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. 2014 Feb 14;9(2):e88320.
doi: 10.1371/journal.pone.0088320. eCollection 2014.

A Petunia homeodomain-leucine zipper protein, PhHD-Zip, plays an important role in flower senescence

Xiaoxiao Chang  1 , Linda Donnelly  2 , Daoyang Sun  1 , Jingping Rao  3 , Michael S Reid  4 , Cai-Zhong Jiang  2
Affiliations

A Petunia homeodomain-leucine zipper protein, PhHD-Zip, plays an important role in flower senescence

Xiaoxiao Chang et al. PLoS One. .

Abstract

Flower senescence is initiated by developmental and environmental signals, and regulated by gene transcription. A homeodomain-leucine zipper transcription factor, PhHD-Zip, is up-regulated during petunia flower senescence. Virus-induced gene silencing of PhHD-Zip extended flower life by 20% both in unpollinated and pollinated flowers. Silencing PhHD-Zip also dramatically reduced ethylene production and the abundance of transcripts of genes involved in ethylene (ACS, ACO), and ABA (NCED) biosynthesis. Abundance of transcripts of senescence-related genes (SAG12, SAG29) was also dramatically reduced in the silenced flowers. Over-expression of PhHD-Zip accelerated petunia flower senescence. Furthermore, PhHD-Zip transcript abundance in petunia flowers was increased by application of hormones (ethylene, ABA) and abiotic stresses (dehydration, NaCl and cold). Our results suggest that PhHD-Zip plays an important role in regulating petunia flower senescence.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Expression of PhHD-Zip in petunia corollas during flower senescence.
A. A representative gel image from semi-quantitative PCR of RNA isolated from corollas harvested at intervals after anthesis. D0: at anthesis; D2, D4, D7: 2, 4, and 7 days after anthesis, respectively. 26S RNA: the internal control. Samples were analyzed after 30 cycles of amplification for PhHD-Zip, and after 24 cycles of amplification for 26S RNA. B. Relative expression levels of PhHD-Zip (quantification of the gel pictures; error bars show SE of the means of three biological replicates).
Figure 2
Figure 2. Expression of PhHD-Zip in different tissues of petunia.
A. A representative gel image from semi-quantitative PCR of RNA isolated from different tissues. 26S RNA: the internal control. Samples were analyzed after 33 cycles for PhHD-Zip, and after 24 cycles for 26S RNA. B. Relative expression levels of PhHD-Zip in different tissues (quantification of the gel pictures; error bars show SE of the means of three biological replicates; different letters denote significant differences using Duncan’s test at P<0.05).
Figure 3
Figure 3. Expression of PhHD-Zip in petunia flowers in response to ethylene and 1-MCP treatments.
“Ethylene” Flowers harvested at anthesis and treated continuously with ethylene (3 ppm), “1-MCP/Ethylene” Flowers harvested at anthesis and treated with 1-MCP (50 nL/L) for 4 hours before a continuous ethylene treatment. A. A representative gel image from semi-quantitative PCR of RNA isolated from corollas harvested at intervals. 26S RNA: the internal control. Samples were analyzed after 30 cycles for PhHD-Zip and after 24 cycles for 26S RNA. B. Relative expression levels of PhHD-Zip (quantification of the gel pictures; error bars show SE of the means of three biological replicates).
Figure 4
Figure 4. Expression of PhHD-Zip in petunia flower under abiotic stress.
Petunia flowers harvested at anthesis were placed in tubes with water, without water, with 50°C. A. A representative gel image from semi-quantitative PCR of RNA isolated from corollas harvested at intervals. 26S RNA: the internal control. Samples were analyzed after 30 cycles for PhHD-Zip, and after 24 cycles for 26S RNA. B. Relative expression levels of PhHD-Zip (quantification of the gel pictures; error bars show SE of the means of three biological replicates). C. Relative expression levels of PhHD-Zip determined using the same RNA samples, but using real-time quantitative PCR (error bars correspond to SE of the means of three biological replicates).
Figure 5
Figure 5. Effect of silencing PhHD-Zip on longevity of petunia flowers.
Photographs were taken on D0 and D8 of attached purple control flowers (WT), white (silenced) flowers of plants inoculated with the CHS/TRV reporter construct, and white (silenced) flowers of plants inoculated with the PhHD-Zip/CHS/TRV silencing construct.
Figure 6
Figure 6. Effect of silencing PhHD-Zip on ethylene production of petunia flowers.
Ethylene production was measured at D7 for wild type (WT) and for silenced (white) flowers (PhHD-Zip W). (Asterisks denote statistical difference using Duncan’s test at P<0.05; n = 5, error bars denote SE of the means of five biological replicates).
Figure 7
Figure 7. Expression of senescence-related genes in D7 petunia flowers.
Abundance of transcripts of genes associated with senescence were determined at D7 in purple control flowers (WT), in white flowers of plants inoculated with the CHS/TRV reporter construct (VW), and in white flowers of plant inoculated with the PhHD-Zip/CHS/TRV silencing construct. A. A representative gel image from semi-quantitative PCR of RNA isolated from corollas. 26S RNA: the internal control. Samples were analyzed after 33 cycles for ACS, after 30 cycles for other genes, and after 24 cycles for 26S RNA, respectively. B. Relative expression levels of different genes (quantification of the gel pictures; error bars show SE of the means of three biological replicates; different letters denote significant differences using Duncan’s test at P<0.05).
Figure 8
Figure 8. Effect of transgenic over-expression of PhHD-Zip on abundance of transcripts of PhHD-Zip and of ethylene biosynthesis genes in petunia corollas.
WT: wild type flower; #3, #7: two transgenic lines of 35S::PhHD-Zip. A. A representative gel image from semi-quantitative PCR of RNA isolated from harvested corollas. 26S RNA: the internal control. Samples were analyzed after 30 cycles for PhHD-Zip, ACO1 and ACO4; after 33 cycles for ACS; and after 24 cycles for 26S RNA. B. Relative expression level of PhHD-Zip and ethylene biosynthesis genes (quantification of the gel pictures; error bars show SE of the means of three biological replicates; different letters denote significant differences using Duncan’s test at P<0.05).
Figure 9
Figure 9. The model of PhHD-Zip regulating flower senescence.
Solid lines denote relationships supported by our study and those of other researchers; dashed lines denote hypothetical relationships.
See this image and copyright information in PMC

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Grants and funding

This work was partially supported by United States Department of Agriculture (USDA) CRIS project 5306-21000-019-00D, USDA Floriculture Initiative (5306-13210-001-02S) and National Key Technology Research and Development Program of the Ministry of Science and Technology of China (2013BAD19B04). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.