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Proc Natl Acad Sci U S A. Oct 7, 2008; 105(40): 15629–15634.
Published online Sep 22, 2008. doi:  10.1073/pnas.0805539105
PMCID: PMC2563077
From the Cover
Plant Biology

Regulation of floral organ abscission in Arabidopsis thaliana

Sung Ki Cho,* Clayton T. Larue,*§ David Chevalier,* Huachun Wang,** Tsung-Luo Jinn,*†† Shuqun Zhang,‡‡ and John C. Walker*‡‡

Abstract

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.

Keywords: protein phosphorylation, signal transduction

Abscission is a physiological process that involves the programmed separation of entire organs, such as leaves, petals, flowers, and fruit. Abscission allows plants to discard nonfunctional or infected organs, and promotes dispersion of progeny. At the cellular level, abscission is the hydrolysis of the middle lamella of an anatomically specialized cell layer, the abscission zone (AZ), by cell wall-modifying and hydrolyzing enzymes. Thus, abscission requires both the formation of the AZ early in the development of a plant organ and the subsequent activation of the cell separation response (14).

Studies using Arabidopsis thaliana have implicated the involvement of several different genes in the control of abscission including potential signal molecules, receptors and other gene products (4). HAESA (HAE), one of the first Arabidopsis receptor-like protein kinases (RLK) identified, is expressed in floral organ AZs and antisense experiments show a reduction in the level of HAE protein is correlated with the degree of defective floral organ abscission. Expression of HAE is not altered in etr1-1 (an ethylene-insensitive mutation), implying an ethylene-independent role in abscission (5). Inflorescence Deficient in Abscission (IDA) encodes a small protein with an N-terminal signal peptide. Analysis of ida mutant plants indicates IDA regulates floral organ abscission through an ethylene insensitive pathway (6). Overexpression of IDA results in early abscission and the production of a white substance in the floral AZs. The main components of the white substance are arabinose and galactose (7).

Here, we report that components of a MAPK signaling cascade also have roles in the regulation of abscission. A MAPK cascade is a regulatory module with three protein kinases, a MAP kinase kinase kinases (MKKK) that activates a MAP kinase kinases (MKK), which in turn, activates a MAP kinase (MPK). MAPK cascades play important roles in plant responses to pathogens, hormone responses, and development (8). In addition to demonstrating a role for a MAPK cascade in abscission we also link the MAPK pathway to a putative ligand, IDA, and the two RLKs HAE and HAESA-like 2 (HSL2). Based on the genetic interactions between the genes encoding these proteins we propose a model where the sequential action of IDA, HAE and HSL2, and a MAP kinase cascade regulate floral organ abscission.

Results and Discussion

A growing paradigm in signal transduction pathways features receptor modules that perceive signals and modules such as MAPK cascades that relay and amplify this information to downstream effectors. Because little is known about the signaling modules that regulate abscission in plants, we investigated the potential that MAPK cascades play a role in this process. In Arabidopsis, recent evidence shows that MKK4 and MKK5 have important and overlapping functions in multiple physiological and developmental processes (912). Therefore, we investigated a potential role these genes play in floral organ abscission.

Because loss of function mutant alleles of Arabidopsis MKK4 and MKK5 are not available in public depositories, we used RNAi to silence these genes. Single RNAi lines of MKK4 or MKK5 did not display mutant phenotypes (10). However, transgenic lines expressing a tandem RNAi transgene of MKK4 and MKK5 (MKK4-MKK5RNAi) have severe stomata developmental defects, and the majority of transgenic plants are unable to survive beyond the seedling stage (10). Among the transgenic plants that are able to survive, three independent lines were recovered with a ≈50% reduction in the expression of MKK4 and a ≈80% reduction in MKK5 expression [see supporting information (SI) Fig. S1], and they display an abscission-defective phenotype (Fig. 1A). The MKK4-MKK5RNAi transgene appears to selectively silence MKK4 and MKK5 because the expression of the two most closely related Arabidopsis MKKs, MKK7 and MKK9, are not significantly altered in MKK4-MKK5RNAi plants that have an abscission defective phenotype (Fig. S1). To determine the basis of the phenotype, we examined the morphology of the AZ in flowers at different stages of development. Flower development is commonly described using a standardized nomenclature based on the morphology of the floral organs (13). The floral stages examined in this study include stage 12, petals with long stamens; stage 13, buds open, petals visible, anthesis; stage 14, long anthers extend above stigma; stage 15, stigma extends above long anthers; stage 16, petals and sepals withering; and stage 17, all organs fall from green siliques. In addition, the flower position, which reflects the relative developmental stage along the inflorescence from the top to the bottom, is frequently used in studies of abscission in Arabidopsis (1). Position 1 is defined as the youngest flower after anthesis, with older flowers numbered consecutively. With the Col-0 ecotype under our standard growth conditions abscission occurs from flower positions 7 to 9.

