| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online November 9, 2007; 10.1104/pp.107.107870 Plant Physiology 146:140-148 (2008) © 2008 American Society of Plant Biologists Diarch Symmetry of the Vascular Bundle in Arabidopsis Root Encompasses the Pericycle and Is Reflected in Distich Lateral Root Initiation1,[W]Laboratoire de Biologie du Développement des Plantes, Department of Plant Biology and Environmental Microbiology, The Institute of Environmental Biology and Biotechnology, Direction des Sciences du Vivant, Commissariat à l'Energie Atomique, Centre National de la Recherche Scientifique, Université Aix-Marseille, Saint Paul lez Durance F–13108, France (B.P., L.R., V.B., L.N.); Department of Plant Systems Biology, Root Development Group, Flanders Interuniversity Institute of Biotechnology and Department of Molecular Genetics, Ghent University, B–9052 Ghent, Belgium (B.P., I.D.S., T.B.); Equipe Rhizogenèse, Université Mixte de Recherche DIA-PC, Institut de Recherche pour le Développement, 34394 Montpellier cedex 5, France (L.L.); Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom (L.R., J.H.); Université Pierre et Marie Curie, F–75252 Paris cedex 05, France (E.B.-D., D.C.); Plant Molecular Biology Laboratory, Institute of Biotechnology, University of Helsinki, FI–00014 Helsinki, Finland (M.B., Y.H.); and Carolyn Lynch Laboratory, Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104 (S.R.P.)
The outer tissues of dicotyledonous plant roots (i.e. epidermis, cortex, and endodermis) are clearly organized in distinct concentric layers in contrast to the diarch to polyarch vascular tissues of the central stele. Up to now, the outermost layer of the stele, the pericycle, has always been regarded, in accordance with the outer tissue layers, as one uniform concentric layer. However, considering its lateral root-forming competence, the pericycle is composed of two different cell types, with one subset of cells being associated with the xylem, showing strong competence to initiate cell division, whereas another group of cells, associated with the phloem, appears to remain quiescent. Here, we established, using detailed microscopy and specific Arabidopsis thaliana reporter lines, the existence of two distinct pericycle cell types. Analysis of two enhancer trap reporter lines further suggests that the specification between these two subsets takes place early during development, in relation with the determination of the vascular tissues. A genetic screen resulted in the isolation of mutants perturbed in pericycle differentiation. Detailed phenotypical analyses of two of these mutants, combined with observations made in known vascular mutants, revealed an intimate correlation between vascular organization, pericycle fate, and lateral root initiation potency, and illustrated the independence of pericycle differentiation and lateral root initiation from protoxylem differentiation. Taken together, our data show that the pericycle is a heterogeneous cell layer with two groups of cells set up in the root meristem by the same genetic pathway controlling the diarch organization of the vasculature.
The Arabidopsis (Arabidopsis thaliana) root displays two different levels of tissue organization: a concentric organization formed by the ground layers (endodermis/cortex) and the epidermis, and a bilateral symmetry of the diarch vascular bundle consisting of two poles of xylem elements and two poles of phloem elements (Dolan et al., 1993  ). The outermost layer of the central cylinder or stele is the pericycle, which is traditionally regarded as one extra concentric layer. Indeed, all pericycle cells share common physical properties and form a unique layer of regularly shaped cells in contact with each other by their tangential cell walls (Dolan et al., 1993). During embryogenesis, the pericycle initiates from the same subset of initial cells as the rest of the stele and can be recognized as a distinct concentric layer already formed at the heart stage, even before the endodermal and cortical cell files become specified (Scheres et al., 1994). However, many studies in different species have emphasized the differences between pericycle cells according to their position adjacent to the xylem or the phloem poles in terms of cell division competence (Dubrovsky et al., 2000), cell cycle progression (Beeckman et al., 2001), cell size (Casero et al., 1989; Dubrovsky et al., 2000), cell surface arabinogalactan-protein distribution and cell wall thickening (Dolan and Roberts, 1995; Casero et al., 1998; Majewska-Sawka and Nothnagel, 2000), methyl blue staining (Toriyama, 2005), plasmodesmatal connections (Wright and Oparka, 1997; Complainville et al., 2003), physical disposition against endodermis cells (Dolan et al., 1993), microtubule content (Hardham and Gunning, 1979), and marker gene expression (Laplaze et al., 2005; Mahonen et al., 2006).
