DELLA Signaling Mediates Stress-Induced Cell Differentiation in Arabidopsis Leaves through Modulation of Anaphase-Promoting Complex/Cyclosome Activity    

Abstract

Drought is responsible for considerable yield losses in agriculture due to its detrimental effects on growth. Drought responses have been extensively studied, but mostly on the level of complete plants or mature tissues. However, stress responses were shown to be highly tissue and developmental stage specific, and dividing tissues have developed unique mechanisms to respond to stress. Previously, we studied the effects of osmotic stress on dividing leaf cells in Arabidopsis (Arabidopsis thaliana) and found that stress causes early mitotic exit, in which cells end their mitotic division and start endoreduplication earlier. In this study, we analyzed this phenomenon in more detail. Osmotic stress induces changes in gibberellin metabolism, resulting in the stabilization of DELLAs, which are responsible for mitotic exit and earlier onset of endoreduplication. Consequently, this response is absent in mutants with altered gibberellin levels or DELLA activity. Mitotic exit and onset of endoreduplication do not correlate with an up-regulation of known cell cycle inhibitors but are the result of reduced levels of DP-E2F-LIKE1/E2Fe and UV-B-INSENSITIVE4, both inhibitors of the developmental transition from mitosis to endoreduplication by modulating anaphase-promoting complex/cyclosome activity, which are down-regulated rapidly after DELLA stabilization. This work fits into an emerging view of DELLAs as regulators of cell division by regulating the transition to endoreduplication and differentiation.

The role of gibberellin signalling in plant responses to abiotic stress

“…However, the early onset of endoreduplication and cellular differentiation did not appear to be affected (Skirycz et al, 2011). Consistent with the predicted role for ethylene and GA in proliferating cells ) differential expression of GA metabolism genes and DELLA-regulated transcripts as well as accumulation of RGA was observed in proliferating cells of mannitol-treated seedlings by 24 h post-transfer (Claeys et al, 2012;Skirycz et al, 2011). Early onset of endoreduplication triggered by mannitol was found to be abolished in several mutant lines with altered GA metabolism or signalling, including lines with increased (quintuple ga2ox) and reduced (ga3ox1-3) endogenous GA, or increased GA signalling (rga28, gai-2) (Claeys et al, 2012).…”

“…Our understanding of the role of GA in growth restriction triggered by abiotic stress has recently been advanced by a number of studies focusing on the response of A. thaliana seedlings to mild osmotic stress (Claeys et al, 2012;Skirycz et al, 2011;. Seedlings were exposed to a low concentration of the solute mannitol, which resulted in a 50% reduction in final leaf size as a result of effects on both cell proliferation and cell expansion (Skirycz et al, 2011;.…”

From network to phenotype: the dynamic wiring of an Arabidopsis transcriptional network induced by osmotic stress

“…Previous reports (Claeys et al , 2012; Dubois et al , 2013) have shown the importance of gibberellic acid (GA) degradation in the response to mannitol treatment. To further explore this finding in our experimental setup, the expression profile of genes encoding two GA degradation ( GIBBERELLIN2‐OXIDASE4 and GIBBERELLIN2‐OXIDASE6 ) and two GA biosynthesis enzymes ( GIBBERELLIN3‐OXIDASE1 and GIBBERELLIN20‐OXIDASE1 ) was measured in expanding leaves over time (20 min, 40 min, 1 h, 2 h, 4 h, 8 h, 12 h, 16 h, and 24 h after transfer to mannitol‐containing or control medium).…”

“…Remarkably, in expanding leaf tissue, the upregulation by mannitol reached higher levels (log 2 (FC) = 4.71 compared to log 2 (FC) = 0.90 in proliferating tissue, Dataset EV1) and in addition, the timing of the upregulation was altered. Already 2 h after mannitol treatment, GA2‐OX6 expression levels reached significant values (log 2 (FC) = 5.21, FDR = 0.014, Student's t ‐test) in expanding tissues, whereas the induction was only significant after 24 h in proliferating tissue (Skirycz et al , 2011; Claeys et al , 2012) (Dataset EV1). In accordance with previous observations (Skirycz et al , 2011; Dubois et al , 2013), none of the other tested GA oxidases showed a significant upregulation over the analyzed time course.…”

“…Few members of this transcriptional cascade have been studied previously, such as the rapidly induced ETHYLENE RESPONSE FACTOR 6 ( ERF6 ), which activates the expression of GIBBERELLIN2‐OXIDASE6 ( GA2‐OX6 ), a gene encoding a gibberellin‐inactivating enzyme (Rieu et al , 2008; Dubois et al , 2013). Because of the resulting lower levels of gibberellin, DELLA proteins are stabilized, which ensures that cells permanently exit the cell division phase and are pushed to cell differentiation (Claeys et al , 2012). The transcriptional repressor ERF11 also has been characterized and could counteract the effect of ERF6 both on molecular and phenotypic level (Dubois et al , 2015).…”