Abscission is an active process that enables plants to shed unwanted organs. Because the purpose of the flower is to facilitate pollination, it often is abscised after fertilization. We have identified an Arabidopsis ethylene-sensitive mutant, inflorescence deficient in abscission (
In Arabidopsis thaliana, the final step of floral organ abscission is regulated by INFLORESCENCE DEFICIENT IN ABSCISSION (IDA): ida mutants fail to abscise floral organs, and plants overexpressing IDA display earlier abscission. We show that five IDA-LIKE (IDL) genes are expressed in different tissues, but plants overexpressing these genes have phenotypes similar to IDA-overexpressing plants, suggesting functional redundancy. IDA/IDL proteins have N-terminal signal peptides and a C-terminal conserved motif (extended PIP [EPIP]) at the C terminus (EPIP-C). IDA can, similar to CLAVATA3, be processed by an activity from cauliflower meristems. The EPIP-C of IDA and IDL1 replaced IDA function in vivo, when the signal peptide was present. In addition, synthetic IDA and IDL1 EPIP peptides rescued ida and induced early floral abscission in wild-type flowers. The EPIP-C of the other IDL proteins could partially substitute for IDA function. Similarly to ida, a double mutant between the receptor-like kinases (RLKs) HAESA (HAE) and HAESA-LIKE2 (HSL2) displays nonabscising flowers. Neither overexpression of IDA nor synthetic EPIP or EPIP-C peptides could rescue the hae hsl2 abscission deficiency. We propose that IDA and the IDL proteins constitute a family of putative ligands that act through RLKs to regulate different events during plant development.
Throughout their life cycle, plants produce new organs, such as leaves, flowers, and lateral roots. Organs that have served their purpose may be shed after breakdown of primary cell walls between adjacent cell files at the site of detachment. In Arabidopsis, floral organs abscise after pollination, and this cell separation event is controlled by the peptide INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), which signals through the leucine-rich repeat receptor-like kinases HAESA (HAE) and HAESA-LIKE2 (HSL2). Emergence of new lateral root primordia, initiated deep inside the root under the influence of auxin, is similarly dependent on cell wall dissolution between cells in the overlaying endodermal, cortical, and epidermal tissues. Here we show that this process requires IDA, HAE, and HSL2. Mutation in these genes constrains the passage of the growing lateral root primordia through the overlaying layers, resulting in altered shapes of the lateral root primordia and of the overlaying cells. The HAE and HSL2 receptors are redundant in function during floral organ abscission, but during lateral root emergence they are differentially involved in regulating cell wall remodeling genes. In the root, IDA is strongly auxin-inducible and dependent on key regulators of lateral root emergence-the auxin influx carrier LIKE AUX1-3 and AUXIN RESPONSE FACTOR7. The expression levels of the receptor genes are only transiently induced by auxin, suggesting they are limiting factors for cell separation. We conclude that elements of the same cell separation signaling module have been adapted to function in different developmental programs.root development | peptide signaling | pectin degradation | polygalacturonases | propidium iodide M ore than 200 genes encoding leucine-rich repeat receptorlike kinases (1) and more than 1,000 genes encoding putative secreted peptides have been identified in Arabidopsis thaliana (2), suggesting that peptide ligand-receptor interactions are important for cell-to-cell communication in plants. However, fewer than a dozen signaling modules, including INFLORESCENCE DE-FICIENT IN ABSCISSION (IDA)-HAESA (HAE)/HAESA-LIKE2 (HSL2) controlling the separation step of floral organ abscission, have been identified by genetic and/or biochemical methods (3). Both the ida mutant and the hae hsl2 double mutant retain their floral organs indefinitely owing to lack of breakdown of the middle lamella between cell layers of the abscission zone (AZ) at the base of organs to be shed (4-6). IDA is expressed in the AZ region of the flowers (4), whereas both HAE and HSL2 expression is confined specifically to the specialized AZ cells (5, 6). Overexpression of IDA leads to premature and ectopic abscission, but not in hae hsl2 mutant background, consistent with IDA being the ligand of these receptors (5, 6).The abscission process involves initial cell wall loosening by enzymes like xyloglucan endotransglucosylase/hydrolases (XTHs) and expansins (EXPs) (7,8). The loosening facilitates the access of cell wall degradation enzymes like p...
