Ca²⁺-Activated Reactive Oxygen Species Production by Arabidopsis RbohH and RbohJ Is Essential for Proper Pollen Tube Tip Growth

In flowering plants, pollen germinates on the stigma and pollen tubes grow through the style to fertilize the ovules. Enzymatic production of reactive oxygen species (ROS) has been suggested to be involved in pollen tube tip growth. Here, we characterized the function and regulation of the NADPH oxi...

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Bibliographic Details
Published in:The Plant cell 2014-03, Vol.26 (3), p.1069-1080
Main Authors: Kaya, Hidetaka, Nakajima, Ryo, Iwano, Megumi, Kanaoka, Masahiro M., Kimura, Sachie, Takeda, Seiji, Kawarazaki, Tomoko, Senzaki, Eriko, Hamamura, Yuki, Higashiyama, Tetsuya, Takayama, Seiji, Abe, Mitsutomo, Kuchitsu, Kazuyuki
Format: Article
Language:English
Subjects:
Amino Acid Sequence
Arabidopsis - growth & development
Arabidopsis - metabolism
Arabidopsis Proteins - chemistry
Arabidopsis Proteins - genetics
Arabidopsis Proteins - physiology
Calcium - metabolism
Cell growth
Cell walls
HEK293 cells
Ionomycin - pharmacology
Molecular Sequence Data
Mutation
NADPH Oxidases - chemistry
NADPH Oxidases - genetics
NADPH Oxidases - physiology
Oxazoles - pharmacology
Oxidases
Plant cells
Plant growth regulators
Plants
Pollen
Pollen Tube - growth & development
Pollen tubes
Reactive oxygen species
Reactive Oxygen Species - metabolism
Sequence Homology, Amino Acid
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Summary:In flowering plants, pollen germinates on the stigma and pollen tubes grow through the style to fertilize the ovules. Enzymatic production of reactive oxygen species (ROS) has been suggested to be involved in pollen tube tip growth. Here, we characterized the function and regulation of the NADPH oxidases RbohH and RbohJ (Respiratory burst oxidase homolog H and J) in pollen tubes in Arabidopsis thaliana. In the rbohH and rbohJ single mutants, pollen tube tip growth was comparable to that of the wild type; however, tip growth was severely impaired in the double mutant. In vivo imaging showed that ROS accumulation in the pollen tube was impaired in the double mutant. Both RbohH and RbohJ, which contain Ca²⁺ binding EF-hand motifs, possessed Ca²⁺-induced ROS-producing activity and localized at the plasma membrane of the pollen tube tip. Point mutations in the EF-hand motifs impaired Ca²⁺-induced ROS production and complementation of the double mutant phenotype. We also showed that a protein phosphatase inhibitor enhanced the Ca²⁺-induced ROS-producing activity of RbohH and RbohJ, suggesting their synergistic activation by protein phosphorylation and Ca²⁺. Our results suggest that ROS production by RbohH and RbohJ is essential for proper pollen tube tip growth, and furthermore, that Ca²⁺-induced ROS positive feedback regulation is conserved in the polarized cell growth to shape the long tubular cell.
ISSN:1040-4651
1532-298X
DOI:10.1105/tpc.113.120642