Salt-triggered expression of the ANAC092-dependent senescence regulon in Arabidopsis thaliana

Abstract

The NAC domain transcription factor ANAC092 plays a central role in leaf senescence in Arabidopsis thaliana. We recently identified 170 genes whose expression increases upon activation of ANAC092 in a chemically (estradiol) controlled experimental set-up, 78 of which are known senescence-associated genes (SAGs). In accordance with the well-known phenomenon that salt stress promotes early leaf senescence in many plant species, we previously observed salt stress-enhanced expression of many SAGs of the ANAC092 regulon. Global expression profiling now revealed that 36 genes, representing 46% of all ANAC092 downstream SAGs, are induced by long-term (4 days) salt stress in shoots of Arabidopsis, whereas short-term stress (6 hours) only slightly affects gene expression. Expression analysis also showed that 14 of the 36 genes are induced by hydrogen peroxide (H2O2) treatment. Additionally, 15 senescence-associated NAC genes (senNACs), including ANAC092, respond to H2O2 exposure. Our data support the model that salt-triggered senescence is at least partly mediated through the ANAC092 gene regulatory network. Other senNACs most likely contribute to the coordination of this process, potentially in concert with H2O2-mediated signaling.

Figure 1

Role of ANAC092/AtNAC2/ORE1 transcription factor in salt-promoted senescence. Left: The currently known ANAC092 senescence regulon includes 78 genes of which 36 genes are induced by long-term salt stress. Twenty-six of the salt-induced SAGs contain an ANAC092-binding site in their 1-kb upstream promoter (see Suppl. Table 1). Middle: Hierarchical clustering of the 36 salt-induced SAGs (plus ANAC092 itself, bold). Clusters were generated from expression data obtained from salt-treated plants (150 mM NaCl; 6 h and 4 d time-points). Gene expression ratios: dark blue, maximum (+3: more than 3 cycles difference to control, or 8-fold upregulation); dark red, minimum (−3: more than 3 cycles, or 8-fold downregulation). Right: Model for salinity stress-induced induction of SAG gene expression and promotion of senescence. Salt stress-induced senescence may be triggered through an elevation of cellular H₂O₂ level that triggers the expression of various senNAC genes, some of which respond rapidly to elevated H₂O₂ levels (including the positive senescence regulator AtNAP), whereas others (e.g., ANAC092) exhibit a delayed response. The mechanisms of cross-talk between H₂O₂ and phytohormone signaling [e.g., involving ethylene, salicylic acid (SA) or abscisic acid (ABA)] in relation to salt-induced senescence are not yet known in detail.