Interplay between ABA and GA Modulates the Timing of Asymmetric Cell Divisions in the Arabidopsis Root Ground Tissue

Abstract

In multicellular organisms, controlling the timing and extent of asymmetric cell divisions (ACDs) is crucial for correct patterning. During post-embryonic root development in Arabidopsis thaliana, ground tissue (GT) maturation involves an additional ACD of the endodermis, which generates two different tissues: the endodermis (inner) and the middle cortex (outer). It has been reported that the abscisic acid (ABA) and gibberellin (GA) pathways are involved in middle cortex (MC) formation. However, the molecular mechanisms underlying the interaction between ABA and GA during GT maturation remain largely unknown. Through transcriptome analyses, we identified a previously uncharacterized C2H2-type zinc finger gene, whose expression is regulated by GA and ABA, thus named GAZ (GA- AND ABA-RESPONSIVE ZINC FINGER). Seedlings ectopically overexpressing GAZ (GAZ-OX) were sensitive to ABA and GA during MC formation, whereas GAZ-SRDX and RNAi seedlings displayed opposite phenotypes. In addition, our results indicated that GAZ was involved in the transcriptional regulation of ABA and GA homeostasis. In agreement with previous studies that ABA and GA coordinate to control the timing of MC formation, we also confirmed the unique interplay between ABA and GA and identified factors and regulatory networks bridging the two hormone pathways during GT maturation of the Arabidopsis root.

Control of Asymmetric Cell Divisions during Root Ground Tissue Maturation

“…Under normal growth conditions, Columbia wild-type (Col WT) roots undergo periclinal ACDs in the endodermis around 7 to 14 dpg, resulting in an average of 20 to 35% of plants with the MC layer, depending on experimental conditions ( Cui and Benfey, 2009a ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ). Under gibberellin (GA)-deficient conditions, induced by treatment with a GA biosynthesis inhibitor (e.g., paclobutrazol; PAC) or by loss-of-function mutations in a key GA biosynthesis enzyme (e.g., ga1-3 ), seedling roots exhibit a 2- to 3-fold increase in MC formation ( Cui and Benfey, 2009a ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ). In contrast, exogenous GA application substantially suppresses periclinal ACDs in the endodermis, thus resulting in delayed MC formation ( Cui and Benfey, 2009a ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ).…”

“…Under gibberellin (GA)-deficient conditions, induced by treatment with a GA biosynthesis inhibitor (e.g., paclobutrazol; PAC) or by loss-of-function mutations in a key GA biosynthesis enzyme (e.g., ga1-3 ), seedling roots exhibit a 2- to 3-fold increase in MC formation ( Cui and Benfey, 2009a ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ). In contrast, exogenous GA application substantially suppresses periclinal ACDs in the endodermis, thus resulting in delayed MC formation ( Cui and Benfey, 2009a ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ). These findings indicate that modulation of bioactive GA levels is critical for the regulation of MC formation in the Arabidopsis root GT.…”

“…In addition, transgenic Arabidopsis plants with XERICO fused to the 35S promoter ( XER overexpressor; XER-OX ), which substantially increases cellular ABA levels, probably through the ubiquitin/proteasome-dependent degradation pathway ( Ko et al, 2006 ), have almost no MC layer at 7 dpg ( Cui and Benfey, 2009a ; 2009b ; Lee et al, 2016 ). In contrast, under ABA-deficient conditions caused by loss-of-function mutations in a key ABA biosynthesis enzyme ( aba2-2 ) or in the XER gene ( xer ), seedlings display more frequent periclinal ACDs for MC formation ( Lee et al, 2016 ). Interestingly, the ABA-deficient aba2-2 and xer mutants are sensitive to PAC, resulting in the precocious formation of the MC layer.…”

“…Therefore, production of the MC layer by periclinal ACDs in the endodermis is considered to be an indication that post-embryonic root development has entered a more mature phase ( Baum et al, 2002 ; Paquette and Benfey, 2005 ; Pauluzzi et al, 2012 ). To assess maturation of the Arabidopsis root GT, the formation of the MC layer, as measured by the proportion of plants with MC either at a specific time point or in time courses, has been used ( Baum et al, 2002 ; Cui and Benfey, 2009a ; 2009b ; Gong et al, 2016 ; Heo et al, 2011 ; Koizumi et al, 2012a ; 2012b ; Lee et al, 2016 ; Paquette and Benfey, 2005 ; Pauluzzi et al, 2012 ).…”

APETALA 2‐domain‐containing transcription factors: focusing on abscisic acid and gibberellins antagonism

“…The rose ( Rosa hybrida ) homeodomain‐leucine zipper I transcription factor RhHB1 directly binds to the promoter of RhGA20ox1 , and thus mediates the antagonistic effect of GA on ABA and ethylene during rose petal senescence processes (Lu et al ., ). Recently, the transcription factor GA‐ AND ABA‐RESPONSIVE ZINC FINGER (GAZ) was shown to mediate ABA–GA homeostasis in the root, controlling middle cortex formation, in which GAZ served as a point of convergence for the interaction between ABA and GA by regulating the expression levels of GA biosynthesis genes GA20ox and GA3ox and the ABA catabolism gene CYP707A1 (Lee et al ., ).…”