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An ARID domain-containing protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana.

Zheng B, He H, Zheng Y, Wu W, McCormick S - PLoS Genet. (2014)

Bottom Line: In plants, each male meiotic product undergoes mitosis, and then one of the resulting cells divides again, yielding a three-celled pollen grain comprised of a vegetative cell and two sperm cells.An arid1 mutant and antisense arid1 plants had an increased incidence of pollen with only a single sperm-like cell and exhibited reduced fertility as well as reduced expression of DUO1.In vitro and in vivo evidence showed that ARID1 binds to the DUO1 promoter.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Engineering, Collaborative Innovation Center for Genetics and Development, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China; Plant Gene Expression Center, USDA/ARS and Dept. of Plant and Microbial Biology, UC-Berkeley, Albany, California, United States of America.

ABSTRACT
In plants, each male meiotic product undergoes mitosis, and then one of the resulting cells divides again, yielding a three-celled pollen grain comprised of a vegetative cell and two sperm cells. Several genes have been found to act in this process, and DUO1 (DUO POLLEN 1), a transcription factor, plays a key role in sperm cell formation by activating expression of several germline genes. But how DUO1 itself is activated and how sperm cell formation is initiated remain unknown. To expand our understanding of sperm cell formation, we characterized an ARID (AT-Rich Interacting Domain)-containing protein, ARID1, that is specifically required for sperm cell formation in Arabidopsis. ARID1 localizes within nuclear bodies that are transiently present in the generative cell from which sperm cells arise, coincident with the timing of DUO1 activation. An arid1 mutant and antisense arid1 plants had an increased incidence of pollen with only a single sperm-like cell and exhibited reduced fertility as well as reduced expression of DUO1. In vitro and in vivo evidence showed that ARID1 binds to the DUO1 promoter. Lastly, we found that ARID1 physically associates with histone deacetylase 8 and that histone acetylation, which in wild type is evident only in sperm, expanded to the vegetative cell nucleus in the arid1 mutant. This study identifies a novel component required for sperm cell formation in plants and uncovers a direct positive regulatory role of ARID1 on DUO1 through association with histone acetylation.

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Model for ARID1 function during sperm cell formation in Arabidopsis.miR159 plays a major role in restricting DUO1 expression in the vegetative cell. As pollen development proceeds, miR159 abundance is gradually decreased and ARID1 expands its expression into the generative cell, possibly by responding to the decreased repressive role of miR159 in bicellular pollen. ARID1 then promotes DUO1 activation by directly binding to the DUO1 promoter, and thereby facilitates the initiation of sperm cell formation. On the other hand, ARID1 might repress expression of unknown negative regulators (orange) of cell cycle progression, by altering the epigenetic status of the generative cell. Once sperm cells are formed, ARID1 gradually decreases until it is eliminated from germline cells, so that DUO1 is steadily present and negative regulators possibly related to germline function start to be active, due to dissociation of ARID1 and histone deacetylase. Thus we hypothesize that the alteration of epigenetic status during sperm cell formation is correlated with a change in the subcellular localization of ARID1, which could facilitate cell cycle progression of the two consecutive mitoses. VN, vegetative nucleus; GN, generative cell; SC, sperm cells.
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pgen-1004421-g007: Model for ARID1 function during sperm cell formation in Arabidopsis.miR159 plays a major role in restricting DUO1 expression in the vegetative cell. As pollen development proceeds, miR159 abundance is gradually decreased and ARID1 expands its expression into the generative cell, possibly by responding to the decreased repressive role of miR159 in bicellular pollen. ARID1 then promotes DUO1 activation by directly binding to the DUO1 promoter, and thereby facilitates the initiation of sperm cell formation. On the other hand, ARID1 might repress expression of unknown negative regulators (orange) of cell cycle progression, by altering the epigenetic status of the generative cell. Once sperm cells are formed, ARID1 gradually decreases until it is eliminated from germline cells, so that DUO1 is steadily present and negative regulators possibly related to germline function start to be active, due to dissociation of ARID1 and histone deacetylase. Thus we hypothesize that the alteration of epigenetic status during sperm cell formation is correlated with a change in the subcellular localization of ARID1, which could facilitate cell cycle progression of the two consecutive mitoses. VN, vegetative nucleus; GN, generative cell; SC, sperm cells.

