AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis

Abstract

BackgroundSugar plays a central role as a source of carbon metabolism and energy production and a signaling molecule in diverse growth and developmental processes and environmental adaptation in plants. It is known that sugar metabolism and allocation between different physiological functions is intimately associated with flowering transition in many plant species. The INDETERMINATE DOMAIN (IDD)-containing transcription factor IDD8 regulates flowering time by modulating sugar metabolism and transport under sugar-limiting conditions in Arabidopsis. Meanwhile, it has been reported that SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE 1 (SnRK1), which acts as a sensor of cellular energy metabolism, is activated by sugar deprivation. Notably, SnRK1-overexpressing plants and IDD8-deficient mutants exhibit similar phenotypes, including delayed flowering, suggesting that SnRK1 is involved in the IDD8-mediated metabolic control of flowering.ResultsWe examined whether the sugar deprivation-sensing SnRK1 is functionally associated with IDD8 in flowering time control through biochemical and molecular genetic approaches. Overproduction of AKIN10, the catalytic subunit of SnRK1, delayed flowering in Arabidopsis, as was observed in IDD8-deficient idd8-3 mutant. We found that AKIN10 interacts with IDD8 in the nucleus. Consequently, AKIN10 phosphorylates IDD8 primarily at two serine (Ser) residues, Ser-178 and Ser-182, which reside in the fourth zinc finger (ZF) domain that mediates DNA binding and protein-protein interactions. AKIN10-mediated phosphorylation did not affect the subcellular localization and DNA-binding property of IDD8. Instead, the transcriptional activation activity of the phosphorylated IDD8 was significantly reduced. Together, these observations indicate that AKIN10 antagonizes the IDD8 function in flowering time control, a notion that is consistent with the delayed flowering phenotypes of AKIN10-overexpressing plants and idd8-3 mutant.ConclusionOur data show that SnRK1 and its substrate IDD8 constitute a sugar metabolic pathway that mediates the timing of flowering under sugar deprivation conditions. In this signaling scheme, the SnRK1 signals are directly integrated into the IDD8-mediated gene regulatory network that governs flowering transition in response to fluctuations in sugar metabolism, further supporting the metabolic control of flowering.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0503-8) contains supplementary material, which is available to authorized users.

Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle

“…SnRK1 phosphorylates the Indeterminate Domain (IDD) transcription factor IDD8, which results in its inactivation and delayed flowering under sugar starvation (Jeong et al, 2015). While SnRK1 and IDD8 have opposite functions in the regulation of flowering in response to carbon availability, overlapping functions between SnRK1 and its target FUS3 (which is stabilized after phosphorylation by SnRK1) have been described (Tsai and Gazzarrini, 2012).…”

STOREKEEPER RELATED1/G-Element Binding Protein (STKR1) Interacts with Protein Kinase SnRK1

“…Previous data suggest that SnRK1 can be localized to the cytosol as well as to the nucleus in Arabidopsis and N. benthamiana (Gazzarrini et al, 2004;Bitrián et al, 2011) and that the binding of SnRK1 to nucleus-localized proteins can change the partitioning in favor of a nuclear localization of the kinase (Nietzsche et al, 2014). Along that line, the interaction of SnRK1 with other transcription factors, such as FUSCA3, IDD8, and PETAL LOSS, also has been shown to occur inside the plant cell nucleus (Tsai and Gazzarrini, 2012;Jeong et al, 2015;O'Brien et al, 2015). Thus, we consider the nuclear localization of the SnRK1-STKR1 interaction physiologically relevant.…”

“…Negative regulation of a transcription factor by SnRK1-mediated phosphorylation has been shown for IDD8, which regulates flowering time in Arabidopsis by modulating sugar metabolism and transport under sugar-limiting conditions (Jeong et al, 2015). In this case, the protein stability of IDD8 is unaffected by protein phosphorylation but the modification inhibits the transcriptional activation activity of IDD8 through a yet unknown mechanism (Jeong et al, 2015).…”

“…FUS3 is a short-lived protein that is degraded rapidly by the 26S proteasome (Lu et al, 2010), and overexpression of AKIN10 delays FUS3 degradation by a yet uncharacterized mechanism and, thus, enhances its activity (Tsai and Gazzarrini, 2012). Negative regulation of a transcription factor by SnRK1-mediated phosphorylation has been shown for IDD8, which regulates flowering time in Arabidopsis by modulating sugar metabolism and transport under sugar-limiting conditions (Jeong et al, 2015). In this case, the protein stability of IDD8 is unaffected by protein phosphorylation but the modification inhibits the transcriptional activation activity of IDD8 through a yet unknown mechanism (Jeong et al, 2015).…”

“…In general, SnRK1-mediated transcriptional reprogramming results in the downregulation of energy-consuming processes and the induction of catabolic pathways to provide alternative energy sources. Although the broad effect on transcription and the specificity that is required to respond to a particular stress are likely to require modulation of a range of different downstream target proteins, only a few transcription factors representing potential direct SnRK1 substrates have been identified (Kleinow et al, 2009;Tsai and Gazzarrini, 2012;Jeong et al, 2015;O'Brien et al, 2015;Zhai et al, 2017). Recently, Mair et al (2015) identified the Arabidopsis transcription factor bZIP63 as a key regulator of the starvation response and a direct target of the SnRK1 kinase.…”