Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root

Abstract

During plant development, because no cell movement takes place, control of the timing and extent of cell division and coordination of the direction and extent of cell expansion are particularly important for growth and development. The plant hormone gibberellins (GAs) play key roles in the control of these developmental processes. However, little is known about the molecular components that integrate the generic GA signaling into a specific cell/tissue to coordinate cell division and cell expansion. Here we report that SCARECROW-LIKE 3 (SCL3), a GRAS protein, acts as a positive regulator to integrate and maintain a functional GA pathway by attenuating the DELLA repressors in the root endodermis. The tissue-specific maintenance of GA signaling in the root endodermis plays distinct roles along the longitudinal root axis. While in the elongation/differentiation zone (EDZ), the endodermis-confined GA pathway by SCL3 controls primarily coordination of root cell elongation; in the meristem zone (MZ) SCL3 in conjunction with the SHORT-ROOT/SCARECROW (SHR/SCR) pathway controls GA-modulated ground tissue maturation. Our findings highlight the regulatory network of the GRAS transcription regulators (SCL3, DELLAs, and SHR/SCR) in the root endodermis, shedding light on how GA homeostasis is achieved and how the maintenance of GA signaling controls developmental processes in roots.

SEUSS Integrates Gibberellin Signaling with Transcriptional Inputs from the SHR-SCR-SCL3 Module to Regulate Middle Cortex Formation in the Arabidopsis Root

“…3D). This finding is consistent with previous reports showing that SHR is indispensable for MC formation (Paquette and Benfey, 2005;Heo et al, 2011). Since a reduction of SHR is necessary to permit the formation of MC (Koizumi et al, 2012b), we hypothesized that SEU is required to maintain high levels of SHR that prevent MC formation (Koizumi et al, 2012b).…”

“…During the last decade, several interconnected mechanisms have been proposed to be responsible for the MC formation (Paquette and Benfey, 2005;Cui et al, 2007;Heo et al, 2011;Koizumi et al, 2012a;Koizumi et al, 2012b;Koizumi and Gallagher, 2013). Two GRAS family transcription factors, SHORT-ROOT (SHR; Helariutta et al, 2000) and SCARECROW (SCR; Di Laurenzio et al, 1996), have been shown to play crucial roles in shaping these mechanisms.…”

“…High levels of SHR in the endodermis inhibit the formation of the MC, whereas intermediate levels of SHR, which occur physiologically during root development or if induced by a reduction or loss of SCR activity, promote MC formation (Koizumi et al, 2012b). GA function, which decreases in the meristem starting at 5 d postgermination under physiological conditions (Paquette and Benfey, 2005;Moubayidin et al, 2010;Heo et al, 2011), is thought to influence the abundance of SHR and subsequently the formation of MC (Koizumi et al, 2012b). In addition, GA has also been shown to repress SCARECROW-LIKE3 (SCL3), a SHR and SCR target (Levesque et al, 2006;Cui et al, 2007) that encodes another GRAS family transcription factor and positively regulates GAmediated control of MC formation .…”

“…The repressive effect of GA on SCL3 is most likely accomplished through GA-mediated degradation of DELLA domain GRAS family transcription factors, which are critical negative regulators of GA signaling and direct upstream activators of SCL3 (Zentella et al, 2007;Heo et al, 2011). SEUSS (SEU) encodes an Arabidopsis protein with a conserved central domain that shares sequence homology with the dimerization domain of the LIMdomain-binding transcriptional coregulators (Franks et al, 2002), which play fundamental roles in animal development (Matthews and Visvader, 2003;Bronstein et al, 2010;Bronstein and Segal, 2011).…”

Crystal Structure of the GRAS Domain of SCARECROW-LIKE7 inOryza sativa

“…Moreover, GRAS proteins have been reported to form homodimers and heterodimers with other GRAS family members and this is likely important for their transcriptional regulation function (Itoh et al, 2002;Cui et al, 2007;Heo et al, 2011;Zhang et al, 2011;Gobbato et al, 2012;Murakami et al, 2013;Xue et al, 2015). Here, our structure of Os-SCL7 was determined in a dimer with helices A12, A79, and A69 at the dimer interface.…”