into a root hair. These factors include both external cues (such as the mineral content of the soil) and signals from the plant itself (such as hormones).
Brassinosteroids are plant hormones that regulate the development of shoots and roots, as well as the timing of when flowers begin to develop. These hormones are detected on the outside of plant cells, and activate a signaling pathway within the cell that causes changes in gene expression. Brassinosteroids also control if a root cell will become a hair cell or not, although the mechanism behind this activity is unclear.
Here, Cheng et al. have looked at the root hairs of mutant Arabidopsis thaliana plants that have had individual genes involved in brassinosteroid signaling knocked-out. Plant biologists commonly study this plant species because it is small and grows quickly—and Arabidopsis has regular stripes of root hair cells and ‘non-hair cells’ in the outer layer of its roots. Cheng et al. reveal that brassinosteroids prevent the formation of root hairs via signaling pathways that involve proteins called GSK3-like kinases. These hormones ‘switch off’ these kinases’ activity, so knocking-out the genes that code for these kinases has the same effect as adding extra brassinosteroids to the plant roots: fewer root hair cells.
Cheng et al. show that one of the GSK3-like kinases binds and adds phosphate groups to protein complexes that control gene expression—and this causes these protein complexes to be less active. When GSK3-like kinase activity is switched off by brassinosteroids, these complexes instead become more active and trigger the expression of genes that direct a plant cell to become a non-hair cell.
The findings of Cheng et al. reveal the pathways that allow brassinosteroids to stop plant cells in roots from becoming hair cells, and that instead encourage these cells to become non-hair cells. However, further work is needed to uncover how the striped pattern of hair cells and non-hair cells on Arabidopsis roots is established, and how brassinosteroids work with other plant hormones to control this pattern.
PMCID: PMC4005458  PMID: 24771765
brassinosteroids; GSK3-like kinases; root epidermal cell fate; EGL3; phosphorylation; TTG1; Arabidopsis
15.  Association of Azospirillum with Grass Roots † 
The association between grass roots and Azospirillum brasilense Sp 7 was investigated by the Fahraeus slide technique, using nitrogen-free medium. Young inoculated roots of pearl millet and guinea grass produced more mucilaginous sheath (mucigel), root hairs, and lateral roots than did uninoculated sterile controls. The bacteria were found within the mucigel that accumulated on the root cap and along the root axes. Adherent bacteria were associated with granular material on root hairs and fibrillar material on undifferentiated epidermal cells. Significantly fewer numbers of azospirilla attached to millet root hairs when the roots were grown in culture medium supplemented with 5 mM potassium nitrate. Under these growth conditions, bacterial attachment to undifferentiated epidermal cells was unaffected. Aseptically collected root exudate from pearl millet contained substances which bound to azospirilla and promoted their adsorption to the root hairs. This activity was associated with nondialyzable and proteasesensitive substances in root exudate. Millet root hairs adsorbed azospirilla in significantly higher numbers than cells of Rhizobium, Pseudomonas, Azotobacter, Klebsiella, or Escherichia. Pectolytic activities, including pectin transeliminase and endopolygalacturonase, were detected in pure cultures of A. brasilense when this species was grown in a medium containing pectin. These studies describe colonization of grass root surfaces by A. brasilense and provide a possible explanation for the limited colonization of intercellular spaces of the outer root cortex.
PMCID: PMC291307  PMID: 16345490
16.  Lateral root development in the maize (Zea mays) lateral rootless1 mutant 
Annals of Botany  2013;112(2):417-428.
Background and Aims
The maize lrt1 (lateral rootless1) mutant is impaired in its development of lateral roots during early post-embryonic development. The aim of this study was to characterize, in detail, the influences that the mutation exerts on lateral root initiation and the subsequent developments, as well as to describe the behaviour of the entire plant under variable environmental conditions.
Mutant lrt1 plants were cultivated under different conditions of hydroponics, and in between sheets of moist paper. Cleared whole mounts and anatomical sections were used in combination with both selected staining procedures and histochemical tests to follow root development. Root surface permeability tests and the biochemical quantification of lignin were performed to complement the structural data.
Key Results
The data presented suggest a redefinition of lrt1 function in lateral roots as a promoter of later development; however, neither the complete absence of lateral roots nor the frequency of their initiation is linked to lrt1 function. The developmental effects of lrt1 are under strong environmental influences. Mutant primordia are affected in structure, growth and emergence; and the majority of primordia terminate their growth during this last step, or shortly thereafter. The lateral roots are impaired in the maintenance of the root apical meristem. The primary root shows disturbances in the organization of both epidermal and subepidermal layers. The lrt1-related cell-wall modifications include: lignification in peripheral layers, the deposition of polyphenolic substances and a higher activity of peroxidase.