Fig. 1.
MKK4 and MKK5 regulate floral organ abscission. (A) Representative siliques from Col-0 (wild type) and MKK4-MKK5RNAi plants at flower position 10. The floral organs of the position 10 flower of the Col-0 have abscised, but the flower from MKK4-MKK5RNAi ...

AZs are characterized by the presence of small, cytoplasmically dense cells two to six layers deep. AZs from stage 15 MKK4-MKK5RNAi flowers, before abscission, appear to be the same as the wild type (Fig. 1 B and E). Scanning electron microscopy (SEM) is an effective approach to examine the progressive changes during abscission (1). Before cell separation occurs, floral organs can be forcibly removed to create a fracture plane at the AZ (Fig. 1C). After separation, the cells of the AZ are enlarged and rounded to form a characteristic abscission scar (1) (Fig. 1D). In the MKK4-MKK5RNAi flowers, the floral organs do not abscise (Fig. 1A) and have to be forcibly removed. The AZ fracture plane (Fig. 1G) of older MKK4-MKK5RNAi floral organs appears to be identical to what is observed in early flowers that have not completed the cell separation response (Fig. 1 C and F). Exogenous ethylene, which promotes the cell separation phase of abscission in wild-type plants, does not alter the abscission defective phenotype in the MKK4-MKK5RNAi plants (data not shown). If MKK4 and MKK5 have roles in abscission we would expect they would be expressed in the AZ. GUS reporter genes were used to analyze the expression of MKK4 and MKK5 in floral organs (Fig. 1 H and I). Expression of MKK4 and MKK5 is detected in the floral organs and the AZs. To quantify the difference in abscission between the wild-type and the MKK4-MKK5RNAi plants, we measured the amount of force required to pull the petals from the flower, using a petal breakstrength meter (1, 14) (Fig. 1J). Force is required to remove the petals from the MKK4-MKK5RNAi plants at all flower positions, which suggest that the normal weakening of the middle lamella of the AZ is disrupted. Based on these observations, we conclude the MKK4 and MKK5 are not required for the formation of the AZ but function subsequently during the cell separation phase of abscission.

The abscission-defective phenotype and the morphology of the AZ in the MKK4-MKK5RNAi plants suggest that a MAPK cascade is required for abscission. The MKK4-MKK5RNAi phenotype is very similar to the phenotype observed in ida plants (6). In addition, the normal AZ morphology and the lack of progressive changes in the AZ are characteristic of both the MKK4-MKK5RNAi (Fig. 1) and ida flowers (6). These observations suggest IDA and a MAPK cascade involving MKK4/MKK5 function in a signaling pathway that regulates floral organ abscission. The phenotype of antisense HAE plants (5) suggests that HAE, a RLK, may also function in this signaling pathway.

To determine whether IDA, HAE, MKK4, and MKK5 function in a common signaling pathway, we first examined the morphology and progressive AZ changes in a hae mutant background. Unlike the HAE antisense lines, T-DNA insertion loss-of-function hae alleles (Fig. S2) do not have an abscission-defective phenotype (Fig. 2A). HAE belongs to a gene family that includes two paralogs (15) that we have named HAESA-like 1 (HSL1) and HSL2. Gene expression data show the expression pattern of HSL2, but not HSL1, is similar to HAE. Developmental expression patterns of HAE and HSL2 were assessed by compiling publicly available microarray data and confirmed by GUS reporter gene expression. The compiled data show an increase in the expression of HAE and HSL2 but decreased expression of HSL1 just before the onset of floral organ abscission (Fig. S3). Plants expressing promoter GUS reporter genes, using the HAE or HSL2 promoter, were examined in stage 17 flowers. GUS expression in the floral organs is restricted in the AZ (Fig. 2E).

