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

Abstract

A decade of studies on middle cortex (MC) formation in the root endodermis of Arabidopsis (Arabidopsis thaliana) have revealed a complex regulatory network that is orchestrated by several GRAS family transcription factors, including SHORT-ROOT (SHR), SCARECROW (SCR), and SCARECROW-LIKE3 (SCL3). However, how their functions are regulated remains obscure. Here we show that mutations in the SEUSS (SEU) gene led to a higher frequency of MC formation. seu mutants had strongly reduced expression of SHR, SCR, and SCL3, suggesting that SEU positively regulates these genes. Our results further indicate that SEU physically associates with upstream regulatory sequences of SHR, SCR, and SCL3; and that SEU has distinct genetic interactions with these genes in the control of MC formation, with SCL3 being epistatic to SEU. Similar to SCL3, SEU was repressed by the phytohormone GA and induced by the GA biosynthesis inhibitor paclobutrazol, suggesting that SEU acts downstream of GA signaling to regulate MC formation. Consistently, we found that SEU mediates the regulation of SCL3 by GA signaling. Together, our study identifies SEU as a new critical player that integrates GA signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate MC formation in the Arabidopsis root.

Uncovering Gene Regulatory Networks Controlling Plant Cell Differentiation

“…Both SCR and SCL3 act to repress middle cortex division, as single mutants of either results in precocious middle cortex formation [25,27]. Recently, a predicted transcriptional co-regulator, SEUSS (SEU), was identified as a positive regulator of SHR , SCR and SCL3 , and prevents middle cortex formation by keeping SHR levels high [28]. Although SEU has been shown to be a negative co-regulator in flower development, in middle cortex formation it can directly bind to upstream regions of SHR , SCR and SCL3 [28–30].…”

“…Recently, a predicted transcriptional co-regulator, SEUSS (SEU), was identified as a positive regulator of SHR , SCR and SCL3 , and prevents middle cortex formation by keeping SHR levels high [28]. Although SEU has been shown to be a negative co-regulator in flower development, in middle cortex formation it can directly bind to upstream regions of SHR , SCR and SCL3 [28–30]. This suggests the role of SEU is context dependent and characterizing its interaction factors and its binding to DNA will be of interest for further study.…”

“…Like shr mutants, shby is insensitive to effects of GA inhibitors on middle cortex formation, suggesting that SHBY is required for middle cortex regulation via GA signaling [23]. Recently, it has been shown that GA represses SCL3 indirectly by repressing the SCL3 -activator SEU, resulting in precocious middle cortex formation [28]. This provides another common link between the SHR/SCR pathway and the GA pathway in middle cortex formation [28].…”

“…Recently, it has been shown that GA represses SCL3 indirectly by repressing the SCL3 -activator SEU, resulting in precocious middle cortex formation [28]. This provides another common link between the SHR/SCR pathway and the GA pathway in middle cortex formation [28]. It is notable that CYCD6 is expressed at the onset of middle cortex formation and that seuss and shby mutants, as well as wild-type roots, treated with GA inhibitor have expanded CYCD6 expression [23,28].…”

“…This provides another common link between the SHR/SCR pathway and the GA pathway in middle cortex formation [28]. It is notable that CYCD6 is expressed at the onset of middle cortex formation and that seuss and shby mutants, as well as wild-type roots, treated with GA inhibitor have expanded CYCD6 expression [23,28]. Therefore, it is likely that GA and SHR/SCR also commonly regulate CYCD6 .…”