Root Apical Meristem Organization Research Articles

Effects of Cadmium Stress on Root and Root Border Cells of Some Vegetable Species with Different Types of Root Meristem.

Cadmium is one of the most toxic heavy metals and can be easily absorbed by plants, affecting root growth. Root border cells (RBCs), that are located in the periphery of the root cap and originate from the root cap meristem, represent a convenient tool to study the toxic effects of Cd on root performance. In this work, vegetables with contrasting types of root apical meristem (RAM) organizations were used. The open RAM organizations included pea and cucumber, and the closed RAM organizations included tomato, chili, and eggplant. The number of RBCs were significantly higher in the species possessing open RAM organization: pea (11,330 cells per root) > cucumber (8200) > tomato (2480) > eggplant (1830) > chili (1320). The same trend was observed for cell viability: pea (61%) > cucumber (59%) > tomato (49%) > eggplant (44%) > chili (42%). Pea and cucumber had higher relative radicle elongation rates and a lower increase in stress-induced accumulation of malondialdehyde (MDA), making them more resistant to Cd stress than the vegetables with close RAM organization. Under Cd treatment, the number and viability of RBCs in vegetables with both types of RAM organization were significantly decreased. However, the decreasing ratio of the number and viability of RBCs in pea and cucumber was higher than in tomato, chili, and eggplant. Taken together, the plants with the open-type RAM are more tolerant to Cd, and it can be speculated that the cadmium tolerance of the vegetables may be correlated with the number and viability of RBCs in response to cadmium stress.

The quiescent centre and root apical meristem: organization and function.

This special issue is dedicated to the 100th anniversary of the birth of Frederick Albert Lionel Clowes, who discovered the quiescent centre (QC) of the root apical meristem (RAM). His discovery was a foundation for contemporary studies of the QC and RAM function, maintenance, and organization. RAM function is fundamental for cell production and root growth. This special issue bundles reviews on the main tendencies, hypotheses, and future directions, and identifies unknowns in the field.

The quiescent centre of the root apical meristem: conceptual developments from Clowes to modern times.

In this review we discuss the concepts of the quiescent centre (QC) of the root apical meristem (RAM) and their change over time, from their formulation by F.A.L. Clowes to the present. This review is dedicated to the 100th anniversary of the birth of Clowes, and we present his short biography and a full bibliography of Clowes' work. Over time, the concept of the QC proved to be useful for the understanding of RAM organization and behaviour. We focus specifically on conceptual developments, from the organization of the QC to understanding its functions in RAM maintenance and activity, ranging from a model species, Arabidopsis thaliana, to crops. Concepts of initial cells, stem cells, and heterogeneity of the QC cells in the context of functional and structural stem cells are considered. We review the role of the QC in the context of cell flux in the RAM and the nature of quiescence of the QC cells. We discuss the origin of the QC and fluctuation of its size in ontogenesis and why the QC cells are more resistant to stress. Contemporary concepts of the organizer and stem cell niche are also considered. We also propose how the stem cell niche in the RAM can be defined in roots of a non-model species.

Root apical meristem diversity and the origin of roots: insights from extant lycophytes.

The independent origin of roots in lycophytes and euphyllophytes has been proposed, mainly based on paleobotanical records. However, the question of how roots evolved within these lineages remains unresolved. Root apical meristem (RAM) organization in lycophytes would provide a clue toward understanding the early evolution of roots. Recently, we examined RAM organization in lycophytes (Lycopodiaceae, Isoetaceae, and Selaginellaceae) in terms of cell division activity and anatomy, comparing RAM among vascular plants. Lycophyte RAM exhibited four organization types (I, II, III, and apical); thus, RAM organization in extant lycophytes was more diverse than expected. Type I RAM contained a region with very low cell division frequency, reminiscent of the quiescent center (QC) in seed plant RAM. Although some euphyllophyte RAMs were structurally similar to types II and III and apical cell-type RAM, lycophyte RAM of types II and III had no QC-like area. These results support the paleobotanical predictions that roots evolved several times in lycophytes, as well as in euphyllophytes. In this review, we also introduce recent findings on RAM organization in extant lycophytes and discuss the origin of roots in vascular plants.

Analysis of Cell Division Frequency in the Root Apical Meristem of Lycophytes, Non-seed Vascular Plants, Using EdU Labeling.

The organization of the root apical meristem (RAM) provides insights into the evolution of roots in vascular plants. The RAM of seed plants has a quiescent center (QC), in which the cells divide infrequently and function to maintain neighboring stem cells. However, the existence of a QC and the mechanisms of RAM maintenance in non-seed plants are poorly understood. We analyzed the RAM organization of lycophytes focusing on cell division activity using the EdU labeling method and showed that the RAM of Lycopodium species has a region with a very low cell division frequency, which was named the QC-like region. Here, we describe an in situ EdU labeling method for the RAM of growing roots in nature.