Fig. 2.
HAE and HSL2 regulate floral organ abscission. (A) Representative siliques from Col-0 (wild type), hae, hsl2, and hae hsl2 plants at flower position 10. The floral organs of the position 10 flower of the Col-0, and single mutant hae or hsl2 plants have ...

The expression data and the phenotype of the hae hsl2 plants suggest that HAE and HSL2 have overlapping functions. Similar to the hae single mutant alleles, plants with T-DNA insertion loss-of-function alleles of HSL2 (Fig. S2) do not show any phenotypic changes (Fig. 2A). However, double mutants of hae and hsl2 have a strong abscission defect; the floral organs never abscise (Fig. 2A). Like ida-2 (Fig. S2), a T-DNA insertion allele of ida (6) in the Col-0 ecotype, and MKK4-MKK5RNAi mutant lines, the hae hsl2 plants appear to be defective in cell separation. The morphology of the AZ in the hae hsl2 plants appears normal (Fig. 2B), but SEM of the AZ at different stages of development (Fig. 2 C and D) suggest that the middle lamella remains intact in floral organs that normally would have undergone abscission.

The force required to remove the petals from wild-type, hae and hsl2 single mutants and the hae hsl2 double mutant was used as a quantitative measure of abscission (Fig. 2F). The hae and hsl2 single mutants require approximately the same amount of force as wild type to remove the petals from flowers before abscission. However, force is required to remove the petals from the hae hsl2 double mutant plants at all flower positions. Exogenous ethylene treatment does not have an effect on the abscission defective phenotype of hae hsl2 plants (data not shown). Thus, the mutant phenotypes, AZ morphology and absence of cell separation in plants with altered expression of IDA, HAE, HSL2, MKK4, and MKK5 suggests these proteins may function in a common signaling pathway to regulate abscission.

MKK4 and MKK5 have been shown to act through the Arabidopsis MAP kinases MPK3 and MPK6 in plant defense responses (8) and in stomatal patterning (10). An in-gel protein kinase assay was used to test the hypothesis that IDA, HAE, and HSL2 modulate the activity of a MAPK cascade. Proteins were isolated from the receptacle, the portion of the pedicel that bears the floral organs and includes the AZ, of wild-type, hae hsl2, and ida. There is a 40% decrease in the activity of MPK6, a known target MAPK of MKK4 and MKK5 (8), in the mutant lines relative to the wild type (Fig. 3A and Fig. S4). This result is consistent with a role for MPK6 in abscission, but the inability to measure MAPK activity specifically in the AZ makes it difficult to determine whether MPK6 is required for abscission using this assay.

Fig. 3.
MPK6 and MPK3 are required for floral organ abscission. (A) (Upper) An in-gel MAP kinase assay of protein extracted from the receptacles of Col-0, hae hsl2, and ida-2 flowers at positions 6–8. (Lower) Western blot, using a MPK6 antibody of the ...

