Stepwise understanding of root development
Introduction
The Arabidopsis root is composed of four concentric cell layers: epidermis, cortex, endodermis, and stele (Figure 1). Each layer is made of cell files that are derived from initial cells located at their apical end. The initial cells surround quiescent center (QC) cells, which promote the continuous cell division of the initial cells [1]. Root cap cells are also formed from their initial cells. Therefore, a root is a bundle of cell files in which cells are aligned along an age gradient from the initial daughter cells to mature cells that are differentiated according to their cell types. Recent studies have identified several genes that are involved in regulating this impressive patterning of a root (reviewed in 2., 3., 4.). In this review, we summarize the developmental process of root patterning by dividing it into three key stages: cell fate determination, fate fixation, and cell differentiation. We outline root hair formation, cortex/endodermis (co/en) formation, and the formation of QC cells and the columella root cap as examples of the basic root patterns (Table 1).
Section snippets
Circumferential patterning — fate and morphology of root hair cells
The outermost epidermis generates root hairs to absorb water and nutrients from soils. Epidermal cells originate from their initial cells and differentiate according to one of two alternative fates: to be a hair cell that forms a root hair or to be a non-hair cell. An epidermal cell that contacts to two cortical cells is specified as a hair cell, whereas an epidermal cell that touches only one cortical cell adopts the non-hair cell fate (Figure 1). The positional relationship between the hair
Radial patterning — separation of endodermis and cortex
Among the genes involved in radial patterning, the best-characterized are SHORT-ROOT (SHR) and SCARECROW (SCR), both of which encode a putative transcription factor of the GRAS family 26., 27., 28.. SHR is transcribed in entire stele and moves into the adjacent cell layer, which includes the QC, the co/en initial, and endodermis (Figure 1). After moving, SHR induces SCR expression in these cells. Both SHR and SCR proteins are responsible for specifying QC [29] and for controlling the periclinal
Proximo-distal patterning — specification of QC and columella root cap
The plant hormone auxin plays crucial roles in the proximo-distal patterning of root. Auxin is transported polarly to root tips, and accumulates in the QC and the columella root cap (Figure 1; reviewed in [33]). When exogenous auxin or an inhibitor of auxin transport is applied, the accumulation pattern of auxin is disrupted, interfering with proximo-distal root patterning [34]. Similar defects were observed in the mutant of PIN-FORMED4 (PIN4), a member of PIN family of putative auxin efflux
Chromatin stabilization and programmed proteolysis in root pattern formation
Disruption of the cellular organization of the root meristem was reported in a set of mutants that are missing chromatin stabilization factors: FASCIATA1 (FAS1) and FAS2 (CAF-1 subunits) [46], MRE11 [47], condensin genes [48], and BRUSHY1 (BRU1)/MUGOUN3/TONSOKU (TSK) 49., 50., 51.. In fas and tsk mutants, the expression pattern of SCR is disturbed, and in the bru1 mutant, the transcriptional gene silencing system is released. Taken together, chromatin stabilization might maintain the expression
Exploring novel players in root development
We expect that many unidentified genes have crucial roles in root development (Table 1), and that these genes will have a stage- or tissue-specific expression pattern that is related to their roles. In addition to the traditional genetic approach, a novel post-genomic analysis has been proposed to identify these genes. Birnbaum et al. [53••] developed a technique to generate high-resolution spatiotemporal expression profiles throughout the Arabidopsis root (called ‘digital in situ’). They
Conclusions
Molecular and genetic studies have identified various genes that are involved in the processes of root patterning. When these genes are classified on the basis of the types of root axis and the developmental stages in which each gene is expressed, as shown in Table 1, there are many boxes in which no or only a few genes have been identified, showing that our knowledge is still partial. There remain two major questions. First, we know little about the nature of positional signals and their
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank Renze Heidstra and Ben Scheres for providing helpful information. We also thank Taisuke Nishimura for useful suggestions. We would like to acknowledge funding from the Core Research of Science and Technology (CREST) Research Project and from the Japanese Ministry of Education, Culture, Sports, Science and Technology. MU was supported by Research Fellowships from the Japan Society for the Promotion of Science for Young Scientists. KO and YK were supported by The Grant for the
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