Arabidopsis ZUOTIN RELATED FACTOR1 Proteins Are Required for Proper Embryonic and Post-Embryonic Root Development.

The H2A/UBIQUITIN-binding proteins AtZRF1a/b have been reported as key regulators involved in multiple processes of Arabidopsis plant growth and development. Yet, the cellular and molecular mechanisms underlying the mutant phenotype remain largely elusive. Here we show that loss-of-function of AtZRF1a/b causes defective root elongation and deformed root apical meristem organization in seedlings. The premature termination of the primary root in the atzrf1a;atzrf1b double mutant is associated with an advanced onset of endoreduplication and subsequent consumption of reservoir stem cells. Cytological analyses using cell type-specific markers and florescent dyes indicate that AtZRF1a/b are involved in maintenance of proper cell layer organization, determinacy of cell identity, and establishment of auxin gradient and maximum at the root tip. During embryogenesis AtZRF1a/b act dominantly in regulating the maintenance of ground tissue initial cells and production of lateral root cap. Lastly, quantitative real-time polymerase chain reaction analysis shows mis-expression of some key genes involved in regulating cell patterning, cell proliferation and/or hormone pathways. Our results provide important insight into AtZRF1a/b function in cell fate determinacy and in establishment and maintenance of proper stem cell reservoir during embryonic and post-embryonic root development.

Comparison of Promeristem Structure and Ontogeny of Procambium in Primary Roots of Zea mays ssp. Mexicana and Z. mays 'Honey Bantam' with Emphasis on Metaxylem Vessel Histogenesis.

Classical histology describes the histological organization in Zea mays as having a “closed organization” that differs from Arabidopsis with the development of xylem conforming to predictable rules. We speculated that root apical meristem organization in a wild subspecies of Z. mays (a teosinte) would differ from a domestic sweetcorn cultivar (‘Honey Bantam’). Careful comparison could contribute to understanding how evolutionary processes and the domestication of maize have affected root development. Root tips of seedlings were prepared and sectioned for light microscopy. Most sections were treated with RNase before staining to increase contrast between the walls and cytoplasm. Longitudinal and serial transverse sections were analyzed using computer imaging to determine the position and timing of key xylem developmental events. Metaxylem development in mexicana teosinte differed from sweetcorn only in that the numbers of late-maturing metaxylem vessels in the latter are typically two-fold greater and the number of cells in the transverse section of procambium were greater in the latter, but parenchymatous cell sizes were not statistically different. Promeristems of both were nearly identical in size and organization, but did not operate quite as previously described. Mitotic activity was rare in the quiescent centers, but occasionally a synchronized pulse of mitoses was observed there. Our reinterpretation of histogen theory and procambium development should be useful for future detailed studies of regulation of development, and perhaps its evolution, in this species.

Root apical meristem diversity in extant lycophytes and implications for root origins.

Root apical meristem (RAM) organization in lycophytes could be a key to understanding the early evolution of roots, but this topic has been insufficiently explored. We examined the RAM organization of lycophytes in terms of cell division activities and anatomies, and compared RAMs among vascular plants. RAMs of 13 species of lycophytes were semi-thin-sectioned and observed under a light microscope. Furthermore, the frequency of cell division in the RAM of species was analyzed using thymidine analogs. RAMs of lycophytes exhibited four organization types: type I (Lycopodium and Diphasiastrum), II (Huperzia and Lycopodiella), III (Isoetes) and RAM with apical cell (Selaginella). The type I RAM found in Lycopodium had a region with a very low cell division frequency, reminiscent of the quiescent center (QC) in angiosperm roots. This is the first clear indication that a QC-like region is present in nonseed plants. At least four types of RAM are present in extant lycophytes, suggesting that RAM organization is more diverse than expected. Our results support the paleobotanical hypothesis that roots evolved several times in lycophytes, as well as in euphyllophytes.

Analysis of the rrl3 Mutants Reveals the Importance of Arginine Biosynthesis in the Maintenance of Root Apical Meristem in Rice

We characterized reduced root length3(rrl3) mutantsof rice that exhibit a short-root phenotype under conditions producing mechanical impediments to growth, such as aerated water culture medium. The mutants were not able to maintain the quiescent center (QC) identity and produced disorganized root apical meristem (RAM) under aeration because of impaired cell division. A map-based cloning approach showed that RRL3 encodes carbamoyl phosphate synthetase (CPS) which is thought to be required for the conversion of ornithine into citrulline during arginine biosynthesis. The RRL3 gene is expressed highly at the root tip area that includes the root cap and division zone. The RRL3 gene expression level was greatly affected by aeration treatment, indicating that the spatiotemporal expression of the RRL3 gene with respect to the aeration is important for the maintenance of RAM. Furthermore, the application of citrulline and arginine could rescue the root phenotype, which implied that arginine biosynthesis was impaired in the rrl3-1 mutant. These results suggest that the RRL3 regulated arginine biosynthesis is important for the maintenance of RAM organization in the presence of mechanical impediments.