The present study provides novel insights into the function of the lrt1 gene in root system development. The lrt1 gene participates in the spatial distribution of initiation, but not in its frequency. Later, the development of lateral roots is strongly affected. The effect of the lrt1 mutation is not as obvious in the primary root, with no influences observed on the root apical meristem structure and maintenance; however, development of the epidermis and cortex are impaired.
PMCID: PMC3698386  PMID: 23456690
Zea mays; lrt1; lateral root; lateral root emergence; root apical meristem; lignin; peroxidase
17.  Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance 
Annals of Botany  2012;110(2):349-360.
Background and Aims
The root apical meristem (RAM) is the plant stem cell niche which provides for the formation and continuous development of the root. Auxin is the main regulator of RAM functioning, and auxin maxima coincide with the sites of RAM initiation and maintenance. Auxin gradients are formed due to local auxin biosynthesis and polar auxin transport. The PIN family of auxin transporters plays a critical role in polar auxin transport, and two mechanisms of auxin maximum formation in the RAM based on PIN-mediated auxin transport have been proposed to date: the reverse fountain and the reflected flow mechanisms.
The two mechanisms are combined here in in silico studies of auxin distribution in intact roots and roots cut into two pieces in the proximal meristem region. In parallel, corresponding experiments were performed in vivo using DR5::GFP Arabidopsis plants.
Key Results
The reverse fountain and the reflected flow mechanism naturally cooperate for RAM patterning and maintenance in intact root. Regeneration of the RAM in decapitated roots is provided by the reflected flow mechanism. In the excised root tips local auxin biosynthesis either alone or in cooperation with the reverse fountain enables RAM maintenance.
The efficiency of a dual-mechanism model in guiding biological experiments on RAM regeneration and maintenance is demonstrated. The model also allows estimation of the concentrations of auxin and PINs in root cells during development and under various treatments. The dual-mechanism model proposed here can be a powerful tool for the study of several different aspects of auxin function in root.
PMCID: PMC3394645  PMID: 22510326
Auxin response; root apical meristem; patterning; reverse fountain; reflected flow; mathematical model; Arabidopsis thaliana
18.  Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the Schizosaccharomyces pombe mitotic inducer, cdc25 
BMC Plant Biology  2012;12:45.
Entry into mitosis is regulated by cyclin dependent kinases that in turn are phosphoregulated. In most eukaryotes, phosphoregulation is through WEE1 kinase and CDC25 phosphatase. In higher plants a homologous CDC25 gene is unconfirmed and hence the mitotic inducer Schizosaccharomyces pombe (Sp) cdc25 has been used as a tool in transgenic plants to probe cell cycle function. Expression of Spcdc25 in tobacco BY-2 cells accelerates entry into mitosis and depletes cytokinins; in whole plants it stimulates lateral root production. Here we show, for the first time, that alterations to cytokinin and ethylene signaling explain the rooting phenotype elicited by Spcdc25 expression in Arabidopsis.
Expressing Spcdc25 in Arabidopsis results in increased formation of lateral and adventitious roots, a reduction of primary root width and more isodiametric cells in the root apical meristem (RAM) compared with wild type. Furthermore it stimulates root morphogenesis from hypocotyls when cultured on two way grids of increasing auxin and cytokinin concentrations. Microarray analysis of seedling roots expressing Spcdc25 reveals that expression of 167 genes is changed by > 2-fold. As well as genes related to stress responses and defence, these include 19 genes related to transcriptional regulation and signaling. Amongst these was the up-regulation of genes associated with ethylene synthesis and signaling. Seedlings expressing Spcdc25 produced 2-fold more ethylene than WT and exhibited a significant reduction in hypocotyl length both in darkness or when exposed to 10 ppm ethylene. Furthermore in Spcdc25 expressing plants, the cytokinin receptor AHK3 was down-regulated, and endogenous levels of iPA were reduced whereas endogeous IAA concentrations in the roots increased.
We suggest that the reduction in root width and change to a more isodiametric cell phenotype in the RAM in Spcdc25 expressing plants is a response to ethylene over-production. The increased rooting phenotype in Spcdc25 expressing plants is due to an increase in the ratio of endogenous auxin to cytokinin that is known to stimulate an increased rate of lateral root production. Overall, our data reveal important cross talk between cell division and plant growth regulators leading to developmental changes.
