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Low temperature-induced DNA hypermethylation attenuates expression of RhAG, an AGAMOUS homolog, and increases petal number in rose (Rosa hybrida).

Ma N, Chen W, Fan T, Tian Y, Zhang S, Zeng D, Li Y - BMC Plant Biol. (2015)

Bottom Line: Quantitative RT-PCR analysis revealed that the expression pattern of RhAG, a rose homolog of the Arabidopsis thaliana AGAMOUS C-function gene, is associated with low temperature regulated flower development.Our results provide highlights in the role of RhAG gene in petal number determination and add a new layer of complexity in the regulation of floral organ development.We propose that RhAG plays an essential role in rose flower patterning by regulating petal development, and that low temperatures increase petal number, at least in part, by suppressing RhAG expression via enhancing DNA CHH hypermethylation of the RhAG promoter.

View Article: PubMed Central - PubMed

Affiliation: Department of Ornamental Horticulture, China Agricultural University, Beijing, 100193, China. ma_nan@cau.edu.cn.

ABSTRACT

Background: Flower development is central to angiosperm reproduction and is regulated by a broad range of endogenous and exogenous stimuli. It has been well documented that ambient temperature plays a key role in controlling flowering time; however, the mechanisms by which temperature regulates floral organ differentiation remain largely unknown.

Results: In this study, we show that low temperature treatment significantly increases petal number in rose (Rosa hybrida) through the promotion of stamen petaloidy. Quantitative RT-PCR analysis revealed that the expression pattern of RhAG, a rose homolog of the Arabidopsis thaliana AGAMOUS C-function gene, is associated with low temperature regulated flower development. Silencing of RhAG mimicked the impact of low temperature treatments on petal development by significantly increasing petal number through an increased production of petaloid stamens. In situ hybridization studies further revealed that low temperature restricts its spatial expression area. Analysis of DNA methylation level showed that low temperature treatment enhances the methylation level of the RhAG promoter, and a specific promoter region that was hypermethylated at CHH loci under low temperature conditions, was identified by bisulfite sequencing. This suggests that epigenetic DNA methylation contributes to the ambient temperature modulation of RhAG expression.

Discussion: Our results provide highlights in the role of RhAG gene in petal number determination and add a new layer of complexity in the regulation of floral organ development.

Conclusions: We propose that RhAG plays an essential role in rose flower patterning by regulating petal development, and that low temperatures increase petal number, at least in part, by suppressing RhAG expression via enhancing DNA CHH hypermethylation of the RhAG promoter.

No MeSH data available.


Related in: MedlinePlus

Expression pattern of RhAG in response to low temperatures during flower development. Expression of RhAG was monitored by quantitative RT-PCR. Two-year-old rose plants were cultivated at 25/15 °C (black column) or 15/5 °C (white column). Flowers were collected at stage 1 to stage 4. RhTCTP was used as an internal control for all the tested genes. The expression level of RhAG at stage 1 grown at 25/15 °C was defined as 1.0. Values are means ± SD (n = 3). Asterisks indicate significant differences calculated using the t test (**p < 0.01; *p < 0.05)
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Fig2: Expression pattern of RhAG in response to low temperatures during flower development. Expression of RhAG was monitored by quantitative RT-PCR. Two-year-old rose plants were cultivated at 25/15 °C (black column) or 15/5 °C (white column). Flowers were collected at stage 1 to stage 4. RhTCTP was used as an internal control for all the tested genes. The expression level of RhAG at stage 1 grown at 25/15 °C was defined as 1.0. Values are means ± SD (n = 3). Asterisks indicate significant differences calculated using the t test (**p < 0.01; *p < 0.05)

Mentions: It has been reported that AG gene plays a dual role in specifying reproductive organ identity and floral meristem determinacy [9], as well as being involved in the determination of petal number [23]. To understand whether AG gene is associated with the low-temperature-regulated petal doubling in rose, we analyzed the effect of low temperature on the expression of RhAG, a rose homolog of AG [23], during rose flower development through quantitative RT-PCR. Results showed that the expression level of RhAG was low at stages 1 and 2, when the sepal and petal primordia form, before rising markedly at stages 3 and 4, when the stamen and carpel primordia form (Fig. 2). This expression pattern correlates with its classification as a C-class gene. Furthermore, low temperature exposure significantly decreased its expression level at the stamen and carpel formation stages, suggesting that RhAG may be involved in the low temperature induced homeotic conversion of stamens into petals.Fig. 2


Low temperature-induced DNA hypermethylation attenuates expression of RhAG, an AGAMOUS homolog, and increases petal number in rose (Rosa hybrida).

