Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis

Yechun Hong; Zhen Wang; Huazhong Shi; Juanjuan Yao; Xue Liu; Fuxing Wang; Liang Zeng; Zhi Xie; Jian-Kang Zhu

doi:10.1371/journal.pgen.1008892

Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis

PLoS Genet. 2020 Jun 22;16(6):e1008892. doi: 10.1371/journal.pgen.1008892. eCollection 2020 Jun.

Authors

Yechun Hong^{1

2}, Zhen Wang¹, Huazhong Shi³, Juanjuan Yao^{1

2}, Xue Liu¹, Fuxing Wang^{1

2}, Liang Zeng¹, Zhi Xie^{1

2}, Jian-Kang Zhu^{1

4}

Affiliations

¹ Shanghai Center for Plant Stress Biology and Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China.
² University of Chinese Academy of Sciences, Shanghai, P.R. China.
³ Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, Texas, United States of America.
⁴ Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana, United States of America.

Abstract

Nicotinamide adenine dinucleotide (NAD) is an essential coenzyme that has emerged as a central hub linking redox equilibrium and signal transduction in living organisms. The homeostasis of NAD is required for plant growth, development, and adaption to environmental cues. In this study, we isolated a chilling hypersensitive Arabidopsis thaliana mutant named qs-2 and identified the causal mutation in the gene encoding quinolinate synthase (QS) critical for NAD biosynthesis. The qs-2 mutant is also hypersensitive to salt stress and abscisic acid (ABA) but resistant to drought stress. The qs-2 mutant accumulates a reduced level of NAD and over-accumulates reactive oxygen species (ROS). The ABA-hypersensitivity of qs-2 can be rescued by supplementation of NAD precursors and by mutations in the ABA signaling components SnRK2s or RBOHF. Furthermore, ABA-induced over-accumulation of ROS in the qs-2 mutant is dependent on the SnRK2s and RBOHF. The expression of QS gene is repressed directly by ABI4, a transcription factor in the ABA response pathway. Together, our findings reveal an unexpected interplay between NAD biosynthesis and ABA and stress signaling, which is critical for our understanding of the regulation of plant growth and stress responses.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Abscisic Acid / metabolism
Arabidopsis / physiology*
Arabidopsis Proteins / genetics
Arabidopsis Proteins / isolation & purification
Arabidopsis Proteins / metabolism
Feedback, Physiological
Gene Expression Profiling
Gene Expression Regulation, Plant*
Multienzyme Complexes / genetics*
Multienzyme Complexes / isolation & purification
Multienzyme Complexes / metabolism
Mutation
NAD / biosynthesis
NADPH Oxidases / metabolism
Plant Growth Regulators / metabolism*
Plants, Genetically Modified
Protein Serine-Threonine Kinases / metabolism
Reactive Oxygen Species / metabolism
Recombinant Proteins / genetics
Recombinant Proteins / isolation & purification
Recombinant Proteins / metabolism
Signal Transduction / physiology
Stress, Physiological / genetics*
Transcription Factors / genetics
Transcription Factors / isolation & purification
Transcription Factors / metabolism

Substances

ABI4 protein, Arabidopsis
Arabidopsis Proteins
Multienzyme Complexes
Plant Growth Regulators
Reactive Oxygen Species
Recombinant Proteins
Transcription Factors
NAD
quinolinic acid synthetase
Abscisic Acid
NADPH Oxidases
RbohF protein, Arabidopsis
Protein Serine-Threonine Kinases

Grants and funding

This work was supported by the Strategic Priority Research Program (XDB27040101 to J.-K.Z.) and the Youth Innovation Promotion Association (2020273 to Z.W.) of the Chinese Academy of Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.