Lateral root development in dicotyledonous plants occurs postembryonically from pericycle cells and guarantees the spatial development and plasticity of root systems (Torrey, 1950
Pericycle Is Made of Two Different Cell Types as Revealed by Cytological Analyses
Only few reports have examined the ultrastructural features of the Arabidopsis root pericycle (Dolan et al., 1993 In untreated roots, the protoxylem-pole pericycle cells displayed meristematic features with frequently three or more vacuoles and a dense cytoplasm containing numerous electron-dense ribosomes (Fig. 1A ). At the phloem pole, all pericycle cells presented a single and large central vacuole and a parietal cytoplasm with less ribosomes, characteristic of more differentiated status (Fig. 1B). An opposite situation was found for NPA-treated seedlings. Whereas the protoxylem-pole pericycle cells reduced their meristematic appearance by acquiring one large central vacuole and a reduction in the number of ribosomes (Fig. 1C), the protophloem-pole pericycle cells showed, under these conditions, meristematic appearance with a densely stained cytoplasm, loss of the central vacuole in most of the cells, and enrichment in endoplasmic reticulum (Fig. 1D). In some sections, we could even notice the result of a recent periclinal cell division event by the appearance of a thin cell wall subdividing former pericycle cells into two daughter cells (Fig. 1D, arrowheads). These divisions are, however, rare and never give rise to lateral root formation. After transfer to NAA, the situation was pushed over again with the two types of pericycle cells reacting in an opposite manner. At the xylem poles, pericycle cells clearly became meristematic with the development of numerous small vacuoles, nuclei with large nucleoli (Fig. 1E), whereas phloem pericycle cells reacquired parietal cytoplasm and a central vacuole (Fig. 1F). These analyses indicate that both types of pericycle cells react differentially and even in an opposite way to lateral root-inhibiting versus lateral root-inducing conditions.
Pericycle Bilateral Heterogeneity Already Occurs in Stele Initials
Having demonstrated the clear difference between protoxylem-pole and phloem-pole pericycle cells, we used GAL4 enhancer trap lines (see "Materials and Methods") as markers to study further the organization of the root pericycle. The J0121 line (Laplaze et al., 2005
Another population of Arabidopsis GAL4 enhancer trap lines (Columbia [Col-0] background) was screened to identify novel pericycle markers. This led to the identification of the reporter line Rm1007, which expresses GFP specifically in the pericycle associated with xylem poles (Fig. 2, I–N) and mainly in three contiguous pericycle files (Fig. 2L). Compared to J0121, GFP expression was detected earlier in the root tip, starting from the initials immediately above the quiescent center cells (Fig. 2, K and L). Furthermore, this expression pattern could be detected in heart-stage embryos (Fig. 2M). This early expression is comparable to the expression pattern observed in young lateral root primordia before emergence (Fig. 2J, arrow). It persists in older parts of the root where GFP remains exclusively expressed in the pericycle associated with xylem poles (Fig. 2N). Unlike J0121, expression is more intense in young tissues and fades away progressively in older parts (Fig. 2I). In conclusion, expression of the GFP enhancer trap marker in both J0121 and Rm1007 lines labeled a subset of cells in the pericycle, associated with the xylem poles, with Rm1007 labeling the xylem-pole pericycle from the first initials.
Lateral root initiation, which takes place in the pericycle cells facing xylem poles, is regulated by exogenous and endogenous signals (Malamy, 2005
To get insight into the mechanisms that specify the different populations of pericycle cells, we performed a genetic screen on the J0121 enhancer trap line. For further analysis, J0121 was preferred instead of Rm1007 because variation in the intensity of the GFP was noticed in Rm1007 probably due to epigenetic regulations. Fifteen hundred independent F2 progeny of ethyl methanesulfonate-mutagenized seedlings were screened to isolate mutants exhibiting qualitative or quantitative alteration of the GFP expression pattern. This led to the identification of 12 mutants showing different phenotypes related to J0121 expression: discontinuity, ectopic expression in the pericycle, ectopic expression outside the pericycle, and down-regulation of GFP expression. Interestingly, most of these mutants showed an alteration in their lateral root initiation ability (Supplemental Fig. S2). We have focused on two mutants showing a strong and stable phenotype with altered radial pattern of GFP expression in the pericycle, lonesome highway (lhw; Fig. 3, D–F ) and impaired vasculature development (ivad; Fig. 3, G–I), as compared with the J0121 marker line control (Fig. 3, A–C).