Ma N, Chen W, Fan T, Tian Y, Zhang S, Zeng D, Li Y - BMC Plant Biol. (2015)

Expression pattern of RhAG in response to low temperatures during flower development. Expression of RhAG was monitored by quantitative RT-PCR. Two-year-old rose plants were cultivated at 25/15 °C (black column) or 15/5 °C (white column). Flowers were collected at stage 1 to stage 4. RhTCTP was used as an internal control for all the tested genes. The expression level of RhAG at stage 1 grown at 25/15 °C was defined as 1.0. Values are means ± SD (n = 3). Asterisks indicate significant differences calculated using the t test (**p < 0.01; *p < 0.05)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4595006&req=5

Fig2: Expression pattern of RhAG in response to low temperatures during flower development. Expression of RhAG was monitored by quantitative RT-PCR. Two-year-old rose plants were cultivated at 25/15 °C (black column) or 15/5 °C (white column). Flowers were collected at stage 1 to stage 4. RhTCTP was used as an internal control for all the tested genes. The expression level of RhAG at stage 1 grown at 25/15 °C was defined as 1.0. Values are means ± SD (n = 3). Asterisks indicate significant differences calculated using the t test (**p < 0.01; *p < 0.05)
Mentions: It has been reported that AG gene plays a dual role in specifying reproductive organ identity and floral meristem determinacy [9], as well as being involved in the determination of petal number [23]. To understand whether AG gene is associated with the low-temperature-regulated petal doubling in rose, we analyzed the effect of low temperature on the expression of RhAG, a rose homolog of AG [23], during rose flower development through quantitative RT-PCR. Results showed that the expression level of RhAG was low at stages 1 and 2, when the sepal and petal primordia form, before rising markedly at stages 3 and 4, when the stamen and carpel primordia form (Fig. 2). This expression pattern correlates with its classification as a C-class gene. Furthermore, low temperature exposure significantly decreased its expression level at the stamen and carpel formation stages, suggesting that RhAG may be involved in the low temperature induced homeotic conversion of stamens into petals.Fig. 2

Bottom Line: Quantitative RT-PCR analysis revealed that the expression pattern of RhAG, a rose homolog of the Arabidopsis thaliana AGAMOUS C-function gene, is associated with low temperature regulated flower development.Our results provide highlights in the role of RhAG gene in petal number determination and add a new layer of complexity in the regulation of floral organ development.We propose that RhAG plays an essential role in rose flower patterning by regulating petal development, and that low temperatures increase petal number, at least in part, by suppressing RhAG expression via enhancing DNA CHH hypermethylation of the RhAG promoter.

View Article: PubMed Central - PubMed

Affiliation: Department of Ornamental Horticulture, China Agricultural University, Beijing, 100193, China. ma_nan@cau.edu.cn.

ABSTRACT

Background: Flower development is central to angiosperm reproduction and is regulated by a broad range of endogenous and exogenous stimuli. It has been well documented that ambient temperature plays a key role in controlling flowering time; however, the mechanisms by which temperature regulates floral organ differentiation remain largely unknown.

Results: In this study, we show that low temperature treatment significantly increases petal number in rose (Rosa hybrida) through the promotion of stamen petaloidy. Quantitative RT-PCR analysis revealed that the expression pattern of RhAG, a rose homolog of the Arabidopsis thaliana AGAMOUS C-function gene, is associated with low temperature regulated flower development. Silencing of RhAG mimicked the impact of low temperature treatments on petal development by significantly increasing petal number through an increased production of petaloid stamens. In situ hybridization studies further revealed that low temperature restricts its spatial expression area. Analysis of DNA methylation level showed that low temperature treatment enhances the methylation level of the RhAG promoter, and a specific promoter region that was hypermethylated at CHH loci under low temperature conditions, was identified by bisulfite sequencing. This suggests that epigenetic DNA methylation contributes to the ambient temperature modulation of RhAG expression.

Discussion: Our results provide highlights in the role of RhAG gene in petal number determination and add a new layer of complexity in the regulation of floral organ development.

Conclusions: We propose that RhAG plays an essential role in rose flower patterning by regulating petal development, and that low temperatures increase petal number, at least in part, by suppressing RhAG expression via enhancing DNA CHH hypermethylation of the RhAG promoter.

No MeSH data available.


Related in: MedlinePlus