Plants that are mutant for either mpk3 or mpk6 do not have an abscission defective phenotype and the mpk3 mpk6 double mutant is embryo lethal (10). Therefore, to further investigate the role of MPK6 in abscission, we expressed mutant forms of MPK6 in wild-type and mpk3 mutant plants. A mutated MPK6 transgene that contains a Lys to Arg mutation in the protein kinase catalytic domain was constructed. The Lys targeted for mutagenesis is an invariant amino acid present in the protein kinase catalytic domain. This Lys is required for transfer of the phosphate from ATP to the protein substrate. A mutation of this conserved Lys often creates a dominant-negative form of the protein kinase (16). The MPK6 Lys to Arg (MPK6KR) transgene, driven by the MPK6 promoter, was transformed into wild-type and mpk3 plants. All of the MPK6KR plants in the wild-type background are normal. However, ≈10% of independently isolated MPK6KR transgenic lines in the mpk3 background have an abscission defective phenotype (Fig. 3B). The morphology of the AZ in the MPK6KR plants appears normal (Fig. 3C), but SEM of the AZ at different stages of development (Fig. 3 D and E) suggests that the cell separation response is defective. Another mutated form of MPK6 (MPK6AF) also confers an abscission defective phenotype in mpk3 but not the wild-type background (Fig. 3B). The conserved Thr and Tyr in the MAPK activation motif ThrXaaTyr, which are sites of phosphorylation by the upstream MKK and are required for MAPK activation (16), were mutated to Ala and Phe in MPK6AF. These results support the hypothesis that MPK6 is a positive regulator of abscission and that MPK3 can substitute for MPK6 in plants lacking a functional MPK6. The expression of a GUS reporter gene fused with the promoter of MPK3 or MPK6 shows high expression in floral organs and both genes are expressed in the AZs (Fig. 3F), which is also consistent with the roles of these genes in the regulation of floral organ abscission in Arabidopsis.

To test the hypothesis that the putative ligand and the receptor-like protein kinases are in a common pathway with a MAP kinase cascade, ida-2 and hae hsl2 plants were transformed with constitutively active forms of MKK4 or MKK5 under the control of a steroid-inducible promoter (GVG-MKK4DD and GVG-MKK5DD) (9). Due to the hypersensitive reaction and cell death induced by high expression of the MKKs, the plants were not treated with the steroid inducer. However, the basal level of expression of either transgene is sufficient to rescue MAPK pathway mutant phenotypes (10). Several lines in each mutant background showed a rescued abscission phenotype (Fig. 4). These data suggest that MKK4 and MKK5 are epistatic to IDA, HAE and HSL2 and support the hypothesis that they are in a common pathway upstream of MKK4 and MKK5.

Fig. 4.
IDA and HAE HSL2 regulate abscission via a MAPK signaling cascade. Representative siliques from Col-0, ida-2, hae hsl2, GVG-MKK4DD ida-2 and GVG-MKK4DD hae hsl2 plants at flower position 10. The abscission defective phenotype of ida-2 or hae hsl2 is rescued ...

Although the constitutively active MKK transgenes revert both the ida-2 and hae hsl2 mutant phenotypes and expression of dominant-negative forms of MPK6 have abscission defective phenotypes, these results do not distinguish between the role of IDA and HAE HSL2 functioning in common or parallel pathways to regulate a MAPK cascade. To test these alternative hypotheses, we reasoned that a gain of function IDA gene would require HAE and HSL2 if they were in a shared pathway but that the gain of function IDA phenotype would not be altered if IDA and HAE HSL2 were in parallel pathways. Therefore, we combined hae hsl2 with overexpression of IDA. Similar to the report in ref. 7, overexpression of IDA (IDAOE) in wild type shows a premature abscission phenotype and the production of a white substance in the region of abscission (Fig. 5A). However, IDAOE in hae hsl2 has an abscission-defective phenotype, the same as that of hae hsl2 (Fig. 5A). These results show that hae hsl2 are epistatic to IDAOE and support the hypothesis IDA and HAE HSL2 function in a common pathway to regulate abscission.

Fig. 5.
HAE and HSL2 are epistatic to IDA. (A) Representative siliques from Col-0, hae hsl2, IDAOE, and IDAOE hae hsl2 plants at flower position 10. The flowers from the hae hsl2 double mutant plants display an abscission defective phenotype, and overexpression ...

Multiple gene products, including potential signaling ligands, membrane receptors, protein kinase cascades, regulators of hormone responses, and transcription factors have been implicated in the regulation of abscission in plants (4). We have demonstrated, by several different lines of evidence, that there is a signaling cascade (Fig. 5B), from putative ligand (IDA) to receptors (HAE HSL2) to cytoplasmic effectors (MKK4, MKK5, MPK3, and MPK6), which function together to control cell separation during abscission. Additional gene products are also likely to play important roles in abscission and the relationships between them and the signaling pathway outlined here remain to be determined. However, based on the genetic interactions between IDA, HAE, HSL2, MKK4, and MKK5, it seems that this core signaling cascade is an important regulator of floral abscission.

