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Transcriptomic characterization of a synergistic genetic interaction during carpel margin meristem development in Arabidopsis thaliana.

Wynn AN, Rueschhoff EE, Franks RG - PLoS ONE (2011)

Bottom Line: Our in situ hybridization analyses indicate that many of these genes are preferentially expressed within the developing CMM.This study is the first step toward a detailed description of the transcriptional regulatory hierarchies that control the development of the CMM and ovule initiation.Understanding the regulatory hierarchy controlled by SEU and ANT will clarify the molecular mechanism of the functional redundancy of these two genes and illuminate the developmental and molecular events required for CMM development and ovule initiation.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
In flowering plants the gynoecium is the female reproductive structure. In Arabidopsis thaliana ovules initiate within the developing gynoecium from meristematic tissue located along the margins of the floral carpels. When fertilized the ovules will develop into seeds. SEUSS (SEU) and AINTEGUMENTA (ANT) encode transcriptional regulators that are critical for the proper formation of ovules from the carpel margin meristem (CMM). The synergistic loss of ovule initiation observed in the seu ant double mutant suggests that SEU and ANT share overlapping functions during CMM development. However the molecular mechanism underlying this synergistic interaction is unknown. Using the ATH1 transcriptomics platform we identified transcripts that were differentially expressed in seu ant double mutant relative to wild type and single mutant gynoecia. In particular we sought to identify transcripts whose expression was dependent on the coordinated activities of the SEU and ANT gene products. Our analysis identifies a diverse set of transcripts that display altered expression in the seu ant double mutant tissues. The analysis of overrepresented Gene Ontology classifications suggests a preponderance of transcriptional regulators including multiple members of the REPRODUCTIVE MERISTEMS (REM) and GROWTH-REGULATING FACTOR (GRF) families are mis-regulated in the seu ant gynoecia. Our in situ hybridization analyses indicate that many of these genes are preferentially expressed within the developing CMM. This study is the first step toward a detailed description of the transcriptional regulatory hierarchies that control the development of the CMM and ovule initiation. Understanding the regulatory hierarchy controlled by SEU and ANT will clarify the molecular mechanism of the functional redundancy of these two genes and illuminate the developmental and molecular events required for CMM development and ovule initiation.

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Spatial domains of the developing Arabidopsis gynoecium.A) Diagrammatic representation of the Arabidopsis gynoecial primordia at stage 6. Blue dotted arcs separate the lateral domains from the medial domain. The medial domain represents the fused margins of the two component carpels. The red dotted oval separates abaxial (outer) positions from adaxial (inner) positions. adm - adaxial margin; abm - abaxial margin; adv - adaxial valve; abv - abaxial valve, CMM - carpel margin meristem. B) Scanning electron micrograph of stage 6 gynoecial primordium. Medial plane is marked with a black line. C) False colored confocal cross section of a stage 8 gynoecium. Gynoecial domains have been colored with approximation. orange - carpel margin meristem/medial ridge; red - abaxial margin/replum; blue - adaxial valve; green - abaxial valve. D) Histological cross section of a stage 11 Arabidopsis gynoecium. Ovules (ov) are indicated.
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pone-0026231-g001: Spatial domains of the developing Arabidopsis gynoecium.A) Diagrammatic representation of the Arabidopsis gynoecial primordia at stage 6. Blue dotted arcs separate the lateral domains from the medial domain. The medial domain represents the fused margins of the two component carpels. The red dotted oval separates abaxial (outer) positions from adaxial (inner) positions. adm - adaxial margin; abm - abaxial margin; adv - adaxial valve; abv - abaxial valve, CMM - carpel margin meristem. B) Scanning electron micrograph of stage 6 gynoecial primordium. Medial plane is marked with a black line. C) False colored confocal cross section of a stage 8 gynoecium. Gynoecial domains have been colored with approximation. orange - carpel margin meristem/medial ridge; red - abaxial margin/replum; blue - adaxial valve; green - abaxial valve. D) Histological cross section of a stage 11 Arabidopsis gynoecium. Ovules (ov) are indicated.

Mentions: Gynoecial development in Arabidopsis initiates at stage 6 of floral development (floral stages according to Smyth; [7]). The gynoecial primordium is first morphologically recognizable as a dome or mound of cells, oval in cross section, that forms from the cells of the central most portion of floral meristem (i.e. floral whorl 4). During stage 6 the different spatial domains of the gynoecial tube are already discernable based on the differential expression of genes within the medial portion of the gynoecium versus the lateral domains, as well as along the inner to outer (adaxial to abaxial) axis [8], [9], [10] (Fig. 1A). During floral stages 6 and 7 the proliferation of cells along the perimeter of the gynoecial dome leads to the formation of a tube-shaped structure (Fig. 1B).