Pericycle Determination and Lateral Root Initiation Potency Are Intimately Correlated with Vascular Organization in the lhw Mutant
Two recessive mutant alleles of the previously reported lhw mutant (Ohashi-Ito and Bergmann, 2007
To study the lateral root-forming capacity of the pericycle in lhw mutants, plants were germinated on medium supplemented with NPA and then transferred to medium supplemented with NAA to synchronously stimulate lateral root formation along the whole root of the plant, according to the lateral root-inducible system (Himanen et al., 2002
Protoxylem Differentiation Is Not Required for Pericycle Differentiation and Lateral Root Initiation The recessive ivad mutant shows ectopic GFP expression in the root: GFP expression extends in the pericycle additionally to the normal pattern, above the differentiation zone in plants grown 4 to 5 DAG (Fig. 3I). Primary root growth is drastically reduced (Supplemental Fig. S2) and root gravitropism is altered (data not shown). Further analysis revealed that this mutant was dramatically impaired in vascular and endodermis development (Fig. 3, G and H). Fewer cells constitute the vascular bundle. Phloem and protoxylem development are altered, these tissues being partially or even fully absent (Fig. 3, G and H). In parts of the root where normal J0121 GFP expression was observed, the vascular bundle appears not to be affected by the mutation (data not shown). The endodermis also shows similar alterations (Fig. 3, G [absent] and H [partially absent]). However, regions with altered GFP patterning in the mutants were found where the endodermis was correctly formed. These aspects of the ivad phenotype highlight the intimate link between the correct diarch development of the vascular bundle and the proper bilateral symmetry of the pericycle.
Whereas the root phenotype of the lhw mutants clearly illustrated the relationship between xylem poles and lateral root initiation, we wondered whether impaired protoxylem differentiation of the ivad mutant would result in aberrant lateral root initiation. Differential interference contrast (DIC) microscopy analysis allows easy distinction between meta- and protoxylem elements in Arabidopsis roots, the first having reticulate and the latter helical cell wall thickening. DIC analysis of this mutant revealed that lateral root initiation could still proceed in regions where no protoxylem differentiated (Fig. 5, D–F
). To confirm this observation, J0121 marker GFP expression and lateral root initiation were investigated in one mutant and one transgenic line, respectively, ahp6 and Pro35S-VND7:SDRX, in which affected protoxylem differentiation was already described (Kubo et al., 2005
Suppression of Vascular Heterogeneity in the wol Mutant Correlates with Loss of Heterogeneity in the Pericycle
To determine whether the qualitative loss in vasculature heterogeneity has consequences on the ability of pericycle cells to divide and form new lateral roots, we used the wol mutant (Scheres et al., 1995
GFP expression in wol J0121 cross spreads over the whole pericycle compared to the control (Fig. 6, A and D), suggesting that all pericycle cells differentiate in only one type of tissue in the mutant background. Furthermore, wol can be described as a nonrooting mutant because it makes almost no lateral roots. The ability of wol to produce lateral roots under NAA treatment was tested (Fig. 6); no organized primordia were observed above the root tip after 48-h (Supplemental Fig. S5, A–D) or after 96-h (data not shown) treatments as compared with the wild type. Microscope observation of root sections revealed that, in this mutant, all pericycle cells are adjacent to protoxylem elements (Fig. 6E), express GFP (Fig. 6D), are able to divide in a periclinal way upon auxin treatment (Fig. 6F), but do not form primordia.
In Arabidopsis, lateral roots originate deep inside the parent root in one layer of cells that surrounds the vascular tissues: the pericycle (Dolan et al., 1993 ). Only pericycle cells in contact with xylem poles have the competence to initiate lateral root development (De Smet et al., 2006). This process of lateral root initiation occurs above the root tip in the differentiated zone of the root. Competence to form lateral roots is associated with different cell cycle behavior. The pericycle cells adjacent to the xylem poles were shown to continue to divide after leaving the root apical meristem, whereas the other pericycle cells stop dividing (Dubrovsky et al., 2000; Beeckman et al., 2001). Accordingly, xylem pole-associated pericycle cells are shorter than other pericycle cells in the differentiation zone (Beeckman et al., 2001) and differ by their cytological content.
