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Transcription factor CDF4 promotes leaf senescence and floral organ abscission by regulating abscisic acid and reactive oxygen species pathways in Arabidopsis.

ABSTRACT: Leaf senescence is a highly complex developmental process that is tightly controlled by multiple layers of regulation. Abscisic acid (ABA) and reactive oxygen species (ROS) are two well-known factors that promote leaf senescence. We show here that the transcription factor CDF4 positively regulates leaf senescence. Constitutive and inducible overexpression of CDF4 accelerates leaf senescence, while knockdown of CDF4 delays it. CDF4 increases endogenous ABA levels by upregulating the transcription of the ABA biosynthesis genes 9-cis-epoxycarotenoid dioxygenase 2, 3 (NCED2, 3) and suppresses H₂ O₂ scavenging by repressing expression of the catalase2 (CAT2) gene. NCED2, 3 knockout and CAT2 overexpression partially rescue premature leaf senescence caused by CDF4 overexpression. We also show that CDF4 promotes floral organ abscission by activating the polygalacturonase PGAZAT gene. Based on these results, we propose that the levels of CDF4, ABA, and ROS undergo a gradual increase driven by their interlinking positive feedback loops during the leaf senescence and floral organ abscission processes.

SUBMITTER: Xu P

PROVIDER: S-EPMC7332990 | biostudies-literature |

REPOSITORIES: biostudies-literature

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CDF4 promotes leaf senescence by regulating ABA and reactive oxygen species pathways in Arabidopsis

Project description:Abstract Leaf senescence is a highly complex developmental process that is tightly controlled by multiple layers of regulation. Abscisic acid (ABA) and reactive oxygen species (ROS) are two well-known factors that promote leaf senescence. We show here that the transcription factor CDF4 positively regulates leaf senescence. Constitutive and inducible overexpression of CDF4 accelerates leaf senescence, while knockdown of CDF4 delays it. CDF4 increases endogenous ABA levels by upregulating the transcription of the ABA biosynthesis genes 9-cis-epoxycarotenoid dioxygenase 2, 3 (NCED2, 3) and suppresses H2O2 scavenging by repressing expression of the catalase2 (CAT2) gene. NCED2, 3 knockout and CAT2 overexpression partially rescue premature leaf senescence caused by CDF4 overexpression. We also show that CDF4 promotes floral organ abscission by activating the polygalacturonase PGAZAT gene. Based on these results, we propose that the levels of CDF4, ABA and ROS undergo a gradual increase driven by their interlinking positive feedback loops during the leaf senescence and floral organ abscission processes.

| S-SCDT-EMBOR-2019-48967-T | biostudies-other

Regulation of floral organ abscission in Arabidopsis thaliana.

Project description:Abscission is a developmental program that results in the active shedding of infected or nonfunctional organs from a plant body. Here, we establish a signaling pathway that controls abscission in Arabidopsis thaliana from ligand, to receptors, to downstream effectors. Loss of function mutations in Inflorescence Deficient in Abscission (IDA), which encodes a predicted secreted small protein, the receptor-like protein kinases HAESA (HAE) and HAESA-like 2 (HSL2), the Mitogen-Activated Protein Kinase Kinase 4 (MKK4) and MKK5, and a dominant-negative form of Mitogen-Activated Protein Kinase 6 (MPK6) in a mpk3 mutant background all have abscission-defective phenotypes. Conversely, expression of constitutively active MKKs rescues the abscission-defective phenotype of hae hsl2 and ida plants. Additionally, in hae hsl2 and ida plants, MAP kinase activity is reduced in the receptacle, the part of the stem that holds the floral organs. Plants overexpressing IDA in a hae hsl2 background have abscission defects, indicating HAE and HSL2 are epistatic to IDA. Taken together, these results suggest that the sequential action of IDA, HAE and HSL2, and a MAP kinase cascade regulates the programmed separation of cells in the abscission zone.

| S-EPMC2563077 | biostudies-literature

Ligand-Induced Receptor-like Kinase Complex Regulates Floral Organ Abscission in Arabidopsis.

Project description:Abscission is a developmental process that enables plants to shed unwanted organs. In Arabidopsis, the floral organ abscission is regulated by a signaling pathway consisting of the peptide ligand IDA, the receptor-like kinases (RLKs) HAE and HSL2, and a downstream MAP kinase (MAPK) cascade. However, little is known about the molecular link between ligand-receptor pairs and intracellular signaling. Here, we report that the SERK family RLKs function redundantly in regulating floral organ abscission downstream of IDA and upstream of the MAPK cascade. IDA induces heterodimerization of HAE/HSL2 and SERKs, which transphosphorylate each other. The SERK3 residues mediating its interaction with the immune receptor FLS2 and the brassinosteroid receptor BRI1 are also required for IDA-induced HAE/HSL2-SERK3 interaction, suggesting SERKs serve as co-receptors of HAE/HSL2 in perceiving IDA. Thus, our study reveals the signaling activation mechanism in floral organ abscission by IDA-induced HAE/HSL2-SERK complex formation accompanied by transphosphorylation.

| S-EPMC4758877 | biostudies-literature

HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission.