Mentions: In addition, unlike the DUO1 expression pattern, ARID1 is initially expressed in the microspore nucleus and subsequently expanded or segregated into the generative nucleus during the first asymmetric division (Figure 4 and Figure S4), indicating that DUO1 activation is an active process mediated by ARID1 from the vegetative cell, and not passively accomplished due to the completion of the first asymmetric division. We propose a model (Figure 7) to explain how DUO1 could be coordinately and sequentially regulated by the negative regulator miR159 and by the positive regulator ARID1. In the vegetative cell, MIR159 is transcribed abundantly during the unicellular stage, and so might play a major role in blocking DUO1 expression. As pollen development proceeds, in spite of the gradually decreasing but still detectable repressive role of miR159 in bicellular pollen, ARID1, inherited from the microspore, partitions into the generative cell to bind to DUO1 and gradually promote DUO1 activation. We hypothesize that other factors together with AIRD1 are potentially involved in DUO1 activation, as duo1 is 100% penetrant and because the generative cell fails to divide in all duo1 pollen grains. In contrast, disruption of ARID1 only caused partial defects in sperm cell formation. Due to the absence of DUO1 accumulation in the vegetative nucleus of arid1-1, we hypothesize that unknown factors (other than ARID1-associated histone modification machinery) might take over the major role of miR159 restricting DUO1 expression in the vegetative cell nucleus in the weak arid1-1 mutant (Figure 2). In parallel, ARID1 might promote sperm cell formation by altering the epigenetic status in both the vegetative cell and the generative cell; ARID1 physically associates with histone deacetylases, which could affect expression of the unknown gene(s) involved in sperm cell formation. Our data showed that ARID1 is necessary for the balance of histone acetylation between the vegetative cell and sperm cells of mature pollen (Figure 6A), indicating that this characteristic could be carried over from bicellular pollen. Moreover, a recent study showed that increased histone acetylation in cultured microspores led to the switch from gametophytic division to sporophytic division [33], further indicating that histone acetylation is critical for cell cycle progression during sperm cell formation.


An ARID domain-containing protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana.

Zheng B, He H, Zheng Y, Wu W, McCormick S - PLoS Genet. (2014)

Model for ARID1 function during sperm cell formation in Arabidopsis.miR159 plays a major role in restricting DUO1 expression in the vegetative cell. As pollen development proceeds, miR159 abundance is gradually decreased and ARID1 expands its expression into the generative cell, possibly by responding to the decreased repressive role of miR159 in bicellular pollen. ARID1 then promotes DUO1 activation by directly binding to the DUO1 promoter, and thereby facilitates the initiation of sperm cell formation. On the other hand, ARID1 might repress expression of unknown negative regulators (orange) of cell cycle progression, by altering the epigenetic status of the generative cell. Once sperm cells are formed, ARID1 gradually decreases until it is eliminated from germline cells, so that DUO1 is steadily present and negative regulators possibly related to germline function start to be active, due to dissociation of ARID1 and histone deacetylase. Thus we hypothesize that the alteration of epigenetic status during sperm cell formation is correlated with a change in the subcellular localization of ARID1, which could facilitate cell cycle progression of the two consecutive mitoses. VN, vegetative nucleus; GN, generative cell; SC, sperm cells.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4109846&req=5