Moreover, the GAL4 enhancer trap line J0121 is specifically expressed in xylem pole-associated pericycle cells, thus suggesting the existence of distinct patterns of gene expression for this subset of cells. However, all these differences between xylem-pole and phloem-pole pericycle cells appear at a distance from the root tip in a mature region of the root where the differentiation of the first vascular elements is fulfilled. This has led to the notion that the lateral root initiation competence of pericycle cells at the xylem poles might rely, to some extent, on correct differentiation of neighboring protoxylem cells. In this view, the lateral root initiation capacity of protoxylem-pole pericycle cells would be a relatively late achieved characteristic. The same train of thought can be found in the earlier reported primed pericycle model (Barlow, 1984
However, in contrast to these hypotheses, our results indicate that the positioning of lateral root primordia is most likely controlled by a different mechanism. We used Rm1007 and J0121 enhancer trap lines and lateral root organogenesis as markers of pericycle cell identity. We show that xylem pole- and phloem pole-associated pericycle cells represent two distinct cell populations with different cellular characteristics. In particular, we observed differential responses of these cells to auxin. Indeed, exogenous treatment with NPA and NAA induces opposite responses between the cells of the pericycle (by blocking division at the xylem poles, whereas the cells in front of phloem poles dedifferentiate and even appear able to divide). This suggests that these two kinds of pericycle cells might have differences in the auxin transport system and/or auxin sensitivity. However, no data have been available to support this hypothesis.
We demonstrate using enhancer trap lines that these two types of pericycle cells might become specified as early as, or coinciding with, the formation of the pericycle initials. Moreover, our genetic analysis indicates that pericycle and vasculature determination in the root meristem are controlled by common mechanisms. This is notably illustrated by a concomitant reduction of the cell number of the vasculature and the pericycle in lhw and wol mutants, whereas the external layers present the same number as the wild type (Supplemental Fig. S3; Dolan et al., 1993 Taken together, our data suggest a new model of pericycle organization (Fig. 7B) where the bilateral organization of the stele, including the pericycle, is set up in the initials and maintained throughout the root, as illustrated by the continuous cell files expressing first Rm1007 and later J0121 markers. Stele determination is notably dependent on the activity of the WOL and LHW genes. Both wol and lhw mutations induce a concomitant loss of one vascular pole and the associated pericycle. These observations further suggest that the vascular tissue and its associated pericycle would belong to the same morphogenetic field. Later on, the vascular tissues and the pericycle differentiate as illustrated by vessel formation and lateral root initiation competence, respectively. The lateral root initiation defect in wol mutant plants can be either a direct consequence of defects in cytokinin signaling or a result from the loss of the heterogeneity of the pericycle. Quiescent phloem-pole pericycle cells might be needed to border the area of divisions that is required to get proper organogenesis. We therefore argue for the existence of at least two different pericycle cell identities that are closely associated with the adjacent vascular elements. These tissues might therefore be regarded as a full member of the stele, rather than being considered as one other concentric layer of the root.
Materials Used
Arabidopsis (Arabidopsis thaliana L. Heynh.) ecotype Col-0 and C24 seeds were obtained from the Nottingham Arabidopsis Stock Center. We analyzed the mutants wol (Mahonen et al., 2000
Seeds were surface sterilized and sown on one-half-strength selective Murashige and Skoog medium supplemented with 1% Suc and 0.8% agar (Sigma) on vertically oriented square plates (Greiner Labortechnik). For treatments with NPA (Duchefa) or NAA (Sigma-Aldrich), 10 µM was added to the Murashige and Skoog medium (Murashige and Skoog, 1962
J0121 seeds homozygous for the enhancer trap insertion (M0) were chemically mutagenized with 0.25% ethyl methanesulfonate) for 12 h and then washed for 5 min with 0.5 M NaOH. Each of the M1 plantlets was grown independently on soil. The mutant selection was carried out on M2 plantlets grown in vitro on one-half-strength selective Murashige and Skoog medium and screened for GFP patterning with a fluorescence stereomicroscope MZFLIII (Leica). Allelism of the mutants was tested by crossing them together and by phenotyping the progeny.
Root length was measured from digital images of the plates using National Institutes of Health ImageJ 1.34S software (http://rsb.info.nih.gov/ij). Emerged lateral roots were counted using a Leica MZ16 binocular microscope. Experiments were repeated at least two times independently.
For whole-mount microscopic analysis, samples were cleared by mounting in a 90% solution of lactic acid (Acros Organics). All samples were analyzed by DIC microscopy (DMLB; Leica Microsystems). For anatomical analysis using light microscopy, transverse sections of roots were performed as described by De Smet et al. (2004)
The following materials are available in the online version of this article.
We thank Dr. M. Kubo for providing Pro35S-VND7:SDRX, and Dr. S. Svistoonoff (Equipe Rhizogenèse, IRD Montpellier), L. Jansen (Root Development Group, VIB Ghent), and A.P. Mähönen (Utrecht University) for critical reading of the manuscript. Received August 23, 2007; accepted November 1, 2007; published November 9, 2007.
