Coordinated Responses to Oxygen and Sugar Deficiency Allow Rice Seedlings to Tolerate Flooding

Abstract

Flooding is a widespread natural disaster that leads to oxygen (O(2)) and energy deficiency in terrestrial plants, thereby reducing their productivity. Rice is unusually tolerant to flooding, but the underlying mechanism for this tolerance has remained elusive. Here, we show that protein kinase CIPK15 [calcineurin B-like (CBL)-interacting protein kinase] plays a key role in O(2)-deficiency tolerance in rice. CIPK15 regulates the plant global energy and stress sensor SnRK1A (Snf1-related protein kinase 1) and links O(2)-deficiency signals to the SnRK1-dependent sugar-sensing cascade to regulate sugar and energy production and to enable rice growth under floodwater. Our studies contribute to understanding how rice grows under the conditions of O(2) deficiency necessary for growing rice in irrigated lowlands.

Nitrogen metabolism in plants under low oxygen stress

“…2 we put forward the hypothesis of a cross-talk between hypoxia and darkness signaling pathways for the induction of AlaAT expression. This hypothesis is consistent with the observation that in flooded rice, CIPK15 [calcineurin B-like (CBL)-interacting protein kinase] controls the expression of ADH as a response to low oxygen stress through SnRK1A (Lee et al 2009). …”

“…KIN10/KIN11 two members of the Snrk family were shown to mediate darkness and oxygen stress signal in Arabidopsis isolated mesophyll cells and whole plants (Baena-González et al 2007). CIPK15 was shown to act through Snrk1A for the regulation of sugar fermentation in anoxic rice (Lee et al 2009). Posttranslational regulation of GDC is triggered by hypoxia-induced increase in cytoplasmic (cyto) H + and Ca 2+ concentrations.…”

“…In coleoptiles of rice growing under low oxygen the abundance of SUS4, enzymes involved in several steps of glycolysis, e.g., pyrophosphate (PPi)-Fru-6-P 1-phosphotransferase, Fructose-bisP aldolase, triosephosphate isomerase, glyceraldehyde-3-phosphate dehydrogenase and enzymes of ethanolic fermentation, ADH1 and PDC1 increased significantly compared to aerobic condition (Shingaki-Wells et al 2011). Up-regulation of hypoxia-induced genes of sugar metabolism was mediated by the protein kinase CIPK15 (Calcineurin B-like protein kinase interfering protein kinase) that activated the stress sensor SnRK1A (sugar non-fermenting related protein kinase) thus connecting sensing of O 2 -deficiency signal to the flooding response of rice seedling (Lee et al 2009). …”

Differential Anoxic Expression of Sugar-Regulated Genes Reveals Diverse Interactions between Sugar and Anaerobic Signaling Systems in Rice

“…One of mechanisms that underlie the anaerobic induction of type-2 genes would be transcriptional activation through specific cis-regulatory elements as seen in many anaerobic genes (Hoeren et al, 1998;Mohanty et al, 2012;Olive et al, 1991). Previous molecular characterization of rice knockout mutant for CIPK15 gene suggested that this protein may serve as a positive key regulator to direct the O 2 deficiency signal to sugar sensing cascade via activating SnRK1 (Lee et al, 2009). Therefore, the interference with sugar signaling by O 2 deprivation observed in type-1 and -2 genes may be mediated by this CIPK15-SnRK1 pathway.…”

EXORDIUM-LIKE1 Promotes Growth during Low Carbon Availability in Arabidopsis

“…AtSnAK1/GRIK2 and AtSnAK2/GRIK1 act as upstream kinases and activate SnRK1 (Hey et al, 2007;Shen et al, 2009). The calcineurin B-like-interacting protein kinase CIPK15 is an upstream regulator of SnRK1A in rice (Oryza sativa) and links oxygen-deficiency signals to the SnRK1-dependent sugar sensing cascade (Lu et al, 2007;Lee et al, 2009).…”