PMCID: PMC3362767  PMID: 22452972
19.  Endodermal cell–cell contact is required for the spatial control of Casparian band development in Arabidopsis thaliana 
Annals of Botany  2012;110(2):361-371.
Background and Aims
Apoplasmic barriers in plants fulfil important roles such as the control of apoplasmic movement of substances and the protection against invasion of pathogens. The aim of this study was to describe the development of apoplasmic barriers (Casparian bands and suberin lamellae) in endodermal cells of Arabidopsis thaliana primary root and during lateral root initiation.
Modifications of the endodermal cell walls in roots of wild-type Landsberg erecta (Ler) and mutants with defective endodermal development – scarecrow-3 (scr-3) and shortroot (shr) – of A. thaliana plants were characterized by light, fluorescent, confocal laser scanning, transmission and cryo-scanning electron microscopy.
Key Results
In wild-type plant roots Casparian bands initiate at approx. 1600 µm from the root cap junction and suberin lamellae first appear on the inner primary cell walls at approx. 7000–8000 µm from the root apex in the region of developing lateral root primordia. When a single cell replaces a pair of endodermal and cortical cells in the scr-3 mutant, Casparian band-like material is deposited ectopically at the junction between this ‘cortical’ cell and adjacent pericycle cells. Shr mutant roots with an undeveloped endodermis deposit Casparian band-like material in patches in the middle lamellae of cells of the vascular cylinder. Endodermal cells in the vicinity of developing lateral root primordia develop suberin lamellae earlier, and these are thicker, compared wih the neighbouring endodermal cells. Protruding primordia are protected by an endodermal pocket covered by suberin lamellae.
The data suggest that endodermal cell–cell contact is required for the spatial control of Casparian band development. Additionally, the endodermal cells form a collet (collar) of short cells covered by a thick suberin layer at the base of lateral root, which may serve as a barrier constituting a ‘safety zone’ protecting the vascular cylinder against uncontrolled movement of water, solutes or various pathogens.
PMCID: PMC3394653  PMID: 22645115
Apoplasmic (apoplastic) barriers; Arabidopsis thaliana; Casparian band; development; endodermis; lateral roots; lignin; suberin; suberin lamellae
20.  A SCARECROW-RETINOBLASTOMA Protein Network Controls Protective Quiescence in the Arabidopsis Root Stem Cell Organizer 
PLoS Biology  2013;11(11):e1001724.
Ben Scheres and colleagues report that in the growing tip of plant roots, a gene regulatory network that includes the plant homologue of Retinoblastoma regulates the divisions of long-term stem cells to replenish tissue and to protect the root stem cell niche.
Quiescent long-term somatic stem cells reside in plant and animal stem cell niches. Within the Arabidopsis root stem cell population, the Quiescent Centre (QC), which contains slowly dividing cells, maintains surrounding short-term stem cells and may act as a long-term reservoir for stem cells. The RETINOBLASTOMA-RELATED (RBR) protein cell-autonomously reinforces mitotic quiescence in the QC. RBR interacts with the stem cell transcription factor SCARECROW (SCR) through an LxCxE motif. Disruption of this interaction by point mutation in SCR or RBR promotes asymmetric divisions in the QC that renew short-term stem cells. Analysis of the in vivo role of quiescence in the root stem cell niche reveals that slow cycling within the QC is not needed for structural integrity of the niche but allows the growing root to cope with DNA damage.
Author Summary
In the plant Arabidposis thaliana, root meristems (in the growing tip of the root) contain slowly dividing cells that act as an organizing center for the root stem cells that surround them. This centre is called the quiescent centre (QC). In this study, we show that the slow rate of division in the QC is regulated by the interaction between two proteins: Retinoblastoma homolog (RBR) and SCARECROW (SCR), a transcription factor that controls stem cell maintenance. RBR and SCR regulate quiescence in the QC by repressing an asymmetric cell division that generates short-term stem cells. Here we genetically manipulate the cells in the QC to alter their quiescence by regulating the RBR/SCR interaction to demonstrate that quiescence is not needed for the organizing capacity of the QC but instead provides cells with a higher resistance to genotoxic stress, allowing stem cells in the QC to survive even if more rapidly cycling stem cells are damaged. A role for mitotic quiescence has been reported in animal stem cells, in which Rb has been implicated. These findings indicate that it might serve a similar role in plant stem cells.
