Limits...
Interaction between two timing microRNAs controls trichome distribution in Arabidopsis.

Xue XY, Zhao B, Chao LM, Chen DY, Cui WR, Mao YB, Wang LJ, Chen XY - PLoS Genet. (2014)

Bottom Line: Reduced LOM abundance by overexpression of miR171 led to decreased trichome density on stems and floral organs, and conversely, constitutive expression of the miR171-resistant LOM (rLOM) genes promoted trichome production, indicating that LOMs enhance trichome initiation at reproductive stage.Importantly, other growth and developmental events, such as flowering, are also modulated by LOM-SPL interaction, indicating a broad effect of the LOM-SPL interplay.Our data uncover an antagonistic interplay between the two timing miRNAs in controlling plant growth, phase transition and morphogenesis through direct interaction of their targets.

View Article: PubMed Central - PubMed

Affiliation: National Key Laboratory of Plant Molecular Genetics and National Plant Gene Research Center, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China.

ABSTRACT
The miR156-targeted squamosa promoter binding protein like (SPL) transcription factors function as an endogenous age cue in regulating plant phase transition and phase-dependent morphogenesis, but the control of SPL output remains poorly understood. In Arabidopsis thaliana the spatial pattern of trichome is a hallmark of phase transition and governed by SPLs. Here, by dissecting the regulatory network controlling trichome formation on stem, we show that the miR171-targeted lost meristems 1 (LOM1), LOM2 and LOM3, encoding GRAS family members previously known to maintain meristem cell polarity, are involved in regulating the SPL activity. Reduced LOM abundance by overexpression of miR171 led to decreased trichome density on stems and floral organs, and conversely, constitutive expression of the miR171-resistant LOM (rLOM) genes promoted trichome production, indicating that LOMs enhance trichome initiation at reproductive stage. Genetic analysis demonstrated LOMs shaping trichome distribution is dependent on SPLs, which positively regulate trichome repressor genes TRICHOMELESS 1 (TCL1) and TRIPTYCHON (TRY). Physical interaction between the N-terminus of LOMs and SPLs underpins the repression of SPL activity. Importantly, other growth and developmental events, such as flowering, are also modulated by LOM-SPL interaction, indicating a broad effect of the LOM-SPL interplay. Furthermore, we provide evidence that MIR171 gene expression is regulated by its targeted LOMs, forming a homeostatic feedback loop. Our data uncover an antagonistic interplay between the two timing miRNAs in controlling plant growth, phase transition and morphogenesis through direct interaction of their targets.

Show MeSH

Related in: MedlinePlus

Overexpression of N-terminal of LOM1 in nucleus triggers a flowering delay.(A) The number of leaves at flowering of wild-type, lomt mutant and LUC-rLOM1OE plants under long-day condition. Data are given as mean s.d (n>61), and analyzed by t test. **P<0.01. (B) qRT-PCR analysis of expression of SOC1 in 7-day-old long-day-grown seedlings. SOC1 was repressed in 35S::MIR156F and increased in 35S::MIM156 as reported [2]. (C and D) View of 10-day-old wild-type (C) and 35S::nLOM1-NLS-YFP (D) plants. 35S::nLOM1-NLS-YFP plants look normal. Scale bars, 1 cm. (E) 35S::nLOM1-NLS-YFP delayed flowering very significantly under long-day condition. The number of days to flowering was counted when the floral buds were visible. Data are given as mean s.d. (n = 18) and analyzed by t test, **P<0.01. (F) Expression of SOC1. SOC1 was down-regulated in 35S::nLOM1-NLS-YFP plants, consistent with delayed flowering. (G) Trichome numbers of wild-type and 35S::nLOM1-NLS-YFP plants. The y axis indicates the total trichome number on main stems. Data are given as mean s.d. (n = 32) and analyzed by t test, **P<0.01. (H) Subcellular localization of nLOM1-YFP and nLOM1-NLS-YFP in leaf trichome (left panel) and leaf vein (right panel). Scale bars, 100 µm.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3974651&req=5