Transcriptomic characterization of a synergistic genetic interaction during carpel margin meristem development in Arabidopsis thaliana.

Wynn AN, Rueschhoff EE, Franks RG - PLoS ONE (2011)

Spatial domains of the developing Arabidopsis gynoecium.A) Diagrammatic representation of the Arabidopsis gynoecial primordia at stage 6. Blue dotted arcs separate the lateral domains from the medial domain. The medial domain represents the fused margins of the two component carpels. The red dotted oval separates abaxial (outer) positions from adaxial (inner) positions. adm - adaxial margin; abm - abaxial margin; adv - adaxial valve; abv - abaxial valve, CMM - carpel margin meristem. B) Scanning electron micrograph of stage 6 gynoecial primordium. Medial plane is marked with a black line. C) False colored confocal cross section of a stage 8 gynoecium. Gynoecial domains have been colored with approximation. orange - carpel margin meristem/medial ridge; red - abaxial margin/replum; blue - adaxial valve; green - abaxial valve. D) Histological cross section of a stage 11 Arabidopsis gynoecium. Ovules (ov) are indicated.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198736&req=5

pone-0026231-g001: Spatial domains of the developing Arabidopsis gynoecium.A) Diagrammatic representation of the Arabidopsis gynoecial primordia at stage 6. Blue dotted arcs separate the lateral domains from the medial domain. The medial domain represents the fused margins of the two component carpels. The red dotted oval separates abaxial (outer) positions from adaxial (inner) positions. adm - adaxial margin; abm - abaxial margin; adv - adaxial valve; abv - abaxial valve, CMM - carpel margin meristem. B) Scanning electron micrograph of stage 6 gynoecial primordium. Medial plane is marked with a black line. C) False colored confocal cross section of a stage 8 gynoecium. Gynoecial domains have been colored with approximation. orange - carpel margin meristem/medial ridge; red - abaxial margin/replum; blue - adaxial valve; green - abaxial valve. D) Histological cross section of a stage 11 Arabidopsis gynoecium. Ovules (ov) are indicated.
Mentions: Gynoecial development in Arabidopsis initiates at stage 6 of floral development (floral stages according to Smyth; [7]). The gynoecial primordium is first morphologically recognizable as a dome or mound of cells, oval in cross section, that forms from the cells of the central most portion of floral meristem (i.e. floral whorl 4). During stage 6 the different spatial domains of the gynoecial tube are already discernable based on the differential expression of genes within the medial portion of the gynoecium versus the lateral domains, as well as along the inner to outer (adaxial to abaxial) axis [8], [9], [10] (Fig. 1A). During floral stages 6 and 7 the proliferation of cells along the perimeter of the gynoecial dome leads to the formation of a tube-shaped structure (Fig. 1B).

Bottom Line: Our in situ hybridization analyses indicate that many of these genes are preferentially expressed within the developing CMM.This study is the first step toward a detailed description of the transcriptional regulatory hierarchies that control the development of the CMM and ovule initiation.Understanding the regulatory hierarchy controlled by SEU and ANT will clarify the molecular mechanism of the functional redundancy of these two genes and illuminate the developmental and molecular events required for CMM development and ovule initiation.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
In flowering plants the gynoecium is the female reproductive structure. In Arabidopsis thaliana ovules initiate within the developing gynoecium from meristematic tissue located along the margins of the floral carpels. When fertilized the ovules will develop into seeds. SEUSS (SEU) and AINTEGUMENTA (ANT) encode transcriptional regulators that are critical for the proper formation of ovules from the carpel margin meristem (CMM). The synergistic loss of ovule initiation observed in the seu ant double mutant suggests that SEU and ANT share overlapping functions during CMM development. However the molecular mechanism underlying this synergistic interaction is unknown. Using the ATH1 transcriptomics platform we identified transcripts that were differentially expressed in seu ant double mutant relative to wild type and single mutant gynoecia. In particular we sought to identify transcripts whose expression was dependent on the coordinated activities of the SEU and ANT gene products. Our analysis identifies a diverse set of transcripts that display altered expression in the seu ant double mutant tissues. The analysis of overrepresented Gene Ontology classifications suggests a preponderance of transcriptional regulators including multiple members of the REPRODUCTIVE MERISTEMS (REM) and GROWTH-REGULATING FACTOR (GRF) families are mis-regulated in the seu ant gynoecia. Our in situ hybridization analyses indicate that many of these genes are preferentially expressed within the developing CMM. This study is the first step toward a detailed description of the transcriptional regulatory hierarchies that control the development of the CMM and ovule initiation. Understanding the regulatory hierarchy controlled by SEU and ANT will clarify the molecular mechanism of the functional redundancy of these two genes and illuminate the developmental and molecular events required for CMM development and ovule initiation.

Show MeSH
Related in: MedlinePlus