Arabidopsis Class I KNOTTED-Like Homeobox Proteins Act Downstream in the IDA-HAE/HSL2 Floral Abscission Signaling Pathway

Abstract

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...

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“…This set of cellular characteristics is reminiscent of meristematic tissues. Several genes involved in SAM maintenance and the initiation of axillary meristems are expressed in the AZ (Shi et al, 2011;Nakano et al, 2013;Wang et al, 2013). Therefore, it has been proposed that AZ cells have a meristematic identity.…”

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“…2 and 3). In Arabidopsis, during the last step of petal senescence, abscission, the expression of BREVIPEDICELLUS (BP)/ KNAT1 is induced, and the accelerated petal abscission phenotype of its knockout mutant, bp, indicates that BP/KNAT1 plays an antagonistic role in the petal abscission process (Shi et al, 2011). It has also been shown that in sunflower, increased expression of HaHB-4 suppresses flower senescence (Manavella et al, 2006).…”

Floral organ abscission is regulated by a positive feedback loop

“…A mitogen-activated protein kinase (MAPK) cascade consisting of MITOGEN-ACTIVATED PROTEIN KINASE KINASE 4/5 (MKK4/5) and MPK3/6 is positioned genetically downstream from HAE/HSL2 (8). Mutations in the transcription factor BREVIPEDI-CELLUS (a knotted1-like homeobox transcription factor) suppress the abscission defect of the hae hsl2 double mutant (10). Additionally, nevershed (nev; an ARF-GAP domain protein) plants do not abscise, whereas secondary mutations in evershed [evr; a leucine-rich repeat (LRR) receptor-like protein kinase], somatic embryogenesis receptor kinase1 (a LRR receptor-like protein kinase), and cast away (a receptor-like cytoplasmic protein kinase) suppress the abscission defect of nev (11)(12)(13)(14).…”