pgen-1004266-g005: Overexpression of N-terminal of LOM1 in nucleus triggers a flowering delay.(A) The number of leaves at flowering of wild-type, lomt mutant and LUC-rLOM1OE plants under long-day condition. Data are given as mean s.d (n>61), and analyzed by t test. **P<0.01. (B) qRT-PCR analysis of expression of SOC1 in 7-day-old long-day-grown seedlings. SOC1 was repressed in 35S::MIR156F and increased in 35S::MIM156 as reported [2]. (C and D) View of 10-day-old wild-type (C) and 35S::nLOM1-NLS-YFP (D) plants. 35S::nLOM1-NLS-YFP plants look normal. Scale bars, 1 cm. (E) 35S::nLOM1-NLS-YFP delayed flowering very significantly under long-day condition. The number of days to flowering was counted when the floral buds were visible. Data are given as mean s.d. (n = 18) and analyzed by t test, **P<0.01. (F) Expression of SOC1. SOC1 was down-regulated in 35S::nLOM1-NLS-YFP plants, consistent with delayed flowering. (G) Trichome numbers of wild-type and 35S::nLOM1-NLS-YFP plants. The y axis indicates the total trichome number on main stems. Data are given as mean s.d. (n = 32) and analyzed by t test, **P<0.01. (H) Subcellular localization of nLOM1-YFP and nLOM1-NLS-YFP in leaf trichome (left panel) and leaf vein (right panel). Scale bars, 100 µm.

Mentions: To substantiate the potentially wide implication of LOM-SPL interaction, we examined the effect of LOMs on the flowering pathway. In long-day conditions, LOM1 overexpression delayed flowering time (Figure 5A and Figure S3B–S3E) and consistently down-regulated the expression of the MADS-box gene, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), which was under the direct control of miR156-tageted SPLs [2]; by contrast, SOC1 was up-regulated in lomt mutant along with earlier flowering (Figure 5A and 5B). As the N-terminal domain of LOM1 (nLOM1) was responsible for interaction with SPL9 (Figure 4K), we overexpressed nLOM1 fused to the nuclear localization signal (NLS). The 35S::nLOM1-NLS-YFP plants showed normal development (Figures 5C and 5D) except for late flowering and more trichomes on stems (Figures 5E–5G). A drastic drop of the SOC1 transcript levels (Figure 5F) was accompanied by severe delay of flowering (Figure 5E) in 35S::nLOM1-NLS-YFP plants. It is the same to rLOM1OE plants that nLOM1-NLS-YFP triggered more stem trichomes (Figure 5G). However, remarkable flowering delay and ectopic trichomes were not observed in 35S::nLOM1-YFP plants, in which the NLS was removed and the nLOM1-YFP signal was diffused in cytoplasm (Figure 5H). Because nLOM1 does not contain the DNA binding domain, these data further support that it is the LOM-SPL interaction that caused, or at least contributed to, the flowering delay and trichome increase.


Interaction between two timing microRNAs controls trichome distribution in Arabidopsis.

Xue XY, Zhao B, Chao LM, Chen DY, Cui WR, Mao YB, Wang LJ, Chen XY - PLoS Genet. (2014)

Overexpression of N-terminal of LOM1 in nucleus triggers a flowering delay.(A) The number of leaves at flowering of wild-type, lomt mutant and LUC-rLOM1OE plants under long-day condition. Data are given as mean s.d (n>61), and analyzed by t test. **P<0.01. (B) qRT-PCR analysis of expression of SOC1 in 7-day-old long-day-grown seedlings. SOC1 was repressed in 35S::MIR156F and increased in 35S::MIM156 as reported [2]. (C and D) View of 10-day-old wild-type (C) and 35S::nLOM1-NLS-YFP (D) plants. 35S::nLOM1-NLS-YFP plants look normal. Scale bars, 1 cm. (E) 35S::nLOM1-NLS-YFP delayed flowering very significantly under long-day condition. The number of days to flowering was counted when the floral buds were visible. Data are given as mean s.d. (n = 18) and analyzed by t test, **P<0.01. (F) Expression of SOC1. SOC1 was down-regulated in 35S::nLOM1-NLS-YFP plants, consistent with delayed flowering. (G) Trichome numbers of wild-type and 35S::nLOM1-NLS-YFP plants. The y axis indicates the total trichome number on main stems. Data are given as mean s.d. (n = 32) and analyzed by t test, **P<0.01. (H) Subcellular localization of nLOM1-YFP and nLOM1-NLS-YFP in leaf trichome (left panel) and leaf vein (right panel). Scale bars, 100 µm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3974651&req=5