Materials and Methods

Plant Materials and Growth.

Columbia ecotype (Col-0) of Arabidopsis thaliana was used as wild type and is the background ecotype for all mutants. T-DNA insertion alleles (17) were obtained from the Arabidopsis Biological Resources Center (Ohio State University, Columbus, OH) (SALK_105975, SALK_015074, SALK_057117, SALK_030520, and SALK_133209 for hae-1, hae-2, hsl2-1, hsl2-2, and ida-2, respectively). After identifying homozygous mutant plants, the single hae-1 and hsl-12 T-DNA insertion plants were crossed to make hae hsl2 double mutants, and confirmed by PCR. All of the primers for PCR genotyping are listed in Table S1. Plants were grown at 22°C on a 16 h light:8 h dark cycle.

Cloning and Plant Transformation.

Plants were transformed using the floral dip method (18). For the generation of the MKK4-MKK5 RNAi lines, a transgene identical to that in Wang et al. (10) was used. A total of three lines showing an abscission defective phenotype for the MKK4-MKK5RNAi transgenics from ≈300 total T1 plants screened were recovered. For the generation of the MPK6KR and MPK6AF constructs, a 2834-bp fragment upstream of ATG start codon of MPK6 was amplified with MPK6-F and MPK6-B. This upstream sequence was then cloned into pCAMBIA3300 between EcoR1 and SmaI. cDNA of MPK6 containing the KR or AF mutations was amplified with cMPK6-F and cMPK6-Nosterminator-B with the NOS terminator incorporated at the 3′. The KR and AF mutations were generated (16). This cMPK6-NOS terminator fragment was then cloned into the SmaI and XbaI sites of pCAMBIA3300 to generate the final construct of pCAMBIA3300-PMPK6:cMPK6-NOSter. For overexpression constructs of IDA, a genomic fragment of IDA was amplified using Pfu (Stratagene) and cloned into to the KpnI and SacI sites of pBIB-Hyg (19) under CaMV35S promoter. A total of 60 IDAOE Col-0 and 80 IDAOE hae hsl2 transgenic plants were screened on half-strength Murashige and Skoog salts (½ MS) media with 20 μg/ml hygromycin (Sigma), and their phenotypes scored. Seventeen plants containing the IDAOE transgene in Col-0 showed a premature abscission phenotype and the production of a white substance in the receptacle (28.3% of selected plants). All of the IDAOE hae hsl2 transgenic plants had the abscission defective phenotype (100% of selected plants). Constitutively active MKK4 (GVG-MKK4DD) and MKK5 (GVG-MKK5DD) (9) in the pTA7002 vector (20) were transformed into ida-2 and hae hsl2, and 90 individual plants each were screened on ½ MS media with 20 μg/ml hygromycin (Sigma). Three plants from GVG-MKK4DD in ida-2 (3.3% of screened plants), three plants from GVG-MKK4DD in hae hsl2 (3.3% of selected plants), and six plants from GVG-MKK5DD in hae hsl2 (6.7% of screened transgenics) showed normal abscission. A different transgene in the pTA7002 vector was transformed into ida-2 and hae hsl2, and 80 individual plants each were screened on ½ MS media with 20 μg/ml hygromycin. None showed normal abscission. The region toward the 5′ end of the start codons (1.6 kb upstream) of HAE or HSL2 was amplified by Pfu (Stratagene) and inserted in pBIG-Hyg (19) for GUS constructs. All of the primers for the construction of the transgenes are listed in Table S1.

Expression of MKK4 and MKK5 by Quantitative Real-Time PCR.

The expression of MKK4 and MKK5 was assayed using unopened floral buds from Col-0 and MKK4-MKK5RNAi plants. RNA was extracted using TRIzol Reagent (Invitrogen) according to the manufacturer's recommendations. One microgram of total RNA was reverse transcribed using an oligo dT primer and the Omniscript RT Kit (Qiagen). For the real-time PCR, Absolute QPCR SYBR green mix (ABgene) was used, and PCR was performed using DNA Engine Opticon 2 (MJ Research). All samples were log-transformed and normalized to an EF-1-α control. Primers for the real-time PCR are listed in Table S1.