1 This work was supported by the Commissariat à l'Energie Atomique, the Marie Curie Foundation, the Institut de Recherche pour le Développement, and Tournesol (bilateral grant no. 11532RD to L.L. and T.B.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Laurent Nussaume (lnussaume{at}cea.fr).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.107870 * Corresponding author; e-mail lnussaume{at}cea.fr.
Barlow P (1984) Positional controls in root development. In PW Barlow, DJ Carr, eds, Positional Controls in Plant Development. Cambridge University Press, Cambridge, UK, pp 281–318 Beeckman T, Burssens S, Inzé D (2001) The peri-cell-cycle in Arabidopsis. J Exp Bot 52: 403–411 Casero P, Casimiro I, Knox J (1998) Occurrence of cell surface arabinogalactan-protein and extensin epitopes in relation to pericycle and vascular tissue development in the root apex of four species. Planta 204: 252–259[CrossRef][Web of Science] Casero PJ, García-Sánchez C, Lloret PG, Navascués J (1989) Changes in cell length and mitotic index in vascular pattern-related pericycle cell types along the apical meristem and elongation zone of the onion root. Protoplasma 153: 85–90[CrossRef][Web of Science] Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165–171[CrossRef][Web of Science][Medline] Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9: 2131–2142 Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503–508[CrossRef][Web of Science][Medline] Complainville A, Brocard L, Roberts I, Dax E, Sever N, Sauer N, Kondorosi A, Wolf S, Oparka K, Crespi M (2003) Nodule initiation involves the creation of a new symplasmic field in specific root cells of Medicago species. Plant Cell 15: 2778–2791 De Smet I, Chaerle P, Vanneste S, De Rycke R, Inzé D, Beeckman T (2004) An easy and versatile embedding method for transverse sections. J Microsc 213: 76–80[Web of Science][Medline] De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, et al (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681–690 De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60: 871–887[CrossRef][Web of Science][Medline] Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119: 71–84[Abstract] Dolan L, Roberts K (1995) Secondary thickening in roots of Arabidopsis thaliana: anatomy and cell surface changes. New Phytol 131: 121–128[CrossRef][Web of Science] Dubrovsky JG, Doerner PW, Colon-Carmona A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol 124: 1648–1657 Hardham AR, Gunning BE (1979) Interpolation of microtubules into cortical arrays during cell elongation and differentiation in roots of Azolla pinnata. J Cell Sci 37: 411–442[Abstract] Heidstra R, Yang WC, Yalcin Y, Peck S, Emons AM, van Kammen A, Bisseling T (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124: 1781–1787[Abstract] Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339–2351 Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19: 1855–1860 Kurup S, Runions J, Kohler U, Laplaze L, Hodge S, Haseloff J (2005) Marking cell lineages in living tissues. Plant J 42: 444–453[CrossRef][Web of Science][Medline] Laplaze L, Parizot B, Baker A, Ricaud L, Martiniere A, Auguy F, Franche C, Nussaume L, Bogusz D, Haseloff J (2005) GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J Exp Bot 56: 2433–2442 Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29: 751–760[CrossRef][Web of Science][Medline] Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38: 203–214[CrossRef][Web of Science][Medline] Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94–98 Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14: 2938–2943 Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122: 3–10 Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67–77[CrossRef][Medline] Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol Biol 55: 727–741[CrossRef][Web of Science][Medline] Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15: 473–497[CrossRef] Ohashi-Ito K, Bergmann DC (2007) Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development 134: 2959–2968 Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol 118: 1369–1378 Scheres B, Di Laurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121: 53–62[Abstract] Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120: 2475–2487 Skene KR (2000) Pattern formation in cluster roots: some developmental and evolutionary considerations. Ann Bot (Lond) 85: 901–908 Toriyama H (2005) On the remarkable phenomena in the root tip of leguminous plants. Root Research 14: 35–40 Torrey JG (1950) The induction of lateral roots by indole acetic acid and root decapitation. Am J Bot 37: 257–264[CrossRef][Web of Science] Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, et al (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17: 3035–3050 Wright KM, Oparka KJ (1997) Metabolic inhibitors induce symplastic movement of solutes from the transport phloem of Arabidopsis roots. J Exp Bot 48: 1807–1814 Related articles in Plant Physiol.:
This article has been cited by other articles:
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
-naphthalene acetic acid (NAA) and incubated for 10 h. In this way, three different samples were obtained: untreated roots, roots prevented from lateral root initiation (NPA), and roots of which the entire pericycle is synchronously induced for lateral root initiation by NAA treatment (Himanen et al., 2002