Project description:Abcission, the natural shedding of leaves, flowers and fruits, is a fundamental component of plant development. Abscission is a highly regulated process that occurs at distinct zones of cells that undergo enlargement and subsequent separation. Although some components of abscission, including accumulation of the hormone ethylene and cell wall-degrading enzymes, have been described, the regulatory pathways remain largely unknown. In this paper we describe a critical component required for floral organ abscission in Arabidopsis thaliana, the receptor-like protein kinase HAESA. Histochemical analysis of transgenic plants harboring a HAESA promoter:: beta-glucuronidase reporter gene and in situ RNA hybridization experiments show HAESA expression in the abscission zones where the sepals, petals, and stamens attach to the receptacle, at the base of pedicels, and at the base of petioles where leaves attach to the stem. Immunodetection, immunoprecipitation, and protein kinase activity assays reveal HAESA is a plasma membrane serine/threonine protein kinase. The reduction of function of HAESA in transgenic plants harboring an antisense construct results in delayed abscission of floral organs, and the severity of the phenotype is directly correlated with the level of HAESA protein. These results demonstrate that HAESA functions in developmentally regulated floral organ abscission.

| S-EPMC316334 | biostudies-literature

Role of ARABIDOPSIS A-FIFTEEN in regulating leaf senescence involves response to reactive oxygen species and is dependent on ETHYLENE INSENSITIVE2.

Project description:Leaf senescence is a highly regulated developmental process that is coordinated by several factors. Many senescence-associated genes (SAGs) have been identified, but their roles during senescence remain unclear. A sweet potato (Ipomoea batatas) SAG, named SPA15, whose function was unknown, was identified previously. To understand the role of SPA15 in leaf senescence further, the orthologue of SPA15 in Arabidopsis thaliana was identified and characterized, and it was named ARABIDOPSIS A-FIFTEEN (AAF). AAF was expressed in early senescent leaves and in tissues with highly proliferative activities. AAF was localized to the chloroplasts by transient expression in Arabidopsis mesophyll protoplasts. Overexpression of AAF (AAF-OX) in Arabidopsis promoted, but the T-DNA insertion mutant (aaf-KO), delayed age-dependent leaf senescence. Furthermore, stress-induced leaf senescence caused by continuous darkness was enhanced in AAF-OX but suppressed in aaf-KO. Transcriptome analysis of expression profiles revealed up-regulated genes related to pathogen defence, senescence, and oxidative stress in 3-week-old AAF-OX plants. Indeed, elevated levels of reactive oxygen species (ROS) and enhanced sensitivity to oxidative and dark stress were apparent in AAF-OX but reduced in aaf-KO. ETHYLENE INSENSITIVE2 (EIN2) was required for the dark- and ROS-induced senescence phenotypes in AAF-OX and the induction of AAF expression by treatment with the immediate precursor of ethylene, 1-aminocyclopropane-1-carboxylic acid. The results indicate the functional role of AAF is an involvement in redox homeostasis to regulate leaf senescence mediated by age and stress factors during Arabidopsis development.

| S-EPMC3245469 | biostudies-literature

Post-translational maturation of IDA, a peptide signal controlling floral organ abscission in Arabidopsis

Project description:ABSTRACT The abscission of sepals, petals and stamens in Arabidopsis flowers is controlled by a peptide signal called IDA (Inflorescence Deficient in Abscission). IDA belongs to the large group of small post-translationally modified signaling peptides that are synthesized as larger precursors and require proteolytic processing and specific side chain modifications for signal biogenesis. Using tissue-specific expression of proteinase inhibitors as a novel approach for loss-of-function analysis, we recently identified the peptidases responsible for IDA maturation within the large family of subtilisin-like proteinases (subtilases; SBTs). Further biochemical and physiological assays identified three SBTs (AtSBT5.2, AtSBT4.12, AtSBT4.13) that cleave the IDA precursor to generate the N-terminus of the mature peptide. The C-terminal processing enzyme(s) remain(s) to be identified. While proline hydroxylation was suggested as additional post-translational modification required for IDA maturation, hydroxylated and non-hydroxylated IDA peptides were found to be equally active in bioassays for abscission.

| S-EPMC5824936 | biostudies-literature

MSD2-mediated ROS metabolism fine-tunes the timing of floral organ abscission in Arabidopsis.