Activation of embryo during rape (Brassica napus L.) seed germination. I. Structure of embryo and organization of root apical meristem

The Structure of the mature rape embryo was examined on longitudirna microtome sections, and1, its developmental interpretation is given, based on the author's own studies and literature data. The boundaries between the epicotyl, hypocotyl and radicle are recognized and identified with the limits between the proembryo segments. The radicle Structure and root apical meristem organization are described. In the dermatogen and periblem cell patterns four segments are distinguished, separated successively from the initial cells. Their position is recognized as almost the same on both sides of the root axis and in different embryos. The easily discernible limits between the dermatogen sectors are to be utilized as reference points in studies on the root apical meristem activation and growth during rape seed germination.

Anatomical aspects of angiosperm root evolution.

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. 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.

Redox regulation of root apical meristem organization: Connecting root development to its environment

Post-embryonic root growth relies on the proliferative activity of the root apical meristem (RAM), consisting, in part, of cells with juvenile characteristics (stem cells). It is generally, but erroneously held that the RAM indefinitely produces new cells throughout the lifespan of a plant, resulting in indeterminate root growth. On the contrary, convincing data, mainly from the lab of Thomas L. Rost, show in all species analyzed so far, including Arabidopsis, that RAM organization changes over time in parallel with both a cessation of the production of new cells, and a consequent reduction in root growth, even under optimal conditions. In addition, RAM organization evolved to become highly plastic and dynamic in response to environmental triggers (e.g. water and nutrient availability, pollutants). Under unfavourable conditions, the RAM is rapidly reorganized, and, as a result of the cessation of new cell production at the root tip, root growth is altered, and lateral root production is enhanced, thus providing the plant additional strategies to overcome the stress. It is now becoming increasingly clear that this environment-responsive developmental plasticity is linked to reactive oxygen/nitrogen species, antioxidants, and related enzymes, which form part of a complex signalling module specifically operating in the regulation of RAM functioning, in strict relationship with hormonal control of root development exerted by auxin, gibberellins and cytokinins. In turn, such redox/hormone crosstalk regulates gene expression.

AnAGAMOUS-Related MADS-Box Gene,XAL1(AGL12), Regulates Root Meristem Cell Proliferation and Flowering Transition in Arabidopsis

MADS-box genes are key components of the networks that control the transition to flowering and flower development, but their role in vegetative development is poorly understood. This article shows that the sister gene of the AGAMOUS (AG) clade, AGL12, has an important role in root development as well as in flowering transition. We isolated three mutant alleles for AGL12, which is renamed here as XAANTAL1 (XAL1): Two alleles, xal1-1 and xal1-2, are in Columbia ecotype and xal1-3 is in Landsberg erecta ecotype. All alleles have a short-root phenotype with a smaller meristem, lower rate of cell production, and abnormal root apical meristem organization. Interestingly, we also encountered a significantly longer cell cycle in the strongest xal1 alleles with respect to wild-type plants. Expression analyses confirmed the presence of XAL1 transcripts in roots, particularly in the phloem. Moreover, XAL1beta-glucuronidase expression was specifically up-regulated by auxins in this tissue. In addition, mRNA in situ hybridization showed that XAL1 transcripts were also found in leaves and floral meristems of wild-type plants. This expression correlates with the late-flowering phenotypes of the xal1 mutants grown under long days. Transcript expression analysis suggests that XAL1 is an upstream regulator of SOC, FLOWERING LOCUS T, and LFY. We propose that XAL1 may have similar roles in both root and aerial meristems that could explain the xal1 late-flowering phenotype.

Developmental Anatomy of the Root Cortex of the Basal Monocotyledon, Acorus calamus (Acorales, Acoraceae)

The anatomical structure and development of adventitious roots were analysed in the basal monocotyledon, Acorus calamus, to determine to what extent those features are related to phylogenetic position. Root specimens were harvested and sectioned, either with a hand microtome or freehand, at varying distances from the root tip and examined under the microscope using a variety of staining techniques. Roots of Acorus calamus possess a unique set of developmental characteristics that produce some traits similar to those of another basal angiosperm group, Nymphaeales. The root apical meristem organization seems to be intermediate between that of a closed and an open monocotyledonous root apical meristem organization. The open-type root apical meristem consists of a curved zone of cortical initials and epidermal initials overlying the vascular cylinder initials; the epidermal part of the meristem varies in its association with the cortical initials and columellar initials of the promeristem. The cortex develops an endodermis with only Casparian bands, a dimorphic exodermis with Casparian bands and suberin lamellae, and a polygonal aerenchyma by differential expansion, as also observed in the Nymphaeales and some dicotyledonous species. The stele has characteristics like those of members of the Nymphaeaceae. Specific anatomical and developmental attributes of Acorus roots seem to be related to the phylogenetic position of this genus.

