Elsevier

Plant Science

Volumes 215–216, February 2014, Pages 157-171
Plant Science

Review
BLADE-ON-PETIOLE genes: Setting boundaries in development and defense

https://doi.org/10.1016/j.plantsci.2013.10.019Get rights and content

Highlights

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    BLADE-ON-PETIOLE (BOP) genes encode BTB-ankryin transcription factors.

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    BOPs control development at lateral organ boundaries.

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    BOPs regulate leaf, flower, inflorescence architecture, abscission and nodulation.

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    BOPs are distant paralogs of NPR1 with a requirement in plant defense.

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    BOPs may be evolved in coordinating development and defense in land plants.

Abstract

BLADE-ON-PETIOLE (BOP) genes encode an ancient and conserved subclade of BTB-ankryin transcriptional co-activators, divergent in the NPR1 family of plant defense regulators. Arabidopsis BOP1/2 were originally characterized as regulators of leaf and floral patterning. Recent investigation of BOP activity in a variety of land plants provides a more complete picture of their conserved functions at lateral organ boundaries in the determination of leaf, flower, inflorescence, and root nodule architecture. BOPs exert their function in part through promotion of lateral organ boundary genes including ASYMMETRIC LEAVES2, KNOTTED1-LIKE FROM ARABIDOPSIS6, and ARABIDOPSIS THALIANA HOMEOBOX GENE1 whose products restrict growth, promote differentiation, and antagonize meristem activity in various developmental contexts. Mutually antagonistic interactions between BOP and meristem factors are important in maintaining a border between meristem-organ compartments and in controlling irreversible transitions in cell fate associated with differentiation. We also examine intriguing new evidence for BOP function in plant defense. Comparisons to NPR1 highlight previously unexplored mechanisms for co-ordination of development and defense in land plants.

Section snippets

Overview

BTB-ankryin proteins are plant-specific transcriptional co-activators. They are so called because of two conserved protein-protein interaction motifs: a BTB/POZ (for Broad Complex, Tramtrack, and Bric-a-brac/POX virus and Zinc finger) domain at the N-terminus and four ankryin motifs near the C-terminus. The Arabidopsis (Arabidopsis thaliana) genome encodes six BTB-ankryin proteins with functions in development and defense (Fig. 1A).

The first BTB-ankyrin protein to be characterized was

Developmental function in a basal land plant

A glimpse into the ancient developmental function of BOP genes comes from their characterization in a moss, Physcomitrella patens, used as a model for basal land plants [11]. During the juvenile phase of its development, germination of a haploid spore produces a linear array of cells that branch and form a filamentous network called a protonema. Meristematic cells at tip of the protonema divide and extend the network. The first filaments consist of green chloronemal cells. As the plant matures,

Lateral organ boundaries

BOP genes in seed plants have now been studied in the eudicots Arabidopsis, tobacco, pea, and the model legume, Medicago truncatula, affording a more detailed understanding of their activities, which predominate at lateral organ boundaries.

Lateral organ boundaries are specialized junctions in the plant that separate emerging lateral organs from the meristem or plant body [15], [16]. All of the aerial parts of a plant, including the leaves, shoots, and internodes are generated by the shoot

Leaf patterning

Leaf architecture is broadly classified as simple versus compound. Simple leaves have a single undivided blade. Compound leaves of typical eudicots have a divided blade composed of several pairs of leaflets attached to a central stalk, the rachis. In both cases, a narrow petiole joins the blade to the stem [23], [24]. As implied, the BOP genes were named after their mutant phenotype in leaves. In the dominant negative bop1-1 point mutant or bop1 bop2 double T-DNA insertion mutants, simple

Specification of floral meristems

Floral inductive signals acting on the shoot apical meristem result in acquisition of inflorescence meristem fate and new patterns of aerial development. In Arabidopsis, internodes are elongated and axillary meristems proliferate in the axils of leaves whose development is suppressed, resulting in the production of an inflorescence. Axillary meristems are indeterminate at early nodes, giving rise to secondary inflorescences. Axillary meristems at subsequent nodes become determinate through

Inflorescence architecture

Spatial regulation of BOP1/2 expression is an important determinant of inflorescence architecture. Parameters such as the timing, length, and pattern of internode elongation and the orientation of flowers are key variables that contribute to architectural diversity [86]. Elongation of Arabidopsis internodes begins at the transition to flowering, contributing to a regular spiral arrangement of upwardly oriented flowers on the primary stem [87], [88]. When elongation is complete, the

Abscission

BOPs are essential in abscission, a process that merges potential functions in development and defense [21], [111], [112]. Primary abscission zones at the site of detachment of leaves, floral organs, and fruits differentiate simultaneously with lateral organs at the boundaries where they are connected to the plant body (Fig. 2A). The abscission zone is typically comprised of several layers of small cytoplasmically dense cells that acquire responsiveness to separation-inducing signals that

Patterning of fruits

Preliminary evidence suggests that an antagonistic interaction between KNOX-BELL and BOP1/2 activities also governs the architecture of fruits. The Arabidopsis silique is a fruit pod composed of two valves joined at their margins to a meristematic replum that generates seeds attached on the interior. The valves are homologous structures to leaves. The valve margins that separate the valves from the replum are lateral organ boundaries specialized in dehiscence, comprised of a separation layer

Signaling mechanism

The NPR1 signaling mechanism serves as a paradigm for BOPs. BOPs and NPR1 share homologous functional domains that support a similar mode-of-action (Fig. 1B). Both have a BTB/POZ domain at the N-terminus and two ankyrin repeats near the C-terminus that mediate interaction with TGA bZIP transcription factors [8], [126], [127]. BTB-ankryins also have an uncharacterized domain of unknown function (DUF3420) adjacent to the first ankyrin motif (Fig. 1B). Divergent C-termini for BOP1/2 and NPR1

Plant defenses

Basal resistance based on preformed structural and chemical barriers including the plant cuticle, cell wall, and anti-microbial compounds is the first line of defense against pathogens [155]. Penetration of these barriers stimulates localized responses geared to the life-style of the pathogen. In general, salicylic acid-induced defenses are most effective against biotrophic and hemi-biotrophic pathogens, which require nutrients from living tissue to complete their life cycle. Jasmonic

Nodulation

Legumes are well-studied for their ability to establish symbiotic relationships with nitrogen-fixing rhizobia [58], [163]. BOP2 orthologs NOOT and COCH from M. truncatula and pea transcribed in roots are essential for maintenance of nodule meristem identity and size (Fig. 2A; [58], [164]). Despite defects in nodule identity, rhizobium infection and symbiosis in noot mutant plants is not adversely affected [58].

M. truncatula and pea have persistent tip-growing nodule meristems that originate

Concluding remarks

BOP genes encode a distinct subclade of BTB-ankryin transcriptional co-activators, divergent in the NPR1 family of plant defense regulators. Combining data from Arabidopsis, moss, tobacco, pea, and M. truncatula provides a more complete understanding of their conserved roles in development. The emerging picture is that BOPs function at lateral organ boundaries—uniquely patterned transitional zones in the plant that separate determinate lateral organs from the apical meristem or plant body and

Acknowledgements

This work was supported by an NSERC Discovery Grant to S.R.H. We thank Shabnam Gholoobi for compiling phylogenetic data and Owen Rowland for critical reading of the manuscript. We also thank the editor and anonymous reviewers of this manuscript for insightful comments.

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