Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling

Elitsa A. Ananieva, Glenda E. Gillaspy, Amanda Ely, Ryan N. Burnette, F. Les Erickson

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

In plants, myoinositol signaling pathways have been associated with several stress, developmental, and physiological processes, but the regulation of these pathways is largely unknown. In our efforts to better understand myoinositol signaling pathways in plants, we have found that the WD40 repeat region of a myoinositol polyphosphate 5-phosphatase (5PTase13; At1g05630) interacts with the sucrose nonfermenting-1-related kinase (SnRK1.1) in the yeast two-hybrid system and in vitro. Plant SnRK1 proteins (also known as AKIN10/11) have been described as central integrators of sugar, metabolic, stress, and developmental signals. Using mutants defective in 5PTase13, we show that 5PTase13 can act as a regulator of SnRK1 activity and that regulation differs with different nutrient availability. Specifically, we show that under low-nutrient or -sugar conditions, 5PTase13 acts as a positive regulator of SnRK1 activity. In contrast, under severe starvation conditions, 5PTase13 acts as a negative regulator of SnRK1 activity. To delineate the regulatory interaction that occurs between 5PTase13 and SnRK1.1, we used a cell-free degradation assay and found that 5PTase13 is required to reduce the amount of SnRK1.1 targeted for proteasomal destruction under low-nutrient conditions. This regulation most likely involves a 5PTase13-SnRK1.1 interaction within the nucleus, as a 5PTase13:green fluorescent protein was localized to the nucleus. We also show that a loss of function in 5PTase13 leads to nutrient level-dependent reduction of root growth, along with abscisic acid (ABA) and sugar insensitivity. 5ptase13 mutants accumulate less inositol 1,4,5-trisphosphate in response to sugar stress and have alterations in ABA-regulated gene expression, both of which are consistent with the known role of inositol 1,4,5-trisphosphate in ABA-mediated signaling. We propose that by forming a protein complex with SnRK1.1 protein, 5PTase13 plays a regulatory role linking inositol, sugar, and stress signaling.

Original languageEnglish (US)
Pages (from-to)1868-1882
Number of pages15
JournalPlant physiology
Volume148
Issue number4
DOIs
StatePublished - Dec 1 2008

Fingerprint

Polyphosphates
polyphosphates
Inositol
Phosphoric Monoester Hydrolases
Abscisic Acid
sugars
Food
Inositol 1,4,5-Trisphosphate
abscisic acid
Physiological Phenomena
nutrients
Plant Proteins
Two-Hybrid System Techniques
Physiological Stress
Starvation
Green Fluorescent Proteins
two hybrid system techniques
mutants
plant proteins
Proteins

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Ananieva, Elitsa A. ; Gillaspy, Glenda E. ; Ely, Amanda ; Burnette, Ryan N. ; Erickson, F. Les. / Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling. In: Plant physiology. 2008 ; Vol. 148, No. 4. pp. 1868-1882.
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abstract = "In plants, myoinositol signaling pathways have been associated with several stress, developmental, and physiological processes, but the regulation of these pathways is largely unknown. In our efforts to better understand myoinositol signaling pathways in plants, we have found that the WD40 repeat region of a myoinositol polyphosphate 5-phosphatase (5PTase13; At1g05630) interacts with the sucrose nonfermenting-1-related kinase (SnRK1.1) in the yeast two-hybrid system and in vitro. Plant SnRK1 proteins (also known as AKIN10/11) have been described as central integrators of sugar, metabolic, stress, and developmental signals. Using mutants defective in 5PTase13, we show that 5PTase13 can act as a regulator of SnRK1 activity and that regulation differs with different nutrient availability. Specifically, we show that under low-nutrient or -sugar conditions, 5PTase13 acts as a positive regulator of SnRK1 activity. In contrast, under severe starvation conditions, 5PTase13 acts as a negative regulator of SnRK1 activity. To delineate the regulatory interaction that occurs between 5PTase13 and SnRK1.1, we used a cell-free degradation assay and found that 5PTase13 is required to reduce the amount of SnRK1.1 targeted for proteasomal destruction under low-nutrient conditions. This regulation most likely involves a 5PTase13-SnRK1.1 interaction within the nucleus, as a 5PTase13:green fluorescent protein was localized to the nucleus. We also show that a loss of function in 5PTase13 leads to nutrient level-dependent reduction of root growth, along with abscisic acid (ABA) and sugar insensitivity. 5ptase13 mutants accumulate less inositol 1,4,5-trisphosphate in response to sugar stress and have alterations in ABA-regulated gene expression, both of which are consistent with the known role of inositol 1,4,5-trisphosphate in ABA-mediated signaling. We propose that by forming a protein complex with SnRK1.1 protein, 5PTase13 plays a regulatory role linking inositol, sugar, and stress signaling.",
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Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling. / Ananieva, Elitsa A.; Gillaspy, Glenda E.; Ely, Amanda; Burnette, Ryan N.; Erickson, F. Les.

In: Plant physiology, Vol. 148, No. 4, 01.12.2008, p. 1868-1882.

Research output: Contribution to journalArticle

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T1 - Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling

AU - Ananieva, Elitsa A.

AU - Gillaspy, Glenda E.

AU - Ely, Amanda

AU - Burnette, Ryan N.

AU - Erickson, F. Les

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AB - In plants, myoinositol signaling pathways have been associated with several stress, developmental, and physiological processes, but the regulation of these pathways is largely unknown. In our efforts to better understand myoinositol signaling pathways in plants, we have found that the WD40 repeat region of a myoinositol polyphosphate 5-phosphatase (5PTase13; At1g05630) interacts with the sucrose nonfermenting-1-related kinase (SnRK1.1) in the yeast two-hybrid system and in vitro. Plant SnRK1 proteins (also known as AKIN10/11) have been described as central integrators of sugar, metabolic, stress, and developmental signals. Using mutants defective in 5PTase13, we show that 5PTase13 can act as a regulator of SnRK1 activity and that regulation differs with different nutrient availability. Specifically, we show that under low-nutrient or -sugar conditions, 5PTase13 acts as a positive regulator of SnRK1 activity. In contrast, under severe starvation conditions, 5PTase13 acts as a negative regulator of SnRK1 activity. To delineate the regulatory interaction that occurs between 5PTase13 and SnRK1.1, we used a cell-free degradation assay and found that 5PTase13 is required to reduce the amount of SnRK1.1 targeted for proteasomal destruction under low-nutrient conditions. This regulation most likely involves a 5PTase13-SnRK1.1 interaction within the nucleus, as a 5PTase13:green fluorescent protein was localized to the nucleus. We also show that a loss of function in 5PTase13 leads to nutrient level-dependent reduction of root growth, along with abscisic acid (ABA) and sugar insensitivity. 5ptase13 mutants accumulate less inositol 1,4,5-trisphosphate in response to sugar stress and have alterations in ABA-regulated gene expression, both of which are consistent with the known role of inositol 1,4,5-trisphosphate in ABA-mediated signaling. We propose that by forming a protein complex with SnRK1.1 protein, 5PTase13 plays a regulatory role linking inositol, sugar, and stress signaling.

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