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PMID: 23370720 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development.

Plant physiology ·Vol. 161 ·No. 2 ·2013-02-00 ·Pages 1010-20

Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF

Abstract

Cyclic nucleotide-gated channels (CNGCs) have been implicated in diverse aspects of plant growth and development, including responses to biotic and abiotic stress, as well as pollen tube growth and fertility. Here, genetic evidence identifies CNGC16 in Arabidopsis (Arabidopsis thaliana) as critical for pollen fertility under conditions of heat stress and drought. Two independent transfer DNA disruptions of cngc16 resulted in a greater than 10-fold stress-dependent reduction in pollen fitness and seed set. This phenotype was fully rescued through pollen expression of a CNGC16 transgene, indicating that cngc16-1 and 16-2 were both loss-of-function null alleles. The most stress-sensitive period for cngc16 pollen was during germination and the initiation of pollen tube tip growth. Pollen viability assays indicate that mutant pollen are also hypersensitive to external calcium chloride, a phenomenon analogous to calcium chloride hypersensitivities observed in other cngc mutants. A heat stress was found to increase concentrations of 3',5'-cyclic guanyl monophosphate in both pollen and leaves, as detected using an antibody-binding assay. A quantitative PCR analysis indicates that cngc16 mutant pollen have attenuated expression of several heat-stress response genes, including two heat shock transcription factor genes, HsfA2 and HsfB1. Together, these results provide evidence for a heat stress response pathway in pollen that connects a cyclic nucleotide signal, a Ca(2+)-permeable ion channel, and a signaling network that activates a downstream transcriptional heat shock response.

MeSH Terms
Adaptation, Physiological/drug effects,genetics Arabidopsis Proteins/genetics,metabolism Base Sequence Calcium Chloride/pharmacology Cyclic GMP/metabolism Cyclic Nucleotide-Gated Cation Channels/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Droughts Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Heat Shock Transcription Factors Heat-Shock Proteins/genetics,metabolism Hot Temperature Molecular Sequence Data Mutation Plant Leaves/genetics,growth & development,metabolism Plant Proteins/genetics,metabolism Plants, Genetically Modified Pollen/genetics,growth & development,metabolism Pollen Tube/genetics,growth & development,metabolism Reproduction/genetics Reverse Transcriptase Polymerase Chain Reaction Stress, Physiological Transcription Factors/genetics,metabolism
Chemicals
Arabidopsis Proteins CNGC16 protein, Arabidopsis Cyclic Nucleotide-Gated Cation Channels DNA-Binding Proteins HSFA2 protein, Arabidopsis HSFB1 protein, Arabidopsis Heat Shock Transcription Factors Heat-Shock Proteins Plant Proteins Transcription Factors Cyclic GMP Calcium Chloride
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Tunc-Ozdemir Meral
Department of Biochemistry, University of Nevada, Reno, Nevada 89557, USA.
Tang Chong
Ishka Maryam Rahmati
Brown Elizabeth
Groves Norman R
Myers Candace T
Rato Claudia
Poulsen Lisbeth R
McDowell Stephen
Miller Gad
Mittler Ron
Harper Jeffrey F
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Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
DOI
10.1104/pp.112.206888
Published
2013-02-00
Epub
2012-00-12
Pages
1010-20
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3560999
Subset
IM
Grants
NCRR NIH HHS · RR024210 · United States
NCRR NIH HHS · P20 RR024210 · United States
NCRR NIH HHS · P20 RR-016464 · United States
NIGMS NIH HHS · 1R01 GM070813-01 · United States
NIGMS NIH HHS · P20 GM103554 · United States
PHS HHS · FG03-94ER20152 · United States
External Links
PubMed source DOI: 10.1104/pp.112.206888 PMC Full Text View journal details
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