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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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Results of in situ hybridization with AtGRF5 (AT3G13960) antisense probe.Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression. ov - ovule; b - boundary region between floral meristem and inflorescence meristem. Scale bars in all panels are 100 microns. All panels are Col-0 wild type tissue except as otherwise noted.
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pone-0026231-g009: Results of in situ hybridization with AtGRF5 (AT3G13960) antisense probe.Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression. ov - ovule; b - boundary region between floral meristem and inflorescence meristem. Scale bars in all panels are 100 microns. All panels are Col-0 wild type tissue except as otherwise noted.

Mentions: Expression of AtGRF5 (AT3G13960) has been previously reported as strongly expressed in actively growing tissues but only weakly detected in mature tissues suggesting a role in regulation of cellular proliferation [53]. Analysis of a GRF5:GUS reporter line revealed expression within the proximal half of the young leaf primordia, a domain with a high proportion of actively dividing cells, however a detailed description of the expression within the flower was not reported [54]. We detected expression of AtGRF5 (AT3G13960) in stage 1 floral primordia, and in a line that marks the boundary between later stage floral primordia and the inflorescence meristem (Fig. 9A). Expression was not detected in floral stage 2 meristems, nor in the inflorescence meristem. Expression was again detected in stage 3 floral meristems in the sepal primordia and then in stamen and petal primordia as they arise during stage 5 (data not shown). Within the gynoecium expression is detected during stage 6 and 7 in the marginal portion of the gynoecium, most strongly detected in abaxial portions of the margin (Fig. 9C and D). During stage 8 AtGRF5 is detected in a somewhat punctate pattern throughout the gynoecial primordia, but with highest expression within the medial portions (Fig. 9E). GRF5 is also detected in the ovule primordia are they arise (Fig. 9G) and in subepidermal layers through at least stage 11 (Fig. 9H). Expression of AtGRF5 in the seu ant double mutant tissue appeared to be slightly reduced in stage 1 and stage 3 floral meristems (Fig. 9B) and then strongly reduced within the later stage gynoecia (Fig. 9F)


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

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

Results of in situ hybridization with AtGRF5 (AT3G13960) antisense probe.Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression. ov - ovule; b - boundary region between floral meristem and inflorescence meristem. Scale bars in all panels are 100 microns. All panels are Col-0 wild type tissue except as otherwise noted.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0026231-g009: Results of in situ hybridization with AtGRF5 (AT3G13960) antisense probe.Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression. ov - ovule; b - boundary region between floral meristem and inflorescence meristem. Scale bars in all panels are 100 microns. All panels are Col-0 wild type tissue except as otherwise noted.
Mentions: Expression of AtGRF5 (AT3G13960) has been previously reported as strongly expressed in actively growing tissues but only weakly detected in mature tissues suggesting a role in regulation of cellular proliferation [53]. Analysis of a GRF5:GUS reporter line revealed expression within the proximal half of the young leaf primordia, a domain with a high proportion of actively dividing cells, however a detailed description of the expression within the flower was not reported [54]. We detected expression of AtGRF5 (AT3G13960) in stage 1 floral primordia, and in a line that marks the boundary between later stage floral primordia and the inflorescence meristem (Fig. 9A). Expression was not detected in floral stage 2 meristems, nor in the inflorescence meristem. Expression was again detected in stage 3 floral meristems in the sepal primordia and then in stamen and petal primordia as they arise during stage 5 (data not shown). Within the gynoecium expression is detected during stage 6 and 7 in the marginal portion of the gynoecium, most strongly detected in abaxial portions of the margin (Fig. 9C and D). During stage 8 AtGRF5 is detected in a somewhat punctate pattern throughout the gynoecial primordia, but with highest expression within the medial portions (Fig. 9E). GRF5 is also detected in the ovule primordia are they arise (Fig. 9G) and in subepidermal layers through at least stage 11 (Fig. 9H). Expression of AtGRF5 in the seu ant double mutant tissue appeared to be slightly reduced in stage 1 and stage 3 floral meristems (Fig. 9B) and then strongly reduced within the later stage gynoecia (Fig. 9F)

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