Project description:The timely removal of end-of-purpose flowering organs is as essential for reproduction and plant survival as timely flowering. Despite much progress in understanding the molecular mechanisms of floral organ abscission, little is known about how various environmental factors are integrated into developmental programmes that determine the timing of abscission. Here, we investigated whether reactive oxygen species (ROS), mediators of various stress-related signalling pathways, are involved in determining the timing of abscission and, if so, how they are integrated with the developmental pathway in Arabidopsis thaliana. MSD2, encoding a secretory manganese superoxide dismutase, was preferentially expressed in the abscission zone of flowers, and floral organ abscission was accelerated by the accumulation of ROS in msd2 mutants. The expression of the genes encoding the receptor-like kinase HAESA (HAE) and its cognate peptide ligand INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), the key signalling components of abscission, was accelerated in msd2 mutants, suggesting that MSD2 acts upstream of IDA-HAE. Further transcriptome and pharmacological analyses revealed that abscisic acid and nitric oxide facilitate abscission by regulating the expression of IDA and HAE during MSD2-mediated signalling. These results suggest that MSD2-dependent ROS metabolism is an important regulatory point integrating environmental stimuli into the developmental programme leading to abscission.

| S-EPMC9543660 | biostudies-literature

Transcription Factor NAC075 Delays Leaf Senescence by Deterring Reactive Oxygen Species Accumulation in <i>Arabidopsis</i>.

Project description:Leaf senescence is a highly complex genetic process that is finely tuned by multiple layers of regulation. Among them, transcriptional regulation plays a critical role in controlling the initiation and progression of leaf senescence. Here, we found that the NAC transcription factor NAC075 functions as a novel negative regulator of leaf senescence. Loss of function of NAC075 promotes leaf senescence in an age-dependent manner, whereas constitutive overexpression of NAC075 delays senescence in Arabidopsis. Transcriptome analysis revealed that transcript levels of antioxidant enzymes such as catalase (CAT), ascorbate peroxidase (APX), and superoxide dismutase (SOD) are significantly suppressed in nac075 mutants compared with wild-type plants. Electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation (ChIP) analyses revealed that NAC075 directly binds the promoter of catalase 2 (CAT2). Moreover, genetic analysis showed that overexpression of CAT2 suppresses the overproduction of reactive oxygen species (ROS) and the early senescence phenotypes of nac075 mutants, suggesting that CAT2 acts downstream of NAC075 to delay leaf senescence by repressing ROS accumulation. Collectively, our findings provide a new regulatory module involving NAC075-CAT2-ROS in controlling leaf senescence in Arabidopsis.

| S-EPMC7943619 | biostudies-literature

Floral organ abscission is regulated by a positive feedback loop.

Project description:Abscission is the process by which plants shed unwanted organs, either as part of a natural developmental program or in response to environmental stimuli. Studies in Arabidopsis thaliana have elucidated a number of the genetic components that regulate abscission of floral organs, including a pair of related receptor-like protein kinases, HAESA and HAESA-like 2 (HAE/HSL2) that regulate a MAP kinase cascade that is required for abscission. HAE is transcriptionally up-regulated in the floral abscission zone just before cell separation. Here, we identify AGAMOUS-like 15 (AGL15; a MADS-domain transcription factor) as a putative regulator of HAE expression. Overexpression of AGL15 results in decreased expression of HAE as well as a delayed abscission phenotype. Chromatin immunoprecipitation experiments indicate that AGL15 binds the HAE promoter in floral receptacles. AGL15 is then differentially phosphorylated through development in floral receptacles in a MITOGEN-ACTIVATED PROTEIN KINASE KINASE 4/5-dependent manner. MAP kinase phosphorylation of AGL15 is necessary for full HAE expression, thus completing a positive feedback loop controlling HAE expression. Together, the network components in this positive feedback loop constitute an emergent property that regulates the large dynamic range of gene expression (27-fold increase in HAE) observed in flowers when the abscission program is initiated. This study helps define the mechanisms and regulatory networks involved in a receptor-mediated signaling pathway that controls floral organ abscission.

| S-EPMC4352813 | biostudies-other

Arabidopsis NPF4.6 and NPF5.1 Control Leaf Stomatal Aperture by Regulating Abscisic Acid Transport.

Project description:The plant hormone abscisic acid (ABA) is actively synthesized in vascular tissues and transported to guard cells to promote stomatal closure. Although several transmembrane ABA transporters have been identified, how the movement of ABA within plants is regulated is not fully understood. In this study, we determined that Arabidopsis NPF4.6, previously identified as an ABA transporter expressed in vascular tissues, is also present in guard cells and positively regulates stomatal closure in leaves. We also found that mutants defective in NPF5.1 had a higher leaf surface temperature compared to the wild type. Additionally, NPF5.1 mediated cellular ABA uptake when expressed in a heterologous yeast system. Promoter activities of NPF5.1 were detected in several leaf cell types. Taken together, these observations indicate that NPF5.1 negatively regulates stomatal closure by regulating the amount of ABA that can be transported from vascular tissues to guard cells.

| S-EPMC8227765 | biostudies-literature

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