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Mechanism of fertilization-induced auxin synthesis in the endosperm for seed and fruit development.

ABSTRACT: The dominance of flowering plants on earth is owed largely to the evolution of maternal tissues such as fruit and seedcoat that protect and disseminate the seeds. The mechanism of how fertilization triggers the development of these specialized maternal tissues is not well understood. A key event is the induction of auxin synthesis in the endosperm, and the mobile auxin subsequently stimulates seedcoat and fruit development. However, the regulatory mechanism of auxin synthesis in the endosperm remains unknown. Here, we show that a type I MADS box gene AGL62 is required for the activation of auxin synthesis in the endosperm in both Fragaria vesca, a diploid strawberry, and in Arabidopsis. Several strawberry FveATHB genes were identified as downstream targets of FveAGL62 and act to repress auxin biosynthesis. In this work, we identify a key mechanism for auxin induction to mediate fertilization success, a finding broadly relevant to flowering plants.

SUBMITTER: Guo L

PROVIDER: S-EPMC9271072 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Auxin production in the endosperm drives seed coat development in Arabidopsis.

Project description:In flowering plants, seed development is initiated by the fusion of the maternal egg and central cells with two paternal sperm cells, leading to the formation of embryo and endosperm, respectively. The fertilization products are surrounded by the maternally derived seed coat, whose development prior to fertilization is blocked by epigenetic regulators belonging to the Polycomb Group (PcG) protein family. Here we show that fertilization of the central cell results in the production of auxin and most likely its export to the maternal tissues, which drives seed coat development by removing PcG function. We furthermore show that mutants for the MADS-box transcription factor AGL62 have an impaired transport of auxin from the endosperm to the integuments, which results in seed abortion. We propose that AGL62 regulates auxin transport from the endosperm to the integuments, leading to the removal of the PcG block on seed coat development.

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Additional nitrogen fertilization at heading time of rice down-regulates cellulose synthesis in seed endosperm.

Project description:The balance between carbon and nitrogen is a key determinant of seed storage components, and thus, is of great importance to rice and other seed-based food crops. To clarify the influence of the rhizosphere carbon/nitrogen balance during the maturation stage of several seed components, transcriptome analysis was performed on the seeds from rice plants that were provided additional nitrogen fertilization at heading time. As a result, it was assessed that genes associated with molecular processes such as photosynthesis, trehalose metabolism, carbon fixation, amino acid metabolism, and cell wall metabolism were differentially expressed. Moreover, cellulose and sucrose synthases, which are involved in cellulose synthesis, were down-regulated. Therefore, we compared cellulose content of mature seeds that were treated with additional nitrogen fertilization with those from control plants using calcofluor staining. In these experiments, cellulose content in endosperm from plants receiving additional nitrogen fertilization was less than that in control endosperm. Other starch synthesis-related genes such as starch synthase 1, starch phosphorylase 2, and branching enzyme 3 were also down-regulated, whereas some α-amylase and β-amylase genes were up-regulated. On the other hand, mRNA expression of amino acid biosynthesis-related molecules was up-regulated. Moreover, additional nitrogen fertilization caused accumulation of storage proteins and up-regulated Cys-poor prolamin mRNA expression. These data suggest that additional nitrogen fertilization at heading time changes the expression of some storage substance-related genes and reduces cellulose levels in endosperm.

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Fertilization Independent Endosperm genes repress NbGH3.6 and regulate the auxin level during shoot development in Nicotiana benthamiana.

Project description:The Fertilization Independent Endosperm (FIE) gene is required to restrict endosperm development without fertilization, and it represses flowering during embryo and seedling development in Arabidopsis thaliana However, the regulatory mechanism of the FIE gene in postembryonic shoot development is not well understood. Silencing of Nicotiana benthamiana homologues of the FIE gene, NbFIE1 and NbFIE2, resulted in the enhanced outgrowth of axillary buds and the impairment of secondary xylem differentiation. RNA sequencing analysis found that one of the auxin-responsive GRETCHEN HAGEN 3(GH3) family genes, NbGH3.6, was upregulated and maintained a high expression during the time course of silencing NbFIE genes. Chromatin immunoprecipiation (ChIP)-PCR results showed a lack of H3K27me3 marks on NbGH3.6 chromatin in NbFIE-silenced plants compared with negative control plants, indicating that NbGH3.6 was a direct target of NbFIE genes during postembryonic shoot development. Moreover, the free IAA content was reduced significantly in NbFIE-silenced plants, which might cause the enhanced outgrowth of axillary buds as well as impaired secondary xylem differentiation. These results clearly indicated that NbGH3.6 was a primary target of NbFIE genes during postembryonic shoot development, and NbFIE genes regulated axillary bud growth and secondary xylem formation through tuning endogenous auxin homeostasis, possibly by regulating the expression of the NbGH3.6 gene.

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Auxin production in the endosperm drives seed coat development in Arabidopsis

Project description:This SuperSeries is composed of the SubSeries listed below.

2016-11-15 | GSE85848 | GEO

Into the Seed: Auxin Controls Seed Development and Grain Yield.