PMCID: PMC3841101  PMID: 24302889
21.  Effect of mechanical stress on Zea root apex. I. Mechanical stress leads to the switch from closed to open meristem organization 
Journal of Experimental Botany  2011;62(13):4583-4593.
The effect of mechanical stress on the root apical meristem (RAM) organization of Zea mays was investigated. In the experiment performed, root apices were grown through a narrowing of either circular (variant I) or elliptical (variant II) shape. This caused a mechanical impedance distributed circumferentially or from the opposite sides in variant I and II, respectively. The maximal force exerted by the growing root in response to the impedance reached the value of 0.15 N for variant I and 0.08 N for variant II. Significant morphological and anatomical changes were observed. The changes in morphology depended on the variant and concerned diminishing and/or deformation of the cross-section of the root apex, and buckling and swelling of the root. Anatomical changes, similar in both variants, concerned transformation of the meristem from closed to open, an increase in the number of the cell layers at the pole of the root proper, and atypical oblique divisions of the root cap cells. After leaving the narrowing, a return to both typical cellular organization and morphology of the apex was observed. The results are discussed in terms of three aspects: the morphological response, the RAM reorganization, and mechanical factors. Assuming that the orientation of division walls is affected by directional cues of a tensor nature, the changes mentioned may indicate that a pattern of such cues is modified when the root apex passes through the narrowing, but its primary mode is finally restored.
PMCID: PMC3170553  PMID: 21659665
Mechanical stress; root apical meristem organization; tiers of initials; Zea mays
22.  Synchronous high-resolution phenotyping of leaf and root growth in Nicotiana tabacum over 24-h periods with GROWMAP-plant 
Plant Methods  2013;9:2.
Root growth is highly responsive to temporal changes in the environment. On the contrary, diel (24 h) leaf expansion in dicot plants is governed by endogenous control and therefore its temporal pattern does not strictly follow diel changes in the environment. Nevertheless, root and shoot are connected with each other through resource partitioning and changing environments for one organ could affect growth of the other organ, and hence overall plant growth.
We developed a new technique, GROWMAP-plant, to monitor growth processes synchronously in leaf and root of the same plant with a high resolution over the diel period. This allowed us to quantify treatment effects on the growth rates of the treated and non-treated organ and the possible interaction between them. We subjected the root system of Nicotiana tabacum seedlings to three different conditions: constant darkness at 22°C (control), constant darkness at 10°C (root cooling), and 12 h/12 h light–dark cycles at 22°C (root illumination). In all treatments the shoot was kept under the same 12 h/12 h light–dark cycles at 22°C. Root growth rates were found to be constant when the root-zone environment was kept constant, although the root cooling treatment significantly reduced root growth. Root velocity was decreased after light-on and light-off events of the root illumination treatment, resulting in diel root growth rhythmicity. Despite these changes in root growth, leaf growth was not affected substantially by the root-zone treatments, persistently showing up to three times higher nocturnal growth than diurnal growth.
GROWMAP-plant allows detailed synchronous growth phenotyping of leaf and root in the same plant. Root growth was very responsive to the root cooling and root illumination, while these treatments altered neither relative growth rate nor diel growth pattern in the seedling leaf. Our results that were obtained simultaneously in growing leaves and roots of the same plants corroborate the high sensitivity of root growth to the environment and the contrasting robustness of diel growth patterns in dicot leaves. Further, they also underpin the importance to carefully control the experimental conditions for root growth analysis to avoid or/and minimize artificial complications.
PMCID: PMC3573902  PMID: 23343327
Growth; Phenotyping; Diel; Diurnal; Temperature; Leaf; Shoot; Root; Nicotiana tabacum; Circadian
23.  Determinate primary root growth as an adaptation to aridity in Cactaceae: towards an understanding of the evolution and genetic control of the trait 
Annals of Botany  2013;112(2):239-252.
Background and Aims
Species of Cactaceae are well adapted to arid habitats. Determinate growth of the primary root, which involves early and complete root apical meristem (RAM) exhaustion and differentiation of cells at the root tip, has been reported for some Cactoideae species as a root adaptation to aridity. In this study, the primary root growth patterns of Cactaceae taxa from diverse habitats are classified as being determinate or indeterminate, and the molecular mechanisms underlying RAM maintenance in Cactaceae are explored. Genes that were induced in the primary root of Stenocereus gummosus before RAM exhaustion are identified.
Primary root growth was analysed in Cactaceae seedlings cultivated in vertically oriented Petri dishes. Differentially expressed transcripts were identified after reverse northern blots of clones from a suppression subtractive hybridization cDNA library.
