SCARECROW, SCR‐LIKE 23 and SHORT‐ROOT control bundle sheath cell fate and function in Arabidopsis thaliana

Abstract

SUMMARYBundle sheath (BS) cells form a single cell layer surrounding the vascular tissue in leaves. In C3 plants, photosynthesis occurs in both the BS and mesophyll cells, but the BS cells are the major sites of photosynthesis in C4 plants, whereas the mesophyll cells are only involved in CO 2 fixation. Because C4 plants are more efficient photosynthetically, introduction of the C4 mechanism into C3 plants is considered a key strategy to improve crop yield. One prerequisite for such C3-to-C4 engineering is the ability to manipulate the number and physiology of the BS cells, but the molecular basis of BS cell-fate specification remains unclear. Here we report that mutations in three GRAS family transcription factors, SHORT-ROOT (SHR), SCARECROW (SCR) and SCARECROW-LIKE 23 (SCL23), affect BS cell fate in Arabidopsis thaliana. SCR and SCL23 are expressed specifically in the BS cells and act redundantly in BS cell-fate specification, but their expression pattern and function diverge at later stages of leaf development. Using ChIP-chip experiments and sugar assays, we show that SCR is primarily involved in sugar transport whereas SCL23 functions in mineral transport. SHR is also essential for BS cell-fate specification, but it is expressed in the central vascular tissue. However, the SHR protein moves into the BS cells, where it directly regulates SCR and SCL23 expression. SHR, SCR and SCL23 homologs are present in many plant species, suggesting that this developmental pathway for BS cell-fate specification is likely to be evolutionarily conserved.

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

“…S1B) likely is accompanied by an increased rate of cell division during this stage. In addition, vascular tissue and BS development are apparent during this period because relevant TFs such as MONOPTEROS (MP), HOMEOBOX GENE 8 (HB8), PHABULOSA/ PHAVOLUTA (PHB/PHV), REVOLUTA (REV), SHORTROOT (SHR), and SCARECROW (SCR) (6,13,14) were all found in modules C16-C20 ( Fig. 2A).…”

The MYB36 transcription factor orchestrates Casparian strip formation

“…Existing evidence suggests that MYB36 expression is directly regulated by SCARECROW (SCR), as part of the differentiation program controlled by SHORT-ROOT (6)(7)(8)(9)(10). Considering the key role that Casparian strip development plays in marking endodermal differentiation, and the specific localization of MYB36-GFP to the endodermis ( that MYB36 may be directly controlling Casparian strip formation.…”

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).…”

“…AtSHR is expressed specifically in the vasculature, but the protein, which is a member of the GRAS transcription factor family, moves outward to surrounding cell layers, where it interacts with a second GRAS family member, SCARECROW (SCR). SHR-SCR interactions specify cells as endodermis in the root or bundle sheath in the shoot Cui et al, 2014). Given that stomatal patterning is coordinated with vascular patterning, and that both SHR and SCR are expressed during stomatal development in rice (Kamiya et al, 2003), we speculated that the SHR pathway might act to induce the bHLH pathway in epidermal cell files that flank leaf veins and, thus, to regulate the spacing and localization of stomatal rows.…”

“…In considering what might induce stomatal specification in those cell files, we reflected on known patterning mechanisms that operate around the vasculature. Of note is the SHORTROOT (SHR) pathway, which acts to radially pattern cells around veins in Arabidopsis (Levesque et al, 2006;Cui et al, 2014). AtSHR is expressed specifically in the vasculature, but the protein, which is a member of the GRAS transcription factor family, moves outward to surrounding cell layers, where it interacts with a second GRAS family member, SCARECROW (SCR).…”