Project description:Seed development, which involves mainly the embryo, endosperm and integuments, is regulated by different signaling pathways, leading to various changes in seed size or seed weight. Therefore, uncovering the genetic and molecular mechanisms of seed development has great potential for improving crop yields. The phytohormone auxin is a key regulator required for modulating different cellular processes involved in seed development. Here, we provide a comprehensive review of the role of auxin biosynthesis, transport, signaling, conjugation, and catabolism during seed development. More importantly, we not only summarize the research progress on the genetic and molecular regulation of seed development mediated by auxin but also discuss the potential of manipulating auxin metabolism and its signaling pathway for improving crop seed weight.

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Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry.

Project description:The critical role of auxin in strawberry fruit set and receptacle enlargement was demonstrated previously. While fertilization is known to trigger auxin biosynthesis, the specific tissue source of fertilization-induced auxin is not well understood. Here, the auxin reporter DR5ver2::GUS was introduced into wild strawberry (Fragaria vesca) to reveal auxin distribution in the seed and fruit receptacle pre- and post-fertilization as well as in the root. In addition, the expression of TAR and YUCCA genes coding for enzymes catalysing the two-step auxin biosynthesis pathway was investigated using their respective promoters fused to the ?-glucuronidase (GUS) reporter. Two FveTARs and four FveYUCs were shown to be expressed primarily in the endosperm and embryo inside the achenes as well as in root tips and lateral root primordia. Expression of these reporters in dissected tissues provided more detailed and precise spatial (cell and tissue) and temporal (pre- and post-fertilization) information on where auxin is synthesized and accumulates than previous studies in strawberry. Moreover, we generated CRISPR-mediated knock-out mutants of FveYUC10, the most abundant YUC in seeds; the mutants had a lower free auxin level in young fruit, but displayed no obvious morphological phenotypes. However, overexpression of FveYUC10 resulted in elongated hypocotyls in Arabidopsis caused by elevated auxin level. Overall, the study revealed auxin accumulation in the chalazal seed coat, embryo, receptacle vasculature, root tip, and lateral root primordia and highlighted the endosperm as the main auxin biosynthesis site for fruit set.

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Auxin production in the endosperm drives seed coat development in Arabidopsis

Project description:Auxin production in the endosperm drives seed coat development in Arabidopsis

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Genes controlling fertilization-independent seed development in Arabidopsis thaliana.

Project description:We have cloned two genes, FIS1 and FIS2, that control both fertilization independent seed development and postpollination embryo development in Arabidopsis. These genes confer female gametophytic phenotypes. FIS2 encodes a protein with a C2H2 zinc-finger motif and three putative nuclear localization signals, indicating that it is likely to be a transcription factor. FIS1 encodes a protein with homology to the Drosophila Polycomb group gene Enhancer-of-zeste and is identical to the recently described Arabidopsis gene MEDEA. FIS1 is a protein with a number of putative functional domains, including the SET domain present in Enhancer-of-zeste-related proteins. Comparison of the position of the lesions in the fis1 and medea mutant alleles indicates that fis1 is a null allele producing a truncated polypeptide lacking all the protein domains whereas the deduced protein from medea lacks only the SET domain. We present a model of the role of FIS1 and FIS2 gene products in seed development.

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EML histone readers prevent seed development without fertilization

Project description:EML1 and EML3 were previously shown to be histone readers involved in plant-pathogen interactions. To learn more about the developmental function of EML1 and EML3, we generated eml1 eml3 double mutant and showed that it had specific seed developmental phenotypes, including a capability to develop seed without fertilization. Next, we analyzed the mRNA expression of genes in the eml1 eml3 double mutant and compared it to its wild type. Differentially expressed (DE) genes in the mutant were identified and compared with DE of the mutants known to be involved in regulating seed development and in fertilization-independent endosperm development. Our results suggest that some targets are shared between EML histone readers and known regulators of seed development, such as MEA. Auxin response seems to be affected in both types of mutants. However, unlike MEA, EML proteins regulate auxin responsive genes not only in the endosperm, but also in the embryo. This capability makes EML proteins very good candidates for engineering apomictic seeds.

2019-05-01 | GSE113847 | GEO

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Project description:Fruit set of plants largely depends on the biosynthesis and crosstalk of phytohormones. To date the role of cytokinins (CKs) in the fruit development is less understood. Here, we showed that parthenocarpic fruit could be induced by 1-(2-chloro-4-pyridyl)-3-phenylurea (CPPU, an active CK) in tomato (Solanumlycopersicum cv. Micro-Tom). The fresh weight of CPPU-induced parthenocarpic fruits was comparable with that induced by GA3. Importantly, CPPU-induced parthenocarpy was found to be compromised by simultaneous application of paclobutrazol (a GA biosynthesis inhibitor), and this effect could be restored by exogenous GA3. Like pollination, CPPU-induced fruit showed enhanced accumulation of GA1+3 and indole-3-acetic (IAA), which were accompanied by elevated expression of GA biosynthesis genes like SlGPS, SlGA20ox1, SlGA20ox2 and SlGA3ox1, and IAA biosynthesis gene ToFZY. Elevated GAs level in CPPU-induced fruits was also associated with down-regulation of GA inactivation genes, namely SlGA2ox1,2,3,4,5 in comparison with untreated control. These results suggested that CKs may induce parthenocarpy in tomato partially through modulation of GA and IAA metabolisms.

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