Key Results
All species analysed from six tribes of the Cactoideae subfamily that inhabit arid and semi-arid regions exhibited determinate primary root growth. However, species from the Hylocereeae tribe, which inhabit mesic regions, exhibited mostly indeterminate primary root growth. Preliminary results suggest that seedlings of members of the Opuntioideae subfamily have mostly determinate primary root growth, whereas those of the Maihuenioideae and Pereskioideae subfamilies have mostly indeterminate primary root growth. Seven selected transcripts encoding homologues of heat stress transcription factor B4, histone deacetylase, fibrillarin, phosphoethanolamine methyltransferase, cytochrome P450 and gibberellin-regulated protein were upregulated in S. gummosus root tips during the initial growth phase.
Primary root growth in Cactoideae species matches their environment. The data imply that determinate growth of the primary root became fixed after separation of the Cactiodeae/Opuntioideae and Maihuenioideae/Pereskioideae lineages, and that the genetic regulation of RAM maintenance and its loss in Cactaceae is orchestrated by genes involved in the regulation of gene expression, signalling, and redox and hormonal responses.
PMCID: PMC3698391  PMID: 23666887
Root development; determinate growth of primary root; Cactaceae; Cactoideae; Opuntioideae; Maihuenioideae; Pereskioideae; adaptation to aridity; differential gene expression
24.  ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling PLETHORA Expression in Arabidopsis 
PLoS Genetics  2014;10(12):e1004791.
Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
Author summary
Abscisic acid (ABA) plays crucial roles in plant growth and development, and also in plant responses to abiotic and biotic stresses. ABA can stimulate the production of reactive oxygen species (ROS) that act as signals in low concentrations, but as cell-damaging agents in high concentrations. A mutation in ABO8, encoding a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3, leads to hypersensitivity to ABA in root growth, and root tips of the abo8-1 mutants accumulate more ROS than those of the wild type; this accumulation of ROS in abo8-1 root tips is enhanced by ABA treatment. We also found that auxin signaling and/or accumulation is greatly reduced in root tips of the abo8-1 mutants. Addition of the reducing agent GSH to the growth medium partially recovers the root hypersensitivity to ABA, and also the ABA-inhibited expression of PLT1/2 in abo8-1. Furthermore, the inducible expression of PLT2 largely rescues the root growth defect of abo8-1 with and without ABA treatment. Our results reveal the important roles of ROS in regulating root meristem activity in the ABA signaling pathway.
PMCID: PMC4270459  PMID: 25522358
25.  Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea 
Annals of Botany  2010;107(2):285-292.
Background and Aims
Merwilla plumbea is an important African medicinal plant. As the plants grow in soils contaminated with metals from mining activities, the danger of human intoxication exists. An experiment with plants exposed to cadmium (Cd) was performed to investigate the response of M. plumbea to this heavy metal, its uptake and translocation to plant organs and reaction of root tissues.
Plants grown from seeds were cultivated in controlled conditions. Hydroponic cultivation is not suitable for this species as roots do not tolerate aquatic conditions, and additional stress by Cd treatment results in total root growth inhibition and death. After cultivation in perlite the plants exposed to 1 and 5 mg Cd L−1 in half-strength Hoagland's solution were compared with control plants. Growth parameters were evaluated, Cd content was determined by inductively coupled plasma mass spectroscopy (ICP-MS) and root structure was investigated using various staining procedures, including the fluorescent stain Fluorol yellow 088 to detect suberin deposition in cell walls.
Key Results
The plants exposed to Cd were significantly reduced in growth. Most of the Cd taken up by plants after 4 weeks cultivation was retained in roots, and only a small amount was translocated to bulbs and leaves. In reaction to higher Cd concentrations, roots developed a hypodermal periderm close to the root tip. Cells produced by cork cambium impregnate their cell walls by suberin.
It is suggested that the hypodermal periderm is developed in young root parts in reaction to Cd toxicity to protect the root from radial uptake of Cd ions. Secondary meristems are usually not present in monocotyledonous species. Another interpretation explaining formation of protective suberized layers as a result of periclinal divisions of the hypodermis is discussed. This process may represent an as yet unknown defence reaction of roots when exposed to elemental stress.
PMCID: PMC3025738  PMID: 21118841
Cadmium; environmental stress; medicinal plants; Merwilla plumbea; monocotyledonous plants; periderm; plant anatomy; root structure

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