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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 At3g53310 (REM16) antisense probe.Results of in situ hybridization with At3g53310 (REM16) antisense probe (A–K) or with sense strand control probe (L). Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression; ov - ovule; as, archesporial precursors; tp, tapetum. All scale bars are 100 microns. All panels are Col-0 wild type tissue unless otherwise indicated.
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pone-0026231-g002: Results of in situ hybridization with At3g53310 (REM16) antisense probe.Results of in situ hybridization with At3g53310 (REM16) antisense probe (A–K) or with sense strand control probe (L). Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression; ov - ovule; as, archesporial precursors; tp, tapetum. All scale bars are 100 microns. All panels are Col-0 wild type tissue unless otherwise indicated.

Mentions: At3G53310 (REM16) was previously reported in stamen primordia at stage 4 and carpel primordia at stage 6 [43]. We detected expression of At3G53310 (REM16) weakly in the stage 1–4 floral primordia, chiefly in L1 layer and in peripheral portions of the floral meristem that will give rise to the sepal primordia (Fig. 2A). Expression is also detected in stamen and petal primordia as they arise at stage 4 and 5 (data not shown). Expression in the gynoecium is difficult to detect before early stage 7 when expression is observed in the abaxial portions of the medial gynoecial domain (Fig. 2B). Expression during stage 8 is seen in the medial domains and begins to be detected in both adaxial and abaxial portions. However expression is not observed in the L1 layer (Fig. 2C and G). The stage 8 medial domain expression appeared reduced in the seu single and the seu ant double mutant relative to wild type (Figs. 2D, E, F). In wild type tissue expression continues to be detected in the ovule primordia throughout stages 9 through 11 and is confined to subepidermal cell layers (Fig. 2I). During stage 7 and 8 expression in the stamens is detected mostly in the subepidermal cells from which archesporial and tapetal cells are derived (Fig. 2 C, H). During stage 9 expression is most strongly detected in the tapetal cells (Fig. 2 H). Expression within the stamen primordia also appeared to be reduced in the seu mutant tissues (Fig. 2D, K). Hybridizations with sense strand probes gave very little background staining (Fig. 2L).


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 At3g53310 (REM16) antisense probe.Results of in situ hybridization with At3g53310 (REM16) antisense probe (A–K) or with sense strand control probe (L). Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression; ov - ovule; as, archesporial precursors; tp, tapetum. All scale bars are 100 microns. All panels are Col-0 wild type tissue unless otherwise indicated.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0026231-g002: Results of in situ hybridization with At3g53310 (REM16) antisense probe.Results of in situ hybridization with At3g53310 (REM16) antisense probe (A–K) or with sense strand control probe (L). Numbers indicate floral stages. All panels show transverse (cross sectional) tissue orientation. Arrowheads indicate medial domain expression; ov - ovule; as, archesporial precursors; tp, tapetum. All scale bars are 100 microns. All panels are Col-0 wild type tissue unless otherwise indicated.
Mentions: At3G53310 (REM16) was previously reported in stamen primordia at stage 4 and carpel primordia at stage 6 [43]. We detected expression of At3G53310 (REM16) weakly in the stage 1–4 floral primordia, chiefly in L1 layer and in peripheral portions of the floral meristem that will give rise to the sepal primordia (Fig. 2A). Expression is also detected in stamen and petal primordia as they arise at stage 4 and 5 (data not shown). Expression in the gynoecium is difficult to detect before early stage 7 when expression is observed in the abaxial portions of the medial gynoecial domain (Fig. 2B). Expression during stage 8 is seen in the medial domains and begins to be detected in both adaxial and abaxial portions. However expression is not observed in the L1 layer (Fig. 2C and G). The stage 8 medial domain expression appeared reduced in the seu single and the seu ant double mutant relative to wild type (Figs. 2D, E, F). In wild type tissue expression continues to be detected in the ovule primordia throughout stages 9 through 11 and is confined to subepidermal cell layers (Fig. 2I). During stage 7 and 8 expression in the stamens is detected mostly in the subepidermal cells from which archesporial and tapetal cells are derived (Fig. 2 C, H). During stage 9 expression is most strongly detected in the tapetal cells (Fig. 2 H). Expression within the stamen primordia also appeared to be reduced in the seu mutant tissues (Fig. 2D, K). Hybridizations with sense strand probes gave very little background staining (Fig. 2L).

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