Histochemical GUS Expression.

GUS reporter analyses were performed as reported in ref. 21 with minor modification. Stage 17 (13) flowers from the transgenic plants were harvested and fixed in ice-cold 90% acetone for 1 h at −20 C. The tissues were stained in GUS solution [2 mM potassium ferricyanide, 2 mM potassium ferrocyanide, 10 mM EDTA, 0.2% Triton X-100, 100 μg/ml chloramphenicol, 1 mg/ml 5-bromo-4-chloro-3-indolyl-β-glucuronic acid in 50 mM sodium phosphate buffer (pH 7.0)] for 3 h at 37°C and then cleared in 70% ethanol. GUS expression was observed on a Nikon SMZ-2T microscope.

Petal Breakstrength.

The force that is required for pulling a petal from a flower was measured using a petal breakstrength meter (14). Breakstrength from each indicated floral position of Col-0, hae, hsl2, and hae hsl2 was analyzed from 15 plants (additional data were collected for the early stage flowers). The maximum and minimum values were considered as outliers. Therefore, a total of 13 petals per position were assayed. In the case of MKK4-MKK5RNAi plant, two petals per each flower position from seven plants were analyzed (n = 14).

Light Microscopy and Scanning Electron Microscopy.

Flowers are numbered from the youngest flowers, where the petals first emerge above the sepals to the oldest, most mature flowers. In Col-0 plants, abscission occurs from flower positions 7 to 9. Flowers from stage 15 (13) of 8-week-old Col-0, MKK4-MKK5RNAi, hae hsl2, and MPK6KR were embedded in Epon–Spurr's resin (22). Thin sections (2.5 μm) were obtained with a Leica RM2065 microtome equipped with glass knives and stained with in 0.05% toluidine blue. For SEM analysis, flowers from positions 4 and 10 of 8-week-old Col-0, MKK4-MKK5RNAi, and hae hsl2 were collected, fixed in 4% (vol/vol) gluteraldehyde in 0.05 M potassium phosphate buffer (pH 7.4), and then rinsed four times in the buffer. After dehydration in a graded ethanol series, flower samples were critical-point dried in liquid CO2. Samples were mounted on plates with double-stick tape, and then floral organs were forcibly removed. Samples were sputter coated with Pt, and AZs were viewed at 5 KV on a Hitachi S4700 Field Emission Scanning Electron Microscope or an Amray 1600T Scanning Electron Microscope.

In-Gel Kinase Assay.

Protein was isolated as described in ref. 23 from the receptacles of Col-0, hae hsl2, and ida-2. Fifteen micrograms of protein were separated in 10% SDS/PAGE embedded with myelin basic protein (0.25 mg/ml) as a MAP kinase substrate. H2O2-treated leaves (1 mM for 1 h) of Col-0 were used as positive control for MAP kinase activity. The relative amount of myelin basic protein phosphorylation was analyzed using Fuji phosphoimage analyzer and quantified using Multi Gauge software, Version 2.0 (Fuji Film). For the quantity control, the protein was separated in 10% SDS/PAGE, transferred to Immobilon-P transfer membranes (Millipore), and quantified using Anti-AtMPK6 (Sigma).

Supplementary Material

Supporting Information:

Acknowledgments.

We thank F. Tax, W. Gassmann, and members of the J.C.W. laboratory for comments on the manuscript; J. Doke and S. Park for technical support; D. Ren (State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University, Beijing 100094, China) for pMKK4:GUS and pMKK5:GUS transgenic seeds; and Y. Wang for assaying MKK7 and MKK9 expression in the MKK4MKK5 tandem RNAi plants. This work was supported by Korean Research Foundation Grant M01-2004-000-10035-0 (to S.K.C.), a MU-Monsanto Graduate Research Fellowship (to C.T.L.), National Science Foundation Grants IBN-0133220 (to S.Z.) and MCB-0418946 (to J.C.W.), and the University of Missouri Food for the 21st Century Program (J.C.W.).

Footnotes

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0805539105/DCSupplemental.

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    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Protein
    Published protein sequences
  • PubMed
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    PubMed citations for these articles
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    Taxonomy
    Related taxonomy entry
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