RESULTSLoss of abscission in bop1 bop2 mutants is independent of senescence Loss of floral organ abscission is a striking phenotype of bop1 bop2 plants (Fig. 1A). In wild type, sepals, petals and stamens normally abscise shortly after anthesis (flower opening). The convention used Development 135 (8) RESEARCH ARTICLE
Plants constantly renew during their life cycle and thus require to shed senescent and damaged organs. Floral abscission is controlled by the leucine-rich repeat receptor kinase (LRR-RK) HAESA and the peptide hormone IDA. It is unknown how expression of IDA in the abscission zone leads to HAESA activation. Here we show that IDA is sensed directly by the HAESA ectodomain. Crystal structures of HAESA in complex with IDA reveal a hormone binding pocket that accommodates an active dodecamer peptide. A central hydroxyproline residue anchors IDA to the receptor. The HAESA co-receptor SERK1, a positive regulator of the floral abscission pathway, allows for high-affinity sensing of the peptide hormone by binding to an Arg-His-Asn motif in IDA. This sequence pattern is conserved among diverse plant peptides, suggesting that plant peptide hormone receptors may share a common ligand binding mode and activation mechanism.DOI: http://dx.doi.org/10.7554/eLife.15075.001
Plants may shed organs when they have been injured or served their purpose. The differential pattern of organ abscission in different species is most likely the result of evolutionary adaptation to a variety of life styles and environments. The final step of abscission-related cell separation in floral organs of wild-type Arabidopsis thaliana, which only abscises sepals, petals, and stamens, is controlled by INFLORESCENCE DEFICIENT IN ABSCISSION (IDA). Here, we demonstrate that Arabidopsis 35S:IDA lines constitutively overexpressing IDA exhibit earlier abscission of floral organs, showing that the abscission zones are responsive to IDA soon after the opening of the flowers. In addition, ectopic abscission was observed at the bases of the pedicel, branches of the inflorescence, and cauline leaves. The silique valves also dehisced prematurely. Scanning electron microscopy indicated a spread of middle lamella degradation from preformed abscission zone cells to neighboring cells. A transcript encoding an arabinogalactan protein (AGP) was upregulated in the 35S:IDA lines, and large amounts of AGP were secreted at the sites of abscission. AGP was shown to be a constituent of wild-type floral abscission zones during and soon after cell separation had been completed. We suggest that the restricted expression pattern of IDA precludes abscission of nonfloral organs in Arabidopsis.
Floral organ abscission in Arabidopsis thaliana is regulated by the putative ligand-receptor system comprising the signaling peptide INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) and the two receptor-like kinases HAESA and HAESA-LIKE2. The IDA signaling pathway presumably activates a MITOGEN-ACTIVATED PROTEIN KINASE (MAPK) cascade to induce separation between abscission zone (AZ) cells. Misexpression of IDA effectuates precocious floral abscission and ectopic cell separation in latent AZ cell regions, which suggests that negative regulators are in place to prevent unrestricted and untimely AZ cell separation. Through a screen for mutations that restore floral organ abscission in ida mutants, we identified three new mutant alleles of the KNOTTED-LIKE HOMEOBOX gene BREVIPEDICELLUS (BP)/KNOTTED-LIKE FROM ARABIDOPSIS THALIANA1 (KNAT1). Here, we show that bp mutants, in addition to shedding their floral organs prematurely, have phenotypic commonalities with plants misexpressing IDA, such as enlarged AZ cells. We propose that BP/KNAT1 inhibits floral organ cell separation by restricting AZ cell size and number and put forward a model whereby IDA signaling suppresses BP/KNAT1, which in turn allows KNAT2 and KNAT6 to induce floral organ abscission. INTRODUCTIONCell separation processes are critical for the development of a plant and play key roles from sculpting the form of the plant to scattering seeds. Abscission, a physiological process that involves programmed changes in cellular adhesion, allows the plant to discard nonfunctional or infected organs. At the cellular level, the presence of an abscission zone (AZ), consisting of small densely cytoplasmic cells at the boundary between organ and plant, is a prerequisite for abscission to take place (McKim et al., 2008). During the subsequent activation of the cell separation process, AZ cells acquire competence to respond to abscission signals and secrete cell wall-modifying and hydrolyzing enzymes that act to degrade the middle lamella between two adjacent cell files (Bleecker and Patterson, 1997;Patterson, 2001;Roberts et al., 2002;Lewis et al., 2006;Stenvik et al., 2006). Shortly before organ shedding, the cells at the proximal side of the AZ expand; however, the relationship between AZ cell enlargement and organ separation is unclear (Patterson, 2001). It has been proposed that the functional role of AZ cell expansion might be to create the tension needed for the final mechanical rupture of the AZ (Sexton and Redshaw, 1981); indeed, the receptor-like kinase (RLK) EVERSHED (EVR) has recently been implicated in regulating the proper timing of floral organ abscission in Arabidopsis thaliana in part by restricting AZ cell size .The correct temporal and spatial regulation of abscission is crucial during plant development. Premature abscission of reproductive organs or immature seeds can compromise reproduction, and unrestricted cell separation can lead to shedding of organs in the proximity of activated AZ cells or interfere with tissue integrity. Studies using Arabidopsis...
HighlightThis study presents new members of the IDA/IDL and PIP/PIPL families of peptide ligands in Arabidopsis, and highlights that family members are linked to stress responses as well as development.
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