The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis

Abstract Background Nuclear endosperm development is a common mechanism among Angiosperms, including Arabidopsis. During nuclear development, the endosperm nuclei divide rapidly after fertilization without cytokinesis to enter the syncytial phase, which is then followed by the cellularized phase. Th...

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Main Authors: Tobias Hoffmann, Xiuling Shi, Chuan-Yu Hsu, Aakilah Brown, Quintera Knight, La’ Shyra Courtney, Ruqiyah J. Mukarram, Dongfang Wang
Format: Article
Language:English
Published: BMC 2022-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-021-03399-3
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author Tobias Hoffmann
Xiuling Shi
Chuan-Yu Hsu
Aakilah Brown
Quintera Knight
La’ Shyra Courtney
Ruqiyah J. Mukarram
Dongfang Wang
author_facet Tobias Hoffmann
Xiuling Shi
Chuan-Yu Hsu
Aakilah Brown
Quintera Knight
La’ Shyra Courtney
Ruqiyah J. Mukarram
Dongfang Wang
author_sort Tobias Hoffmann
collection DOAJ
description Abstract Background Nuclear endosperm development is a common mechanism among Angiosperms, including Arabidopsis. During nuclear development, the endosperm nuclei divide rapidly after fertilization without cytokinesis to enter the syncytial phase, which is then followed by the cellularized phase. The endosperm can be divided into three spatial domains with distinct functions: the micropylar, peripheral, and chalazal domains. Previously, we identified two putative small invertase inhibitors, InvINH1 and InvINH2, that are specifically expressed in the micropylar region of the syncytial endosperm. In addition, ectopically expressing InvINH1 in the cellularized endosperm led to a reduction in embryo growth rate. However, it is not clear what are the upstream regulators responsible for the specific expression of InvINHs in the syncytial endosperm. Results Using protoplast transient expression system, we discovered that a group of type I MADS box transcription factors can form dimers to activate InvINH1 promoter. Promoter deletion assays carried out in the protoplast system revealed the presence of an enhancer region in InvINH1 promoter, which contains several consensus cis-elements for the MADS box proteins. Using promoter deletion assay in planta, we further demonstrated that this enhancer region is required for InvINH1 expression in the syncytial endosperm. One of the MADS box genes, AGL62, is a key transcription factor required for syncytial endosperm development. Using promoter-GFP reporter assay, we demonstrated that InvINH1 and InvINH2 are not expressed in agl62 mutant seeds. Collectively, our data supports the role of AGL62 and other type I MADS box genes as the upstream activators of InvINHs expression in the syncytial endosperm. Conclusions Our findings revealed several type I MADS box genes that are responsible for activating InvINH1 in the syncytial endosperm, which in turn regulates embryo growth rate during early stage of seed development.
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spelling doaj.art-c0fe5a9ee7dc414f8a44d34028f9b57c2022-12-21T17:49:29ZengBMCBMC Plant Biology1471-22292022-01-0122111310.1186/s12870-021-03399-3The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in ArabidopsisTobias Hoffmann0Xiuling Shi1Chuan-Yu Hsu2Aakilah Brown3Quintera Knight4La’ Shyra Courtney5Ruqiyah J. Mukarram6Dongfang Wang7Biology Department, Spelman CollegeBiology Department, Spelman CollegeInstitute for Genomics, Biocomputing and Biotechnology, Mississippi State UniversityBiology Department, Spelman CollegeBiology Department, Spelman CollegeBiology Department, Spelman CollegeBiology Department, Spelman CollegeBiology Department, Spelman CollegeAbstract Background Nuclear endosperm development is a common mechanism among Angiosperms, including Arabidopsis. During nuclear development, the endosperm nuclei divide rapidly after fertilization without cytokinesis to enter the syncytial phase, which is then followed by the cellularized phase. The endosperm can be divided into three spatial domains with distinct functions: the micropylar, peripheral, and chalazal domains. Previously, we identified two putative small invertase inhibitors, InvINH1 and InvINH2, that are specifically expressed in the micropylar region of the syncytial endosperm. In addition, ectopically expressing InvINH1 in the cellularized endosperm led to a reduction in embryo growth rate. However, it is not clear what are the upstream regulators responsible for the specific expression of InvINHs in the syncytial endosperm. Results Using protoplast transient expression system, we discovered that a group of type I MADS box transcription factors can form dimers to activate InvINH1 promoter. Promoter deletion assays carried out in the protoplast system revealed the presence of an enhancer region in InvINH1 promoter, which contains several consensus cis-elements for the MADS box proteins. Using promoter deletion assay in planta, we further demonstrated that this enhancer region is required for InvINH1 expression in the syncytial endosperm. One of the MADS box genes, AGL62, is a key transcription factor required for syncytial endosperm development. Using promoter-GFP reporter assay, we demonstrated that InvINH1 and InvINH2 are not expressed in agl62 mutant seeds. Collectively, our data supports the role of AGL62 and other type I MADS box genes as the upstream activators of InvINHs expression in the syncytial endosperm. Conclusions Our findings revealed several type I MADS box genes that are responsible for activating InvINH1 in the syncytial endosperm, which in turn regulates embryo growth rate during early stage of seed development.https://doi.org/10.1186/s12870-021-03399-3MADS-boxInvertase inhibitorEndospermPRC2Seed development
spellingShingle Tobias Hoffmann
Xiuling Shi
Chuan-Yu Hsu
Aakilah Brown
Quintera Knight
La’ Shyra Courtney
Ruqiyah J. Mukarram
Dongfang Wang
The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
BMC Plant Biology
MADS-box
Invertase inhibitor
Endosperm
PRC2
Seed development
title The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
title_full The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
title_fullStr The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
title_full_unstemmed The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
title_short The identification of type I MADS box genes as the upstream activators of an endosperm-specific invertase inhibitor in Arabidopsis
title_sort identification of type i mads box genes as the upstream activators of an endosperm specific invertase inhibitor in arabidopsis
topic MADS-box
Invertase inhibitor
Endosperm
PRC2
Seed development
url https://doi.org/10.1186/s12870-021-03399-3
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