SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis

Abstract

The diterpenoid phytohormone gibberellin (GA) controls diverse developmental processes throughout the plant life cycle. DELLA proteins are master growth repressors that function immediately downstream of the GA receptor to inhibit GA signaling. By doing so, DELLAs also play pivotal roles as integrators of internal developmental signals from multiple hormone pathways and external cues. DELLAs are likely nuclear transcriptional regulators, which interact with other transcription factors to modulate expression of GA-responsive genes. DELLAs are also involved in maintaining GA homeostasis through feedback up-regulating expression of GA biosynthesis and receptor genes. However, the molecular mechanisms by which DELLAs restrict growth and development are largely unknown. This study reveals an important step of the mechanism. Previous microarray studies identified SCARECROW-LIKE 3 (SCL3) as a direct target gene of DELLA in Arabidopsis seedlings. SCL3 expression is induced by DELLA and repressed by GA. Unexpectedly, a scl3 null mutant displays reduced GA responses and elevated expression of GA biosynthesis genes during seed germination and seedling growth, indicating that SCL3 functions as a positive regulator of GA signaling. SCL3 seems to act as an attenuator of DELLA proteins. Transient expression, ChIP, and co-IP studies show that SCL3 autoregulates its own transcription by directly interacting with DELLA. Our data further show that SCL3 and DELLA antagonize each other in controlling both downstream GA responses and upstream GA biosynthetic genes. This work is beginning to shed light on how this complex regulatory network achieves GA homeostasis and controls GA-mediated growth and development in the plant.gibberellin-regulated development | hormone homeostasis | SCARECROW-LIKE 3-DELLA interaction | DELLA attenuator B ioactive gibberellins (GAs) are a class of phytohormones that plays critical roles in modulating plant growth and development in response to internal developmental programs and environmental cues (1-4). DELLA proteins are likely nuclear transcriptional regulators that function as master growth repressors by inhibiting all aspects of GA responses (1, 5, 6). Binding of GA to its receptor GA INSENSITIVE DWARF1 (GID1) enhances the GID1-DELLA interaction, which, in turn, leads to the rapid proteolysis of DELLA through the ubiquitin-proteasome pathway and allows transcriptional reprogramming of GA-responsive genes (7-11). A specific ubiquitin E3 ligase SCF SLY1/GID2 (Skp1-Cullin-Fbox protein complex) is responsible for recruiting DELLA for polyubiquitination (12)(13)(14)(15). DELLA proteins belong to a subfamily of the plant-specific GRAS family [for GA INSENSITIVE (GAI), REPRESSOR OF gal-3 (RGA), and SCARECROW (SCR)] of regulatory proteins (5, 16). In addition to the C-terminal GRAS domain that is common in all GRAS family members, DELLA protein also contains a unique DELLA domain in its N terminus that is required for GID1 binding and GA-induced degradation (7,(17)(18)(19)(20). Arabidopsis contains five DEL...

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

“…S5). These characteristics are reminiscent to those reported for SCL3 Zhang et al, 2011), which were also observed under our experimental conditions ( Fig. 4B; Supplemental Fig.…”

“…SEU Mediates the Regulation of SCL3 Expression by GA Signaling SCL3 expression is induced by DELLA proteins and repressed by GA Zhang et al, 2011), which acts in conjunction with SHR and SCR to regulate the formation of MC . Because our results showed that SCL3 is epistatic to SEU, we next examined whether GA signals through SEU to repress SCL3 expression.…”

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.…”

“…DELLA proteins lack a DNA binding domain; however, they function as transcription activators by interacting with INDETERMINATE Domain (IDD) proteins (Yoshida et al, 2014). In addition to interacting with IDDs, At-SCL3 can directly bind with its own promoter to regulate the expression in planta (Zhang et al, 2011). Mt-NSP1 can bind to the AATTT motif on the promoters, but Mt-NSP2 may have to associate with Mt-NSP1 for transcriptional regulation .…”

ARABIDOPSIS THALIANA HOMEOBOX25 Uncovers a Role for Gibberellins in Seed Longevity

“…The transcription factors that directly regulate the expression of GA3OX genes in Arabidopsis are only partially known (Hedden and Thomas, (Matsushita et al, 2007), SCARECROW-LIKE13 (Zhang et al, 2011), and SOMNUS (Kim et al, 2008), affects GA3OX1 and GA3OX2 expression, but there is no evidence for their binding to the promoter of the genes. Only FUS3 (Curaba et al, 2004) and DOF AFFECTING GERMINATION1 (Gabriele et al, 2010) have been shown to repress GA3OX1 and GA3OX2, respectively, by binding to the promoter of the regulated gene.…”