Phylogenetic Distribution and Evolution of Root Apical Meristem Organization in Dicotyledonous Angiosperms

Root apical meristem (RAM) organization was characterized in a wide range of dicotyledonous angiosperms and interpreted in light of recent phylogenies based on DNA sequence data. RAM organization was classified using the open and closed system of Guttenberg. In longitudinal section, closed RAMs have clonally distinct tiers of initials, but in open RAMs the initials are shared among the primary tissues. For open RAMs, we distinguished between intermediate-open (fate of derivatives easily identified) and basic-open (fate of derivatives not immediately evident). The ancestral state of angiosperm RAMs was intermediate-open, with closed organization first appearing near the base of the core eudicots. Basic-open was derived and was found in the eurosid I orders Fabales and Cucurbitales; therefore, at least two new RAM organizations appeared during the radiation of angiosperms. In the core eudicots, there is evidence for multiple independent reversions, from closed to intermediate-open. In all the species we observed, T divisions of the root cap protoderm initial delimit protoderm from the innermost cell layer of the peripheral root cap. Changes in RAM organization appear to be a normal part of the life cycle of the root; therefore, the choice of root age is important in studies of RAM organization.

Primary Root Growth and the Pattern of Root Apical Meristem Organization are Coupled

Root apical meristems (RAMs) in dicotyledonous plants have two organizational schemes; closed (with highly organized tiers) and open (tiers lacking or disorganized). These schemes are commonly believed to remain unchanged during the growth of the root axis. Individual roots are commonly thought to have indeterminate growth. We challenge these two generalizations through the study of five species with closed apical organization: Clarkia unguiculata L., Oxalis corniculata L., Dianthus caryophyllus L., Blumenbachia hieronymi Urb., and Salvia farinaceae Benth. cv. “Strata”. These roots have phased growth patterns where early growth is followed by deceleration, after which the initial cells stop dividing, elongation ceases, and the root reaches its determinate length. At or before reaching determinacy, the root apical meristem stops maintaining its closed organization and becomes less organized. These observations will be placed in context with observations from the literature to suggest two new generalizations, namely, that apical organization does change over the growth phases of roots, and that roots are determinate.

FASCIATA Genes for Chromatin Assembly Factor-1 in Arabidopsis Maintain the Cellular Organization of Apical Meristems

Postembryonic development of plants depends on the activity of apical meristems established during embryogenesis. The shoot apical meristem (SAM) and the root apical meristem (RAM) have similar but distinct cellular organization. Arabidopsis FASCIATA1 ( FAS1) and FAS2 genes maintain the cellular and functional organization of both SAM and RAM, and FAS gene products are subunits of the Arabidopsis counterpart of chromatin assembly factor-1 (CAF-1). fas mutants are defective in maintenance of the expression states of WUSCHEL ( WUS) in SAM and SCARECROW ( SCR) in RAM. We suggest that CAF-1 plays a critical role in the organization of SAM and RAM during postembryonic development by facilitating stable maintenance of gene expression states.

ADVENTITIOUS ROOT DEVELOPMENT IN TYPHA GLAUCA, WITH EMPHASIS ON THE CORTEX

Adventitious root development was investigated in Typha glauca plants grown under experimental conditions with the previous year's dead, sterile stalk either emerged above or submerged below the surface of Hoagland's solution. Adventitious roots emerged from buds in which most primordia had been earlier formed. Most roots elongated to 14–19 cm in 3–4 weeks and produced abundant lateral roots to their tips. Root apical meristem organization was typically monocotyledonous with a single tier of ground meristem/protoderm over the procambium. The ground meristem had zones of periclinal divisions in its innermost and outermost layers; the innermost layer initiated the endodermis and midcortex, and the outermost layers initiated the hypodermis. Crystalliferous cells with raphides were produced in the midcortex, and aerenchyma resulted from the radial expansion of schizogenous air spaces and some lysigeny in the midcortex. The procambium produced a vascular cylinder with 10–13 phloem and xylem poles, 6–9 large metaxylem elements, and central sclerenchyma. As roots stopped elongating, they narrowed, the vascular cylinder diminished in size, typical aerenchyma was lost from the cortex, crystal production ceased, and the rootcap diminished in size with its storage starch used up. Growth was determinate in these adventitious roots. The results suggested that a periclinally derived outer ground meristem was a prerequisite for a hypodermis, which, in turn, was necessary as a structural framework for aerenchyma. Without a hypodermis, typical aerenchyma was not present.

Zonation and Organization of Root Apical Meristem of Glycine Max

Zonation and Organization of Root Apical Meristem of Glycine Max