SHORT-ROOT and SCARECROW Regulate Leaf Growth in Arabidopsis by Stimulating S-Phase Progression of the Cell Cycle

Abstract

SHORT-ROOT (SHR) and SCARECROW (SCR) are required for stem cell maintenance in the Arabidopsis (Arabidopsis thaliana) root meristem, ensuring its indeterminate growth. Mutation of SHR and SCR genes results in disorganization of the quiescent center and loss of stem cell activity, resulting in the cessation of root growth. This paper reports on the role of SHR and SCR in the development of leaves, which, in contrast to the root, have a determinate growth pattern and lack a persistent stem cell niche. Our results demonstrate that inhibition of leaf growth in shr and scr mutants is not a secondary effect of the compromised root development but is caused by an effect on cell division in the leaves: a reduced cell division rate and early exit of the proliferation phase. Consistent with the observed cell division phenotype, the expression of SHR and SCR genes in leaves is closely associated with cell division activity in most cell types. The increased cell cycle duration is due to a prolonged S-phase duration, which is mediated by up-regulation of cell cycle inhibitors known to restrain the activity of the transcription factor, E2Fa. Therefore, we conclude that, in contrast to their specific roles in cortex/endodermis differentiation and stem cell maintenance in the root, SHR and SCR primarily function as general regulators of cell proliferation in leaves.Stem cells are undifferentiated, totipotent cells that are able to duplicate themselves and to form offspring that differentiates into multiple cell types. They are situated in a microenvironment, the stem cell niche, where extracellular signals maintain stem cell division at low rates and prevent differentiation (Ohlstein et al., 2004;Li and Xie, 2005). In plants, the best studied stem cell niches are within the root and shoot apical meristems. There, stem cells produce somatic daughter cells that go on dividing and expanding, thereby forming the postembryonic tissues and organs that make up the body of the plant. It is the balance between stem cell maintenance within the meristem and differentiation of cells that exit the niche that facilitates indeterminate root and shoot growth.SHORT-ROOT (SHR) and SCARECROW (SCR) are members of the GRAS family of transcription factors (Pysh et al., 1999;Lee et al., 2008), required for stem cell maintenance in the root apical meristem. Mutation of SHR and SCR genes causes a disorganization of the quiescent center (QC) and loss of stem cell activity, resulting in the depletion of proliferating cells in the root meristem and, consequently, cessation of root growth. Essentially, loss of SHR/SCR function renders root growth determinate. Furthermore, shr and scr mutants lack longitudinal cell divisions that separate the cortex/endodermis initial daughter cells, resulting in only one ground tissue cell layer (Benfey et al

Genome-Wide Direct Target Analysis Reveals a Role for SHORT-ROOT in Root Vascular Patterning through Cytokinin Homeostasis

“…To distinguish between these possibilities, we next measured cytokinin content in shr and wild-type plants. As shown in Table II, the concentrations of several types of cytokinin were significantly higher in both root and shoot of shr, consistent with the expression of SHR in both organs Dhondt et al, 2010;Gardiner et al, 2011). This result, along with the observations that exogenous cytokinin causes shr-like vascular patterning, strongly suggests that high cytokinin concentration is a major cause of the vascular patterning defect in shr.…”

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

“…Figure 2 shows that OsSHR2 transcripts accumulate in developing veins of plastochron P2 to P4 rice leaf primordia (where a plastochron is the time interval between the initiation of leaf primordia, and P1 is the youngest and closest to the shoot meristem from which the leaves are derived). In contrast to Arabidopsis, where AtSHR transcripts accumulate in procambium and persist throughout vascular development (Dhondt et al, 2010;Gardiner et al, 2011;Cui et al, 2014), OsSHR2 transcripts are detectable only in veins after the surrounding bundle sheath cells have differentiated, and then expression is relatively short-lived (Fig. 2C).…”

SCARECROW Has a SHORT-ROOT-Independent Role in Modulating the Sugar Response

“…In contrast, the ABI4 transcript level in the shr mutant remained almost unchanged, and the ABI5 transcript level was only moderately increased. Because SCR and SHR are also expressed in the shoot apical meristem, leaf primordium, and young leaves Dhondt et al, 2010;Gardiner et al, 2010) and shr and scr leaves showed obvious differences in sugar hypersensitivity, we also analyzed these ABI genes in the shoot. A similar trend was observed for ABI4 and ABI5 (Supplemental Fig.…”