pgen-1004421-g007: Model for ARID1 function during sperm cell formation in Arabidopsis.miR159 plays a major role in restricting DUO1 expression in the vegetative cell. As pollen development proceeds, miR159 abundance is gradually decreased and ARID1 expands its expression into the generative cell, possibly by responding to the decreased repressive role of miR159 in bicellular pollen. ARID1 then promotes DUO1 activation by directly binding to the DUO1 promoter, and thereby facilitates the initiation of sperm cell formation. On the other hand, ARID1 might repress expression of unknown negative regulators (orange) of cell cycle progression, by altering the epigenetic status of the generative cell. Once sperm cells are formed, ARID1 gradually decreases until it is eliminated from germline cells, so that DUO1 is steadily present and negative regulators possibly related to germline function start to be active, due to dissociation of ARID1 and histone deacetylase. Thus we hypothesize that the alteration of epigenetic status during sperm cell formation is correlated with a change in the subcellular localization of ARID1, which could facilitate cell cycle progression of the two consecutive mitoses. VN, vegetative nucleus; GN, generative cell; SC, sperm cells.
Mentions: In addition, unlike the DUO1 expression pattern, ARID1 is initially expressed in the microspore nucleus and subsequently expanded or segregated into the generative nucleus during the first asymmetric division (Figure 4 and Figure S4), indicating that DUO1 activation is an active process mediated by ARID1 from the vegetative cell, and not passively accomplished due to the completion of the first asymmetric division. We propose a model (Figure 7) to explain how DUO1 could be coordinately and sequentially regulated by the negative regulator miR159 and by the positive regulator ARID1. In the vegetative cell, MIR159 is transcribed abundantly during the unicellular stage, and so might play a major role in blocking DUO1 expression. As pollen development proceeds, in spite of the gradually decreasing but still detectable repressive role of miR159 in bicellular pollen, ARID1, inherited from the microspore, partitions into the generative cell to bind to DUO1 and gradually promote DUO1 activation. We hypothesize that other factors together with AIRD1 are potentially involved in DUO1 activation, as duo1 is 100% penetrant and because the generative cell fails to divide in all duo1 pollen grains. In contrast, disruption of ARID1 only caused partial defects in sperm cell formation. Due to the absence of DUO1 accumulation in the vegetative nucleus of arid1-1, we hypothesize that unknown factors (other than ARID1-associated histone modification machinery) might take over the major role of miR159 restricting DUO1 expression in the vegetative cell nucleus in the weak arid1-1 mutant (Figure 2). In parallel, ARID1 might promote sperm cell formation by altering the epigenetic status in both the vegetative cell and the generative cell; ARID1 physically associates with histone deacetylases, which could affect expression of the unknown gene(s) involved in sperm cell formation. Our data showed that ARID1 is necessary for the balance of histone acetylation between the vegetative cell and sperm cells of mature pollen (Figure 6A), indicating that this characteristic could be carried over from bicellular pollen. Moreover, a recent study showed that increased histone acetylation in cultured microspores led to the switch from gametophytic division to sporophytic division [33], further indicating that histone acetylation is critical for cell cycle progression during sperm cell formation.

Bottom Line: In plants, each male meiotic product undergoes mitosis, and then one of the resulting cells divides again, yielding a three-celled pollen grain comprised of a vegetative cell and two sperm cells.An arid1 mutant and antisense arid1 plants had an increased incidence of pollen with only a single sperm-like cell and exhibited reduced fertility as well as reduced expression of DUO1.In vitro and in vivo evidence showed that ARID1 binds to the DUO1 promoter.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Engineering, Collaborative Innovation Center for Genetics and Development, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China; Plant Gene Expression Center, USDA/ARS and Dept. of Plant and Microbial Biology, UC-Berkeley, Albany, California, United States of America.

ABSTRACT
In plants, each male meiotic product undergoes mitosis, and then one of the resulting cells divides again, yielding a three-celled pollen grain comprised of a vegetative cell and two sperm cells. Several genes have been found to act in this process, and DUO1 (DUO POLLEN 1), a transcription factor, plays a key role in sperm cell formation by activating expression of several germline genes. But how DUO1 itself is activated and how sperm cell formation is initiated remain unknown. To expand our understanding of sperm cell formation, we characterized an ARID (AT-Rich Interacting Domain)-containing protein, ARID1, that is specifically required for sperm cell formation in Arabidopsis. ARID1 localizes within nuclear bodies that are transiently present in the generative cell from which sperm cells arise, coincident with the timing of DUO1 activation. An arid1 mutant and antisense arid1 plants had an increased incidence of pollen with only a single sperm-like cell and exhibited reduced fertility as well as reduced expression of DUO1. In vitro and in vivo evidence showed that ARID1 binds to the DUO1 promoter. Lastly, we found that ARID1 physically associates with histone deacetylase 8 and that histone acetylation, which in wild type is evident only in sperm, expanded to the vegetative cell nucleus in the arid1 mutant. This study identifies a novel component required for sperm cell formation in plants and uncovers a direct positive regulatory role of ARID1 on DUO1 through association with histone acetylation.

Show MeSH
Related in: MedlinePlus