Push–pull strategy in the regulation of postembryonic root development
Introduction
Unlike animals, a distinctive property of plants is to set up their basic body plans as embryos and undergo postembryonic growth and development in an indeterminate manner, thereafter. The indeterminate growth involves both the growth of a single organ in apical and radial directions and the generation of new organs from pre-existing ones. These processes allow plants to survive under ever-changing environments, even if parts of their bodies are heavily damaged. Stem cell populations present in shoot and root play critical roles in these processes.
Roots have highly conserved tissue organization in radial direction, consisting of dermal, ground, and vascular tissues from the periphery to the center. As roots grow, cells constituting the radial tissues are constantly generated in the meristem through a combination of symmetric and asymmetric cell divisions. Undifferentiated cells that undergo asymmetric cell divisions are called “initials.” In Arabidopsis roots, proximal stem cells are easily distinguishable as a single layer of cells, with the initials located in shoot-ward direction, right above the “quiescent center” (QC). “Columella initial cells,” or “distal stem cells,” are located in root-ward direction. “Cap cells” are generated from columella initials and “epidermal/lateral root cap initials” by asymmetric cell division for protection of root apical meristem, as the root grows through the soil. Proximal stem cells undergo asymmetric cell divisions in anticlinal direction; one daughter cell adjacent to the QC stays as a stem cell and the other undergoes another round of asymmetric cell division periclinally to generate progenitors for two different cell types. These progenitors actively undergo several rounds of division before entering the differentiation programs. A pool of these actively dividing cells is called “transit-amplifying cells.” The transition from cell proliferation to differentiation in radial tissues occurs simultaneously with a clear shift of isodiametric cells to rapidly elongating cells (Figure 1b).
During postembryonic root growth, cell division activities of stem cells and transit-amplifying cells should be maintained for a long term. Laser ablation studies in 1990s [1, 2] suggested that QC is required for maintaining the stemness of surrounding cells by sending out local signals. Therefore, the QC and surrounding stem cells are together considered as a stem cell niche. In the present review, we have introduced local regulatory programs in each root zone and have discussed how they coordinate the postembryonic root growth.
Section snippets
Local transcriptional networks and signaling that regulate the stem cell niche
Forward genetic studies of mutants that display short root phenotype revealed two key pathways for the formation of stem cell niche [3]. One is directed by PLETHORAs (PLTs) [4] and the other by SHORTROOT (SHR) [5] and SCARECROW (SCR) [6]. PLT1 and PLT2 are essential for QC specification and stem cell activity. They are expressed in a gradual manner, peaking around the QC and decreasing toward the transition zone between the meristem and elongation zones. PLT1 and PLT2 respond positively to
Crosstalk between the stem cell niche and transit-amplifying cells
In the root, transitions in cellular status from proliferation to cell expansion and then to differentiation occur in a synchronous manner. This indicates the presence of signaling molecules, like morphogens, that set up the boundary between the stem cell niche and transit-amplifying cell and the one between transit-amplifying cell and differentiation zone.
Auxin is transported from the shoot to the root by PINs, auxin efflux carriers, and is distributed like a reflux-loop in the root, thereby,
“Top-down signals” as coordinators of stem cell niche regeneration and root growth
The presence of “top-down signals” that control root stem cells is implicated in regeneration studies. Plant roots can regenerate when their tips are excised. Interestingly, mutant roots with defects in the maintenance of stem cell niche in Arabidopsis, such as shr and scr, can still regenerate [44]. Careful examination of regenerating cells after cutting-off of root tips suggested that multiple cell types contribute to the stem cell reconstitution. Single cell transcriptome analysis indicated
Conclusion
Postembryonic root growth is a dynamic process that integrates multiple internal and external signals. Stem cell niche is indispensable as the supplier of building blocks for root growth. Thus, mechanisms underlying stem cell specification and maintenance have been the focus of research. The studies discussed in this review suggest highly complex regulation of stem cells and QC in response to both endogenous and exogenous changes. The next challenge would be to put each piece of regulatory
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
Work at the Ji-Young Lee Lab was supported by National Research Foundation of Korea (2016R1A2B2015258), Golden Seed Project (213002041SBO20), and Next-Generation Bio Green 21 Project (PJ011133). G.C was supported by postdoctoral fellowship from Brain Korea 21 Plus Program.
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2021, Advances in Botanical ResearchCitation Excerpt :Other aspects of root development were also discussed in articles in the series dealing more specifically with interaction with microbes and response to environmental stress. Since the publication of these chapters, numerous reviews have been published (Choe & Lee, 2017; Hochholdinger, Yu, & Marcon, 2018; Petricka, Winter, & Benfey, 2012). The hormone interactions have been investigated in much more detail (Du & Scheres, 2018; Fonouni-Farde, Diet, & Frugier, 2016; Hu, Vandenbussche, & Van Der Straeten, 2017; Wei & Li, 2016) and a new class of hormones, strigolactones, has been discovered (Sun, Tao, Gu, & Zhang, 2016).
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These authors contributed equally.