pgen-1004266-g005: Overexpression of N-terminal of LOM1 in nucleus triggers a flowering delay.(A) The number of leaves at flowering of wild-type, lomt mutant and LUC-rLOM1OE plants under long-day condition. Data are given as mean s.d (n>61), and analyzed by t test. **P<0.01. (B) qRT-PCR analysis of expression of SOC1 in 7-day-old long-day-grown seedlings. SOC1 was repressed in 35S::MIR156F and increased in 35S::MIM156 as reported [2]. (C and D) View of 10-day-old wild-type (C) and 35S::nLOM1-NLS-YFP (D) plants. 35S::nLOM1-NLS-YFP plants look normal. Scale bars, 1 cm. (E) 35S::nLOM1-NLS-YFP delayed flowering very significantly under long-day condition. The number of days to flowering was counted when the floral buds were visible. Data are given as mean s.d. (n = 18) and analyzed by t test, **P<0.01. (F) Expression of SOC1. SOC1 was down-regulated in 35S::nLOM1-NLS-YFP plants, consistent with delayed flowering. (G) Trichome numbers of wild-type and 35S::nLOM1-NLS-YFP plants. The y axis indicates the total trichome number on main stems. Data are given as mean s.d. (n = 32) and analyzed by t test, **P<0.01. (H) Subcellular localization of nLOM1-YFP and nLOM1-NLS-YFP in leaf trichome (left panel) and leaf vein (right panel). Scale bars, 100 µm.
Mentions: To substantiate the potentially wide implication of LOM-SPL interaction, we examined the effect of LOMs on the flowering pathway. In long-day conditions, LOM1 overexpression delayed flowering time (Figure 5A and Figure S3B–S3E) and consistently down-regulated the expression of the MADS-box gene, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), which was under the direct control of miR156-tageted SPLs [2]; by contrast, SOC1 was up-regulated in lomt mutant along with earlier flowering (Figure 5A and 5B). As the N-terminal domain of LOM1 (nLOM1) was responsible for interaction with SPL9 (Figure 4K), we overexpressed nLOM1 fused to the nuclear localization signal (NLS). The 35S::nLOM1-NLS-YFP plants showed normal development (Figures 5C and 5D) except for late flowering and more trichomes on stems (Figures 5E–5G). A drastic drop of the SOC1 transcript levels (Figure 5F) was accompanied by severe delay of flowering (Figure 5E) in 35S::nLOM1-NLS-YFP plants. It is the same to rLOM1OE plants that nLOM1-NLS-YFP triggered more stem trichomes (Figure 5G). However, remarkable flowering delay and ectopic trichomes were not observed in 35S::nLOM1-YFP plants, in which the NLS was removed and the nLOM1-YFP signal was diffused in cytoplasm (Figure 5H). Because nLOM1 does not contain the DNA binding domain, these data further support that it is the LOM-SPL interaction that caused, or at least contributed to, the flowering delay and trichome increase.

Bottom Line: Reduced LOM abundance by overexpression of miR171 led to decreased trichome density on stems and floral organs, and conversely, constitutive expression of the miR171-resistant LOM (rLOM) genes promoted trichome production, indicating that LOMs enhance trichome initiation at reproductive stage.Importantly, other growth and developmental events, such as flowering, are also modulated by LOM-SPL interaction, indicating a broad effect of the LOM-SPL interplay.Our data uncover an antagonistic interplay between the two timing miRNAs in controlling plant growth, phase transition and morphogenesis through direct interaction of their targets.

View Article: PubMed Central - PubMed

Affiliation: National Key Laboratory of Plant Molecular Genetics and National Plant Gene Research Center, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China; University of Chinese Academy of Sciences, Beijing, China.

ABSTRACT
The miR156-targeted squamosa promoter binding protein like (SPL) transcription factors function as an endogenous age cue in regulating plant phase transition and phase-dependent morphogenesis, but the control of SPL output remains poorly understood. In Arabidopsis thaliana the spatial pattern of trichome is a hallmark of phase transition and governed by SPLs. Here, by dissecting the regulatory network controlling trichome formation on stem, we show that the miR171-targeted lost meristems 1 (LOM1), LOM2 and LOM3, encoding GRAS family members previously known to maintain meristem cell polarity, are involved in regulating the SPL activity. Reduced LOM abundance by overexpression of miR171 led to decreased trichome density on stems and floral organs, and conversely, constitutive expression of the miR171-resistant LOM (rLOM) genes promoted trichome production, indicating that LOMs enhance trichome initiation at reproductive stage. Genetic analysis demonstrated LOMs shaping trichome distribution is dependent on SPLs, which positively regulate trichome repressor genes TRICHOMELESS 1 (TCL1) and TRIPTYCHON (TRY). Physical interaction between the N-terminus of LOMs and SPLs underpins the repression of SPL activity. Importantly, other growth and developmental events, such as flowering, are also modulated by LOM-SPL interaction, indicating a broad effect of the LOM-SPL interplay. Furthermore, we provide evidence that MIR171 gene expression is regulated by its targeted LOMs, forming a homeostatic feedback loop. Our data uncover an antagonistic interplay between the two timing miRNAs in controlling plant growth, phase transition and morphogenesis through direct interaction of their targets.

Show MeSH
Related in: MedlinePlus